contribución y efecto de la hojarasca derivada de mangle en la

Transcription

CONTRIBUCIÓN Y EFECTO DE LA HOJARASCA DERIVADA DE MANGLE
EN LA PRODUCTIVIDAD PRIMARIA Y COMPOSICIÓN DEL
FITOPLANCTON DE UNA LAGUNA COSTERA
TESIS QUE PRESENTA JOSÉ ANTOLÍN AKÉ CASTILLO
PARA OBTENER EL GRADO DE DOCTOR EN CIENCIAS
ECOLOGÍA Y MANEJO DE RECURSOS NATURALES DOCTORADO
DIRECTOR DE TESIS
DRA. GABRIELA VÁZQUEZ
Xalapa, Veracruz, México 2006
2
RECONOCIMIENTOS CONACYT Y PROYECTOS
La realización de este trabajo doctoral fue posible gracias a la beca de manutención
otorgada por el CONACYT a José Antolín Aké Castillo bajo el número de registro 90031.
Durante las diferentes etapas de desarrollo del trabajo se obtuvo financiamiento de los
siguientes proyectos:
Proyecto 902-11. Instituto de Ecología A. C. Xalapa, Departamento de Ecología
Funcional a cargo de la Dra. Gabriela Vázquez.
Proyecto 902-11-280. Instituto de Ecología A. C. Xalapa, Departamento de Ecología
Funcional a cargo de la Dra. Gabriela Vázquez.
Proyecto 32732-T. CONACYT a cargo de la Dra. Gabriela Vázquez.
Proyecto 902-17-144. Instituto de Ecología A. C. Xalapa, Departamento de Ecología
Funcional a cargo del Dr. José G. García Franco.
3
Ponche de los ponches, cumple mis deseos:
Que de todos los mares y los ríos
la contaminación desaparezca,
y repletos de peces y límpidos,
como en el pasado, permanezcan.
Ponche de los ponches, cumple mis deseos:
Que el océano conserve la vida
y se diluya la marea negra,
que los mares y las costas sigan
dando alimentos a la Tierra
Michael Ende (1989)
Der satanarchäolügenialkohöllische Wundschpunsch
(El ponche de los deseos genialcoholorososatanarquiarqueologicavernoso)
4
AGRADECIMIENTOS
A mis padres, hermanos y sobrinos que han sido los pilares más importantes en el logro
de mis metas.
A la Dra. Gabriela Vázquez por heberme dado la oportunidad de trabajar en la laguna de
Sontecomapan; por sus sugerencias, revisiones y comentarios en la realizacion del protocolo y la
escritura de los diferentes capítulos de esta tesis; y por su constante preocupación por mi
situacion como estudiante del Posgrado y facilitar mi estancia en Xalapa por medio de los
contratos de trabajo.
A los miembos de mi comité Tutorial, Dr. Jorge López-Portillo por sus sugerencias y
correcciones durante los tutoriales y al Dr. Fernando Martínez Jerónimo por la revisón del
protocolo de esta tesis, sus sugerencias para mejorarlo, y su interés para asistir siempre a mis
tutoriales.
A los miembros de mi jurado por sus comentarios y sugerencias en la revisión de la tesis:
Dra. Ana Laura Lara, Dra. Patricia Moreno, Dr. Francisco Flores y en especial al Dr. Francisco
Gutiérrez por todas las molestias ocasionadas.
Al Sr. Adolfo Moreno (Agente Municipal de Sontecomapan) y su familia por todas sus
atenciones: gracias por su ayuda para disminuir la pérdida de las canastas colectoras de hojarasca
pero sobre todo por hacer ameno el trabajo en la laguna.
A todas las personas que me ayudaron durante el trabajo de campo: Ricardo, José Luis,
Ari, Almudena, Oli, Luis Alberto, Raúl, Fabricio, Tolome, Soco, Ulises, Lorenzo, Mariana y
Angélica. Mil gracias Ric por tu disponibilidad para conducir y llevarme a campo siempre que lo
necesité, por tus sugerencias en el trabajo de campo y las risas. Oli, muchisimas gracias por
haberte comprometido con mi trabajo de campo, por los cafecitos y pláticas tan productivas en tu
laboratorio, por permitirme compartir momentos importantes con tu familia, y por tu amistad.
5
A los técnicos del Laboratorio de Ecología Funcional Ariadna Martínez y Javier Tolome.
Ari!!! Mil gracias por tu paciencia, ayuda, sugerencias, enseñanzas y disponibilidad inmediata
para el procesamiento de las muestras de hojarasca y agua. Muchas gracias Javier por conducir en
los viajes de colecta, facilitarme el equipo y material, y tu ayuda en campo. A Alma y Maricela
por haberme librado de una parte de sufrimiento en el molido de la hojarasca ¡gracias niñas!
A los técnicos del laboratorio de suelos Lulu y Ninfa por las facilidades para el
procesamiento de las muestras de hojarasca. Al Dr. Oscar Briones por el préstamo de los tamices
y el molino. Al Dr. Mario Favila por facilitarme su laboratorio para la esterilización de material
de cultivo, por sus sugerencias en algunos de los diseños experimentales y sus comentarios de
algunos capítulos de esta tesis.
A Araceli Toga por su ayuda en la orientacion de los miles de trámites administrativos
relacionados con el INECOL. A Bianca Delfosse por la revisión del inglés de los capítulos de
esta tesis y de la cual asumo la responsabilidad de cualquier omisión a sus correcciones.
A todos mis profesores e invitados del INECOL, ya que indudablemente influyeron en mi
crecimiento académico.
A mis amigos y compañeros del INECOL que en diferentes momentos hicieron agradable
y académicamente productiva mi estancia en Xalapa: Oli, Angélica, Marianita, Tania Chew,
Socorro, Miriam Ramos, Karina, Ceci, Javier, Victor, Clemen, Arlette, Lucianita, Luis Alberto,
Cuauhtémoc, Pablo, Aarón, Gaby, Arturo, Miriam Ferrer, Felipe, Ana, Nora y Juanita.
A mis amigos de toda la vida: Sandy Vázquez, quien con sus “porras” me ayudó a
librarme de las dudas para comenzar esta aventura; Sandy Guerra, Olimpia, Alicia y Fabricio
porque siempre están para mí para escucharme y ayudarme. Gracias Luis por haber sido un
soporte fundamental al venirme a Xalapa y por tu tiempo y compañía durante las terapias de
rehabilitación de mi pierna.
6
7
ÍNDICE
0. Resumen ……………………………………………………………...……………………… 15
1. Introducción general ……………………………………………………………….………… 16
1.1. Literatura citada ……………………………………………………..……………... 21
2. Litterfall and decomposition of Rhizophora mangle L. in a coastal lagoon in the southern Gulf
of Mexico ……………………………………………………………………………………...... 25
2.1. Abstract …………...………....……..………………………………………………. 26
2.2 Introduction ………………………………………..………………………………... 26
2.3. Study site ………………………………………...….……………………………… 27
2.4. Material and methods ………………………………….………………………...…. 27
2.5. Results ……………………………………………………………..……………….. 29
2.6. Discussion ………………………………………………………….………………. 31
2.7. References ………………………………………………………….………………. 35
3. Dynamics of C, P, N and tannins associated with the leaf litter production and decomposition
of Rhizophora mangle L. in a tropical coastal lagoon in Mexico ………………………………. 37
3.1. Abstract ………………………………………….…………………………………. 38
3.2. Introduction …………………………..…………………………………………….. 38
3.3. Methods ……………………………………………………………………………. 40
3.4. Results ……………………………………………………………………………… 42
3.5. Discussion …………….……………………………………………………………. 45
3.6. Literature cited ……………………………….…………………………………….. 49
4. Phytoplankton variation over a year and its relation to nutrients and allochthonous organic
matter in Sontecomapan, a tropical coastal lagoon on the Gulf of Mexico ….…………………. 59
4.1. Abstract …………………………………………………………………………….. 60
8
4.2. Introduction ………………………………………………………………………… 62
4.3. Study site and methods ……………………………….……………………………. 63
4.4. Results ……………………………………………………………………………… 67
4.5. Discussion ………………………………………………………………………….. 73
4.6. Summary and conclusion …………………………………………………………... 76
4.7. References ………………………………………………………………………….. 78
5. Effect of the products of mangrove leaf litter decomposition on primary productivity and
phytoplankton growth ………………………………………..……………………………...… 100
5.1. Abstract ………………………………………………………………………….... 101
5.2. Introduction ………………...………………………………………………..……. 102
5.3. Methods ……………………………………………………………...………..….. 103
5.4. Results …………………………………………………………………………..… 107
5.5. Discussion ………………………………………………………...………………. 109
5.6. Literature cited ………………………………………………….………………… 112
6. Conclusión general ……………………………………...………………………………….. 122
6.1. Literatura citada …………………………………………………………………... 127
7. Apéndice: Peridinium quinquecorne var. trispinifera var. nov. (Dinophyceae) from a
brackishwater environment ……………………………………………………………………. 130
7.1. Abstract …………………………………………………………………………… 131
7.2. Introduction …….…………………………………………………………………. 132
7.3. Material and methods ………………………………...…………………………… 133
7.4. Results …………………………………………………………………………….. 133
7.5. Discussion ……………………...…………………………………………………. 135
7.6. References ………………………………………………………………………… 138
9
LISTA DE FIGURAS
Figure 2.1. Location of Sontecomapan Lagoon and the mangrove sites studied. Gray fill indicates the
distribution of mangrove forest surrounding the lagoon. A, B and C represent the sites studied ………. 28
Figure 2.2. Salinity for each site by month. Circle: site A, square: site B, rhombus: site C ………… 30
Figure 2.3. Monthly litterfall production of Rhizophora. mangle in the Sontecomapan Lagoon
from November 2002 to October 2003 for each season. Vertical bars represent 95% confidence
intervals. Plus symbol: total litterfall, square: leaf fall, rhombus: flower fall, circle: propagule fall,
triangle: twig fall …………………………………………………………………..…………… 30
Figure 2.4. Mass of Rhizophora mangle leaves remaining in fine mesh litter bags (circle) and
coarse mesh litter bags (square). Vertical bars represent 95% confidence intervals …………… 32
Figure 2.5. Mass of Rhizophora mangle leaves remaining in litter bags during the “nortes” (circle), dry
(square) and rainy season (rhombus).Vertical bars represent 95% confidence intervals ……………….. 32
Figure 2.6. Mass of Rhizophora mangle leaves remaining in fine mesh litter bags (circle) and
coarse mesh litter bags (square) in the “nortes”, dry and rainy seasons. Vertical bars represent
95% confidence intervals ………………………………………………………………………. 33
Figure 3.1. Location of Sontecomapan Lagoon. Letters A, B and C are the sites studied. Gray
fill represents the mangrove forest ……………………………………………………….…….. 54
Figure 3.2. Seasonal dynamics in the mean concentrations of a) carbon, b) phosphorous, c)
nitrogen, d) tannins, and e) leaf litter production of R. mangle in Sontecomapan Lagoon from
December 2002 to October 2003. Vertical bars are 95% confidence intervals ………………… 55
Figure 3.3. Dynamics in the mean concentration of a) carbon, b) phosphorous, c) nitrogen, and
d) tannins in leaf litter decomposition in coarse (3 x 7 mm) and fine (1 x 1 mm) litterbags. Initial
values represent the concentration of each nutrient at the beginning of the experiments. Vertical
10
bars represent 95% confidence intervals. The continuous line is the coarse mesh litterbag and the
dotted line is the fine mesh litterbag ………………………………………………………...….. 56
Figure 3.4. Dynamics in the mean concentration of a) carbon, b) phosphorous, c) nitrogen, and
d) tannins in leaf litter decomposition at the three sites. Initial values represent the concentration
of each nutrient at the beginning of the experiments. Vertical bars represent 95% confidence
intervals. Site A is the continuous line, site B the coarse dotted line, and site C the fine dotted
line. ………………………………………………………………………………………...…… 57
Figure 4.1. The Sontecomapan Lagoon with sampling stations ……..……………………… 87
Figure 4.2. Variation in physicochemical parameters measured from October 2002 to October
2003. a) salinity, b) O2, c) temperature, d) pH, e) N-NH4+, f) N-NO3-, g) P-PO43-, h) Si-SiO2, i)
FPAS. Middle points represent the mean, whiskers are 95% confidence intervals. L indicates
lagoon and R rivers. The continuous line represents the surface level and the dotted line is the
bottom level. …………………………………….……………………………………………… 88
Figure 4.3. Variation in the mean of the first axis extracted from PCA. Whiskers are 95%
confidence intervals. The continuous line represents the lagoon and the dotted line is the rivers. L
indicates lagoon and R rivers. Different letters indicate significant differences (P < 0.05) ….… 89
Figure 4.4. Dynamics of dominant phytoplankton species. a) nortes season, b) dry season, c)
rainy season. Middle points represent the mean, whiskers show the minimum and maximum
values. Note Y scale is logarithmic …………………………………………………..………… 90
Figure 4.5. Cell density for each month in the (a) lagoon and (b) rivers. The middle point
represents the mean and whiskers are 95% confidence intervals. The continuous line represents
the surface level and the dotted line is the bottom level. Note Y scale is logarithmic …………. 91
Figure 4.6. Correlation biplot based on CCA analyses. a) Environmental-species biplot of the
lagoon. b) Environmental-site biplot of the lagoon. c) Environmental-species biplot of the rivers.
11
d) Environmental-site biplot of the rivers. Environmental variables are indicated by arrows.
