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portada y contra 68(1) NOVEDADES2:portada y contra 66(1).qxd 16/06/2011 11:22 Página 1
ISSN: 0211-1322
Zamora, N.A. El caso de Lonchocarpus costaricensis (Leguminosae, Papilionoideae), una especie
endémica de Costa Rica: un complejo taxonómico-nomenclatural, y una nueva especie / The case
of Lonchocarpus costaricensis (Leguminosae, Papilionoideae), an endemic species of Costa Rica:
a taxonomic-nomenclatural complex, and a new species ................................................................
Cano-Maqueda, J. & Talavera, S. A taxonomic revision of the Campanula lusitanica complex (Cam pa nulaceae) in the Western Mediterranean region / Una revisión taxonómica del com plejo Campanula lusitanica (Campanulaceae) en la región occidental mediterránea ...........................................................................................................................................
Venhuis, C. & Oostermeijer, J.G.B. Distinguishing colour variants of Serapias perez-chiscanoi (Orchidaceae) from related taxa on the Iberian Peninsula / Distinción de variantes en color de Serapias perezchiscanoi (Orchidaceae) en relación con táxones de la Península Ibérica ..........................................
Lado, C., Wrigley de Basanta, D. & Estrada-Torres, A. Biodiversity of Myxomycetes from the Monte
Desert of Argentina / Biodiversidad de Myxomycetes en el Desierto de Monte (Argentina) ...............
Peñas, J., Lorite, J., Alba-Sánchez, F. & Taisma, M.A. Self-incompatibility, floral parameters, and pollen
characterization in the narrow endemic and threatened species Artemisia granatensis (Asteraceae) /
Autoincompatibilidad, parámetros florales y caracterización de polen en la especie endémica y amenazada Artemisia granatensis (Asteraceae) ......................................................................................
Schneider, A.A. & Boldrini, I.I. Microsculpture of cypselae surface of Baccharis sect. Caulopterae (Asteraceae) from Brazil / Microescultura de la superficie de las cipselas de Baccharis sect. Caulopterae
(Asteraceae) de Brasil ......................................................................................................................
Domínguez-Álvarez, S., Rico, J.M. & Gil-Rodríguez, M.C. Photosynthetic response and zonation of
three species of Gelidiales from Tenerife, Canary Islands / Respuestas fotosintéticas y zonación de
tres especies de Gelidiales de Tenerife, Islas Canarias ......................................................................
http://rjb.revistas.csic.es
N.º 1
enero-junio 2011
Madrid (España)
ISSN: 0211-1322
Madrid
SUMARIO / CONTENTS
Volumen 68
7/14
15/47
2011
Madrid (España)
N.º 1
enero-junio 2011
49/59
61/95
97/105
107/116
117/124
Volumen 68
N.º 1
Anales del Jardín Botánico de Madrid
Volumen 68
REAL JARDÍN BOTÁNICO
www.publicaciones.csic.es
CONSEJO SUPERIOR DE INVESTIGACIONES CIENTÍFICAS
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Volumen 68
N.º 1
enero-junio 2011
Madrid (España)
ISSN: 0211-1322
Volumen 68
N.º 1
enero-junio 2011
Madrid (España)
ISSN: 0211-1322
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Volumen 68
N.º 1
enero-junio 2011
Madrid (España)
ISSN: 0211-1322
SUMARIO / CONTENTS
Zamora, N.A. El caso de Lonchocarpus costaricensis (Leguminosae, Papilionoideae), una especie endémica de Costa Rica: un complejo taxonómico-nomenclatural, y una nueva especie / The case of Lonchocarpus costaricensis (Leguminosae, Papilionoideae), an endemic species of Costa Rica: a taxonomic-nomenclatural complex, and a new species ......
Cano-Maqueda, J. & Talavera, S. A taxonomic revision of the Campanula lusitanica complex (Campanulaceae) in the Western Mediterranean region / Una revisión taxonómica del complejo Campanula lusitanica (Campanulaceae) en la región occidental mediterránea .........................................................................................................................
Venhuis, C. & Oostermeijer, J.G.B. Distinguishing colour variants of Serapias perezchiscanoi (Orchidaceae) from related taxa on the Iberian Peninsula / Distinción de variantes en color de Serapias perez-chiscanoi (Orchidaceae) en relación con táxones de
la Península Ibérica ........................................................................................................
Lado, C., Wrigley de Basanta, D. & Estrada-Torres, A. Biodiversity of Myxomycetes from
the Monte Desert of Argentina / Biodiversidad de Myxomycetes en el Desierto de Monte
(Argentina) .....................................................................................................................
Peñas, J., Lorite, J., Alba-Sánchez, F. & Taisma, M.A. Self-incompatibility, floral parameters,
and pollen characterization in the narrow endemic and threatened species Artemisia granatensis (Asteraceae) / Autoincompatibilidad, parámetros florales y caracterización de polen en la especie endémica y amenazada Artemisia granatensis (Asteraceae) ..................
Schneider, A.A. & Boldrini, I.I. Microsculpture of cypselae surface of Baccharis sect.
Caulopterae (Asteraceae) from Brazil / Microescultura de la superficie de las cipselas de
Baccharis sect. Caulopterae (Asteraceae) de Brasil ........................................................
Domínguez-Álvarez, S., Rico, J.M. & Gil-Rodríguez, M.C. Photosynthetic response and
zonation of three species of Gelidiales from Tenerife, Canary Islands / Respuestas fotosintéticas y zonación de tres especies de Gelidiales de Tenerife, Islas Canarias ..............
7/14
15/47
49/59
61/95
97/105
107/116
117/124
La Serapias perez-chiscanoi (Orchidaceae) es una orquídea endémica
que se puede observar al suroeste de la Península Ibérica. En general, tiene flores verde pálido,
pero ocasionalmente se pueden encontrar ejemplares con flores rosadas o rojas.
[Fotografía: Caspar Venhuis].
Serapias perez-chiscanoi (Orchidaceae) is a narrow endemic orchid
of the southwestern part of the Iberian Peninsula. It generally has pale green flowers,
but plants with pinkish or even red flowers are occasionally found.
[Photograph: Caspar Venhuis].
2255 lonchocarpus:Maquetación 1 13/06/2011 11:57 Página 7
Vol. 68(1): 7-14
enero-junio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2255
El caso de Lonchocarpus costaricensis
(Leguminosae, Papilionoideae), una especie endémica
de Costa Rica: un complejo
taxonómico-nomenclatural, y una nueva especie
por
Nelson A. Zamora
Unidad Estratégica de Botánica, Instituto Nacional de Biodiversidad (INBio), Costa Rica. Apdo. 22-3100, Santo Domingo
[email protected]
Resumen
Abstract
Zamora, N.A. 2011. El caso de Lonchocarpus costaricensis (Leguminosae, Papilionoideae), una especie endémica de Costa Rica:
un complejo taxonómico-nomenclatural, y una nueva especie.
Anales Jard. Bot. Madrid 68(1): 7-14.
Zamora, N.A. 2011. The case of Lonchocarpus costaricensis (Leguminosae, Papilionoideae), an endemic species of Costa Rica: a
taxonomic-nomenclatural complex, and a new species. Anales
Jard. Bot. Madrid 68(1): 7-14 (in Spanish).
La mezcla de colecciones, la ausencia de la designación de un
espécimen tipo y la fuerte similitud morfológica entre colecciones citadas en el protólogo de la descripción de Derris costaricensis generaron una situación taxonómica y nomenclatural
confusa alrededor de la entidad Lonchocarpus costaricensis
(Donn. Sm.) Pittier; un estudio taxonómico detallado del caso reveló que una nueva especie (Lonchocarpus felipei N. Zamora),
aquí descrita, está implicada. Asimismo se restablece aquí la lectotipificación original de Lonchocarpus macrocarpus Benth.
Mixed collections, a lack of type specimen designation and
strong morphological similarity between collections cited in the
Derris costaricensis protologue has led to a very confused taxonomic and nomenclatural situation surrounding the species Lonchocarpus costaricensis (Donn. Sm.) Pittier; a detailed taxonomic
study has revealed that a new species (Lonchocarpus felipei
N. Zamora) here described, is involved. Also, the original lectotipification of Lonchocarpus macrocarpus Benth., is re-establish it
here.
Palabras clave: Taxonomía, nomenclatura, Leguminosae, Lonchocarpus, complejo de especies, lectotipificación, una nueva
especie.
Keywords: Taxonomy, nomenclature, Leguminosae, Lonchocarpus, species complex, lectotypification, a new species.
Introducción
citados por Pittier (1917) y aquellos citados en el protólogo de Derris costaricensis determinó que Pittier
3654 (fr) y Tonduz 2880 (fr) corresponden a un taxon
distinto. Este taxon posee una gran semejanza en su
follaje y frutos con Lonchocarpus costaricensis (Donn.
Sm.) Pittier. Debido y a partir de esta situación de
mezcla de colecciones, el concepto de L. costaricensis
se adoptó (p.e., Standley, 1937: 543) y se ha venido
aplicando en forma equivocada. Además, ha favorecido tal confusión la condición del verdadero L. costaricensis, al ser una especie endémica de Costa Rica relativamente escasa o rara, mientras la aquí descrita
(L. felipei N. Zamora) es más común y conocida ampliamente de Nicaragua y Costa Rica.
En la descripción original de Derris costaricensis
Donn. Sm., Bot. Gaz. 44: 110-111. 1907, el autor citó
dos colecciones (síntipos), Tonduz 2880 (CR!, US!) y
Tonduz 13993 (BM!, NY!, US!), que fueron utilizadas
para elaborar el protólogo, sin dar indicación de la
colección tipo. Más tarde, Pittier (1917) hizo la transferencia al género Lonchocarpus y designó Tonduz
13993 (fl y fr) como el lectótipo; en esta misma publicación, Pittier citó otras colecciones: Pittier 3654 (fr)
(NY!, US!), y Tonduz 13528 (fl y fr) (F!, US!) y 13532
(fl y fr) (BM!, NY!, P!, US!).
Un estudio, aquí detallado, de todos los ejemplares
8
N.A. Zamora
Sousa (1990), consciente de esta situación (mezcla
de colecciones) y aunque sin describirla y estudiarla en
detalle, prefirió relectotipificar el nombre L. macrocarpus Benth., para acomodar la entidad aquí definida
como distinta de L. costaricensis (Donn. Sm.) Pittier.
Pero L. macrocarpus es un binomio heterogéneo compuesto de tres síntipos: Fendler 1861 (Venezuela), Orbigny 578 (Bolivia) y “New Spain, Herb Pavón” [lectótipo elegido por Sousa (1990)]. Sin embargo, ya
previamente Pittier (1928), en ausencia de una designación de un tipo para L. macrocarpus, había seleccionado la colección Fendler 1861 (K!) como el lectótipo;
designación con la que Sousa (1990) más tarde argumentó estar en desacuerdo con Pittier, señalando que
fue una “escogencia mecánica”, y propuso relectotipificar L. macrocarpus con el ejemplar Herb. Pavón s.n.
(G!). El síntipo “Pavón” lleva anotado por Bentham
una etiqueta “Nueva España Herb. Pavón” y marcada
por Pavón “Classis 17 N 204 dubia N E. Securidaca?”.
La colección se compone de dos folíolos sueltos y frutos, cuya apariencia general (en especial por sus frutos)
parece corresponder más bien a L. costaricensis.
La validez de la lectotipificación de L. macrocarpus
hecha por Pittier había sido respaldada y aceptada
por Tozzi (1989); además, a su vez este autor analizó
con mayor detalle la naturaleza del concepto de L. macrocarpus, restringiéndolo al síntipo Fendler 1861
(K!), apoyando con esto la decisión de Pittier (1928).
Vale mencionar también que, siguiendo este concepto
del tipo [Fendler 1861], la mayoría del material recolectado de L. macrocarpus proviene del área geográfica del tipo (Venezuela). Para el síntipo Orbigny 578
(G!, P!), Tozzi (1989) no resolvió sobre su identificación; pero dicha colección fue identificada como Lonchocarpus hedyosmus Miq., por H.H. Poppendieck
(HBG) en julio de 1993. También, según Tozzi (1989)
y confirmado por este estudio, la colección Spruce
4597 (K!, G!, NY!, P!, W!; tipo, K!) de L. macrocarpus var. sericophyllus Benth., citada por Bentham
(1860) en el protólogo de L. macrocarpus, corresponde a L. hedyosmus Miq.; identificación a su vez respaldada por H.H. Poppendieck (HBG), en julio de 1993.
Finalmente, Tozzi (1989) señaló que L. hedyosmus y
L. macrocarpus están altamente emparentadas. Pero
en esta última las inflorescencias tienden a ser más
cortas; el cáliz, denticulado, y los folíolos, persistentemente denso y sedoso-pubescentes en el envés, versus
inflorescencias más alargadas, el cáliz truncado y folíolos glabrescentes o no denso sedoso-pubescentes
en el envés en L. hedyosmus; también existen algunas
diferencias a nivel de frutos.
Basándonos en la situación antes descrita, se concluye que la nueva lectotipificación establecida por
Sousa (1990) para L. macrocarpus no es válida, y considero más apropiado proponer un nombre nuevo
para la especie históricamente identificada en forma
equivocada como Lonchocarpus costaricensis o L. macrocarpus sensu Sousa (1990, 2001). Además, el restablecer la lectotipificación de L. macrocarpus hecha por
Pittier estaría en mayor concordancia con la descripción que se provee en el protólogo original de L. macrocarpus, tanto con el tamaño del fruto, al cual el epíteto hace referencia, como en el número de folíolos (917) y área geográfica (Sudamérica) de dos de los síntipos citados [Fendler 1861(Venezuela) y Orbigny 578
(Bolivia)], excepto la colección Herb. Pavón s.n., cuya
procedencia específica sigue siendo aún dudosa o sin
resolver (véase McVaugh, 2000: 322). Por lo que se
conserva aquí el lectótipo seleccionado por Pittier
(1928): Lonchocarpus macrocarpus Benth., J. Linn.
Soc., Bot. 4 (Suppl.): 91. 1860. Tipo: “Fendler 1861
(Venezuela)” (lectótipo, K!, aquí redesignado). El restablecer la lectotipificación de Pittier (1928) significa
a su vez oficializar aquí, por primera vez, que la especie Lonchocarpus margaritensis Pittier es sinónimo de
Lonchocarpus macrocarpus Benth (véase Tozzi, 1989;
Tozzi & Silva, 2007).
La especie aquí descrita es ampliamente conocida
(según abundante material de herbario citado y examinado) y estudiada por ecólogos y biólogos en la
Provincia de Guanacaste (Costa Rica) desde mediados de los años 1960, mientras la verdadera (endémica, algo rara y más localizada) Lonchocarpus costaricensis permanece más o menos oculta o aislada en algunas colinas del Área de Conservación Guanacaste
(especialmente Sector Murciélago) y algunos cerros
de formaciones calcáreas en la Península de Nicoya.
Lonchocarpus felipei N. Zamora, sp. nov.
Tipo: Costa Rica. Puntarenas: Cantón de Puntarenas, ridges between Río Guacimal and Río Lagarto on
road from Inter American Highway to Monteverde,10°16’N, 84°50’W, 800-1000 m, 20 April 1991 (fl),
Haber & Zuchowski 10656 (holótipo, INB; isótipos,
CR, K, MEXU, MO, PMA,). Figs. 1, 2.
Lonchocarpus costaricensis similis, sed floribus minoribus [usque ad 9-10(12) mm, non 15-18(20) mm],
vinaceis vel atropurpureis (non roseis) recedit; a Lonchocarpus retifer foliolis paucioribus, fructibus latioribus differt.
Árbol de 7-14 m de alto, ramitas conspicuamente
lenticeladas, denso a esparcido ferrugíneo pubescentes hacia el ápice o partes jóvenes; estípulas deciduas, no vistas. Hojas imparipinnado-compuestas,
con 5-7(9) folíolos; pecíolo de 5,5-11 cm de largo; ra-
Anales del Jardín Botánico de Madrid 68(1): 7-14, enero-junio 2011. ISSN: 0211-1322. doi: 10.3989/ajbm: 2255
Lonchocarpus costaricensis, especie endémica de Costa Rica
9
Fig. 1. Lonchocarpus felipei: A, rama con frutos (Zamora 2281, INB); B, rama con inflorescencias; C, flor; D, estambres, E, pétalos (Haber & Zuchowski 10656, INB). Ilustración de Claudia Aragón.
10
N.A. Zamora
quis de 4-10 cm de largo, levemente caniculado, glabrescente a ferrugíneo pubescente, peciolulos 5-9 mm
de largo; folíolos distales (6,5)9-21 × 3,6-10,2 cm,
oblongos a obovados, mediales (5)9-14,5 × (3)3,9-7,5
cm, oblongos a obovados, basales de (4)6-11 × (2,4)
3,6-7,7 cm, ovados a oblongos o suborbiculares, ápice
redondeado, base aguda, obtusa a levemente asimétrica, glabros cuando adultos o esparcido pilosos cuando jóvenes en el haz, glabrescentes a ferrugíneo pilosos en el envés, nervios secundarios 9-17 por lado, venación terciaria conspicuamente reticulada. Inflorescencias racemosas, axilares, 2-16 cm de largo, eje
principal glabrescente a diminuto estrigoso o esparcido seríceo, pedúnculos o ejes laterales secundarios de
1-5 mm de largo; brácteas deciduas, no vistas, bractéolas 0,5-0,6 mm, escuamiformes, decíduas. Flores
de color marrón a púrpura oscuro, 9-10(12) mm de
largo; pedicelo 3,5-4 mm de largo; cáliz (1,5)2-3 mm
de largo, cupuliforme, diminuto seríceo, truncado o
ligeramente ondulado-denticulado; pétalos 5, estandarte 8-11(12) × 9-10 mm, suborbicular y cóncavo,
con los márgenes levemente involutos, ligeramente recurvado, nervado, seríceo por fuera y glabro por dentro, con una mácula verde basal y punteado cerca de la
base en la cara interna, emarginado en ápice y auriculado en la base, la uña ca. 2 mm de largo; alas 5-7 ×
2,5-3(3,5) mm, oblongo-oblicuas, redondeadas en
el ápice y levemente auriculadas en la base, la uña
ca. 3 mm; quilla 5-6 × 3-3,2 mm, oblongo-oblicua,
unida distalmente, diminuto serícea por fuera, uña ca.
2,8-3 mm; tubo estaminal 6-6,5 mm, glabro; pistilo linear, 6-7,5 mm, denso seríceo, óvulos 1(2); estilo fuertemente recurvado; estigma inconspicuo; anteras basifijas. Frutos legumbres, 7-12(16) × 3-5 cm, elípticos
a ovado-elípticos u obovado-elípticos a veces falcadoelípticos, redondeados en el ápice y obtusos a atenuados en la base, coriáceos, ambos márgenes afilados,
pardo-amarillentos, glabros o glabrescentes cuando
adultos y pardo-amarillento sedoso pubescentes
cuando jóvenes, con verrugas evidentes a la altura de
las semillas; semillas 1 ó 2, 1,5-1,6 × 0,8 cm, aplanadas,
oblongo-reniformes, pardo-rojizas cuando secas.
A pesar de la larga confusión en la que L. costaricensis estuvo inmersa, ésta difiere de L. felipei de manera notable, como se resume en el siguiente cuadro
(Tabla 1).
Ambas especies poseen hojas con 5-7 folíolos y éstos son muy semejantes en su apariencia general, por
lo que es algo difícil diferenciarlas en forma vegetativa, aunque las ramitas y hojas (raquis y envés de los
folíolos) de L. costaricensis poseen una pubescencia
tomentosa pardo-rojiza o ferrugíneo-oscura; mientras, en L. felipei la pubescencia es más amarillenta a
pardo-amarillenta.
A nivel de flores (Fig. 2), tamaño y color, y en cierto grado los frutos, la mayor afinidad de L. felipei es
más bien con la especie L. retifer Standl. & L.O. Williams, pero en ésta última sus flores son relativamente
más pequeñas (5-6 mm), las hojas normalmente tienen
más folíolos (comúnmente 9) y sus frutos son más angostos (2-2,6(2,9) cm). Además, L. retifer se da en climas más húmedos y su floración ocurre cuando el árbol tiene hojas.
Fig. 2. A, estandarte; B, cáliz; C, frutos de: Lonchocarpus retifer
(flores, Espinoza & al. 1472, INB; frutos, Morales 5559, INB),
L. felipei (flores, Haber & Zuchowski 10656, INB; frutos, Zamora
2281, INB) y L. costaricensis (flores, Zamora & al. 2243, INB; frutos, González & Garita 3052, INB). Ilustración de Claudia Aragón.
Hábitat, distribución, conservación y ecología: Lonchocarpus felipei es propio de bosques secos a húmedos, a lo largo de la costa pacífica de Nicaragua
(Chontales) hasta Costa Rica (Valle Central); es de frecuente a común en vegetación caducifolia o semicaducifolia, de preferencia en terreno sedimentario,
11
Tabla 1. Principales caracteres diferenciadores entre Lonchocarpus felipei y L. costaricensis. Medidas de flores para L. felipei fueron
tomadas de Haber & Zuchowski 10656 (fl) (INB!) y para L. costaricensis tomadas de Zamora & al. 2243 (fl) (INB!).
Carácter
L. felipei
Flores, color
marrón o púrpura oscuro
L. costaricensis
rosadas
Flores, tamaño (mm)
9-10(12)
15-18(20)
Estandarte, mácula
presente, verde
ausente o no diferenciada
Cáliz, tamaño (mm)
(1,5)2-3
4-5
Cáliz, forma
cupuliforme
campanulado
Cáliz, margen
truncado a ondulado-denticulado
dentado, el vexilar 2-3 mm
Bractéolas, forma
escuamiformes
filiformes
Bractéolas, tamaño (mm)
0,5-0,6 mm, deciduas
5-7 mm, persistentes
Inflorescencia, pubescencia
diminuto estrigosa o serícea esparcida
denso ferrugíneo tomentosa
Frutos adultos
verdoso-amarillentos o pardo-amarillentos,
glabros, glabrescentes a tomentosos,
con verrugas a la altura de las semillas
pardo-rojizos o ferrugíneo-oscuros,
denso tomentosos,
lisos a la altura de las semillas
Hábitat
bosque seco a húmedo,
prefiere terreno sedimentario
bosque seco,
prefiere terreno cálcareo
Distribución
Nicaragua-Costa Rica
Endémica, Costa Rica
desde el nivel del mar hasta los 800(1000) m. Al menos en Costa Rica la especie se encuentra protegida y
poblaciones importantes se encuentran en el Área de
Conservación Guanacaste (ACG: Sector Santa Rosa,
Sector Santa Elena, Sector Murciélago, Sector Pocosol), Parque Nacional Palo Verde, Refugio de Vida
Silvestre Macacona-Esparza y Zona Protectora El Rodeo-San José. Su floración ocurre de febrero a abril,
siendo máxima cuando el árbol está completamente
caducifolio. Es interesante añadir que he observado el
fenómeno del albinismo en un individuo en el Sector
Santa Rosa, ACG; fenómeno también visto en Lonchocarpus cultratus (Vell.) A.M.G. Azevedo & H.C.
Lima (A.M.G. Azevedo Tozzi, com. pers., 2010). Sus
frutos se han observado la mayor parte del año, aunque permanecen en el árbol durante toda la estación
lluviosa y maduran y caen en el primer mes del verano
siguiente; cada individuo reproductivo florece un año
y tiene frutos hasta el siguiente, pero no sincronizadamente entre árboles (D.H. Janzen, com. pers., 2010).
Ensayos de reproducción y propagación han dado
buenos resultados, con importantes porcentajes de
germinación y desarrollos en vivero y campo.
Es importante mencionar que toda la literatura
ecológica, química y molecular (p.ej., Chapman,
1989; Evans & al., 1985; Fellows & al., 1979; Janzen,
1980, 1982, 1983, 1986; Janzen & Liesner, 1980; Janzen & al., 1990; Navarro & al., 2005; Waterman &
Mahmoud, 1985) generada para la especie (o donde
se cita el nombre) Lonchocarpus costaricensis corresponde más bien a la especie aquí descrita. A menudo
su follaje se encuentra altamente infestado de agallas,
provocadas por insectos hemípteros del género Eu-
phalerus, situación frecuente que padecen varias especies de Lonchocarpus (Hollis & Martin, 1997).
Etimología: Dedico esta especie en honor a su Alteza Real el Príncipe Don Felipe de Borbón, por su apoyo al estudio de la biodiversidad de Costa Rica.
Colecciones examinadas
COSTA RICA. Guanacaste: Cantón de La Cruz, P.N. Guanacaste, Cordillera de Guanacaste, Camino a la Estación Maritza, a
orillas del Río Espavelar, 10°58’10’’N, 85°33’35’’W, 300 m, 25-V1995 (fr), Zamora 2290 (MO); Bahía Salinas a Santa Cecilia, camino a la Estación Maritza, alrededores de la Quebrada Espavelar,
10°58’10”N 85°38’40’’W, 290 m, 5-VIII-1995 (fr), Ramírez & Soto
392 (INB); Cuajiniquil, camino entre Cuajiniquil y Junquillal,
10°57’20”N, 85°42’00”W, 0 m, 8-IX-1995 (fr), J. Sánchez 534
(CR). Cantón de Liberia, Parque Nacional Santa Rosa, Llano Jicaral, hacia la playa, 280 m, 25-I-1983 (fr), Sousa & al. 12688 (MO);
Parque Nacional Santa Rosa, Llano Jicaral, hacia la playa, 280 m,
25-I-1983 (fr), Sousa 12688 (CR); Parque Nacional Santa Rosa,
10 m, 4-XII-1985 (fr), Zamora & al 1152 (CR, MO); Parque Nacional Santa Rosa, bosque seco, 317 m, 3-IV-1976, Tinney 236
(CR); Parque Nacional Santa Rosa, bosque secundario, 317 m, 3-I1976, Chazdon 210 (CR); Parque Nacional Santa Rosa, entrada al
mirador Valle Naranjo, 10°48’00’N, 85°38’37’’W, 200 m, 11-IV2000 (str), Acosta & al. 847 (MO); Liberia, Parque Nacional Santa Rosa, alrededor de la entrada a Nancite y playa Naranjo,
10°48’30’’N, 85°40’55’’W, 10 m, 26-IV-2000 (fr), Acosta & al. 931
(INB, MO); faja costeña del golfo de Papagayo, Hacienda Horizontes, 10°42’25’’N, 83°34’30’’W, 130 m, 1-III-1995 (st), Zamora
2241 (MO). Cantón de Carrillo, Península de Nicoya, Sardinal
Nuevo Colón, 2-3 km después del cruce a Zapotal, cerro Judas, camino a playa Guacamaya, 10°29’45”N, 85°44’05’’W, 29 m, 24-V1995 (fr), Zamora & al. 2285 (INB); faja costeña del golfo de Papagayo, Sardinal alrededores playa Monte del Barco, 10°36’30’’N,
85°38’20’’W, 20 m, 3-II-1996 (fr), Jiménez & al. 2065 (INB); bahía
El Coco, bahía Playa Hermosa, and Sardinal, 10°32’00”N,
85°40’00”W, 0-150 m, 10-XI-1975 (fr), Burger & Baker 9933 (CR);
12
N.A. Zamora
a
b
c
d
e
Fig. 3. Lonchocarpus felipei: a, b, flores maduras, mostrando el color vivo, el estandarte reflexo y mácula verde; c, rama con inflorescencias inmaduras, con hojas; d, rama en máxima floración, sin hojas; e, tallo, con la corteza lisa. Fotografías de D. Solano (Zamora &
Solano 4913, INB).
cerro el Hacha, 28-VII-1986 (fr), Chacón & Chacón 2038 (CR,
MO); faja costeña del golfo de Papagayo, camino entre Nuevo Colón y Zapotal, cerca del cerro Matapalo. 10°30’30”N
85°46’20’’W, 300 m, 4-VIII-1995 (fr), Ramírez & Soto 384 (INB),
386 (INB). Cantón Santa Cruz, 4 km E. Santa Cruz, 130 m, XII1973, Solomon 667, (CR); Cañas, La Pacífica, 24-VIII-1990 (fr),
Jiménez 54 (CR). Cantón de Bagaces, Parque Nacional Palo Verde,
valle del Tempisque, cerro Jocote, sector Carreta, 10°22’45”N,
85°19’15’’W, 0-100 m, 11-VI-1993 (fr), Chavarría 822 (INB, CR);
Parque Nacional Palo Verde, Estación Catalina, sendero Botija,
saliendo al Cenicero, 10°21’N, 85°16’W, 10-20 m, 9-XII-1991 (fr),
Chavarría 450 (INB, CR, MO); R.B. Lomas Barbudal, valle del
Tempisque; Lomas Barbudal, Marañonal, Oja de Agua y Agua
Fría, 10°26’25”N, 85°19’05’’W, 100-200 m, 2-V-1993 (fr), Chavarría 797 (INB); Cuenca del Temspisque, Hacienda Monteverde,
10°33’00’’N, 85°18’20’’W, 100-300 m, 9-VI-1996 (fl), Ronchi
& Frankie 830 (INB); Cuenca del Tempisque, 3,5 km del cruce
al Parque, sobre la carretera Interamericana, 10°29’50’’N,
85°15’40’’W, 70 m, 23-XI-2000 (fr), Acosta & al. 3009 (INB); Refugio de Vida Silvestre-Palo Verde, sin fecha (fl), Ramírez 220
(CR); finca La Pacífica, 2 miles N of Cañas along Pan-Am Hwy.,
gallery forest between río Corobicí and irrigation ditch, 5-VI-1971
(fr), Gentry 810 (CR, MO); Lomas Barbudal, Bagaces 100 m, 10V-1984 (fr), Gómez 23012 (CR, MO); road from Bagaces to Aguas
Claras about 5 km North of Bagaces, 150-200 m, 7-VII-1976 (fr),
Utley 5305 (MO, CR). Cantón de Cañas, Hacienda La Pacífica
near Cañas, 14-VIII-1986 (fr), Seigler 12774 (MO), 12401A (MO);
Comelco Ranch, Bagaces (MO), remnant forest along stream, 2 km
southwest of La Cruz, 11°4’ N, 85°40’W, 10 m, 29-I-1978 (fr),
Liesner 4635 (CR, MO); seasonal swamp, dry now, OTS Área A3
site a Comelco, 31 March 1972 (fl), Stone & Opler 3157 (MO); Comelco Ranch, 10°20-35’N, 85°18-25’W, V-1970 (fr), Hartshorn
910 (MO); Palo Verde, 4-VI-1969 (fr): valle del Tempisque, cerca
del río Lajas, 174-175, 600 m antes de la Escuela de Buenos Aires,
10°19’40”N, 85°03’10’’W, 120 m, 3-VIII-1995 (fr), Ramírez &
Soto 383 (INB). Cantón de Abangares, valle del Tempisque, Abangares, orillas de la carretera Interamericana ruta 1, 173-74, 1 km
después del río Lajas, 10°19’10’’N, 85°02’50’’W, 100 m, 20-IV1991 (fr), Zamora 2281 (MO); valle del Tempisque, orillas de la carretera Interamericana, ruta 1, km 173-174, entre Lourdes y río Lajas, 10°19’10’’N, 85°02’50’’W, 100 m, 28-II-1995 (fl), Zamora &
Mora 2239 (INB). Puntarenas: Cantón de Puntarenas, Hacienda
Santa Marta, Cascajal, along ditch near Cascajal Station (25 km
ESE of Puntarenas), 2-VI-1949 (fr), Holm & Iltis 221 (BM, MO,
U); ridges between río Guacimal and río Lagarto on road from Inter American Highway to Monteverde, 10°16’N, 84°50’W, 8001000 m, 20-IV-1991 (fls), Haber & Zuchowski 10653 (INB, CR),
10656 (INB, CR); Monteverde, valle del río Guacimal, Lindora,
vertiente pacífica, 10°18’N, 84°50’ W, 1000 m, 17-VI-1998 (fr), Bello 402 (CR, MO); Monteverde, road from Santa Elena to village
of San Luis and Lagarto, Pacific slope, moist forest, 10°16’N,
84°50’W, 750-900 m, 10-VII-1990 (fr), Haber 9987 (CR, INB,
MO); Santa Elena to Coyolar de Guacimal, Pacific Slope, roadside
and remnant forest patches of dry forest, 10°15’N, 84°51’W, 250900 m, 16-VII-1988 (fr), Hammel 17111 (CR). R.N.A. Cabo Blanco, estación Cabo Blanco, bosque primario y secundario, 9°35’N,
85°06’W, 20-100 m, 4-XI-1991 (fr), Chavarría 295 (INB, CR,
MO); R.N.A. Cabo Blanco, Camaronal, sendero el Barco,
9°34’42’’N, 85°08’10’’W, 0 m, 25-VI-2001 (fr), Chavarría & al.
2183 (INB); isla San Lucas, golfo de Nicoya, 9°57’N, 84°54’W,
0-400 m, 20-X-1984 (fr), Grayum & al. 4236 (MO); R.N.A. Cabo
Blanco, península de Nicoya, sendero a El Atracadero de San Miguel, 9°35’00’’N,85°07’00’’W, 1-300 m, 17-XII-1993 (fr), Fernán-
13
dez & al. 1300 (INB); golfo de Nicoya, isla San Lucas, entre playa
Cocos y playa Bellavista, 9°57’18’’N, 84°54’11’’W, 20 m, 17-III2005 (fl), Soto & González 539 (INB); Punta Morales, 1-3 m, 19VII-1984 (fr), Gómez-Laurito 10071 (CR). San José: Cantón de
San José, Villa Colón, 800 m, 19-I-1972 (fr), Caffrey 86 (CR); vicinity of Villa Colón, 15-II-1965 (fl), Godfrey 66479 (MO). Cantón
de Mora, Zona Protectora El Rodeo, camino que desciende de la
Universidad a La Paz hacia el río Jaris, pequeños bosquetes a orilla
del camino junto a potreros y cultivos, 9°54’00”N, 84°16’00”W,
500-1000 m, 8-VII-1996 (fr), Cascante 1040 (CR); Z.P. El Rodeo,
valle del Tárcoles, bajo morales, 9°55’00’’N, 84°16’00’’W, 8001000 m, 08-VII-1995 (st), Jiménez & Ramírez 1886 (MO). Cantón
de Acosta, valle del Candelaria, cuenca del río Candelaria, parches
remanentes y potreros cerca del puente, 9°46’50’’N, 84°11’43’’W,
700 m, 19-XI-1994 (fr), Morales 3155 (INB, CR, MO); Cantón de
Orotina, N outskirts of Orotina, 9°55’N, 84°32’W, 200 m, 6-IV1983 (fr), Judziewicz 4559 (CR).
NICARAGUA. Chontales: 0,9 km NE of Hwy 7 on road to Comalapa, ca. 12°10’N, 85°33’W, 160 m, 12-VI-1982 (fr), Stevens &
al. 21570 (MO). Granada: km 75, carretera Sur, 8 km de Nandaime, Llanos el Dorado, 11°41’N, 86°00’W, 70 m, 25-I-1984 (fr),
Moreno & Stevens 22855 (MO); camino de Casa Tejas, 1,2 km antes de la finca San José del Mombacho, 11°46’N, 85°54’W, 40-60
m, 21-VI-1982 (fr), Moreno 16644 (MO); camino a Charco Muerto, 3 km al E de Casa de Tejas, sobre el camino, 100-200 m, 5-VI1980 (fr), Araquistain & Moreno 2855 (MO). Managua: carretera a
Montelimar, comarca Aduana, al N del río Aduana, 80-100 m, 21VII-1980 (fr), Guzmán & al. 410 (MO). Rivas: along road SE from
San Juan del Sur, 3-4 km NW of río La Flor, playa El Coco, quebrada El Coco, 11°09’N, 85°47’W, 0-95 m, 17-XII-1977 (fr), Stevens 5492 (MO).
Agradecimientos
Deseo expresar un profundo agradecimiento a mis colegas
Claudia Aragón, por la preparación de las ilustraciones, y Henk
van der Werff, por su asistencia en la elaboración de la diagnosis en
latín. A Michael H. Grayum, A.M.G.A. Tozzi, Lourdes Rico, D.H.
Janzen y los revisores de esta revista, por sus valiosos aportes, comentarios y sugerencias en una versión preliminar de este artículo.
Además, a todos los herbarios citados, en especial aquellos que albergan colecciones históricas, por facilitarme acceso y ayuda para
el estudio de las mismas.
Esta investigación fue posible gracias al convenio de cooperación entre el Ministerio de Ambiente, Energía y Telecomunicaciones (MINAET) y el Instituto Nacional de Biodiversidad (INBio),
al apoyo económico de particulares y a la red de especialistas taxónomos que contribuyen a completar el Inventario Nacional de Biodiversidad en Costa Rica.
Referencias bibliográficas
Bentham, G. 1860. Synopsis of Dalbergieae, a tribe of Leguminosae. Journal of Linnean Society Botany 4 (Suppl.): 1-28.
Chapman, C.A. 1989. Primate Seed Dispersal: The Fate of Dispersed Seeds. Biotropica 21(2): 148-154.
Evans, S. , Fellows, L.E., Janzen D.H., Chambers, J., & Hider,
R.C. 1985. Erythro-gamma-hydroxyhomo-L-arginine: an amino acid from seed of Lonchocarpus costaricensis, and its preferential interaction with borate. Photochemistry 24: 12891292.
14
N.A. Zamora
Fellows, L.E., Bell, E.A., Lee, T.S. & Janzen, D.H. 1979. Tetrahydrolathyrine; a new amino acid from seeds of Lonchocarpus
costaricensis. Phytochemistry 18: 1333-1335.
Hollis, D. & J.H. Martin. 1997. Jumping plantlice (Insecta: Hemiptera) attacking Lonchocarpus species (Leguminosae), including “Black Cabbage Bark”, in Belize. Journal of Natural
History 31: 237-267.
Janzen, D.H. 1980. Specificity of seed-attacking beetles in a Costa
Rican deciduous forest. Journal of Ecology 68: 929-952.
Janzen, D.H. 1982. Weight of seeds in 1-3 seeded fruits of Lonchocarpus costaricensis (Leguminosae), a Costa Rican winddispersed tree. Brenesia 19/20: 363-368.
Janzen, D.H. 1983. Costa Rican Natural History. University of Chicago Press, Chicago. 816 pp.
Janzen, D.H. 1986. Mice, big mammals, and seeds: it matters who
defecates what where. In: Estrada, A. & Fleming, T.H. (eds),
Frugivores and seed dispersal. Pp. 251-271. Dr. W. Junk Publishers, Dordrecht.
Janzen, D.H. & Liesner, R. 1980. Annotated check-list of plants of
lowland Guanacaste Province, Costa Rica, exclusive of grasses
and non-vascular cryptogams. Brenesia 18: 15-90.
Janzen, D.H., Fellows, L.E. & Waterman, P.G. 1990. What protects Lonchocarpus (Leguminosae) seeds in a Costa Rican dry
forest? Biotropica 22: 272-285.
McVaugh, R. 2000. Botanical Results of the Sessé & Mociño Expedition (1787-1803). VII. A Guide to Relevant Scientific Names
of Plants. Hunt Institute for Botanical Documentation. Carnegie Mellon University, Pittsburgh.
Navarro, C., S. Cavers, N. Colpaert, G. Hernández, P. Breyne &
A.J. Lowe. 2005. Chloroplast and Total Genomic Diversity in
the Endemic Costa Rican Tree Lonchocarpus costaricensis (J.
Donn. Smith) Pittier (Papilionaceae). Silvae Geniticae 54(6):
293-300.
Pittier, H. 1917. The Middle American species of Lonchocarpus.
Contributions from the United States National Herbarium 20:
37-93.
Pittier, H. 1928. Contribuciones a la dendrología de Venezuela.
Árboles y arbustos del orden de las Leguminosas. III-Papilionáceas. Trab. Mus. Com. Venezuela (Bol. Minist. R. R. E. E.
n.º 4-7) 4: 179-259.
Sousa, M. 1990. Adiciones a las Papilionadas de la flora de Nicaragua y una nueva combinación para Oaxaca, México. Annals of
the Missouri Botanical Garden 77: 573-577.
Sousa, M. 2001. Lonchocarpus. In: Stevens, W.D., Ulloa, C., Pool,
A. & Montiel, O. (eds.), Flora de Nicaragua. Monographs in
Systematic Botany from the Missouri Botanical Garden 85(2):
1-2666. Pp. 1017-1028.
Standley. P. 1937-1938. Flora of Costa Rica. Field Museum of Natural History. Botanical Series 18: 1-1571.
Tozzi, A.M.G.A. 1989. Estudos taxonômicos dos gêneros Lonchocarpus Kunth e Deguelia Aubl. no Brasil. Tesis doctoral.
Universidade Estadual Campinas, Campinas.
Tozzi, A.M.G.A. & Silva, M.J. 2007. Sinonimizações em Lonchocarpus Kunth (Leguminosae-Papilionoideae-Millettieae). Rodriguesia 58(2): 275-282.
Waterman, P.G. & Mahmoud, E.N. 1985. Flavonoids from the
seeds of Lonchocarpus costaricensis. Photochemistry 24(3):
571-574.
Editor asociado: L. Rico
Recibido: 17-III-2010
Aceptado: 1-XI-2010
2274 campanula:Maquetación 1 13/06/2011 12:09 Página 15
Vol. 68(1): 15-47
enero-junio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2274
A taxonomic revision of the Campanula lusitanica complex
(Campanulaceae) in the Western Mediterranean region
by
Jara Cano-Maqueda & Salvador Talavera
Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, E-41080 Sevilla, Spain. Corresponding author: [email protected]
Abstract
Resumen
Cano-Maqueda, J. & Talavera, S. 2011. A taxonomic revision of
the Campanula lusitanica complex (Campanulaceae) in the
Western Mediterranean region. Anales Jard. Bot. Madrid 68(1):
15-47.
Cano-Maqueda, J. & Talavera, S. 2011. Una revisión taxonómica del complejo Campanula lusitanica (Campanulaceae) en la región occidental mediterránea. Anales Jard. Bot. Madrid 68(1):
15-47 (en inglés).
The systematics of the annual species of the Campanula lusitanica complex in the Western Mediterranean is reviewed using
ITS sequences, karyology and morphology of all species of the
complex. The information provided by these three sources is
consistent, and the species are reorganized into two groups with
the rank of section: Campanula sect. Rapunculus Boiss. and
Campanula sect. Decumbentes, the latter described as new in
this work. These sections comprise two well-defined subclades
in the phylogenetic analyses. Sect. Rapunculus is composed, in
the W Mediterranean region, by C. lusitanica L. and C. matritensis A. DC., both with 2n = 18 chromosomes, and C. cabezudoi
Cano-Maqueda & Talavera, C. specularioides Coss., C. transtagana R. Fern., and C. broussonetiana Schult., all with 2n = 20
chromosomes. In the Iberian Peninsula, Sect. Decumbentes
comprises two endemic species, C. decumbens A. DC. with
2n = 32 chromosomes and C. dieckii Lange with 2n = 28 chromosomes. In C. decumbens a new subspecies is described:
C. decumbens subsp. baetica Cano-Maqueda & Talavera, which
occurs in the Guadalquivir valley. In the formal systematic part
we provide a key to identify these annual species of the Western
Mediterranean, with a description and typification, photographs
of flowers and fruits, distribution maps, and comments on the
habitat for each taxon.
En este trabajo se revisa la sistemática de las especies anuales del
complejo Campanula lusitanica en el occidente del Mediterráneo usando secuencias ITS, cariología y análisis de los caracteres
morfológicos de todas las especies del complejo. La información
proporcionada por estas tres fuentes de caracteres es congruente, y las distintas especies se reorganizan en dos grupos principales con categoría de sección, que se corresponden con los dos
subclados bien definidos: Campanula sect. Rapunculus Boiss. y
Campanula sect. Decumbentes, descrita como nueva en este
trabajo. En el Mediterráneo occidental, la sect. Rapunculus está
formada por las siguientes especies anuales: C. lusitanica L. y
C. matritensis A. DC., con 2n = 18 cromosomas, y C. cabezudoi
Cano-Maqueda & Talavera, C. specularioides Coss., C. transtagana R. Fern. y C. broussonetiana Schult., con 2n = 20 cromosomas. En la Península Ibérica la sect. Decumbentes está representada por C. decumbens A. DC., con 2n = 32 cromosomas, y
C. dieckii Lange, con 2n = 28 cromosomas, ambas endémicas de
la Península Ibérica; de C. decumbens se describe una subespecie
nueva: C. decumbens subsp. baetica Cano-Maqueda & Talavera,
taxon del valle del Guadalquivir muy bien diferenciado morfológicamente de la subsp. decumbens. En la parte sistemática se
proporciona una clave para la identificación de estas especies
anuales del oeste del Mediterráneo, así como una descripción y
tipificación, fotografías de las flores y frutos, mapas de distribución, y aspectos de la ecología para cada uno de los táxones.
Keywords: phylogeny, rn DNA ITS, karyology, systematic, typification.
Palabras clave: filogenia, secuencias ITS, cariología, sistemática, tipificación.
Introduction
there are also some annual herbs, the latter mainly in
the Mediterranean. This genus has a high morphological complexity that is reflected in the different classifications that have been proposed.
Based mainly on the morphology of the calyx, A. de
The genus Campanula comprises about 420 species
distributed mainly in temperate regions of the Northern Hemisphere (Lammers, 2007a, b). They are usually perennial herbs, although some are shrubby, and
16
J. Cano-Maqueda & S. Talavera
Candolle (1830, 1838) divided the genus Campanula
into two sections: sect. Medium A. DC., with calycine
appendages, and sect. Eucodon A. DC., without them.
This classification was followed by most nineteenth
century authors (e.g. Endlicher, 1838; Willkomm,
1868; Bentham & Hooker, 1876; Rouy, 1908). In contrast, Boissier (1875) divided the genus into two sections based on fruit dehiscence: sect. Medium A. DC.,
with capsules opening by basal pores or valves, and
sect. Rapunculus Boiss., with apical or middle position
pores or valves. This classification was followed with
some modifications by Fedorov (1957, 1976).
Perhaps the taxonomic treatment with most insight
was that by Damboldt (1976) during the preparation
of the Flora of Turkey. He divided the genus Campanula into six subgenera: Campanula, Megalocalyx
Damboldt, Sicyocodon (Feer) Damboldt, Roucela (Dumort.) Damboldt, Brachycodonia (Fedorov) Damboldt
and Rapunculus (Boiss.) Kharadze. The subgenus
Campanula includes plants with 3 or 5 stigmas, with or
without calycine appendages, and with the capsules
opening by basal or middle position pores, or indehiscent. This is the most complex subgenus, with 12-15
recognized sections and it contains most of the species
of the genus. According to Sáez & Aldasoro (2003),
subgenera Megalocalyx and Sicyocodon are annual
herbs with flowers with calycine appendages and with
capsules opening by basal valves; the two subgenera
differ in the size of style: very long (exceeding 35 mm)
in the subgen. Sicyocodon, and short (less than 15 mm)
in the subgen. Megalocalyx. The around 15 species of
these two subgenera are distributed in the Mediterranean Basin, SW Asia and Macaronesia. The subgenus Roucela comprises annual plants, with flowers
without calycine appendages and capsules opening
by basal valves; it consists of 5 species distributed
throughtout the E Mediterranean and SW Asia, with
the exception of C. erinus L. which has a wider distribution. The subgenus Brachycodonia comprises only
C. fastigiata Dufour, an annual plant with axillary inconspicuous flowers, without calycine appendages,
and with capsules opening by three apical valves;
C. fastigiata occurs on gypsum soils in Spain, N Africa,
C Asia and Transcaucasia.
The subgenus Rapunculus includes annual and
perennial plants, without calycine appendages, with a
large campanulate or infundibuliform corolla, and
with capsules opening by apical or middle position
pores. Damboldt (1976, 1978) divided this subgenus
in three sections: Pterophyllum Damboldt, Alaria
Damboldt and Rapunculus. Sect. Pterophyllum includes three species: C. primulifolia Brot. (Iberian
Peninsula), C. alata Desf. (Algeria and Morocco), and
C. peregrina L. (E Mediterranean, including Cyprus,
Lebanon and SW Turkey and S Anatolia); they are
hispid perennial plants with large infundibuliform
flowers, arranged in spikes or panicles, with capsules
opening by three pores of middle position, and with
winged seeds.
Sect. Alaria contains a single species, C. pterocaula
Hausskn., endemic to N and C Anatolia (Turkey); it is
a biennial glabrous plant, with winged stems, large
flowers arranged in spiciform inflorescences, and capsules opening by apical pores.
Sect. Rapunculus contains around 50 species distributed mainly in the Mediterranean region; it comprises perennial, biennial or annual plants, glabrous
or tomentose, with wingless stems, the inflorescence a
panicle, or sometimes spiciform, the capsules opening
by apical or middle position pores, and wingless
seeds.
Recent molecular phylogenies (Eddie & al., 2003;
Park & al., 2006; Roquet & al., 2008, 2009; Cellinese &
al., 2009; Borsch & al., 2009; Haberle & al., 2009; Stefanović & Lakušić, 2009) have revealed that the genus
Campanula is paraphyletic. Studies by Roquet & al.
(2008) using ITS sequences, show that Campanula
sect. Pterophyllum together with the genera Musschia
Dumort. and Gadellia Schulkina form a clade (Musschia clade) that is sister to the Campanula core.
The Campanula core consists of two subclades: one
formed by the subgenera Campanula, Megalocalyx
and Roucela, together with other genera of Campanulaceae; and a second subclade comprising subgenus
Rapunculus (sections Rapunculus and Alaria) and subgenus Brachycodonia, again with some other genera of
Campanulaceae.
The annual species of sect. Rapunculus sensu
Damboldt have two centers of diversity: the Iberian
Peninsula and W Morocco, and the E Mediterranean
(Greece and Turkey). The annual species of the Iberian Peninsula (which include many species names,
viz. C. lusitanica L., C. broussonetiana Schult., C. transtagana R. Fern., C. matritensis A. DC., C. decumbens
A. DC., C. specularioides Coss. C. cabezudoi CanoMaqueda & Talavera and C. diekii Lange) have received diverse treatments in recent taxonomic studies,
i.e as varieties of Campanula patula L. (Pau, 1921;
Cuatrecasas, 1929), as subspecies or varieties of C. lusitanica L. (Pau, 1924; Sáez & Aldasoro, 2001), or as varieties of C. decumbens A. DC. (López-González,
1979-1980). In all cases most taxa have been relegated
to infraspecific status.
However, our detailed morpho-geographical analysis of the exsiccata available for this group (which we
call the Campanula lusitanica complex) lead us to con-
Taxonomic review of the Campanula lusitanica complex
clude that not only are many of the species described
by various authors valid, but that several new taxa can
be recognised. Moreover, our analyses (Cano-Maqueda & al., 2008 and the present study) based on combined analysis of ITS sequences and trnT-L using
samples from most of the annual species of the Western Mediterranean area not only support recognition
of these species, but have also revealed that the annual species of sect. Rapunculus sensu Damboldt comprise a polyphyletic assemblage.