Environmental scores were multiplied by 2 to fit the coordinate system. Abbreviations of species
are given in Table 3. In figures (a) and (c), the dominant species are marked as follows: solid
rhombus nortes season, solid circles dry season, and solid triangles rainy season. In figures (b)
and (d), solid circles represent samples from October 2002; plus symbol December 2002; empty
triangle February 2003; solid rhombus April 2003; solid triangle June 2003; solid square August
2003; and empty circle October 2003 ……………………………………………………...…… 92
Figure 5.1. Location of Sontecomapan Lagoon with primary productivity experiments study
sites ……………………………………………………………………………………….…… 117
Figure 5.2. Mean concentration of a) N-NH4+, b) N-NO3-, c) P-PO43- and d) FPAS release
from the decomposition of 1 g of leaf litter in 1 l of water over time. Dotted line represents the
treatment with leaf litter; continuous line represents the control without litter. Whiskers are 95%
confidence intervals. …………………………………………...……………………………… 118
Figure 5.3. Figure 3. Mean gross primary productivity for two sites on Sontecomapan Lagoon
for three different months in 2003. Treatments tested are given in Table 1. Whiskers are 95%
confidence intervals. Empty circles are controls without extract, squares are controls without
extract but with incubating medium, the rhombus are treatments with extract from day 2,
triangles are treatments with extract from day 10, and the filled circles are treatments with extract
from day 45 ……………………………………………….…………………………...………. 119
Figure 5.4. Figure 4. Mean cell density during phytoplankton growth: a) Chaetoceros muelleri
var. subsalsum, b) Cyclotella spp., and c) Skeletonema subsalsum subjected to different
treatments (see Table 1). Whiskers are 95% confidence intervals. Empty circles are controls
without extract, squares are controls without extract but with incubating medium, the rhombus
12
are treatments with extract from day 2, triangles are treatments with extract from day 10, and the
filled circles are treatments with extract from day 45 ..………………………………..……… 120
Figura 6.1. Contribución y efecto de la hojarasca derivada de Rhizophora mangle en la
productividad primaria y composición del fitoplancton en la Laguna de Sontecomapan. La figura
muestra la entrada de nutrientes por los ríos y la hojarasca, los ciclos biogeoquímicos del P y N,
los procesos de acumulación y liberación de nutrientes y taninos por la descomposición de
hojarasca y su relación con los detritívoros, y la dinámica fitoplanctónica caracterizada por las
especies dominantes en cada época climática. Las líneas verticales separan las épocas climáticas:
nortes, secas y lluvias. En la parte de abajo se presentan las constantes de descomposición (k) de
la hojarasca en cada época. Se presentan las especies fitoplanctónicas dominantes a) Skeletonema
subsalsum, b) S. pseudocostatum, c) S. costatum, d) Chaetoceros subtilis var. abnormis f.
simplex, e) Peridinium aff. quinquecorne, f) Ceratium furca var. hircus, g) Thalassiosira
cedarkeyensis, h) Prorocentrum cordatum, i) Scrippsiella sp., j) Cyclotella meneghiniana, k) C.
cryptica, l) C. striata, m) Chaetoceros holsaticus, n) C. simplex, la diatomea o) Chaetoceros
muelleri var. subsalsum, que puede crecer potencialmente y el molusco p) Neritina reclivata
asociado a la descomposición de hojarasca. C = carbono, P = fósforo, N = nitrógeno, SAFF =
sustancias activas al folín fenol. Las letras en negritas representan mayor concentración de estos
nutrientes. Las flechas con O2 en el interior representan la productividad primaria y su tamaño la
intensidad del proceso …………………………………………………………………..…….. 129
Figures 7.1.-7.4. Plate tabulation of Peridinium quinquecorne var. trispinifera. Fig. 1. Ventral
view. Fig. 2. Dorsal view. Fig. 3. Epitheca. Fig. 4. Hypotheca. Scale bar = 20 µm ………..… 144
Figures 7.5.-7.8. Peridinium quinquecorne var. trispinifera LM. Fig. 5. Ventral view. Fig. 6.
Plate pattern of epitheca. Note 1a, large 2a plates and the pore plate (arrow). Fig. 7. View of
13
hypotheca showing three thick spines (arrows) Fig. 8. View of hypotheca with additional small
spines at postcingular plates (arrows). Scale bars = 10 µm …………………………………… 145
Figures 7.9.-7.12. Peridinium quinquecorne var. trispinifera SEM. Fig. 9. Ventral view. Note
1a plate (arrow). Fig. 10. Dorsal view showing 1a plate (arrow) and the large 2a. fig. 11. Position
of spines at hypotheca: one spine at 1’’’’ plate and two at 2’’’’. Fig. 12. Detail of spines. Note
position of spines at edges of plates. Scale bars = 5 µm (Figs 9-11) or 2 µm (Fig. 12) …….… 146
14
LISTA DE TABLAS
Table 2.1. Mean mass production (g) of different fractions of litter and the total for each
month for sites A, B, and C. Letters (a, b) indicate homogenous groups according to the Tukey
test. ……………………………………………………………………………………………… 31
Table 2.2. Summary of ANOVA for remaining leaf mass of Rhizophora mangle. Only
significant interactions are shown. ………………………………………………..……………. 31
Table 2.3. Decay constants for Rhizophora mangle. Values in parentheses represent ±1
standard error. Letters (a, b, c) show homogeneous groups. Intercept estimates are presented as
recommended by Harmon et al. (1999) as well as t50 estimates from the models. …..…………. 33
Table 2.4. Decay constants for different mangrove species. ……………………………..…. 34
Table 3.1. Coefficient of correlations between chemicals and leaf litter fall. …………….… 58
Table 3.2. Mean values (mg g-1) of C, P, N, and tannin concentrations in leaves of R. mangle
by site and month. ………………………………………………………………………...…….. 58
Table 4.1. Annual mean values and concentrations of physicochemical characteristics of the
Sontecomapan Lagoon and three rivers. Standard deviation in parenthesis. * Significantly greater
(P < 0.015). ………………………………………………………………………..……………. 93
Table 4.2. Factor loadings from the first axis extracted from the PCAs on data sets for the
Sontecomapan Lagoon and three rivers. Numbers in bold indicate major loading. ……………. 94
Table 4.3. List of species found in the Sontecomapan Lagoon and the three rivers draining into
it. * indicates a species is present, and ** indicates the species that were used in the CCA
analyses. ………………………………………………………………………………………… 95
Table 4.4. Shanon-Wiener Diversity Index (H’) and evenness by month. Letters a, b, c, d show
significant differences between sites for a given month (P < 0.05). …...………………………. 99
Table 5.1. Characteristics of extracts obtained from decomposing mangrove leaf litter and
used in experiments on primary productivity and phytoplankton growth. …………………… 121
15
Table 5.2. Species composition and cell density (cell ml-1) at the beginning of the experiments
of phytoplankton growth. …………………………………………………………...………… 121
Table 7.1. Descriptive statistics of cell density, salinity and temperature of samples where
Peridinium quinquecorne var. trispinifera occurred. …………………………………...…….. 147
16
RESUMEN
En zonas tropicales y subtropicales las lagunas costeras están rodeadas por comunidades de
manglar que son una fuente de gran cantidad de materia orgánica que entra al sistema acuático a
través de la caída de hojarasca. Esta materia orgánica se descompone llegando a ser una fuente de
nutrientes y otras sustancias como taninos, ácidos fúlvicos y ácidos húmicos que pueden afectar
la composición y productividad de las comunidades fitoplanctónicas. El objetivo de este trabajo
fue analizar la contribución de la hojarasca como aporte directo de materia orgánica proveniente
del manglar (Rhizophora mangle) en la laguna de Sontecomapan, Veracruz, México, y
determinar su efecto en la productividad primaria y composición fitoplanctónica durante un ciclo
anual. En el período comprendido entre Octubre del 2002 a Octubre del 2003, se estudió la
producción de hojarasca y su descomposición evaluando la dinámica del contenido de carbono,
nitrógeno, fósforo y taninos durante estos procesos. Se analizó la relación entre la concentración
de nutrientes y sustancias fenólicas en la laguna con la composición fitoplanctónica. Asimismo se
evaluó experimentalmente el efecto de extractos obtenidos de la descomposición de hojarasca en
la productividad primaria y el crecimiento del fitoplancton de la laguna. Los resultados mostraron
que la hojarasca representa una fuente de fósforo y una trampa de nitrógeno. A través de los
procesos de mineralización y de organismos detritívoros como el gastrópodo Neritina reclivata,
estos nutrientes pueden ser potencialmente utilizados por el fitoplancton. El alto contenido de
taninos en la hojarasca que es liberado a la laguna y la relación encontrada con las diferentes
especies fitoplanctónicas, su productividad primaria y su crecimiento, sugieren que las
concentraciones de las sustancias fenólicas en la laguna contribuyen en la modulación de la
dinámica del fitoplancton estacionalmente.
17
CAPÍTULO 1
Introducción general
18
INTRODUCCIÓN
Los ecosistemas lagunares-estuarinos son sistemas con una alta productividad primaria
acuática. Para algunas lagunas se han registrado valores de producción primaria fitoplanctónica
que alcanzan hasta 16 gCm-2día-1 y que comparados con valores registrados en ambientes
marinos en zonas de surgencia (1 gCm-2día-1) resultan muy elevados (Santoyo 1991). Es
ampliamente conocido el hecho de que la productividad primaria está limitada por la
disponibilidad de nutrientes y otros factores como la luz y la temperatura. El fitoplancton,
principal componente autótrofo del sistema acuático, incorpora compuestos inorgánicos mediante
la fotosíntesis que repercuten en la productividad de todo el sistema. Los principales nutrientes
que limitan el crecimiento del fitoplancton son el amonio y nitratos como fuentes principales de
nitrógeno, ortofosfatos como fuente principal de fósforo, y el sílice, elemento indispensable para
las diatomeas, grupo que resulta importante en la composición del fitoplancton de cualquier
ambiente acuático (Darley 1987). La disponibilidad de estos nutrientes en los sistemas lagunares
está sujeta a una gran variabilidad al conformar sistemas abiertos que permiten la entrada y salida
de tales nutrientes. Las entradas en estos sistemas están dadas por los escurrimientos de agua
dulce que alimentan al sistema y por el aporte de materia orgánica del medio circundante
(Contreras 1993). Aunque existe un intercambio de masas de agua entre la laguna y el mar
dependiendo de la dinámica de comunicación entre estos dos sistemas, el flujo de nutrientes
comúnmente ocurre hacia el mar (De la Lanza-Espino y Rodríguez-Medina 1993), representando
esta conexión una salida de nutrientes del sistema lagunar.
En el caso de las lagunas costeras, una de las principales entradas de nutrientes es a través
del aporte de materia orgánica proveniente de las zonas de manglar (Tam et al. 1990). Este aporte
de materia orgánica se produce como hojas, madera, flores y frutos, y depende de las especies de
19
manglar y los factores climatológicos (Mackey y Smail 1996, Twilley et al. 1997). Los valores de
producción (peso seco) se han reportado entre un intervalo de 170 gm-2 año-1 a 1700 gm-2 año-1
(Arreola-Lizárraga et al. 2004, Wafar et al., 1997), lo que representa un aporte alto de materia
orgánica cuya descomposición se traduce en un suministro de nutrientes y otras sustancias
(Herrera-Silveira y Ramírez-Ramírez 1996) que pueden afectar el flujo de energía de todo el
ecosistema del manglar (Wafar et al. 1997).
Las hojas representan la mayor proporción de los detritus vegetales del manglar (Wafar et
al. 1997) y su descomposición en el medio acuático empieza con una rápida pérdida de sustancias
solubles (Davis III et al. 2003). La degradación microbiana sucede durante todo el proceso y
juega un papel importante en la dinámica del carbono (C), nitrógeno (N) y fósforo (P) (Cundell et
al. 1993). La fragmentación de la hojarasca por los organismos detritívoros acelera el proceso de
descomposición (Asthon et al. 1999).
La velocidad de descomposición de las hojas se ha evaluado a través de la pérdida de peso
seco (Flores-Verdugo et al. 1990, Twilley et al. 1997, Wafar et al. 1997, Davis III et al. 2003) y
comúnmente se expresa como el tiempo necesario para sufrir una pérdida del 50% de la biomasa
inicial (t50) (Mackey y Smail 1996). La velocidad de descomposición varía entre las especies y de
acuerdo a las condiciones climáticas. Así por ejemplo, se han reportado diferencias en el tiempo
de la pérdida total de biomasa de hojarasca entre Rhizophora spp. y Avicennia officinalis, siendo
de 105 días para las primeras y de 56 días para la segunda (Wafar et al. 1997). En una misma
especie el t50 puede variar en diferentes épocas climáticas, como en Avicennia marina que en el
verano varía de 44 a 59 días, mientras que en el invierno el proceso dura de 78 a 98 días (Mackey
y Smail 1996). En diferentes latitudes estas diferencias son notables en Rhizophora mangle. En
Florida hay una pérdida de peso significativa después de 361 días (Davis III et al. 2003) mientras
que en Ecuador el t50 se ha estimado entre 60 y 112 días (Twilley et al. 1997).
20
La dinámica de los nutrientes durante la descomposición de hojarasca de manglar ha sido
estudiada ampliamente y los resultados muestran una gran variación en la dinámica de C, N, y P
(Rice y Tenore 1987, Tam et al. 1990, Chale 1993). Diferentes patrones de acumulación y
liberación de diferentes nutrientes pueden suceder en el tiempo (Harmon et al. 1999), por lo que
las características químicas de la hojarasca y las características del ambiente parecen ser
importantes para que sucedan estos procesos y afecten su duración (Davis III et al. 2003).
Muchos trabajos han demostrado la influencia positiva de los escurrimientos provenientes
de las zonas de manglar en los productores primarios planctónicos (Rivera-Monrroy et al. 1998,
Flores-Verdugo et al. 1990, Wolf et al. 2000). Este efecto es el resultado de las elevadas
concentraciones de nutrientes disueltos en el agua de los escurrimientos de tales zonas (Dham et
al. 2002). Sin embargo, junto con estos nutrientes, se encuentran otros compuestos orgánicos
disueltos de origen vegetal que tienen implicaciones en las funciones biológicas del sistema.
Entre estos compuestos de importancia ecológica se encuentran las sustancias húmicas, en cuya
formación se involucran a las ligninas y diversos compuestos fenólicos como los taninos (Weber
2005). Se ha demostrado que estas sustancias en ambientes naturales tienen un efecto positivo
(Conzonno y Fernández 1996, Danilov y Ekelund 2001) o negativo (Jackson y Hecky 1980,
Guildford et al. 1987) en las funciones de los productores primarios. Bioensayos en diferentes
especies fitoplanctónicas han mostrado que la respuesta en el crecimiento depende de la
concentración de tales compuestos, pudiendo estimularlo o inhibirlo. Por lo tanto, en sistemas
naturales la respuesta depende de la naturaleza química de las sustancia y la composición
fitoplanctónica de la comunidad (Klug 2002).
La mayoría de los trabajos hechos con anterioridad han evaluado en forma aislada ya sea
la producción de hojarasca o la dinámica de su descomposición y son pocos los trabajos que
integran estos dos aspectos (Wafar et al. 1997). Por otro lado, aunque existen trabajos
21
relacionados con la producción primaria fitoplanctónica y su relación con ambientes de manglar,
son escasos los trabajos que consideren la composición de especies fitoplanctónicas que puede
estar influyendo en la respuesta (Herrera-Silveira y Ramírez-Ramírez 1996).
En este trabajo se estudiaron los aspectos de producción de hojarasca, la dinámica de su
descomposición, y su posible relación con ciertas características biológicas de la comunidad
fitoplanctónica (productividad primaria y composición de especies) en la laguna de
Sontecomapan, Veracruz, México. Esta laguna está rodeada por una gran extensión de manglar
donde la especie dominante es Rhizophora mangle L. (Menéndez 1976). Por lo tanto, para
integrar los aspectos estudiados, se planteó como objetivo general analizar la contribución como
aporte directo de la hojarasca proveniente del manglar (Rhizophora mangle) en la laguna y
determinar su efecto en la productividad primaria y composición fitoplanctónica en un ciclo
anual. Para llevar a cabo este objetivo general, se plantearon cuatro diferentes hipótesis y
objetivos particulares que fueron los ejes conductores de esta investigación.
La primera hipótesis planteada fue que debido a las condiciones climáticas que se
presentan en el Golfo de México y que se resumen en tres periodos (nortes, secas y lluvias), la
dinámica de producción y descomposición de hojarasca de Rhizophora mangle presenta
variaciones con respecto a estas estaciones climáticas. Como objetivo particular para probar esta
hipótesis se planteó determinar el aporte de biomasa de hojarasca proveniente de Rhizophora
mangle y el tiempo de descomposición en la laguna en un ciclo anual (Capítulo 2).
Dado que algunos de los nutrientes y compuestos que afectan a los productores primarios
son compuestos nitrogenados, ortofosfatos así como sustancias fenólicas, la segunda hipótesis se
planteó con base en la dinámica de los nutrientes y taninos contenidos en la hojarasca. Esta
hipótesis propone que independientemente de la dinámica de producción de hojarasca y pérdida
de biomasa durante la descomposición, debido a la dinámica del contenido de C, N, P y taninos,
22
la hojarasca es una fuente de nutrientes y sustancias fenólicas que son liberados directamente al
medio con una variación estacional. El objetivo particular fue entonces determinar el contenido
de C, N, P y taninos de las hojas de R. mangle y su dinámica durante la producción de hojarasca
y durante su descomposición en un ciclo anual (Capítulo 3).
Como tercera hipótesis se planteó que si la producción de hojarasca representa el ingreso
de una cantidad grande de materia orgánica y ésta tiene un efecto en la comunidad
fitoplanctónica, entonces la concentración de nutrientes y sustancias fenólicas en la laguna
presenta una dinámica similar a la producción de hojarasca y la composición y densidad de
especies fitoplanctónicas varían estacionalmente de acuerdo a la concentración de sustancias
fenólicas en la columna de agua. Así el objetivo para probar esta hipótesis fue analizar la
concentración de amonio, nitratos, ortofosfatos, silicatos y sustancias fenólicas en la laguna en un
ciclo anual y estudiar su relación con la composición fitoplanctónica (Capítulo 4).
La última hipótesis fue que si realmente los productos de la descomposición de hojarasca
de mangle tienen un efecto en las funciones fisiológicas del fitoplancton y tal efecto depende de
la composición de especies, entonces los nutrientes y sustancias fenólicas derivadas de la
descomposición de la hojarasca en distintos días, tienen efectos diferentes en la productividad
primaria y el crecimiento fitoplanctónico en cada época climática. Por lo tanto el objetivo
particular para probar esta hipótesis fue examinar el efecto de las sustancias liberadas de la
descomposición de la hojarasca de Rhizophora mangle en la productividad primaria y
crecimiento fitoplanctónica en las tres épocas características de la región (Capítulo 5).
LITERATURA CITADA
23
Ashton, E. C., P. J. Hogarth y R. Ormond. 1999. Breakdown of mangrove leaf litter in a managed
mangrove forest in Peninsular Malaysia. Hydrobiologia 413: 77-88.
Arreola-Lizárraga, J. A., F. J. Flores-Verdugo, y A. Ortega-Rubio. 2004. Structure and litterfall
of an arid mangrove stand on the Gulf of California, Mexico. Aquatic Botany 79: 137-143.
Contreras, F. 1993. Ecosistemas costeros mexicanos. CONABIO-UAMI. México, 415 pp.
Conzonno, V. H. y A. Fernandez. 1996. Humic substances and phytoplankton primary production
in Chascomus pond (Argentina). Facts and speculations. Revista de la Asociación de Ciencias
Naturales y Litoral 27: 35-42
Cundell, A. M., M. S. Brown, R. Standford, R.Mitchell. 1979. Microbial degradation of
Rhizophora mangle leaves immersed in the sea. Estuarine, Coastal and Shelf Science 9, 281286.
Chale, F. M. M. 1993. Degradation of mangrove leaf litter under aerobic conditions.
Hydrobiologia 257: 177-183.
Danilov, R. A. y N. G. A. Ekelund. 2001. Effects of solar radiation, humic substances and
nutrients on phytoplankton biomass and distribution in lake Solumsjö, Sweden.
Hydrobyologia 444, 2003-212.
Davis III, S. E., C. Corronado-Molina, D. L. Childers, J. W. Day, Jr. 2003. Temporally dependent
C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter in
oligotrophic mangrove wetlands of the Southern Everglades. Aquatic Botany 75: 199-215.
Darley, W. M. 1987. Biología de las algas. Enfoque fisiológico. Limusa, México. 236 pp.
De la Lanza-Espino G. y M. A. Rodríguez-Medina. 1993. Nutrient exchange between subtropical
lagoons and the marine environment. Estuaries 16: 273-279.
Dham, V. V., A. M. Heredia, S. Wafar y M. Wafar. 2002. Seasonal variations in uptake and in
situ regeneration of nitrogen in mangrove waters. Limnology and Oceanography 47. 241-254.
24
Flores-Verdugo, F., F. González-Farías, O. Ramírez-Flores, F. Amescua-Linares, A. YánezArancibia, M. Alvarez-Rubio, y J. W. Day, Jr. 1990. Mangrove ecology, aquatic primary
productivity, and fish community dynamics in the Teacapán-Agua Brava Lagoon-Estuarine
system (Mexican Pacific). Estuaries 13(2): 219-230.
Guildford, S. J., F. P. Healey y R. E. Hecky. 1987. Depression of primary production by humic
matter and suspended sediment in limnocorral experiments at Southern Indian Lake, northern
Manitoba. Canadian Journal of Fisheries and Aquatic Sciences 44: 1408-1417.
Harmon, M. E., K. J. Nadelhoffer y J. M. Balir. 1999. Measuring decomposition, nutrient
turnover, and stores in plant litter. Páginas 202-240 in G. P. Robertson, D. C. Coleman, C. S.
Bledsoe y P. Sollins, editors. Standard Soil Methods for Long-term Ecological Research.
Oxford University Press, Inc. USA.
Herrera-Silveira, J. A. y J. Ramírez-Ramírez. 1996. Effect of natural phenolic material (tannin)
on phytoplankton growth. Limnology and Oceanography 41: 1018-1023.
Jackson, T. A. y R. E. Hecky. 1980. Depression of primary productivity by humic matter in lake
and reservoir waters of the boreal forest zone. Canadian Journal of Fisheries and Aquatic
Sciences 37: 2300-2317.
Klug, J. L. 2002. Positive and negative effects of allchtonous dissolved organic matter and
inorganic nutrients on phytoplanlton growth. Canadian Journal of Fisheries and Aquatic
Sciences 59: 85-95.
Menéndez, L. F. 1976. Los manglares de la laguna de Sontecomapan, Los Tuxtlas, Veracruz.
Estudio florístico ecológico. Tesis de Licenciatura, Univ. Nal. Autón. México, México. 115pp.
Mackey, A. P. y G. Smail. 1996. The decomposition of mangrove litter in a subtropical mangrove
forest. Hydrobiologia 332: 93-98.
25
Rice, D. L. y K. R. Tenore. 1981. Dynamics of carbon and nitrogen during the decomposition of
detritus derived from estuarine macrophytes. Estuarine, Coastal and Shelf Science 13: 681690.
Rivera-Monroy, V. H., C. J. Madden, J. W. Day, Jr, R. R. Twilley, F. Vera.Herrera y H. AlvarezGuillén. 1998. Seasonal coupling of a tropical mangrove forest and estuarine water column:
enhancement of aquatic primary productivity. Hydrobiologia 379: 41-53.
Santoyo, H. 1991. Fitoplancton y productividad de lagunas costeras. Páginas 31-45 in G.
Figueroa, C. Alvarez, A. Esquivel y E. Ponce, editores. Serie Grandes temas de la
Hidrobiología 1. Fisicoquímica y biología de las lagunas costeras Mexicanas. UAMIztapalapa, México.
Tam, N. F. Y., L. L. P. Vrijmoed y Y. S. Wong, 1990. Nutrient dynamics associated with leaf
decomposition in a small subtropical mangrove community in Hong Kong. Bulletin of Marine
Science 47, 68-78.
Twilley, R. R., M. Pozo, V. H. García, V. H. Rivera-Monroy, R. Zambrano y A. Bodero. 1997.
Litter dynamics in riverine mangrove forests in the Guayas River estuary, Ecuador. Oecologia
111: 109-122.
Wafar, S., A. G. Untawale y M. Wafar. 1997. Litter fall and energy flux in a mangrove
ecosystem. Estuarine, Coastal and Shelf Science 44: 111-124.
Weber, J. 2005. Definition of soil organic matter and humic acids based products.
http//www.humintech.com/01/articles/articles_definition_of_soil_organic_matter3.html
Wolff, M., V. Koch y V. Isaac. 2000. A trophic model flor of the Casté mangrove Estuary (North
Brazil) with considerations for the sustainable use of its resources. Estuarine, Coastal and
Shelf Science 50: 789-803.
26
CAPÍTULO 2
Litterfall and decomposition of Rhizophora mangle L. in a coastal lagoon in the southern
Gulf of Mexico
Hydrobiologia 2006, 559: 101-111
27
Springer 2006
Hydrobiologia (2006) 559:101–111
DOI 10.1007/s10750-005-0959-x
Primary Research Paper
Litterfall and decomposition of Rhizophora mangle L. in a coastal lagoon
in the southern Gulf of Mexico
José Antolı́n Aké-Castillo*, Gabriela Vázquez & Jorge López-Portillo
Ecologıá Funcional, Instituto de Ecologia, A. C., Km. 2.5 Carretera Antigua a Coatepec No. 351, Congregacıón El Haya,
Xalapa, Veracruz, Me´xico
(*Author for correspondence: Tel.: +52-228-8421800 ext. 4201; Fax: +52-228-8421800 ext. 4222; E-mail: ake@
posgrado.ecologia.edu.mx, [email protected])
Received 8 September 2004; in revised form 14 June 2005; accepted 24 June 2005
Key words: brackish water, decay constant, leaf litter, litter bag, mangrove, Mexico
Abstract
The dynamics of Rhizophora mangle litter production and decomposition were studied in a tropical coastal
lagoon on the Gulf of Mexico in Veracruz, Mexico over a year (October 2002–October 2003). This region is
characterized by three seasons: northerly winds (called ‘nortes’), dry, and rainy. Annual litter production
(1116 g m)2) followed a seasonal pattern with leaf litter as the main fraction (70%) with two peaks in the dry
and one in the rainy season. Leaf decomposition was evaluated with two types of litter bag in each season:
fine mesh (11 mm) and coarse mesh (37 mm). Decomposition data were adjusted to a single negative
exponential model. The results indicated faster decomposition rates in the coarse litter bag and significant
differences among seasons. However these differences occurred after the 60th day of decomposition, indicating that leaching and microbial action were responsible for more than 50% of mass loss. After this period,
the effects of aquatic invertebrates were evident but depended on climatic conditions. In the rainy season, the
gastropod Neritina reclivata was associated with increasing leaf decomposition rate. In the ‘nortes’ season,
the effect of aquatic invertebrates was smaller, and there were no differences in the decay constants calculated
for the two litter bag types. High litter production represents an important input of organic matter which,
through decomposition, may represent an important source of C, N, and P in this aquatic system.
Mangrove communities are diverse and their
species composition varies longitudinally through
out the world (Tomlinson, 1986), so the litter
production and decomposition of different species
have been studied worldwide. Depending on the
species and climatic factors, litterfall varies from
3.4 to 17 ton ha)1 year)1 (Flores-Verdugo et al.,
1990; Wafar et al., 1997) and leaf litter has been
recognized as the main fraction commonly determining litterfall dynamics (Wafar et al., 1997).
Most of these studies have been oriented towards
determining the time needed for 50% of an initial
mass to disappear (t50) and this value is commonly
compared among species. Estimates of t50 for
Introduction
Many studies have shown that the mangrove community is an important source of nutrients for
adjacent zones (Rivera-Monroy et al., 1995) and
directly enhances phytoplankton production (Rivera-Monroy et al., 1998). As mangrove litterfall
drops into the lagoon, a flow of energy, driven by
decomposition processes, is established between the
mangrove and its surrounding aquatic environment. Lugo & Snedaker (1974) stressed the importance of functional mangrove studies to illustrate
how a balance is established and maintained among
the components of the whole ecosystem.
28
102
different species of mangrove range from 7 to
361 days, varying even within the same species
(Flores-Verdugo et al., 1987; Twilley et al., 1997;
Wafar et al., 1997; Davis et al., 2003).
Studies of the abiotic and biotic factors
involved in the decomposition process have been
carried out and among the abiotic factors that
increase the decomposition rate are tidal movement (Mackey & Smail, 1996; Flores-Verdugo
et al., 1987; Tovilla & de la Lanza, 1999), high
salinity (Twilley et al., 1997) and temperature
(Mackey & Smail, 1996). Among the biotic
factors, bacteria and fungi have been shown to be
very important at the onset of decomposition
(Cundell et al., 1979). Robertson (1986) and
Middleton & Mckee (2001), noted important
effects of aquatic invertebrates on the removal of
leaf litter in studies dealing mainly with the influence of large crustaceans inhabiting the intertidal
zone.
In Mexico, most studies have been oriented
toward the evaluation of the litterfall production
of the four species present in the country:
Avicennia germinans L., Laguncularia racemosa
L., Conocarpus erectus L., and Rhizophora mangle
L. (Rico-Gray & Lot, 1983; López-Portillo &
Ezcurra, 1985; Flores-Verdugo et al., 1990; Day
et al., 1996; Barreiro-Güemes, 1999), but information on the decomposition of these species in
Mexican coastal systems is limited to L. racemosa
(Flores-Verdugo et al., 1987) and C. erectus
(Tovilla & de la Lanza, 1999). Sontecomapan
Lagoon is located in the coastal portion of The
Tuxtlas Biosphere Reserve, and R. mangle is the
dominant species of the margin and some inner
parts of the lagoon. Litterfall from this species
falls in a zone that is hydrologically dynamic
owing to tides, making for short residence time
on the forest floor; litterfall is quickly transported
to the lagoon and constantly submerged during
decomposition. In order to understand the
litterfall and decomposition processes of R.
mangle in this lagoon, the objectives of this study
were: (a) to evaluate litterfall production during a
1-year cycle at three sites with different hydrological dynamics, (b) to estimate decomposition
rates through a decay model for different climatic
periods under totally submerged conditions, and
(c) to evaluate the effect of macroinvertebrates on
the decomposition rate.
Study site
Sontecomapan Lagoon is located to the south of
the Gulf of Mexico between 1830¢ and 1834¢ N
lat., and 9459¢ and 9504¢ W long., along a volcanic coastline (Fig. 1). The climate in this region
is humid tropical (3000–4000 mm of rain year)1)
and is characterized by three seasons: dry from
March to May, rainy from June to September, and
‘nortes’ from October to February (Day et al.,
1996). This last season is characterized by cold
fronts that produce strong winds and rain, and by
the presence of tropical storms and hurricanes.