In this study we present a formal taxonomic revision of the Campanula lusitanica complex from the
Iberian Peninsula and Morocco, based on our studies of exsiccata, karylogical parameters, and molecular markers. And using information provided by the
nrDNA ITS for a large number of Campanula species
and allied taxa we have also attempted to place the
species of Campanula sect. Rapunculus sensu Damboldt within the context of the ongoing molecular systematics of the genus Campanula.
Materials and methods
Molecular Phylogeny
Fresh material and herbarium vouchers of seven
samples of the Campanula lusitanica complex (four of
C. lusitanica s.str., one of C. decumbens, one of C. sparsa
Friv., and one sample of C. ramosissima Sibth. & Sm.),
two samples of C. primulifolia and one of Walhenbergia
hederacea L., were sequenced for this molecular survey.
Additionally, 100 sequences were taken from GenBank
(Eddie & al., 2003; Susanna & al., 2006; Roquet & al.,
2008, 2009; Cano-Maqueda & al., 2008; Park & al.,
2006). The list of taxa, with locality, herbarium vouchers or collector’s numbers, authorities and GenBank
accession numbers is shown in the Appendix I.
Genomic DNA was extracted from silica-gel-dried
leaves collected in the field and from herbarium material using the DNeasy Plant Mini Kit (Qiagen) following the protocols provided by the manufacturer.
Amplification of the ribosomal ITS region (ITS15.8S-ITS2) was performed in 25 µL reaction volume
with 22.5 µL Thermo-Start ReddyMix Master Mix, 0.5
µL of each primer, 1 µL of DMSO (100%) and 0.5 µL
of DNA. Forward ITS5 and reverse ITS4 primers
(White & al., 1990) were used in the amplification and
sequencing processes. The polymerase chain reaction
(PCR) sequence profile was one cycle of 1 min at 96 ºC,
followed by 35 amplification cycles of 10 s denaturing
step at 96 ºC, 5 s annealing at 50 ºC, and 3 min elongation step at 60 ºC, plus an ending cycle of 8 min at 72 ºC.
Amplified products were purified using the QIAquick PCR Purification Kit (Qiagen) according to
17
the manufacturers protocols. Purified products were
sequenced in both directions. The sequence PCR profile was of a time of incubation of 15 min at 37 ºC and
15 min at 80 ºC.
The direct and reverse sequences of each sample
were compared and corrected using the program
Geneious 4.8.3, obtaining the respective consensus
sequence. Sequences were aligned using the algorithm of the program ClustalX, and then adjusted
manually using the options of the program Se-Al v. 1.0
alpha 1 (Rambaud, 1996). Gap indels were coded as
binary characters by their presence/absence (0/1 matrix). Only those gaps that were unambiguous and potentially informative (Torrecilla & Catalán, 2002)
were added to their correspondent sequence matrix
and used for parsimony-based analysis.
Phylogenetic analyses
The phylogenetic analyses were based on parsimony
and Bayesian inference searches, which were respectively conducted with PAUP* v. 4.0 beta 10 (Swofford,
2002) and MRBAY ES v. 3.0 (Huelsenbeck & Ronquist, 2002) using Galactites tomentosa Moench.
(Compositae) to root the trees.
In the parsimony analysis, the data matrix was subjected to two heuristic searches (first search: closest,
TBR, MULTIPARS ON; second search: randomorder-entry of 10,000 replicates, TBR, MULTIPARS
OFF, saving no more than 10 trees of score > 10 per
replicate) aimed at finding different putative islands
of most-parsimonious trees. Bootstrap support for the
best trees found under the parsimony criterion was estimated by heuristic search with 1,000 bootstrap
replicates (Felsenstein, 1985) using the TBR and
MULTIPARS OFF strategy proposed by DeBry and
Olmstead (2000) to reduce the tree-search effort in
bootstrap resampling analysis. Initial MaxTrees setting was 300,000 with an auto-increase of 100. Previous to the Bayesian inference search, 24 models of nucleotide substitution were tested for which the optimal model GTR + G + I. The Bayesian analysis was
performed through 1,100,000 generations using the
Markov chain Monte Carlo (MCMC), sampling trees
every 100 generations and burn-in all sampled point
from generations previous to convergence to a stable
likelihood value (Huelsenbeck & Ronquist, 2002;
Leaché & Reeder, 2002). From each search, a 50%
majority-rule consensus tree that showed de posterior-probability values of branches was constructed.
Karyological study
Plants or seeds of each taxon of the Campanula lusitanica complex sensu Cano-Maqueda & al. (2008),
18
were collected from natural populations (Table 1) and
cultivated in the greenhouses of the University of
Seville. Chromosomes were observed from meristematic cells of root tips or meiosis in the anthers of flower
buds. The root tips were treated with 8-hidroxiquinoleine 0,002M for three hours and a half at 4 ° C.
Subsequently, roots and flower buds were fixed with
Carnoy solution (3:1 ethanol 96%: glacial acetic acid)
for a minimum of 24 hours. Staining of chromosomes
was performed with-alcoholic-hydrochloric carmine
(Snow, 1963). The images were taken with a Leica DC
300 inserted in a Zeiss Axiophot microscope with
Plan-apochromatic objective 63/1.4 and an increase
of 1.25. Levan & al. (1964) were followed for the morphological terminology and Stebbins (1938) for size
terminology of the chromosomes.
Systematic Treatment
A morpho-geographical analysis of herbarium
specimens of all relevant taxa associated with the C.
lusitanica complex was performed, based on the following Herbaria: C, COI, FCO, G, HVR, LISE,
LISU, MA, MGC, P, SALA, SALAF, SEV, W. All recognized species and most heterotypic synonyms have
been typified. The initials of the provinces of Spain
and Portugal which are cited in the description of
each taxon follow those used in “Flora iberica”.
Results and discussion
Molecular Phylogeny
The ITS region comprised 726 aligned nucleotide
positions of which 469 were variable and 368 were
parsimony informative. The first heuristic search
found 101,914,528 equally parsimonious trees that
were 2,480 steps long, with a consistency index of
0.353, excluding uniformative characters, and a retention index of 0.748. The second search did not find
any other island of most-parsimonious trees, and trees
from the first search were used to compute the strict
consensus tree. The Bayesian analysis sampled 7,639
trees, which reached a stable likelihood value after
burn-in 1,500 trees. The 50% majority-rule consensus
tree of all sampled trees showed a topology totally
concordant with that recovered from the parsimony
analysis. The Bayesian tree was better resolved than
the parsimony-based tree, so only the Bayesian tree
with both bootstrap and posterior probability support values for branches is shown in Fig. 1.
Topology within the ITS tree is consistent with results obtained in previous phylogenetic studies of the
genus Campanula and allies (Eddie & al., 2003; Park
& al., 2006; Roquet & al., 2008, 2009; Cellinese & al.,
2009; Haberle & al., 2009; Stefanović & Lakušić,
2009). These show that the genus is paraphyletic and
divided into two major clades, the ‘Campanula s.str.’
clade and the ‘Rapunculus’ clade, plus two small
clades: the ‘Musschia’ clade (99% bootstrap support,
BS; 100% posterior probability support, PPS), that
includes Musschia Dumort., Gadellia Schulkina, Campanula peregrina and Campanula primulifolia; and
the ‘Platycodon’ clade (79%BS; 100%PPS), that includes Codonopsis Wall., Cyananthus Wall., Canarina
L. and Leptocodon Hook. The genus Jasione L. is
sister to Campanula s. l. The ‘Campanula s. str.’ clade
has good support (72%BS; 100%PPS) although it
Table 1. Chromosome numbers for annual species of the Campanula luisitanica complex in the W Mediterranean area. Origin of material, gametic (n) or somatic (2n) chromosome number of and authors who have studied the different annual species in this complex.
Taxa
C. lusitanica
Studied material
Rivadavia (Orense, Spain)
Serra de Lousã (Beira Litoral, Portugal)
C. matritensis
Hervás (Cáceres, Spain)
Hinojos (Huelva, Spain)
Coimbra (Beira Litoral)
C. cabezudoi
Venta de Zafarraya (Granada, Spain)
C. specularioides
C. transtagana
C. broussonetiana
Ubrique (Cádiz, Spain)
Benaocaz (Cádiz, Spain)
Montejaque (Málaga, Spain)
Valverde (Huelva, Spain)
Vila Velha de Rodão (Beira Baixa, Portugal)
Don Benito (Badajoz, Spain)
n
2n
Authors
9
18
18
In this work
Fernandes (1962)
18
18
Fernández et al. (2001) (as C. lusitanica)
In this work
Larsen (1954) (as C. loefingii)
9
10
10
Jbel Tazzeka (Taza, Morocco)
C. decumbens
Benaoján (Málaga, Spain)
Villamartín (Cádiz, Spain)
C. dieckii
Alfarnate (Málaga, Spain)
20
In this work
20
García-Martín & Silvestre (1985)
Gallego (1986)
In this work
10
10
20
20
In this work
Fernandes (1962)
Gallego (1986) (as C. lusitanica subsp. transtagana)
20
In this work
16
16
In this work
In this work
28
In this work
19
Fig. 1. Bayesian 50% MR concensus tree topology of Campanulaceae ITS. Bootstrap and posterior probability values are indicated on corresponding branches. Symbols indicate the habit of the species: ●, annual; ⽧, biennial; 䊱, perennial. The two sections that are the focus of this
article are marked in gray. The chromosome numbers shown for the species that are not are specified in the text, derive from indices of plant
chromosome number (Castroviejo, S. & Valdés-Bermejo, E. (eds.). 1991. Archivos de Flora iberica I: números cromosomáticos de plantas vasculares ibéricas. CSIC. Madrid; Index to plant chromosome numbers. Monographs in Systematic Botany from the Missouri Botanical Garden
[www.tropicos. org]; Moore, D.M. 1982. Flora Europaea. Checklist and chromosome index. Cambridge University press).
20
showed little internal resolution. This clade includes
species of Campanula subgenera Campanula and
Roucela and the genera Diosphaera Buser, Azorina
Watson, Edraianthus A. DC., Michauxia L’Hér., Trachelium L., Symphyandra A. DC., and Feeria Buser.
The two genera Heterocodon Nutt. and Githopsis
Nutt. form a small clade, (the ‘Githopsis’ clade,
99%BS; 100%PPS) that appears between the ‘Campanula s. str.’ and ‘Rapunculus’ clades.
The ‘Rapunculus’ clade forms a monophyletic and
strongly supported group (100%,BS; 100%PPS),
and as with the ‘Campanula s. str.’ clade, it includes
taxa treated as separate genera [Hanabusaya Nakai,
Adenophora Fisch., Legousia Durande, Triodanis
Rafin., Campanulastrum Small, Asyneuma Griseb. &
Schenk, Phyteuma L., Physoplexis (Endl.) Schur.,
Petromarula R. Hedw.] in addition to many species of
Campanula. It comprises five principal well-resolved
subclades: one subclade (100%BS; 100%PPS) corresponds to the ‘garganica’ subclade of Park & al.
(2006); two subclades, ‘rotundifolia’ and ‘pulla’ subclade (81%BS; 100%PPS and 51%BS; 93%PPS) include the isophyllous and heterophyllous species of
Park & al. (2006); And the other two subclades both
include elements of the Campanula lusitanica complex of Cano-Maqueda & al. (2008) which we have
called the ‘decumbens’ subclade and the ‘lusitanica’
subclade.
The ‘decumbens’ subclade (67%PPS) is formed
by C. ramosissima and C. hawkinsiana Hausskn. &
Heldr., that are sister to C. decumbens and C. dieckii Lange. The ‘lusitanica’ subclade (100%BS;
100%PPS) corresponds to the ‘lusitanica’ lineage of
Cano-Maqueda & al. (2008). In this subclade, C. patula, C. sparsa and C. rapunculus L. are sister to C. matritensis A. DC., C. lusitanica s. s., C. cabezudoi CanoMaqueda & Talavera, C. specularioides Coss., C.
transtagana R. Fern. and C. broussonetiana Schult. The
four samples of C. lusitanica s.str. (from three different
populations, see Appendix I) collapse into a moderately supported subclade (66%BS; 77%PPS) and they
appear as sister to C. matritensis in a well supported
clade (100%BS; 100%PPS). Moreover, C. lusitanica
s.str. presents morphological differences with C. matritensis, and it has a more restricted geographical distribution than the latter (see systematic treatment), so
we have treated these two as separate species.
Karyological study
All species of ‘lusitanica’ subclade have 2n = 20 or
n = 10 chromosomes, except C. matritensis and C.
lusitanica with 2n = 18 or n = 9. The taxa of ‘decumbens’ subclade, C. decumbens and C. dieckii, have 2n
= 32 or n = 16 and 2n = 28 chromosomes, respectively (Table 1). All species studied have small or moderately small chromosomes (1.2-4.1 µm), with the centromere located in the middle or submid region (Fig.
2). In C. specularioides, one pair of chromosomes with
the centromere in the submiddle region has a satellite
on the short arm. Chromosomes form bivalents in the
meiotic metaphase.
The basic number found in annual species of the
‘lusitanica’ subclade in the W Mediterranean, x = 10,
coincides with that found in other species of this subclade: C. rapunculus, C. patula and C. sparsa (Larsen,
1956; Contandriopoulos, 1966). The basic number
x = 9 found in C. lusitanica and C. matritensis can be
considered as aneuploid of x = 10. The base number
n = 10 is extremely rare in Campanulaceae, and has
only been previously reported for C. ramosissima
(Podlech & Damboldt, 1964). The chromosome number found in C. dieckii, 2n = 28, has been previously
found in the subgenus Roucela sensu Damboldt, in
C. erinus (Gallego, 1986) and C. drabifolia Sibth. &
Sm. (Contandriopoulos, 1964a), and in C. edulis
Forssk. (according to Goldblatt & Johnson, 1990), all
species of ‘Campanula s. str.’ clade, and also in C. arvatica Lag. (Podlech & Damboldt, 1964), a species of
‘Rapunculus’ clade (Fig. 1). The chromosome number
found in C. decumbens, 2n = 32, is also found in some
species of the ‘Rapunculus’ clade, [C. raineri Perpenti
(Podlech & Damboldt, 1964), C. fragilis Cyr. (Damboldt, 1965), C. isophylla Moertti (Merxmüller &
Damboldt, 1962), C. herminii Hoffmans. & Link
(Damboldt & Podlech, 1964), and C. stevenii Bieb. (according to Goldblatt, 1985), and Edraianthus graminifolius (L.) A. DC. (Contandriopoulos, 1964b), a taxon of the ‘Campanula s. str.’ clade, and Musschia aurea
Dumort. (according to Goldblatt & Johnson, 1994), a
taxon of ‘Musschia’ clade]. Since 2n = 34 is the most
frequent number in Campanulaceae, it seems likely
that 2n = 32 is an aneuploid of 2n = 34 (see Fig. 1).
Systematic treatment
After reviewing all specimens we found that the different species can be separated in two groups on basis
on the morphology of the style and stigma: one
formed by C. decumbens and C. dieckii, with the style
glabrous and with three stigmas with arms straight
and erect or erect-patent; and another formed by all
other species, with the style hairy in the upper half,
and a trifid stigma, with the stigmatic arms curved or
circinate. These two groups are consistent with the
molecular results and karyology, so that they are probably natural, and the most appropriate taxonomic
treatment is to recognise them as sections. The second
21
Fig. 2. Karyology of Campanula species. A-F and I, mitotic metaphase; G, meiotic anaphase I; H, meiotic metaphase I. A, C. lusitanica, 2n = 18 (Rivadavia, Orense, Spain, SEV 218947); B, C. matritensis, 2n = 18 (Hinojos, Huelva, Spain, SEV 216214); C, C. cabezudoi, 2n = 20 (Venta de Zafarraya, Granada, Spain, SEV 218873); D, C. specularioides, 2n = 20 (Montejaque, Málaga, Spain,
SEV 216210); E, C. transtagana, 2n = 20 (Valverde del Camino, Huelva, Spain, SEV 216212); F, C. broussonetiana, 2n = 20
(Jbel Tazzeka, Taza, Morocco, SEV 216476); G, C. decumbens, n = 16 (Benaoján, Málaga, Spain, SEV 218875); H, C. decumbens, n = 16 (Villamartín, Cádiz, Spain, SEV 256653); I, C. dieckii, 2n = 28 (Alfarnate, Málaga, Spain, SEV 256652). The scale
bar = 20 µm.
22
group, which includes Campanula rapunculus L.,
would constitute the sect. Rapunculus. The first group
would establish a new section, sect. Decumbentes
which is formally described below. Within these sections, the most significant characters are: the shape of
the corolla (campanulate or infundibuliform), middle
cauline leaves (petiolate or sessile), capsule morphology (obpyramidal, subglobose or subovoid), and
ovary indumentum (setose, glabrous or papillose).
We used this combination of characters to create a
key for the identification of all annual species of the
C. lusitanica complex in the Western Mediterranean.
KEY TO THE SPECIES
1. Style 2.1-4(4.8) mm, glabrous, with three stigmas; stigmas
straight, erect or erect-patent ........................................... 2
1. Style (4.5)5-14 mm, hairy in the upper half, with one trifid
stigma; stigmatic branches curved or circinate, patent ....... 3
2. Stems glabrous or with few antrorse hairs, often scabrid near
the flowers; upper cauline leaves cuneate or shortly petiolate;
corolla 12-21 mm ................................... 7. C. decumbens
2. Stems densely pubescent with setose hairs, sometimes
glabrescent towards the apex; upper cauline leaves sessile,
subauriculate; corolla (6.6)8-13.7 mm ............. 8. C. dieckii
3. Corolla infundibuliform, with three purple nerves in each
lobe; middle cauline leaves petiolate; plant decumbent ..... 4
3. Corolla campanulate, without purple nerves in the lobes;
middle cauline leaves sessile or petiolate; plant erect or decumbent .......................................................................... 5
4. Capsule 2-3 × 3-4.5 mm, subspherical, generally glabrous,
dehiscing by 3 pores of middle position, with 10 subwinged
nerves; stems and leaves glabrous or glabrescent; calyx-teeth
oblanceolate ...................................... 4. C. specularioides
4. Capsule 2.1-5.9 × 2.2-5 mm, ovoid or subspherical, usually
densely hairy, dehiscing by three apical pores, with 10 ±
acute but non-winged nerves; stems and leaves pubescent;
calyx-teeth lanceolate or linear .................. 3. C. cabezudoi
5. Middle cauline leaves petiolate and elliptic or sessile and
cuneate ............................................................................ 6
5. Middle cauline leaves sessile, ovate-lanceolate or lanceolate ................................................................................. 7
6. Upper half of the stem and leaves with short hairs 0.1-0.3
mm; middle cauline leaves with petiole 0.2-4.5 mm .............
............................................................... 5. C. transtagana
6. Upper half of the stem and leaves with long hairs, the longest
0.4-2 mm, or rarely glabrous; middle cauline leaves sessile
and cuneate or with petiole up to 2 mm and rounded at the
base ................................................. 6. C. broussonetiana
7. Middle cauline leaves ovate-lanceolate, subauriculate, densely patent-hairy, with long hairs up to 0.8-1.1 mm; capsule subovoid, with 10 subwinged acute nerves ....... 1. C. lusitanica
7. Middle cauline leaves lanceolate, glabrous or with sparse
hairs 0.1-0.5 mm; capsule obpyramidal, with 10 very wide
nerves, like flat ribs .................................. 2. C. matritensis
A. Sect. Rapunculus Boiss., Fl. Orient. 3: 895. 1875
Campanula subgen. Rapunculus (Boiss.) Kharadze in
Zametki Sist. Geogr. Rast. Tiflis 28: 100. 1970
Type: C. rapunculus L.
Annual or biennial plants. Lower leaves oblanceolate or spathulate, petiolate. Without calycine appendages. Corolla campanulate or infundibuliform.
Stamens with white or blue anthers. Style with numerous pollen collecting hairs on the upper half, with
a trifid stigma; stigmatic arms curved or circinate,
patent, white or blue, with numerous pollen collecting hairs on the abaxial surface glabrous, and receptive on the adaxial surface. Capsule subspherical,
ovoid or obpyramidal, dehiscing by three apical or
middle position pores. x = 9, 10 (see karyology).
Observations: This section includes: Campanula rapunculus and C. patula of the Mediterranean region;
C. lusitanica, C. matritensis, C. cabezudoi, C. specularioides, C. transtagana and C. broussonetiana from
the W Mediterranean; and C. sparsa and possibly
C. spatulata Sibth. & Sm. of the E Mediterranean.
The section is monophyletic (see lusitanica clade in
Fig. 1).
Experimental manual crosses showed that all annual species of the W Mediterranean had hybridization
barriers at different levels: (1)- fruits were not produced, (2)- seeds do no germinated, (3)- germinated
seeds formed chlorotic seedlings which did not survive and (4)- no chlorotic seedlings survived after the
cotyledon state but they did not complete their development (Cano-Maqueda unpublished studies).
1. Campanula lusitanica L. in Loefl., Iter Hispan.:
111, 126. 1758
Campanula loeflingii Brot., Phytogr. Lusitan. Select.
Fasc. I: 20. 1800, nom. superfl. C. patula var. lusitanica (L.) Pau in Bol. Soc. Iber. Ci. Nat. 20: 181.
1921. Ind. loc.: “Habitat in Lusitania ad Porto in
collibus & muris”. Type: Portugal. Porto, June
1917, Mário de Castro s.n. [Sennen, Pl. Espagne n.º
3305] (neotype, here desinated, G 104248!, Fig. 3;
see observations).
C. duriaei Boiss., Voy. Bot. Espagne 2: 402. 1839. Ind.
loc.: “Hab. In Hispaniâ circà Olyssiponem (L. Et
Hoffm.), Hispaniâ septentr. In Asturiis (Durieu)”.
Type: Spain. Asturias, Cangas de Tineo, 25 July
1835, Durieu s.n. [Plant. Select. Hispano-Lusit.
Sect. 1ª n.º 280] (lectotype, here designated,
G 104093!; see observations).
C. loeflingii var. occidentalis Lange in Vidensk. Meddel. Dansk Naturhist. Foren. Kjøbenhavn 1861:
107, 108. 1862. Ind. loc.: “In Gallecia frequent!”.
Type: Spain. Galicia [not found in the Lange herbarium (C)].
C. lusitanica var. puberula C. Vicioso in Anales Jard.
Bot. Madrid 6: 78. 1946. Ind. loc.: “Hab. Ribadelago (Zamora)”. Type: Spain. Zamora, Ribaldelago,
19 July 1945, C. Vicioso s.n. (lectotype, here designated, MA 121525!; see observations).
Illustrations: Fig. 4 A, B.
Herb 16-50 cm, annual, erect, branched from the
base, rarely in the upper half, densely pubescent, not
brittle. Stems angled, branched or simple, densely pubescent, rarely glabrescent in the uppermost portion,
with short and long hairs, the longest 0.5-1.5 mm.
Leaves somewhat coriaceous, entire, crenulate or
toothed; middle cauline leaves 5-30 × 3.1-10.9 mm,
sessile, ovate-lanceolate, subauriculate, entire or
toothed, densely pubescent, ± long hairs, the longest
0.8-1.1 mm; upper cauline leaves 4-14.5 × 0.5-4.4 mm,
sessile, lanceolate, truncate or somewhat auriculate,
pubescent, with hairs up to 0.9 mm. Inflorescence
paniculate, highly branched, lax or dense and spiciform. Flowers pedicellate or subsessile; pedicel (3)716 mm, glabrous or with hairs 0.1-0.2 mm. Calyxteeth 3.7-9(17.3) × 0.4-0.6(1.3) mm, linear, recurved
in the female phase flower. Corolla (8.2)10-18.9 mm,
campanulate, with tube longer or shorter than lobes;
tube 3.5-9.7 mm, blue at the apex, white at the base;
lobes 3.7-9.2 × 2.2-6.1 mm, elliptic-lanceolate, not re-
Fig. 3. Neotype of Campanula lusitanica (G 104248).
23
flexed in the female phase flower, blue. Stamens with
enlarged base of 0.6-1 × 0.4-0.5 mm; filaments 0.2-0.5
mm; anthers (1.5)3-5 mm, whitish. Ovary papillose or
with setose hairs of 0.1-0.2 mm; style 7.5-11.8 mm,
hairy in the upper half; stigma trifid, with stigmatic
branches of 0.3-1.2(2.8) mm, patent, circinate, white.
Capsule (2.4)4-6 × (2.5)3-4 mm, subovoid, longer
than wide, papillose, rarely with some setose hairs 0.10.2 mm, with 10 subwinged and acute nerves, dehiscing by three apical pores. Seeds 0.3-0.5 × 0.2-0.3 mm,
ellipsoid, shining, yellowish to brown. 2n = 18; n = 9.
Habitat, phenology and distribution: Wet grasslands
on generally acid substrates, sometimes draining and
river banks; 15-1800 m. (V)VI-VIII. • Endemic to the
NW of the Iberian Peninsula, common in Galicia and
N Portugal, and also occurring in S Portugal, Monchique (Fig. 5). Portugal: Ag BA BL DL Mi TM.
Spain: C Le Lu O Or Po Sa Za.
Observations: López-González (in litere) has commented apropos the type of Campanula lusitanica: “Al
parecer, Linneo no conoció nunca Campanula lusitanica, porque dicha planta no figura en la lista de materiales de Loefling enviados a Linneo en 1752 (Spanish
list), pero en una carta de Loefling a Linneo, fechada
el 7.VII.1751 y escrita en Oporto, le indicó que «Campanula caule angulato, ramoso, vago, calice corollae
tubulosae aequali», la que Linneo denominaría
C. lusitanica, habita aquí [Porto] en los caminos y en
las tapias. Tampoco figura esta planta ni como Campanula lusitanica ni como «Campanula caule angulato…» en la lista del herbario de Loefling que redactó
un capellán sueco, probablemente porque en esta lista
solo figuraban las plantas identificadas, y «Campanula caule anguloso…» aún no tenía nombre. Es en el
herbario de Loefling donde se podría encontrar la
planta como Campanula sp., pero este herbario lo
perdió Casimiro Gómez Ortega, que al parecer, según
cuenta en una carta, lo prestó a un botánico francés y
éste no lo devolvió”.
Since it was impossible to find the type material of
C. lusitanica in the different Linnean herbaria, the
election of a neotype has been proposed. The plants in
question have long and patent cauline hairs, and so do
not correspond to the plant described by Loefling,
who indicates “Caulis … leviter hispidus pilis pallidis,
brevissimis”. The shape of the cauline leaves, ovateoblong or ovate-lanceolate, are however like those of
the plants described by Loefling, who indicates “Folia
caulina & subramorum ovato-oblonga, subglabra,
sessilia, subserrata, alterna; ramorum superiora ovatolanceolata, vix serrata” and the whitish colour at the
base of the corolla tube is also consistent with the description of Loefling: “Cor. caeruleis, tubulo infimo
24
brevísimo albo”. In accordance with these characteristics, we have chosen the plants from Porto as neotype of Campanula lusitanica.
Brotero (1800: 20-21) gave a new name, C. loeflingii, to the plant collected in Porto by Loefling, but
this name is illegitimate, since Linneus had named it
as C. lusitanica in the work of Loefling. Brotero (1804:
287) subsequently not only described the Loefling
plant, but also included characters from another
species later described by Alphonse De Candolle
Fig. 4. Flowers and fruits of Campanula species. A, B, C. lusitanica (Rivadavia, Orense, Spain, SEV 218947); C, D, C. matritensis (Hinojos, Huelva, Spain, SEV 261264); E, F, C. cabezudoi (Venta de Zafarraya, Granada, Spain, SEV 218873). The scale bar = 3 mm.
(1830) as C. matritensis. Indeed, the illustration that
appears in his “Phytographia Lusitanieae Selectior”
(Brotero, 1816, tab. 18) corresponds more closely to
C. matritensis than to C. lusitanica. Hoffmannsegg &
Link (1820-1824: 14) also provided a brief description of C. loeflingii, but like Brotero, they could be referring to both C. lusitanica and C. matritensis.
Boissier (1839) described C. duriaei based on the
characters of plants collected by Durieu in Cangas
de Tineo (Asturias) distributed as the Exiccata No
280 in 1835. In the herbarium at Geneva there are
three sheets of this collection (G 104093, G 104120 y
G 104116). The first (G 104093) consists of 4 complete plants mounted on two sheets, and comes from the
Boissier Herbarium. One of the sheets contains two
plants of 30 cm and 22 cm respectively, and a Boissier
handwritten label indicating “C. Duriaei/284”. We
have chosen as lectotype the 30 cm plant because it is
the closest to the description; the other plant, of 22
cm, is an isolectotype. The other sheet also contains
two plants without any annotation by Boissier; they
are also likely isolectotypes. The other two sheets (G
25
104120 and G 104116) are from the herbarium of
Moïse-Etienne Moricand which were incorporated
into the herbarium of the Conservatoire et Jardín
Botanique de Genève in 1908; the plants contained in
them, which were not seen by Boissier, are not part of
the type material. Boissier was the first author to clearly describe the characteristic hairs of the Asturian
plants: “Toute la plante est d’une consistance délicate
et couverte de poils long et étalés, tandis que la C. loeflingii est u glabre ou hérissée de poils rudes et
courts”. Boissier’s concept of C. loeflingii was very
wide, since he included in this species most of the taxa
of this group which had been collected by him in
southern Spain or that he had seen in the Fouche or
De Candolle herbaria. We identify Fouche herbarium
plants as C. decumbens subsp. baetica Cano-Maqueda
& Talavera and those in the De Candolle herbarium
as C. broussonetiana, and the plants that he collected
in Southern Spain as C. matritensis and C. dieckii (see
these species below).
The type material of C. lusitanica var. puberula consists of three plants mounted on the same sheet. We
Fig. 5. Distribution map of Campanula lusitanica (䊱) and C. matritensis (䡬).
26
have chosen as lectotype the larger specimen mounted on the left, and the other two plants are isolectotypes
Campanula lusitanica is very similar in the indumentum and the branching to C. broussonetiana, but
C. lusitanica has 2n = 18 chromosomes, as does C. matritensis, while C. broussonetiana has 2n = 20 chromosomes, as do almost all species of sect. Rapunculus.
The ITS phylogenetic tree shows that C. lusitanica
and C. matritensis are sister species (see Fig. 1).
Selected specimens
PORTUGAL. Algarve: Serra de Monchique, entre Monchique
e Alferce, Rouxinel, 27-VI-1978, M. Beliz (MA 270314); ibidem, de
Pesos a Monchique, 24-VII-2009, S. & M. Talavera (SEV 248712).
Beira Alta: Figueira de Castelo Rodrigo, Escalhão, 26-V-1996, M.
Santos & M. Sequeira (HVR 8048). Serra da Estrela, without date,
Romariz (LISU 2054); ibidem, Garganta de Loriga, VIII-1912,
A.A. Silva Martins (LISU 36386). Vizeu, Santa Comba Dão, Pinheiro de Azer, arredores da ponte sobre a barragem, 20-VI-1982, A.
Marques (MA 377387). Beira Litoral: Coimbra, Penacova, Oliveira
do Mondego, 13-V-1982, A. Marques (MA 391392). Douro Litoral:
entre Oliveira y San Joao de Madeira, dirección Oporto, 24-VI1986, J.A. Devesa & al. (SEV 161720). Porto, Castelo prox. Souto
de Lafões, 27-V-1940, recolector ilegible (LISU 36362). Minho: Ancora, VI-1886, A.R. da Cunha (LISU 36367). Areosa, VI-1886, A.R.
da Cunha (LISU 36404). Barcelos, VI-1886, A.R. da Cunha (LISU
36368). Caldas do Gerez, IX-1882, M.L. Enriques (COI). Caminha,
Retorta, VI-1885, A.R. da Cunha (LISU 36379). Celorico de Basto,
VI-1884, A.R. da Cunha (LISU 36380). Entre Ponte de Barca y Vila
Verde, 27-VI-1982, M.J. Gallego & al. (SEV 161716). Fafe,
Lameira, 7-VIII-1977, M. Beliz (MA 270317). Gondarem, VI-1885,
A.R. da Cunha (LISU 36377). Melgaço, VI-1894, A. Moller (COI).
Monção, Lavandeira, VI-1885, A.R. da Cunha (COI, LISU 36407).
Ponte de Lima, VII-1894, M. Rodr. Maraes (COI). Povoa de Lanhoso, VI-1920, J. Sampaio (MA 121499). Senhora da Peneda, Serra
do Soajo, VII-1890, A. Moller (COI). Serra Amarela, Mata do
Cabril, Carvalhal do Sono, 8-VIII-1977, M. Beliz & J. Guerrero
(MA 270316), Serra da Peneda, 880m, VI-1956, R. Bentos (LISE
48610). Serra do Gerez, 2-VII-1948, Romariz (LISU 922). Soajo,
Serra do Soajo, VI-1890, A. Moller (COI). Vanlença, Olivar de Santa Barbara, VI-1885, A.R. da Cunha (LISU 36403). Veiga de
Chaves, V-1910, F. Mendez & al. (LISU 36389). Veiga de Ganfei,
VI-1885, A.R. da Cunha (LISU 36392). Vila Nova da Cerveira, VI1885, A.R. da Cunha (LISU 36402). Trás-os-Montes: arredores de
Bragança, VI-1882, P.F.M. Var (COI). Bragança, 1877, Pereira
Coutinho (LISU 36358). Entre Montalegre e Chaves, Sapiãos, VI1910, R. Palhinha & al. (LISU 36385). Estação do Pocinho, VI1915, Mendes & Palhinha (LISU 36387). Mogadouro, a montante
da pte. de Ramondes, na margem dta. do rio Sabor., 18-V-1997, A.
Castro & Tjarda De Koe (HVR 9475). Montalegre, 21-VII-1959, M.
da Silva (G 104096). Montinho, Seixas, VI-1885, A.R. da Cunha
(LISU 36401). Santa Marta de Penaguião, Veiga, Aldeia do Bertelo, 25-VI-1993, A. Coelho Costa & A.L. Crespí, A (HVR 10177).
Vila Nova de Foz Côam, margem do Douro (esquerda) a jusante da
Foz do Sabor, frente à Ilha, 30-IV-1995, M. Sequeira (HVR 5937).
Vila Real Coêdo, 10-VII-1981, A. Além (HVR 3902, SANT 39046).
Vimioso, VI-1888, G. Mariz (COI).
SPAIN. Asturias: Cangas de Tineo, 2-VI-1864, E. Bourgeau, in
E. Bourgeau, Pl. d’ Espagne 1864: nº 2657 (G 104119, G 104118,
MA 121552, MA 152778). Corneliana, 16-VIII-1868, E. Boissier
(G 104109). Pravia, without date, La Gasca (MA 121844). Taramundi, VII-1979, T.E. Diaz (MGC 14104). Asturias, VII-VIII-
1878, E. Boissier (G 104121, G 104117). La Coruña: Aranga, 30VI-1967, J. Dalda (SALA 35816). Cariño, Landoi, 4-VIII-1994, X.
Soñora (SANT 31851). Carnota, 1-VI-1996, R.I. Louzán (FCO
24813, MA 581374, SANT 35758). Cuenca del río Deo, 1966-1968,
J. Dalda (SANT 55699). Ferrol, 27-VI-1994, X. Soñora (SANT
29263). Mazaricos, 25-VI-1995, R.I. Louzán (SANT 35746). Santiago de Compostela, Pontepedriña, VI-1995, Rodríguez-Hergueta
(SANT 42394). Sobrado, 24-VII-1882, J. Lange (G 104115). Somozas, 17-VII-1994, X. Soñora (SANT 31883). León: La Baña,
Sierra de Cabrera, camino del Lago, 10-VII-1981, Lansac & Nieto
(MA 317215, MA 317216, MA 317216). Palacios del Sil, Salentinos, 27-VIII-1996, Martín-Blanco (MA 597090). Ponferrada, Villanueva de Valdueza, VIII-1995, Rodríguez-Hergueta (SANT
42467). Riocastrillo de Ordás, 22-VI-1997, C. J. Martín-Blanco (MA
612392). Sobrado, Castropetre, 30-V-1990, J. Amigo & J. Giménez
(SANT 26556). Valle del Bierzo, VI-1905, M. Gandoger (G
104142). Lugo: alrededores de la ciudad, 26-VI-1987, E. Carreira
(MA 513456). Becerreá, El Cruzul, 18-VII-1989, S. Castroviejo &
al. (MA 471686). Cabreira-Fonsagrada, VII-1957, E. Carreira (MA
204700). Cervantes, Correal, entre El Portelo y Piedrafita, 28-VI1994, M. A. Carrasco & al. (MA 543383). Chantada, 18-VI-1988, M.
Buján (SANT 25112). Entre Esperante y Carbedo, 5-VII-1979,
J. Amigo & al. (SANT 16230). Ferreiravella, 19-VI-1980, J. Amigo
& al. (SANT 16229). Meiraos, 16-VII-1981, J. Amigo & al. (SANT
16226). Monforte, 18-V-1991, J. Amigo & M. Romero (SANT
25426). O Saviñao, Mourelos, 14-VII-1992, J. Amigo & M. Romero
(SANT 22471, MA 517178). Palas de Rey, 16-VI-1951, Seijas
(SANT 6124). Piornedo, 23-VII-1952, Bellot & Casaseca (SANT
6783). Quiroga, Hermida, San Victorio, 18-VI-1988, M. Buján &
M. I. Romero (MA 546783, SANT 25107). Riberas de Lea, 25-VII1956, E. Carreira (MA 201352). Sierra del Caurel, Seoane, 28VII-1992, E. Blanco (MA 564613). Tardad. Villalba, 30-VII-1951,
M. Orosa (G 104101). Vilamelle, 6-VI-1990, M.I. Romero (MA
546757. SANT 26231). Orense: Carballeda, 10-VII-1984, S. Ortiz
(SANT 16523). Chandreja de Queija, pr. Paradaseca, 24-VII-1974,
S.I. Laínz (MA 345998). Corrainzas, 12-VIII-2000, J. De Jesús & al.
(SANT 46020). Entre Sobradelo y Casayo, 15-VI-1958, Bellot &
Casaseca (SANT 9940). Leboreiro, 13-VII-1958, F. Bellot & B.
Casaseca (MA 180705). Lobios, 9-VII-1993, I. Pulgar (SANT
56572). Río Lonia, 15-VII-2000, A.R. Romero & al. (SANT 45644).
Río Sil, 15-VI-1958, Bellot & Casaseca (SANT 10066). Rivadavia,
carretera a la Franqueirán, 24-VIII-2007, R. Pino (SEV 218947).
Rubiá, Pardellán, Río Sil, 29-VI-1994, M.A. Carrasco & al. (MA
542966, SALA 115638). Serra do Invernadeiro, inter Rocín et Suacenza, 11-VII-1973, S. Castroviejo (MA 219730, MA 196712).
Verín, 7-VI-1988, M. Buján & M. I. Romero (SANT 25110, SANT
25108). Pontevedra: Albeos, 14-VI-1988, M. Buján (SANT 25113).
Cangas de Morrazo, 6-VIII-2007, S. Castroviejo (SEV 218948).
Crecente, 24-V-1998, J. Amigo & al. (SANT 39787). Cuntis, 9-VI2007, J. García Devesa (SANT 57381). Ermelo, Bueu, 15-VII-1970,
S. Castroviejo (MA 196710). Meaño, 16-III-1988, M. Buján & M.I.
Romero (SANT 25109). Porteliña, 16-VIII-1983, S. Sivestre (SEV
161714). Prado, 15-VII-1947, Vieiter (SANT 213). Salvaterra de
Miño, 24-V-1998, J. Amigo & al. (SANT 39806). Salamanca: Aldeadavila, 22-IV-1977, F. Amich (SALA 15518). La Fregeneda, 30-IV1977, F. Amich (SALA 15519). Zamora: Montelarreina, 31-V-1987,
R. García Ríos (SALA 54045). Ribadelago, 14-VI-1987, A. Roa & P.
García (MA 510330).
2. Campanula matritensis A. DC., Monogr. Campan.: 332. 1830
C. lusitanica subsp. matritensis (A. DC.) Franco, Nova
Fl. Portugal: 2, 569. 1984. C. patula var. matritensis
(A. DC.) Pau in Bol. Soc. Iber. Ci. Nat.: 20, 181.
1921. C. loeflingii var. matritensis (A. DC.) Lange in
Vidensk. Meddel Dansk Naturhist. Foren. Kjøbenhavn 1861: 108. 1862. Ind. loc.: “Habitat in Hispania circa Matritum (Lagasc.!)”. Type: Spain.
Madrid, 1806, Lagasca s.n. (lectotype, here designated, G 138402! (G-DC.), Fig. 6; see observations).
Illustrations. Gallego (1987: 564, as C. lusitanica);
Brotero (1816, tab 18, as C. loeflingii); Hoffmannsegg
& Link (1820, tab. 82, as C. loeflingii ); Sáez & Aldasoro (2001: 130, fig. 39b-h, as C. lusitanica subsp. lusitanica); Fig. 4 C, D.
Herb (6)10-55 cm, annual, erect, branched at the
base or in the upper half, often laxly pubescent, not
brittle. Stems angled, little branched, laxly pubescent
in the lower half with setose hairs 0.1-0.3(0.5) mm.
Leaves not coriaceous, crenate, dentate or entire; middle cauline leaves 4.5-27 × 0.9-9.2 mm, sessile, lanceolate, entire or toothed, glabrous or laxly pubescent,
with hairs 0.1-0.5 mm; upper cauline leaves 2-22 ×
4.5-5.8 mm, sessile, lanceolate, glabrous or with some
hairs of 0.1-0.4 mm. Inflorescence laxly paniculate.
Flowers pedicellate; pedicel 3.5-123 mm, glabrous or
with some hairs of 0.1-0.2 mm. Calyx-teeth (2.2)4-15
× 0.3-1(1.3) mm, linear, filiform. Corolla (8.8)11-26
mm, campanulate, with the tube much longer or
much shorter than the lobes; tube (4.2)7-15.3 mm,
bluish; lobes (5.5)6-16 × 2-7 mm, ovate, blue. Stamens
with enlarged base of 0.6-1 × 0.3-0.7 mm; filaments
0.4-0.6 mm; anthers (2)3-5 mm, white, rarely bluish.
Ovary glabrous, papillose or with scattered hairs of
0.1-0.2 mm; style 5-14 mm, hairy in the upper half;
stigma trifid, with stigmatic branches of 1-2(3.1) mm,
patent, circinate at the end of the female phase of the
flower, white. Capsule (2.5)4-9.2 × 2-5 mm, obpyramidal, much longer than wide, glabrous, papillose or
with some setose hairs less than 0.1 mm, with 10 very
wide nerves like flat ribs, dehiscing by three apical
pores. Seeds 0.4-0.6 × 0.2-0.3 mm, ovoid, shining, yellowish to brown. 2n = 18; n = 9.
Habitat, phenology and distribution: Pine, cork oak
and holm oak woodlands or their shrubby secondary
communities, often on sandy substrates, but also on
clay; 0-2200 m. V-VI(VII). • Endemic to the Iberian
Peninsula. Distributed almost throughout the entire
peninsula, but rare in limestone areas of C, E and N of
Spain, and absent in NE of Spain (Fig. 5). Portugal:
AAl Ag BA BAl BB BL E Mi R TM. Spain: Ab Al Av
Ba Bu C Ca Cc Co CR Cu Gr Gu H J Le Lo Lu M Ma
O S Sa Se Sg So Te To Va Vi Z Za.
Observations: This species is very variable in size,
flower size, indumentum and shape of the calyx, and
27
indumentum and size of the capsules. The plants that
live in very shady banks are usually delicate, have
small flowers and, in general, asymmetric capsules
due to lack of fertilization in one or two of the three
locules, probably caused by deficient pollination. In
contrast, plants living in sunny and humid areas are
vigorous, highly branched, with large flowers and perfectly symmetrical obpyramidal capsules, with all
locules full of seeds, denoting a very efficient fertilization. On shallow soils, in montane areas, plants are
very small, slightly branched, with small flowers and
sometimes with ± ovoid and malformed capsules due
to a deficient pollination, and these may be confused
with C. transtagana or even with C. lusitanica.
The three plants of type material of C. matritensis
(Fig. 6), about 15 cm, attached to the label, have sessile
cauline linear-lanceolate leaves, and obconical capsules. These agree with the characters described by
Fig. 6. Lectotype of Campanula matritensis (plant located in the
lower left corner) (G 138402, indicated by the arrow). The lectotype is the plant of the center, the other two plants are isolectotypes. The other two plants with their respective labels are not
material type.
28
Alphonse De Candolle (1830). That these three plants
include the type material is further indicated by an
Alphonse De Candolle label at the bottom of the sheet
with “Campanula matritensis Alph. DC.”. Of these
three plants, the largest, located in the middle, is chosen as lectotype of Campanula matritensis A. DC. The
other two plants are isolectotypes. In the same sheet
there are other two plants which are not type materials
(see Fig. 6). One [Herb. Prodr. (G-DC)G 138459] indicates “Campanula/ex hispania/m’ Guillemin 1827”
and the plant, branched and young, is identified as
C. matritensis; the other [Herb. Prodr. (G-DC)G
138462] indicates “C. pulla herb Lag./prope la Venta
del Gorro in nov. Castell./1827 [1827? manuscript Lagasca?]/Londres 1828 [manuscript Lagasca]”. Coupled with this label there is another, probably handwritten by A. De Candolle, with the following inscription: “C. matritensis?/differt ab ómnibus affinibus lobis/calicinis marginem extus revolutis.”. Stitched to
both labels there is a very small plant with a single
flower, which we identify as C. dieckii Lange.
Selected specimens
PORTUGAL. Algarve: Broussailles à Monchique, 14-VI-1853,
E. Bourgeau, in E. Bourgeau, Pl. d’ Espagne et de Portugal, 1853: nº
1943 (G 104070, G 104125, G 104140). Cabo de San Vicente, Chodat (G 104147). Castro Marim, Terras da Ordem, 24-IV-1975, M.
Sequeira & al. (HVR 4734). Entre Corte-Figueira y Mù, VI/VII1885, J. Daveau (LISU 36408). Faro, Santo Antonio do Alto, V1889, J. Brandeiro (G 104123). Olhão, Quinta de Marim, 24-V-1986,
A. Moura (MA 430492). Entre Santa Catharina e Sagres, V-1906, F.
Mendes & Palhinha (LISU 36391). Serra da Picota, VII-1891, J.
Brandeiro (COI). Serra de Monchique, Ribeira da Perna Negra, 30V-1979, M. Beliz & J. Guerrero (MA 270313). Alto Alentejo: Elvas,
próximo da estrada Elvas-Badajoz, 1-I-1900, A. Forque (LISE
31816). Évora, V-1891, A. Moller (COI). Évora Monte, entre Estremoz y Évora, 28-V-1996, S. Castroviejo & al. (MA 588831). Gavião,
26-VI-1952, P. Silva, F. Fontes & B. Rainha (G 104102). Margen do
rio Alirilungo, afluente de Xevora, V-1922, Fernandes (LISU
36417). Marvão, Serra de San Mamede, 16-V-1978, J.A. Devesa & J.
Pastor (SEV 39778). Montargil, V-1883, G. Corteisão (COI). Mora,
arredores nas arelas do leito da Ribeira da Raia, 13-V-1953, Bento
Rainha (LISE 51183). Portalegre, Serra de Penha, VI-1882, A.R. da
Cunha (LISU 36400). Portel, 15-V-1969, P. Silva & al. (LISE
93823). Povoa e Meadas, VI-1882, A.R. da Cunha (LISU 36370). Redondo, V-1892, D. Pita Simões (LISU 36361, LISU 36366). Reguengos, Berrocal, IV-1908, F. Mendes & Palhinha (LISU 36411). Serra
d’Ossa, V-1891, A. Moller (COI). Baixo Alentejo: Cazevel, V-1888,
A. Moller (COI). Cuba, entre Cuba e Vila de Frades, 4-V-1962,
M. Silva (LISE 76879). Entre Garvão e Panóias, VI/VII-1885, J.
Daveau (LISU 36393). Odemira, V-1915, F. Gomez & R. Machado
(LISU 36415). Santiago de Cacém, 14-V-1958, B. Rainha, M. Silva &
A.N. Teles (LISE 64924). Margen do rio Chança, VI-1913, F. Mendes, H. Navel & Palhinha (LISU 36414). Serra do Caldeirão, 12-V1905, M. Gandoger (G 104143). Sines, a 1 Km a norte de porto
Covo, 21-V-1982, F. Catarino & al. (LISU 145357). Tarrão, 29-V1952, F. Fontes & al. (LISE 41814). Beira Alta: Águeda, perto de Escalhão, 26-V-1996, M. Santos & M. Sequeira (HVR 7845). Barca
d’Alva, margen do Douro, VI-1915, F. Mendes & Palhinha (LISU
36416). Castelo Mendo, Moita do Carvalho, VII-1884, A.R. da Cunha (LISU 36399). Covilhã, VI/VII-1881, A.R. da Cunha (LISU
36395). Entre Guarda y Valhelhas, 16-VII-1983, S. Castroviejo & al.
(MA 248455). Figueira de Castelo Rodrigo, Barca D’ Alva, 28-IV1943, J. Castro & A. Rozeira (MA 514273). Sabugal, 14-VI-1976, I.
Melo & al. (LISU 69654). Serra da Estrela, VII-1887, A. Moller (MA
121501). Serra da Lapa e Mata da Vide, VI-1890, M. Ferreira (COI).
Vale do Zêzere, 3-VIII-1949, C. Romariz (LISU 2053). Vouzela, 27V-1940, Palhinha (LISU 36363). Sabugal, à saída da vila, na estrada
Castelo Branco (Miradouro), 14-VI-1976, I. Melo,& al. (SEV
121226). Beira Baixa: Alcaide, Barroca do Chorão, VI-1882, A.R. da
Cunha (LISU 36369). Castelo Branco, VI-1881, A.R. da Cunha
(LISU 36398). Covilhã, nos latudes da estrada prose da ribeira da
Carapinheira, 23-VI-1946, B. Rainha (G 104146, LISE 21736, MA
121494). Monfortinho, prox. das termas, 14-VI-1948, B. Rainha
(LISE 22693, MA 152780). Tavanca do Mondego. 31-V-1990. Z.
Díaz & al. (SEV 161692). Beira Litoral: Arganil, Moita, V-1895, M.
Ferreira (COI). Cantanhede, VI-1888, C.M. Ferreira (COI).