Sontecomapan Lagoon is classified as a
tectonic type of volcanic origin extensively modified by run-off (Lankford, 1977). It is 12 km long
and 1.5 km wide, and covers an area of 943.5 ha.
Connection with the sea is permanent through a
15 m deep channel, but the mean depth of the
whole lagoon is only about 1.5 m. The tidal regime
is semidiurnal with a tidal range lower than 60 cm.
Three permanent rivers drain into the lagoon and
it is also fed by small creeks during the rainy
season. The lagoon is a brackish water system
where salinity varies spatially and temporally from
0 to 35& (Aké-Castillo et al., 1995).
This lagoon is bordered by a mangrove forest
formed by R. mangle, L. racemosa, and A.
germinans, the former being the dominant species
in the system (Menéndez, 1976). Total mangrove
area is estimated to be 533.8 ha (Aké-Castillo:
unpublished data). Along the river and creek
margins, R. mangle is mixed with riparian species
such as Pachira aquatica Aubl. and the fern
Achrostichum aureum L. is also associated in their
interior. This system shelters a high diversity of
epiphytes (bromeliads, orchids, and cacti).
Material and methods
The study period was from October 2002 through
October 2003. Three sites were selected in preserved mangrove zones of the three lagoon basins
(Fig. 1). Site A, representing a mangrove fringe
remnant, is located in the western part of the
lagoon, in the basin where the main river drains
into it. Site B is located in the smallest basin, a
zone with little hydrological dynamics as no rivers
drain into it. Site C is located in the basin which is
29
103
Litterfall was dried to a constant weight for 48 h at
60 C. Morphological components were separated
into leaves, twigs, flowers, and propagules (LópezPortillo & Ezcurra, 1985) and weighed with a
10)4 g precision analytical balance.
To determine differences in total, leaf, flower,
propagule, and twig production among months, a
one-factor repeated measures ANOVA by ranks
was performed. Significant differences were
identified using Tukey tests. For these analyses,
data from November were excluded as no complete records were available for one site due to the
loss of the baskets. Differences in monthly leaf,
flower, propagule, and total production among
sites were evaluated with a Kruskal–Wallis test
followed by multiple comparisons of mean ranks
to detect the differences. All statistical analyses
were conducted with Statistica 6.1 (StatSoft, 2003)
and SigmaStat 2.03 (SPSS, 1997).
Decomposition
Leaf decomposition rate was evaluated using the
litter bag technique (Wieder & Lang, 1982;
Harmon et al., 1999). Senescent yellow leaves were
collected from the three sites, and air dried for
20 days and then mixed (Mackey & Smail, 1996).
Nylon litter bags of two types, fine (11 mm) and
coarse mesh (37 mm) measuring 2020 cm, were
filled with 10 g of air dried leaves. Following
Twilley et al. (1997), at the beginning of each
season, three lines with five fine litter bags spaced
50 cm apart, and three lines with five coarse litter
bags, were placed randomly at each site along the
same transect as the baskets. The lines were tied to
R. mangle roots and remained submerged
throughout the study period. Three bags of each
type were retained to correct initial leaf weights by
drying leaves to constant weights at 60 C. One
bag from each line was collected every month, so
that 30, 60, 90, 120 and 150 days of accumulated
decomposition were estimated for each season.
Material from litter bags was rinsed with fresh
water and then with distilled water using sieves
with mesh sizes 5, 2, 0.5, and 0.25 mm in order to
recover the remaining material and to separate
organisms (Middleton & Mckee, 2001). Leaf
material thus obtained was dried to a constant
weight at 60 C (Mackey & Smail, 1996).
Figure 1. Location of Sontecomapan Lagoon and the mangrove sites studied. Gray fill indicates the distribution of mangrove forest surrounding the lagoon. A, B and C represent the
sites studied.
directly influenced by tidal currents and run-off
from a small river. Sites B and C represent well
preserved mangrove zones. Water salinity was
recorded monthly at each site (YSI Mod. 30
portable Meter).
Litterfall
Litterfall was collected in 0.28 m2 baskets
constructed with a 4 mm nylon mesh (FloresVerdugo et al., 1987; Day et al., 1996). Following
Twilley et al. (1997), a 50 m transect parallel to the
margin of the lagoon was established at each site
and 10 baskets were randomly hung along the
transect above the highest water level marks on
roots. Material from baskets was collected
monthly and transported to the laboratory.
30
104
A nested factorial ANOVA (days of decomposition nested in season) with arcsin transformed data
(Zar, 1999) was carried out in order to evaluate the
effect of the following factors: season, site, mesh size
of litter bag and days of leaf litter decomposition.
To calculate a decay constant (k) as an
estimator of decomposition velocity (Mackey &
Smail, 1996), the percentages of remaining mass
for each season and type of mesh litter bag were
fitted to a single exponential negative function
Yf=Yi exp)kt where k=decay constant, t=any
time, Yf=mass remaining at t, Yi=initial mass.
An analysis of covariance (ANCOVA) was
performed to test differences among the estimated
k (Wieder & Lang, 1982). To identify the k that
differed, a Tukey test was used. All analyses and
model adjustments were made with Statistica 6.1
(StatSoft, 2003). For the ANCOVA we followed
the procedure indicated by Zar (1999).
determined the total pattern. Leaf litter peaks were
registered in the dry season (March and May),
contrasting with low production in April (q=4.65,
p<0.05; q=5.93, p<0.05). Flower litter followed
the two leaf litter peaks (dry season) reaching a
maximum value in September, a month that differed significantly from those of the ‘nortes’ and
dry seasons (q values ‡ 5.9, p<0.05). Propagule
production followed an increasingly similar pattern to that of flower litter until September and
reached a maximum value in October (beginning
of the ‘nortes’ season), a month when flower litter
diminished markedly. Twig litter showed a peak in
March mirroring that of leaf litterfall (Fig. 3).
Leaf litter and twig litter showed differences
among sites in one month (leaf litter in August:
H=7.8, d.f.=2, p=0.01; twig litter in March:
H=8.5, d.f.=2, p=0.01), whereas flower litter was
the fraction with most differences among sites in
different months (December: H=10.4, d.f.=2,
p=0.005; January: H=13.8, d.f.=2, p=0.001;
February: H=15.3, d.f. = 2, p<0.001; March:
H=7.96, d.f.=2, p=0.018; May: H=13.2,
d.f.=2, p=0.001; June: H=6.2, d.f.=2, p=
0.044). Site C had the most differences among sites
for all litter fractions: for leaf litter in August site
C differed from site A (z=2.71, p=0.01); for twig
litter in March site C differed from site A (z=
2.84, p=0.01); and for flower litter in December,
February, May, and June site C differed from site
B (z=3.3, p=0.003; z=3.8, p<0.001, z=3.62, p<
0.001; z=2.4, p=0.037, respectively for each
month); in January site C differed from sites A and
B (z=2.76, p=0.017; z=3.4, p=0.001), and in
March site C differed from site A (z=2.46, p=
0.041). Total litterfall was not different among
sites for any month (Table 1).
Results
Salinity
Spatial variation is noteworthy, with site C having
the highest salinities recorded in February, May
and June (Fig. 2). Salinities below 10& were
recorded in the ‘nortes’ season as well as in the
rainy season at the three sites.
Litterfall
Total litterfall had three peaks with the greatest
values recorded in September, corresponding to
the late rainy season, and in March and May,
corresponding to the beginning and end of the dry
season (Fig. 3). Minimum litter production was
recorded from November 2002 to February 2003
(within the ‘nortes’ season). Leaf litter represented
the greatest percentage of total annual litter production (70%), followed by flower litter (15%),
twigs (10%), and propagules (5%).
Variation in litter fraction production showed
significant differences over time (leaf litter: v2=
132.3, d.f.=10, p £ 0.001; flower litter: v2=134.4,
d.f.=10, p £ 0.001; propagule litter: v2=29.4,
d.f.=10, p £ 0.001; twig litter: v2=43.4, d.f.=10,
p £ 0.001; total litter: v2=118.2, d.f.=10, p £
0.001) (Fig. 3). As the highest fraction, leaf litter
Decomposition
There were significant differences in the remaining
mass among seasons and between litter bag types
(Table 2). There was a significant interaction
between litter bag type and days of decomposition,
and differences between litter bag types occurred
regardless of the season.
Significant differences in remaining mass
between litter bags types were detected after
60 days (Fig. 4), with the coarse litter bag having
31
105
Figure 2. Salinity for each site by month. Circle: site A, square: site B, rhombus: site C.
the lowest remaining mass. The effect of season is
marked after 60 days of decomposition, with the
highest remaining mass in the ‘nortes’ season and
the lowest in the rainy season (Fig. 5).
There was a rapid initial loss of mass during the
first month and this represented 40% of the initial
mass for all three seasons and the two litter bag
types (Fig. 6). In the ‘nortes’ season there were no
Figure 3. Monthly litterfall production of Rhizophora mangle in the Sontecomapan Lagoon from November 2002 to October 2003 for
each season. Vertical bars represent 95% confidence intervals. Plus symbol: total litterfall, square: leaf fall, rhombus: flower fall, circle:
propagule fall, triangle: twig fall.
32
106
Table 1. Mean mass production (g) of different fractions of litter and the total for each month for sites A, B, and C
Litter
Site
Dec
Jan
Feb
Mar
Apr
Leaf
A
20.4a
33.3a
30.9a
104.46a
67.9a
96.0a
68.9a
62.9a
67.8a
86.3a
66.9a
B
26.0a
22.0a
35.9a
96.04a
67.7a
106.5a
81.5a
81.8a
79.6ab
90.7a
80.4a
C
A
17.6a
4.5ab
30.9a
6.4a
28.1a
3.1ab
92.61a
5.70a
49.5a
0.9a
142.5a
7.4ab
77.5a
20.9ab
79.2a
27.4a
97.7b
21.1a
91.9a
31.5a
67.7a
18.3a
24.2a
Flower
Propagule
Twig
Total
May
Jun
Jul
Aug
Sep
Oct
B
9.8a
6.6a
9.4a
3.63ab
0.9a
13.4a
28.2a
29.3a
24.8a
45.9a
C
1.9b
0.1b
0.0b
1.25b
0.2a
1.5b
14.8b
20.5a
27.2a
30.6a
19.1a
A
0.3a
0.2a
1.5a
4.57a
1.9a
2.3a
7.2a
8.7a
8.9a
30.4a
31.8a
B
1.0a
1.0a
0.3a
2.32a
0.0a
0.0a
0.0a
1.3a
0.7a
6.5a
11.3a
C
1.7a
0.0a
1.3a
0.67a
0.5a
4.1a
1.5a
2.1a
8.6a
13.2a
14.2a
A
0.4a
9.0a
0.9a
76.16a
5.1a
0.7a
3.2a
25.8a
2.1a
5.3a
7.5a
B
C
1.7a
23.1a
5.6a
4.1a
2.5a
21.1a
14.95ab
12.05b
12.4a
10.4a
0.1a
0.0a
0.1a
0.0a
0.3a
2.8a
8.5a
1.2a
24.4a
5.8a
2.8a
11.7a
A
25.6a
48.8a
37.1a
190.91a
75.8a
106.4a
100.2a
124.9a
99.8a
153.6a
124.5a
B
38.4a
35.3a
48.2a
116.95a
81.1a
119.9a
109.8a
112.7a
113.6a
167.4a
118.6a
C
44.5a
35.2a
50.6a
106.59a
60.7a
148.1a
93.8a
104.5a
134.6a
141.5a
112.7a
Letters (a, b) indicate homogenous groups according to the Tukey test.
Discussion
Table 2. Summary of ANOVA for remaining leaf mass of
Rhizophora mangle
Source of variation
Season (S)
Site (ST)
Litter bag type (L)
Day of decomposition (D) nested in (S)
LD
F
Litterfall
p
45.44
0.0001
0.24
104.41
NS
0.0001
27.33
0.0001
3.07
0.0001
The peaks of litterfall production registered in the
dry and rainy seasons, matched the peaks reported
for the same species by Rico-Gray & Lot (1983)
and Day et al. (1996) for two close coastal
lagoons situated to the north and south of
Sontecomapan Lagoon. Twilley et al. (1986)
reported only one peak in south-western Florida,
USA, at 25N lat.
Barreiro-Güemes (1999) recorded the highest
production of R. mangle in a coastal system in the
southern Gulf of Mexico during both the rainy
and ‘nortes’ seasons. This was, however, an
exceptional case: at the beginning of the ‘nortes’
season, two cyclones caused unprecedented litterfall production. In Sontecomapan Lagoon, even
though 36 cold fronts, 4 hurricanes, and 10
tropical storms were registered from December
2002 to February 2003, litterfall records show the
lowest values. This low litter production could be a
consequence of low leaf availability resulting from
the peak litterfall of the previous period.
The total litterfall pattern was determined
mainly by the leaf litter fraction. Even though the
highest peak of total litterfall occurred during the
Only significant interactions are shown.
differences between litter bag types until day 150.
For the dry and rainy season, these differences
occurred after 60 days.
Estimates of decay constants (k) of the single
exponential model for each litter bag type per
season are shown in Table 3. The ANCOVA
revealed significant differences among k (F=10.59,
p<0.05). In the ‘nortes’ season, there were no
significant differences in k for the two litter bag
types (q=3.26, p>0.05), while in the dry and rainy
seasons k differed with litter bag type (q=5.98,
p<0.05; q=5.04, p<0.05). Significant differences
between the ‘nortes’ and rainy season were noted
only for the coarse litter bag (q=4.32, p<0.05).
Intercept values were significantly lower than
100%.
33
107
Figure 4. Mass of Rhizophora mangle leaves remaining in fine mesh litter bags (circle) and coarse mesh litter bags (square). Vertical
bars represent 95% confidence intervals.
rainy season, the highest peak for leaf litter
occurred in the dry season. In this period, there
was a notable decrease in April, resulting in two
peaks during this dry season. The peak recorded in
March could be the result of leaf age (refoliation
takes 3–5 months: Barreiro-Güemes, 1999), and
the peak recorded in May, in addition to the aging
process, could be the result of saline stress, which
may induce abscission of leaves (Orcutt & Nilsen,
2000) as a consequence of the increase of the
salinity in the lagoon that we recorded. The
September litterfall peak matched the increase in
flower and propagule litter, as was found for the
same species in the Atasta-Pom system
Figure 5. Mass of Rhizophora mangle leaves remaining in litter bags during the ‘nortes’ (circle), dry (square) and rainy season
(rhombus). Vertical bars represent 95% confidence intervals.
34
108
Figure 6. Mass of Rhizophora mangle leaves remaining in fine mesh litter bags (circle) and coarse mesh litter bags (square) in the
‘nortes’, dry and rainy seasons. Vertical bars represent 95% confidence intervals.
Table 3. Decay constants for Rhizophora mangle
Season
Litter bag
Intercept
k
r2
t50
Nortes
Fine
87.46 (3.23)
0.0048 (0.0005) a
0.63
144
Coarse
91.03 (3.59)
0.0075 (0.0007) ab
0.76
121
Fine
88.15 (2.76)
0.0057 (0.0004) a
0.77
82
Coarse
93.59 (2.81)
0.0099 (0.0005) bc
0.87
92
Fine
Coarse
91.08 (2.71)
96.47 (2.86)
0.0084 (0.0006) ab
0.0142 (0.0008) c
0.84
0.91
70
48
Dry
Rainy
Values in parentheses represent ±1 standard error. Letters (a, b, c) show homogeneous groups. Intercept estimates are presented as
recommended by Harmon et al. (1999) as well as t50 estimates from the models.
(Barreiro-Güemes, 1999). Flower litter was the
only fraction that showed more differences among
the sites studied, with site C differing from the
other sites. This site is more exposed to marine
influence than the others, so variation in salinity is
greater due to tidal effects.
Annual R. mangle litterfall in Sontecomapan
Lagoon (1116 g m)2) is high compared to estimates for other regions: 248–319 g m)2 in
La Mancha, Mexico (Rico-Gray & Lot, 1983);
337–442 g m)2 in Florida, USA (Twilley et al.,
1986);
630–1040 g m)2
(R.
mangle
and
R. harrisonii) in Guayas River Estuary, Ecuador
(Twilley et al., 1997); 1048 g m)2 in Atasta-Pom,
Mexico (Barreiro-Güemes, 1999). In Sontecomapan, mangrove trees vary between 10 and 25 m in
height (Menéndez, 1976) so high litterfall and,
ultimately, mangrove species productivity may be
associated with greater mangrove height (Saenger
& Snedaker, 1993).
Decomposition
The difference between the two litter bag types
suggests the effect of a fractioning mechanism in
the decomposition process. In addition to hydrological dynamics such as currents and tides
(Tovilla & de la Lanza, 1999), fractioning may be
caused by aquatic invertebrates. Gastropods,
amphipods, polichaetes, and decapods were found
consistently during all seasons in the material
extracted from the coarse litter bags. Robertson
35
109
(1986) and Middleton & Mckee (2001) have
associated these organisms with the decomposition
process. Their influence on leaf decomposition,
regardless of the season, was unnoticed until leaves
had been submerged for 60 days. During the first
2 months, decomposition processes can be attributed to leaching, and fungal and bacterial action
(Davis et al., 2003). These mechanisms were
responsible for a mass loss of 50% or more as
found in the rainy season.
After 60 days, differences among seasons were
noticeable and factors associated with each season
affected leaf decomposition differently. Decomposition rate during the rainy season was the
fastest and the gastropod Neritina reclivata (Say),
which was collected from the litter bags at all
stages, also reached its maximum biomass in this
season (mean wet weight 5.16±1.8 g bag)1 vs.
1.7±0.6 g bag)1
in
the
‘nortes’
and
1.18±0.1 g bag)1 in the dry season). This suggests that leaf decomposition could be related to
the seasonal population growth of aquatic invertebrates. Slim et al. (1997) found that the
gastropod Terebralia palustris (Linnaeus) played
an important role in removing the leaves of
Rhizophora species by consuming them, and
N. reclivata may be acting similarly in Sontecomapan Lagoon.
Studies on R. mangle leaf decomposition have
estimated that k ranges from 0.003 to 0.016
(Twilley et al., 1986, 1997). Decay constants esti-
mated in the present study fall within that interval.
In the dry season, the k value for the coarse litter
bag was as high as that of the rainy season (no
significant difference). Since the dry season lasts
only three months, the estimates over 90 days included two months of the rainy season. The fact
that during the ‘nortes’ season the k values for the
two litter bag types did not differ indicates that
climatic conditions are important for the establishment of the aquatic invertebrates that
contribute to leaf litter removal as we observed
with N. reclivata in the rainy season.
Rhizophora mangle decay constants estimated
in this study are similar to those for species of the
same family (Table 4). The greatest value reported
for a mangrove species corresponds to L. racemosa
and the lowest to Sonneratia alba. These species
preferentially establish on the extremes of Rhizophora species (marginal communities). The former
is typically restricted to the landward fringe, while
the second often forms a seaward fringe
(Tomlinson, 1986).
In studies focusing on mangrove litter decomposition, the single negative exponential model has
been used extensively and seems to be effective as
determination coefficients have high values
(Flores-Verdugo et al., 1987; Mackey & Smail,
1996; Wafar et al., 1997; Twilley et al., 1997). The
determination coefficients from our study ranged
from 0.63 to 0.91, and are similar to estimates for
different Rhizophora species (Ashton et al., 1999).
Table 4. Decay constants for different mangrove species
Species
k
Reference
Rhizophora mangle L.
0.0048–0.0142
This study
0.003, 0.005
Twilley et al. (1986) in Twilley et al. (1997)
R. harrisonii Leech. and R. mangle
0.0062–0.0114
Twilley et al. (1997)
R. apiculata Blume
0.0024
Wafar et al. (1997)
R. mucronata Lamk.
0.0091, 0.0163
0.0020
Ashton et al. (1999)
Wafar et al. (1997)
0.0057, 0.0204
Avicennia marina (Forsk.) Vierh.
0.0071–0.0158
Mackey & Smail (1996)
A. officinalis L.
0.0104
Wafar et al. (1997)
Bruguiera parviflora (Roxb.) Wight & Arnold ex. Griffith
0.0057, 0.0099
Conocarpus erectus L.
0.01, 0.03
Tovilla & de la Lanza (1999)
Laguncularia racemosa L.
0.257
Flores-Verdugo et al. (1987)
Sonneratia alba J. Smith
0.0019
0.031, 0.0469
Wafar et al. (1997)
36
110
(902-17) and CONACYT (32732-T) provided
partial financial support. We thank B. Delfosse for
helping with the English. This study is part of the
Ph.D. thesis of the first author who gratefully
acknowledges the support of CONACYT (scholarship 90031) during his doctoral studies.
Values for the intercept indicate a faster decomposition rate at the beginning of the process, so
estimates from the model must be carefully
analysed when they are made during early
decomposition (Harmon et al., 1999).
Total litterfall in Sontecomapan Lagoon
represent a very high input of organic matter, with
seasonal variation, to the aquatic system. The leaf
litter peaks represent significant loads of organic
matter available for decomposition, thus providing
an important source of C, N, and P that flow from
the mangrove to the aquatic system. This process
could have an effect on the lagoon’s primary
productivity (Rivera-Monroy et al., 1998).
Through leaching and microbial decomposition,
there is a constant flow of nutrients within 60 days
of leaves entering the system, as demonstrated by
the decomposition experiments. This means that
from March to November, there is a higher flow of
nutrients through the system than during the rest
of the year when litter production is lower.
The litterfall pattern of R. mangle in Sontecomapan Lagoon was seasonal and reflected the
hydrological dynamics and the way in which these
affected the different litter fractions. Leaf litter was
the main contributing fraction, with two peaks in
the dry season and a small one in the rainy season.
Leaf decomposition rate was different in each season, being fastest in the rainy season and slowest
during ‘nortes’. For the first 60 days of decomposition, leaching and microbial action were the main
mechanisms and no differences were found among
seasons. After 60 days, removal by aquatic invertebrates or hydrological dynamics increased to
different degrees depending on season. N. reclivata
was associated with the high rate of decomposition
in the rainy season, while during ‘nortes’, removal
by aquatic invertebrates and water movement did
not exert an observable influence. In the dry season, leaching and microbial action were dominant
due to the brevity of the season.
References
Aké-Castillo, J. A., M. E. Meave & D. U. Hernández-Becerril,
1995. Morphology and distribution of species of the diatom
genus Skeletonema in a tropical coastal lagoon. European
Journal of Phycology 30: 107–115.
Ashton, E. C., P. J. Hogarth & R. Ormond, 1999. Breakdown
of mangrove leaf litter in a managed mangrove forest in
Peninsular Malaysia. Hydrobiologia 413: 77–88.
Barreiro-Güemes, M. T., 1999. Aporte de hojarasca y renovación foliar del manglar en un sistema estuarino del Sureste de
México. Revista de Biologı́a Tropical 47: 729–737.
Cundell, A. M, M. S. Brown, R. Stanford & R. Mitchell, 1979.
Microbial degradation of Rhizophora mangle leaves
immersed in the sea. Estuarine and Coastal Marine Science
9: 281–286.
Davis, S. E. III, C. Coronado-Molina, D. L. Childers &
J. W. Day Jr., 2003. Temporally dependent C, N, and P
dynamics associated with the decay of Rhizophora mangle L.
leaf litter in oligotrophic mangrove wetlands of the Southern
Everglades. Aquatic Botany 75: 199–215.
Day, J. W. Jr., C. Coronado-Molina, F. R. Vera-Herrera, R.
Twilley, V. H. Rivera-Monroy, H. Alvarez-Guillén, R. Day
& W. Conner, 1996. A 7 year record of above-ground net
primary production in a southeastern Mexican mangrove
forest. Aquatic Botany 55: 39–60.
Flores-Verdugo, F. J., J. W. Day Jr. & R. Briseño-Dueñas,
1987. Structure, litterfall, decomposition, and detritus
dynamics of mangroves in a Mexican coastal lagoon with an
ephemeral inlet. Marine Ecology Progress Series 35: 83–90.
Flores-Verdugo, F., F. González-Farı́as, O. Ramı́rez-Flores,
F. Amezcua-Linares, A. Yánez-Arancibia, M. Alvarez-Rubio & J. W. Day Jr., 1990. Mangrove ecology, aquatic primary productivity, and fish community dynamics in the
Teacapán-Agua Brava Lagoon-Estuarine system (Mexican
Pacific). Estuaries 13: 219–230.
Harmon, M. E., K. J. Nadelhoffer & J. M. Balir, 1999. Measuring decomposition, nutrient turnover, and stores in plant
litter. In Robertson, G. P., D. C. Coleman, C. S. Bledsoe,
& P. Sollins (eds) Standard Soil Methods for Long-term
Ecological Research. Oxford University Press, Inc, USA:
202–240.
Lankford, R. R., 1977. Coastal lagoons of Mexico, their origin
and classification. In Wiley, M. (ed.), Estuarine Processes.
Academic Press Inc.: 182–215.
López-Portillo, J. & E. Ezcurra, 1985. Litterfall of Avicennia
germinans L. in a one-year cycle in a mudflat at the
Laguna de Mecocacán, Tabasco, Mexico. Biotropica 17:
186–190.
Acknowledgements
We are indebted to R. Madrigal, J. Tolome and O.
Hernández for providing support during the field
work. R. Langrave made Figure 1. M. Favila
kindly reviewed the manuscript and made important suggestions. The Instituto de Ecologia, A.C.
37
111
Slim, F. J., M. A. Hemminga, C. Ochieng, N. T. Jannink, E. C.
de Cocheret La Morinière & G. Van der Velde, 1997. Leaf
litter removal by snail Terebralia palustris (Linnaeus) and
sesarmid crabs in an East African mangrove forest (Gazi
Bay, Kenya). Journal of Experimental Marine Biology and
Ecology 215: 35–48.
SPSS, Inc., 1997. Sigma Stat for windows, version 2.03.
StatSoft, Inc., 2003. STATISTICA (data analysis software
system), version 6. www.statsoft.com.
Tomlinson, P. B., 1986. The Botany of Mangrove. Cambridge
University Press, USA, 413 pp.
Tovilla, H. C. & E. G. de la Lanza, 1999. Ecologı́a, producción
y aprovechamiento del mangle Conocarpus erectus L. en
Barra de Tecoanapa Guerrero, México. Biotropica 31:
121–134.
Twilley, R. R., A. E. Lugo & C. Patterson-Zucca, 1986. Litter
production and turnover in basin mangrove forest in
southwest Florida. Ecology 676: 670–683.
Twilley, R. R., M. Pozo, V. H. Garcı́a, V. H. Rivera-Monroy,
R. Zambrano & A. Bodero, 1997. Litter dynamics in riverine
mangrove forests in the Guayas River estuary, Ecuador.
Oecologia 111: 109–122.
Wafar, S., A. G. Untawale & M. Wafar, 1997. Litterfall and
energy flux in a mangrove ecosystem. Estuarine, Coastal and
Shelf Science 44: 111–124.
Wieder, R. K. & G. E. Lang, 1982. A critique of the analytical
methods used in examining decomposition data obtained
from litter bags. Ecology 63: 1636–1642.
Zar, J. H., 1999. Biostatistical Analysis. Prentice-Hall, Inc.,
USA, 662 pp.
Lugo, A. E. & S. C. Snedaker, 1974. The ecology of mangroves.
Annual Review Ecology and Systematics 5: 39–64.
Mackey, A. P. & G. Smail, 1996. The decomposition of
mangrove litter in a subtropical mangrove forest. Hydrobiologia 332: 93–98.
Menéndez, L. F. J., 1976. Los manglares de la laguna de
Sontecomapan, los Tuxtlas, Ver. Estudio florı́stico-ecológico.
BSc. Thesis Biólogo. UNAM. Facultad de Ciencias, 115 pp.
Middleton, B. A. & K. L. Mckee, 2001. Degradation of mangrove tissues and implications for peat formation in Belizean
island forests. Journal of Ecology 89: 818–828.
Orcutt, D. M. & E. T. Nilsen, 2000. Physiology of Plants under
Stress. Soil and Biotic Factors. John Wiley & Sons, Inc.
USA, 683 pp.
Rico-Gray, V. & A. Lot, 1983. Producción de hojarasca del
manglar de la laguna de la Mancha, Veracruz, México.
Biotica 8: 295–301.
Rivera-Monroy, V. H., J. W. Day, R. R. Twilley, F. VeraHerrera & C. Coronado-Molina, 1995. Flux of nitrogen and
sediment in a fringe mangrove forest in Terminos lagoon,
Mexico. Estuarine, Coastal and Shelf Science 40: 139–160.
Rivera-Monroy, V. H., C. J. Madden, J. W. Day Jr., R. R.
Twilley, F. Vera-Herrera & H. Alvarez-Guillén, 1998. Seasonal coupling of a tropical mangrove forest and an estuarine water column: enhancement of aquatic primary
productivity. Hydrobiologia 379: 41–53.
Robertson, A. I., 1986. Leaf-burying crabs: their influence on
energy flow and export from mixed mangrove forests
(Rhizophora spp.) in northeastern Australia. Journal of
Experimental Marine Biology and Ecology 102: 237–248.
Saenger, P. & S. C. Snedaker, 1993. Pantropical trends in
mangrove above-ground biomass an annual litterfall.
Oecologia 96: 293–299.
38
CAPÍTULO 3
Dynamics of C, P, N and tannins associated with Rhizophora mangle L. leaf litter
production and decomposition in a tropical coastal lagoon in Mexico.