Choupal prope Conimbricam, VI-1878, A. Moller (G 104124, G
104122). Coimbra,, 6-VIII-1883, A. Moller (G 104139). Guardinha,
arred. do Louriçal, VI-1897, J.A. Vaz Serra (COI). Meco, 16-IV1995, A. Crespi & M. Sequeira (HVR 4604). Taboa, V-1883, A. Costa Carvalho (COI). Estremadura: Alfeite, V-1906, J. dos Santos
(LISU 36384). Alrededores de Lisboa, Serra de Monsanto, VI-1884,
A.R. da Cunha, in Flora Lusitanica (Soc. Brot. 7º. Anno) nº 910
(LISU 36360). Arredores de Setúbal, V-1906, F. Gomez (LISU
36409). Lagoa de Albufeira, V-1882, J. Daveau (LISU 36371). Moita, Arganil, V-1895, M. Ferreira (COI). Praia das Maçãs, V-1930, F.
Matos (LISU 36364). S. Simão, Piedade, VIII/IX-1848, J. Daveau
(LISU 36396). Sacavém, 1952, Duarte de Castro (LISE 40720). Seixal, V-1881, A.R. da Cunha (LISU 36397). Serra da Arrabida, Colina
de Santa Margarida, 18-V-1942, C. Fontes & al. (LISE 15267, MA
121496). Serra de Montejunto, 31-I-1947, Romariz & Mendes (LISU
56937). Sesimbra, Alfarim, 2-VI-1971, M. Beliz & J. Guerreiro (MA
270318). Vila Nogueira, 25-V-1978, J.A. Devesa & al. (SEV 39777).
Minho: Gerez, VII-1889, F. Loureiro (COI). Valença, Olivar de Sta.
Barbara, VI-1885, A.R. da Cunha (COI). Ribatejo: Almeirim, 22-V1952, P. Silva & M. Silva (LISE 41804). Trás-os-Montes: arred. de
Miranda do Douro, Iffanes, VI-1888, J. de Mariz (COI). Arredores
de Bragança, 16-VI-1941, A. Carneiro (COI). Arredores de Moncorvo, Concelho de Mogadouro, Urrós, 20-V-1997, J. Hernándes &
E. Rico (SALA 90849). Avelanoso, arred. de Vimioso, VI-1888, J. de
Mariz (COI). Ligares, V-1884, J. de Mariz (COI). Valença, Olival de
Santa Barbara, VI-1885, A.R. da Cunha (COI). Vila Real, Coêdo, 10VII-1981, A. Além (COI).
SPAIN. Álava: Bernedo, Urturi, 1-VII-1987, J.A. Alejandre (MA
423674). Albacete: San Pedro, 11-VI-1984, J.M. Herranz (MA
318970). Almería: Abrucena, Las Rozas, 17-VI-1988, B. Valdés & al.
(G 104090). Ávila: Arévalo, 20-VI-1971, J. Gómez (MA 432025).
Castronuevo, 19-VI-1984, Barrera & al. (MA 314814, SALA 34644).
Hoyocasero, Cueva del Moragato, 15-VI-1985, M. Luceño & P. Vargas (MA 407310). Hoyos del Espino, Las Chorreras, 9-VII-1988,
Aizpuru & al. (MA 451362). Piedralaves, La Adrada, 22-VI-1982, F.
de Diego Calonge (MA 538909, MA 538611). Poyales del Hoyo, 30VI-1917, J. Cuesta (MA 121528). Ramacastañas, Cerro de las Cuevas
del Águila, 30-V-1987, Vargas (MA 655999). Sierra de Ojos Albos,
Los Regajales, 3-VII-1984, A.R. Burgaz & al. (MA 389677). Sotillo
de la Adrada, 15-VI-1973, G. López & E. Valdés Bermejo (MA
430972). Valle de Iruelas, 12-VI-1956, C. Vicioso (MA 170174).
Venta del Obispo, 20-VI-1945, A. Caballero (MA 121586). Villanueva de Gómez, 19-VI-2003, M. Ladero (SALA 108263). Valle de
Amblés, Villatoro, 12-VII-1974, Ladero & Fuertes (SALAF 23155).
Badajoz: Campanario, V-1911, V. Lagares (MA 121534). Castuera,
14-IV-2001, P. Escobar García (MA 707044). El Berrocal, 25-V2001, P. Escobar García (MA 707042). El Toril, V-1951, Moreno
Márquez (SEV 5005). Mérida, embalse de Proserpina, 16-IV-1994,
F. Amich & al. (MA 717798). Oliva de la Frontera, 23-IV-1994, F.
Amich & al. (MA 717195). Sierra del Palenque, 7-V-2000, P. Escobar
García (MA 766400). Talarrubias, 19-V-2001, P. Escobar García
(MA 707043). Valdecaballeros, 17-III-1977, M. Figueroa & al. (MA
269851). Burgos: Aranda de Duero, V-1942, A. Caballero (MA
121572, MA 121526). Cardeñajimeno, 21-VI-1914, C. Pau (MA
121533). Ciruelos de Cervera, pie del Alto de la Cabeza, 11-VII1979, Pons Sorolla & Susanna (G 104082, MA 413025). De Quintanar de la Sierra a Neila, 1-VII-1925, M. Losa (MA 433608). La Revilla, camino de Ahedo, 17-VII-1979, Muñoz Garmendia & al. (G
104085, MA 414202). Miranda de Ebro, 15-VI-1912, H. Elías (MA
433606). Santa Gadea del Cid, 11-VII-1915, H. Elías, in F. Sennen,
Plantes D’ Espagne, nº 2447 (MA 121573). Tejada, Pico Valdosa, 3VII-1979, J. Fernández Casas & al. (G 104084). Cáceres: Baños de
Montemayor, 15-IV-1944, A. Caballero (MA 121543). Barrado, 19V-1988, A. Amor (SALAF 16729, SALAF 23633). Cañaveral, cerro
de Cabezarrubias, 14-V-1988, Ladero & Santos (SALAF 16506).
Casatejada, Las Cabezas, Sexta Suerte, Arroyo de Fresno, 7-V-1983,
Ruiz Téllez (SALAF 6774). En las bajadas de Puerto Viejo, hacia
Valverde del Fresno, 23-V-1982, A. Valdés Franzi (SALAF 12190).
Guadalupe, 16-VI-1948, A. Caballero (MA 121539). Hervás, 12-X1987, R. González (SALA 101150). Jaraíz de la Vera, Las Costeras,
19-V-1988, A. Amor (SALAF 16703). La Bazagona, 1-V-1983, Ruiz
Téllez (SALAF 6775). Losar de la Vera, Valle del Tiétar, 20-III1980, Meana & al. (MA 393441, SANT 18476). Mirabel, 4-V-1980,
D. Belmonte (MA 344687). Montánchez, Sierra de Montánchez,
carretera a Cerro Moro, 20-VI-1998, S. Castroviejo (MA 613395).
Navalmoral de la Mata, 25-V-1984, Ruiz Téllez (SALAF 10761, MA
680829). Plasencia, 19-V-1988, Ladero & al. (SALAF 16507). Puerto de Hoyos, 17-VII-1978, A. Valdés Franzi (SALAF 12191). Puerto
de Santa Clara, San Martín de Trevejo, 28-VI-1983, M. Ladero & A.
Valdés (SALA 114203, SALAF 12192). Santiago de Alcántara, 26IV-1994, F. Amich & al. (MA 718573). Sierra de San Pedro, 17-V1909, M. Gandoger (G 104144). Torrecillas de la Tiesa, 22-V-1999,
L. Medina (MA 624469). Valle del Jerte, 18-VI-1975, Carrasco &
Castroviejo (SALA 25804). Cádiz: Algodonales, Sierra de Líjar, 11VII-1980, A. Aparicio & al (SEV 57983). Aprox. 5 km al E de Vejer
de la Frontera, entre los pinos a lo largo de la carretera, 28-IV-1975,
S. Holmdahl (MGC 50213). Bornos, 28-IV-1978, B. Molesworth
Allen (SEV 53284). Chiclana de la Frontera, 22-V-1982, A. Charpin
& C. Defferrand (G 104083, MA 243115). Grazalema, Puerto de las
Palomas, 10-VI-1993, A. Aparicio & al. (MA 526987). Jeréz de la
Frontera, 17-V-1985, A. Asensi & J. Cuenca (MA 570487). Los Barrios, Barranco del Arroyo de Valdeinfierno, 28-V-1978, J. Fernández Casas (G 104086, MA 226312, SALA 22564). Puerto de Santa
María, Chiclana, et pr. Grazalema, V-1895, Porta & Rigo, Iter IV
Hisp. 1895: 321 (G 104107). Sierra de Palma, 19-VII-1887, E.
Reverchon, in E. Reverchon, Plantes de L’Andalousie, 1887: nº 17
(MA 121509). Tarifa, Sierra de Saladavieja, El Carrascal, 22-VII1980, J. Arroyo & J.M. Gil (SEV 64621). Ubrique, 30-V-1972, S.
Holmdahl (MGC 50212). Cantabria: Valderredible, páramo de la
Lora, 2-IX-1983, E. Loriente (MA 683841, MA 599290). Ciudad
Real: Argamasilla de Calatrava, finca La Laguna de las Carboneras,
13-V-2001, M. Bellet & al. (MA 711976). Cabezarrubias del Puerto,
22-V-1998, R. García Ríos (MA 711940). Casas del Río, Navalagrulla, 1-VI-2001, S. Castroviejo & M. A. Carrasco (MA 692324). Sierra
de Alhambra, 30-IV-1933, González Albo (MA 121583). Sierra
Madrona, 29-V-1950, S. Rivas Goday & J. Borja (SALA 376). Sierra
Morena, Venta de Cárdenas, 30-IV-1933, J. Cuatrecasas (MA
121520). Córdoba: Belalcázar, finca de Pedroche, 8-VII-1976, J.A.
Devesa (SEV 33720). Cardeña, finca de Yegüerizo (UH-83), 30-V1976, J.A. Devesa (SEV 33723). Torrecampo, ribazos del río Guadamora, 16-V-1976, J.A. Devesa (SEV 33388). Trassierra, 14-V-1982,
J. Arroyo (SEV 87091). Villaviciosa de Córdoba, Tres puentes, V1920, C. Pau (MA 121518). Cuenca: Ródenos de Cañete, 9-VI-1971,
E. Valdés Bermejo & al. (MA 431991). Talayuelas, 18-VI-1979,
G. Mateo (MA 256531). Granada: Cañar, Bco. río Chico, 20-VII1979, J. Molero Mesa (MA 432023). Capileira, 3-VII-1948, Vieiter
29
(SANT 211). In arenosis Regn. Granat. a littore, 1837, E. Boissier (G
104111). Jatar, Sierra Almijara, supra Jatar, 11-VI-1983, B. Cabezudo & J.M. Nieto (MGC 41527). Puerto de la Ragua, cruce con la carretera a la Alpujarra, 19-VI-1988, B. Valdés & al. (G 104089). Sierra
Nevada, 21-VII-1879, Huter & al. Extinere hispanico 1879: 234 (G
104137); ibidem, Cáñar, 28-VII-1930, C. Vicioso (MA 121558).
Guadalajara: Campillejo, VII-1973, Demetrio (FCO 4103). Cantalojas, Valle del Lillas, 20-VI-1985, Burgos & Cardiel (MA 487000).
Checa, 25-VI-1997, L.M. Ferrero & L. Medina (MA 595634). El Pedregal, VII-1894, J. Benedicto (MA 121566). La Fuensaviñán, 26-V1994, J. Castillo & al. (MA 543882). Prado Redondo, Monte del
Condado (MA 153134). Valverde de los Arroyos, 13-VII-1998, F.
Lamata (MA 615546). Guadalajara, VI-1994 (MA 546347). Huelva:
Almonte, 28-IV-1943, C. Vicioso (MA 121510); ibídem, 12-V-2006,
A. Quintanar (MA 772195). Ayamonte, 5-V-1902 (MA 121515).
Calañas, 28-IV-1921, Gros (MA 121513). Chucena, Cerro de las
Palomas, 19-IV-2001, B. Cabezudo & al. (MGC 48566). Higuera de
la Sierra, 24-V-1988, E. Bayón & E. Villanueva (MA 438689). Hinojos, 26-V-2004, J. Cano-Maqueda & al. (SEV 216214). La Barra de
Huelva, 22-IV-1943, C. Vicioso (MA 121512). Sierra de Aracena,
Aracena, 15-V-1979, J. Rivera (SEV 48340). Jaén: Andújar, El Abogado, 11-V-1985, E. Cano (MA 716641). Baños de la Encina, mina
Matacabras, 23-IV-1988, C. Fernández & al. (FCO 21720, G
104155, MA 553899, MGC 38654, SALA 59048, SANT 29973).
Guarromán, camino hacia la mina de los Dolores, 5-V-1966, S. Silvestre (SEV 19712). Sierra Morena, Arroyo de Oruga, 7-VI-1923,
Fernández & al. (MA 121519). La Rioja: Ezcaray, barranco Reoyo,
pr. Urdanta, 16-VII-1998, Gracía-Baquero & al. (SALA 100212).
Ocón, 27-VII-1930 (MA 121531). San Millán de la Cogolla, 16-VII1981, S. Castroviejo & Fernández Quirós (MA 433427). Sierra de la
Demanda, de Anguiano a Tabladas, 26-VII-1995, L. Loidi & A. Berastegui, in Lambinon, Pl. Europe Occid.-Bas. Méd., 1997: nº 17459
(G 104092, MA 589694). León: Castroquilame, 12-V-1973, Andrés
& Carbó (SEV 16643). La Gotera, 8-VII-1944, Rojas (MA 121550).
Ponferrada, 10-VII-1933, W. Rothmaler, in W. Rothmaler, Plantae
Hispaniae Boreali-Occidentalis, nº 128 (MA 121551); ibidem, carretera de San Esteban de Valdueza a San Pedro de Montes, 21-VI1981, Alamillo & Nieto (MA 317259). Trabadelo, San Fiz do Seo,
valle del río Barjas, 18-VII-1998, Martín-Blanco (MA 641637). Lugo:
Tardad, Villalba, 30-VII-1951, M. Orosa (G 104101). VillardíazFonsagrada, 22-VII-1953, E. Carreira (G 104197). Madrid: Madrid,
VI-1841, Reuter (G 104130, G 104131). Buitrago, 1-VI-1918, C. Vicioso (MA 121559). Collines à la base de la Sierra de Gredos, 8-VII1863, E. Bourgeau, in E. Bourgeau, Pl. d’Espagne et de Portugal,
1863: nº 2442 (G 104127, G 104132, MA 721360, MA 121530,
MA 121529, MA 152777). Casa de campo pres Madrid, 7-VI-1854,
E. Bourgeau (G 104128, G 104145, MA 720519). Chamartín, 17-V,
Isern (MA 153136). Chinchón, cerros de Butarrón, VI-1919, C. Vicioso (MA 121576). El Escorial, VI-1914, C. Vicioso (MA 121577).
El Pardo, 4-VI-1936, M. Martínez & A. Rodríguez (MA 432685).
Guadalix de la Sierra, 29-VI-1983, F. Gómez Manzaneque (MA
450150). Hoyo de Manzanares, VI-1998, A. Izuzquiza & al. (MA
615516). La Pedriza, V-1932 (MA 432723). Miraflores, 25-VI-1945,
L.C. & A.R. (MA 201400). Monte del Pardo, 20-V-1917, C. Vicioso
(MA 121578). Montejo de la Sierra, 2-VII-1954, A. Rodríguez (G
104103). Navacerrada, VI-1915, C. Vicioso & Beltrán (MA 121580).
Puerto de la Cruz Verde, 22-VI-1973, Rivas-Martínez & Costa (MA
432036). Robledo de Chavela, 19-VI-1988, M. Costa Tenorio &
H. Sainz Ollero, in J. Lambinon, Pl. Europe Occ.-Bas. Méd. 1993:
nº 15575 (G 104153, MA 532060, SALA 88527). San Martín de
Valdeiglesias, Rozas de Puerto Real, 6-VI-1992, P. Vargas (MA
515427). Sierra de Guadarrama, 4-VII-1968, O. Polunin (MGC
5003). Sierra de la Cabrera, 4-VII-1993, A. Izuzquiza & al. (MA
529567). Torrelaguna, V-1912, C. Vicioso (MA 121582). Málaga:
Benaoján, Sierra del Palo, 27-V-2007, J. Cano-Maqueda (SEV
218872). Benarrabá, carril de los Pepes, 29-V-2004, O. Gavira
30
(MGC 60964). Casares, Monte del Duque, 20-V-1988, B. Cabezudo
& A.V. Pérez-Latorre (MGC 35466). Estepona, 16-V-1919, E. Gros
(MA 121506). Gaucín, VI-1916, E. Gros (MA 121508). Gobantes,
garganta de El Gaitán, 11-VI-1930, C. Vicioso (MA 121486). Los
Villares, 12-V-1988, B. Cabezudo & al. (MGC 24576). Ronda, 07VI-1889, E. Reverchon, in E. Reverchon, Plantes de L’Andalousie
1889: nº 17 (G 104260). Sedella, Los Picaricos, 30-V-2003, B.
Cabezudo & al. (MGC 60070). Sierra Bermeja, 18-V-1919, E. Gros
(MA 121507). Sierra Tejeda, 26-VI-1982, J.M. Nieto (MGC 18110).
Tolox, Castañar de los Hornillos, 13-VI-1932, L. Ceballos (MA
121505). Torrox, VI-1909, Domingo (G 104138). Orense: Lovios,
6-VI-1993, I. Pulgar (FCO 21431, MA 551003). Serra do Invernadeiro, entre Rocín y Suacenza, 11-VII-1973, S. Castroviejo (G
104080). Salamanca: Cantalapiedra, 25-V-1987, X. Giráldez &
Aragón (SALA 46173). Ciudad Rodrigo, 4/6-VII-1932, C. Pau (MA
121549). Embalse del río Águeda, 6-VI-1976, E. Rico (SALA 9431).
Entre Fuentes de Béjar y Navas de Béjar, 21-VI-1978, J.A. Devesa &
J. Pastor (SEV 39776). Entre La Alberca y Sotoserrano, 20-VII1972, Fernández Díez (SALA 5451). Guijuelo, 7-VI-1987, E. Rico &
J. Serradilla (MA 476539, SALA 46836). Hurdes, 5-VII-1946, A. Caballero (MA 121547). Ledesma, 19-V-1976, J. Sánchez (SALA
17419). Linares de Riofrío, VII-1980, J. L. Fernández Alonso (MA
519040). Masueco, laderas del río Uces, 16-VI-1976, F. Amich
(SALA 15517). Monleras, 22-X-1976, J. Sánchez (SALA 17428).
Montemayor del Río, 3-VII-1983, A. Guillén (SALA 36167).
Navacarros, 15-VII-1983, F. Amich & F. Herrero (SALA 34909,
SALA 34910). Pelabravo, 2-VI-1990, A. Pastor (SALA 57034).
Peñamecer, 23-V-1976, J. Sánchez (MA 219749, SALA 17427).
Puerto Seguro, 9-V-1976, E. Rico (SALA 9432). San Esteban de la
Sierra, 20-VI-1971, Fernández Díez (SALA 5595). Topas, 9-VI1967, B. Casaseca (SALA 375). Valdelageve, 28-IV-1996, J. Barrios
Pérez (SALA 121888, SALA 121889). Segovia: Aguilafuente, Cotarra de Juriñas, 6-VI-2002, M. Pérez Valero (MA 756780). Entre Riaza y Ayllón, cruce de la carretera hacia Pajares del Fresno, 28-V1992, A. Izuzquiza (MA 508024). Fresno de la Fuente, 20-VI-1985,
A. Izuzquiza (MA 348898). Fuentidueña, 15-VI-1983, T. Romero
(SALA 40297). Lastras de Cuéllar, Molino Ladrón, 24-V-1998, P.
Bariego Hernández & A. Gastón González (MA 754632). Ochando,
19-VI-2002, M. Sanz Elorza (MA 687112). Puerto de los Cotos, 5VII-1989, A. Charpin & P.A. Loizeau (G 104151). Riofrío de Riaza,
7-IX-1975, F.J. Fernández Casas (MA 347715). Siguero, 1-VII-1983,
T. Romero (MA 567697). Torrecilla del Pinar, 12-VII-1984, T.
Romero (SALA 40298). Sevilla: al S de Villamanrique de la Condensa, 7-V-1988, E. Bayón & al. (MA 438338). Aznalcázar, 20-IV-2003,
Z. Díaz (MA 707168). Castilblanco de los Arroyos, Los Melonares,
1-VI-2006, J. Cano-Maqueda & al. (SEV 218870). Constantina, Hermita Virgen de Robledo, 1-VI-2006, J. Cano-Maqueda & al. (SEV
218869). Dehesa de Covarrubias, 6-IV-2001, B. Cabezudo & al.
(MGC 48568). Gerena, 3-V-2001, B. Cabezudo & al. (MGC 48568).
Paradas, 5-V-1933, C. Vicioso (MA 121517). Soria: Berlanga de
Duero, 18-VI-1977, A. Segura Zubizarreta (G 104087, MA 226315,
SALAF 437, SEV 74840). Canredondo, 22-VI-1990, A. Segura Zubizarreta (MA 581101). Cañón del río Lobos, 30-VI-1983, A. Buades
(MA 504440). Carbonera de Frentes, 2-VII-1989, A. Charpin (G
104152). Herrera de Soria, 30-VI-1983, A. Buades (MA 504408).
Molinos de Duero, 21-VIII-1987, G. Mateo (MA 383713). Quintana
Redonda, 30-VI-1974, A. Segura Zubizarreta (SEV 41098). Tozalmoro, 6-VII-1935, C. Vicioso (MA 121527). Teruel: Orihuela del
Tremedal, 18-VI-1907, C. Pau (MA 433607). Segura de los Baños,
VII-1894, J. Benedicto (MA 121566b). Toledo: Almorox, El Pinar,
3-VII-1982, M. Luceño (MA 430416). Nacimiento del río Estena,
19-VI-1986, J. Assens & al. (MA 430409). Valladolid: Castronuño,
Sendero de los Ladrones, 22-V-1988, G. Balbás (SALAF 23342). Pedrajas de San Esteban, 7-VII-1975, F.J. Fernández Díez (FCO 4601,
SALA 7575). Zamora: Aspariegos, La Salgada, 10-V-1990, R. García Ríos (SALA 54046). Corrales, 15-VI-1951, Casaseca (SANT
5565). Cubo del Vino, 19-VI-1981, X. Giráldez (SALA 31612). Escober, Los Linares, 15-VII-1996, P. Bariego Hernández (MA
651736). Lago de Sanabria, 25-VIII-1953, A. Rodríguez (MA
201347). San Cebrián de Castro, El Barrucal, 28-V-1990, R. García
Ríos (SALA 54048). Villaseco del Pan, La Era del Campo, 30-IV1988, R. García Ríos (SALA 54047). Zaragoza: Atea, 29-V-1909, C.
Vicioso (MA 121565). Calatayud, VI-1987, C. Vicioso (MA 121560).
Moncayo, 19-VII-1893, C. Vicioso (MA 121560). Belmonte, 4-V1931, Gros, in F. Sennen, Plantes d’ Espagne 1932: nº 8206 (G
104149, MA 121514).
3. Campanula cabezudoi Cano-Maqueda & Talavera
in Acta Bot. Malacitana 32: 254. 2007
C. decumbens var. pseudospecularioides G. López
in Bol. Soc. Brot. ser. 2, 53: 301 (1979-1980) [syn.
subst.]. Ind. loc.: “Habitat locis umbrosis, inter rupes calcareas, loco dicto Boquete de Zafarraya,
Sierra Tejeda (Málaga-Granada), ubi cum P. Cubas
et J.M. Moreno, die 28-VI-1976, legi. Holotype:
MA 210975, Fig. 7; Isotype: MA 210994”.
Illustrations: Gallego (1987: 564, as C. decumbens);
Fig. 7. Holotype of Campanula cabezudoi (MA 210975).
Sáez & Aldasoro (2001: 130, fig. 39a, as C. lusitanica
subsp. lusitanica); Fig. 4 E, F.
Herb 8-30(45) cm, annual, decumbent, branched
from the base, pubescent, not brittle. Stems slightly
angled, branched, pubescent, sometimes glabrescent
at the apex, with setose hairs of 0.1-1.4 mm. Leaves
subcoriaceous, entire or toothed, petiolate; middle
cauline leaves 6.2-18.2 × (2.9)5-9 mm, petiolate, elliptical, ± pubescent, with hairs to 1.1 mm, with petioles
up to 2 mm; upper cauline leaves 4.5-14.5 × 1.3-3.9
mm, oblanceolate, ± hairy, with hairs up to 1.2 mm,
with petioles of c. 0.5 mm. Inflorescence laxly paniculate. Flowers pedicellate; pedicel (9.8)20-68 mm,
glabrous or setose, with hairs of 0.1-0.7(1.5) mm. Calyx-teeth (4)5-11 × 0.4-1.2 mm, lanceolate or linear.
Corolla (7.3)8-16 mm, infundibuliform, with the tube
shorter than the lobes; tube 3.1-6.9 mm, white; lobes
(3.6)5-10.3 × 3.1-6.2 mm, elliptic, blue, with three
purple nerves. Stamens with enlarged base of 0.6-1 ×
0.5-0.7 mm, deltoid; filaments 0.4-0.5 mm; anthers
(2.5)3-6.4 mm, whitish. Ovary densely hispid, with setose hairs 0.2-1.8 mm; style (5)7-12.3 mm, hairy in the
31
upper half; stigma trifid, with stigmatic branches 11.7 mm, patent, arched, white. Capsule 2.1-5.9 × 2.25 mm, subspherical or ovoid, generally wider than
long, densely hairy, with papillose hairs up to 1.5 mm,
with 10 nerves ± acute but not winged, dehiscing by
three apical pores. Seeds 0.5-0.6 × 0.2-0.3 mm, ovoid,
shining, yellowish to brown. 2n = 20.
Habitat, phenology and distribution: Fissures of calcareous rocks; 400-1600 m. VI-VII. • Endemic to the
Sierra Subbética from Seville to Jaén, and the Penibética, where it is very frequent, especially in the
Sierra de Loja and Tejeda (Fig. 8). Spain: Ca Co Gr J
Ma Se.
Observations: Sáez & Aldasoro (2001) comment
with reference to C. decumbens var. pseudospecularioides G. López: “existen formas intermedias entre
esta subespecie [which they refer to C. specularioides]
y C. decumbens [which they refer to C. dieckii], que
han recibido reconocimiento taxonómico”. It is very
likely that they are referring to C. cabezudoi. In fact,
the vegetative characters of decumbent habit and
the presence of petiolate middle leaves of the stem,
Fig. 8. Distribution map of Campanula cabezudoi (䊱) and C. specularioides (䡬).
32
are similar in C. cabezudoi and C. decumbens, but
C. cabezudoi has hairy style in the upper half and a single trifid stigma with curved and patent stigmatic
lobes, while C. decumbens has a glabrous style and
three straight and erect-patent stigmas. Moreover, in
the topology of the ITS analysis, C. cabezudoi and
C. decumbens are in two different clades (Fig. 1) and
they have different chromosomes number (Table 1,
Fig. 2).
Selected specimens
SPAIN. Cádiz: Grazalema, Puerto de las Palomas, El Pinar, 5VII-1984, A. Aparicio (SEV 161693). Córdoba: Almedinilla, Sierra
de Albayate, 7-VI-1980, J. Muñoz (MA 749306). Priego de Córdoba, Sierra Horconera, 4-VII-1980, J. Muñoz & R. Tormo (MA
749309). Rute, Sierra de Rute, Pico Las Cruces, 26-VI-1978, J.
Muñoz (MA 749308, SEV 161894). Granada: entre Venta de Zafarraya y Zafarraya, Sierra Gorda, VI-2007, Cano-Maqueda & al.
(SEV 218873). Sierra Harana, cercanías de la Cueva del Agua, 16VI-1982, Casares & al. (MA 432054). Sierra Tejeda, 7-VII-1935,
M. Laza (MA 121470). Jaén: Mágina, 3-VII-1925, J. Cuatrecasas
(MA 121522). Sierra de Cazorla, El Tranco, 30-VI-1988, S. Talavera & al. (G 104061, SEV 161662). Málaga: Alfarnate, Sierra de la
Torca, 7-VI-2006, B. Cabezudo & al. (MGC 63804). Álora, Sierra
de Huma, 26-VI-1986, B. Cabezudo & R. Suan (MGC 36711). Antequera, 14-VI-1930, C. Vicioso (MA 121488). De Ronda a El Burgo, 18-VI-1972, L. Bernardi (G 104157). Los Alazores, Puerto de
los Alazores, Sierra de Alhama, Tres Mogotes, 5-VII-1973, B.
Cabezudo & B. Valdés (SEV 161891). Puerto del Viento, 29-VI1849, E. Bourgeau in Bourgeau, Pl. Espagne 1849: nº 320 (G
104256). Sierra Prieta, 07-VI-1879, Hunter, Porta & Rigo in Iter.
Hisp. 1879: nº 232 (G 104184). Ronda-Sierra de las Nieves, entrando al Sabinar, Monte de la Peineta, 19-VI-1974, S. Talavera &
B. Valdés (SEV 161889). Sierra de Peñarrubia, 12-VI-1930, C. Vicioso (MA 121487). Valle de Abdajalís, cortado del Cuervo, 15-VI1973, S. Talavera & B. Valdés (SEV 161888). Villanueva del
Rosario, Sierra Camorolos, 5-VII-1973, B. Cabezudo & B. Valdés
(SEV 161887). Yunquera, P. N. Sierra de las Nieves, entre el Puerto Bellina y el cruce del camino con la Cañada de los Hornillos, 18VI-1998, B. Cabezudo & al. (MGC 46750). Sevilla: Algámitas, Sierra del Tablón, 5-VII-1978, B. Cabezudo & E. Ruíz de Clavijo
(SALA 13425, SEV 31778).
angled, branched, glabrous, rarely with setiform hairs
to 1.2 mm. Leaves fleshy, entire or toothed, petiolate;
middle cauline leaves 7.5-13.4 × 4.5-20 mm, broadly
elliptical, glabrous or glabrescent, with hairs 0.1-0.2
mm, and petiole 1-6.4(14) mm; upper cauline leaves
3.5-14.5 × (1)1.9-6.4 mm, elliptic, glabrous, with petiole 0.4-1.7 mm. Inflorescence laxly paniculate. Flowers pedicellate; pedicel (5.7)7-35 mm, glabrous or setose hairs 0.1-0.8 mm. Calyx-teeth (1.7)3-7.6 × 0.7-1.5
mm, oblanceolate. Corolla (6.6)8-10(14) mm, broadly
infundibuliform, with the tube shorter than lobes;
tube 2.6-4.9 mm, whitish; lobes 4.1-7.5(10.3) × 2.25.4 mm, elliptical, pinkish or bluish, with three purple
nerves. Stamens with enlarged base of 0.5-1 × 0.2-0.5
mm, deltoid; filaments 0.6-0.8 mm; anthers 2.1-3.2
mm, blue or whitish. Ovary glabrous, rarely densely
hairy; style (4.7)6-7.3(8.5) mm, hairy in the upper half;
trifid stigma, with stigmatic branches 0.6-1(1.4) mm,
patent, curved, white or blue. Capsule 2-3 × 3-4.5
mm, subspherical, wider than long, with 10 subwinged, glabrous nerves, rarely with setose hairs up to
1.5 mm, dehiscing by three pores of middle position.
4. Campanula specularioides Coss., Notes Pl. Crit.:
41. 1849
C. lusitanica subsp. specularioides (Coss.) Aldasoro &
L. Sáez in Anales. Jard. Bot. Madrid 59: 173. 2001.
Ind. loc.: “In fissuris rupium regionis montanae
regni Granatensis, loco dicto Cortijo blanco prope
Ronda, a Bourgeau inventa”. Type: Spain. Málaga,
Ronda, Cortijo Blanco, 20 June 1849, Bourgeau s.n.
[Pl. D’Espagne, 1849] (lectotype, here designated,
P 185468!, Fig. 9; see observations).
Illustrations: Gallego (1987: 565); Sáez & Aldasoro
(2001: 130, fig. 39i-m, as C. lusitanica subsp. specularioides); Fig. 10 A, B.
Herb 6-26 cm, annual, decumbent, branched from
the base, glabrous or glabrescent, very brittle. Stems
Fig. 9. Lectotype of Campanula specularioides (P 185468, herb.
Cosson).
Seeds 0.5-0.7 × 0.2-0.3 mm, ovoid, shining, yellowish
to brown. 2n = 20; n = 10.
Habitat, phenology and distribution: In crevices in
walls or limestone rocks; 500-1650 m. V-VI(VII). •En-
33
demic to Sierra de Grazalema and Serranía de Ronda
(Fig. 8). Spain: Ca Ma.
Observations: Despite its narrow distribution, this
species is markedly variable in the colour of anthers
Fig. 10. Flowers and fruits of Campanula species. A, B, C. specularioides (Montejaque, Málaga, Spain, SEV 218871); C, D, C. transtagana (Valverde del Camino, Huelva, Spain, SEV 216212); E, F, C. broussonetiana (Jbel Tazzeka, Taza, Morocco, SEV 216476). The scale bar = 3 mm.
34
and stigmas, and in the indumentum of calyx and capsule. since both can be very hairy or completely
glabrous, even in the same population, although more
commonly all plants of a population have glabrous calyx, and likewise the capsule. Within populations
there are plants with white anthers and stigmas, and
others with blue anthers and stigmas, or even plants
with white anthers and blue stigma or vice versa. All
these colour morphs, which certainly have a genetic
basis, seem to be interfertile so this trait has little taxonomic value. Based on the middle position of the
pores in the capsule, this species was included by Fedorov (1976) in the sect. Campanula. The phylogenetic tree of nr DNA ITS shows that C. transtagana and
C. broussonetiana are sister species of C. specularioides
(see Fig. 1).
The type material of C. specularioides consists of
three complete plants and several fragments. The
largest of the three plants, placed at the top of the
sheet was chosen as lectotype, since it is consistent
with the description of E. Cosson (see Fig. 9). In the
general herbarium of the “Conservatoire et Jardín
Botanique de Genève” there is a sheet (G 104263)
with several plants of the same collection of E. Bourgeau, that are also possible type materials.
C. lusitanica subsp. transtagana (R. Fern.) Fedorov in
Bot. J. Linn. Soc. 67: 281. 1973. Ind. loc.: “Habitat
in Lusitania, regione Transtagana, ad marginem
sinistram fluminis Tagis pr. pagum dictum Vila Velha de Ródâo, ubi super declives solo argilloso et sicco inter sepes copiosa, 21-VI-1959, A. Fernandes,
J. Matos & A. Sarmiento 2923 (COI, holotype)”,
(Fig. 11; see observations).
C. loeflingii var. filiformis Lange in Vidensk. Meddel.
Dansk. Naturhist. Foren. Kjøbenhavn 1861: 108.
1862. Ind. loc.: “La Carolina (Sierra Morena) 10
Mai.”. Type : not found in the Lange herbarium (C).
Illustrations: Fig. 10 C, D.
Herb 6-45 cm, annual, decumbent or erect,
branched from the base, rarely in the upper half, very
laxly pubescent, not brittle. Stems angled, branched,
glabrescent, with hairs 0.1-0.2, commonly very laxly
located in the stem angles. Leaves not coriaceous, crenate, entire or toothed, petiolate; middle cauline
leaves (4.6)9-20(30) × 2.2-8(13.2) mm, elliptic, laxly
pubescent, with hairs 0.1-0.3 mm scattered over the
limb and margin of the leaf, and with petiole 0.2-4.5
Selected spcimens
SPAIN. Cádiz: Benaocaz, Km 16-17 a Ubrique, 22-VI-1984, A.
Aparicio & J. G. Rowe (MA 490917, SEV 161738). Entre Benaocaz
y Ubrique, 13-VII-1978, J. Devesa & al. (MA 465708, MA 111772,
SEV 103546). Entre Ubrique y Grazalema, 13-VI-1970, E.F. Galiano & B. Valdés (SEV 108955). Entre Villaluenga del Rosario y
Benahocaz, 26-VI-1988, Férnandez Díez & Mochales (SALA
47474, MA 476540). Grazalema, 21-VI-1890, E. Reverchon, in E.
Reverchon, Plantes de L’ Andalousie, 1890: nº 331 (G 104191).
Idem, 9-VII-2003, J. Cano-Maqueda (SEV 216211). Cerro de San
Cristóbal, V-1961, J. Borja (MA 177095, SEV 5016). Manga de Villaluenga, 22-VI-1983, A. Aparicio & J.G. Rowe (SEV 161737).
Sierra de la Silla, 21-VI-1983, A. Aparicio & S. Silvestre (G 104188,
MA 490918, SEV 161731). Sierra de Zafalgar, Puerto de la Miera,
28-VI-1984, A. Aparicio & al. (SEV 161726). Sierra del Caillo,
Navazo Alto, 30-VI-1983, A. Aparicio (SEV 161730). Sierra del
Endrinal, Pozo de las Presillas, 12-VII-1984, A. Aparicio & S. Silvestre (SEV 161736). Ubrique, 26-VI-1925, P. Fonti Quer & E.
Gros (MA 702195, MGC 53268, SALA 114797). Villaluenga del
Rosario, 24-VI-1973, A. Asensi & B. Diez (MGC 81). Málaga: Benaoján, 17-VI-2007, J. Cano-Maqueda (SEV 218871). Cartajima,
Cancha Almola, 12-VI-2004, O. Gavira (MGC 60974, MGC
60975). De Ronda a Montejaque et circa Cueva de la Pileta, 17/18VI-1972, L. Bernardi (G 104194, MA 269887). Jimera de Líbar,
Alto del Conio, 4-VII-2004, O. Gavira (MGC 60868). Montejaque, 8-VI-2005, J. Cano-Maqueda (SEV 216210). Serranía de
Ronda, 23-VII-1888, E. Reverchon, in E. Reverchon, Plantes de
L’Andalousie, 1889: nº 331 (G 104264, G 104185, G 104186,
G 104187, G 104192, G 104193, LISU 50130, MA 121476, MA
121477).
5. Campanula transtagana R. Fern. in Bot. Soc. Brot.
ser. 2, 36: 121-126. 1962
Fig. 11. Holotype of Campanula transtagana (COI).
mm; upper cauline leaves (3)5-11(15) × 0.6-3.4 mm,
elliptic, laxly pubescent, with hairs 0.1-0.3 mm scattered over the limb and leaf margin, and with petiole
0.2-0.3 mm. Inflorescence laxly paniculate. Flowers
pedicellate; pedicel 9.6-64 mm, glabrous or with some
hairs of c. 0.5 mm. Calyx-teeth (2.9)3.5-16.6 × 0.3-0.7
mm, linear. Corolla (6.5)8-12(14) mm, campanulate,
with the tube greater or equal, rarely shorter, than the
lobes; tube (2.9)3.7-7 mm, light blue with a white
base; lobes 3.6-7 × 2.2-3.5 mm, elliptic, bluish. Stamens with enlarged base of 0.5-1 × 0.3-0.6 mm; filaments 0.2-0.6 mm; anthers 1.6-2.7 mm, whitish.
Ovary glabrous, rarely with setose hairs 0.1-0.2 mm;
style 4.5-6.4 mm, hairy in the upper half; stigma trifid,
with estigmatic branches 0.6-1.2 mm, patent, curved,
white. Capsule 2-4.4 × 1.5-3 mm, subovoid or subspherical, longer than wide, glabra, rarely with some
setose hairs of 0.1-0.2 mm, with 10 angled nerves, but
not winged, dehiscing by three pores of middle or
subapical position. Seeds 0.4-0.6 × 0.1-0.2 mm, ovoid,
shining, yellowish to brown. 2n = 20; n = 10.
Habitat, phenology and distribution: Wet grasslands
on sandy or slate-rich substrates; 50-800 m. V-VI
(VII). • Endemic to SW Iberian Peninsula, from the
River Tajo to the Guadiana, Sierra de Guadalupe and
almost all Sierra Morena (Fig. 12). Portugal: AAl Ag
BAl BB. Spain: Ba Cc Co H J Se.
Observations: C. transtagana is rare in Portugal and
in Sierra de Guadalupe but very common throughout
the Sierra Morena, especially in shady slopes and valley bottoms, where it normally co-habits with C. matritensis. The profuse branching, small corollas with
white background tube and petiolate leaves of the
stem, clearly differentiate it from C. matritensis.
The holotype of C. transtagana consists of five cultivated plants that are very branched from the base,
between 20 and 35 cm, and placed on three sheets in
Coimbra herbarium.
35
bar García (MA 707042). Oliva de la Frontera, riberas del río
Ardilla, 23-IV-1994 VI itinera Mediterranea nº 557 (MA 717195).
Cáceres: Guadalupe, 31-V-1958, E. Guinea (MA 432639). Córdoba: Alcolea, margen derecha del Guadalquivir, 21-V-1987, Z. Díaz
& C. López (SEV 130952). Cardeña, 24-VI-2005, J. Cano-Maqueda
& al. (SEV 216480). Entre Azuel y el río de las Yeguas, 28-V-1982,
J. Devesa & García (SEV 161896). Entre Montoro y Adamuz,
proximidades a Montoro, 4-V-1982, M.J. Díez & I. Fernández
(SEV 161898). Río Zújar, cruce con la carretera Los BlázquezPeraleda de Zaucejo, 6-VI-1979, J.M. Muñoz & E. Ruiz de Clavijo
(SEV 161897). Trassierra, derecha del Guadiato, Cerro del Trigo,
pantano de la Breña, 16-VI-1978, J.A. Varela (SEV 161900). Villafranca, central eléctrica, río Guadalquivir, 21-V-1987, Z. Díaz &
C. López (SEV 130876). Huelva: Alosno, 26-V-1942, C. Vicioso
(MA 121571). Aracena, entre la Cefiña y la N433, 23-V-2005,
J. Cano-Maqueda & al. (SEV 216213). Corterrangel, 18-VI-1978,
J. Rivera (SEV 48336). Entre Aroche y Las Cantiendas, 6-VI-1979,
J. Rivera & B. Cabezudo (MGC 8832, SEV 48900). Escacena
del Campo, Reserva de la Pata del Caballo, arroyo del Chacho,
31-V-2001, B. Cabezudo & al. (MGC 48565). Higuera de la Sierra,
400 m, 24-V-1988, E. Bayón & E. Villanueva (MA 438691).
Linares de la Sierra, 22-VI-1942, C. Vicioso (MA 121570). Río
Múrtiga, 8-VI-1984, F.J. García & al. (G 104154). Valverde del
Camino, El Manzanito, 23-V-2005, J. Cano-Maqueda (SEV
216212). Jaén: Andújar, Arroyo de los Santos, 22-VII-1992, J.M.
Mancebo (MA 651609). Baños de la Encina, Charca de la Enea,
29-VII-1992, J.M. Mancebo & J.R. Molina (MA 651610). Despeñaperros, 1-VII-1975, J. Fernández Casas & al. (MA 412612).
Sevilla: Castilblanco de los Arroyos, 1-VI-2006, J. Cano-Maqueda
& al. (SEV 232786). El Castillo de las Guardas, V-1914, C. Vicioso (MA 121569). El Garrobo, junto a la carretera, 15-V-1982,
J.M. Rodríguez & al. (SEV 161950). Entre el Ronquillo y Almadén
de la Plata, 22-VI-1976, E.F. Galiano (SEV 161899). Guillena,
Arroyo Herrero, without date, C. Fernández & J.A. Fariña (SEV
109874).
Selected specimens
PORTUGAL. Algarve: Serra da Picota, VII-1891, J. Brandeiro
(COI). Alto Alentejo: Redondo, V-1892, A. Fernandes & al.
(COI). Idem, VI-1893, A. Fernandes & al. (COI). Riveira da Sapatoa, a 5 km de Montoito e a 16 de Reguengos de Monsaraz, 10-VI1962, A. Fernandes & al. (COI). Baixo Alentejo: Concelho de
Moura, margens do rio Guadiana, 2-IV-1999, P. Bringe & T. Rego,
in Exsiccata Flora Iberomacaronesica Selecta, centuria IV: nº 340:
(FCO 25015, MA 632684, SALA 99329, SANT 42025). Entre
Eiras Altas e Claúdia, 11-VI-1962, M. da Silva (LISE 76991, MA
199926). Margem da ribeira de Chança, prox. Vila Verde de Ficalho, 11-VI-1962, A. Fernandes & al. (COI). Beira Baixa: Encosta da
margem esquerda do Tejo, entre a estrada e o rio Tejo, 8-VI-1962,
A. Fernandes & al. (COI). Salvaterra do Extremo, 14-VI-2005, A.
Charpin (G 104159).
SPAIN. Badajoz: Don Benito, La Zafrilla, 28-VI-1985, M.J.
Gallego (SEV161715). Magacela, El Berrocal, 25-V-2001, P. Esco-
Fig. 12. Distribution map of Campanula transtagana (䡬) and
C. broussonetiana (䊱).
36
6. Campanula broussonetiana Schult. in Roem. &
Schult., Syst. Veg. 5: 104. 1819-1820
C. lusitanica var. broussonetiana (Schult.) Pau in Mem.
Real Soc. Esp. Hist. Nat. 12: 356. 1924. Ind. loc.:
“In Mogador. Broussonet”. Type: Morocco. Safi,
Mogador, Broussonet s.n. (lectotype: here designated, W 03798!; see observations).
C. loeflingii var. maura Murb., Contr. Fl. Maroc. 2: 50.
1923. Ind. loc.: “Pentes herbeuses entre Amismiz et
Oucheffine; Ighen Draa près Demnat. 900-1000
m.- J’ai vu la même plante des environs de
Casablanca (leg. Mellerio)”. Type: not studied.
C. lusitanica f. pallidiflora Maire in Jahand. et Maire,
Cat. Pl. Maroc: 735. 1934. Ind. loc.: “Mont Tazzeka
(Humbert et Maire)”. Type: not studied.
C. lusitanica f. tenuis Caball. in Trab. Mus. Ci. Nat.
Madrid, Ser. Bot. 30: 5. 1935. Ind. loc.: “Legi basi
montis Tamarrut dicto, 6-VII-1934”. Type: Morocco. Agadir, Tamarrut, 6 July 1934, Caballero s.n.
(lectotype, here designated, MA 121492!; see observations).
C. vincaeflora Pau in Bol. Soc. Esp. Hist. Nat. 21: 278.
1921, nom. illeg., non Vent. 1804. Ind. loc.: “Tiguisar, 26-IV[-1921]”. Type: Morocco. Tittáguen,
Tiguisar (Gomara), 26 April 1921, Vidal López s.n.
(lectotype, here designated, MA 121493!; see observations).
Illustrations: Fig. 10 E, F.
Herb 6-45 cm, annual, erect or decumbent,
branched from the base, pubescent, not brittle. Stems
angled, branched, pubescent, rarely glabrous at the
apex, with long hairs up to 0.4-2 mm. Leaves scarcely
coriaceous, crenulated, entire or toothed; middle
cauline leaves 8-37 × (4)6-15.5 mm, broadly elliptical
or obovate, sessile and cuneate or with petiole up to 2
mm and rounded at the base, entire or toothed, ± pubescent, with hairs up to 1.2 mm; upper cauline leaves
(4.2)6-13.5 × 1-7.6 mm, elliptical or lanceolate, generally entire, sessile, cuneate, pubescent, with hairs up
to 0.4 mm or rarely glabrous, without a differentiated
petiole. Inflorescence laxly paniculate. Flowers pedicellate; pedicel 7-67 mm, glabrous or with hairs 0.21.2 mm. Calyx-teeth (3.6)5.2-13.5 × (0.4)0.7-2(2.7)
mm, oblanceolate, rarely linear. Corolla (7.2)8.8-17
mm, campanulate, with the tube usually shorter or
equal in length to the lobes, rarely longer than lobes;
tube 4,1-8,3 mm, with the base whitish and the apex
light blue; lobes (2.4)3.5-8 × 2.1-5,2 mm, ellipticlanceolate, bluish. Stamens with enlarged base of 0.60.7 × 0.4-0.6 mm; filaments 0.6-0.7 mm; anthers 2.1-4
mm, bluish or white. Ovary glabrous, rarely with hairs
0.1-0.8 mm; style 5-8.2 mm, hairy; stigma trifid, with
stigmatic branches of 1-2 mm, patent, curved, white
or blue. Capsule 3-6.6 × 2-4.1 mm, subovoid, longer
than wide, glabrous, rarely with setose hairs, with 10
nerves ± angled but not winged, dehiscing by three
subapical pores. Seeds 0.4-0.6 × 0.2-0.3 mm, ellipsoid, shining, yellowish to brown. 2n = 20.
Habitat, phenology and distribution: Shady hollows
and the understory of cork woodlands, on limestone,
or slate-rich or sandy substrates, from sea level to high
mountains; 0-2000 m. IV-VII(VIII). • Endemic to W
and N Morocco, along most of the Atlantic coastlands
from Sidi Ifni to the Mamora forests; also the Rif,
Middle Atlas and Great Atlas (Fig. 12).
Observations: This species has the same color
morphs for anthers and stigmas as those found in
C. specularioides, and similary, the morphs seem to be
interfertile. Alphonse De Candolle (1830) syno nymized this species with C. loeflingii Brot., possibly
influenced by the illustration 18 of the “Phytographia
Lusitaniae Selector” (Brotero, 1816) under this name.
Certainly, C. lusitanica and C. broussonetiana are very
similar morphologically. Both have long hairy indumentum that is straight and patent on the stem, and
wide leaves, but in C. broussonetiana the middle
cauline leaves are attenuate at the base or petiolate
and in C. lusitanica are sessile and subauriculate. The
molecular phylogeny has shown that C. broussonetiana is more closely related to C. transtagana than any
other species of sect. Rapunculus (see Fig. 1).
The sheet of type material of C. broussonetiana
(W03798) contains a complete highly branched plant
with many flowers. Schultes (1819-1820: 104) already
indicated that the type material was in the Willdenow
herbarium under the name Campanula ramosissima.
In the herbarium of the Prodromus of De Candolle there are two sheets (G 138472 and G 138271G 138478), one (G 138472) with a complete plant of
c. 30 cm and the other (G 138271, G 138478) with
three smaller plants (15-22 cm), all belonging to the
expedition by Broussonet in 1804, collected at Mogador (Essaouira, Morocco). This last sheet contains
two labels. In one (G 138478), handwritten by A. De
Candolle, is indicated “Voyage de Broussonet 1804”
at the base of two of the plants, and in the other (G
138271), with orthography of Broussonet, is written:
“Campanula/Mogador” and also, with orthography of
Alphonse De Candolle, “Campanula loeflingii Brot./ _
Broussonetiana Roem. Et Sch./ A. DC.”. These materials were probably not studied by Schultes, and
therefore they can not be considered type material
(Fig. 13).
The sheet of type material of C. lusitanica f. tenuis
contains two complete plants with flowers in postan-
thesis and two single flowered small stems. The larger
sized plant (c. 20 cm) is chosen as lectotype. The sheet
also contains three determinavit labels, one handwritten by C. Pau, which reproduces all the information of
the name, the diagnosis and the protological description from Caballero; the second label was identified as
C. lusitanica by Yvonne Nyman in 1987 and the third
label by Juan José Aldasoro and Llorenç Sáez who
identified the specimen as C. broussonetiana
The type material of C. vincaeflora consists of a single whole plant in flower that we have chosen as lectotype. The sheet contains some other stems and a label
printed with the original description.