Enviado a Aquatic Botany
39
DYNAMICS OF C, P, N AND TANNINS ASSOCIATED WITH Rhizophora mangle L. LEAF
LITTER PRODUCTION AND DECOMPOSITION IN A TROPICAL COASTAL LAGOON IN
MEXICO
José Antolín Aké-Castillo, Gabriela Vázquez & Ariadna Martínez Virués
Instituto de Ecología, A.C., Departamento de Ecología Funcional, Carretera antigua a
Coatepec No. 351, Congregación El Haya, Xalapa C.P. 91070, Veracruz, México
Fax: +52 (228) 842 1800 ext. 4222, E-mail: [email protected]
Abstract. Litter fall from mangrove represents an important contribution of organic matter to
the soil and aquatic environment. Through decomposition the nutrients are returned to the
surrounding system. In Sontecomapan, a coastal lagoon located on the southern Gulf of Mexico,
the litter production of Rhizophora mangle L. has been recorded as one of the highest for the
species with fast decomposition rates. We analyzed the C, P, N and tannin concentration in the
leaf litter produced over a year and the dynamics of these nutrients and tannins during
decomposition in experiments carried out in different seasons. The best quality of leaf litter (rich
of nutrients) was recorded during the nortes season. The litterbag experiments indicated that leaf
litter was a source of C and P and a trap of N. The concentrations of these nutrients in the litter
during decomposition represent an important stock of nutrients for different routes of the
biogeochemical cycling of nutrients in Sontecomapan Lagoon. The tannins released into this
aquatic system represent a high input of phenolic compounds that may affect the
physicochemical characteristics of the lagoon water.
Keywords: biogeochemical cycles, decomposition, litterfall, nutrients, tannins
40
INTRODUCTION
Mangrove communities are common components in subtropical and tropical estuaries and
coastal lagoons, so numerous studies of community structure and litter dynamics have been done
worldwide (Twilley et al. 1986, 1997, Woodroffe et al. 1988, Lee 1989, Wafar et al. 1997,
Barreiro-Güemes 1999, de Boer 2000, Betoulle et al. 2001). These studies have shown that
mangroves play an important role in the maintenance of the whole ecosystem through their
influence on energy fluxes (Lugo and Snedaker 1974, Wafar et al. 1997).
Litter fall from mangrove represents an important contribution of organic matter to the soil
and aquatic environment. Commonly, leaf litter represents the main fraction of mangrove litter
(Wafar et al. 1997) and studies on its chemical quality have shown that the leaves are rich in
carbon (C), phosphorus (P) and nitrogen (N) (Medina et al. 1995). Tannins, aromatic compounds
bearing hydroxyl substituents (Hättenschwiler and Vitousek 2000), are a product of the
metabolism of vascular plants. These phenolic compounds play different roles including defense
against herbivores and pathogens, and they occur in high concentrations in mangroves
(Tomlinson 1986, Hernes and Hedges 2004). Through decomposition these nutrients and
phenolic compounds are returned to the surrounding system.
The decomposition process of plant litter in aquatic environments involves leaching, microbial
activity, and consumption by grazers as the main mechanisms (Valiela et al. 1985, Cundell et al.
1979, Harrison 1977), and they can occur simultaneously. These phases involve the loss of litter
fall biomass as well as the loss of nutrients from it. Analyses of mass loss is the approach that has
been most widely used in studies of litter decomposition (Flores-Verdugo 1987, Mackey and
Smail 1996, de Boer 2000), and several models that explain this process have been proposed
(Wieder and Lang 1982). The time for 50% of the initial mass to disappear (t50) is often used to
41
compare the rate of decomposition among species. Estimates of t50 from a negative exponential
model are good as the process of decomposition fits this model well (Wieder and Lang 1982,
Mackey and Smail 1996, Aké-Castillo et al. 2006). In contrast, there are fewer studies of the
dynamics of nutrients such as C, N, and P on mangrove leaf litter decomposition in water, and
these are commonly limited to a description of their variation over time. In contrast to the
dynamics of biomass loss during decomposition, nutrient dynamics varies and nutrients are either
lost or increase at different stages of decomposition (Rice and Tenore 1981, Tam et al. 1990,
Chale 1993). Phases of accumulation and release of N and P occur during decomposition, and the
duration of these phases seems to depend on the particular environmental characteristics of the
system studied (Davis III et al. 2003).
Rhizophora mangle L. is a species whose distribution is limited to the mangrove systems of
the west coast of Africa and both coasts of the Americas (Tomlinson 1986). This species is
dominant in Sontecomapan, a coastal lagoon located on the southern Gulf of Mexico. Litter
production by this species has been recorded as one of the highest. (Aké-Castillo et al. 2006).
The rates of leaf litter decomposition are fast in the different seasons (t50= 48-144) and leaching
and microbial action are the main decomposition mechanisms with a seasonal association
between aquatic invertebrates and the loss of litter mass (Aké-Castillo et al. 2006). The peaks in
litter production contributed abundant organic matter to the lagoon and may represent an
important source of nutrients for the aquatic system; so, two main questions regarding the
chemical composition of leaf litter arise: Does variation in the chemical quality of leaf litter
reflect the seasonal litter fall pattern? and, How are nutrient dynamics associated with leaf litter
decomposition in this system?
42
In order to answer these questions, C, P, N and tannin were analyzed for the leaf litter
produced over a year. The dynamics of these nutrients and tannins during decomposition was
studied in experiments carried out in different seasons.
METHODS
Sontecomapan is a small coastal lagoon located in the south of the Gulf of Mexico (18º 30’34’N and 94º59’- 95º04’ W) (Fig. 1). This region is characterized by three climatic seasons:
nortes (cold rainy fronts from October to February), dry (March to May) and rainy (June to
September). The lagoon is bordered by a mangrove forest (533.8 ha) dominated by Rhizophora
mangle (Menéndez 1976, Aké-Castillo et al. 2006).
The samples of leaf litter used for this study were collected from November 2002 to October
2003. Methods of sampling and experimental design are provided in Aké-Castillo et al. (2006),
so only a brief description is given here. Litter fall collection and experiments on decomposition
were carried out at three sites (Fig. 1) with different characteristics: Site A represents a remnant
of mangrove fringe in the main basin of the lagoon where the Coscoapan River drains into it.
Sites B and C represent well preserved mangrove zones with different hydrological
characteristics: B is located in a small basin with no rivers draining into it, and C is influenced
directly by tidal currents and run-off from the Sabalo River. Litter fall was collected using
baskets (10 baskets per site), and leaf litter decomposition was evaluated using fine (1 x 1 mm)
and coarse (3 x 7 mm) mesh litterbags for each of the three seasons (3 pairs of lines with 5 litter
bags of each type). Each month the litter in the baskets and one litterbag from each line were
collected and transported to the laboratory.
Five samples of leaf litter from each site and the remaining leaf litter from the litterbags was
oven-dried. The dried material was finely ground (mesh size: 1 mm) and kept in plastic bags
43
labeled with the site, month and type of litter fall data. This was done each month until the end of
the litter fall collection period in the field and the end of the decomposition experiments. For the
different chemical analyses we followed Anderson and Ingram (1995). A small quantity of the
ground leaf litter was combusted for C analysis. For P analysis we followed the Vanatemolybdate method. For nitrogen (N) analysis the ground sample was digested with H2SO4 using
Cu catalyst and evaluated with micro-Kjeldahl equipment. A small quantity of the ground
material was extracted with methanol to analyze tannin following the Folin-Denis method.
The data for each nutrient in the litter was analyzed with a one-factor repeated measure
analysis of variance (ANOVA) by rank, with month as the factor. Differences were identified
with a Tukey test. A Kruskall-Wallis test was done to determine differences among sites for each
month and for each nutrient and tannin. Multiple comparisons of mean ranks were used to detect
the sites that differed (Zar 1999). Correlation coefficients were calculated to determine any
relationship among concentrations of nutrients with leaf litter production biomass.
Each chemical data set of the remaining litter from the decomposition experiments was
analyzed using a nested factorial ANOVA for each chemical. Variables of interest in this design
were season, site, litterbag mesh size and days of decomposition (nested in season). A multiple
comparisons test was performed to find the groups that differed from each other (Zar 1999).
All analyses were performed using the Statistica ver. 7.0 (StatSoft 2004) statistical package
except for the repeated measures ANOVA for which SigmaStat 2.03 software (SPSS 1997) was
used.
RESULTS
Litter production
44
C concentration was the highest in December 2002 (nortes season) and then decreased in
January and February to its lowest values from March to May (dry season). The highest value
was significantly different from the lowest values (q values > 7.94, P < 0.05) (Fig. 2a). From June
to October (rainy season) C concentration increased. The concentration of P was highest in
December 2002 (nortes season) and decreased in January and February, and was low for the
remaining months. The highest value differed from the lowest values recorded from June to
August (rainy season) (q values > 9.18, P < 0.05) (Fig. 2b). N concentration was high from
December to March (nortes season) and decreased in April and May (dry season), with the lowest
values in June, July and August (rainy season). N concentration increased in September and
October (nortes season). The highest values were significantly different from the lowest (q values
> 7.47, P < 0.05) (Fig. 2c). Tannin concentration was the only chemical that followed a pattern
similar to of that leaf litter production (Figs 2d, 2e). In December the lowest value was recorded
and tannin concentration increased in January to its maximum concentrations from February to
May (dry season). After this peak, concentration decreased in June to low values in July and
August (rainy season). In September tannin concentration increased and in October, it decreased
again (nortes season). The peak of the dry season differed significantly from the lowest values of
the nortes season (q values > 7.08, P < 0.05) (Fig. 2d).
P was the only nutrient significantly correlated with all the other nutrients and with tannins
(Table 1). When the maximum concentrations of P occurred, C and N were at their highest, and
tannins were at their lowest. Leaf litter fall was negatively correlated with C and P
concentrations and positively correlated with tannin concentration (Table 1).
Differences in nutrient concentrations among sites were most evident for P. Site A had the
highest concentration for seven of the eleven months of the study (Table 2).
45
Litter decomposition
The dynamics of C, P, N and tannin concentrations in the leaf litter during decomposition
were different among seasons (C: F = 14.01; P: F = 55.40; N: F = 63.54; tannin: F = 127.11; all P
values < 0.001) (Fig. 3). The concentration of C decreased throughout the experiments in the
nortes and rainy seasons, while in the dry season it increased after 90 days of decomposition. No
differences were detected between litter bag types within each season. P dynamics during
decomposition showed that its concentration increased during the first 30 days indicating the
accumulation of this nutrient within each season (Fig. 3b). After 30 days, variation was different
for the seasons: During the nortes season P was liberated until the end of the experiment. In the
dry season although P was mobilized, P concentration did not decrease significantly from the
initial concentration, and actually increased again at day 120. In the rainy season P was released,
decreasing in concentration compared to initial concentrations, with an accumulation at day 120
and released again to the end of the experiment. No differences between litter bag type within
seasons were detected (Fig. 3b). The N concentration of litter fall increased throughout the time
decomposition was studied (Fig. 3c). The increase in N concentration indicated that leaf litterfall
accumulated this nutrient for a long time. Litterbag type had a significant effect (F = 3.08, P <
0.001) on day 120 in the dry season, and day 90 in the rainy season. The remaining litter in the
fine litterbag had a lower concentration of N. The dynamics of tannin concentration showed a
quick release during the first 30 days of decomposition in each season (Fig. 3d). Litterbag type
had a significant effect (F = 2.73, P = 0.006) in the nortes seasons on day 150; the coarse litterbag
had a higher tannin concentration (P = 0.019).
There were differences in the dynamics of C, P, N and tannin among the sites within each
season (C: F = 2.89, P = 0.023; P: F = 2.51, P = 0.042; N: F = 2.32, P <0.001; tannin: F = 2.73, P
46
< 0.001) (Fig. 4). In the nortes season on day 150, there had been a greater loss of C at site C (P
values < 0.005). In the dry season no significant differences were detected among sites. In the
rainy season on day 60 all the sites differed from each other, with site A losing the most C,
followed by site C and then site B (A vs. C: P = 0.10; A vs. B: P = 0.0001; B vs. C: P = 0.02)
(Fig. 4a). Differences in P concentrations among sites occurred only in the nortes season on day
60. Sites A and C had lower P concentrations than site B (P values < 0.002) (Fig. 4b). There were
differences among sites for N concentration in all three seasons. In the nortes season, site C
accumulated more N than sites A or B (P = 0.0003, P = 0.01) on day 120. In the dry season site B
had accumulated more N than site A (P = 0.02) on day 60. In the rainy season on day 60 site C
had accumulated more N than sites A or B (P = 0.0004, P = 0.01) and from day 90 to 120 sites B
and C accumulated more N than site A (P values < 0.02) (Fig. 4c). Tannin liberation was
different among sites for the three seasons. In the nortes season site C lost more tannin than sites
A or B on day 60 (P = 0.00002, P = 0.009). On day 150, the remaining leaf litter at sites B and C
had lower concentrations of tannin than site A (P-values < 0.01). In the dry season, sites differed
on different days. On day 30 site A had lost more tannin than site C (P = 0.006); on day 90 site B
had lost more tannin than site A (P = 0.02); and on day 150 site C had lost more tannin than sites
A or B (P = 0.01, P = 0.03). In the rainy season differences only occurred on day 30 when site A
had a lower concentration than site B (P = 0.03) (Fig 4d).
DISCUSSION
Litter production
The dynamics of C and P concentrations in leaf litter can be explained by the aging of the
leaves. The lowest values of these nutrients coincided with the highest leaf litter production, and
this may be the result of translocation of nutrients as a normal process of leaf growth (Feller et al.
47
1999). Barreiro-Güemes (1999) found that the refoliation in R. mangle takes 3-5 months, so the
peaks of leaf litter in Sontecomapan also reflect the appearance of new leaves (Aké-Castillo et al.
2006). The highest concentrations of C and P recorded in December (nortes season), just two
months after the peak in leaf litter production in September, may indicate that these
concentrations were the result of falling mature leaves (prior to nutrient translocation) during the
strong winds, as reported for a similar mangrove system in the southern Gulf of Mexico in the
nortes season (Barreiro-Güemes 1999).
On the other hand, variation in N concentration did not show an obvious relationship to aging
of leaves as maximum N concentrations were found at the peaks of leaf litter production. This
indicates that N may be forming refractory compounds that not are completely translocated
before the old leaves fall (Feller et al. 1999). Alternatively, N concentration may be related to the
salinity of the lagoon. Medina et al. (1995) found a direct relationship between the concentrations
of nutrients in leaf litter and the salinity of the lagoon: leaves from mangrove in zones with a
fresh water influence had higher concentrations of nutrients than those exposed to the marine
influence. In our study, higher concentrations of N were found in litter from leaves that grew
during the months when lowest salinities were recorded in the lagoon, while the lowest N
concentrations were found in litter from leaves that grew when salinity of the lagoon was higher
(Aké-Castillo et al. 2006). Tannin concentrations were the highest from March to May (dry
season) with a peak in September similar to the leaf litter pattern (Aké-Castillo et al. 2006). This
may indicate that this compound was stored while the leaves were growing until they were shed
naturally.
Differences among P concentrations at the sites for most the months may indicate that there
were differences in the soil-water concentration of P. Sites B and C represent the preserved
mangrove forest, which differed markedly from the site A. Site A is the most deforested area
48
surrounded by pastures, so the load of P may be high in this zone owing to cattle manure and
fertilization. The high concentration of this nutrient in the leaves could reflect this P enrichment
phenomenon as demonstrated in P enrichment experiments examining the nutrient quality of
leaves (Feller et al. 1999).
Litter decomposition
The variations of C and P concentrations in the leaf litter during decomposition were similar to
the results for other species of mangrove evaluated in Hong Kong (Tam et al. 1990). The decay
of C was slow in all three seasons (i.e. it did not reach a loss of 50% in 150 days evaluated) and
the increased concentration detected in the dry season indicates an increase in microbial activity
(Rice and Tenore 1981). P dynamics indicates an accumulation-release process (Nielsen and
Andersen 2003, Davis III et al. 2003) which varied depending on the season. Leaf litter was a
source of P to the aquatic environment during the nortes and rainy seasons, while in the dry
season leaf litter functioned as a P trap.
The dynamics of N during R. mangle leaf litter decomposition indicate an accumulation
mechanism of this nutrient similar to that reported by Twilley et al. (1986) for this species. This
result is contrary to the N dynamics observed in other species of mangrove (i.e. Avicennia
germinans (L.) L., A. marina (Forsk.) Vierh., Kandelia candel (L.) Druce) in which there was a
liberation mechanism at some stage of their decomposition (Twilley et al. 1986, Tam et al. 1990).
The leaf litter of R. mangle in Sontecomapan Lagoon acts as an N nutrient conservation
mechanism that may recycle N to the environment via the action of detritivorous organisms
(Gürel et al. 2005).
The abrupt decrease in tannin concentration indicated that this is a highly leachable compound
that is rapidly lost at the beginning of decomposition (Cundell et al. 1979). Mangrove leaf litter
49
fall represents a constant source of phenolic compounds for the lagoon, and may have effects on
the chemical characteristics of water as observed in coastal lagoons and estuaries (HerreraSilveira and Ramírez-Ramírez 1996, Kalesh et al. 2001).
Litterbag type did not have any effect on the chemical concentrations recorded within each
season, with the exception of N. This difference occurred at an advanced stage of decomposition
(90 and 120 days) in the dry and rainy seasons, and it is hard to explain because the main
mechanisms are bacterial and fungal activity and there is no reason to think these organisms were
excluded or their activity suppressed.
The differences in the dynamics of C, P, N and tannin among sites indicate that the physical
and chemical characteristics of the sites exerted an effect at some stage of the decomposition
process. The gradient of salinity in these coastal systems is a determinant of the type of bacteria
and fungi (i.e. freshwater or marine) that colonizes the leaf litter (Willoughby 1974, Perkins
1974). The hydrological condition and chemical characteristics of the site can affect the rate of
colonization by microorganisms (Gulis and Suberkropp 2003), being slower in sites with high
turbulence. Most of the differences occurred between site A and site C, the sites with the most
extreme salinity and tidal influence.
Litterfall and decomposition studies in aquatic systems allow us to understand how terrestrial
and aquatic systems are linked. In Sontecomapan Lagoon, chemical analyses of litter fall show
that C and P were negatively correlated to leaf litter biomass indicating that these nutrients are
translocated before the old leaves fall. N metabolism in senescent leaves is indicative of
incomplete resorption and may be related to the salinity of the environment at the time leaves
were growing. Differences in the concentrations of P among sites indicate the influence of
anthropogenic activities close to the lagoon. Tannin accumulated during the lifetime of the
leaves. In the windy nortes season, mechanical forces may increase the defoliation of green
50
leaves and result in leaf litter with a high nutrient concentration. This would explain why the best
quality of leaf litter (rich in nutrients) was recorded in this season.
The litterbag experiments indicated that the concentrations of C, P, N, and tannins recorded in
the remaining litter during the decomposition process provided a constant flow of nutrients and
tannins to the aquatic environment. Leaf litter was a source of C and P liberated to the
environment although there were short periods of accumulation. The accumulation of N was an
alternate pathway, through detrivory, for cycling this nutrient. The seasonal variation in P
concentrations and the differences among sites in concentrations of N during decomposition
shows that microbes and fungi are sensitive to changes in the physicochemical characteristics of
the water in the lagoon. Although there is a rapid loss of leaf litter biomass during the first stage
of R. mangle decomposition, the concentrations of C, P, and N in the litter during decomposition
represent an important stock for different routes of the biogeochemical cycling of nutrients in
Sontecomapan Lagoon. The tannins released into this aquatic system represent a high input of
phenolic compounds that may affect the physicochemical characteristics of the lagoon water.
LITERATURE CITED
Aké-Castillo, J. A., G. Vázquez and J. López-Portillo. 2006. Litterfall and decomposition of
Rhizophora mangle L. in a coastal lagoon in the southern Gulf of Mexico. Hydrobiologia 559:
101-11.
Anderson, J.M. and J. S. I. Ingram. 1995. Tropical soil biology and fertility. A handbook of
methods. Second edition. A. A. B. Internacional U.K.
Barreiro-Güemes, M. T. 1999. Aporte de hojarasca y renovación foliar del manglar en un sistema
estuarino del Sureste de México. Revista de Biología Tropical 47: 729-737.
51
Betoulle, J. L., F.Fromard, A. Fabre and H. Puig. 2001. Caractérisation des chutes de litière et des
apports au sol en nutriments dans une mangrove de Guyane française. Canadian Journal of
Botany 79: 238-249.
Cundell, A. M, M. S.Brown, R. Stanford and R. Mitchell. 1979. Microbial degradation of
Rhizophora mangle leaves immersed in the sea. Estuarine and Coastal Shelf Science 9: 281286.
Chale, F. M. M. 1993. Degradation of mangrove leaf litter under aerobic conditions.
Davis III, S. E., C. Corronado-Molina, D. L. Childers and J. W. Day Jr. 2003. Temporally
dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter
in oligotrophic mangrove wetlands of the Southern Everglades. Aquatic Botany 75: 199-215.
de Boer, W. F. 2000. Biomass dynamics of seagrasses and the role of mangrove and seagrass
vegetation as different nutrient sources for an intertidal ecosystem. Aquatic Botany 66: 225239.
Feller, I. C., D. F.Whigham, J. P. O’neill and K. L. Mckee. 1999. Effects of nutrient enrichment
on within-stand cycling in a mangrove forest. Ecology 80: 2193-2205.
Flores-Verdugo, F. J., J. W. Day Jr. and R. Briseño-Dueñas, 1987. Structure, litterfall,
decomposition, and detritus dynamics of mangroves in a Mexican coastal lagoon with an
ephemeral inlet. Marine Ecology Progress Series 35: 83-90.
Gulis, V. and K. Suberkropp. 2003. Leaf litter decomposition and microbial activity in nutrientenriched and unaltered reaches of a headwater stream. Freshwater Biology 48: 123-134.
Gürel, M., A.Tanik, R. C. Russo and I. E. Gönenç. 2005. Biogeochemical cycles. In: I. E.Gönenç
and J. P. Wolflin, editors. Coastal lagoons. Ecosystem processes and modelling for sustainable
use and development. CRC Press. USA.
52
Harrison, P. G. 1977. Decomposition of macrophyte detritus in seawater: effects of grazing by
amphipods. Oikos 28: 165-169.
Hättenschwiler, S. and P. M. Vitousek, 2000. The role of poly phenols in terrestrial ecosystem
nutrient cycling. Trends in Ecology & Evolution 15: 238-243.
Hernes, P. J. and J. I. Hedges. 2004. Tannin signatures of barks, neddles, leaves, cones, and wood
at the molecular level. Geochimica et Cosmochimica Acta 68: 1293-1307.
Herrera-Silveira, J. A. and J.Ramírez-Ramírez. 1996. Effect of natural phenolic material (tannin)
on phytoplankton growth. Limnology and Oceanography 41: 1018-1023.
Kalesh, N. S., C. H. Sujatha, and S. M. Nair. 2001. Dissolved folin phenol active substances
(tannin and lignin) in the seawater along the west coast of India. Journal of Oceanography 57:
29-36.
Lee, S. Y. 1989. Litter production and turnover of the mangrove Kandelia candel (L.) Druce in a
Hong Kong tidal shrimp pond. Estuarine, Coastal and Shelf Science 29: 75-87.
Lugo, A. E. and S. C. Snedaker. 1974. The ecology of mangroves. Annual Review of Ecology
and Systematics 5: 39-64.
Mackey, A. P. and G. Smail, 1996. The decomposition of mangrove litter in a subtropical
mangrove forest. Hydrobiologia 332: 93-98.
Medina, E., A. E. Lugo and A. Novelo. 1995. Contenido mineral del tejido foliar de especies de
manglar de la laguna de Sontecomapan (Veracruz, México) y su relación con la salinidad.
Biotropica 27: 317-323.
Menéndez, L. F. J., 1976. Los manglares de la laguna de Sontecomapan, los Tuxtlas, Ver.
Estudio florístico-ecológico. BSc. Thesis Biólogo. UNAM. Facultad de Ciencias. 115 pp.
53
Nielsen, T. and F. Ø. Andersen. 2003. Phosphorus dynamics during decomposition of mangrove
(Rhizophora apiculata) leaves in sediments. Journal of Experimental Marine Biology and
Ecology 293: 73-88.
Perkins, E. J. 1974. The marine environment. Pages 683-721 in C. H. Dickinson and G. J. F.
Pugh, editors. Biology of plant litter decomposition. Volume 2. Academic Press, London.
Rice, D. L. and K. R. Tenore. 1981. Dynamics of carbon and nitrogen during the decomposition
of detritus derived from estuarine macrophytes. Estuarine, Coastal and Shelf Science 13: 681690.
SPSS, Inc. 1997. Sigma Stat for Windows, version 2.03.
StatSoft, Inc. 2004. STATISTICA (data analysis software system), version 7. www.statsoft.com.
Tam, N. F. Y., L. L. P. Vrijmoed and Y. S. Wong. 1990. Nutrient dynamics associated with leaf
decomposition in a small subtropical mangrove community in Hong Kong. Bulletin Marine of
Science 47: 68-78.
Tomlinson, P. B.1986. The botany of mangrove. Cambridge University Press. USA, 413 pp.
Twilley, R. R., M. Pozo, V. H.García, V. H. Rivera-Monroy, R. Zambrano and A. Bodero. 1997.
Litter dynamics in riverine mangrove forests in the Guayas River estuary, Ecuador. Oecologia
111: 109-122.
Twilley, R. R., A. E. Lugo and C. Patterson-Zucca. 1986. Litter production and turnover in basin
mangrove forest in southwest Florida. Ecology 676: 670-683.
Valiela, I., J. M. Teal, S. Allen, R. V. Etten, D. Goehringer and S. Volkmann. 1985.
Decomposition in salt marsh ecosystems: the phases and major factors affecting disappearance
of above-ground organic matter. Journal of Experimental Marine Biology and Ecology 89: 2954.
54
Wafar, S., A. G. Untawale and M. Wafar. 1997. Litterfall and energy flux in a mangrove
ecosystem. Estuarine, Coastal and Shelf Science 44: 111-124.
Wieder, R. K. and G. E. Lang. 1982. A critique of the analytical methods used in examining
decomposition data obtained from litter bags. Ecology 63: 1636-1642.
Willoughby, L. G. 1974. Decomposition of litter in fresh water. Pages 659-681 in C. H.
Dickinson and G. J. F. Pugh, editors. Biology of plant litter decomposition. Volume 2.
Academic Press, London.
Woodroffe, C. D., K. N. Bardsley, P. J. Ward and J. R. Hanley. 1988. Production of mangrove
litter in a macrotidal embayment, Darwin Harbour, N. T., Australia. Estuarine, Coastal and
Shelf Science 26: 581-598.
Zar, J. H. 1999. Biostatistical analysis. Prentice-Hall, Inc. USA, 662 pp.
55
Table 1. Coefficient of correlations between chemicals and leaf litter fall
-1
-1
C mg g
-1
P mg g
-1
N mg g
-1
1.00
-1
0.71*
1.00
-1
0.00
0.32*
1.00
-0.75*
-0.41*
0.15
1.00
-0.58*
-0.39*
-0.14
0.38*
C mg g
P mg g
N mg g
-1
tannin mg g
-2
leaf litter g m
-2
tannin mg g
leaf litter g m
1.00
* significative P < 0.05
Table 2. Mean values (mg g-1) of C, P, N, and tannin concentrations in leaves of R. mangle by site
and month
Chemical
Site
Dec
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
C
A
552.08a
550.37a
525.08a
517.88a
519.96a
519.47a
524.04a
532.91a
527.44ab
529.83a
535.21a
555.65a
541.71a
523.74a
517.42a
519.88a
515.67ab 520.93ab 530.90ab
530.69a
527.17a
531.15ab
551.70a
535.24a
524.73a
508.55a
513.36a
511.42b
516.39b
525.71b
523.85b
523.21a
526.10b
8.88a
7.10a
3.87a
4.93a
3.00a
3.61a
3.35a
3.09a
2.85a
3.70a
4.19a
7.91a
3.14b
2.73b
2.98a
2.54a
2.30b
1.91b
1.94a
2.19ab
2.89ab
3.49ab
7.75a
3.27b
3.03b
2.87a
2.55a
2.23b
1.79b
2.02a
1.81b
2.61b
2.53b
7.55a
6.45a
7.94a
8.85a
5.27a
6.05a
4.20ab
4.47a
3.99ab
7.05a
6.46a
6.71ab
7.17a
7.30a
7.04a
6.07a
5.50a
4.53a
4.18a
3.99a
7.09a
5.02a
5.31b
7.01a
7.27a
7.46a
6.26a
5.99a
3.79b
4.52a
3.16b
6.34a
5.60a
0.51a
1.04a
1.78a
1.90a
1.91a
1.63a
1.55a
1.21a
1.20a
1.35a
0.94ab
0.65a
0.94a
1.80a
1.75a
1.71ab
1.75a
1.56a
1.09a
1.09a
1.13a
0.65a
0.61a
1.09a
1.62a
1.86a
1.68b
1.75a
1.49a
1.19a
1.12a
1.35a
1.09b
B
C
P
A
B
C
N
A
B
C
tannin
A
B
C
Letters a, b indicate homogenous groups within months and for each nutrient according to
multiple comparison tests.
56
Figure legends
Figure 1. Location of Sontecomapan Lagoon. Letters A, B and C are the sites studied. Gray fill
represents the mangrove forest.
Figure 2. Seasonal dynamics in the mean concentrations of a) carbon, b) phosphorous, c)
nitrogen, d) tannins, and e) leaf litter production of R. mangle in Sontecomapan Lagoon from
December 2002 to October 2003. Vertical bars are 95% confidence intervals.