Selected specimens
MOROCCO. Agadir: Col du Kerdous (Anti-Atlas), 26-V1980, A. Charpin & al. (G 104179, MA 227542). Ida Ouehembal,
Sud-ouest du Maroc, 1875, Mardochée (G 104254, G 104168, G
104255). O. Querat, Sous, 29-IV-1923, E. Jahandiez, in E. Jahandiez. Plantes Marocaines, 1923: nº 211 (G 104173). 3 Km Sidi
Ifni, 16-IV-1989, F. Jacquemoud (G 104160). Beni Mellal: entre le
Fig. 13. Materials of Campanula broussonetiana. Collected by
Broussonet in Mogador (Essaouira, Morocco) during his campaign in Morocco in 1805. The type material of this collection is
located in Willdenow herbarium (B).
37
Col du Tizi Mlil et Beni Mellal, 5-VI-1980, A. Charpin & al. (G
104180, MA 243114). Entre Oulad M’ Barek y Ouaouizarhte, cerca de Beni Mellal, 12-VI-1982, J. Fernández Casas & al. (MA
633188, MA 430482). Gran Atlas, entre Afourer y Bin-el-Ouidane,
9-VII-1996, S. Cirujano & al. (MA 625034). Subida al Jbel
Tassemit, 23-IV-2003, S. Talavera & al. (SEV 216216). Dar el Beïda: Sidi Abd-Er-Rahman, 1886, Ibrahim (G 104250). El Jadida: 20
Km NE Benahmed an der Strase nach El-Khatouat (1419), 6-V1989, D. Podlech (G 104182). Er Ribat: Arbaa-Sehoul, en la carretera hacia Romani, 2-V-2007, S. Talavera & al. (SEV 224279).
Fes: subida a Jbel. Zalagh, al NE de Fes, 16-V-2006, S. Talavera &
al. (SEV 217539, SEV 217537, SEV 217536, SEV 217535, SEV
217534). Bab Zitouna, collado del Jbel Zalagh, en la ruta de Fes a
Ouezzane, 10-V-1994, A. Achhal & al. (SEV 161661). Jbel Zalagh,
al NE de Fes, 17-V-2006, S. Talavera & al. (SEV 216499). Kenitra:
entre Sidi-Slimane y Khemisset, en saladares, 9-IV-1983, J.A. Devesa & al. (SEV 161658). Forèt de la Mamora, entre Khemisset y
Tiflet, a la izquierda en dirección a Máaziz, 25-V-2006, S. Talavera
& al. (SEV 234710). Mamora, Dar Salem, sables, 29-IV-1924, E.
Jahandiez, in E. Jahandiez, Plantes Marocaines, 1924: nº 211 (G
104174, MA 121503). Montes de Zaïan, entre Tiddas y Jbel,
Bouchchene, 24-V-2006, S. Talavera & al. (SEV 234709). Salé, 25IV-1888, Grant (G 104251). Marrakech: cerca de Toufliht, entre
Marrakech y Taddert, 14-VI-1982, J. Fernández Casas & al. (MA
430483). De Marrakech a Oukaimeden, Ogaionar, a 53 km de
Marrakech, 1-VI-2007, S. Talavera & al. (SEV 223071). Gran Atlas, V-1871, Hooker (LISUG 50012). Krifla, 16/18-IV-1887, Grant
(G 104167). Medna Ben Abou, 11-IV-1921, G. Wibagek (G
104175). Tabgourt, 20-VII-1884, Ibrahim (G 104259). Sidi-Ouasmin, 12-VI-1889, Ibrahim (G 104252). Meknés: Atlas Medio, entre Oulmés y Aguelmous, 24-V-2006, S. Talavera & al. (SEV
234711). Entre Meknés et Fes, 2 Km avant le croisement à Ain
Taoujdate, 15-V-1989, B. Valdés & al (SEV 161657). Zerhoun, c.
25 Km due NE of Meknès road from Moulay Idriss to Nzaia-desBeni-Ammar, 5-VI-1994, S.L. Jury, M. Ait Lafkih & B. Tahiri (SEV
161660). Oudjda: Berkane, Refuge Zegzel, 23-V-1928, A. Faure (G
104165). Env. de Martimprey-du-Kiss, Pelouses et broussailes, 14V-1930, A. Faure (G 104177, G 104166, MA 121481). Monts des
Beni-Snassèn, Djbel Fourhal, près de Taforalt, 23-V-1994, J. Lambinon & G. Van Den Sande (MA 562384). Safi: environs de Mogador, 1867, B. Balansa (G 104253). Falaises da Cap Safi, 17-IV1924, in E. Jahandiez, Pl. Maroc. 1924: nº 82 (MA 121482). Mogador, 1804, Broussonet (G 138271, G 138472, G 138478). Tandja: Chaouia, 25-IV-1935, Gattefossé (G 104163). Taza: c. 32 Km
from Taza on minor road near Bab-Bou-Idir, 6-VII-1993, S.L. Jury
& al. (SEV 161656). 11 Km from Taza on minor road below RasEl-Ma, 4-VII-1993, M. Ait Lafkih & al. (MA 577072, SEV
161659). Entre Bab-Azhar y Bab-Bou-Idir, 17-VI-2003, S. Talavera & al. (SEV 216476, SEV 216478). Entre Sidi-Abdallah-desRhiata y Bab-Azhar, 17-VI-2003, S. Talavera & al. (SEV 216475).
Tittáguen: Armautah, lower part of Jbel Bouhalla, 3-VII-1993,
J.A. Mejías & S. Silvestre (SEV 139107). Bou-Ahmed, pista entre
Souk-el-Had e Imazerdane, 29-IV-1995, M.A. Mateos & al. (SEV
139102). C. Iaarguit ( Beni Hosmar), 26-V-1930, Font Quer, in
Font Quer, iter maroc. 1930: nº 637 (G 104162, MA 121489). Entre Bou-Ahmed y Targha, 3-V-1996, M.A. Mateos & al. (SEV
155222). Kaa Asras, Imarsboutene, 5-V-1996, M.A. Mateos & al.
(SEV 155672). Oued-el-Kannar, 7-VI-1930, Font Quer (SEV
139142). Oued Laou, 9-IV-1995, A.J. Caruz & al. (SEV 139100).
SE of Chefchaouen, E of Bab Taza, on road from Cherafat to Bab
Berred, Matrasse Lakhmasse, 28-V-2002, M. Ait Lafkih & al. (MA
698258). Sok-el-Jemis (Beni Selman), pr. Tiguisas, 7-VI-1930,
Font Quer, in Font Quer, Iter Maroc., 1930: nº 638 (G 104164, MA
121484). Talembote, 1 Km vor dem Ort in Flussbett des Oued
Talembote, zw. Tamarix u. Oleander, 7-VII-1971, M. Dittrich (G
104178, G 104172). Targha, 7-IV-1995, A.J. Caruz & al. (SEV
38
139141); ibidem, valle en la ladera W del Djebel Azenti, 8-IV1995, A.J. Caruz & al. (SEV 154716). Tarsif , próximo a OuedLaou, 30-IV-1995, M.A. Mateos & al. (SEV 139101). Tétouan, entre Chechaouen y Talembote, 31-V-1981, (MA 236533). Xauen,
14-V-1921, Font Quer, in Font Quer, iter maroc., 1928: nº 391 (G
104161, MA 121483, MA 121502, MA 121491).
B. Sect. Decumbentes Cano-Maqueda & Talavera,
Sect. nov.
Type (here designated): Campanula decumbens A.
DC.
Plantae annuae vel perennes. Sinus calycis exappendiculati. Corolla infundibuliformis. Antherae albae.
Stylus glaber. Stigma tripartitum erectum vel erectopatens rectum album, in pagina abaxiali multos pilos
pollen collectores exhibet, pagina adaxiali glabra in qua
pollen germinat. Capsula obpyramidali vel ovata 5angulari, poris tribus versus apicem vel subapicem sitis
dehiscente.
Annual or perennial plants. Without calycine appendages. Corolla infundibuliform. Anthers white.
Style glabrous with a tripartite stigma. Stigma erect or
erect-patent, straight, white, with numerous pollen collecting hairs on the abaxial surface, glabrous and receptive in the adaxial side. Capsule obpyramidal or ovoid,
dehiscing by three apical or middle position pores.
“Habitat in Hispaniâ propè Aranjuez … [description]. Specimina numerosa apud dominum Delessert, in herbario Ventenatii vidi. Circâ Aranjuez
in Hispania lecta fuerunt”. Type: Spain. Madrid.
Aranjuez, 1827, Delessert s.n. [lectotype, here designated, G 138256! (G-DC), Fig. 14; see observations].
Herb 8(14)-38 cm, annual, decumbent or erect,
branched in the upper half or from the base, glabrescent. Stems angled, branched only in the inflorescence, glabrous or with a few antrorse hairs 0.10.3(1.4) mm long, often scabrid near the flowers.
Leaves not coriaceous, entire, toothed or crenulate;
middle cauline leaves 9(13)-28 × 4.7-10 mm, elliptic
or lanceolate, petiolate or sessile, toothed or entire,
glabrous or with some hairs 0.1-0.2 mm scattered on
the underside nerves, and petioles up to 7-12 mm; upper cauline leaves 3(5)-15 × (0.5)2.5-8 mm, elliptic or
lanceolate, cuneate or shortly petiolate, glabrous or
glabrescent, with some hairs 0.1-0.3 long on the
Observations: This section consists of two species
from the Iberian Peninsula (C. decumbens and C. dieckii), and two species from the Eastern Mediterranean
(C. ramosissima and C. hawkinsiana). In the topology
of the ITS tree (Fig. 1), this section forms a moderately supported clade (67% PPS), where C. decumbens
appears as sister of C. dieckii (63% PPS), and C. ramosissima and C. hawkinsiana join into a well-supported
subclade (99% BS; 100% PPS). This section thus includes both annual (C. decumbens, C. dieckii, C. ramosissima) and perennial (C. hawkinsiana) taxa, and
also shows great variability in chromosome number:
with 2n = 32 in C. decumbens (in this work), 2n = 28
in C. dieckii (in this work), 2n = 20 in C. ramosissima (Damboldt & Podlech, 1964) and 2n = 22 in
C. hawkinsiana (Contandriopoulos, 1964a). The
morphological characters that define this section
(glabrous style with three straight, erect or erectpatent stigmas) are very rare in the Campanulaceae,
and only co-occur in Campanula sect. Pterophyllum
Damboldt.
7. Campanula decumbens A. DC., Monogr. Campan.: 334. 1830
C. patula var. decumbens (A. DC.) Cuatrec. in Trab.
Mus. Ci. Nat. Barcelona 12: 441. 1929. Ind. loc.:
Fig. 14. Lectotype and isolectotype of Campanula decumbens
(G 138256). The lectotype is the plant located in the center, on
the right, the only one with a flower in anthesis. The other plants
are isolectotypes.
nerves of the underside, and petioles up to 2 mm. Inflorescence laxely paniculate. Flowers pedicellate;
pedicel (10.5)40-60(206) mm, glabrous or with some
setose hairs near the ovary. Calyx-teeth (6)8-15 × 0.81.6 mm, lanceolate or closely oblanceolate, with the
apex obtuse or acute, entire. Corolla 12-21 mm, infundibuliform, with the tube shorter than the lobes;
tube 3-8 mm, light blue, with white base; lobes (7)910(14) × 5-8.1 mm, broadly triangular or elliptical,
blue, with three darker nerves. Stamens with enlarged
base of 0.7-1.5 × 0.5-1.5 mm; filaments c. 1 mm; anthers 1.6-3(3.8) mm, whitish. Ovary glabrous or papillose, rarely hairy; style (3)3.5-4(4.8) mm, glabrous,
with 3 stigmas; stigmas (2)2.3-5(5.5) × 0.35-0.4 mm,
erect-patent at anthesis, ± straight, flat in the adaxial
side, convex and with numerous pollen collecting
hairs on the abaxial side. Capsule (2.2)3-8 × 2.4-4(5.7)
mm, ovoid or obpyramidal, longer than wide,
glabrous or papillose, with 10 thick nerves, dehiscing
by three apical or middle position pores. Seeds 0.40.7 × 0.2-0.3 mm, ovoid or ellipsoid, shining, brownyellowish. 2n = 32.
Habitat, phenology and distribution: Grassland and
wet meadows, on basic substrates (limestone and
dolomite); 10-1250 m. VI-VII(VIII). •Endemic to the
S of Spain, in the Guadalquivir valley, Sierra de
Grazalema and Serranía de Ronda, cited only once
from Aranjuez. Spain: Ca M? Ma, Se.
Observations: The identity of C. decumbens has
been discussed by various authors (Pau, 1896; Cuatrecasas, 1929; Caballero, 1942; Fedorov, 1976; LópezGonzález, 1979-1980); but in fact most authors do
not treat with the decumbent plant from Aranjuez described by Alphonse De Candolle. These authors
looked for this species near Aranjuez, but they only
found an upright and very hairy plant with crenate
leaves. This upright plant is the species described by
Lange (1893) as C. dieckii and later by Pau (1896) as
C. semisphaerica. Only Fedorov (1976) indicated that
C. decumbens A. DC. is indeed decumbent. From the
type he thought it endemic to Aranjuez, and that it
might be better treated as subspecies or variety of
C. patula L., as proposed by Cuatrecasas (1929).
The type material of Campanula decumbens (G
138256) contains two complete plants of 20 and 25
cm and two stems, all with flower buds and only one
plant with an open flower. This flowering plant is chosen as lectotype. The other materials are isolectotypes
(see Fig. 14). In the general herbarium at Geneva
there is another sheet (G 104141), also from the Ventenat herbarium, containing an incomplete plant of 20
cm with two flowers. The label indicates “Campanula/
affinis vincaeflorae/ Aranjuez près Madrid”. The
39
plant contained in this sheet may also form part of
type material.
The type material has petiolate middle leaves of the
stem, and a small and infundibuliform corolla, in
which it resembles C. cabezudoi [described by LópezGonzález (1979-1980) as C. decumbens var. pseudospecularioides]. But the style with three ± straight
stigmas is similar to that of C. dieckii and so, it is clear
that C. decumbens A. DC. belongs to sect. Decumbentes. Cano-Maqueda & al. (2008) indicated that
this species, apparently only known only from the Delessert type materials, could be extinct. However, several populations have been located in Sierra de Grazalema and Serrania de Ronda, with the same characters
as the type material of C. decumbens A. DC. Plants
from two of these populations were cultivated in the
greenhouses of the University of Seville. They retained the decumbent habit, are self-incompatible
(Cano-Maqueda & al., unpublished data) and the
meiotic number of chromosomes is n = 16.
Due to this discovery that C. decumbens occurs on
diverse localities on alkaline substrates in the Serranía
de Ronda and surrounding areas, it is likely that the
material studied by Alphonse de Candolle came from
the Southern Betic Cordillera and not from Aranjuez
as stated in the sheet of the type.
Subsequently, a number of exsiccata by previous
collectors in this area and also from the Guadalquivir
valley and Cádiz coastland were also identified as C.
decumbens. However, the Guadalquivir valley plants
are morphologically rather different from those of the
Sierras Béticas, although the molecular phylogeny has
shown that both groups of plants do not present any
changes in the nucleotide sequence (Fig. 1). They also
have the same chromosome number (n = 16; Table 1
and Fig. 2H). However, since in addition to the morphological differences, the populations present a different ecology and distribution, we have considered it
most appropriate to treat these two groups of populations as two subspecies.
KEY TO THE SUBSPECIES
1. Middle cauline leaves petiolate; capsule (2.2)3-4(4.4) × 2,4-4
mm, ovoid ............... a. C. decumbens subsp. decumbens
1. Middle cauline leaves sessile; capsule 4-8 × 3-5.7 mm,
obpyramidal ................... b. C. decumbens subsp. baetica
a. Campanula decumbens A. DC. subsp. decumbens
Illustrations: De Candolle (1830, tab. 12 fig. A);
Fig. 15 A, B.
Herb 20-36 cm, decumbent. Middle cauline leaves
petiolate. Calyx-teeth (6)8-10 × 0.8-1.1 mm, lanceolate, with the apex obtuse. Corolla 12-14 mm; tube 3-
40
Fig. 15. Flowers and fruits of Campanula species. A, B, C. decumbens subsp. decumbens (Benaoján, Málaga, Spain, SEV 218875);
C, D, C. decumbens subsp. baetica (Villamartín, Cádiz, Spain, SEV 256653); E, F, C. dieckii (Alfarnate, Málaga, Spain, SEV 256652).
The scale bar = 3 mm.
4 mm; lobes 9-10 × 5-6 mm, broadly triangular. Stigmas 2-3.2 mm. Capsule (2.2)3-4(4.4) × 2.4-4 mm,
ovoid. 2n =32.
Habitat, phenology and distibution: Wet meadows,
on basic substrates (limestone and dolomite); (480)
1000-1250 m. VI-VII(VIII). • Endemic to the Sierra
de Grazalema and Serranía de Ronda (Fig. 16). Spain:
Ca M? Ma.
Selected specimens
SPAIN. Cádiz: Benaocaz, Manga de Villaluenga, 22-VI-1984,
A. Aparicio & S. Silvestre (SEV 161834). Grazalema, 11-VI-1890,
E. Reverchon, in E. Reverchon, Plantes de l ‘Andalousie, 1889: nº
17 (G 104066). Sierra del Endrinal, 10-VII-1925, Font i Quer & E.
Gros (G 104158, MA 702573, MGC 53045); ibidem, 29-VI-1849,
P. Fonti i Quer & E. Gros (SALA 114817). Málaga: Benaoján, Carretera hacia Ronda, 15-V-1988, D. Montilla (MGC 40574); ibidem, Sierra del Palo, 17-VI-2007, J. Cano-Maqueda (SEV 218875);
ibidem, 6-VI-2001, M. Becerra & al. (MGC 52844, MGC 51636);
ibidem, Puerto España, 25-V-2002, M. Becerra & F. Sánchez
(MGC 51972). Ronda, 18-VI-1889, E. Reverchon, in E. Reverchon,
Plantes de l’Andalousie, 1889 nº 17 (G 104072).
b. Campanula decumbens subsp. baetica CanoMaqueda & Talavera, subsp. nov.
41
A Campanula decumbens subsp. decumbens foliis
caulinis sessilibus non petiolatibus, caule erecto non
decumbente, capsula obpyramidali non ovata differt.
A Campanula dieckii foliis glabrescentibus integris
vel serratis, calyce, corolla stigmatibusque majoribus
differt.
This subspecies differs from Campanula decumbens
subsp. decumbens in its non-petiolate, sessile cauline
leaves, erect rather than decumbent stems, and obpyramidal capsule, not ovoid. It differs of Campanula
dieckii by its entire or toothed and glabrescent leaves,
and by the larger size of the calyx, corolla and stigmas.
Type: Spain. Sevilla. El Coronil, bujeos, June 1990,
Aparicio & Silvestre s.n. (holotype: SEV 217838!, Fig.
17; isotype: SEV 238167!).
Illustrations: Boissier (1839, tab. 120a, as C. erinoides); Fig. 15 C and D.
Herb (8)14-38 cm, erect. Middle cauline leaves sessile. Calyx-teeth (8)8.5-15 × 1-1.6 mm, closely
oblanceolate, with the apex acute. Corolla (12)14.5-
Fig. 16. Distribution map of Campanula decumbens subsp. decumbens (䡬), C. decumbens subsp. baetica (夡) and C. dieckii (䊱).
42
decabras i Provinsen Cuenca, 1.juni 1892 blomstrencle (Dieck)!”.Type: Spain. Cuenca, Uña, 1 June 1892,
Dieck s.n. (lectotype, here designated, C, herb. J.
Lange, Fig. 18; see observations).
C. matritensis var. nevadensis A. DC. in DC., Prodr.
7(1): 481. 1838. Ind. loc.: “in editioribus SierraeNevadae. (Boiss.!)”. Type: Spain. Granada, Sierra
Nevada, 1838, Boissier s.n. (lectotype, here designated, G138396!; see observations).
C. semisphaerica Pau, Not. Bot. Fl. Españ. fasc. 6: 76.
1896. Ind. loc.: “Sacañet, á 1100 m de alt. en compañía de la C. dichotoma; 8 julio 1895”. Type: Spain.
Castellón, Sacañet, 8 July 1895, Pau s.n. (lectotype,
here designated, MA121465!; see observations).
C. argutidens Porta et Rigo, Iter. Hisp. III: n.º 309
(1891), in sched., nom. nud.
C. specularioides var. argutidens Porta et Rigo, Iter.
Hisp. III: nº 309 (1891), in sched., nom. nud.
Illustrations: Sáez & Aldasoro (2001: 132, fig. 40, as
C. decumbens); Fig. 15 E, F.
Fig. 17. Holotype of Campanula decumbens subsp. baetica
Cano-Maqueda & Talavera (SEV 217838).
21 mm; tube (3.4)4-8 mm; lobes 7-14 × 5-8 mm, elliptical. Stigmas (4)4.3-5.5 mm. Capsule 4-8 × 3-5.7 mm,
obpiramidal. n = 16.
Habitat, phenology and distribution: Grasslands on
basic substrates, usually very clay soils; 10-200 m;
(V)VI-VIII. • Endemic to the S of Spain, in the Guadalquivir valley (Fig. 16). Spain: Ca Se.
Selected specimens
SPAIN. Cádiz: Cádiz, without date, Chaubert (G 104126). Cerca de Villamartín, 31-V-1969, E.F.Galiano & al. (SEV 161833); ibidem, en la carretera a El Bosque, 17-VI-2009, S. Talavera & al.
(SEV 248711). Vejer de la Frontera, Caños de Meca, 15-V-1959,
D.M.C. Brinton-Lee (SEV 81177). Villamartín, 8-V-2010, J. CanoMaqueda (SEV 256653). Sevilla: Carmona, J.M. Triguero (SEVhistórico 1077).
8. Campanula dieckii Lange in Overs. Kongel.
Danske Vidensk. Selsk. Forh. Medlemmers Arbeider 1893: 195. 1893
Ind. loc.: “Ciudad Encantada mellem Uña og Val-
Herb (3)8-20(30) cm, annual, erect, usually
branched in upper half, often densely pubescent, at
least in the lower half. Stem angled, little branched,
densely pubescent, with ± antrorse setose hairs, 0.10.7 mm, sometimes glabrescent at the apex. Leaves
somewhat fleshy, crenate, lobed or pedate, sometimes
the uppermost subentire; middle cauline leaves (4)718 × 3-9(14) mm, ± elliptical, sessile, subauriculate,
densely pubescent, with hairs 0.1-0.7 mm; upper
cauline leaves 3-13.5 × 0.5-2.5(7.7) mm, ± lanceolate,
sessile, subauriculate, glabrous or more often with
scattered hairs 0.1-0.6 mm. Inflorescence paniculate,
lax. Flowers pedicellate; pedicel (11.9)19-90(155)
mm, glabrous or papillose on top. Calyx-teeth (2.3)
3-10.5 × 0.7-1.5 mm, lanceolate, obtuse, with thickened margins. Corolla (6.6)8-13.7 mm, infundibuliform, with the tube much shorter than the lobes; tube
(1.5)3-4.5 mm, light blue with white base; lobes 712.3 × (3)4-5.5(7.6) mm, ovate-lanceolate, blue, with
three purple nerves. Stamens with enlarged base of
1.1-1.9 × 1.5-1.9 mm; filaments 0.6-0.7 mm; anthers
2.1-3(3.8) mm, whitish. Ovary glabrous, papillose
or densely hairy, with setose hairs of (0.2)0.7-2.2 mm;
style 2.1-4(4.7) mm, glabrous, with three stigmas;
stigmas (2.1)2.5-4 mm, erect-patent at anthesis,
± straight. Capsule (3.5)4.9-9(11.5) × 3.5-6.5 mm,
obpyramidal, longer than wide, from papillose to
densely hairy, with setose hairs of 0.3-1 mm, with 10
very wide nerves like flat ribs, dehiscing by three middle position pores. Seeds 0.5-0.8 × 0.2-0.3 mm, ovoid,
shining, yellowish to brown. 2n = 28.
Habitat, phenology and distribution: Wet meadows
and kermes oak woodlands on basic substrates (gypsum, limestone and dolomite); 600-2300 m. VIVII(VIII). • Endemic to the Iberian Peninsula, C, E
and SE Spain, where it is frequent, and rare in CW
Portugal, Serra do Sintra (Fig. 16). Portugal: E. Spain:
Ab Al Bu Cs CR Cu Gr Gu J Lo M Ma Mu Sa Sg So
To Va Z Za.
Observations: This species has been confused with
C. decumbens by several authors. Cuatrecasas (1929)
commented: “Las diferencias que separan a la planta
de De Candolle [C. decumbens] de la de Loefling
[C. lusitanica] son mínimas. La primera son simplemente formas de tallos menos ramificados y lacinias
calicinales más anchas que en la última, la cual, en
general, también difiere por su mayor estrechez de la
corola. Estos caracteres están, sin embargo, sujetos a
variaciones, lo mismo que la vestidura del tubo de los
cálices entre unos muy híspidos y otros muy lampiños”. However, in this comment Cuatrecasas is referring to three different species from the Sierra de Má-
43
gina (Jaen): C. matritensis with a glabrous ovary, and
C. cabezudoi and C. dieckii, both with very hairy, almost hispid ovary.
We have seen material of this species from two collections from Sintra (Estremadura, Portugal). One
collected by F. Fernandes in V-1914 (G 104249,
104150; LISU 36374; MA 121500), distributed in exiccata by F. Sennen (in F. Sennen Pl. Esp. n.º 6006),
and another by W. Rothmaler on 13-V-1938 (G
104148; LISE 4368). Since this plant has not been collected again at this locality, the presence of this species
as a native in Portugal may be considered doubtful.
However, this kind of disjunction is not uncommon in
other species of the Iberian Peninsula, i.e., Silene distichia Willd., a common species in the Eastern half
of Spain and rare in the W Portugal (Talavera, 1990).
The type material of Campanula dieckii is composed by 7 whole plants at anthesis of 10-20 cm with
sessile, elliptic, crenate cauline leaves, infundibuliform corolla, glabrous style, straight stigma and
densely setose ovary. The sheet also contains two flowers in an envelope. The first plant, in the upper left
corner of the sheet is chosen as lectotype, because it is
the one that best fits the description of the author. The
other six plants are isolectotypes (see Fig. 18). In the
Geneva herbarium there is a sheet (G104244) with
three plants that are also isolectotypes.
The sheet of type material of C. matritensis var.
nevadensis contains 6 plants in flower. We have chosen as lectotype the plant placed at the top right,
about 10 cm, very hairy, with crenate leaves and two
flowers in anthesis. The remaining plants are isolectotypes.
The type material of C. semisphaerica consists of
two very small plants, each with one flower open. The
plant on the right is the lectotype. On the sheet there
is a typed label by Ginés López-González dated 1311-1979 indicating the material contained on the
sheet as holotype. Pau’s indication “genuine” may be
understood that this material was chosen as type by
the author of the binomial.
Selected specimens
Fig. 18. Lectotype (in the upper left corner) and isolectotypes
(the rest of plants) of Campanula dieckii (C, herb. Lange).
PORTUGAL. Estremadura: Sintra, V-1914, F. Fernandes, in F.
Sennen, Plantes D’Espagne, 1926, nº 6006 (G 104150, G 104249,
LISU 36374, MA 121500, MA 474598); ibidem, 13-V-1938,
W. Rothmaler, in W. Rothmaler, Flora Lusitanica nº 13133 (G
104148, LISE 4368).
SPAIN. Albacete: Alcaraz, La Molata, 24-V-1993, B. Casaseca
& M.A. Carrasco (MA 531238). Alrededores de Santa Elena de
Ruidera, 24-V-1933, González Albo (MA 121567). El Ballestero,
28-VI-1935, González Albo (MA 432730). El Cascajal, 24-V-1933,
González Albo (MA 121480, MA 121479). Pontegruelos, 28-VI1935, González Albo (MA 432731). Tús, vertiente SE del Calar del
Mundo, 29-V-1987, E. Villanueva & al. (MA 393151). Villaverde
44
de Guadalimar, 18-VI-1969, P.E. Gibbs (SEV 161752). Almería:
Bacares, 4-VI-1929, E. Gros (MA 433604). De Bacares a la Venta
de Lleiva, 5-VI-1929, E. Gros (MA 433605). Burgos: Ciruelos de
Cervera. Pie del Alto de la Cabeza, 11-VII-1979, Pons Sorolla & Susanna (MA 413025). Hortezuelos, 17-VI-1982, M.A. Carrasco &
M. Velayos (MA 312710, SALA 32983). Huidobro, 5-VII-1987,
Galán Cela & A. Martín (MA 639955). Tejada. Pico Valdosa, 3VII-1979, J. Fernández Casas & al. (MA 413017). Ciudad Real: La
Molata, 2-VI-1934, González Albo (MA 201345). Cuenca: Barajas
de Melo, valle del río Calvache, pr. Urbanización Valderíos, 580 m,
30-V-1998, V.J. Arán & M.J. Tohá (MA 614852. MA 620787).
Pinar de Beteta, 8-VII-1932, A. Caballero (MA 121464). Talayuelas, 1100m, 18-VI-1979, G. Mateo (MA 256531). Granada: Alhama de Granada, Barranco del Malinfierno, 17-VI-2004, B.
Cabezudo & al. (MGC 59291). Arenas del Rey, El Cenacho, 3-VI2004, B. Cabezudo & al. (MGC 59289). Ascenso a Sierra Nevada,
falla del Purche, 8-V-1966, S. Silvestre (SEV 19702). Guadix, 11VI-1921, E. Gros (MA 31778). Sierra de Albuñuelas, 15-VI-1976,
A. Asensi & P. Díez (MGC 3617). Sierra de Baza, ascenso a Santa
Bárbara, 21-VI-1988, S. Talavera & al. (G 104091). Sierra de Castril, VI-1903, E. Reverchon., in E. Reverchon, Plantes d’Espagne
1903: nº 1209 (G 104074, MA 121523). Sierra de Cázulas, 23-VI1976, Ladero & al. (MA 204705, SALA 8787). Sierra de Guillimona, Cuerda de los Mirabetes, 23-VI-1988, S. Talavera & al. (G
104059). Huéscar, Sierra de la Sagra, cara sur, 14-VI-1995, B.
Cabezudo & al. (MGC 39893). Padul, 4-VI-1980, M. Ladero & al.
(SALA 92232). Sierra del Pinar, without date, Reverchon (G
104076). Sierra Nevada, Trevenque, VI-1973, J. Fernández-Casas
(G 104078, SEV 19866). Guadalajara: Codes, 21-VI-1988, M.A.
Carrasco & M. Velayos (MA 711892). Sacecorbo, 9-VI-1973, A. Segura Zubizarreta (G 104064, MA 269833). Tamajón, alrededores
de la ermita de los Enebrales, 4-VII-1978, M.A. Rivas & C. Soriano
(MA 385718). Torremocha del Pinar, 19-VI-1995, M.A. Martín
Ballesteros (SALA 59846). Jaén: between Tobos and Vites, bed of
river Zumeta, 25-VI-1988, S. Talavera & al. (G 104058). Cambil,
Sierra de Mágina, Matabegí, 15-VI-1995, B. Cabezudo & al. (MGC
39707). Cazorla, aledaños de la C. F. Fuente del Oso, 31-V-1976,
F. Muñoz Garmendia & C. Soriano (MA 454856). La Iruela, barranco de Guadahornillos, 16-VI-1976, F. Muñoz Garmendia & C.
Soriano (MA 454825). Las Altarillas, 16-VI-1941, E. Guinea (MA
432654). Orcera, 6-VI-1980, C. Soriano (MA 592112). Pozo Alcón,
pico de Cabañas, 20-VI-1975, F. Muñoz Garmendia & C. Soriano
(MA 454823). Santiago de la Espada, cabecera del arroyo del
Membrillo, 5-VI-1975, F. Muñoz Garmendia & C. Soriano (MA
454816). Segura de la Sierra, 17-VI-1850, E. Bourgeau, in E.
Bourgeau, Pl. d’ Espagne, 1850: nº 992 (G 104100). Sierra del
Pozo, VI-1905, E. Reverchon, in E. Reverchon, Plantes d’ Espagne
1905: nº 1209 (G 104134). Sierra Mágina, entre el Cortijo de los
Prados y Cerro Carceles, 11-VI-1987, E. Villanueva & al. (MA
401189). Siles, VI-1850, M. Blanco (G 104113). Madrid: Algodor,
31-V-1925, A. Caballero & González Guerrero (MA 432742, MA
432744). Aranjuez, V-1897, C. Pau (MA 121457). Idem, 25-V1919, C. Vicioso (MA 121459). Arganda, IV-1932, C. Pau (MA
432687). Piul de Rivas, V-1915, C. Vicioso (MA 121456). Venta del
Gorro, 1802, Lagasca (G 138462). Málaga: Alcaucín. Sierra Tejeda, loma de las Víboras, 7-VI-2002, D. Navas & al. (MGC 52239).
Alfarnate, 30-III-2007, (SEV256652). Canillas de Albaida, Los
Horcajos, puerto de la Orza, 5-VI-1919, E. Gros (MA 121468).
Castillo de Frigiliana, VI-1919, E. Gros (MA 121467). Cómpeta,
Navachica, 22-VI-2004, B. Cabezudo & al. (MGC 59293). Sedella,
14-VI-1994, A. Aparicio & al. (MA 543877). Sierra Tejeda, V1914, E. Gros (MA 121471). Murcia: Sierra de Moratalla, Revolcadores, 15-VII-1974, A. Charpin & J. Fernández. Casas (G
104079). Salamanca: Ledesma, 19-V-1976, J. Sánchez (MA
219750). Molinillo, 1859, Sainz (MA 153143). Segovia: Cedillo de
la Torre, 5-VI-1985, A.R. Burgaz & A. Izuzquiza (MA 306519).
Fuentidueña, 24-VI-1983, T. Romero (SALA 41198). Lastras de
Cuéllar, Molino Ladrón, 840 m, 24-V-1998, P. Bariego Hernández
& A. Gastón González (MA 754470). Villaseca, 12-VI-1983, T.
Romero (SALA 41951). Soria: Andaluz, 26-VI-1975, A. Segura Zubizarreta (FCO 7873, SEV 69199). Cañón del río Lobos, 17-VI1982, A. Buades (MA 502178). Herrera de Soria, 30-VI-1983, A.
Buades (MA 504408). Ucero, cuesta de la Galiana, 28-V-1983, A.
Buades (MA 504043). Toledo: Toledo, 22-V-1897, C. Pau (MA
121458). Valladolid: Castronuño, 20-VI-1984, F.J. González & C.
J. Valle (SALAF 7361). Encinas de Esgueva, 7-VII-1983, J.L. Fernández Alonso (MA 517691). Rábano, 15-VI-1983, T. Romero
(SALA 41197). Urueña, 20-VI-1980, Fernández Díez (SALA
22002). Valladolid, 17-VI-1906, Sennen (MA 121463). Zamora:
Castrillo de la Guareña, 30-V-1983, X. Giráldez (SALA 31601).
Zaragoza: Calatayud, 15-VI-1910, C. Vicioso (G 104095, MA
121462). Cerros de Andrés, VI-1898, C. Vicioso (MA 121460).
Acknowledgements
We thank Drs. B. Cabezudo (Málaga, Spain), the late S. Castroviejo (Madrid, Spain) and E. Rico (Salamanca, Spain) for their
help in field collections. We are grateful to curators of the cited
herbaria for the loan of specimens. We are also grateful to Dr. Peter Gibbs (St. Andrews, UK) for reviewing the manuscript.
This work has been financed by grants from the Ministerio de
Educación y Ciencia to M. Arista (REM2002-04354-C02-02
and CGL2005-01951), to S. Talavera (CGL2006-00817 and
CGL2009-08178) and by a predoctoral grant to J. Cano-Maqueda
(BES-2003-0332).
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Appendix 1
Species, origin of plant material,
voucher, collector or reference
and ITS GenBank accession no.
Adenophora divaricata Franch. & Sav.; cultivated in Royal
Botanic Gardens Edinburgh; Eddie & al. (2003); AY 322005 &
AY 331418. Asyneuma japonicum (Miq.) Briq.; Korea; Kim & al.
(1999); AF 183437 & AF 183443. Azorina vidalii (Wats.) Feer.;
cultivated in University of Edinburgh; Eddie & al. (2003); AY
322007 & AY 331420. Campanula alliarifolia Willd.; cultivated in
Royal Botanic, Garden, Kew; Eddie & al. (2003); AY 322008 &
AY 331421. C. alpina Jacq.; Austria, Niedere Tauern; Park & al.
(2006), DQ 304573. C. armazica Kharadze; Caucasus; Eddie & al.
(2003); AY 322009 & AY 331422. C. arvatica Lag.; cultivated in
University of Edinburgh; Eddie & al. (2003); AY 322010 & AY
331423. C. barbata L.; Italy; Eddie & al. (2003); AY 32211 & AY
331424. C. beckiana Hayek; Austria, Northeastern Alps; Park & al.
(2006); DQ 304619. C. bellidifolia Adams; Caucasus; Eddie & al.
(2003); AY 322012 & AY 331425. C. bononiensis L.; Austria, Leithagebirge; Park & al. (2006); DQ 304571. C. broussonetiana
Schult.; Morocco, Tazzeka (Middle Atlas); Cano-Maqueda & al.
(2008); FM 212711. C. cabezudoi Cano-Maqueda & Talavera;
Spain, Málaga, Junquera; Cano-Maqueda & al. (2008); FM
212727. C. carpatica Jacq.; USA, Illinois; Eddie & al. (2003); AY
322013 & AY 331426. C. cenisia L.; Austria, Lechtaler Alps; Park
& al. (2006); DQ 304622. C. cespitosa Scop.; Austria, Northeastern
Alps; Park & al. (2006); DQ 304621. C. decumbens A. DC. subsp.
decumbens; (1): Spain, Málaga: Benaoján; Cano-Maqueda & al.
(2008); FM 212735. C. decumbens subsp. baetica Cano-Maqueda
& Talavera; (2): Spain, Cádiz, Villamartín; Cano-Maqueda; HQ
407547. C. dichotoma L.; Italy, Calabria, NW of Nicótera; Park &
al. (2006); DQ 304579. C. dieckii Lange; (1) Spain, Granada, Alhama de Granada; Cano-Maqueda & al. (2008); FM 212733. C.
dieckii Lange; (2) Spain, Cuenca, Barajas de Melo; Roquet & al.
(2008) as C. decumbens; EF 090526 & EF 090567.C. divaricata
Michx.; USA, Virginia; Eddie & al. (2003); AY 322014 & AY
331427. C. drabifolia Sibth. & Sm.; Greece, Ionian islands, Atokos;
Park & al. (2006); DQ 304578. C. edulis Forssk.; Saudi Arabia; Eddie & al. (2003); AY 233015 & AY 331428. C. elatines L.; Italy,
Alpi Cozie; Park & al. (2006); DQ 304624. C. elatinoides Moretti;
Italy, Southern Alps; Park & al. (2006); DQ 304625. C. erinus L.;
Spain, Sevilla, Sevilla City; Cano-Maqueda & al., (2008); FM
212737. C. fenestrellata Feer subsp. fenestrellata; Croatia, Velebit,
Velika Paklenica; Park & al. (2006); DQ 304592. C. fragilis subsp.
cavolinni (Ten.) Damb.; Italy, Abruzzo; Park & al. (2006); DQ
304629. C. garganica Ten. subsp. garganica; cultivated in Botanical
Garden Zagreb (material from Italy); Park & al. (2006); DQ
304596. C. glomerata L.; cultivated in University of Edinburgh;
Eddie & al. (2003); AY 322017 & AY 331430. C. grossheimii
Kharadze; Caucasus; Eddie & al. (2003); AY 322018 & AY
331431. C. hawkinsiana Hausskn. & Heldreich; Eddie & al.
(2003); AY 322019 & AY 331432. C. hercegovina Degen & Fiala;
Bosnia & Herzergovina, Blidinje; Park & al. (2006); DQ 304616.
C. herminii Hoffmans. & Link.; Portugal; Eddie & al. (2003); AY
322020 & AY 331433. C. isophylla Moertti; cultivated in Botanical
Garden Zagreb (material from Italy); Park & al. (2006); DQ
304630. C. justiniana Witasek; Croatia, Čabranka river; Park & al.
(2006); DQ 304613. C. kolenatiana C.A. Mey.; Caucasus; Eddie &
al. (2003); AY 322022 & AY 331435. C. lanata Friv.; cultivated in
331436. C. latifolia L.; Eddie & al. (2003); AY 322024 & AY
331437. C. lusitanica L.; (1): Spain, Orense, Rivadavia, R. Pino;
HQ 407553. C. lusitanica; (2): Portugal, Sierra de Monchique, Talavera & al.; HQ 407550. C. lusitanica; (3): Portugal, Sierra de
Monchique; Talavera & al.; HQ 407551. C. lusitanica L. (4): Spain,
Pontevedra, Cangas de Morrazo, S. Castroviejo; HQ 407552. C.
marchesettii Witasek; Croatia, Učka; Park & al. (2006); DQ
304612. C. matritensis A. DC.; Spain, Huelva, Hinojos; Cano-Maqueda & al. (2008) as C. lusitanica; FM 212703. C. mirabilis Albov;
Royal Botanic Gardens Edinburgh; Eddie & al. (2003); AY
322026 & AY 331439. C. mollis L.; Spain; Eddie & al. (2003); AY
322027 & AY 331440. C. morettiana Rchb.; Italy, Dolomites; Park
& al. (2006); DQ 304602. C. ossetica Bieb.; Caucasus; Eddie & al.
(2003); AY 322028 & AY 331441. C. patula L.; Spain, Huesca, Hecho (Pyrenees); Cano-Maqueda & al. (2008); FM 212739. C. peregrina L.; Turkey; Eddie & al. (2003); AY 322029 & AY 331442. C.
persicifolia L.; cultivated in University of Edinburgh; Eddie & al.
(2003); AY 322030 & AY 331443. C. petraea L.; France; Eddie &
al. (2003); AY 322031 & AY 331444. C. portenschlagiana Schultes;
Croatia, Biokovo; Park & al. (2006); DQ 304600. C. poscharskyana
Degen; Croatia, Dubrovnik region; Park & al. (2006); DQ 304601.
C. primulifolia L.; (1): Portugal, Sirerra de Monchique, between
Monchique and Odemira; Talavera & al.; HQ 407555. C. primulifolia Brot.; (2): Spain, Huelva, Sierra de Aracena; Aldea de las Veredas, Arroyo del Acebuche; Talavera & al.; HQ 407554. C. pulla
L.; Austria; northeastern Alps; Park & al. (2006); DQ 304605. C.
punctata Lam.; cultivated in University of Edinburgh; Eddie & al.
(2003); AY 322033 & AY 331446. C. pyramidalis L.; cultivated in
331447.C. raddeana Trautv.; Caucasus; Eddie & al. (2003); AY
322035 & AY 331448. C. raineri Perpenti; Italy, Alpi Bergamaschi;
Park & al. (2006); DQ 304604. C. ramosissima Sibth. & Sm.; Greece, Lakonia; SALA 135597; Aedo & al.; HQ 407548. C. rapunculus L.; Spain, Huelva, Hinojos; Cano-Maqueda & al. (2008); FM
212738. C. reatina Lucchese; Italy, Turano Valley; Park & al.
(2006); DQ 304599. C. reverchonii A. Gray; USA, Texas; Eddie &
al. (2003); AY 322036 & AY 331449. C. rotundifolia L.; Spain, Cádiz, Grazalema; Cano-Maqueda & al. (2008); FM 212736. C. sarmatica Ker-Gawl.; Caucasus; Eddie & al. (2003); AY 322038 & AY
331451. C. siegizmundii Fed.; Caucasus; Eddie & al. (2003); AY
322039 & AY 331452. C. sosnowskyi Charadze; Caucasus; Eddie
& al. (2003); AY 322040 & AY 331453. C. sparsa Friv.; Greece,
Grevená, Palaiokastro; SALA 135596; Aedo & al.; HQ 407549. C.
specularioides Coss.; Spain, Cádiz, Grazalema; Cano-Maqueda &
al. (2008); FM 212705. C. spicata L.; Italy, Southern Alps; Park &
al. (2006); DQ 304574.C. stenocodon Boiss. & Reuter; Italy, Alpi
Cozie; Park & al. (2006); DQ 304620. C. steveni Bieb.; Caucasus;
Eddie & al. (2003); AY 322041 & AY 331454. C. thyrsoides L.; cultivated in University of Edinburgh; Eddie & al. (2003); AY 322042
& AY 331455. C. tommasiana Koch; Croatia, Učka; Park & al.
(2006); DQ 304611. C. transtagana R. Fern.; Spain, Córdoba,
Azuel (Sierra Morena); Cano-Maqueda & al. (2008); FM 212721.
C. tridentata Schreb.; Caucasus; Eddie & al. (2003); AY 322043 &
AY 331456. C. uniflora L.; Noeway, Sor-Trondelag; Park & al.
(2006); DQ 304588. C. versicolor Andrews; Greece, Ionian Islands, Kefallinía; Park & al. (2006); DQ 304607; C. waldsteiniana
Schultes; Croatia, Velebit Mtns.; Park & al. (2006); DQ 304610. C.
zoysii Wulfen; Slovenia, Kamniške Alps; Park & al. (2006); DQ
304603. Campanulastrum americanum (L.) Small.; Eddie & al.
(2003); AY 322044 & AY 331457. Canarina canariensis (L.) Vatke;
Spain, Canary Islands; Eddie & al. (2003); AY 322045 & AY
331458. Codonopsis dicentrifolia W. W. Sm.; Nepal; Eddie & al.
(2003); AY 322046 & AY 331459. Craterocapsa congesta Hilliard
& B.L. Burtt; Lesotho; Eddie & al. (2003); AY 322049 & AY
331462. Cynanthus lobatus Wall. ex Benth; Eddie & al. (2003); AY
322050 & AY 331463. Diosphaera rumeliana (Hampe) Bornm.;
47
322051 & AY 331464. Edraianthus graminifolius (L.) A. DC.; cultivated in Royal Botanic Gardens Edinburgh; Eddie & al. (2003);
AY 322052 & AY 331465. Feeria angustifolia (Schousb.) Buser;
Morocco; Eddie & al. (2003); AY 322054 & AY 331467. Gadellia
lactiflora (M. Bieb.) Schulkina; cultivated in Royal Botanic Gardens Edinburgh; Eddie & al. (2003); AY 322055 & AY 331468.
Galactites tomentosa Moench.; Sussana & al. (2006); AY 826285.
Githopsis diffusa A. Gray; Eddie & al. (2003); AY 322056 & AY
331469. Hanabusaya asiatica Nakai; South Korea; Eddie & al.
(2003); AY 322057 & AY 331470. Heterocodon rariflorum Nutt.;
USA, California; Eddie & al. (2003); AY 322058 & AY 331471. Jasione montana L.; Spain; Eddie & al. (2003); AY 322062 & AY
331475. Legousia falcata (Ten.) Fritsch; cultivated in Royal Botanic Gardens Edinburgh and University of Texas; Eddie & al.
(2003); AY 322064 & AY 331477. Leptocodon gracilis Lem.; Nepal; Eddie & al. (2003); AY 322066 & AY 331479. Michauxia tchihatcheffii Fisch. & C.A. Mey.; cultivated in Royal Botanic Gardens
Edinburgh; Eddie & al. (2003); AY 322068 & AY 331480. Musschia aurea Dumort.; cultivated in Royal Botanic Gardens Edinburgh and University of Texas; Eddie & al. (2003); AY 322067 &
AY 331481. Petromarula pinnata (L.) A. DC.; Greece; Eddie & al.
(2003); AY 322069 & AY 331482. Physoplexis comosa (L.) Schur;
cultivated in Royal Botanic Gardens Edinburgh; Eddie & al.
(2003); AY 322070 & AY 331483. Phyteuma orbiculare L.; Eddie
& al. (2003); AY 322071 & AY 331484. Roella ciliata L.; Eddie &
al. (2003); AY 322074 & AY 331487. Symphyandra armena (Stev.)
A. DC.; cultivated in Royal Botanic Gardens Edinburgh; Eddie &
al. (2003); AY 322075 & AY 331488. Trachelium caeruleum L.;
322078 & AY 331491. Triodanis leptocarpa (Nutt.) Nieuwl.; USA,
Texas; Eddie & al. (2003); AY 322079 & AY 331492. Wahlenbergia hederacea L.; Portugal, Sierra de Monchique, Talavera & al.;
HQ 407556.
Associate Editor: C. Aedo
Received: 27-X-2010
Accepted: 25-I-2011
2269 serapias:Maquetación 1 13/06/2011 12:11 Página 49
Vol. 68(1): 49-59
enero-junio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2269
Distinguishing colour variants of
Serapias perez-chiscanoi (Orchidaceae) from related
taxa on the Iberian Peninsula
by
Caspar Venhuis 1 & J. Gerard B. Oostermeijer 2
Derde Goudsbloemdwarsstraat 21, 1015 KA Amsterdam, The Netherlands. [email protected]
Institute for Biodiversity and Ecosystem Dynamics (IBED), Universiteit van Amsterdam, Science Park 904,
1098 XH Amsterdam, The Netherlands. [email protected]
1
2
Abstract
Resumen
Venhuis, C. & Oostermeijer, J.G.B. 2011. Distinguishing colour
variants of Serapias perez-chiscanoi (Orchidaceae) from related
taxa on the Iberian Peninsula. Anales Jard. Bot. Madrid 68(1):
49-59.
Venhuis, C. & Oostermeijer, J.G.B. 2011. Distinción de variantes
en color de Serapias perez-chiscanoi (Orchidaceae) en relación
con táxones de la Península Ibérica. Anales Jard. Bot. Madrid
68(1): 49-59 (en inglés).
Serapias perez-chiscanoi has a stable and uniform appearance
with green flowers. Throughout its distribution area, however,
plants have been found with deviant pink to red flowers that
show similarities with other taxa that are occasionally pale flowered. S. perez-chiscanoi is easy to differentiate from S. cordigera
subsp. cordigera by the colour of the flowers (S. cordigera
subsp. cordigera has red to purple flowers) and the fact that the
hypochile dimensions of S. perez-chiscanoi are significantly
smaller. It is, however, more difficult to distinguish it from individuals of S. cordigera subsp. gentilii with pale flowers, which
occur frequently. The two taxa differ in colour pattern and floral
dimensions, especially the hypochile length, which is shorter in
S. perez-chiscanoi. Pale-flowered individuals of another species, S. parviflora, are easily distinguished by their significantly
smaller flowers. S. perez-chiscanoi occurs in Spain in the autonomous regions of Extremadura and Castilla-La Mancha and
in Portugal, S. cordigera subsp. gentilii seems to occur along the
coastal regions of SW Portugal, while S. cordigera subsp. cordigera and S. parviflora are distributed throughout the Iberian
Peninsula.
La Serapias perez-chiscanoi tiene una apariencia estable y uniforme con flores verdes. Sin embargo, a lo largo de su área de
distribución, se han encontrado ejemplares de flores con coloraciones desviantes de color rosa hasta rojo que muestran similitudes con otros táxones que presentan ocasionalmente flores pálidas. Serapias perez-chiscanoi es fácil de diferenciar con
respecto a S. cordigera subsp. cordigera por el color de las flores (S. cordigera subsp. cordigera tiene flores de rojizas hasta
púrpura) y por las dimensiones significativamente más pequeñas del hipoquilo de S. perez-chiscanoi. Sin embargo es más difícil hacer una distinción con respecto a S. cordigera subsp. gentilii, ya que los individuos de este taxon presentan flores pálidas,
lo que ocurre con frecuencia. Estos dos táxones se diferencian
por el patrón de colores y por las pequeñas dimensiones de las
piezas florales, especialmente el tamaño del hipoquilo más corto en S. perez-chiscanoi. Los individuos de flores pálidas de
S. parviflora se pueden distinguir fácilmente gracias a sus flores
de pequeño tamaño. Serapias perez-chiscanoi se localiza en
España en las comunidades autónomas de Extremadura y
Castilla-La Mancha y en Portugal, S. cordigera subsp. gentilii se
puede encontrar en las zonas costeras del suroeste de Portugal,
mientras que S. cordigera subsp. cordigera y S. parviflora se encuentran en la mayor parte de la Península Ibérica.
Keywords: Orchidaceae, Serapias perez-chiscanoi, Serapias
cordigera subsp. gentilii, flower colour, floral dimensions, Spain,
Portugal.
Palabras clave: Orchidaceae, Serapias perez-chiscanoi, Serapias cordigera subsp. gentilii, color de las flores, dimensiones de
las flores, España, Portugal.
50
C. Venhuis & G. Oostermeijer
Introduction
In 1976 Jose Luis Pérez Chiscano discovered deviant Serapias plants along the Guadiana river basin in
Extremadura (Spain). After a twelve-year study, Pérez
Chiscano (1988) described these plants as a new
species, Serapias viridis Pérez Chiscano. Acedo
(1990), however, found that the same name had been
used for a Brazilian species by Vellozo (1825). To
avoid confusion, the Spanish species was renamed
S. perez-chiscanoi C. Acedo. Pérez Chiscano & al.
(1991) reported that only some eight populations of
this species were known, all located in the Guadiana
river basin in Extremadura. However, due to an increased interest in this species, many new populations
were found in Extremadura during the past ten years
(Venhuis & al., 2006). Furthermore, the species was
also found in Castilla-La Mancha (Venhuis & al.,
2006), and also in Portugal (Jansen, 1993). Observations on these recently found populations have increased our knowledge of the species. One new aspect
is that plants with deviant reddish flower colours were
found among the “normal” S. perez-chiscanoi individuals that have pale green flowers, or pale green flowers with a red venation. In this article, we describe the
variation in flower colour in S. perez-chiscanoi and the
differences and similarities in morphology and geographic distribution with other Serapias taxa.
ed as this species is morphologically readily distinctive
from the other taxa. According to the analyses by Venhuis & al (2007), the dimensions of the epichile and
hypochile are the most distinctive characters, and so
in each population we measured the width and length
of both the epichile and hypochile (Fig. 1).
Results and discussion
Variation in flower colour
Serapias perez-chiscanoi in Extremadura has a fairly
uniform morphology and flower colour. The plants
can be divided into two extremes, which present
“green” or “red veined” variants. In the green variation (Fig. 2a, b), the leaves, stem, bracts, ovary, gynostegium, lamellae, flowers and veins are all pale green,
with whitish hairs on the labellum. The lateral lobes of
the flowers are yellowish and greenish. The “red
veined” variation (Fig. 2c, d) is also greenish but with
a red venation on the leaves, stem, bracts and ovary. It
also has red veins and reddish hairs on the labellum
and pinkish to reddish lateral lobes and lamellae. Intermediate colour variations occur very frequently
(Venhuis & al., 2004).
In Portugal, most of the known populations mainly
comprise the “red veined” variation. A population of
about 80 flowering plants in C Portugal contained in-
Material and methods
a
In 2004 and 2010, we obtained morphological data
for populations of Serapias cordigera subsp. cordigera L., S. cordigera subsp. gentilii C. Venhuis, P. Venhuis & Kreutz, S. perez-chiscanoi and S. parviflora Parl.
in Spain and Portugal. For both subspecies of S. cordigera, we measured 25 plants, from one population of
subsp. cordigera in Extremadura, and likewise for
subsp. gentilii in the Algarve. With S. perez-chiscanoi
we measured 75 plants from three populations in Extremadura (Spain), and 5 plants from a population in
mid-western Portugal. For S. parviflora, 50 plants
were measured from two populations (Algarve and
Extremadura) (Table 1). The latter data is not includ-
d
b
Table 1. Sampled populations of the studied Serapias taxa.
Species
Location
S. cordigera subsp. cordigera
S. cordigera subsp. gentilii
S. perez-chiscanoi
S. perez-chiscanoi
S. perez-chiscanoi
S. perez-chiscanoi
Badajoz
Cotifo
Badajoz
Aljucén
Trujillanos
Ereiras
Region
Country
Extremadura Spain
Algarve
Portugal
Extremadura Spain
Extremadura Spain
Extremadura Spain
Beira Litoral Portugal
c
Fig. 1. Measured floral dimensions of the labellum: a, hypochile
width; b, epichile lenght; c, epichile width; d, hypochile lenght.
Colour variation in Serapias perez-chiscanoi
a
b
c
d
51
Fig. 2. a, Serapias perez-chiscanoi, Obando, Extremadura, Spain, 27-IV-2007; b, S. perez-chiscanoi, Trujillanos, Extremadura, Spain,
29-IV-2010; c, S. perez-chiscanoi, Vila Nova da Baronia, Baixo Alentejo, Portugal, 23-IV-2007; d, S. perez-chiscanoi, Alange, Extremadura, Spain, 30-IV-2010. All photographs: C. Venhuis.
52
a
b
c
d
Fig. 3. a, Serapias perez-chiscanoi, Ereiras, Beira Litoral, Portugal, 1-V-2010; b, S. perez-chiscanoi, Ereiras, Beira Litoral, Portugal,
1-V-2010; c, S. perez-chiscanoi, Ereiras, Beira Litoral, Portugal, 1-V-2010; d, S. perez-chiscanoi, Ereiras, Beira Litoral, Portugal,
25-IV-2011. All photographs: C. Venhuis.
dividuals with three flower colour variations. About
ten plants were of the “green” variation, whilst some
50 plants were quite similar to the “red veined” variation, but differed from it by a bright red hypochile and lateral lobes, an epichile that was both
greenish and pinkish, and the sepals, petals and bracts
were also often slightly pinkish (Fig. 3a, b). The most
deviant plants, however, about 20 individuals, had
a bright red labellum (hypochile, lateral lobes and
epichile), red petals and red veins on all plant parts.
In addition, the bracts and sepals were pinkish
(Fig. 3c, d).
Hybridization
Although hybridization cannot be excluded, the
occurrence of hybrids is unlikely. The pollinia of
S. perez-chiscanoi flowers disintegrate very rapidly
onto their own stigmatic surface, often before the
flowers open (Perez Chiscano & al., 1991), and so the
possibility that intact pollinia are transferred to another flower is limited. Moreover, S. perez-chiscanoi, is
a diploid (Bernardos & al., 2004), while S. lingua L.,
a species with which it is frequently sympatric, is
tetraploid (D’Emerico & al., 2000), so that the difference in ploidy level makes cross-fertility unlikely. In
contrast, S. perez-chiscanoi very rarely co-occurs with
the diploid S. cordigera, which makes hybridisation
between these two species also highly unlikely. Nevertheless, hybrids between S. perez-chiscanoi and both
S. lingua and S. cordigera have been reported. A hybrid between S. perez-chiscanoi and S. lingua was mentioned by Wallenwein & Breier (1992) and was described subsequently as S. × venhuisia by Vázquez
(2009). However, the photo in Wallenwein & Breier
(1992), is clearly of S. lingua; Vázquez did not provide
any photographs. Furthermore, Venhuis & al. (2004)
and Vázquez (2009) suggested hybridization between
S. perez-chiscanoi and S. cordigera. This putative hybrid was based on a plant near Aljucén (Venhuis & al.,
2004), from the same population as the photographs
presented in this paper (Fig. 4a, b). The inflorescences
of these very rare individuals contained salmon-pink
and pink flowers, and it is noteworthy that flower
colour varied within single plants. However, morphological measurements on the flowers of these ‘hybrid’
individuals revealed floral dimensions identical to
S. perez-chiscanoi, and since the other putative parent,
S. cordigera, did not occur in the vicinity, and no morphological character of any other Serapias species was
present, we now conclude that these plants probably
represent a pink-flowered form of S. perez-chiscanoi
rather than a hybrid.
53
Related species
In the south-western part of the Iberian Peninsula
about seven taxa of Serapias occur, which can be divided into two main groups based on their flower size: the
S. vomeracea group and the S. parviflora group (Venhuis & al., 2007). In this region, the S. vomeracea group
includes S. cordigera subsp. cordigera, S. cordigera
subsp. gentilii, S. perez-chiscanoi and S. occidentalis
C. Venhuis & P. Venhuis. The occurrence of S. vomeracea subsp. vomeracea in SW Spain and Portugal is uncertain (Venhuis & al., 2007), and the taxonomic status
of the new species, S. maria F.M. Váquez (Váquez,
2008), needs further study since the dimensions of
morphological characters of this species overlap to a
large extent with those of S. occidentalis. Further research on these taxa is necessary to determine their occurrence and taxonomic status respectively.
Taxa belonging to the S. parviflora group are
S. parviflora, S. strictiflora Welwitsch ex Vega and
S. lingua. Furthermore, two varieties of S. strictiflora
are found in our region: var. elsae (P. Delforge)
C. Venhuis & P. Venhuis, and var. distenta Presser. In
the field, S. perez-chiscanoi is easy to distinguish from
most other co-occurring Serapias taxa on the basis of
flower colour or floral dimensions. However, some
taxa that occasionally have pale flowers, such as
S. cordigera subsp. gentilii and S. parviflora, resemble
S. perez-chiscanoi, and the differences between such
individuals and S. perez-chiscanoi are clarified below.
Differences with S. cordigera subsp. cordigera
Serapias cordigera subsp. cordigera is presumed to
be the parental species of S. perez-chiscanoi, and both
taxa are similar morphologically (Venhuis & al.,
2007) and closely related according to molecular studies (Bellusci & al., 2008). Nevertheless, S. cordigera
subsp. cordigera, with its dark red to purple flowers
with a large, heart-shaped epichile (Fig. 4c, d) is easily
distinguished in the field from S. perez-chiscanoi. It
can also be distinguished on the basis of three other
features: 1) epichile position, 2) emergence of the
lateral lobes and 3) inflorescence architecture. The
epichile of S. cordigera subsp. cordigera is normally positioned parallel to the stem (i.e., pointing downwards), whereas the epichile of S. perez-chiscanoi is
generally positioned at an angle of about 45-90 degrees to the stem (pointing more or less outwards). In
S. cordigera subsp. cordigera, the lateral lobes protrude
from the casco, whereas in S. perez-chiscanoi the lateral lobes remain hidden inside the hood. The flowers in S. cordigera subsp. cordigera are placed more or
less opposite each other, whilst those of S. perezchiscanoi are positioned close together and in a spi-
54
a
b
c
d
Fig. 4. a, Serapias perez-chiscanoi, Aljucén, Extremadura, Spain, 28-IV-2010; b, S. perez-chiscanoi, Aljucén, Extremadura, Spain,
28-IV-2010; c, S. cordigera subsp. cordigera, Badajoz, Extremadura, Spain, 30-IV-2010; d, S. cordigera subsp. cordigera, Badajoz, Extremadura, Spain, 30-IV-2010. All photographs: C. Venhuis.
a
b
c
d
55
Fig. 5. a, Serapias cordigera subsp. gentilii, Barranco do Velho, Algarve, Portugal, 13-IV-1995; b, S. cordigera subsp. gentilii, Galaxos,
Algarve, Portugal, 27-IV-2010; c, S. cordigera subsp. gentilii, Barranco do Velho, Algarve, Portugal, 26-IV-2010; d, S. cordigera subsp.
gentilii, Barranco do Velho, Algarve, Portugal, 17-IV-1995. Photographs: a, d, D. Tyteca; b, c, C. Venhuis.
56
a
b
Fig. 6. a, Serapias parviflora, Aldeia dos Palheiros, Baixo Alentejo, Portugal, 23-IV-2007; b, S. parviflora, Aldeia dos Palheiros, Baixo
Alentejo, Portugal, 23-IV-2007. Photographs: C. Venhuis.
ral, which gives the inflorescence a “twisted” appearance.
Although there is a small overlap in the epichile dimensions between S. cordigera subsp. cordigera and
S. perez-chiscanoi: length (18)23-30(36) mm and
(14)16-18(21) mm respectively, and width (13)1724(29) mm and (10)12-13(15) mm respectively, S. cordigera subsp. cordigera can be distinguished from S.
perez-chiscanoi on the basis of the non-overlapping
hypochile dimensions: length (10)11-14(17) mm and
(6)7-8(9) mm respectively, and width (18)21-27(31)
mm and (14)16-18(19) mm respectively (Fig. 7).
Differences with S. cordigera subsp. gentili
Serapias cordigera subsp. gentilii (Fig. 5a-d) is sometimes difficult to differentiate from S. perez-chiscanoi
because it occasionally has pale flowers that resemble
the latter species. Most flowers of S. cordigera subsp.
gentilii are red, but in many populations some plants
with pale flowers occur, which vary from red with
white edges (resembling S. nurrica Corrias), or completely pink, pink with yellow and pink with reddish
veins, to yellowish, greenish or whitish (resembling S.
perez-chiscanoi). In addition, several features that are
present in S. cordigera subsp. cordigera are absent in S.
cordigera subsp. gentilii and in S. perez-chiscanoi: the
position of the epichile in the latter taxa generally
points more or less outwards (although frequently
downwards), and the inflorescence is, when there are
many flowers, quite dense and spiralled and the edges
of the epichile are often curled upwards. Furthermore, S. cordigera subsp. gentilii, like S. perez-chiscanoi, seems to be autonomously self-pollinating
(Venhuis & al., 2007). It differs from S. perez-chiscanoi, however, by lateral lobes that generally emerge
from the hood in contrast to S. perez-chiscanoi in
which the lateral lobes are always completely hidden
inside it. Although the flowers of S. cordigera subsp.
gentilii generally have a colour pattern quite different
from S. perez-chiscanoi, some individuals have flowers
with a greenish epichile that may superficially look
similar. But in comparison with the “green” variation
of S. perez-chiscanoi, these flowers have a red hypochile, while in comparison with the “red” variation of
that taxon, they lack the reddish hairs on the labellum
57
Fig. 7. Boxplots of Serapias cordigera subsp. gentilii, S. cordigera subsp. cordigera, S. perez-chiscanoi from Extremadura and S.perezchiscanoi from Portugal (Ereiras). Outliers and extremes were not removed. a, epichile width; b, epichile length; c, hypochile width;
d, hypochile length.
58
and the red venation on all plant parts. The red-flowered S. perez-chiscanoi, which until now was known
from only one locality, is also very similar to the flowers of some plants of S. cordigera subsp. gentilii but
differs from the latter subspecies by a striking red venation on all plant parts.
Most floral features are unhelpful to distinguish between these taxa, and the only character that separates
S. cordigera subsp. gentilii from S. perez-chiscanoi
is the length of the hypochile, which in S. cordigera
subsp. gentilii is (9)11-12(13) mm, and in S. perezchiscanoi is (6)7-8(9) mm (Fig. 7). All floral dimensions as well as the flower colour of S. cordigera subsp.
gentilii are more or less intermediate between S. cordigera subsp. cordigera and S. perez-chiscanoi.
Differences to S. parviflora
Serapias parviflora is generally easily distinguished
from S. perez-chiscanoi by its very small flowers. In the
studied area, specimens of S. parviflora with pale pink
and yellowish/greenish flowers (Figs. 6a, b) frequently occur, but these resemble S. perez-chiscanoi in
colour only. Both taxa can be readily distinguished on
the basis of three of the four labellum dimensions:
Epichile length in S. parviflora ranges from (7)9-
11(12) mm and in S. perez-chiscanoi from (14)1618(21) mm, the epichile width in S. parviflora falls between (2)4-6(6) mm and in S. perez-chiscanoi between
(10)12-13(15) mm. Furthermore, S. parviflora differs
from S. perez-chiscanoi in hypochile width (8)1011(13) mm and (14)16-18(19) mm respectively. Hypochile length does not differ: (5)7-8(9) mm and (6)78(9) mm, respectively.
Distribution
Serapias perez-chiscanoi is a rare tongue-orchid,
which was previously only known from the Guadiana
river basin in Extremadura (Spain) (Pérez Chiscano,
1988; Pérez Chiscano & al., 1991; Delforge, 2002).
After a field study, Venhuis & al. (2004) reported six
new populations, and after intensive searches during
the last five years by, amongst others, employees of the
regional government of Extremadura, several new
populations were found along the river basin of the
Tajo and also south of the Guadiana river basin in Extremadura (Venhuis & al., 2006), which increases the
total number of populations known in Extremadura
to around 30 (Fig. 8). Yet another population was
found in Castilla-La Mancha (Venhuis & al., 2006).
In the Algarve (Portugal), Jansen (1993) found a population that disappeared soon after its discovery. And
we have seen a population in the Baixo Alentejo
province that was discovered by M. Pereira, and also
four other populations that were discovered by either
J. Moura, J. Pessoa and J. Monteiro, in the provinces
of Beira Litoral and Ribatejo in the central part of
Portugal and in the province of Trás-os-Montes e Alto
Douro in northern Portugal (Fig. 8).
Serapias cordigera subsp. cordigera is found throughout the Iberian Peninsula, sometimes only locally but
often abundantly. Serapias parviflora also occurs in the
entire Iberian Peninsula, but is much more widespread and often abundant. Serapias cordigera subsp.
gentilii is found predominantly along the coastal regions of the Algarve but also extends further north.
The distribution map (Fig. 8) is based on populations
seen by us, and photos, and also on literature, in which
it was cited as a variety of S. cordigera.
Identification key
Fig. 8. Distribution map of Serapias perez-chiscanoi and S. cordigera subsp. gentilii. All known populations are presented, including populations that have already disappeared ( S. perezchiscanoi; S. cordigera subsp. gentilii).
Here, we present a concise key for the identification of species from the large flowered S. vomeracea
group in the SW Iberian Peninsula. It will be clear
from this article that the identification of the different
species is not too difficult, despite the considerable
variation in flower morphology, flower colours and
venation patterns. More research on the relationships
between the morphological variation and the pollination ecology in S. perez-chiscanoi is underway.
IDENTIFICATION KEY FOR THE SERAPIAS VOMERACEA GROUP
IN THE SOUTHWESTERN PART OF THE IBERIAN PENINSULA
1. Ratio epichile width/hypochile length = 0.6-1.2 ...................
................................................................... S. occidentalis
1. Ratio epichile width/hypochile length = 1.3-2.1 ................ 2
2. Hypochile length (6)7-8(9) mm ............. S. perez-chiscanoi
2. Hypochile length (9)10-14(17) mm ................................... 3
3. Epichile broad and heart-shaped, purple, with no divergent
edges; pollinia coherent ...... S. cordigera subsp. cordigera
3. Epichile slender, usually pale, often with divergent edges;
pollinia friable ......................... S. cordigera subsp. gentilii
Acknowledgements
We thank Marizia Pereira, Daniel Tyteca, Joaquim Pessoa,
Jorge Moura and Karel Kreutz for their kind help with providing
localities and/or photos of the studied species. Marisela Cornado
Garcia is kindly acknowledged for translating the summary into
Spanish.
References
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Jardin Botánico de Madrid 47(2): 510.
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Bernardos, S., Tyteca, D. & Amich, F. 2004. Cytotaxonomic study
of some taxa of the subtribe Orchidinae (Orchidoideae, Orchidaceae) from the Iberian Peninsula. Israel Journal of Plant
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Delforge P. 2002. Guía de las Orquídeas de España y Europa. Lynx
Ediciones, Barcelona, Spain.
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D’Emerico, S., Pignone, D. & Scrugli, A. 2000. Giemsa C-banded
karyotypes in Serapias L. (Orchidaceae). Botanical Journal of
the Linnean Society 133: 485-492.
Jansen H. 1993. Serapias viridis Pérez Chiscano in Portugal! Mitteilungsblatts des Arbeitskreises Heimische Orchideen BadenWürttemberg 10: 50-53.
Pérez Chiscano, J.L. 1988. Nueva especie de Serapias L. en Extremadura (España). Monografias del Instituto Pirenaico de Ecologia, Homenaje a Pedro Montserrat, Jaca y Huesca: 305-309.
Pérez Chiscano, J.L., J.R. Gil Llano & F. Duran Oliva. 1991. Orquídeas de Extremadura. Fonda Natural, Madrid.
Tyteca, D. 1997. The orchid flora of Portugal. Journal Europäischer
Orchideen 29(2/3): 185-581.
Vázquez Pardo, F.M. 2008. Annotations to the Orchidaceae of Extremadura (SW Spain). Journal Europäischer Orchideen 40(4):
699-725.
Vázquez Pardo, F.M. 2009. Revisión de la familia Orchidaceae en
Extremadura (España). Folia Botanica Extremadurensis 3: 5-368
Vellozo, J.M. da C. 1825. Florae fluminensis. Senefelder, Rio de Janeiro, Brasil.
Venhuis, C., Oostermeijer, J.G.B. & Tonk, J.Th.P. 2004. Conservation biology of Serapias perez-chiscanoi Acedo in the Guadiana river basin in Extremadura (Spain). Eurorchis 16: 49-63.
Venhuis, C., Oostermeijer, J.G.B. & Cornado Garcia, M. 2006. Serapias perez-chiscanoi: legal protection and distribution. Eurorchis 18: 88-91.
Venhuis, C., Venhuis, P., Oostermeijer, J.G.B. & van Tienderen,
P.H. 2007. Morphological systematics of Serapias L. (Orchidaceae) in Southwest Europe. Plant Systematics and Evolution
265: 165-177.
Wallenwein, F. & Breier, W. 1992. Bemerkungen zu einigen Arten
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115-121.
Associate Editor: L. Sáez
Received: 27-IX-2010
Accepted: 7-II-2011
2266_Myxomycetes:Anales 68(1).qxd 13/06/2011 12:12 Página 61
Vol. 68(1): 61-95
enero-julio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2266
Biodiversity of Myxomycetes from the Monte Desert
of Argentina
by
C. Lado1, D. Wrigley de Basanta1 & A. Estrada-Torres2
Real Jardín Botánico, CSIC, Plaza de Murillo 2, E-28014 Madrid, Spain. [email protected]
Centro de Investigación en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, km 10.5 carretera Texmelucan-Tlaxcala,
Ixtacuixtla, 90122, Tlaxcala, México. [email protected]
1
2
Abstract
Abstract
Lado, C., Wrigley de Basanta, D. & Estrada-Torres, A. 2011. Biodiversity of Myxomycetes from the Monte Desert of Argentina.
Anales Jard. Bot. Madrid 68(1): 61-95
A biodiversity survey for myxomycetes was carried out in the
Monte Desert (Argentina) and surrounding areas in November
2006 and late February and March 2007. Specimens were collected in seven different provinces (Catamarca, Jujuy, La Rioja,
Salta, San Juan, San Luis and Tucumán), between 23º and 33º S
latitude, and a total of 105 localities were sampled. Cacti and
succulent plants were the most common type of substrate investigated, but shrubs and herbs characteristic of this biome
were also included in the survey. Almost six hundred specimens
of myxomycetes from 72 different species in 22 genera were collected either in the field, or from moist chamber cultures prepared with samples of plant material obtained from the same collecting sites. The results include 1 species new to science, Macbrideola andina three more species recently described based on
material from this survey, 5 species cited for the first time for the
Neotropics, 11 new records for South America and 38 new records for Argentina. Taxonomic comments on rare or unusual
species are included and illustrated with photographs by LM and
SEM. Data are presented on the development of some species
and microenvironmental factors are discussed. An analysis of
the biodiversity of myxomycetes in this area, and a comparison
with other desert areas, are included.
Lado, C., Wrigley de Basanta, D. & Estrada-Torres, A. 2011. Biodiversidad de Myxomycetes en el Desierto de Monte (Argentina). Anales Jard. Bot. Madrid 68(1): 61-95 (en inglés).
Con el objetivo de estudiar la biodiversidad de Myxomycetes en
el Desierto de Monte (Argentina) y áreas circundantes, se realizó
un muestreo en los meses de noviembre de 2006 y febrero y marzo de 2007. Se recolectaron especímenes en un total de 105 localidades pertenecientes a siete provincias (Catamarca, Jujuy, La
Rioja, Salta, San Juan, San Luis y Tucumán), situadas entre los paralelos 23º y 33º de latitud sur. Los cactus y plantas suculentas
fueron los tipos de sustratos más estudiados, pero también se
analizaron arbustos y plantas herbáceas características de este
bioma. Casi 600 especímenes de mixomicetes pertenecientes a
72 especies y 22 géneros fueron recolectados en el campo o se
obtuvieron en el laboratorio, por cultivo en cámara húmeda, a
partir de plantas procedentes de las mismas localidades. Los resultados incluyen una nueva especie, Macbrideola andina, otras
tres recientemente descritas y basadas en material de este estudio, 5 especies que se citan por primera vez para el Neotrópico,
11 nuevos registros para América del Sur y 38 nuevos registros
para Argentina. Se añaden comentarios taxonómicos e ilustraciones fotográficas, tanto con microscopía óptica como electrónica,
de aquellas especies raras o poco comunes. Se discuten nuevos
datos sobre el desarrollo de algunas especies y cómo influyen determinados factores microambientales. También se incluye un
análisis de la biodiversidad de mixomicetes en esta zona árida y se
compara con la obtenida en otros desiertos de América.
Keywords: Amoebozoa, arid environments, Neotropics, Protista, SEM, slime mould, taxonomy.
Palabras clave: Amoebozoa, hongos mucilaginosos plasmodiales, MEB, Neotrópico, Protista, taxonomía, zonas áridas.
Introduction
free-living amoebae, and the social amoebae (dictyostelids), in a protists-like group called the Amoebozoa
(Adl & al., 2005; Baldauf, 2008). They live in almost
all terrestrial ecosystems and are particularly abundant in temperate and tropical forests (Ing, 1994; Rojas & Stephenson, 2008; Kosheleva & al., 2008), but
The myxomycetes are a group of holotrophic eukaryotic organisms of worldwide distribution that for
many years have been regarded as related to fungi, but
are now included, together with several groups of
62
C. Lado & al.
many species are also known to be present in warm
dryland ecosystems (Evenson, 1961; Blackwell & Gilbertson, 1980; Novozhilov & al., 2003; Lado & al.,
2007a; Estrada-Torres & al., 2009; Ndiritu & al.,
2009). Most of the literature describes studies of deserts from North America, and has indicated that a
special myxobiota, adapted to arid conditions, and
much more numerous and varied than previously
imagined, may develop in these environments (Lado
& al., 1999; Estrada-Torres & al., 2009). To see if the
patterns of distribution continue into South America,
and to further investigate the relationships that exist
between myxomycetes and the plants that live in these drylands, an intensive study was undertaken of a selected arid area of the Monte Desert. From a biogeographical point of view, the Monte Desert, with an
area of about 467,000 km2, forms part of the ecoregion of Neotropic deserts (Roig & al., 2009). The
Monte Desert, a subtropical to warm temperate desert and semidesert, is located entirely in Argentina. It
extends approximately from 23° to 42° South latitude
along the eastern border of the Andes, from close to
Bolivia curving down to the Atlantic coast at Peninsula Valdés. There are very few published studies of myxomycetes from this region of Argentina. Spegazzini
(1899) and Fries (1903) reported on the first data
from this area, and Digilio (1946, 1950), and Deschamps (1972, 1976) compiled catalogues including
some data from Catamarca, Jujuy, Salta and Tucumán,
but few of these were from the Monte Desert. This information forms part of the catalogue of the country
published by Crespo & Lugo (2003). In addition, a
biodiversity inventory of myxomycetes, from the Chilean Atacama desert, that runs parallel to the northern
part of the Monte Desert, on the other side (West) of
the Andes, was completed by Lado & al. (2007a).
Study area
The area studied included the northern and central
parts of the Monte Desert in Northwest Argentina,
and the bordering transition zones of prepuna and
puna in the provinces of Jujuy, Salta, Catamarca, Tucumán, La Rioja, San Juan and San Luis (Fig. 1). The
elevation gradient was from 500 m to 4500 m, from
the valleys and endorheic basins to the pre-Andean
and Andean mountains. The soils of the Monte Desert are very poor, sandy or rocky, with very little humus. The climate of the area is semiarid to arid, with
a mean annual rainfall between 50 and 450 mm, being
among the most arid areas of Argentina, and the
mean annual temperature is between 10 and 18 °C.
The area is in the rain shadow of the Andes, and rapid
evaporation, increased even more by windy condi-
tions in the South, also contributes to the aridity of
the region (Abraham & al., 2009). The vegetation of
the Monte (Figs. 2-9) is composed of shrub steppes
dominated by Larrea spp., spiny shrubs such as Chuquiraga spp., and including several tree species of Prosopis (Roig & al., 2009). In addition, several kinds of
cacti of the genera Denmoza, Maihueniopsis, Cereus,
Echinopsis, Opuntia, Tephrocactus and Trichocereus
are present in the area or among the bordering vegetation types at higher altitudes, where the grasslands
of the puna (species of Festuca, Poa and Stipa) also
formed part of the present study. In the basins extensive salt flats form, due to the constant evaporation
caused by intense solar radiation and the lack of precipitation, and in those areas typical halophytic vegetation is found.
Sampling was carried out in 105 localities (Table 1)
in two expeditions during November to December
2006 and February to March 2007 to coincide with
the austral Spring and the end of the summer of the
same phenological year. At each locality, the microhabitats in which myxomycetes are known or suspected
to occur were examined carefully. All localities were
geo-referenced with a portable GPS unit (Magellan
eXplorist 600 5.1, Datum WGS84). Samples were collected in the field and substrate samples were also removed for moist chamber culture. Methods used for
collecting myxomycetes in the field and substrates
for laboratory culture can be found in Stephenson
(1989), Rossman & al. (1998). The field work was
done by the three authors and approximately one
hour was spent in each collecting locality.
Moist chamber cultures were prepared using sterile disposable plastic Petri dishes (9 cm diameter), in
the manner described by Wrigley de Basanta & al.
(2009). The pH of each culture was determined with
a portable pH meter after 24 hours, and then excess
water in each dish was poured off. Cultures were
maintained at room temperature (21-25 ºC) in diffuse
daylight and examined at regular intervals with a dissecting microscope for a period of three months. As
the myxomycetes matured, the portion of the substrate upon which they occurred was removed from the
moist chamber culture, allowed to dry slowly in a closed empty petri dish and then glued in a small cardboard box. All sporophores of a given species that developed in the same culture, were considered to represent a single record.
All specimens are deposited in the MA-Fungi herbarium (sub Lado) with duplicates in TLXM herbarium (sub aet), or in the private collection of Wrigley
Anales del Jardín Botánico de Madrid 68(1): 61-95, enero-julio 2011. ISSN: 0211-1322. doi: 10.3989/ajbm. 2266
Biodiversity of Myxomycetes
63
Fig. 1. Map of Argentina showing the collecting localities (numbers).
de Basanta (dwb). Differential interference contrast
(DIC) microscopy was used to obtain descriptive
data. The light photomicrographs were made using a
Nikon AZ100 microscope and combining sequential
images. Specimens were examined and photographed
at 10-15 kV, with a Hitachi S-3000N scanning electron microscope (SEM), in the Real Jardín Botánico,
CSIC. For all SEM-photographs the critical point
dried material technique was employed. Colour
notations in parenthesis are from the ISCC-NBS Color Name Charts Illustrated with Centroid Colors
(Anonymous, 1976).
Taxonomic diversity was examined using the mean
number of species per genus (S/G),which has been
64
C. Lado & al.
Figs. 2-9. Some characteristic plants of the Monte Desert and sourrounding areas: 2, desert scrub with Larrea spp. (jarillas). 3, Trichocereus sp. and the rosette-leaved plant Puya sp. 4, cardonal of Trichocereus pasacana and Opuntia sp. 5, Prosopis sp. 6, Xerophyllous
scrubland with “retamo” (Bulnesia retama) at El Leoncito National Park. 7, Mahiueniopsis sp. 8, Grassland near to the saltflats in the
Andes. 9, Grassland of the puna (species of Festuca, Poa and/or Stipa).
Jujuy, Tumbaya, on route RN-52, Salinas Grandes
Salta, La Poma, Salinas Grandes, Cerro Negro,
on route RN-52, km 43
Jujuy, Susques, Angosto del Taire, on route RN-52
Jujuy, Susques, Paso de Jama, customs office, on route RN-52
ARG-06-12
ARG-06-13
ARG-06-14
ARG-06-15
Andean puna with Stipa sp. and salt flats
Andean puna with Stipa atacamensis
Salt flat with leguminous tree
Andean puna with Gramineae
Andean puna with Stipa sp. and cacti
Andean puna with Stipa sp.
Xerophyllous scrubland with Puya sp.
Desert scrub with Echinopsis atacamensis,
and Opuntia sp.
Desert scrub with Tephrocactus and Puya sp.
21 Nov. 2006
21 Nov. 2006
20 Nov. 2006
20 Nov. 2006
20 Nov. 2006
20 Nov. 2006
20 Nov. 2006
20 Nov. 2006
20 Nov. 2006
19 Nov. 2006
19 Nov. 2006
19 Nov. 2006
19 Nov. 2006
18 Nov. 2006
18 Nov. 2006
18 Nov. 2006
Date
23°14’14”S 67°01’45”W, 4102 m ± 4 m
23°25’05”S 66°29’54”W, 4001 m ± 8 m
23°25’28”S 66°10’38”W, 3513 m ± 6 m
23°35’10”S 65°53’58”W, 3425 m ± 8 m
23°42’22”S 65°40’20”W, 4147 m ± 7 m
23°41’39 , 65°38’58”W, 4149 m ± 9 m
Jujuy, Tumbaya, Abra de Potrerillos pass,
on route RN-52, East of Saladillas
23°52’12”S 65°27’50”W, 2112 m ± 8 m
ARG-06-11
Jujuy, Tumbaya, Volcán, Huajra
ARG-06-08
Pre-puna with Echinopsis atacamensis,
Opuntia sulphurea and leguminous trees
Pre-puna with leguminous plants,
Compositae and Oreocereus trollii
Desert scrub with Echinopsis atacamensis
and Opuntia sulphurea
Spiny scrubland with Echinopsis atacamensis,
Cereus uruguayensis and Trichocereus thelegonus
Spiny scrubland with Echinopsis atacamensis
and Cereus uruguayensis
Spiny scrubland with Acacia sp.
and Opuntia quimilo
Vegetation
23°21’33”S 65°20’42”W, 2780 m ± 11 m Desert scrub with Echinopsis atacamensis,
Opuntia sulphurea and leguminous trees
Jujuy, Tumbaya, Abra de Potrerillos pass,
on route RN-52, El Quemado
Jujuy, Humahuaca, 16 km South of Humahuaca,
on route RN-9, Chucalesna
ARG-06-07
23°06’28”S 65°22’26”W, 3218 m ± 6 m
ARG-06-10
Jujuy, Humahuaca, 12 km North of Humahuaca,
on route RN-9
ARG-06-06
23°02’03”S 65°22’50” W, 3419 m ± 7 m
23°40’08”S 65°34’33”W, 2972 m ± 6 m
Jujuy: Humahuaca, 20 km North of Humahuaca,
on route RN-9, 6 km from Hornaditas, by Sapaua stream
ARG-06-05
23°40’47”S 65°26’50” W, 2346 m ± 8 m
Jujuy, Tumbaya, Purmamarca, on route RN-52,
12 Km West of Purmamarca, Paso de Lipán
Jujuy: Tumbaya, North of Volcán, on route RN-9,
Cieneguillas
ARG-06-04
25°04’42”S 65°00’12”W, 818 m ± 8 m
ARG-06-09
Salta: General Güemes, Virgilio Tedín, on route RN-9,
Km 1515
ARG-06-03
26°01’24”S 65°07’53”W, 965 m ± 9 m
23°41’58”S 65°32’53”W, 2678 m ± 8 m
Salta: Candelaria, Rosario de la Frontera, on route RN-9,
km 1393
ARG-06-02
26°31’23”S 65°18’18”W, 751 m ± 7 m
Coordinates, elevation
ARG-06-08bis Jujuy, Tumbaya, Purmamarca, La Ciénaga,
on route RN-52
Tucumán: Trancas, Vipos, on route RN-9, km 1331
ARG-06-01
Locality
Table 1. List of collecting localities.
65
Jujuy, Susques, Paso de Jama, Salar de Jama, on route RN-52
Jujuy, Susques, southern end of the Salar de Jama,
on route RN-52
Jujuy, Susques, Archibarca, 68 Km Southwest of Susques,
on route RN-52
Jujuy, Susques, Salar de Olaroz, 43.6 km Southwest
of Susques, on route RN-52
Jujuy, Susques, 9 km East of Susques, on route RN-52
Jujuy, Susques, 20 km East of Susques,
on route RN-52, Quebrada Malpaso
Salta, La Poma, Río Negro, on route RP-75 to Cobres, km 24
Salta, Los Andes, San Antonio de los Cobres, La Polvorilla
viaduct, mine Concordia
Salta, La Poma, San Antonio de los Cobres, Abra Blanca,
129 km Northwest of Salta, on route RN-52
Salta, Rosario de Lerma, Tastil, 119 km Northwest of Salta,
on route RN-51, La Encrucijada
Salta, San Carlos, San Fernando de Escoipe, cemetery,
on route RP-33, km 33
Salta, Cachi, San Martín, Cuesta del Obispo,
Salta, Cachi, Los Cardones National Park, Tin Tin straight
Salta, Cachi, on route RN-40 from Payogasta to La Poma,
km 4513
Salta, Cachi, on route RN-40 from Payogasta to La Poma,
km 4539, Pueblo Viejo, 2 km North of Rodeo
ARG-06-16
ARG-06-17
ARG-06-18
ARG-06-19
ARG-06-20
ARG-06-21
ARG-06-22
ARG-06-23
ARG-06-24
ARG-06-25
ARG-06-26
ARG-06-27
ARG-06-28
ARG-06-29
ARG-06-30
Locality
Table 1. List of collecting localities. (Continuation).
24°50’58”S 66°09’12”W, 2703 m ± 6 m
25°02’32”S 66°05’28”W, 2490 m ± 6 m
25°12’08”S 66°58’27”W, 2911 m ± 5 m
25°10’27”S 65°49’31”W, 2744 m ± 13 m
25°09’54”S 65°44’07”W, 1900 m ± 8 m
24°21’06”S 66°04’18”W, 3559 m ± 5 m
24°19’30”S 66°07’02”W, 4001 m ± 7 m
24°12’21”S 66°24’05”W, 4160 m ± 6 m
24 Nov. 2006
23 Nov. 2006
23 Nov. 2006
23 Nov. 2006
22 Nov. 2006
22 Nov. 2006
22 Nov. 2006
22 Nov. 2006
22 Nov. 2006
21 Nov. 2006
21 Nov. 2006
21 Nov. 2006
21 Nov. 2006
21 Nov. 2006
Date
Spiny scrubland with Echinopsis atacamensis and cacti 24 Nov. 2006
Cultivated area with Prosopis sp.
Desert scrub with Echinopsis atacamensis and bushes
Dry gully with bushes (Compositae, Solanaceae
and Sambucus sp.) and grasses
Spiny scrubland with Puya sp., leguminous plants
and Cereus uruguayensis
Andean puna with Cumulopuntia sp. and grasses
Spiny scrubland with Cumulopuntia sp.
and Compositae
Andean puna with Prosopis sp., bushes and grasses
Scrubland with Cumulopuntia sp.
Borders of a stream with Cortaderia sp. and bushes
High elevation wetland with Stipa sp.
High elevation wetland with Stipa sp.
Vegetation
66
23°36’43”S 66°13’55”W, 3442 m ± 5 m
23°25’51”S 66°16’01”W, 3723 ± 7 m
23°26’39”S 66°19’00”W, 3760 ± 9 m
23°33’29”S 66°39’36”W, 3931 m ± 5 m
23°37’19”S 66°51’18”W, 4043 m ± 8 m
23°24’38”S 66°57’08”W, 4117 m ± 8 m
23°15’15”S 67°00’27”W, 4100 m ± 7 m
C. Lado & al.
Salta, Cachi, Buena Vista, Potrero river, on route RN-40, km 4519
Salta, Cachi, Los Cardones National Park, Tin Tin straight,
2 km up an unmarked path
Salta, Cachi, Los Cardones National Park, Tin Tin straight,
up a path to a copse
Salta, Cachi, Los Cardones National Park,
Salta, Cachi, Los Cardones National Park, on route RP-42, km 5
Salta, Cachi, El Algarrobal
Salta, Molinos, on route RN-40, km 4472
Salta, Molinos, Seclantás, on route RN-40, km 4467
Salta, Molinos, Molinos river, on route RN-40, km 4458
Salta, Molinos, Angostura, on route RN-40, km 4445
Salta, San Carlos, Corte la Flecha, on route RN-40, km 4406
Salta, San Carlos, Los Sauces, on route RN-40, km 4380
Salta, Cafayate, on route RN-40, km 4332
Tucumán, Tafí del Valle, Quilmes, Quilmes
archeaological ruins
Catamarca, Santa María, Punta de Balasto,
Catamarca, Santa María, Guanaco Yacu,
on oute RN-40, km 4206
Catamarca, Santa María, Guanaco Yacu,
ARG-06-31
ARG-06-32
ARG-06-33
ARG-06-34
ARG-06-35
ARG-06-36
ARG-06-37
ARG-06-38
ARG-06-39
ARG-06-40
ARG-06-41
ARG-06-42
ARG-06-43
ARG-06-44
ARG-06-45
ARG-06-46
ARG-06-47
Locality
26°59’56”S 66°15’13”W, 219 1m ± 7 m
27°00’09”S 66°14’00”W, 2188 m ± 8 m
26°56’46”S 66°07’51”W, 2132 m ± 6 m
26°28’06”S 66°01’56” W, 1849 m ± 6 m
26°08’40”S 65°57’30”W, 1640 m ± 9 m
25°47’06”S 65°58’04”W, 1861 m ± 13 m
25°42’29”S 66°07’17”W, 1951 m ± 8 m
25°29’29”S 66°14’10”W, 1986 m ± 7 m
25°25’56”S 66°17’11”W, 2059 m ± 10 m
25°21’47”S 66°16’52”W, 2238 m ± 6 m
25°18’49”S 66°14’50”W, 2135 m ± 6 m
25°05’22”S 66°04’57”W, 2684 m ± 9 m
25°15’06”S 66°06’30”W, 2660 m ± 8 m
25°12’47”S 66°01’06”W, 2805 m ± 5 m
25°11’22”S 65°59’29”W, 2880 m ± 7 m
25°10’13”S 66°00’11”W, 2907 m ± 6 m
25°00’13”S 66°06’03”W, 2504 m ± 6 m
Spiny scrubland on sand dunes with grasses
and succulent-leaved bushes
Spiny scrubland on sand dunes with grasses
and succulent-leaved bushes
Spiny scrubland on sand with Prosopis sp.
Desert scrub with Trichocereus sp., Echinopsis sp.
and leguminous plants
Desert scrub with Puya sp. in a rocky area
Cultivated land with Prosopis sp.
Spiny scrubland
Spiny scrubland with Gymnocalycium sp.,
Austrocylindropuntia sp. and Denmoza sp.
Prosopis sp. woodland
Spiny scrubland with Puya sp.
Spiny scrubland with Opuntia sulphurea
Desert scrub with Echinopsis atacamensis and a
copse of Prosopis alba and Prosopis nigra
Desert scrub with Echinopsis atacamensis,
Cortaderia sp. and Asteraceae
Desert scrub with Echinopsis atacamensis and
leguminous plants
Desert scrub with Echinopsis atacamensis and bushes
Scrubland along a dry stream
Vegetation
26 Nov. 2006
26 Nov. 2006
26 Nov. 2006
26 Nov. 2006
25 Nov. 2006
25 Nov. 2006
25 Nov. 2006
25 Nov. 2006
25 Nov. 2006
25 Nov. 2006
25 Nov. 2006
24 Nov. 2006
24 Nov. 2006
24 Nov. 2006
24 Nov. 2006
24 Nov. 2006
24 Nov. 2006
Date
67
Catamarca, Santa María, Sierra del Hombre Muerto,
Catamarca, Belén, Hualfin, Los Nacimientos,
Catamarca, Belén, on route RN-40 from Belén to Hualfin,
4 km South of Hualfin
Catamarca, Belén, 7 km North of Belén, on route RN-40,
Reserva Natural Morro de los Cóndores
Catamarca, Balén, Londres, up a track 5 km West
from route RP-3 to Tinogasta, La Aguada
Catamarca, Tinogasta, Andaluca,
Catamarca, Belén, Hualfin, Los Nacimientos,
Catamarca, Tinogasta, Fiambalá, on route RN-60,
59 km Southeast of San Francisco pass, Las Losas
34 km Easth of San Francisco pass, Las Peladas
35 km Easth of San Francisco pass, Las Peladas
Catamarca, Tinogasta, Fiambalá, Valle de Chaschuil, on
route RN-60 to San Francisco pass, 50 km West of Fiambalá
Catamarca, Tinogasta, Fiambalá, Valle de Chaschuil,
on route RN- 60 to San Francisco pass, Cañón de Angosturas
Catamarca, Tinogasta, on route RN-60, km 1317,
10 km South of La Puntilla
Catamarca, Tinogasta, Costa de Reyes, on route RP-3
ARG-06-48
ARG-06-49
ARG-06-50
ARG-06-51
ARG-06-52
ARG-06-53
ARG-06-54
ARG-06-55
ARG-06-56
ARG-06-57
ARG-06-58
ARG-06-59
ARG-06-60
ARG-06-61
Locality
28°16’18”S 67°38’51”W, 1437 m ± 7 m
28°06’13”S 67°30’52”W, 1184 m ± 8 m
27°42’16”S 67°56’47”W, 2644 m ± 11 m
27°47’09”S 68°04’55”W, 3085 m ± 10 m
27°01’45”S 68°04’00”W, 3928 m ± 8 m
26°55’33”S 68°04’49”W, 4141 m ± 5 m
27°12’28”S 68°06’25”W, 3764 m ± 7 m
27°12’36”S 66°47’20”W, 1938 m ± 7 m
Desert scrub with rosette-leaved succulent plants .
(Puya sp.), Opuntia sp. and Prosopis sp.
Desert scrub with Puya sp.
Rocky outcrop with Opuntia sp., Parodia sp. .
and Cumulopuntia sp
Scrub with halophytes, bushes, Parodia sp.
and Cumulopuntia sp.
Andean puna with Stipa sp.
Andean puna
Pre-puna with Cumulopuntia sp.
Spiny scrubland with Gymnocalycium sp.,
Prosopis sp. and Cercidium sp.
Spiny scrubland on sand dunes with Leguminosae
and opuntioid cacti
Thorn forest with Leguminosae (Brea sp.)
Desert scrub with Puya sp., and grasses
Desert scrub with Puya sp., and cacti (Trichocereus sp.)
Source of a spring with herbaceous plants
and grasses (Cortaderia sp.)
Scrubland with Asteraceae
Vegetation
29 Nov. 2006
29 Nov. 2006
28 Nov. 2006
28 Nov. 2006
28 Nov. 2006
28 Nov. 2006
28 Nov. 2006
26 Nov. 2006
27 Nov. 2006
27 Nov. 2006
27 Nov. 2006
27 Nov. 2006
26 Nov. 2006
26 Nov. 2006
Date
68
28°18’37”S 67°17’36”W, 1035 m ± 9 m
27°45’09”S 67°12’26”W, 1328 m ± 6 m
27°34’13”S 67°00’10”W, 1308 m ± 16 m
27°36’55”S 67°01’06”W, 1305 m ± 6 m
27°10’02”S 66°44’14”W, 2049 m ± 7 m
27°05’14”S 66°37’01”W, 2305 m ± 5 m
C. Lado & al.
La Rioja, Arauco, Aimogasta, Villa Mazán, on route RN-60
Catamarca, Capayán, 7 km West of Chumbicha,
on route RN-60
ARG-06-75
ARG-06-76
La Rioja, Capital, La Rioja, Los Padercitos,
5ARG-06-70
La Rioja, Arauco, Aimogasta, 2 km South of Aimogasta,
on route RN-75
San Juan, Valle Fértil, El Agua de Arriba,
ARG-06-69
ARG-06-74
San Juan, Valle Fértil, Ischigualasto Provincial Park,
on route RP-510 to the Park, km 104
ARG-06-68
La Rioja, Castro Barros, Pinchas, on route RN-75
La Rioja, Independencia, Talampaya National Park,
ARG-06-67
ARG-06-73
La Rioja, General F. Varela, Villa Unión,
Talampaya National Park, on route RP-26, km 143
ARG-06-66
La Rioja, Sanagasta, 3 km West of Sanagasta, on route RN-75
La Rioja, General F. Varela, Villa Unión, Pagancillo,
ARG-06-65
ARG-06-72
La Rioja, Vinchina, Famatina, El Potrerillo,
ARG-06-64
La Rioja, Sanagasta, Dique Los Sauces,
La Rioja, Vinchina, Campanas, on route RP-11, km 51
ARG-06-63
ARG-06-71
Catamarca, Tinogasta, Costa de Reyes,
34 km South of Tinogasta, on route RP-3
ARG-06-62
Locality
28°51’42”S 66°23’58”W, 582 m ± 8 m
28°39’02”S 66°33’05”W, 950 m ± 10 m
28°34’37”S 66°49’10”W, 906 m ± 5 m
28°55’46”S 66°57’32”W, 1370 m ± 9 m
29°20’27”S 67°00’25”W, 914 m ± 10 m
29°22’41”S 66°58’58”W, 858 m ± 8 m
29°24’20”S 66°56’35”W, 681 m ± 9 m
30°07’54”S 67°03’27”W, 599 m ± 7 m
30°10’44”S 67°48’56”W, 1374 m ± 12 m
30°07’42”S 67°44’19”W, 1378 m ± 8 m
29°49’03”S 67°59’06”W, 1229 m ± 9 m
29°34’00”S 68°05’17”W, 1162 m ± 8 m
28°59’00”S 67°30’51”W, 1390 m ± 7 m
28°36’32”S 67°38’25”W, 1777 m ± 10 m
28°23’12”S 67°39’44”W, 1647 m ± 5 m
Dry forest with Opuntia quimilo
Desert scrubland with Opuntia sp. and Trichocereus sp.
Disturbed zone with palm trees
Disturbed zone with lianas
Desert scrub with Prosopis sp. and Puya sp.
Desert scrub with rosette-leaved succulent
plants of Puya sp.
Spiny scrubland with Stetsonia coryne
Desert scrubland
Desert scrub with Puya sp., Opuntia sp.
and Trichocereus sp.
Desert scrub with Puya sp., Tunilla sp.
and Trichocereus sp.
Sand dunes
Cultivated area with Prosopis alba and Brea sp.
Desert scrub with Puya sp., Gymnocalycium sp. and
cultivated area with leguminous plants and lianas
Spiny scrubland
Spiny scrubland with Trichocereus sp. and other cacti
Vegetation
1 Dec. 2006
1 Dec. 2006
1 Dec. 2006
1 Dec. 2006
1 Dec. 2006
1 Dec. 2006
1 Dec. 2006
30 Nov. 2006
30 Nov. 2006
30 Nov. 2006
30 Nov. 2006
30 Nov. 2006
29 Nov. 2006
29 Nov. 2006
29 Nov. 2006
Date
69
San Juan, Calingasta, Barreal, El Leoncito National Park,
50 km South of Barreal, on route RP-412
San Juan, Calingasta, Barreal, El Leoncito National Park,
25 km South of Barreal, on route RP-412
San Juan, Calingasta, Villa Nueva,
on route RP-412 towards Tocota and Iglesia
San Juan, Iglesia, Rodeo, on route RN-150, km 380,
Paso del Agua Negra, Quebrada Sarmiento
San Juan, Iglesia, Rodeo, on route RN-150,
km 370, Los Corrales
San Juan, Iglesia, Rodeo, on route RN-150, km 366
San Juan, Iglesia, Rodeo, on route RN-150, km 350.5,
Ojo de Agua,17 km West of Arrequintín
San Luis, La Capital, on route RN-7, km 858, Alto Pencoso
San Luis, La Capital, San Luis,
on route RN-147, km 818, San Jerónimo
San Luis, Belgrano, San Antonio, on route RN-147, km 868
San Luis, Belgrano, Hualtarán,
Sierra de las Quijadas National Park, viewpoint
San Luis, Belgrano, Hualtarán, Sierra de las Quijadas
National Park, 2 km East of the viewpoint
San Luis, Belgrano, Hualtarán, Sierra de las Quijadas
National Park, 3 km East of the viewpoint
ARG-07-06
ARG-07-07
ARG-07-08
ARG-07-09
ARG-07-10
ARG-07-11
ARG-07-12
ARG-07-13
ARG-07-14
ARG-07-45
ARG-07-46
ARG-07-47
ARG-07-48
ARG-07-49
ARG-07-50
Locality
32º29’35”S 66º59’23”W, 777 ± 7 m
32º29’49”S 66º59’44”W, 780 ± 10 m
32º29’47”S 67º00’22”W, 805 ± 9 m
33º14’14”S 66º23’45”W, 663 ± 6 m
33º14’14”S 66º23’45”W, 663 ± 6 m
33º25’07”S 67º04’38”W, 512 ± 6 m
30º22’05”S 69º23’38”W, 2387 ± 5 m
30º23’12”S 69º31’11”W, 2730 ± 8 m
30º21’24”S 69º42’04”W, 3710 ± 10 m
Spiny scrubland with Echinopsis sp.
Spiny scrubland with Larrea spp.
and Prosopis flexuosa
Spiny scrubland
Spiny scrubland with Prosopis sp.
Xerophyllous scrubland
Andean puna
Andean puna
Andean puna
Vegetation
7 Mar. 2007
7 Mar. 2007
7 Mar. 2007
7 Mar. 2007
7 Mar. 2007
6 Mar. 2007
26 Feb. 2007
26 Feb. 2007
26 Feb. 2007
26 Feb. 2007
26 Feb. 2007
26 Feb. 2007
24 Feb. 2007
24 Feb. 2007
24 Feb. 2007
Date
70
30º16’04”S 69º47’43”W, 4100 ± 10 m
30º13’30”S 69º47’33”W, 4305 ± 10 m
30º13’36”S 69º48’26”W, 4615 ± 9 m
31º02’49”S 69º27’50”W, 1668 ± 5 m
31º51’23”S 69º26’03”W, 1867 ± 9 m
31º53’20”S 69º25’08”W, 1892 ± 7 m
C. Lado & al.
San Juan, Jáchal, Niquivil, on route RN-40,
km 3525, 20 km North of Talacasto
San Juan, Jáchal, Niquivil, on route RN-40, km 3572, Tucunuco 30º37’23”S 68º38’21”W, 909 ± 9 m
San Juan, Jáchal, San Roque, on route RN-40, km 3619
San Juan, Jáchal, San José de Jáchal, Dique Pachimoco,
San Juan, Ullum, on route RP-436, 79 km Northwest of the
ARG-07-54
ARG-07-55
ARG-07-56
ARG-07-57
ARG-07-58
30º41’41”S 69º01’19”W, 2105 ± 10 m
30º42’41”S 68º58’22”W, 1900 ± 6 m
30º50’58”S 68º57’01”W, 1660 ± 10 m
31º00’46”S 68º45’58”W, 1370 ± 10 m
San Juan, Ullum, on route RP-436, 72 km Northwest of
the crossroads with route RN-40 and 1 km
from the turn to La Invernada
San Juan, Ullum, on route RP-436, 66 km Northwest of
the crossroads with route RN-40, Minas de Gualilán
San Juan, Ullum, La Ciénaga, on route RP-436, 50 km
Northwest of the crossroads with route RN-40
San Juan, Ullum, Quebrada de Las Burras, on route RP-436,
18 km Northwest of the crossroads with route RN-40
31º01’41”S 68º45’44”W, 1333 ± 6 m
San Juan, Ullum, Termas de Talacasto, on route RP-436,
16.2 km Northwest of from the crossroads with route RN-40
ARG-07-60
ARG-07-61
ARG-07-62
ARG-07-63
30º38’47”S 69º03’56”W, 2445 ± 8 m
30º11’52”S 68º49’23”W, 1240 ± 7 m
30º21’03”S 68º38’07”W, 1054 ± 5 m
31º02’36”S 68º38’09”W, 990 ± 8 m
31º19’14”S 68º36’23”W, 1040 ± 10 m
ARG-07-59
crossroads with route RN-40 and 3 km from the turn
to Tocota
San Juan, Ullum, Matagusanos, on route RN-40, km 3491
ARG-07-53
31º23’07”S 68º35’41”W, 830 ± 10 m
San Juan, Albardón, on route RN-40, km 3483
ARG-07-52
31º45’02”S 68º01’56”W, 748 ± 5 m
San Juan, Caucete, Vallecito, Difunta Correa, Valle Fértil
Natural Park, Sierra Pie de Palo, on route RN-141, km 185
ARG-07-51
Locality
plants of Puya sp.
plants of Puya sp.
Spiny scrubland with Eriosyce sp.
Spiny scrubland with Tunilla corrugata
Spiny scrubland with Tephrocactus sp.
Spiny scrubland
Spiny scrubland
plants of Puya sp.
Spiny scrubland
Spiny scrubland
Spiny scrubland with Echinopsis sp.,
Opuntia sp. and Tephrocactus sp.
Spiny scrubland with Tephrocactus sp.,
Opuntia sp. and Puya sp.
Spiny scrubland with Tephrocactus sp.
Vegetation
9 Mar. 2007
9 Mar. 2007
9 Mar. 2007
9 Mar. 2007
9 Mar. 2007
9 Mar. 2007
8 Mar. 2007
8 Mar. 2007
8 Mar. 2007
8 Mar. 2007
8 Mar. 2007
8 Mar. 2007
7 Mar. 2007
Date
71
C. Lado & al.
72
used in other studies of myxomycetes (Stephenson &
al., 1993). To examine community similarity, the Sørensen coefficient of community (CC) index was
used, which considers the presence or absence of species in the study areas compared using the formula CC
= 2z / (x + y), where z = the number of species in common to both communities, and where x and y equal
the number of species in communities A and B, respectively. The completeness of the sampling effort
was evaluated using the ACE and CHAO1 abundance indices (Colwell & Coddington, 1994; Colwell &
al., 2004). Each collecting site was used as the unit of
collecting effort, using the total number of species
found with the programme EstimateS v 7.5.2
(http.://viceroy.eeb.uconn.edu/estimates).
Results
This survey produced a total of 594 collections of
myxomycetes, including 372 that had developed under natural conditions in the field, as well as 222 collections obtained from 127 moist chamber cultures.
The collections represent 72 different species from 22
genera of myxomycetes. The following list of species
includes one species new to science, three species recently described based on material from this survey,
5 more are new records for the Neotropics and a further 11 species previously unknown from South America. The survey has added a total of 38 species to the
catalogue of Argentina.
Annotated list of species
In the list that follows, all the myxomycetes observed are arranged alphabetically by genus and species. Information is provided on the source of each
record, first the locality from which the specimen itself or the sample of dead plant material used to prepare the moist chamber culture was collected (Table
1), followed by the substrate upon which it was collected or cultured, and the collection number. A collection obtained from a moist chamber culture is indicated by [mc] followed by the pH of the culture in
which the specimen appeared. Additional comments
are included for records of particular interest. Nomenclature follows Lado (2005-2010). The abbreviation ‘cf.’ in the name of a taxon indicates that the
specimen representing the source of the record
could not be identified with certainty. Unless otherwise indicated, the data on Neotropical distribution
of myxomycete species is from Lado & Wrigley de
Basanta (2008).
Arcyria afroalpina Rammeloo. (Figs. 10-21).
ARG-06-38: On Puya sp. leaves, MA-Fungi 80230, 80231; on
dead leaf base of Puya sp. (mc, pH 7), dwb 2831; (mc pH 7.1), dwb
2854. ARG-06-50: On Puya sp. leaves, MA-Fungi 80232; on dead
leaf bases of Puya sp (mc, pH 6.8), dwb 2979. ARG-06-60: On
dead leaf bases of Puya sp. (mc, pH 6.9), dwb 2853. ARG-06-61:
On dead leaf bases of Puya sp. (mc, pH 7.4), dwb 2973. ARG-0667: On dead leaf bases of Puya sp. (mc, pH 7.2), dwb 2844; (mc,
pH 6.8), dwb 2866; (mc, pH 6.9), dwb 3152. ARG-06-68: On dead
leaf bases of Puya sp. (mc, pH 7.1), dwb 2849. ARG-07-62: On
dead leaf bases of Puya sp. (mc, pH 6.7), dwb 2924.
These collections have globose to subglobose sporocarps, 225-500 µm in diameter and 875-1050 µm in
total height (Figs. 10-11). The stipe is long and thin
(45-67-70 µm wide) and filled with spore-like cysts 8(12.1)-15.5 µm diameter, the peridium is partially evanescent, and the remaining flattened calyculus is
slightly narrower than the diameter of the sporotheca
and finely warted on the inner surface by LM and
SEM (Figs. 12-13). The capillitium is tubular, slightly
elastic, firmly attached to the calyculus (Fig. 11), the
tubules are 2.5-(3.5)-4.5 µm in diameter, lightly ornamented with warts by LM, the warts fused to form
small crests by SEM (Figs. 14, 15, 17, 18). The spores
are yellowish by LM, 7.3-(8.3)-9.2 µm diameter, finely
warted with groups of more prominent warts readily
visible by SEM (Figs. 16, 19-21). In general the specimens agree with the original description of A. afroalpina by Rammeloo (1981a, 1981b) except for the size
of the spores, which are 9-11 µm diameter for that
species. Rammeloo however comments on the presence of collections (Rammeloo 4061 and Z109) with
smaller spores, which he called A. aff. afroalpina but
he describes the colour as grey, not yellowish like A.
afroalpina and our specimens.
In South America only previously reported from
Ecuador. New for Argentina.
Arcyria cinerea (Bull.) Pers.
ARG-06-22: On twigs, MA-Fungi 80406. ARG-06-38: On dead
leaf bases of Puya sp. (mc, pH 7), dwb 2859. ARG-06-43: On dead
leaf bases of Puya sp. (mc), dwb 2806. ARG-06-51: On dead leaf
bases of Puya sp. (mc, pH 6.9), dwb 2868. ARG-06-61: On Puya
sp. leaves, MA-Fungi 80233, 80234, 80235. ARG-06-64: On bark
of dead liana (mc, pH 7), dwb 2990; (mc, pH 7.1), dwb 3003.
ARG-06-73: On dead liana, (mc, pH 7), dwb 2977. ARG-06-76:
On Opuntia quimilo bark, (mc, pH 7.4), dwb 2995. ARG-07-48:
On dead leaf bases of Puya sp. (mc, pH 6.6), dwb 2907.
Arcyria denudata (L.) Wettst. (Figs. 22-27).
ARG-06-46: On dead leaves of Cortaderia sp., MA-Fungi
80236, 80237, 80238, 80239, 80240, 80241. ARG-06-47: On dead
leaves of Cortaderia sp., MA-Fungi 80404, 80405.
The material has small sub-cylindrical sporocarps
with the capillitium firmly attached to the calyculus
(Fig. 22). The calyculus is plicate with a warted-reticulate ornamentation; the capillitium ornamented with
rings, half rings and a reticulum (Figs. 23-25); spores
73
Figs. 10-11. Sporocarps of Arcyria afroalpina [dwb 2853]: 10, before spore dispersal. 11, after spore dispersal. The capillitial threads
firmly attached to the calyculus and barely expanding.
globose, 7-8 µm diameter, warted with groups of larger warts (Figs. 26, 27).
Arcyria insignis Kalchbr. & Cooke
ARG-06-22: On twigs, MA-Fungi 80242.
The collection confirms the presence of this species
in Argentina (Wrigley de Basanta & al., 2010b).
Arcyria minuta Buchet
ARG-06-52: On wood, MA-Fungi 80243.
Badhamia affinis Rostaf.
ARG-06-42: On bark of living Prosopis sp., MA-Fungi 80149,
80244. ARG-07-45: On Prosopis flexuosa bark (mc, pH 5.8), dwb
2901.
The field collections were plasmodiocarpic mixed
with a few short-stalked sporocarps. The collections
all had a delicate capillitium in the form of columns
arising from the base of the sporotheca, and spores
with a pale band as mentioned by Martin & Alexopoulos (1969).
Badhamia foliicola Lister
ARG-06-40: On decayed Denmoza rhodocantha, MA-Fungi
80245.
Badhamia macrocarpa (Ces.) Rostaf.
ARG-06-04: On Opuntia sulphurea cladodes, MA-Fungi
80246. ARG-06-08bis: On Opuntia sp. cladodes, MA-Fungi
80247. ARG-06-27: On twigs, MA-Fungi 80248. ARG-06-52: On
wood, MA-Fungi 80249. ARG-06-62: On Opuntia sulphurea, MAFungi 80250. ARG-06-63: On wood, MA-Fungi 80251. ARG-0664: On dried legume fruit, MA-Fungi 80252.
Two collections (MA-Fungi 80247, 80248) had
physaroid capillitium, but they keyed out to B. macrocarpa. A physaroid capillitium is also mentioned by
Martin & Alexopoulos (1969).
Badhamia melanospora Speg.
ARG-06-01: On Opuntia quimilo cladodes, MA-Fungi 80071,
80072, 80073, 80074, 80075, 80076, 80077, 80078, 80079, 80080.
ARG-06-03: On Opuntia sp. cladodes, MA-Fungi 80081, 80082.
ARG-06-04: On decayed Echinopsis atacamensis, MA-Fungi
80083; on decayed Gymnocalycium sp., MA-Fungi 80084, 80085;
on decayed Puya sp. leaves, MA-Fungi 80089; on decayed Pyrrhocactus sp., MA-Fungi 80086, 80087; on Opuntia sulphurea cladodes, MA-Fungi 80088; on cactus litter on agar, dwb 2815. ARG-0605: On decayed Orocereus trolli, MA-Fungi 80090; (mc, pH 7.4),
dwb 2813. ARG-06-06: On Opuntia sp. cladodes, MA-Fungi
80091, 80092, 80093, 80094, 80095, 80096, 80097, 80099, 80100.
80101, 80102, 80103, 80104, 80105, 80106, 80107, 80108, 80109,
80110; on decayed legume tree wood, MA-Fungi 80113; on deca-
74
C. Lado & al.
Figs. 12-21. Arcyria afroalpina by SEM: 12, 13, detail of the lightly ornamented inner surface of the calyculus. 14, 15, 17, 18, Capillitial threads. 16, 19-21, Spores. [12, 13, 15, 17, 18, 20, 21: dwb 2866. 14, 16, 19: MA-Fungi 80232]. Bar: 12, 13, 17 = 20 µm; 14-16,
18-21 = 10 µm.
yed Pyrrhocactus sp., MA-Fungi 80114, 80115, 80116, 80117; on
decayed Thillandsia sp. leaves, MA-Fungi 80111, 80112. ARG-0608: On decayed Tephrocactus sp., MA-Fungi 80118; on dead leaf
bases of Puya sp. (mc, pH 7.3), dwb 2949. ARG-06-08bis: On decayed Echinopsis atacamensis, MA-Fungi 80119, 80121; on Opuntia
sp. cladodes, MA-Fungi 80120. ARG-06-21: On Cumulopuntia boliviana bark (mc, pH 7.5), dwb 2810; (mc, pH 8.1), dwb 2827; (mc,
pH 8.1), dwb 2812. ARG-06-24: On decayed Acanthocalycium sp.,
MA-Fungi 80122. ARG-06-25: On decayed Echinopsis atacamen-
sis, MA-Fungi 80123, 80124, 80125. ARG-06-26: On decayed Cereus uruguayensis, MA-Fungi 80129; on decayed Austrocylindropuntia sp., MA-Fungi 80130; on Opuntia sulphurea cladodes, MAFungi 80126, 80127, 80128. ARG-06-28: On decayed Echinopsis
atacamensis, MA-Fungi 80131, 80132. ARG-06-30: On decayed
Echinopsis atacamensis, MA-Fungi 80133; on Opuntia sulphurea
cladodes, MA-Fungi 80134; on Denmoza rhodocantha epidermis
(mc, pH 7.6), dwb 3052; (mc, pH 7.8), dwb 3081, dwb 3082. ARG06-32: On decayed Echinopsis atacamensis, MA-Fungi 80136; on
75
Figs. 22-27. Arcyria denudata by SEM [MA-Fungi 80405]: 22, stalk and remains of the calyculus and capillitial threads. 23-25, capillitial threads. 26, 27, spores. Bar: 22 = 300 µm; 23-25 = 20 µm; 26, 27 = 10 µm.
Opuntia sulphurea cladodes, MA-Fungi 80135. ARG-06-34: On decayed Echinopsis atacamensis, MA-Fungi 80137, 80138. ARG-0635: On decayed Echinopsis atacamensis, MA-Fungi 80139; on twigs,
MA-Fungi 80140. ARG-06-37: On decayed Echinopsis atacamensis, MA-Fungi 80141; on Opuntia sulphurea cladodes, MA-Fungi
80142. ARG-06-38: On Puya sp. leaves, MA-Fungi 80143, 80144.
ARG-06-40: On decayed Austrocylindropuntia sp., MA-Fungi
80145, 80148; on decayed Denmoza rhodocantha, MA-Fungi
80146, 80147. ARG-06-42: On Prosopis sp. bark, (mc, pH 5.1),
dwb 3074, dwb 3073. ARG-06-43: On Opuntia sulphurea cladodes,
MA-Fungi 80150. ARG-06-44: On decayed Trichocereus thelego-
nus, MA-Fungi 80151; on Opuntia sulphurea cladodes, MA-Fungi
80152. ARG-06-45: On decayed Trichocereus sp., MA-Fungi
80153; on Opuntia sulphurea cladodes, MA-Fungi 80154. ARG-0646: On Opuntia sp. cladodes, MA-Fungi 80155. ARG-06-50: On
decayed Trichocereus sp., MA-Fungi 80157, 80158, MA-Fungi
80159. ARG-06-52: On Opuntia sp. cladodes, MA-Fungi 80160.
ARG-06-54: On decayed Gymnocalycium sp., MA-Fungi 80156.
ARG-06-58: On decayed Parodia sp., MA-Fungi 80161. ARG-0659: On decayed Parodia sp., MA-Fungi 80162. ARG-06-62: On decayed Trichocereus sp., MA-Fungi 80163, 80166, 80167; on Opuntia sulphurea cladodes, MA-Fungi 80164, 80165; on Trichocereus
C. Lado & al.
76
sp. cortex, (mc, pH 7.4), dwb 2984. ARG-06-63: On decayed Trichocereus sp., MA-Fungi 80169, 80170; on Opuntia sulphurea cladodes, MA-Fungi 80168. ARG-06-64: On decayed Gymnocalycium
sp., MA-Fungi 80171. ARG-06-68: On Opuntia sulphurea cladodes, MA-Fungi 80172. ARG-06-75: On Tephrocactus sp. remains,
MA-Fungi 80173. ARG-06-76: On Opuntia quimilo cladodes, MAFungi 80174, 80175; on Opuntia quimilo bark, (mc, pH 7.8), dwb
2998. ARG-07-08: On decayed Tephrocactus aoracanthus, MAFungi 80176, 80177; on decayed Tephrocactus aoracanthus, (mc,
pH 7.7), aet 11925; (mc, pH 8.3), aet 11923; (mc, pH 8.5), aet
11921, aet 11924; (mc, pH 7.4), dwb 2899; (mc, pH 7.3), dwb 2926;
(mc, pH 7.2), dwb 2934. ARG-07-11: On twigs, (mc, pH 7.8), aet
11937; on succulent stem of Compositae, (mc, pH 8.0), aet 11942;
(mc, pH 8.2), aet 11947. ARG-07-12: On decayed cladodes of Cumulopuntia boliviana, (mc, pH 8.1), aet 11931; on twigs (mc, pH
5.7), aet 11950. ARG-07-13: On decayed Denmoza rhodacantha,
MA-Fungi 80178; on Opuntia sp. internal tissue (mc, pH 9.2), aet
11949, aet 11920, aet 11930; (mc, pH 9.0), aet 11919, aet 11926.
ARG-07-47: On decayed Echinopsis candicans, MA-Fungi 80181;
on Opuntia sulphurea cladodes, MA-Fungi 80179, 80180, 80182;
(mc, pH, 8.4), aet 12012, aet 12013. ARG-07-48: On decayed Echinopsis candicans, MA-Fungi 80183. ARG-07-50: On decayed Echinopsis candicans, MA-Fungi 80184; on decayed Tephrocactus articulatus, (mc, pH 8.2), aet 12025. ARG-07-51: On decayed Tephrocactus articulatus, (mc, pH 8.2), aet 12024, aet 12033. ARG-07-52:
On decayed Echinopsis strigosa (mc, pH 9.0), aet 12029; on decayed
Tephrocactus sp., MA-Fungi 80185, 80186, 80187. ARG-07-53: On
decayed Echinopsis sp., MA-Fungi 80188. ARG-07-56: On Puya sp.
leaves, MA-Fungi 80189. ARG-07-59: On decayed Eriosyce sp.,
MA-Fungi 80192, 80193; on decayed Tephrocactus articulatus, MAFungi 80190; on Opuntia sulphurea cladodes, MA-Fungi 80191.
ARG-07-60: On decayed Tunilla corrugata, MA-Fungi 80194.
ARG-07-61: On decayed Eriosyce sp., MA-Fungi 80195.
Calomyxa metallica (Berk.) Nieuwl.
ARG-06-71: On Puya sp. leaves, MA-Fungi 80253.
Comatricha laxa Rostaf.
ARG-06-39: On Prosopis sp. bark (mc, pH 5.5), dwb 2819.
Comatricha pulchelloides Nann.-Bremek.
ARG-06-38: On dead leaf base of Puya sp. (mc, pH 7), dwb
2867.
The sporocarps in this large (>40 sporocarps)
moist chamber collection are typical of this species,
except for the shorter stalks measuring 1/5 to 1/3 of
the total height rather than 1/3 to 1⁄2 as in the description by Nannenga-Bremekamp (1985), and the
spores are 9-11 µm diameter, rather than 8-9 µm. A similar species, C. longipila Nann.-Bremek. has shorter
stalks, but smaller spores (6-7 µm diameter) and swollen tips of some free ends of the capillitium, a character not present in our specimens. This is the first time
this species has been recorded in the Neotropics.
Craterium leucocephalum (Pers. ex J.F. Gmel.) Ditmar
ARG-06-20: On Cortaderia sp., MA-Fungi 80254, 80255,
80256. ARG-06-24: On grasses, MA-Fungi 80257. ARG-06-50:
On Puya sp. leaves, MA-Fungi 80258, 80259, 80260, 80261. ARG06-51: On Puya sp. leaves, MA-Fungi 80262, 80263, 80264. ARG06-52: On wood, MA-Fungi 80265. ARG-06-61: On Puya sp. leaves, MA-Fungi 80266, 80267, 80268, 80269. ARG-06-67: On Puya
sp. leaves, MA-Fungi 80270. ARG-06-68: On dead leaf base of
Puya sp. (mc, pH 6.9), dwb 2841. ARG-06-71: On dead leaf base
of Puya sp. (mc, pH 6.8), dwb 2975. ARG-07-63: On dead leaf
base of Puya sp. (mc, pH 6.4), dwb 2895.
Some of the specimens (MA-Fungi 80254, 80255,
80256, 80257, dwb 2841, dwb 2975, dwb 2895) were
the variety scyphoides (Cooke & Balf. f.) G. Lister,
differentiated by the more globose sporotheca and
slightly larger spores.
Cribaria lepida Meyl. (Figs. 28-31).
ARG-07-56: On Puya sp. leaves, MA-Fungi 80271; on dead leaf
base of Puya sp. (mc, pH 6.9), dwb 2886; (fc) dwb 2896. ARG-0661: On dead leaf base of Puya sp. (mc, pH 7.4), dwb 3015. ARG07-63: On Puya sp. leaves, MA-Fungi 80272.
This purple Cribraria, is similar in colour to C. violacea but with longer stalks, up to 8 times the diameter of the sporotheca. The specimens have a shallow
calyculus occupying approximately one third of the
diameter of the sporotheca (Fig. 28), finely dotted
with calcic granules (Fig. 28), the upper margin scalloped giving rise at the points to a fine net with few
thickened pulvinate nodes. The spores are pale violet, 6-7.5 µm diameter and have a smooth but pitted
appearance in transmitted light with Nomarski optics, but are in fact densely and minutely warted by
SEM (Figs. 29-31). The plasmodium was described
as probably white by Meylan (1927) but he may have
seen later stages of the morphogenesis. Pale purple
protoplasmodia were observed during the development of these specimens in moist chamber culture,
giving rise to a pale stalk with the white ball of the
forming sporotheca on top, dotted with purple as the
nodes form, also mentioned by Meylan, then all turning completely purple and exuding water droplets
with the maturation of the spores. These suppose
new records of the species for South America. It has
been cited from dry areas of Mexico (Estrada-Torres
& al., 2009).
Cribraria violacea Rex
Dianema corticatum Lister
Comatricha tenerrima Nann.-Bremek.
ARG-06-64: On bark of dead liana (mc, pH 7.1), dwb 2986;
(mc, pH 7), dwb 2988.
In this collection the specimens were predominate-
ly sporocarpic to short plasmodiocarps, and the sparse
capillitium has branched slender threads, often twisted spirally at the ends and with a roughened surface,
and typical clustered spores but with 5-15 spores per
cluster, not 2-6 as stated in Martin and Alexopolous
(1969). This is the first record for South America. In
the Neotropics it has been reported from Mexico.
77
ceum in the spores, which are subglobose, 13-16 µm
diameter, densely and minutely warted, with a pattern of tiny white lines where there are fewer warts,
the spores appearing almost angular with Nomarski
optics because of the lines, whereas in D. crustaceum
the spores are dark and spiny, mostly 12-14 µm diameter. In the Neotropics, this species has been reported from Mexico.
Dictydiaethalium plumbeum (Schumach.) Rostaf.
Diderma cf. deplanatum Fr.
ARG-06-51: On leaves of Puya sp., MA-Fungi 80276.
Diderma cf. crustaceum Peck
ARG-06-50: On dead leaf bases of Puya sp. (mc, pH 6.8), dwb
3023.
The specimens in this collection are macroscopically similar to D. crustaceum, with white sessile
sporocarps, which are closely gregarious to heaped,
and distorted in shape by mutual pressure. They differ from D. crustaceum in having a brown and membranous hypothallus, not white and limy as in that
species. Our specimen also differs from D. crusta-
The weathered material in this collection did not
permit a definite identification.
Diderma hemisphaericum (Bull.) Hornem.
ARG-06-27: On twigs, MA-Fungi 80277, 80278, 80279, 80280.
Didymium anellus Morgan
ARG-06-03: On decayed Echinopsis atacamensis cf., MA-Fungi
80281. ARG-06-38: On dead leaf base of Puya sp. (mc, pH 7.1),
dwb 2855; (mc, pH 7.1), dwb 2870; (mc, pH 7), dwb 2856.
Figs. 28-31. Cribraria lepida by SEM [dwb 2886]: 28, remains of the peridium forming a shallow calyculus. 29-31, spores. Bar: 28 =
100 µm; 29-31 = 10 µm.
78
C. Lado & al.
The field collection differs from the typical D. anellus in having spores without groups of warts.
Didymium clavus (Alb. & Schwein.) Rabenh.
Didymium obducens P. Karst.
2940.
ARG-06-76: On litter, MA-Fungi 80098; on wood, MA-Fungi
80282, MA-Fungi 80283.
Our specimen fits the description of this species by
Härkönen (1979: 3-5) exactly. It is the first record for
the Neotropics.
Didymium dubium Rostaf.
Didymium quitense (Pat.) Torrend. (Figs. 32-36).
ARG-06-03: On decayed Echinopsis sp., MA-Fungi 80284.
ARG-06-64: On the wood of a leguminous tree, MA-Fungi 80285.
Didymium infundibuliforme D.Wrigley, Lado &
Estrada
ARG-06-08: On dead leaf bases of Puya sp., dwb 2942. ARG06-50: On Puya sp. leaves, MA-Fungi 78321, 80286; on dead leaf
bases of Puya sp. (mc, pH 6.8), dwb 3019. ARG-06-51: On dead
leaf base of Puya sp. (mc, pH 6.8), dwb 2829, dwb 2834. ARG-0660: On dead leaf base of Puya sp. (mc, pH 7.1), dwb 2851. ARG06-61: On Puya sp. leaves, MA-Fungi 78322, 78323, 78320. ARG06-67: On dead leaf base of Puya sp. (mc, pH 6.9), dwb 2825; (mc,
pH 7.2), dwb 2843; (mc, pH 6.8), dwb 2845; (mc, pH 6.9), dwb
dwb 2918. ARG-07-52: On dead leaf base of Puya sp. (mc, pH
7.1), dwb 2927. ARG-07-56: On Puya sp. leaves, MA-Fungi 78324,
78325. ARG-07- 63: On dead leaf base of Puya sp. (mc, pH 6.4),
dwb 2894.
These collections with the exception of MA-Fungi
80286, dwb 2918 and dwb 3154, were included in the
original description of the species by Wrigley de Basanta & al. (2009).
Didymium cf. listeri Massee
This collection has white sporocarps to short plasmodiocarps, with a double peridium, the outer layer
like an egg-shell, formed of tiny closely packed crystals
(Fig. 32), the inner layer membranous and iridescent.
The dehiscence is irregular, leaving a flat base attached
to the substrate. The capillitium is short and rigid,
brown with pale ends, of uniform diameter and with
cross connections forming a loose net, with a granular
surface by SEM (Fig. 34). The spores are dark purplish
brown and polyhedral with the angles slightly lighter
in colour, 13-15 µm diameter, covered with warts united to form a sub-reticulum by LM, much more clearly
seen by SEM. In the SEM micrographs (Figs. 33, 35,
36) the ornamentation can be seen to be a dense network of irregular muri. This rare species was described
by Patouillard & Lagerheim (1895) as Chondrioderma
quitense Pat. from Quito (Ecuador), on leaves. This is
the first time the species has been recorded from Argentina.
Didymium squamulosum (Alb. & Schwein.) Fr.
ARG-07-11: On decayed wood, (mc, pH 7.0), aet 11956.
This collection has many sessile, pulvinate sporocarps to short effuse plasmodiocarps, with irregular dehiscence. The peridium is double, the outer layer like
an egg-shell, formed of closely packed crystals. The inner layer is membranous, iridescent and hyaline by LM.
The capillitium is rigid, formed by hyaline tubules arising from the rudimentary columella. The spores are
globose, 10-11.5 µm diameter, faintly warted and with
a paler area. This species is macroscopically similar to
D. quitense (see below) but has smaller, paler globose
spores, and a hyaline capillitium. It differs from the
original description in the pale area of the spores and
the paler capillitium. If confirmed this would be the
first record of the species for Argentina. In the
Neotropics it has been found in Mexico and Ecuador.
ARG-06-27: On twigs, MA-Fungi 80289, 80290. ARG-06-64:
On legume dried fruits, MA-Fungi 80291, 80292; on legume tree
wood, MA-Fungi 80293, 80294, 80295; on Puya sp. leaves, MAFungi 80296. ARG-06-70: On decayed Stetsonia coryne, MA-Fungi 80297, 80298; on legume tree wood, MA-Fungi 80299. ARG06-76: On Prosopis sp. litter, MA-Fungi 80300; on Opuntia quimilo bark (mc, pH 6.9), dwb 2993.
Some of the collections had sub-sessile sporocarps, and the stipes of some stipitate sporocarps
were less robust. Some also did not have an obvious
white hypothallus.
Didymium vaccinum (Durieu & Mont.) Buchet
80287.
ARG-06-24: On Cumulopuntia boliviana epidermis (mc, pH 8),
dwb 3076; (mc, pH 7.5), dwb 3077. ARG-06-38: On Puya sp. leaves, MA-Fungi 80301, 80302, 80303, 80304; on dead leaf base of
Puya sp. (mc, pH 7), dwb 2832. ARG-06- 50: On Puya sp. leaves,
MA-Fungi 80305, 80306, 80307, 80308; on dead leaf bases of Puya
sp. (mc, pH 7.1), dwb 2978. ARG-06-57: On Stipa atacamensis,
MA-Fungi 80309. ARG-06-60: On Puya sp. leaves, MA-Fungi
80310. ARG-07-56: On Puya sp. leaves, MA-Fungi 80311, 80312,
80313. ARG-06-64: On bark of dead liana (mc, pH 7), dwb 3020.
ARG-06- 67: On dead leaf base of Puya sp. (mc, pH 6.9), dwb 3153.
This is the first record of this species for South America. In the Neotropics it has been found in Mexico.
These represent the first records of this species for
Argentina.
Didymium mexicanum G. Moreno, Lizárraga & Illana
79
Figs. 32-36. Didymium quitense by SEM [MA-Fungi 80288]: 32, detail of the peridium with the outer layer formed of tiny closely packed crystals. 33, 35, 36, spores with a dense network of irregular muri. 34, fragment of a capillitial thread. Figs. 37-39. Physarum
synsporum by SEM [MA-Fungi 80377]: 37, spore with irregular ornamentation. 38, 39, cluster of spores, arrows show the contact
points between the spores. Bar: 32, 34 = 20 µm; 33, 35-39 = 10 µm.
Didymium wildpretii Mosquera, Estrada, BeltránTej., D. Wrigley & Lado
ARG-06-76: On Opuntia quimilo bark (mc, pH 7.4), dwb 2994;
(mc, pH 7.8), dwb 2996; (mc, pH 6.9), dwb 3005.
ARG-06-03: On Opuntia sp. cladodes, MA-Fungi 80208.
These are the first records for South America of this
80
C. Lado & al.
species. It was recently described from material from
arid areas of Mexico and from the Canary Islands,
Spain (Lado & al., 2007b).
Echinostelium arboreum H.W. Keller & T.E. Brooks.
(Fig. 40).
2937; (mc, pH 6.9), dwb 2939. ARG-06-30: On Denmoza rhodocantha epidermis (mc, pH 7.5), dwb 3078. ARG-07-08: On Tephrocactus aoracanthus remains (mc, pH 8.3), aet 11918.
Described from Mexico this species is characterized by pale yellow sporocarps with a persistent shiny
peridium (Fig. 40), which dehisces at the base of the
sporotheca leaving a distinct wide collar. The columella is stout and it has dichotomously branched
capillitial threads. This is the first record of the species
from Argentina.
Echinostelium colliculosum K.D. Whitney & H.W.
Keller
2938. ARG-06-20: On bark and twigs of unidentified shrub (mc,
pH 4.4), dwb 2786; (mc, pH 4.5), dwb 2801 ARG-06-30: On Denmoza rhodocantha epidermis, (mc, pH 7.5), dwb 3042; (mc, pH
7.8), dwb 3043. ARG-06-36: On Prosopis sp. bark (mc, pH 6.1),
dwb 2787 ARG-06-39: On Prosopis sp. bark (mc, pH 6.1), dwb
3039; (mc, pH 6), dwb 3040 ARG-06-51: On dead leaf bases of
Puya sp. (mc, pH 6.9), dwb 2823; (mc, pH 6.8), dwb 2824 ARG06-52: On Brea sp. bark (mc, pH 6.4), dwb 2963. ARG-07-08: On
Tephrocactus aoracanthus remains (mc, pH 7.3), dwb 2887; (mc,
pH 8.5), aet 11913; (mc, pH 8.3), aet 11915. ARG-07-50: On
Opuntia sulphurea remains (mc, pH 8.8), aet 12010; on Tephrocactus articulatus remains (mc, pH 8.4), aet 12009.
This species was reported from arid areas of Mexico (Estrada-Torres & al., 2009) from cacti and tree
bark. The authors commented on the small size and
the slightly different spore-like body and spore shape.
These collections appear to be the same ecotype, and
also measure from 60-130 µm in total height with a
sporotheca of 20-29 µm diameter. Whitney (1980), in
the original description, gives the measurements as
70-150 µm, and 30-50 µm respectively. It was reported for the first time from Argentina from Santa Cruz
(Wrigley de Basanta & al., 2010b).
Echinostelium minutum de Bary
ARG-06-38: On dead leaf bases of Puya sp. (mc, pH 7), dwb
2863. ARG-06-42: On Prosopis sp. bark (mc, pH 5.6), dwb 3045.
Hemitrichia minor G. Lister
80197.
Fig. 40. Echinostelium arboreum [dwb 2937]: Two sporocarps showing the persistent shiny peridium.
Licea belmontiana Nann.-Bremek.
ARG-07-63: On Puya sp. leaves, MA-Fungi 80314. ARG-0748: Dead leaf base of Puya sp. (mc, pH 6.6), dwb 2916.
81
The species is cited here for the first time for the
Neotropics.
These are the first records of this species in South
America. In the Neotropics it has been cited from
Mexico.
Licea scyphoides T.E. Brooks & H.W. Keller. (Figs.
49-53).
Licea denudescens H.W. Keller & T.E. Brooks
The circumscissile equatorial dehiscence leaving a
basal calyculus (Figs. 49, 50), the clearly ornamented
inner peridial surface (Fig. 51) and the very closely
punctate spores (Figs. 52, 53) are characteristics of
this species. Reported previously from Ecuador and
Peru in South America, and on the bark of another living cactus, Opuntia sp. from Mexico (Wrigley de Basanta & Lado, 2005) but these are the first records
from Argentina.
ARG-07-45: On Prosopis flexuosa bark (mc, pH 6), dwb 2902,
dwb 2905.
In South America the species has been recorded
from Brazil, but these represent the first records for
Argentina.
Licea eremophila D. Wrigley, Lado & Estrada
ARG-06-60: On Puya sp. leaves, MA-Fungi 79159; on dead leaf
bases of Puya sp. (mc, pH 7.1), dwb 2837; (mc, pH 6.9), dwb 2888.
2982. ARG-06-62: On Trichocereus sp. cortex (mc, pH 7.4), dwb
3002. ARG-06-67: On Puya sp. leaves, MA-Fungi 79160, 79161;
on dead leaf bases of Puya sp. (mc, pH 6.9), dwb 2826, dwb 3151;
(mc, pH 7.2), dwb 2885. ARG-07-62: On dead leaf bases of Puya
sp. (mc, pH 6.7), dwb 2920.
These collections were included in the paper describing this as a new species (Wrigley de Basanta &
al., 2010a).
Licea pygmaea (Meyl.) Ing. (Figs. 41-48).
ARG-06-06: On bark of living Prosopis sp. (mc, pH 6.2), dwb
3035. ARG-06-10: On Stipa atacamensis (mc, pH 7.1), dwb 2874;
(mc, pH 7), dwb 2875. ARG-06-14: On Stipa atacamensis (mc, pH
6.5), dwb 3006. ARG-06-22: On Stipa sp. (mc, pH 5.5), dwb 3026;
(mc, pH 4.8), dwb 3037. ARG-06-24: On Stipa atacamensis (mc,
pH 5.5), dwb 2999.
These specimens belong to the subgenus Licea, according to the revision of the genus by Nannenga-Bremekamp (1965), dehiscing by platelets (Figs. 41, 42).
They have baculate spore ornamentation by SEM
(Figs. 46-48) and teeth-like protuberances on the
edge of the platelets (Figs. 43-45). The double peridium is slightly warted on edge of the inner surface at
high magnification by SEM (Figs. 43, 44), otherwise
smooth. These are the first records of this species in
South America. In the Neotropics it has been cited
from Mexico.
ARG-06-02: On bark of living Echinopsis atacamensis (mc, pH
6.5), dwb 2778.
Licea succulenticola Mosquera, Lado, Estrada & Beltrán-Tej.
3008. ARG-06-60: On dead leaf bases of Puya sp. (mc, pH 7.1),
dwb 2871. ARG-07-50: On internal tissue of Opuntia sulphurea
(mc, pH 8.8), aet 12021. ARG-07-56: On Puya sp. leaves, MAFungi 80343; on dead leaf bases of Puya sp. (mc, pH 6.9), dwb
2921.
These represent the first records of the species for
Argentina. It was recently described from material
from arid areas of Mexico, from the Canary Islands,
Spain and from USA (Mosquera & al., 2003). In
South America it is also known from Chile and
Ecuador.
Lycogala epidendrum (L.) Fr.
ARG-06-27: On wood, MA-Fungi 80315.
Macbrideola andina D. Wrigley, Lado & Estrada, sp.
nov. (Figs. 54-58).
Holotype: Argentina. Salta, Molinos, Molinos river,
route RN-40, km 4458, 25°25’56”S 66°17’11”W,
2059 m ± 10m, on bark of living Prosopis sp. collected
25-XI-2006, A. Estrada-Torres, C. Lado & D. Wrigley
de Basanta, dwb 3048 (MA-Fungi 79883).
3036, 3026a.
Species Macbrideola oblonga Pando & Lado proxima, sed ab ea densis capillitium atque uniforme diametros, cum acuminis spinosis, sporothecae sine torquis
basalis, sporis densis spinulis ornatis primo icto discernibilis.
The characteristic hyaline tubercles on the platelet
edges of the transparent peridium permit the identification of this tiny species, described by Mitchell
& McHugh (2000), from the British Isles and USA.
Sporocarps scattered or in small groups, stipitate,
0.4-0.9 mm in total height. Sporotheca 0.25-0.6 mm in
height by 0.2-0.4 mm wide, ellipsoidal (Figs. 54, 57),
rarely subglobose, greyish brown (61. gy. Br-62. d. gy.
Licea sambucina D.W. Mitch.
82
C. Lado & al.
Figs. 41-48. Licea pygmaea by SEM: 41, 42, sporocarp showing the dehiscence by plates. 43-45, edge of the peridial platelets showing teeth-like protuberances. 46-48, spores. [41, 47: dwb 3037. 42-46, 48: dwb 2999]. Bar: 41, 42 = 100 µm; 43, 44 = 20 µm; 45-48 = 10 µm.
83
Figs. 49-53. Licea scyphoides by SEM [dwb 2778]: 49, 50, dehisced sporocarps. 51, detail of the ornamentation of the inner peridial
surface. 52, 53, spores with a dense ornamentation of minute warts. Bar: 49, 50 = 100 µm; 51-53 = 10 µm.
84
C. Lado & al.
Br). Hypothallus membranous, translucent, concolourous with the base of the stalk. Stalk 0.1-0.3 mm in
length, hollow, tubular, widening into the hypothallus, brownish black (65. br Black), with a paler area,
orange-yellow to yellowish brown (72. d. OY-75. deep
y Br) at the base. Peridium membranous, completely
evanescent. Columella brownish black (65. br Black),
almost reaching the apex of the sporotheca. Capillitium greyish brown (61. gy. Br-62. d. gy. Br), arising
from all parts of the columella, dichotomously branched, forming a dense internal net, the threads of uniform diameter, not tapering towards the periphery,
making frequent anastomoses with numerous free
ends appearing as spines at the periphery, at the base
of the sporotheca these anastomoses making an irregular surface net (Figs. 55, 58). Spores greyish brown
(61. gy. Br-62. d. gy. Br) in mass, lighter by transmitted
light (63. l. br Gy), globose, 9-11 µm diam., warted by
LM, with closely, evenly distributed spinules by SEM
(Fig. 56). Plasmodium not observed.
Etymology: The epithet andina refers to the geographical area where the species was found.
Habitat: Bark of living Prosopis sp.
Known distribution: Salta and Jujuy, Argentina.
Other specimens examined
3055. ARG-06-36: On bark of living Prosopis sp. (mc, pH 6.1),
dwb 2795. ARG-06-39: On bark of living Prosopis sp. (mc, pH 6),
dwb 3041; (mc, pH 6.1), dwb 3065. Macbrideola oblonga Pando &
Lado. Spain: Soria, Calatañazor, Dehesa de Carrillo, 1050 m,
30TWM1417, on bark of Juniperus thurifera (mc), MA-Fungi
16008 (Holotype).
The distinctive characters of this new species are its
ellipsoid sporotheca (Fig. 54), a short tubular stalk, a
columella gradually tapering upwards to the apex, a
dense, robust, capillitium with threads of uniform diameter, and no collar (Figs. 54, 55, 57, 58). This species
also has a distinctive ornamentation of the spores by
SEM (Fig. 56). The overall habit is most similar to
Macbrideola oblonga from which the new species differs in its denser capillitium, with spiny free ends
(Figs. 55, 58), and its cylindrical stalk (Figs. 54, 57).
In M. oblonga the capillitium was described as
“… hardly or not anastomosing inside ... free ends
blunt slightly swollen or club-shaped” (Pando &
Lado, 1988) and in M. oblonga has 4-6 meshes per radius of the sporotheca, whereas in M. andina there are
10-12 meshes in a much denser net. The stalk in M.
oblonga is conical (Pando & Lado, 1988: fig. 2). The
new species also differs in its total lack of a collar
(transparent red-brown in M. oblonga) and the ornamentation of the spores by SEM. This ornamentation,
in M. oblonga, is of small rounded warts, not spinules,
and they are less uniformly distributed than in M. andina. Another species that lacks a collar and has anastomoses on the periphery of the capillitium is Macbrideola dubia Nann.-Bremek. & Y.Yamam. (NannengaBremekamp & Yamamoto, 1990), but in this species
the columella only reaches around the middle of the
sporotheca, not almost to the apex as in our species,
the lax capillitium attenuates towards the periphery,
and it has a netted fibrous stalk base, absent in the new
species. Macbrideola dubia also has an extensive hypothallus common to groups of sporocarps, and darker spores. The shape of M. andina is somewhat similar to M. ovoidea Nann.-Bremek. & Y. Yamam. (Nannenga-Bremekamp & Yamamoto, 1983) but in this
species the capillitium does not anastomose, which easily distinguishes it from the new species. Macbrideola
ovoidea also has smaller spores, 7-8.5 µm diameter vs.
9-11 µm diameter in M. andina, and the spiny ornamentation by SEM has stellate apices (Moreno & al.,
2006: figs. 29, 30), absent in M. andina. Another species with a dense capillitium is Macbrideola lamprodermoides G. Moreno, Lizárraga, & Illana (Moreno & al.,
2006) but it can be easily distinguished from M. andina by its persistent silvery peridium, evanescent in the
latter, and the presence of a collar, absent in M. andina.
Macbrideola herrerae Lizárraga, G. Moreno & Illana
(Lizárraga & al., 2006) has a well-developed capillitium but it does not anastomose at the periphery and
is made of rigid and parallel threads with free dichotomously branched ends, totally different from the dense and robust net of the capillitium of M. andina. Macbrideola reticulospora Hooff & Nann.-Bremek. is distinguished by its reticulate spores.
The specimens developed on the bark of living Prosopis sp. at over 2000 m elevation at a slightly acidic
pH, in two different provinces (Jujuy and Salta) of the
North of Argentina. The development time in moist
chamber was 4-71 days, probably dependent on whether the species was in the form of sclerotia, microcysts
or spores, when the substrate was wetted.
Macbrideola scintillans H.C. Gilbert
ARG-06-73: On dead liana (mc, pH 7), dwb 2966.
This represents the first record of the species for
South America.
Perichaena calongei Lado, D. Wrigley & Estrada
ARG-06-08: On dead leaf base of Puya sp. (mc, pH 6.9), dwb
2957. ARG-06-38: On Puya sp. leaves, MA-Fungi 78678, 78679,
78680, 78681; on dead leaf base of Puya sp. (mc, pH 7), dwb 2833;
(mc, pH 7.1), dwb 2865; (mc, pH 7), dwb 2857. ARG-06-50: On
Puya sp. leaves, MA-Fungi 78682, 78683, 78684. ARG-06-51: On
Puya sp. leaves, MA-Fungi 78685, 78686, 78687, 78688. ARG-0660: On dead leaf base of Puya sp. (mc, pH 6.9), dwb 2838; (mc, pH
85
Figs. 54-58. Macbrideola andina by SEM [dwb 3048]: 54, 57, sporocarps. 55, detail of the base of the sporotheca with the capillitium attached along the length of the columella. 56, spores. 58, detail of the base of another sporotheca showing anastomoses and
spiny free ends. Bar: 54 = 300 µm; 55, 57, 58 = 100 µm; 56 = 10 µm.
86
C. Lado & al.
7.1), dwb 2852. ARG-06-61: On Puya sp. leaves, MA-Fungi 78689;
on dead leaf base of Puya sp. (mc, pH 7.4), dwb 3009. ARG-06-67:
On Puya sp. leaves, MA-Fungi 78690. ARG-06-68: On dead leaf
base of Puya sp. (mc, pH 7.1), dwb 2850; (mc pH 6.9), dwb 2873.
ARG-07-56: On Puya sp. leaves, MA-Fungi 78691, 78692, 78693.
These collections were included in the paper describing this as a new species (Lado & al., 2009).
Perichaena depressa Lib.
ARG-06-38: On Puya sp. leaves, MA-Fungi 80316, 80317,
80318, 80319, 80320. ARG-06-50: On Puya sp. leaves, MA-Fungi
80321. ARG-06-51: On Puya sp. leaves, MA-Fungi 80322. ARG06-60: On Puya sp. leaves, MA-Fungi 80323. ARG-06-70: On decayed Stetsonia coryne, MA-Fungi 80324. ARG-07-56: On Puya
sp. leaves, MA-Fungi 80325, 80326.
Perichaena quadrata T. Macbr.
ARG-06-06: On bark of living Prosopis sp., (mc, pH 6), dwb
dwb 2955; (mc, pH 6.9), dwb 2956. ARG-06-27: On twigs, MAFungi 80327. ARG-06-38: On Puya sp. leaves, MA-Fungi 80328;
on dead leaf base of Puya sp. (mc, pH 7.1), dwb 2864; (mc, pH 7),
dwb 2858, dwb 2860. ARG-06-39: On Prosopis sp. bark (mc, pH
5.5), dwb 3094. ARG-06-42: On dead leaf base of Puya sp. (mc,
pH 7.2), dwb 3091, ARG-06-61: On dead leaf base of Puya sp.
(mc, pH 7.4), dwb 2981. ARG-06-64: On bark of dead liana (mc,
pH 7), dwb 3021, (mc, pH 7.1), dwb 3010.
These represent the first records of the species for
South America. In the Neotropics, it has been reported from Mexico.
for the Neotropics, if confirmed. The species was described by Martin (1948), from the mountains of California.
Physarum bitectum G. Lister
ARG-06-06: On bark of Prosopis sp. (mc, pH 5.9), dwb 3038.
ARG-06-27: On twigs, MA-Fungi 80344, 80345, 80346, 80347,
80348. ARG-06-38: On Puya sp. leaves, MA-Fungi 80349, 80350
80351, MA-Fungi 80352. ARG-06-39: On bark of Prosopis sp.
(mc, pH 5.5), dwb 3071. ARG-06-42: On bark of Prosopis sp. (mc,
pH 5.8), dwb 3068.
These collections are new records of the species for
Argentina.
Physarum compressum Alb. & Schwein.
80199, 80200. ARG-06-03: On decayed Echinopsis sp., MA-Fungi
80203, 80204, 80205; on Opuntia sp. cladodes, MA-Fungi 80201,
80202, 80206. ARG-06-08: Isolated on agar from remains of a bromeliad, dwb 2814. ARG-06-38: On dead leaf base of Puya sp. (mc,
pH 7), dwb 2861. ARG-06-50: On Puya sp. leaves, MA-Fungi
80207. ARG-06-76: On Opuntia quimilo bark (mc, pH 6.9), dwb
2992; (mc, pH 7.8), dwb 2997.
Physarum decipiens M.A. Curtis
ARG-06-39: On bark of living Prosopis sp. (mc, pH 6), dwb
3070; (mc, pH 5.5), dwb 3072.
These collections are new records of the species for
Argentina.
Physarum didermoides (Pers.) Rostaf.
Perichaena vermicularis (Schwein.) Rostaf.
ARG-06-05: On Oreocereus trollii remains (mc, pH 6.8), dwb
2811. ARG-06-07: On decayed Echinopsis atacamensis, MA-Fungi
80329, 80330, 80331, 80332; on decayed legume tree wood, MAFungi 80333. ARG-06-24: On decayed Acanthocalycium sp., MAFungi 80334. ARG-06-38: On Puya sp. leaves, MA-Fungi 80335.
ARG-06-50: On Puya sp. leaves, MA-Fungi 80336, 80337, 80338.
ARG-06-51: On Puya sp. leaves, MA-Fungi 80339, 80340. ARG-0652: On Brea sp. bark (mc, pH 6.5), dwb 3013. ARG-06-62: On decayed Trichocereus sp., MA-Fungi 80341; on Trichocereus sp. cortex
(mc, pH 7.4), dwb 2985; (mc, pH 7.2), dwb 3017. ARG-06-63: On
decayed Trichocereus sp., MA-Fungi 80342. ARG-06-71: On dead
leaf bases of Puya sp. (mc, pH 6.8), dwb 2983. ARG-07-08: On
Tephrocactus aoracanthus remains (mc, pH 8.3), aet 11960; (mc, pH
8.5), aet 11924b. ARG-07-47: On Opuntia sulphurea remains (mc,
pH 8.2), aet 12030; (mc, pH 8.4), aet 12031. ARG-07-50: On
Tephrocactus articulatus (mc, pH 8.2), aet 12026; (mc, pH 8.4), aet
12027. ARG-07-51: On Tephrocactus articulatus (mc, pH 8.2), aet
12035.
Physarum cf. auripigmentum G.W. Martin
The specimen is close to P. auripigmentum but the
spores are slightly larger [10-12 µm diameter vs. (8)910(11) µm diameter] and have a paler area at one pole.
This would represent the first record of the species
ARG-06-03: On decayed Echinopsis sp., MA-Fungi 80353; on
Opuntia sp. cladodes, MA-Fungi 80401.
Physarum hongkongense Chao H. Chung
The laterally compressed, pale yellow, sessile plasmodiocarps with a double peridum, which separates
at dehiscence, are typical of Physarum hongkongense.
However the spores in our collection are larger (10.512 µm diameter vs. 7.5-9 µm diameter). This species
can be distinguished from P. bogoriense primarily on
the basis of the yellow colour of the plasmodiocarps
(Chung & Tzean, 1998), but the authors have found
the two species occurring together on a single leaf. We
have also seen the same in material from Brazil (unpublished data). Physarum hongkongense, apart from its
colour, differs in the apical fissure of dehiscence,
which is by irregular fracture into fragments in P. bogoriense. As has been stated before (Wrigley de Basanta & al., 2008), these species may be conspecific.
This collection represents the first record of the species for South America. In the Neotropics, it has been
reported from Mexico.
Physarum leucophaeum Fr.
Physarum licheniforme (Schwein.) Lado
ARG-06-16: On Stipa atacamensis, MA-Fungi 80356, 80402,
80357; (mc, pH 7), dwb 2794; (mc, pH 7.1), dwb 2800. ARG-0620: On Cortaderia sp., MA-Fungi 80358. ARG-06-24: On grasses,
MA-Fungi 80359. ARG-06-50: On dead leaf bases of Puya sp. (mc,
pH 6.8), dwb 2980. ARG-07-12: On twigs, MA-Fungi 80360.
These collections represent the first records of the
species for South America. In the Neotropics, it has
been reported from Mexico and Cuba.
87
2796. ARG-07-45: On bark of living Prosopis flexuosa (mc, pH 6),
dwb 2930, dwb 2910.
Physarum spectabile Nann.-Bremek., Lado & G.
Moreno
ARG-06-03: On decayed Echinopsis sp., MA-Fungi 80373.
ARG-06-07: On Echinopsis atacamensis internal tissue (mc, pH
8.9), dwb 2798; (mc, pH 8.6), dwb 2799; (mc, pH 9.1), dwb 2809.
80374. ARG-06-35: On twigs, MA-Fungi 80375. ARG-06-62: On
decayed Trichocereus sp., MA-Fungi 80376. ARG-06-70: On Stetsonia coryne, (mc, pH 7.4), dwb 3007. ARG-07-11: On succulent
stem of Compositae, (mc, pH 8.0), aet 11946; on twigs of an unidentified shrub (mc, pH 7.8), aet 11953. ARG-07-12: On decayed
Cumulopuntia boliviana, (mc, pH 8.1), aet 11959.
Physarum megalosporum T. Macbr.
ARG-06-63: On wood, MA-Fungi 80361. ARG-06-70: On
wood of a leguminous plant, MA-Fungi 80362. ARG-06-76: On
wood, MA-Fungi 80363.
These collections are the first records of this species
for Argentina.
Physarum notabile T. Macbr.
ARG-06-02: On Echinopsis atacamensis remains (mc, pH 6.5),
dwb 2802. ARG-06-61: On leaves of Puya sp., MA-Fungi 80364,
80365, 80366. ARG-06-62: On Trichocereus sp., MA-Fungi 80367
ARG-06-64: On a legume tree wood, MA-Fungi 80368, 80369,
dwb 2842; on leaves of Puya sp., MA-Fungi 80371. ARG-06-68:
On dead leaf base of Puya sp. (mc, pH 6.8), dwb 2872. ARG-0676: On wood, MA-Fungi 80372. ARG-07-12: On twigs of a Compositae, (mc, pH 5.8), aet 11944.
Physarum pusillum (Berk. & M.A. Curtis) G. Lister
ARG-06-03: On decayed Trichocereus thelegonus, MA-Fungi
80209. ARG-06-38: On Puya sp. leaves, MA-Fungi 80210; on
dead leaf base of Puya sp. (mc, pH 7), dwb 2830. ARG-06-42: On
Prosopis sp. wood, MA-Fungi 80212, 80213; on twigs, MA-Fungi
80211; on Prosopis sp. bark (mc, pH 6.5), dwb 3075. ARG-06-43:
On dead leaf base of Puya sp. (mc), dwb 2777. ARG-06-50: On
Puya sp. leaves, MA-Fungi 80214, 80215, 80216; on dead leaf base
of Puya sp. (mc, pH 6.8), dwb 2972. ARG-06-51: On Puya sp. leaves, MA-Fungi 80217, 80218, 80219; on dead leaf base of Puya sp.
(mc, pH 6.8), dwb 2869. ARG-06-52: On Brea sp. bark (mc, pH
6.4), dwb 3011; (mc, pH 6.1), dwb 3012. ARG-06-60: On dead
leaf base of Puya sp. (mc, pH 6.9), dwb 2835. ARG-06-61: On
Puya sp. leaves, MA-Fungi 80220, 80221. ARG-06-64: On legume
tree wood, MA-Fungi 80222; on Puya sp. leaves, MA-Fungi
80223; on bark of dead liana (mc, pH 7.1), dwb 2987; (mc, pH 7),
dwb 2989. ARG-06-67: On Puya sp. leaves, MA-Fungi 80224.
ARG-06-68: On dead leaf base of Puya sp. (mc, pH 6.8), dwb
2846; (mc, pH 6.9), dwb 2847; (mc, pH 7.1), dwb 2848. ARG-0672: On Puya sp. leaves, MA-Fungi 80225. ARG-06-73: On dead
liana (mc, pH 7), dwb 2991. ARG-07-48: On dead leaf base of
Puya sp. (mc, pH 6.6), dwb 2906, dwb 2897. ARG-07-52: On Puya
sp. leaves, MA-Fungi 80226. ARG-07-56: On Puya sp. leaves, MAFungi 80227, 80228, 80229.
Physarum serpula Morgan
These collections represent the first records of the
species for Argentina. In South America, it has been
reported from Chile.
Physarum synsporum S.L. Stephenson & Nann.-Bremek. (Figs. 37-39).
This collection has sessile, elongated plasmodiocarps, with translucent, smooth, membranous peridium, with scanty lime granules on the surface. The
capillitium is typically physaroid, with large, white,
amorphous lime nodes connected by hyaline threads.
The spores are in tight clusters of 2-4 slightly ovoid
spores (Figs. 38, 39), 11-12.5 × 8-9 µm, spinulose on
the outer surface, almost smooth on the inner surface
(Fig. 37). By SEM, some clusters of spores show a
double line of warts along the points of spore to spore
contact (Figs. 38, 39). This is one of the few species of
Physarum with clustered spores.
These collections represent the first record of the
species for the Neotropics. Described from West Virginia, USA by Stephenson & Nannega-Bremekamp
(1990).
Stemonaria irregularis (Rex) Nann.-Bremek., R.
Sharma & Y. Yamam.
ARG-07-45: On Prosopis flexuosa bark (mc, pH 6), dwb 2909,
dwb 2903.
These collections are very similar to the description
of Stemonaria irregularis (Nannenga- Bremekamp &
al., 1984), except for the size of the spores, which are
larger (10-12.5 µm diameter) in our specimens than the
size range given for that species (7.5-9.5 µm diameter).
Stemonitis mussooriensis G.W. Martin, K.S. Thind
& Sohi
ARG-06-62: On decayed Trichocereus sp., MA-Fungi 80378.
88
C. Lado & al.
This collection represents the first record of the
species for Argentina.
Stemonitopsis gracilis (G. Lister) Nann.-Bremek.
ARG-06-02: On Echinopsis atacamensis remains (mc, pH 6.5),
dwb 2790.
species for Argentina.
Trichia affinis de Bary
ARG-06-10: On grasses, MA-Fungi 80379, 80380. ARG-06-46:
On grasses, MA-Fungi 80381. ARG-06-47: On grasses, MA-Fungi
80382, 80383. ARG-06-49: On grasses, MA-Fungi 80384, 80403,
80385, 80386; on Cortaderia sp. (mc, pH 4.6), dwb 3000.
Trichia agaves (G. Moreno, Lizarraga & Illana) Mosquera, Lado, Estrada & Beltran-Tej.
ARG-06-50: On Trichocereus sp., MA-Fungi 80387.
species for South America. In the Neotropics, it has
been reported from Mexico
Trichia contorta (Ditmar) Rostaf.
ARG-06-20: On Cortaderia sp., MA-Fungi 80388.
Trichia scabra Rostaf.
ARG-06-27: On twigs, MA-Fungi 80389, 80390, 80391, 80392,
80393, 80394, 80395.
Willkommlangea reticulata (Alb. & Schwein.) Kuntze
ARG-06-14: On Stipa atacamensis, MA-Fungi 80396. ARG-0622: On grasses, MA-Fungi 80397; on twigs, MA-Fungi 80398.
ARG-06-24: On grasses, MA-Fungi 80399. ARG-06-27: On twigs,
MA-Fungi 80400.
Discussion
This biodiversity survey in the Monte Desert and
surroundings has produced almost six hundred myxomycete collections from 105 localities. They represent 72 species from 22 genera, of which the genera
Dianema and Macbrideola and 38 species, are new to
Argentina, an increase of almost 22% to the country
catalogue (Lado & Wrigley de Basanta, 2008; Wrigley
de Basanta & al., 2010b). Among these 38 species, 11
are new for South America, 5 for the whole Neotropical region and 4 species are new to science, one described herein, Macbrideola andina, and three recently
described based on material from this survey, Didymium infundibuliforme (Wrigley de Basanta & al.,
2009), Perichaena calongei (Lado & al., 2009), and Licea eremophila (Wrigley de Basanta & al., 2010a). This
brings the total number of myxomycete species
known from Argentina to 211, and from this desert
area the results represent 8% of the number of species
known worldwide (Lado, 2005-2010), a notable number for such a dry environment. Among the interesting species from the survey, apart from those newly
described, are Arcyria afroalpina, Comatricha pulchelloides, Didymium mexicanum, D. obducens, D. wildpretii, Licea sambucina, Physarum auripigmentum and
Ph. synsporum, either because they are exclusive to
arid ecosystems or because they are rare species.
The results from the Monte Desert in these seven
provinces show a high biodiversity of myxomycetes.
Although for the whole survey, the species to genus
ratio, a measure used to compare taxonomic diversity,
with the lower numbers indicating greater diversity
(Stephenson & al., 1993), is quite high (3.27), it is lower than the results (3.9) obtained in the dryland
ecosystem in Mexico (Estrada-Torres & al., 2009) or
(3.6) in Colorado, USA (Novozhilov & al., 2003), and
comparable with other results (2.2-4.6) for temperate
and tropical forests (Stephenson & al., 1993). When
the results are separated by province it can be seen
that some provinces have much higher taxonomic diversity than this (Table 2). The total number of species, now known from each province, indicates that
Salta (57 species), Jujuy (47) and Tucumán (43) are
currently the most species-rich. The table also shows
the first data on myxomycetes from La Rioja, San Juan
and San Luis, provinces previously unexplored for
myxomycetes. In order to directly compare the results
from each province, the total number of collections
was adjusted to take into account the number of collecting sites that had identifiable collections of myxomycetes included in the annotated species list (positive site). Catamarca in this case had the greatest
number of collections per positive collecting site, followed by Salta and Tucumán. The mean result was almost 8 species recovered from each locality, irrespective of the province.
The most abundant species (Table 3), by number of
collections, were Badhamia melanospora, Physarum
pusillum, Perichaena calongei, P. vermicularis, Craterium leucocephalum, Didymium infundibuliforme, D.
vaccinum and Echinostelium colliculosum. Many of
these are recognised as characteristic species of arid
environments, and here more abundant than other
species such as Didymium squamulosum, Physarum
bitectum and Arcyria cinerea of broad distribution,
usually among the common species in studies of other
environments. The assemblage of abundant species
coincides with that obtained in other studies of warm
arid areas such as the Tehuacán-Cuicatlán valley in
Mexico (Estrada-Torres & al., 2009), although there
89
Table 2. Summary data on the Myxomycetes in different Provinces of the survey area. Species a) from the literature-all vegetation types, b) this survey-arid vegetation.
Province
Localities
Total (positive)
Collections
Catamarca
19 (15)
151
Jujuy
18 (12)
La Rioja
Collections per
positive site
b
Different
species total
Genera
a
S/G
ratio
10.07
6
33
37
13
2.85
87
7.25
27
21
47
24
1.96
11 (8)
62
7.75
0
20
20
10
2.00
Salta
25 (19)
166
8.74
10
48
57
23
2.48
San Juan
24 (18)
84
4.67
0
21
21
9
2.33
San Luis
6 (4)
28
7.00
0
12
12
8
1.50
Tucumán
2 (2)
17
8.50
41
3
43
18
2.34
are some differences probably due to different substrate species (Wrigley de Basanta & al., 2010a). Surprisingly, in spite of the intense work done over recent
decades in the Neotropics (Lado & Wrigley de Basanta, 2008), almost 30% (27.8) of the species found in
the Monte Desert are new records for South America
and 12.5% are new records for the Neotropics, confirming the exclusive myxobiota of this dryland ecosystem. A relatively high number of species (Didymium infundibuliforme, D. mexicanum, D. wildpretii,
Licea eremophila, L. succulenticola, Macbrideola andina, Perichaena calongei, Physarum spectabile, Trichia
agaves) also belong to the succulenticolous species
group. The most abundant species were also the most
widespread, as can be seen (Table 3) from the number
of localities from which they were recovered.
Of the total 72 species listed above, 25 were only
found once which may indicate that these are the rarer
species such as Didymium obducens, or that at the
time of collecting there were not the ideal phenological conditions for some species or adequate substrate
for others, such as Lycogala epidendrum, a typical lignicolous species.
The most common genera belonged to the order
Physarales which made up almost 50% of the collections. This has been noted in other arid areas, for instance the Tehuacán valley in Mexico (Estrada-Torres
& al., 2009), and Atacama desert in Chile (Lado & al.,
2007a). In the Monte Desert however, the percentage
of species of the genus Physarum was greater than that
of Didymium species, unlike the results from both
Mexico and Chile where the genus Didymium was
predominant. In all three places, the species within
the genera differed, except for the most common species, indicating precise microhabitat preferences, since the substrate species were also different. This was
Species
particularly the case with the genus Didymium which
had only 5 of the 30 species of the genus from
Tehuacán in common. The species in the order Physarales made up only 32% of the total found in the Colorado plateau, USA (Novozhilov & al., 2003), but
different woody vegetation was mainly sampled there.
The sequence of orders was also basically the same in
Mexico, and in a review of all Neotropical myxomycetes (Lado & Wrigley de Basanta, 2008), where results were compared to the percentage of known
species from each order. The order Trichiales were
slightly better represented in these results from Argentina, and in spite of the known number of species
in the order being below that of the Liceales and Stemonitales, more species of Trichiales were found than
of the other two orders.
The most productive substrates of this study were
the more than twenty species of cacti, which produced 37% of all the specimens. The leafy substrates
were the next most productive with 35% of the results. This substrate group includes mainly the leaf bases of the rosette-leaved succulent plant Puya sp. (Fig.
3), a particularly productive substrate both in the field
and in moist chamber culture. The number of species
however was greater in the latter group with 32 different species compared to 25 different species from
cacti. Similar rosette-leaved succulent plants, but of
other genera such as Agave, Beaucarnea, and Hechtia,
were the most productive group of substrata in the
Tehuacán valley in Mexico (Estrada-Torres & al.,
2009). As has been noted previously (Wrigley de Basanta & al., 2010a) the rosettes form a water trap where any available moisture, even from condensation, in
these extreme desert environments is channeled towards the base of the plant. The overlapping leaves
prevent evaporation and, in the field, dead leaves
90
C. Lado & al.
Table 3. Summary data on the most common Myxomycete species.
Species
Field collections
Moist chamber
Total collections
collections
Percentage
Nº localities
of Records
found
Arcyria afroalpina
3
10
13
2.20
7
Arcyria cinerea
4
8
12
2.02
9
123
36
159
26.72
50
17
3
20
3.36
10
7
12
19
3.19
10
Didymium squamulosum
12
1
13
2.20
4
Didymium vaccinum
13
6
19
3.19
8
Echinostelium colliculosum
0
16
16
2.69
9
Licea eremophila
3
8
11
1.85
5
Perichaena calongei
17
9
26
4.37
10
Perichaena depressa
11
0
11
1.85
6
Perichaena quadrata
2
11
13
2.20
8
14
12
26
4.37
14
9
3
12
2.02
5
10
4
14
2.35
6
Physarum notabile
9
4
13
2.20
8
Physarum pusillum
17
12
29
4.87
17
Physarum spectabile
4
7
11
1.85
8
Trichia affinis
9
1
10
1.68
4
284
162
446
75.18
–
Badhamia melanospora
Craterium leucocephalum
Didymium infundibuliforme
Perichaena vermicularis
Physarum bitectum
Physarum compressum
TOTAL (19 species)
around the base were often moist even in the middle
of the day in mid summer. On bark, sixteen species
were recovered, in spite of the paucity of woody substrates in these arid areas. The majority of bark was
from species of the leguminous trees of the genus Prosopis, which was also a productive substrate in Mexican drylands (Estrada-Torres & al., 2009). In the
grasslands of the puna and surrounding areas, in spite
of the high elevation (above 3000 m), the high levels of
solar radiation and extreme temperature differences
day and night, the different species of grasses also produced a reasonable number of collections (almost
8%), and 12.5% of the species found in this survey.
In order to compare the results according to elevation and latitude of the sampling area, the results were
expressed as collections and species of myxomycetes
per locality, to correct for differences in sampling ef-
fort (Fig. 59). In the case of elevation there was a trend
towards decreasing number of specimens with increasing elevation in the sampling range of 500 m to over
4000 m, as was found in other areas of Argentina
(Wrigley de Basanta & al., 2010b). This was not the
case for the number of species, as this remained more
or less constant over the range. These values could
only reflect the moment of sampling, which may represent a better time for myxomycetes at lower elevations and not at higher elevations, since sampling was
done over the same period. The climatic conditions
over this large gradient can vary considerably and affect the substrates for myxomycete development.
The range of latitudes in this survey was from South
latitude 23º to 33º. However the results according to
latitude, corrected for differences in collecting effort,
were fairly uniform, without a significant trend. The
91
Fig. 59. Number of Myxomycetes from different elevations (positive sites only).
largest number of collections (16%), were made at latitude 28ºS and the combined number of collections
at the lower latitudes (23º-27ºS), was much greater
(60%) than the 24% at the higher latitudes (29º33ºS). This is consistent with data from other studies
in Argentina (Wrigley de Basanta & al., 2010b).
The results include 28 species only found in the
field, 19 species only produced in moist chamber culture and 25 species occurring in both field collections
and from moist chamber culture. The 127 moist
chamber cultures were 82% positive for myxomycete
plasmodia or fruiting bodies. As in other studies (Estrada-Torres & al., 2009; Wrigley de Basanta & al.,
2010b) some plasmodia only produced poor or malformed specimens, not included in the results, and in
some cases only formed sclerotia that never fruited in
the time span of the cultures. The productivity is high
for moist chambers made with plants from such a dryland area, and higher than that of 250 moist chambers
of cactus remains from dryland ecosystems of Mexico
(Estrada-Torres & al., 2009), but lower than that for
the whole study area of the Colorado Plateau (Novozhilov & al., 2003).
One of the important microenvironmental factors
affecting the abundance and diversity of myxomycetes is the pH of the substrate, as has been indicated in
other studies (Wrigley de Basanta, 2004; Wrigley de
Basanta & al., 2008). The moist chamber cultures
from this survey had a broad substrate pH range from
4.4-9.2, but the majority of myxomycete collections
were harvested from substrates with a pH falling between 6 and 7.9 (Fig. 60), and the mean pH of all cultures was circumneutral at pH 7.03. All but one of the
cultures with a basic pH of 8.0 or above, were made
with different cactus remains, and although some of
the cultures made with epidermis of cacti had a pH
nearer to 7, the mean of the cactus cultures was almost
8 (pH 7.95). The basic pH may favour the development of the lime-producing Physarales predominant
in these results. The moist chamber cultures made
with leaf bases of Puya sp., the next most productive
of all the substrates after the cacti, had a mean pH of
6.95, again close to neutral as with other productive
substrates (Wrigley de Basanta & al., 2008). Badhamia
melanospora and Echinostelium colliculosum were the
most tolerant species from the moist chamber cultu-
Fig. 60. Proportion of moist chamber collections at different
substrate pH values.
92
C. Lado & al.
res, and were recovered from substrates with pH
across the range. All the species of Arcyria were found
on substrates with a circumneutral pH, as were Licea
eremophila and Perichaena calongei, but Physarum
spectabile was found only on basic substrates.
During this survey 73 taxa, 72 species and one variety (Craterium leucocephalum var. scyphoides) were
obtained from various substrates. The number of species expected, if the sampling effort were exhaustive,
according to the estimators ACE and CHAO1, are
calculated at 104 and 94 respectively (Fig. 61). This
means that the sampling effort of this survey was 7078% complete. If the results of the field collections
and collections recovered from moist chamber culture are assessed separately, the former recovered 6972% of the expected species by each estimator and
the moist chamber cultures 81-84% respectively. This
suggests that the survey recovered a large proportion
of the assemblage of myxomycetes to be expected in
the Monte Desert. The results are surprisingly high
when considering the fact that field sampling may not
coincide with the best phenological moment for some
species. In addition the substrates for moist chamber
cultures may have spores, microcysts or sclerotia that
have been exposed for too long to the harsh conditions of the desert, and are no longer viable.
To assess community similarities between this and
studies of other arid areas in the literature, the Sørensen
coefficient of community (CC) index was used (Table
4). The myxomycete assemblage from the TehuacánCuicatlán desert of Mexico was the most similar to the
Monte Desert of Argentina (CC = 0.46). The relationships between the myxomycete assemblages of these
areas could be due to similarities in their substrates.
The floristic affinities between arid zones of North
America and the Monte Desert were researched by Solbrig (1972) and Roig & al. (2009), who found that the
genera Larrea, Cercidium and Prosopis, and members of
the families Cactaceae, Agavaceae and Bromeliaceae,
are the dominant plants shared in common between
these areas. The microhabitats of the related plants in
these taxa are similar, and so the community of myxomycetes developing in them overlaps, as pointed out
by Wrigley de Basanta & al. (2010a) for the myxobiota
of the genera Hechtia and Puya.
The apparently least similar assemblage (CC= 0.22)
was from the Atacama Desert in Chile, on the other
side of the Andes mountain chain. This is not surprising given the extreme arid environment, which limits
the myxomycete species richness (Lado & al., 2008),
and therefore produced a much smaller sample. However, despite the low number of common species (14)
this number supposed almost 60% of the species
found in that study of one of the driest places on earth.
Fig. 61. Curves of abundante (ACE and CHAO1 estimators) compared to these species accumulation curves (Sobs) of this Surrey.
White lines indicate the polinomial best fit curve.
93
Table 4. Community similarity between myxobiota of arid areas using the coefficient of community index (CC). (Top right CC, number of species in common bottom left).
Monte
Tehuacán-Cuicatlán
Atacama
Colorado Plateau
–
0.46
0.29
0.35
41
–
0.28
0.45
Atacama desert, Chile (Lado & al., 2007)
14
18
–
0.22
Colorado Plateau, USA (Novozhilov & al., 2003)
29
44
13
–
Monte desert, Argentina
Tehuacán-Cuicatlán Valley, Mexico
(Estrada-Torres & al., 2009)
More recently, succulenticolous species Didymium infundibuliforme (Wrigley de Basanta & al., 2009) and
Licea eremophila (Wrigley de Basanta & al., 2010a)
were found associated with species of succulent plants
on both sides of the Andes.
The Colorado Plateau species composition was
between the other two. The uniformity of method has
to be considered when comparing these studies. In all
of them, the results are a combination of field results
and those from moist chamber cultures. However the
total number of collections in each study was different, as was the emphasis placed on fieldwork or cultures. In addition, in the Colorado Plateau study, the
vegetation was very different from the other three areas since the research there centered on sagebrush and
woodland communities, concentrating on woody
substrates absent or very rare in the Monte Desert,
and included herbivore dung, a substrate less common in the Monte.
The present study adds data to confirm some of the
factors that appear to be critical for the development
of myxomycetes. It is evident that the macroenvironmental factors such as temperature, rainfall, elevation
and indirectly latitude, while influencing the growth of
the substrate plants, do not show a direct influence on
the species composition or abundance of the myxomycetes found in this area. On the other hand, the microenvironmental factors do seem to influence which
myxomycetes develop and how abundantly they appear. The microhabitat in and on specific plants is a complex of many variable factors. The chemical composition of different plant species is different which influences the pH of the tissue, its capacity for water
retention, and release of nutrients, which in turn determine the microbial flora living in or on and decomposing the plant, as suggested by Mosquera & al.,
(2003). The microbial biota, the food organisms for
myxomycetes, probably alter the microhabitat in the
course of decay and a succession of flora and other organisms, such as fly larvae, occurs (Fogleman & Foster,
1989; Foster & Fogleman, 1993). This complex of interacting abiotic and biotic factors within the microhabitat could explain the differences in myxobiota on
different substrates and the apparent substrate specificity seen for example in Licea eremophila, that flourished in the Monte Desert on one type of rosette-leaved
plant, Puya sp., and was absent from other similar
plants, e.g. Hechtia sp., in Mexico (Wrigley de Basanta
& al., 2010a). Other substrate, or substrate-group,
specificity has been seen with Didymium infundibuliforme on Puya sp. (Wrigley de Basanta & al., 2009),
Didymium tehuacanense on Agave sp., and Didymium
subreticulosporum, D. wildpretii and Badhamia melanospora on cacti (Estrada-Torres & al., 2009). On the
succulent plant species and cacti of the Monte Desert,
several of the succulenticolous species of myxomycetes, Didymium wildpretti, D. vaccinum, Licea succulenticola, Physarum spectabile, Trichia agaves, found in other desert areas have re-appeared. There are many
species that do not seem to have such a narrow specificity for substrate, and are found on a large variety of
plants, as can be seen with Arcyria cinerea, Didymium
squamulosum, Perichaena vermicularis or Physarum
pusillum, obviously responding to a general number of
conditions common to those microhabitats. It is interesting to note, as mentioned above, that where there
were different plant species within similar habitats,
studied in a similar manner, genus Didymium had only
17% of the species in common.
The myxomycetes found in the Monte Desert represent 8% of the number of species known worldwide, confirming an unexpected species richness of the
area. Their colonization and ability to live in such arid
environments demonstrate the importance of the resistant stages in their life cycle, where three different
life stages, microcysts, sclerotia and spores, increase
their ability to survive the extreme adverse environmental conditions of this dryland ecosystem. In the
sampling for this survey, both in the field and in culturing by moist chamber, as mentioned above, sclerotia
94
C. Lado & al.
were very common, attesting to their importance as
resistant stages. Some of these sclerotia collected from
the field were placed on agar and produced viable
plasmodia. If the fact that myxomycetes require water, at least for their feeding stages as amoebae or plasmodia, a desert could be considered a totally hostile
and impossible place for their development, but these
results, showing an unexpectedly high biodiversity of
myxomycetes, refute this assumption.
Acknowledgements
This research was supported by the Ministry of Science and Innovation, Spain (projects CGL2005-00320/BOS and CGL200800720/BOS). We are grateful to Laura Lorenzo, Comahue University, Argentina, for logistical help and the personnel of the Parques Nacionales de Argentina, and the Parque Natural Provincial
Ischigualasto, for help and permission to collect. We also thank
Yolanda Ruiz for her technical assistance with SEM and Carlos de
Mier for his help with the light photomicrographs.
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Associate Editor: J. Guarro
Received: 27-VII-2010
Accepted: 16-II-2011
2276_Artemisa:Anales 68(1).qxd 13/06/2011 12:22 Página 97
Vol. 68(1): 97-105
enero-julio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2276
Self-incompatibility, floral parameters, and pollen
characterization in the narrow endemic and threatened
species Artemisia granatensis (Asteraceae)
by
Julio Peñas1, Juan Lorite1, Francisca Alba-Sánchez1 & María Angélica Taisma2
2
1
Plant Conservation Unit, Department of Botany, University of Granada, E-18071 Granada, Spain. [email protected]
Instituto de Biología Experimental, Centro de Botánica Tropical, Universidad Central de Venezuela, Caracas, Venezuela
Abstract
Resumen
Peñas, J., Lorite, J., Alba-Sánchez, F. & Taisma, M.A. 2011. Selfincompatibility, floral parameters, and pollen characterization in
the narrow endemic and threatened species Artemisia granatensis (Asteraceae). Anales Jard. Bot. Madrid 68(1): 97-105.
Peñas, J., Lorite, J., Alba-Sánchez, F. & Taisma, M.A. 2011. Autoincompatibilidad, parámetros florales y caracterización de polen
en la especie endémica y amenazada Artemisia granatensis (Asteraceae). Anales Jard. Bot. Madrid 68(1): 97-105 (en inglés).
Artemisia granatensis Boiss. is a paradigmatic species for plant
conservation in Spain and Europe. It is a critically endangered (CR)
endemic species growing above 2500 m in the Sierra Nevada
(southern Spain). Natural populations have been considerably
devastated in the past due to intensive human exploitation for folk
medicine. The sparse available data concerning the reproductive
biology of this species under natural conditions indicate a low reproductive success. To provide additional information on the reproductive biology of A. granatensis, and consequently information useful for the management and conservation of this species,
we studied the breeding system through pollen-tube growth. In
addition, some floral and pollen traits were recorded. No differences were found between populations in terms of the morphological traits of flowers and inflorescences. A. granatensis is an
anemophilous species, and the data indicate that pollen transfer
may be limited between isolated populations, and so contributing
to an extremely low fruit-set. Results show A. granatensis is selfincompatible, probably with a sporophytic self-incompatibility system, and with no evidence of partial self-incompatibility. Reproductive traits, related to pollen morphology and settling speed
may explain the low rate of recruitment in the small populations
separated by geographical barriers.
Artemisia granatensis Boiss. es una especie paradigmática en la
conservación de flora a nivel español y europeo. Es una especie
catalogada como En Peligro Crítico (CR) endémica de Sierra Nevada (sur de España), donde habita por encima de los 2500 m. Las
poblaciones naturales han sido casi exterminadas en el pasado debido a una recolección masiva de la especie, utilizada en medicina
popular. Los escasos datos disponibles acerca de su biología reproductiva en condiciones naturales indican que existe un bajo
éxito reproductivo. Con el objetivo de proporcionar información
adicional acerca de la biología reproductiva de A. granatensis, útil
para la conservación y el manejo de la especie, evaluamos el sistema de compatibilidad a través del crecimiento del tubo polínico.
Además se registraron datos sobre algunos rasgos florales y polínicos de la especie. No se encontraron diferencias entre poblaciones en términos de rasgos morfológicos de flores e inflorescencias. A. granatensis es una especie anemófila para la cual los datos
obtenidos sobre capacidad de dispersión sugieren que la transferencia de polen podría ser difícil entre poblaciones aisladas o
muy distanciadas, pudiendo ser un factor más a tener en cuenta entre las causas que provocan un limitado éxito reproductivo
y una paupérrima producción de semillas. Los resultados muestran que A. granatensis tiene autoincompatibilidad esporofítica
sin evidencias de autoincompatibilidad parcial. Los rasgos reproductivos relacionados con la morfología y la velocidad de sedimentación del polen pueden explicar la baja tasa de reclutamiento de poblaciones pequeñas, a veces separadas por barreras
geográficas.
Keywords: reproductive biology, pollen-tube growth, endemic
and threatened species, conservation.
Palabras clave: biología reproductiva, crecimiento del tubo polínico, especie endémica y amenazada, conservación.
98
J. Peñas & al.
Introduction
The southern area of the Iberian Peninsula has long
been recognized as a centre of plant diversity and endemicity (Molero, 1994; Domínguez & al., 1996;
Peñas & al., 2005), and a “phytogeographical
hotspot”; that is, significant reservoirs of unique genetic diversity favourable to the evolutionary processes of Mediterranean plant species (Médail & Diadema, 2009). The largest number of endemic plant
species, and indeed one of the largest in Europe, is
found in Sierra Nevada (Blanca & al., 1998). This
mountain harbours the narrow endemic Artemisia
granatensis Boiss. (Asteraceae), a paradigmatic species
for the plant conservation in Spain and Europe (Council Directive 92/43/EEC; Fay, 1992), since it was included in the first Spanish catalogue of threatened
species (BOE, 1990). Today, this species is considered
critically endangered (CR) in the latest national
(Moreno, 2008) and regional (Cabezudo & al., 2005)
list of threatened species, with the main threats being
overgrazing and collection for folk medicine. Estimates of population sizes suggest that about 3000 individuals of the species survive (Blanca & al., 1998), distributed in 12 populations (Blanca, 2002).
Habitat fragmentation leading to small isolated
populations may be the most apparent cause for reproductive failure and species loss (Koul & Bhatnagar, 2007). Up to the present, the efforts to recover
natural populations of A. granatensis have not been
based on a knowledge of the reproductive biology of
natural populations. Furthermore, the difficult access
to the small and distant populations of A. granatensis
has constrained reproductive studies in situ. However, field studies on reproductive traits, compatibility
systems, and pollination mechanisms are necessary to
define conservation strategies for the species. Reproductive-biology studies, thus, should be an integral
feature of any conservation project (Weller, 1994;
Weekly & Race, 2001; Koul & Bhatnagar, 2007).
Self-incompatibility, a genetic barrier to prevent inbreeding that is broadly distributed among angiosperms, could be a main constraint against reproductive success in A. granatensis because in selfincompatible species there may be a loss of genetic
diversity among individuals in fragmented and scattered populations that dooms such isolated populations to extinction (Weller, 1994). Since A. granatensis, belonging to Asteraceae, a family with selfincompatible established in around 40 genera
(Charlesworth, 1985), and with some reports on partial self-incompatibility (Ortiz & al., 2006), could have
a self-incompatibility system which has not previously
been tested.
Some studies have related self-incompatibility systems to floral and inflorescence size (Gibbs & al.,
1975; Ortiz & al., 2006). For example, in the genus
Hypochaeris L. partial self-compatible heads are larger than self-incompatible heads (Ortiz & al., 2006).
Thus, the evaluation of a self-incompatibility system
must include the flower and inflorescence morphology in order to gain a full understanding of the reproductive potential.
Artemisia is known to be an anemophilous genus
(O’Brien, 1980; Watson & al., 2002), and ecological
characteristics of in A. granatensis populations could
hamper the transfer of pollen between distant populations due to geographical barriers. Currently we have
no data about the potential A. granatensis pollen
movement in the atmosphere. To help fill this gap,
theoretical data on the settling speed and residence
time in are presented. This information was obtained
based on some morphological pollen features. Data
about some physical properties of the A. granatensis
pollen are important building blocks in a model of its
pollen movement and, as such, later will be helpful in
establishing the main factors influencing the dispersion degree of pollen between A. granatensis populations. Consequently, the settling speed of this pollen is
fundamental for determining the distance that this
particle can be transported in the atmosphere as well
as its probability of being deposited on the plants or
on the ground (Aylor & al., 2005).
The aim of the study is provide information on the
reproductive biology of A. granatensis, in relation to
pollen features and breeding system, useful for the
management and conservation of this species. For this
propose, the present study i) characterizes the basic
pollen morphological and functional parameters and
compares floral morphology within and between
populations, and ii) evaluates the operation presence
of a self-incompatibility system by means of hand pollinations and pollen-tube growth.
Study area and selected sites
Sierra Nevada, a mountain range of some 2,100 km2
located in SE Spain (37ºN, 3ºW), has a complex orography, bedrock, and soil composition (e.g. areas with
dolomitic soils), and reaches a height of 3482 m. This
massif marks the southernmost limit of the influence
of the Quaternary glaciations in Europe, when this
mountain range was covered with glaciers in areas
above around 2,500 m while large areas remained free
of permanent ice (Gómez & al., 2001). All these features have contributed to make the Sierra Nevada a
Artemisia granatensis
refuge for many plant species during glacial ages
(Blanca & al., 1998), thus harbouring isolated populations that have evolved under particular conditions (e.g. soil type or isolated summit areas), and
which have encouraged speciation and a high level of
endemicity (Blondel & Aronson, 1999; Peñas & al.,
2005; Thompson, 2005). In fact, the area above
2,000 m contains about 100 endemic or rare taxa.
Many of these species are threatened by different factors (Blanca & al., 1998; Bañares & al., 2003), with
38 taxa included on the regional protection list (Blanca & al., 1999). Today most of this entire area lies
within National and/or Natural parks. Climatic conditions are typically alpine (with a Mediterranean
character), with mean temperatures below 0 °C during winter months and snow cover that can persist up
to 8 months in the highest places (occasionally up to
10 months in small, protected areas). See Gómez
(2002) for a detailed description of climatic conditions in Sierra Nevada range.
Two populations of A. granatensis were selected in
the summit area of the Sierra Nevada. The first (AG1
hereafter), at 2790 m on the northern slope, included
45 mature individuals, and the second (AG2 hereafter), at 3045 m on the southern slope, had 55 mature
individuals. In both cases there are no other patches
or isolated individuals in the surroundings (at least
300 m around). The populations were c. 6 km apart.
Because of the difficult access to the populations, the
low number of individuals per population, and the
use of a semi-extractive sampling design, we limited
the sampling effort to the minimum necessary to allow
the statistical analysis of the data.
Studied species
Artemisia granatensis Boiss. belongs to the large
family of Asteraceae. Artemisia is the largest genus in
the tribe Anthemideae and one of the largest in the
family, with over 500 species (Martin & al., 2001).
Taxonomically, A. granatensis is closely related to other alpine species such as A. splendens Willd. and A.
umbelliformis Lam. (Watson & al., 2002), and it occasionally forms a hybrid, A. × fragosoana Font Quer
(Blanca, 2002) with the latter. A. granatensis is a longlived perennial herb, caespitose and white-sericeous,
with stems 5-12 cm long, erect, simple or scarcely
branched. Basal leaves are numerous, petiolate, divided with segments of flabellate outline. Flowers are
arranged in terminal discoid capitula of 5-8 mm in
diameter, with 1-5 capitula per stem. The capitula
have external flowers female and internal ones hermaphrodite, being a gynomonoecious species. Flowers are actinomorphic, tubulose, dark purple in
99
colour, with a papillose stigma. Flowering ranges
from July to August and fruit ripening (small achene)
occur in September. Although information concerning the breeding system of the species is scant, A.
granatensis is known to be an anemophyilous species
(e.g. Blanca & al., 1999).
A. granatensis appears in perennial high-mountain
pastures on mica-schists, from 2500 m to the highest
peaks (above 3400 m). Traditionally, the main threat
has been the harvest of complete individuals for medicinal purposes; also ungulates (wild and domestic
ones) browse a large percentage of the reproductive
stems, despite the production of sesquiterpenes that
make the foliage bitter (Watson & al., 2002). The result of these pressures is a major decrease in seed set
(decreasing 20-90 % of the total seed set, depending
on the population; author’s unpublished data).
Inflorescence and flower morphological data
A total of 18 mature inflorescences (heads/capitula)
were randomly collected from each population (AG1
and AG2). The heads were dissected under a bifocal
magnifying glass and the number of female and hermaphrodite flowers per capitulum was counted. A
subsample of 25 mature hermaphrodite flowers were
randomly taken from these 18 inflorescences, and stamen, ovary and style length were measured using a
digital calliper (± 0.001). Data were analysed by means
of one-way ANOVA.
Pollen morphological analysis
and settling speed
Samples of 30 anthers (15 per population) from 30
individuals were randomly selected and collected before anthesis and acetolysed using the method of
Erdtman (1960) as modified by Hideux (1972), and
then mounted in glycer-gelatin for light microscopy.
The pollen terminology used is based on Punt & al.
(2007). For scanning electron microscopy (SEM),
non-acetolysed grains were dehydrated in an alcohol
series, pipetted onto a SEM stub in a few drops of
100% alcohol, and allowed to dry. Samples were coated with gold/palladium and examined using a SEMmicroscopy. In parallel, the principal features of individual pollen grains (emphasizing diameters i.e. polar
axis and equatorial diameter) were measured using a
light microscope at a magnification of 400× in order
to determinate their characteristic dimensions and
shapes. Then, the diameters measures (i.e. the major
and minor diameters P and E) were used to calculate
the volume-equivalent sphere of the pollen grain given by 3PE2. Taking into account the latter measure
both the “theoretical settling speed” (Fuchs, 1964;
100
J. Peñas & al.
Leith, 1987), as well as, the “theoretical residence
time” of A. granatensis pollen (see Chatigny & al.
(1979) for further information about residence times
estimation) assuming dry deposition were calculate.
The settling speed (Vt) of a pollen grain falling in
still air at a constant temperature and pressure is described by Fuchs (1964). Taking into account the volume-equivalent diameter (d) of the pollen grains, the Vt
of Artemisia pollen was calculated based on Stokes’
Law for a sphere (in the absence of electrostatic
forces). This equation calculates the settling speed as a
function of particle size, particle density, acceleration
due to gravity, and the density and viscosity of the air.
Stokes’ Law Equations: solving for settling speed or
terminal velocity
gd2(ρp - ρm)
18µ
Inputs: acceleration of gravity (g); particle diameter
(d); density of particle (ρp); density of medium (ρm);
viscosity of medium (µ).
Vt =
Pollen-tube growth and compatibility system
Pollinations were achieved by rubbing a dissection
needle against the anthers of pollen-bearing flowers
and then against the stigmas of outer female flowers of
the same head (self-crosses, SC) or the female flowers
in the head of a different individual in the same population (intra-population outcrosses, IPC) or against
those of a different head in the other population (AG1
and AG2) i.e. inter-population outcrosses (InPC). All
hand-pollinated heads were bagged with cellophane
bags. Some naturally pollinated heads (no hand-pollinated, and no bagged) were collected to measure
natural tube growth (no hand-pollinated NP).
Prior to hand pollination stylar arms were observed
with a magnifying glass to ensure that the arms were
fully expanded (mature) and had no pollen on them.
We collected five capitula per population and placed
individually in cellophane bags in order to use as
donors in the inter-population outcrosses (lnPC), the
time passed between collection and hand-pollination
was two to three hours, roughly.
Afterwards all hand-pollinated (SC, IPC, InPC)
flowers were collected (24h-48 h after) and fixed in
70% ethanol. After rinsing in distilled water, isolated
gynoecia were softened and cleared in 8 mol/l NaOH
for 48-72 h. Softened gynoecia were placed in distilled
water for at least 1 hour before staining with a 0.1%
solution of aniline blue in 0.1 mol/L K3PO4 for 12 h
(as described in Martin, 1959). Each gynoecium was
examined under UV light (range 360-390 nm for selective excitation of DAPI fluorescence) to observe
tube growth.
Pollen-tube growth was observed of selfs and crosses at the stigma, and along the style. Pollinations were
classified as SI or SC based on whether pollen tubes
reached the base of the style or not. Pollen-tube growth
was compared using the non-parametric X2 test.
Results
Floral morphology (Table 1)
Artemisia granatensis capitula had around 80 flowers each. Heads from plants in AG1 and AG2 populations showed no differences in hermaphrodite and
female flower number. There were no significant
differences in total flowers/head, hermaphrodite
flowers/heads, female flowers/head and natural fruitset/head between populations, although the natural
fruit:flower ratio was higher in AG2. We found no differences between morphological traits of reproductive structures between AG1 and AG2 (Table 2) with
the exception of mature stamen length, which was
higher for AG2 flowers (Table 2).
Table 1. Mean (SD) of inflorescence traits gathered from Artemisia granatensis populations (AG1 and AG2) (n = 18 inflorescences).
AG1
AG2
F-ratio
P
Total flowers/ head
74.0 (19.1)
83.1 (30.3)
F (1, 35) = 0.877
0.356 n.s.
Hermaphrodite flowers/ head
70.7 (18.1)
74.2 (30.5)
F (1, 35) = 0.701
0.408 n.s.
Female flowers/ head
5.4 (3.7)
6.8 (3.7)
F (1, 35) = 0.573
0.454 n.s.
Fruits/ head
0.4 (2.2)
2.1 (1.0)
F (1, 35) = 4.108
0.051 n.s.
0
2.29%
Fruit:flower ratio
Mean (SD) values for floral traits and fruit set of n.s.: not significant.
101
Table 2. Mean (SD) values of female and male floral traits of Artemisia granatensis flowers at AG1 and AG2 populations (n = 25).
AG1
AG2
Anova Results F
P
Ovary length (mm)
0.88 (0.12)
0.87 (0.09)
F (1,405) = 0.330
0.569 n.s.
Style length (mm)
1.50 (0.32)
1.59 (0.26)
F (1,405) = 1.091
0.302 n.s.
Style arms length (mm)
0.74 (0.12)
0.77 (0.12)
F (1,405) = 0.277
0.601 n.s.
Stamen length (mm)
2.12 (0.16)
2.35 (0.23)
F (1,405) = 5.447
0.035 *
Mean (SD) values for floral traits of * = significant, n.s.: no significant.
Pollen morphology and settling speed
A. granatensis pollen has the typical anemophilous
syndrome, based on morphological features and settling speed. It is isopolar, with radial symmetry. In polar view it is circular-lobate (Fig. 1a), and in equatorial view it is circular-elliptical (Fig. 1b). It is spheroidal
or prolate-spheroidal, with a P:E ratio of 1.0, small to
medium in size, the length of the polar axis (P) being
18-20 (19.2 ± 0.8) µm and the equatorial diameter (E)
being 17-22 (19.3 ± 1.3) µm. The pollen grain is trizonocolporate, fossaperturate. The ectoaperture is a
colpus 12-16 (13.7 ± 1.6) µm long; the endoaperture
is a circular or lalongate porous 1.5-3 (1.9 ± 0.5) µm
long. The surface relief of the pollen grain is microechinate, ornamentation of spines shorter than
1 µm, (c. 0.7 µm), showing delicate verrucate surface
sculpturing, broader than high and less than 1 µm in
diameter (around 0.24 µm).
The resulting volume-equivalent diameter of A.
granatensis pollen is c. 19.3 µm. Known this measure
and under the assumption of a dry deposition as well
as a density of 1 g/cm3, the theoretical settling speed
or terminal velocity (Vt) was calculated at around 1.18
cm/s (or 42.48 m/h); taking into account the above
parameter, the resulting theoretical residence time in
the atmosphere was 0.6 days (c. 14 h).
AG2 plants (Fig. 2), signifying a rejection of self pollination and sporophytic self-incompatibility. The X2
test showed that SC produced a significantly lower
a
b
Pollen-tube growth and compatibility system
Self-incompatibility was determined based on
pollen-tube growth inhibition. The inhibition of incompatible pollen occurred at the stigma surface,
where grains either failed to germinate, or the emerging pollen tube was usually inhibited before penetrating the stigma surface. Compatible pollen grains
produced pollen tubes growing through the style. Viability tests showing full fluorochromatic reaction
demonstrated that A. granatensis pollen collected
from populations AG1 and AG2 was viable.
Self crosses (SC) produced failed to germinate,
or did not penetrate in the stigma both for AG1 and
Fig. 1. View of Artemisia granatensis pollen grain (SEM microscopy). a, whole grain: polar view showing three apertures; b,
whole grain: meridional view showing two apertures and details of spines.
102
J. Peñas & al.
Discussion
No-growth
pollen-tube
Fig. 2. Inhibition of pollen tube at the stigmas of Artemisia granatensis for a SC cross in AG2.
number of gynoecia with pollen tubes than did IPC in
both AG1 and AG2 (Table 3).
The number of gynoecia with pollen tubes was
higher for IPC than for SC in both AG1 and AG2.
(Table 3; Fig.3). The X2 test for the comparison of NP
and IPC in AG1 and AG2 showed no significant differences with respect to the number of gynoecia with
pollen tubes (Table 3). InPC showed a high number of
gynoecia with pollen tubes (Table 3; Fig. 4) and also a
higher number of gynoecia with pollen tubes than NP
in both AG1 and AG2 (Table 3).
Artemisia granatensis, as with many Asteraceae, has
a gynomonoecious sexual system, in which female and
bisexual flowers occur in the same inflorescence (capitulum). The isolated A. granatensis populations
studied showed no significant differences between
morphological traits. Flower number per head and
the ratio of hermaphrodite to female flowers showed
no differences between AG1 and AG2. Additionally,
stamen, ovary, and style sizes were comparable. Previous reports in some Asteraceae showed that flowersize differences could be related to the loss of self-incompatibility in small populations (Ortiz & al., 2006),
and this trend has also been found for another selfincompatible species in fragmented habitats (Taisma
& Varela, 2005). Our results indicate that AG1 and
AG2 plants have no morphological differences and,
therefore, these traits could not be related to differential self-incompatibility expression.
Pollen-tube growth after controlled hand pollination in natural populations of A. granatensis showed
that the species has a sporophytic self-incompatibility
system with no evidence of increased self-incompatibility or partial-self incompatibility as has been found
in small, isolated and peripheral populations (Fausto
& al., 2001; Vallejo-Marin & Uyenoyama, 2004; Taisma & Varela, 2005). These results agree with findings
for other members of Asteraceae and suggest that, although population size is small and isolation is high,
there is no breakdown of the self-incompatibility system. These data support the idea that the main constraint on reproductive success in A. granatensis under
natural conditions (Fig. 5) is the reduced number of
compatible mates due to failure in wind pollination.
Table 3. Results of pollination treatments in Artemisia granatensis individuals in populations AG1 and AG2.
Cross Type
AG1
AG2
n
Number of gynoecia
with growing tubes
Number of gynoecia
without growing tubes
X2 critical value
(1gl; p < 0.01 = 6.63)
SC
72
0
72
SC vs. IPC = 77.88 *
IPC
6
6
0
InPC
66
56
10
SC vs. InPC = 11.25 *
NP
29
8
21
InPC vs. NP = 2.03 n.s.
SC
122
0
122
SC vs. IPC = 20.69 *
IPC
104
26
78
InPC
48
16
32
SC vs. InPC = 33.49 *
NP
48
7
41
InPC vs. NP = 4.62 n.s.
SC = self crosses, IPC = intra-population outcrosses, InPC = inter-population outcrosses, NP = no hand-pollinated, natural tube growth; n.s.: not significant.
103
Stigma
Style
Pollen
tubes
Pollen tubes
Stylar
arm
Fig. 3. Growing pollen tubes at the style after a IPC cross in
AG1.
Fragmentation of wind-pollinated populations seriously reduces pollen availability, limiting reproduction (Knapp & al., 2001). Davis & al. (2004) found 9fold more pollen on stigmas of high-density Spartina
alterniflora plants than on those occurring at low density; they also found that the consequences of loss of
appreciable numbers of seed caused by pollen limitation persists for decades.
The low natural fruit set of A. granatensis (Hernández-Bermejo & al., 2003) and the low number of gynoecia with viable pollen tubes after NP (natural tube
growth) agree with the expected reduced seed-set in
small populations of self-incompatible, wind-pollinated species (Widen, 1993, Lienert & Fisher, 2003;
Davis & al., 2004). A critical event for A. granatensis reproduction could be pollen deposition, because this species is self-incompatible in very small isolated populations, and thus compatible pollen flow
could be a critically limiting condition for fruit set. In
this sense, further studies addressing pollen limitation
in relation with population size and isolation are
needed.
Fig. 4. Growing pollen tubes at the stigma, stylar arms and style after a InPC cross in AG2.
Transport and dispersal of pollen grains by the
moving atmosphere as well as their residence time as
airborne particles are strongly linked to physical atmospheric characteristics at their time of flight (Comtois & al., 2000). The settling speed and residence
time estimated for A. granatensis pollen can vary greatly in nature (Sierra Nevada) owing to turbulence and
atmospheric humidity, which can alter the density of
biological particles (Aylor, 2002); including topographic barriers against pollen displacement. However, a cornerstone parameter in any future model of
pollen transport in the atmosphere is calculating the
gravitational settling speed in still air, Vt, of individual
pollen grains, because Vt largely determines both the
distance of travel and the efficiency of deposition on
target organs (Aylor & al., 2005). According to Kohler
& al. (2007) this theoretical information is an essential
parameter for reliably modelling the atmospheric
dispersal of pollen in situ. Despite this, very little is
104
J. Peñas & al.
Stigma
Pollen tubes
Style
required for acquiring a thorough knowledge the reproductive biology and pollination ecology in the case
of A. granatensis.
In any case, it seems obvious that A. granatensis reproductive efficiency has been critically affected by
the devastation of natural population due to human
use. Current population size and plant densities may
be a serious limitation to guarantee enough pollen
from compatible mates. Additionally, present populations are isolated by major geographic barriers that
could also seriously limit compatible pollen flow between populations. Programmes for the recovery of
A. granatensis may need to include reintroduction of
compatible mates in order to enhance pollen flow and
fruit-set efficiency by means of connecting isolated
patches.
Acknowledgements
Fig. 5. Growing pollen tubes at the stigma and style level after
NP in AG2.
known about A. granatensis pollen mobility in the atmosphere. As far as we know, this study is the first to
determine physical characteristics of A. granatensis
pollen, which can contribute to defining the main
parameters involved in reproductive biology in this
species. The model equations for settling speed presented here offers a means for evaluating dispersal potential for a range of environmental conditions.
Our results suggest the potential distance that A.
granatensis pollen can be transported during the estimated residence time (14 h) was 600 m. According to
Mandrioli (1998) small or medium particles, such as
A. granatensis pollen, have a relatively long or medium residence time in the atmosphere, supporting the
hypothesis of intra- and inter-populational pollination
success. Nevertheless, natural pollen-tube growth
suggests a pollen-deposition limitation, probably related to the viability and longevity of pollen grain as
well as pollen dispersion capacity, both intimately
linked to the likelihood of reproductive success (Mandrioli, 1998). These facts suggest that the reproductive success depends on the time spent by the viable
pollen grain to reach the nearest population and the
inter-population range. Obviously, further details
about pollen flow within and between populations is
We wish to thank E. Rico (University of Salamanca) for valuable comments on the manuscript, and we thank B. Forot, B. Benito and C. Ruiz Rejón (University of Granada) for their contribution in the field and laboratory work. The authors are indebted to
David Nesbitt for linguistic advice. This work has been partly financed by the Spanish Education and Science Ministry (project
reference REN2003-09427-C02), and partly by the Consejería de
Innovación, Ciencia y Tecnología de la Junta de Andalucía (project reference P05-RNM1067). Science Faculty of Universidad
Central de Venezuela supported Dra. Taisma’s research at the
University of Granada.
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Associate Editor: C. Herrera
Received: 10-XI-2010
2245_Baccharis:Anales 68(1).qxd 13/06/2011 12:14 Página 107
Vol. 68(1): 107-116
enero-julio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2245
Microsculpture of cypselae surface of Baccharis sect.
Caulopterae (Asteraceae) from Brazil
by
Angelo Alberto Schneider & Ilsi Iob Boldrini
Programa de Pós-Graduação em Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul,
Campus do Vale, prédio 43433, 91501-970, Porto Alegre, Rio Grande do Sul, Brazil
Corresponding author: [email protected]
Abstract
Resumen
Schneider, A.A. & Boldrini, I.I. 2011. Microsculpture of cypselae
surface of Baccharis sect. Caulopterae (Asteraceae) from Brazil.
Anales Jard. Bot. Madrid 68(1): 107-116.
Schneider, A.A. & Boldrini, I.I. 2011. Microescultura de la superficie de las cipselas de Baccharis sect. Caulopterae (Asteraceae)
de Brasil. Anales Jard. Bot. Madrid 68(1): 107-116 (en inglés).
The aim of this study was to characterize the microsculpture of
the cypselae surface of the Brazilian species of Baccharis L. sect.
Caulopterae DC. (Asteraceae), and to compare this data it with
the taxonomy of the group. Scanning electron microscopy was
used to examine the cypsela surface of 25 taxa of Baccharis sect.
Caulopterae from Brazil. According to the micromorphology of
the cypsela surface, the species can be classified into five distinct
groups. The cypselae of the species of the Baccharis trimera
species complex (B. crispa, B. cylindrica, B. jocheniana, B. myriocephala, and B. trimera) share the same micromorphological
features.
Para examinar la superficie de cipselas de 25 táxones de Baccharis L. sect. Caulopterae DC. de Brasil se ha utilizado la microscopía electrónica de barrido. El objetivo del estudio fue caracterizar la microescultura de la superficie de cipselas de la sección y colaborar con la delimitación taxonómica a nivel específico. Las especies fueron clasificadas en cinco grupos distintos
según la micromorfología y asignados a la terminología existente. El complejo Baccharis trimera (B. crispa, B. cylindrica,
B. jocheniana, B. myriocephala y B. trimera) mostró afinidades
micromorfológicas de las cipselas.
Keywords: achene, carpology, carqueja, Compositae, micromorphology, SEM, taxonomy.
Palabras clave: aquenio, carpología, carqueja, Compositae,
MEB, micromorfología, taxonomía.
Introduction
fraspecific taxa included in the section is variable in
the literature, especially due to different taxonomic
concepts (Heiden & al., 2009). The section is restricted to South America, occurring extensively in the
Andes, from Colombia to the Central Argentina, and
in Brazil, where the highest number of species in this
section is concentrated in the south and southwest
(Barroso, 1976; Müller, 2006).
Velez (1981) studied the American genera of Astereae and provided a detailed overview of cypsela morphology and anatomy in the genus Baccharis. Other
studies that have contributed to our knowledge of
cypsela morphology in this genus are Ariza (1973),
Hellwig (1990), Mukherjee & Sarkar (2001) and
Müller (2006). The latter author reviewed cypsela
characteristics for the genus, and present data with re-
The fruits of the Asteraceae, denominated cypselae, are dry, indehiscent, unilocular, with a single seed
that is usually not adnate to the pericarp (linked only
by the funicle) and originating from an inferior ovary
(Marzinek & al., 2008). The pappus, a modified calyx,
is inserted in the apical region of the cypsela, whilst
basally, an abscission region is located in relation to
the inflorescence axis (clinanthium) denominated the
carpopodium (Roth, 1977). Cypsela microsculpture
analysis has been considered more and more a taxonomic tool, being also important for higher and medium level classification within the family (Bremer,
1994; Anderberg, 1991).
Baccharis sect. Caulopterae is represented by
around 35 species, but the number of species and in-
108
A.A. Scheneider & I.I. Boldrini
gard to form, shape, colour, indumentum, number of
vascular bundles encircling the fruits (ribs), details of
the pericarp, and some general considerations concerning microsculpture of the cypsela cuticle.
Here we characterize the microsculpture of the
cypselae surface of the Brazilian species of genus Baccharis sect. Caulopterae, and we were particularly interested to see if cypsela characters could help resolve
the taxonomy of the B. trimera complex, comprising
B. crispa, B. cylindrica, B. jocheniana, B. myriocephala,
and B. trimera (Barroso 1976)".
Scanning Electron Microscopy
Mature cypselae of 25 Brazilian species of Baccharis
sect. Caulopterae were collected from herbarium
specimens (HBR, ICN, PACA and UEC - see Table 1).
One representative dry cypsela was then selected per
species and mounted on a metallic stub using a carbon adhesive tape and sputter-coated with 20 nm gold
using BAL-TEC SCD-050. Electromicrographs of the
cypselae were obtained under 10 kV in magnification
using a Scanning Electron Microscope (SEM) JEOLJSM 6060 at the Centro de Microscopia Eletrônica
(CME) of the Universidade Federal do Rio Grande
do Sul.
Analyses and terminology
The characters we recorded were based on analyses
of morphology of the secondary and tertiary sculpture
of the surface morphology: smooth or folded, presence or absence of papillae, degree of surface rugosity
and presence of cavities. The primary sculpture was
not examined since in most species it was lacking. The
terminology used for cypselae shape (solid structure)
follows Radford (1986), and microsculpture characterization was based on Barthlott (1981; 1990),
Mukherjee & Sarkar (2001) and Müller (2006).
Baccharis burchellii Baker and B. regnellii Sch. Bip.
ex Baker, although belonging to Baccharis sect. Caulopterae and occurring in Brazil were not included in
this study because we could not obtain material with
mature cypselae.
The nomenclature of species follows recent works,
and the following names were considered: B. pentaptera (Less.) DC. (=B. stenocephala Baker, according to Schneider & al., 2009), B. sagittalis (Less.) DC.
(=B. heeringiana Malag., =B. macroptera D.J.N.
Hind), B. subtropicalis Heiden (=B. sagittalis var.
montevidensis Baker), and B. junciformis (Less.) DC.
(=B. usterii Heering, all according to Heiden & al.,
2009). For species belonging to the Baccharis trimera
species complex (B. crispa Spreng., B. cylindrica
(Less.) DC., B. myriocephala DC. and B. trimera
(Less.) DC.) we followed the circumscription proposed by Barroso (1976).
Results
The cypselae of Baccharis sect. Caulopterae can be
divided into three groups with regard to the number
of ribs: 18 species with 5-7 ribs; six with ~14 ribs (B.
crispa, B. cylindrica, B. jocheniana, B. myriocephala, B.
aff. opuntioides, B. trimera); one species with ~20 ribs
(B. riograndensis). Cypsela shape varies from narrowly oblong, narrowly oblong to cylindric, narrowly oblong to obovoid, oblanceoloid, oblong and obovoid
form (Table 1).
The cypselae surface presents a variable microsculpture, mostly with a folded cuticle, but also rugose with the presence of cavities in two species: B. articulata and B. glaziovii. Most species are papillose
with digitiform (B. trimera) or globose papillae (B. articulata and B. sagittalis), with length ranging from 220 µm by 2-5.5 µm in diameter, with variable distribution on the cypselae surface but they are longer on the
vascular bundles (ribs). B. heeringiana, B. pseudovillosa, B. ramboi, B. riograndensis, B. stenocephala, B. usterii and B. vincifolia did not present papillae. A ringshaped carpopodium was observed in all species, and
its diameter ranges from 50-120 µm. The SEM study
of the cypselae provided important characters which
allowed us to distinguish five groups among the sampled species.
GROUP I. Papillose rugose cypselae
In this group, the cypselae present an evenly distributed rugose surface with digitiform papillae. The
papillae are longer on the ribs. Carpopodium present,
ring-shaped, 90-120 µm diameter. Ribs 5-7. Two
species: B. microcephala (Fig. 1A-D) and B. penningtonii (Fig. 1E-H).
GROUP II. Epapillose rugose cypselae
Cypselae present a rugose surface, but papillae are
absent, or just relictual and slightly salient on the ribs.
Cypsela surface slightly folded and with delicate and
irregular rugosities. Carpopodium present, ringshaped, 80-110 µm diameter. Ribs 5-7. Five species:
B. palustris (Fig. 2A-D), B. paranensis (Fig. 2E-H),
B. pseudovillosa (Fig. 2I-L), B. ramboi (Fig. 2M-P) and
B. vincifolia (Fig. 2Q-T).
Microsculpture of cypselae of Baccharis
109
Table 1. Relation of studied species and some characters analyzed with respective vouchers: length (L), diameter (D); approximate (~).
Taxon
Shape
Size ~(length ×
L/D
Ribs (~)
Source
width, mm)
B. apicifoliosa A.A.Schneid. & Boldrini
oblanceloid
1.29 × 0.41
3/1
7
R. Wasum 802 (PACA)
obovoid
0.74 × 0.38
2/1
5
L.A. Mentz s.n. (ICN 59169)
B. crispa Spreng.
narrowly oblong
1.27 × 0.38
3/1
14
I. Fernandes 641 (ICN)
B. cylindrica (Less.) DC.
narrowly oblong
1.38 × 0.32
4/1
14
R. Schmidt s.n (ICN 153106)
B. flexuosiramosa A.A.Schneid.
& Boldrini
narrowly oblong
1.37 × 0.46
3/1
7
C.F. Jurinitz s.n. (ICN 153107)
B. glaziovii Baker
narrowly oblong
1.02 × 0.37
3/1
5
J. Mattos 15953 ( UEC)
B. jocheniana G. Heiden & L. Macias
narrowly oblong
1.24 × 0.37
3/1
14
B. junciformis (Less.) DC.
narrowly oblong
1.12 × 0.32
4/1
5
K.D. Barreto & G.D.
Fernandes 752 (ESA)
B. microcephala (Less.) DC.
narrowly oblong
1.27 × 0.40
3/1
7
J. Dutra 1488 (ICN)
B. milleflora (Less.) DC.
narrowly oblong
1.28 × 0.42
3/1
7
B. Rambo 49318 (PACA)
B. myriocephala DC.
narrowly oblong
1.16 × 0.29
4/1
14
A.A. Schneider 1161 (ICN)
B. aff. opuntioides Mart. ex Baker
narrowly oblong
1.40 × 0.38
4/1
14
B. organnensis Baker
narrowly oblong
1.26 × 0.34
4/1
7
A. Sehnem 5119 (PACA)
B. palustris Heering
narrowly oblong
1.14 × 0.43
3/1
7
B. Rambo 52024 (HBR)
B. paranensis Dusén
narrowly oblong
1.46 × 0.34
4/1
7
J. Iganci 507 (ICN)
B. penningtonii Heering
narrowly oblong
1.00 × 0.31
3/1
7
J.C. Sacco 808 (PACA)
B. pentaptera (Less.) DC.
oblong
1.73 × 0.70
2/1
7
B. phyteumoides (Less.) DC.
narrowly oblong
1.01 × 0.38
3/1
7
B. pseudovillosa Malag. & J.E. Vidal
narrowly oblong
1.73 × 0.34
5/1
7
O. Camargo 2843 (PACA)
B. ramboi G. Heiden & L. Macias
narrowly oblong
1.19 × 0.28
4/1
7
B. riograndensis Malag.
& J.E. Vidal
narrowly
oblong-cylindric
2.55 × 0.37
7/1
20
B. sagittalis (Less.) DC.
narrowly oblong
1.00 × 0.29
3/1
7
obovoid
0.76 × 0.42
2/1
5
M. Sobral & al. 5031 (ICN)
B. trimera (Less.) DC.
narrowly oblong
1.19 × 0.30
4/1
14
B. vincifolia Baker
narrowly
oblong-obovoid
1.37 × 0.42
3/1
5
B. articulata (Lam.) Pers.
B. subtropicalis G. Heiden
GROUP III. Papillose folded cypselae
without cavities
In this group, the cypselae present a folded surface
with evenly distributed papillae. Longer papillae on
the ribs, the number, concentration, and shape of
papillae vary in each species. Carpopodium present,
ring-shaped, 40-110 µm diameter. This group pre-
L.T. Pereira 16 (ICN)
L.T. Pereira 87 (ICN)
B. Rambo 60054 (PACA)
sents 12 species and can be divided in two subgroups
by the number of ribs: a. with 5-7 ribs consists of
B. apicifoliosa (Fig. 3A-D), B. flexuosiramosa (Fig. 3EH), B. milleflora (Fig. 3I-L), B. organensis (Fig. 3M-P),
B. phyteumoides (Fig. 3Q-T) and B. sagittalis (Fig. 4AD); b. with ~14 ribs is composed of B. crispa (Fig. 4EH), B. cylindrica (Fig. 4I-L), B. jocheniana (Fig. 4M-P),
110
Fig. 1. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group I: B. microcephala: A, cypsela; B,
C, papillae detail; D, carpopodium. B. penningtonii: E, cypsela; F, G, papillae detail; H, carpopodium enlarged.
B. myriocephala (Fig. 4Q-T), B. aff. opuntioides (Fig.
5A-D), and B. trimera (Fig. 5E-H).
GROUP IV. Papillose folded cypselae with cavites
The cypselae present a folded surface with evenly
distributed papillae. The papillae are globose (B. articulata) or cylindrical and longer on the ribs than in
the intercostal region (B. glaziovii). Slight cavities occur on the folded surface. Carpopodium present,
ring-shaped, 20-60 µm diameter. Ribs ~ 5. Two
species: B. articulata (Fig. 6A-D) and B. glaziovii (Fig.
6E-H).
GROUP V. Epapillose folded cypselae
The cypselae present a folded surface, with longitudinal folds. Papillae are absent in the intercostal
areas, or just relictual, and slightly prominent on the
ribs. Carpopodium present, ring-shaped, 50-130 µm
diameter. Ribs 5-7 or ~ 20 (B. riograndensis). Four
species: B. junciformis (Fig. 7A-D), B. pentaptera
(Fig. 7E-H), B. riograndensis (Fig. 7I-L) and B. sagittalis (Fig. 7M-P).
Discussion
Patterns observed in cypselae morphology in Baccharis sect. Caulopterae were similar to those previously reported for species of other sections of Baccha-
ris (Velez, 1981; Hellwig, 1990; Mukherjee & Sarkar,
2001; Müller, 2006), which also show a ring-shaped
carpopodium and papillose surface. For the tribe
Astereae, and for other Baccharis species, the presence
of glandular and non-glandular trichomes was also
observed (Mukherjee & Sarkar, 2001; Müller, 2006).
Velez (1981) reported that the cypselae of genus Baccharis are not uniform, and he separated them in two
groups. Velez (1981) also reported that cypselae may
vary from papillose to epapillose, with epidermal cells
with slightly lignified walls or not, and a folded or flat
cuticle, and these features were also observed in the
present study. Additionally, we found that B. articulata and B. glaziovii present cavites, a condition structures not previously reported, although it is possible
that this feature is an artefact. The Baccharis sect.
Caulopterae species present a carpopodium as characterized by Haque & Godward (1984), who emphasized that most species of the Asteraceae family have
this abscission structure.
Species taxonomically close presented similarities
in cypsela surface morphology, reflecting on the
groups formed. However, since species of the “Baccharis trimera complex” (B. crispa, B. cylindrica, B.
jocheniana, B. myriocephala, and B. trimera), all
showed a similar cypsela micromorphology (Group
III.b), cypsela characters were unhelpful to distinguish the species of this group.
111
Fig. 2. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group II: B. palustris: A, cypsela; B, C, epapillose surface; D, carpopodium. B. paranensis: E, cypsela; F, G, epapillose surface; H, carpopodium. B. pseudovillosa: I, cypsela; J, K,
epapillose surface; L, carpopodium. B. ramboi; M, cypsela; N, O, epapillose surface; P, carpopodium. B. vincifolia; Q, cypsela; R, S, epapillose surface; T, carpopodium.
112
Fig. 3. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group III.a: B. apicifoliosa: A, cypsela oblong-cylindrical; B, C, papillae detail; D, carpopodium [C]. B. flexuosiramosa: E, cypsela; F, G, papillae; H, carpopodium. B. milleflora:
I, cypsela; J, K, papillae detail; L, carpopodium. B. organensis: M, cypsela; N, O, papillae; P, carpopodium. B. phyteumoides: Q, cypsela;
R, S, papillae; T, carpopodium.
113
Fig. 4. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group III.a: B. subtropicalis: A, cypsela; B, C,
papillae; D, carpopodium. Group III.b: B. crispa: E, cypsela; F, G, papillae; H, carpopodium. B. cylindrica: I, cypsela; J, K, papillae; L, carpopodium. B. jocheniana: M, cypsela; N, O, papillae; P, carpopodium. B. myriocephala: Q, cypsela; R, S, papillae; T, carpopodium.
114
Fig. 5. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group III.b: B. aff. opuntioides: A, cypsela;
B, C, papillae; D, carpopodium. B. trimera: E, cypsela; F, G, papillae; H, carpopodium.
Fig. 6. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group IV: B. articulata: A, cypsela oblong-cylindrical; B, C, papillae; D, no carpopodium. B. glaziovii: E, cypsela; F, G, papillae; H, carpopodium. [Cav, cavites,
Pap, papilla].
115
Fig. 7. Scanning electron micrographs of cypselae surface of Baccharis sect. Caulopterae - Group V: B. junciformis: A, cypsela; B, C,
epapillose surface; D, carpopodium. B. pentaptera: E, cypsela; F, G, epapillose surface; H, carpopodium. B. riograndensis: I, cypsela;
J, K, epapillose surface; L, carpopodium. B. sagittalis: M, cypsela; N, O, epapillose surface; P, carpopodium.
Acknowledgements
We thank the curators of the herbaria ESA, ICN, PACA and
UEC that provided material for this study, to Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the financial support, to Centro de Microscopia Eletrônica da Universidade Federal do Rio Grande do Sul (CEM) and technics Carlos
Barboza dos Santos and Karina Marckmann for facilities in using
of SEM. Particular thanks to Pedro Maria de Abreu Ferreira for
suggestios on language, Cláudio Augusto Mondin, Mara Rejane
Ritter, Rinaldo Pires dos Santos, Nádia Roque, Jochen Müller and
Gustavo Heiden for the critical revision and suggestions for this
manuscript.
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Haque, M.Z & Godward, M.B.E. 1984. New records of the carpopodium in Compositae and its taxonomic use. Botanical Journal of the Linnean Society 89: 321-340.
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Rodriguésia 60(4): 943-983.
Hellwig, F.H. 1990. Die Gattung Baccharis L.(Compositae-Asteraceae) in Chile. Mitteilungen der Botanischen Staatssammlung
München 29: 1-456.
Marzinek, J., De-Paula, O.C. & Oliveira, D.M.T. 2008. Cypsela or
achene? Refining terminology by considering anatomical and
historical factors. Revista Brasileira de Botânica 31(3): 549-553.
Mukherjee, S.K. & Sarkar, A. 2001. Morphology and structure of
cypselae in thirteen species of the tribe Astereae (Asteraceae).
Phytomorphology 51(1): 17-26.
Müller, J. 2006. Systematics of Baccharis (Compositae-Astereae)
in Bolivia, including an overview of the genus. Systematic
Botany Monographs 76: 1-339.
Radford, A.E. 1986. Fundamentals of plants systematics. New
York. Harper and Row.
Roth, I. 1977. Fruits of angiosperms: encyclopaedia of plant anatomy. Berlin. Gebrüder Borntraeger.
Schneider, A.A., Heiden, G. & Boldrini, I. 2009. Notas nomenclaturais em Baccharis L. sect. Caulopterae DC. (Asteraceae). Revista Brasileira de Biociências 7(2): 225-228.
Velez, M.C. 1981. Karpologische untersuchungen an amerikanischen Astereae (Compositae) Mitteilungen der Botanischen
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Associate Editor: J. Müller
Received: 9-II-2010
Accepted: 1-II-2011
2280_Gelidiales:Anales 68(1).qxd 13/06/2011 12:21 Página 117
Vol. 68(1): 117-124
enero-julio 2011
ISSN: 0211-1322
doi: 10.3989/ajbm.2280
Photosynthetic response and zonation of three species
of Gelidiales from Tenerife, Canary Islands
by
S. Domínguez-Álvarez1, J.M. Rico2 & M.C. Gil-Rodríguez1
1
2
Departamento de Biología Vegetal (Botánica), Universidad de La Laguna, E-38071 La Laguna, Spain.
Departamento de Biología de Organismos y Sistemas, Universidad de Oviedo, E-33071 Oviedo, Spain. [email protected]
Abstract
Resumen
Domínguez-Álvarez, S., Rico, J.M. & Gil-Rodríguez, M.C. 2011.
Photosynthetic response and zonation of three species of Gelidiales from Tenerife, Canary Islands. Anales Jard. Bot. Madrid
68(1): 117-124.
Domínguez-Álvarez, S., Rico, J.M. & Gil-Rodríguez, M.C. 2011.
Respuestas fotosintéticas y zonación de tres especies de Gelidiales de Tenerife, Islas Canarias. Anales Jard. Bot. Madrid 68(1):
117-124 (en inglés).
Three species of Gelidiales (Gelidium arbuscula, Gelidium canariense and Pterocladiella capillacea) (Rhodophyta) were selected
due to their abundance in the marine lower intertidal of the
north coast of the island of Tenerife (Canary Islands), to assess,
using PAM fluorescence, the importance of irradiance and exposure to air on vertical distribution. We compared tolerance to
emersion by air-drying fronds under simulated emersion, and results suggest that recovery of photosynthesis after emersion
plays a major role in the vertical distribution of these three
species. Morphological traits such as clumped fronds explain the
higher tolerances, and reduced water loss of the species upper
on the shore. Local differences between sites may be related to
slight differences in the light regime related to topography.
Se han seleccionado tres especies de Gelidiales (Gelidium arbuscula, Gelidium canariense y Pterocladiella capillacea) que son
abundantes en los niveles inferiores del intermareal de la costa N
de Tenerife para establecer, utilizando fluorescencia tipo PAM,
la importancia de la cantidad de luz y la exposición al aire en su
zonación vertical. Se ha comparado la tolerancia a la emersión
en frondes expuestas al aire, y los resultados sugieren que la capacidad de recuperación de la fotosíntesis tras la emersión tiene
un papel fundamental en la explicación de la posición vertical de
estas tres especies. Además, características morfológicas como
el apelotonamiento de las frondes pueden coadyuvar a la mayor
tolerancia, al reducir la pérdida de agua en emersión en las especies de niveles más altos. Las variaciones entre sitios se
pueden deber a desigualdades locales en la cantidad de luz
provocadas por diferencias topográficas.
Keywords: Canary Islands, ecophysiology, Gelidiales, Gelidium, photosynthesis, Pterocladiella.
Palabras clave: ecofisiología, fotosíntesis, Gelidiales, Gelidium,
Islas Canarias, Pterocladiella.
Introduction
Brown, 1982; Rico & Fredriksen, 1996; Wiencke &
al., 2000; Bischof & al., 2006).
Intertidal seaweeds are exposed to rhythmic emersion and submersion periods. The dehydration of algal thalli during the emersion imposes very stressful
conditions and it has been supposed that the recovery of photosynthesis after emersion could be a factor
involved in the zonation pattern of seaweeds. For example, the recovery of photosynthesis of brown algae, after desiccation during the low tide, was correlated with their heights in the zonation of European
shores (Dring & Brown, 1982). A similar correlation
Zonation of seaweeds is the most conspicuous
characteristic of rocky shores worldwide (Lewis,
1964; Stephenson & Stephenson, 1972; Pérès, 1982).
Algal zonation seems to be due to several causes acting simultaneously, but the relative contribution of
each factor is under debate. Thus, inter-specific competition has usually been the consensus for the main
cause of zonation (Chapman, 1973, 1974). However,
experimental studies propose that physiological limits of seaweeds are also involved in zonation (Dring &
118
S. Domínguez-Álvarez & al.
was argued for the zonation pattern of different
species in Gelidiaceae in N Iberian Peninsula (Rico &
Fredriksen, 1996). However, more experimental
studies are needed/required to improve our knowledge the relationship between photosynthetic performance of intertidal algae and their heights in the
zonation pattern.
It is also known that dynamic photo-inhibition of
photosynthetic quantum yield (Hall & Rao, 1999) occurs in seaweeds exposed to high levels of irradiance
at noon, but such photo-inhibition is more important
the lower in the zonation that the species occurs.
Thus, although a very low level of photo-inhibition
was detected in the red alga Rissoella verruculosa
growing in the upper intertidal (Flores-Moya & al.,
1998) photoinhibition is more important in seaweeds
from the lower part of the intertidal (Huppertz & al.,
1990; Hanelt & al., 1993); moreover, the reduction of
photosynthesis was very high in a subtidal species
transplanted close to sea surface (Gevaert & al.,
2002).
The tides that affect the coasts of the Canaries are
of semidiurnal character, with highest high waters that
do not surpass 3 m above Lowest Astronomical Tide
(LAT), whereas the lowest low tides reach, occasionally, values of 0 m. The steep northern coast of the island of Tenerife is very exposed, and this constitutes
one of the most decisive factors determining the
species composition of the lower intertidal vegetation
that is formed, characteristically, by species that
tolerate big swell. In these lower intertidal and shal-
low subtidal environments, three species of Gelidiales
form successive belts. The upper one is an intense red
colour, dominated by Pterocladiella capillacea (S.G.
Gmelin) Santelices & Hommersand; then P. capillacea
is progressively substituted by Gelidium arbuscula
Bory de Saint-Vincent ex Børgesen (around 0.7-0.8
m above LAT). Below it there is a wide belt, reaching
the upper subtidal, darker in colour, dominated
by Gelidium canariense (Grunow) Seoane-Camba
ex Haroun, Gil-Rodríguez, Díaz de Castro et Prud'
homme van Reine. The three species are present just
in the lower intertidal where they are under the
influence of spray even during low tides (Mercado &
al., 2001). Thus, the zonation pattern of P. capillacea,
G. arbuscula and G. canariense in northern Tenerife
shores is an appropriate model to test the hypothesis
that their heights on the shore may be correlated with
their photosynthetic performance.
The objective of this study was to characterize the
photosynthetic response of the three species of
Gelidiales at two localities on Tenerife and to relate it
to the stress of emersion and changes in irradiance levels associated with their different vertical distribution. In particular, the two hypothesis to be tested
were: (i) that the time of recovery of photosynthetic activity after desiccation in the selected species (estimated via fluorescence parameters) is higher the lower is
the location on the zonation pattern; and (ii) the photoinhibition of the photosynthetic quantum yield
around noon is higher the lower is the location in the
zonation.
Table 1. ANOVA results for Ik and ETRrmax. *the factor ‘Species’ was tested against ‘Species x Run’. ‘Species x Site’ was removed from
the analysis (non-significant, P = 0.27).
Ik
Source of variation
df
ETRrmax
MS
F
P
MS
F
P
Species*
2
281.20
1.00
0.421
164184
4.50
0.064
Site
1
2990.00
5.02
0.111
176026
12.60
0.038
Run
3
840.23
1.41
0.392
45483
3.26
0.179
Species × Site
2
197.43
0.78
0.499
18461
1.64
0.270
Species × Run
6
280.36
1.11
0.451
36515
3.25
0.089
Site × Run
3
596.03
1.26
0.293
13972
1.11
0.350
Species×Site×Run
6
252.66
0.53
0.782
11242
0.89
0.505
Error
96
474.03
Total
119
12624
Photosynthetic response of Gelidiales
119
Fig. 1. Daily cycle of photosynthetic quantum yield (ΦPSII; dimensionless) in Gelidium canariense. Values are represented as
mean ± SD (n = 5) from samples of Puerto de la Cruz (䡬) and
Garachico (䢇).
Fig. 2. Daily cycle of photosynthetic quantum yield (ΦPSII; dimensionless) in Gelidium arbuscula. Values are represented as
mean ± SD (n = 5) from samples of Puerto de la Cruz (䡬) and
Garachico (䢇).
Experiment A: daily variation in
photosynthetic quantum yield
Sampling sites, algal collection
and pre-treatment of samples
The Northern coast of Tenerife is very exposed, with
frequent periods of intense swell 2 to 3 m height, and
occasional calm periods throughout the year, mainly in
spring and summer. During autumn the storms with
waves up to 5 m height are frequent. Water temperature ranges 17 ºC in February to 23 ºC in August.
Two localities separated 30 km were selected: Puerto de la Cruz (UTM 3675447/3588716) and Garachico
(UTM 3700288/3590165). Both sites haves similar patterns of marine vegetation, characterized by a belt of
blue-green algae in the upper intertidal, a lower caespitose belt dominated by Gelidium pusillum (Stackhouse) Le Jolis, Caulacanthus ustulatus (Merthens ex
Turner) Kützing and Ulva rigida C. Agardh, another
below mainly of species of the Corallinaceae and
Rhodomelaceae and, in the lowest levels, the three
species of Gelidiales down to the subtidal (with Pterocladiella capillacea in the upper part, G. arbuscula in the
middle and G. canariense in the lowest part) (Gil-Rodríguez & Wildpret, 1980; Pinedo & Afonso-Carrillo,
1994).
Thalli free from epiphytes of the three Gelidiales
cited above were collected in July 1999. They were
transferred to the laboratory in seawater and darkness
and kept in 50 L aquaria at constant temperature (ca.
20 °C). Natural solar irradiance was reduced by using
plastic mesh that acted as neutral density filters reducing incident PAR to 60-80% of full sunlight.
A system of continuous seawater circulation was
designed to keep 10 L glass aquaria with 10-20 g fresh
weight under a constant temperature of 20 ºC during
incubations. Measurements of photosynthetic activity
were carried out by using a DIVING-PAM (Heinz
Walz GmbH, Germany) during a whole daily cycle,
from sunset to sunrise. Every hour from sunrise, five
Fig. 3. Daily cycle of photosynthetic quantum yield (ΦPSII; dimensionless) in Pterocladiella capillacea. Values are represented
as mean ± SD (n = 5) from samples of Puerto de la Cruz (䡬) and
Garachico (䢇).
120
Fig. 4. Photosynthetic quantum yield (ΦPSII; dimensionless) of Gelidium canariense from Puerto de la Cruz (left) and Garachico (right)
during emersion (values to the left of the vertical broken line) and after resubmergence (values to the right of the broken line). Each
line corresponds to a different run.
Fig. 5. Photosynthetic quantum yield (ΦPSII; dimensionless) of Gelidium arbuscula from Puerto de la Cruz (left) and Garachico (right)
during emersion (values to the left of the vertical broken line) and after resubmergence (values to the right of the broken line). Each
line corresponds to a different run.
fronds from the aquaria for each locality and species
were selected and photosynthesis was measured. During the central hours of the day (–2 to +2 hours
around noon) measurements were taking at 30 min intervals. According to Genty & al. (1989), photosynthetic activity was estimated from the effective quantum yield of chlorophyll a from photosystem II (ΦPSII
defined as ⌬F/Fm’). The use of the ΦPSII values avoid
problems derived from the potential differences be-
tween absorptances in different species (Franklin &
Badger, 2001) although these differences can be minor in species from the same genus/family and with
similar morphology.
Additionally, five fronds per species and locality
were exposed to nine levels of increasing PAR (0, 12, 55,
122, 213, 317, 443, 653, 889 µmol m-2 s-1) during 45 s
each, after which a saturating pulse was applied and
ΦPSII values measured. The relative electron transport
121
Fig. 6. Photosynthetic quantum yield (ΦPSII; dimensionless) of Pterocladiella capillacea from Puerto de la Cruz (left) and Garachico
(right) during emersion (values to the left of the vertical broken line) and after resubmergence (values to the right of the broken line).
Each line corresponds to a different run.
rate (ETRr) was computed as PAR × ΦPSII, when ΦPSII
value was >0.1 (Beer & Axelsson, 2004). The plot of
ETRr versus PAR was used to calculate the irradiancesaturated ETR over the saturation point (ETRrmax) and
the value of PAR above which ETRrmax was detected
(Ik); for this purpose, a non-linear fit to a hyperbolic
curve was applied. The experiment was repeated (using different fronds) every 2 h from sunrise to sunset.
Experiment B: response of photosynthetic
performance to desiccation stress and rehydration
Five fronds from each locality and species were exposed to air by placing them in plastic trays after vigorous shaking to simulate desiccation stress during
low tide exposure to air. Fronds were exposed during
the hours of highest PAR, since low tides occurred
around noon during the experiments. Desiccation
stress was estimated from ΦPSII measurements at 30
min intervals. Fronds were also weighed to the nearest
mg at the start and at the end of the experiment to calculate the proportion of water loss. After an exposure
of 2.5 h (equivalent to the longest emersion period
during spring tides), fronds were rehydrated by submersion in seawater and fluorescence measurements
were conducted for 2.5 h at 30 min intervals.
Statistical analysis of data
Data were analyzed using factorial ANOVAs (see
results for details on each analysis). All data were analyzed using Statistica for Windows.
Results
The daily cycle of ΦPSII in the three species showed
a similar pattern: the highest ΦPSII values were recorded at the sunrise and decreased abruptly to minimum
values (about 50% lower than those on earlier hours)
around solar noon; then, ΦPSII increased gradually at
the sunset (Figs. 1-3).
A marked reduction in ΦPSII was found in the three
species when thalli were exposed to air for 2.5 h simulating emersion conditions (Figs 4-6); however, the
highest reduction of ΦPSII was recorded in Gelidium
canariense (Fig. 4) while Pterocladiella capillacea was
the species with the lowest reduction of ΦPSII (Fig. 6).
The reduction of ΦPSII in G. arbuscula after desiccation was intermediate to that of the two other species
(Fig. 5). However, the relative water loss was similar in
the three species from both localities (overall mean %
water loss = 50.3 ± 7.4, n = 30). The values of ΦPSII after 1.5 h rehydration in G. arbuscula was around 3050% than to those measured prior to exposure to air
(Fig. 5) while recovery in P. capillacea and G. canariense was lower (Figs. 4, 6).
Photoinhibition was not detected in the ETRr-PAR
curves for the three species, and both ETRrmax and
Ik values were similar for the three species at both
localities (Figs. 7, 8, Table 1). Saturation occurred
above 150 µmol m-2 s-1 for the three species, reaching
around 500 µmol m-2 s-1 for some samples of G. arbuscula (Fig. 7).
122
Run
Fig. 7. Values of saturating PAR (Ik) for the three species of Gelidiales from Puerto de la Cruz (䢇) and Garachico (䡬). ‘Run’ refers to the
time period (UTC+2) when the measurements for the curves where taken (1: from 10 to 11 a.m.; 2: from 12 to 13; 3: from 14 to 15;
4: from 16 to 17).
Run
Fig. 8. Values of irradiance-saturated, relative electron transport rate (as ETRrmax) for the three species of Gelidiales from Puerto de la
Cruz (䢇) and Garachico (䡬).‘Run’ refers to the time period (UTC+2) when the measurements for the curves where taken (1: from 10 to
11 a.m.; 2: from 12 to 13; 3: from 14 to 15; 4: from 16 to 17).
Discussion
The presence of several species of Gelidiales in
contiguous altitudinal belts is a common feature of
many temperate coasts (Santelices, 1991) and it has
been suggested that this pattern indicates close similarities among species with respect to environmental
tolerance (Santelices, 1991; Montalva & Santelices,
1981). In the Gelidium-dominated lower shore in N
Spain, irradiance did not appear as a critical factor for
photosynthesis (Rico, 1991), but different Gelidium
species showed different saturation values (Ik) which
could be related to their altitudinal position on the
shore (Rico & Fredriksen, 1996). This is not the case
with the three Gelidiales from Teneriffe, which exhibited similar patterns of both photoinhibition of ΦPSII
along the daily cycle and ETRr-PAR curves, and it has
been shown that ETR values can be used to estimate
photosynthesis in Gelidium species since they compare well with photosynthetic estimations using, for
instance, O2 electrodes (Beer & Axelsson, 2004;
Franklin & Badger, 2001; Silva & al., 1998).
Since the photosynthetic response under standard
conditions did not differ between species, the position on the shore could be explained by negative effects of desiccation on net photosynthesis as it has
been demonstrated in fucoids (Williams & Dethier,
2005). Desiccation occurs during low tide almost
every day, its length determined by the duration of the
tide. Gelidium sesquipedale from Asturias, a lower intertidal species, showed a higher reduction in net photosynthesis after exposure to air (Rico & Fredriksen,
1996), and an exposure longer than 2 h caused a negative net production, thus photosynthesis was overcome by respiration. The same occurred for G. canariense, the species lowest on the shore in Teneriffe,
which was more affected by desiccation and also recovered to a lesser degree after rehydration. Recovery
of photosynthesis after emersion is one of the major
factors explaining the upper limits of seaweeds in the
intertidal (Dring & Brown, 1982). It has been suggested that both tolerance to sustain photosynthesis
under desiccation and reduction in the rate of water
loss can help intertidal species to tolerate longer emersion periods (Oates & Murray, 1983). This could be
the case with the two species located upper in the
shore in our study: G. arbuscula is morphologically
similar to G. pulchellum, which showed a reduced rate
of water loss after emersion periods of more than 3 h
(Rico & Fredriksen, 1996), while P. capillacea showed
a rapid recovery after rehydration. All three species
were able to recover after exposure to periods shorter
than 2.5 h which suggests that small differences in the
recovery rate could explain upper tolerance limits on
the shore. Duration of natural exposure to air in intertidal seaweeds determines the degree of drying, but
during these periods it is the rate of drying which explains the stress (Hunt & Denny, 2008). Thus,
tolerance to desiccation (as opposed to the desiccation stress) and the light environment (Mercado & al.,
2001) are the main factors to explain the zonation pattern of these three species in the coast of Teneriffe.
Apart from the obvious effect of reduced irradiance
levels during high tides affecting photosynthetic production, exposure to full solar radiation during low
tides can also affect photosynthetic performance,
mainly at noon (Gómez & Figueroa, 1998). Accordingly, P. capillacea showed the most intense noon-depleted ETRr rate, while showing intermediate values
of the photosynthetic parameters. Gelidium arbuscula
did not show noon depletion in ΦPSII and showed the
highest values both in ETRrmax and in Ik, and G. canariense showed a moderate reduction in ΦPSII at
noon but not so high values in the photosynthetic parameters. It could be concluded that the upper
species, P. capillacea, is adapted to exposure to air and
123
high irradiance levels during emersion by reducing
ΦPSII and showing fast recovery after rehydration,
while G. arbuscula is able to reduce water loss due to
its compact morphology, which may also produce
frond shading and so attenuate the effect of high irradiance, and ‘clump’ morphology represents a significant advantage to reduce water loss in central portions of the thallus (Hunt & Denny, 2008). Differences in zonation between sites are intriguing, although
between site variation has been reported before and
explained by a multiarray of factors other than exposure (Williams & Dethier, 2005). Further studies will
be needed to fully assess these additional factors
which may explain small scale differences in the zonation pattern, although small topographic differences
may produce differences also in the local light regime.
Acknowledgements
Personnel from the Centro Oceanográfico de Canarias - Instituto Español de Oceanografía de Canarias (IEO), gave support to
experiments. The contribution of J.M. Cejas is especially acknowledge.
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Associate Editor: A. Flores
Received: 27-XII-2010
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10 instrucciones a los autores:01 primeras.qxd 13/06/2011 12:33 Página 130
11 Bolsuscrip. Anales 2011:10. Bolsuscrip. Anales 2009.qxd 13/06/2011 12:34 Página 131
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portada y contra 68(1) NOVEDADES2:portada y contra 66(1).qxd 16/06/2011 11:22 Página 1
ISSN: 0211-1322
Zamora, N.A. El caso de Lonchocarpus costaricensis (Leguminosae, Papilionoideae), una especie
endémica de Costa Rica: un complejo taxonómico-nomenclatural, y una nueva especie / The case
of Lonchocarpus costaricensis (Leguminosae, Papilionoideae), an endemic species of Costa Rica:
a taxonomic-nomenclatural complex, and a new species ................................................................
Cano-Maqueda, J. & Talavera, S. A taxonomic revision of the Campanula lusitanica complex (Cam pa nulaceae) in the Western Mediterranean region / Una revisión taxonómica del com plejo Campanula lusitanica (Campanulaceae) en la región occidental mediterránea ...........................................................................................................................................
Venhuis, C. & Oostermeijer, J.G.B. Distinguishing colour variants of Serapias perez-chiscanoi (Orchidaceae) from related taxa on the Iberian Peninsula / Distinción de variantes en color de Serapias perezchiscanoi (Orchidaceae) en relación con táxones de la Península Ibérica ..........................................
Lado, C., Wrigley de Basanta, D. & Estrada-Torres, A. Biodiversity of Myxomycetes from the Monte
Desert of Argentina / Biodiversidad de Myxomycetes en el Desierto de Monte (Argentina) ...............
Peñas, J., Lorite, J., Alba-Sánchez, F. & Taisma, M.A. Self-incompatibility, floral parameters, and pollen
characterization in the narrow endemic and threatened species Artemisia granatensis (Asteraceae) /
Autoincompatibilidad, parámetros florales y caracterización de polen en la especie endémica y amenazada Artemisia granatensis (Asteraceae) ......................................................................................
Schneider, A.A. & Boldrini, I.I. Microsculpture of cypselae surface of Baccharis sect. Caulopterae (Asteraceae) from Brazil / Microescultura de la superficie de las cipselas de Baccharis sect. Caulopterae
(Asteraceae) de Brasil ......................................................................................................................
Domínguez-Álvarez, S., Rico, J.M. & Gil-Rodríguez, M.C. Photosynthetic response and zonation of
three species of Gelidiales from Tenerife, Canary Islands / Respuestas fotosintéticas y zonación de
tres especies de Gelidiales de Tenerife, Islas Canarias ......................................................................
http://rjb.revistas.csic.es
N.º 1
enero-junio 2011
Madrid (España)
ISSN: 0211-1322
Madrid
SUMARIO / CONTENTS
Volumen 68
7/14
15/47
2011
Madrid (España)
N.º 1
enero-junio 2011
49/59
61/95
97/105
107/116
117/124
Volumen 68
N.º 1
Volumen 68
REAL JARDÍN BOTÁNICO
www.publicaciones.csic.es

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