Figure 3. Dynamics in the mean concentration of a) carbon, b) phosphorous, c) nitrogen, and
d) tannins in leaf litter decomposition in coarse (3 x 7 mm) and fine (1 x 1 mm) litterbags. Initial
values represent the concentration of each nutrient at the beginning of the experiments. Vertical
bars represent 95% confidence intervals. The continuous line is the coarse mesh litterbag and the
dotted line is the fine mesh litterbag.
Figure 4. Dynamics in the mean concentration of a) carbon, b) phosphorous, c) nitrogen, and
d) tannins in leaf litter decomposition at the three sites. Initial values represent the concentration
of each nutrient at the beginning of the experiments. Vertical bars represent 95% confidence
intervals. Site A is the continuous line, site B the coarse dotted line, and site C the fine dotted
line.
57
Figure 1
58
Figure 2
59
Figure 3
60
Figure 4
61
CAPÍTULO 4
Phytoplankton variation over a year and its relation to nutrients and allochthonous
organic matter in Sontecomapan, a tropical coastal lagoon on the Gulf of Mexico.
Enviado a Estuarine, Coastal and Shelf Science
62
Phytoplankton variation over a year and its relation to nutrients and allochthonous organic
matter in Sontecomapan, a tropical coastal lagoon on the Gulf of Mexico.
José Antolín Aké-Castillo & Gabriela Vázquez
Instituto de Ecología, A.C., Departamento de Ecología Funcional, Carretera antigua a
Coatepec No. 351, Congregación El Haya, Xalapa C.P. 91070, Veracruz, México
Fax: +52 (228) 842 1800 ext. 4222, E-mail: [email protected]
Abstract
In tropical and subtropical zones, coastal lagoons are surrounded by mangrove communities
which are a source of high quantity organic matter that enters the aquatic system through litter
fall. This organic matter decomposes, becoming a source of nutrients and other substances such
as tannins, fulvic acids and humic acids that may affect the composition and productivity of
phytoplankton communities. Sontecomapan is a coastal lagoon located in the southern Gulf of
Mexico, which receives abundant litter fall (1116 g m-2 year-1) from Rhizophora mangle L. To
study the phytoplankton composition and its variation in this lagoon from October 2002 to
October 2003, we evaluated salinity, O2, temperature, pH, N-NH4+, N-NO3-, P-PO43-, Si-SiO2,
and phytoplanktonic cell density in the lagoon and the three main rivers that feed it. We also
evaluated the concentrations of dissolved folin phenol active substances (FPAS) as a measure of
plant organic matter. A principal components analysis and analysis of variance of
physicochemical parameters indicated that the lagoon has three seasons: nortes, dry and rainy.
Seasonal variation in N-NO3- and Si-SiO2 depended on freshwater flow, and concentrations
63
decreased during the driest period. Concentrations of P-PO43-, N-NH4+ and FPAS were the
highest in the dry season, when maximum mangrove litter fall is reported. Variation of these
nutrients seemed to depend on the internal biogeochemical processes of the lagoon. Correlations
of the species with environmental parameters indicated that, in addition to nutrients, the
concentration of FPAS may be playing an important role in seasonally shaping the phytoplankton
community. Variation in the phytoplankton community is reflected by the dominant species in
each season: in the nortes season, the diatoms Skeletonema subsalsum, S. pseudocostaum and S.
costatum; during the dry season, the dinoflagellates Peridinium aff. quinquecorne, Prorocentrum
cordatum, Ceratium furca var. hircus, Scrippsiella sp. and the diatom Thalassiosira
cedarkeyensis; and during the rainy season, the diatoms Cyclotella cryptica, C. meneghiniana, C.
striata , Chaetoceros holsaticus and C. simplex. The growth of these species seemed to be a
function of their tolerance to FPAS, with moderate tolerance in the nortes season, high tolerance
in the dry season and low tolerance in the rainy season.
Keywords: phytoplankton, diatoms, dinoflagellates, organic matter, nutrients, coastal lagoon,
Mexico
64
1. Introduction
Coastal lagoons are shallow systems where the hydrological dynamics depend on affluent
rivers and their connection with the sea, which in some cases can be temporally blocked by a
sand bar (Lankford, 1977). Phytoplankton communities can be very diverse as these ecotones
represent complex systems where phytoplankton species from freshwater and marine
environments converge, and form a mixed community that varies spatially, mainly along a
salinity gradient (Emery and Stevenson, 1957). Although studies of phytoplankton communities
indicate that patterns in structure and succession depend on the changes in environmental
parameters (particularly salinity, temperature, light and nutrient availability), these patterns also
vary with geographical region: tropical, temperate and polar (Wetzel, 2001).
In tropical and subtropical zones, coastal lagoons are surrounded by mangrove communities,
which represent a source of high quantity organic matter that enters the aquatic system through
litter fall (Rivera-Monroy et al., 1995). This organic matter becomes a source of nutrients and
other substances through decomposition processes that affect the composition and productivity of
phytoplankton communities (Herrera-Silveira and Ramírez-Ramírez, 1996; Rivera-Monroy et al.,
1998).
The main fraction of organic matter from mangroves is leaf litter, and as it decomposes it
liberates carbon, nitrogen and phosphorous compounds (Tam et al., 1990). Besides these
inorganic substances, organic compounds such as humic material are liberated (Herrera-Siveira
and Ramírez-Ramírez, 1996). The chemical nature of humic substances is poorly understood and
different pathways, involving lignins, polyphenols and sugar condensation, contribute to their
formation (Weber 2005). In natural environments, humic matter has been shown to affect
phytoplankton primary production both negatively (Jackson and Hecky, 1980; Guildford et al.,
65
1987) and positively (Rivera-Monroy et al., 1995; Conzonno and Fernández, 1996; Danilov and
Ekelund, 2001). Bioassays with species of microalgae exposed to the different compounds which
are part of humic substances (i.e. tannins, fulvic acids and humic acids) have shown that the
response is species-specific (Toledo et al., 1980, 1982 Prakash and Rashid, 1968; Prakash et al.,
1973; Herrera-Silveira and Ramírez-Ramírez, 1996), so the effect on natural systems may
depend, in part, on the composition and physiological status of the phytoplankton community
(Klug, 2002).
Sontecomapan Lagoon is a coastal lagoon located in the south of the Gulf of Mexico, in an
area of notable biodiversity, the Los Tuxtlas Biosphere Reserve. This lagoon receives abundant
litterfall from Rhizophora mangle L. (1116 g m-2 year-1) and the leaf litter decomposes rapidly
(Aké-Castillo et al., 2006). To study the phytoplankton composition and its variation through
time in this lagoon, in addition to considering basic physicochemical and biological parameters,
we evaluated the concentrations of dissolved folin phenol active substances (tannins and lignins)
as a measure of the plant organic matter (Kalesh et al., 2001) that enters the lagoon. In addition,
we evaluated the same environmental parameters for three rivers that feed the lagoon in order to
estimate their contribution to nutrient input. By analyzing the relationship between these
biological and environmental parameters we attempt to understand the relative importance of the
environmental factors on this tropical phytoplankton community.
2. Study site and methods
Sontecomapan Lagoon is a small (12 km long and 1.5 km wide) shallow coastal lagoon that is
permanently connected to the Gulf of Mexico. It is located in the Los Tuxtlas Biosphere Reserve
between 18º 30’-18º 34’ N and 94º 59’-95º 04’ W (Fig. 1). This region is characterized by three
66
seasons: the dry season from March to May, the rainy season from June to September, and the
“nortes” season from October to February. The latter is characterized by strong winds coming
from north and intense sporadic rainfall. This lagoon is bordered by a mangrove forest that
covers an area of 533.8 ha, and is comprised of Rhizophora mangle, Laguncularia racemosa, and
Avicennia germinans; the first being the dominant species in the system (Aké-Castillo et al.,
2006). The mean depth of the lagoon is about 1.5 m with a semidiurnal tidal regime (> 60 cm).
Three permanent rivers drain into the lagoon and it is also fed by small creeks during the rainy
season. The lagoon is a brackish water system and its salinity varies spatially and temporally
from 0 to 35 PSU (Aké-Castillo et al., 1995).
2.1. Sampling procedure
The study was conducted from October 2002 to October 2003. Seven sampling stations were
set up in the lagoon with an additional station in each of the 3 main rivers that drain into the
lagoon at a distance of approximately 100 m from the mouth (Fig. 1). Samples were obtained
bimonthly from each station at two depths: superficial and close to the bottom. All field sampling
was done between 9:00 and 14:00 h, sampling the stations in the same order.
Water samples were collected using a Van Dorn bottle. On collection, oxygen, temperature,
salinity, and pH were measured using a YSI Mod. 30 portable meter and a pH meter respectively.
Samples were stored in plastic containers for the analysis of ammonium, nitrate, silica, and
dissolved folin phenol active substances, and in glass containers for orthophosphate analysis.
Samples were kept at 4 ºC for transportation to the laboratory (APHA, 1998). From the water
sample, 125 ml was fixed with lugol-acetate solution to count the phytoplankton. Net hauls (54
67
µm mesh size) were done at each station to get additional phytoplankton material for taxonomic
determination. These samples were fixed with formalin to a final concentration of 4%.
2.2. Laboratory analysis
Ammonium (N-NH4+) was determined using the Nessler method; nitrate (N-NO3-) using a
colorimetric method with brucin; orthophosphate (P-PO43-) using a colorimetric method with
ascorbic acid; and silica (Si-SiO2) using a colorimetric method with molybdate following the
techniques in Strickland and Parsons (1977), Horwitz (1980) and APHA (1998). The dissolved
folin phenol active substances (FPAS) were estimated following APHA (1998) using the sodium
tungstate-phosphomolybdic acid method with the addition of trisodium citrate solution to prevent
the interference of Mg and Ca hydroxides and the bicarbonates present in sea water (Kalesh et al.,
2001).
2.3. Phytoplankton counts
Cells were counted following the Utermöhl method with an inverted Leica DMIL microscope
(Hasle, 1978a). Sedimentation chambers (20 ml) were used, allowing the lugol preserved water
sample to settle for 24 hours before counting. Phytoplankton cells were counted at 100x and 400x
magnification. When identification was not possible during counting, the material was recovered
at the end of the session and observed with a light microscope using 1000x magnification. We
prepared permanent slides for diatoms (Hasle, 1978b) and semi-permanent slides (using glycerine
jelly) for dinoflagellates. These were prepared from both the bottle and net samples, and were
used for taxonomic determination. Additional preparations were made for observation with the
68
scanning electron microscope (JEOL-5600) for abundant species that were hard to identify under
the light microscope.
For identification we mainly consulted Cupp (1943), Hasle and Syvertsen (1997), Krammer
and Lange-Bertalot (1991a, 1991b, 1999), Dodge (1985), Steidinger and Tangen (1997).
2.4. Data analysis
2.4.1. Salt wedge and seasonality
In order to detect the effect of the salt wedge on environmental variables and the effect of the
different seasons, a factorial analysis of variance (ANOVA) was done for each parameter. Factors
tested were level (surface and bottom), month (October 2002-October 2003) and environment
(lagoon and rivers). Data were transformed to log10 (x+1) to achieve normality (Zar, 1999). A
Tukey test followed the ANOVA to reveal which groups differed in each analysis.
A Principal Components Analysis (PCA) was performed with the data for all physicochemical
variables of the lagoon, and another PCA was done on the river data in order to reduce the
number of variables and find the parameters that accounted for most of the variation in each
environment. In order to characterize temporal variation, the first component was used in a twoway ANOVA to detect any significant differences among sampling months and environments. A
Tukey test was performed to detect any months that were different. We used the Statistica
software package, version 7.0, (StatSoft, 2004) for these analyses.
2. 4. 2. Cell density
In order to determine whether there was a pattern of cell density in the lagoon, we did a
factorial ANOVA on cell density data, with level, month and environment as factors. A Tukey
69
test followed this analysis to detect any groups that differed. To achieve normality, data were
transformed to log10 (x+1) (Zar, 1999).
2.4.3. Diversity
The Shanon-Wiener index for diversity and evenness was calculated for phytoplankton species
recorded in the lagoon and the three tributary rivers for each month. Statistical comparisons were
made among indexes to find any significant differences (Zar, 1999).
2.4.4. Relationship between phytoplankton species and environmental parameters
Canonical Correspondence Analysis (CCA) was used to investigate the relationship between
the environmental parameters and phytoplankton abundance (Ter Braak, 1986). Species with a
frequency of less than 5% of all samples were not included in the analysis in order to avoid the
influence of rare species (Jongman et al., 1987). Species abundance data were log10 (x+1)
transformed prior to analysis. A Monte Carlo test was performed to determine the significance of
the correlations between the environmental and biological variables. The analyses were
performed using the CANOCO software package, version 4.0 (Ter Braak and Smilauer, 1998).
These analyses were done using all the data for the lagoon, and again with all the data for the
rivers.
3. Results
3.1. Salt wedge and seasonality
70
The salinity of samples from the bottom of the lagoon was commonly higher at most of the
stations for all months except December 2002 for both the lagoon and the rivers (Fig. 2a). The
ANOVA for salinity resulted in significant differences between the bottom and surface levels (F
= 17.6, P < 0.001) indicating an intrusion of marine water into the lagoon and rivers regardless of
the month. Significant differences between surface and bottom levels were detected only for O2,
N-NH4+ and Si-SiO2, with O2 higher at the surface (F = 16.5, P < 0.001), N-NH4+ higher on the
bottom (F = 6.6, P = 0.011), and Si-SiO2 higher at the surface (F = 8.4, P = 0.004).
Variation in physical and chemical parameters over time (Fig. 2) show maximum salinity was
recorded in April and June, and minimum values in October, December 2002 and August 2003
(Fig. 2a). Maximum O2 concentrations were recorded in February and minimum values in
October 2002 (Fig. 2b). Temperature was highest in April, June and August, and lowest in
December, February and October 2003 (Fig. 2c). The highest values of pH were detected in
February and August, and the lowest in April in the lagoon, while for the rivers pH did not vary
among months (Fig. 2d). For nutrients, in April, the driest month of the year, either maximum or
minimum values occurred. N-NH4+ and P-PO43- were highest in April (Fig. 2e, g) in both the
lagoon and rivers, but N-NO3- and Si-SiO2 decreased (Fig. 2f, h). The concentration of FPAS in
the lagoon was high through February, April and June with a second peak in October 2003 (Fig.
2i).
A comparison of mean annual parameter values between environments indicates that salinity,
O2, temperature and pH in the lagoon were higher than in the rivers, while concentrations of NNO3- , P-PO43- and Si-SiO2 were higher in the rivers (F values ≥ 6.12, P values ≤ 0.001) (Fig. 2f,
g, h). The concentration of FPAS was higher in the lagoon than in the rivers (F = 12.45, P <
0.001) (Table 1).
71
The PCAs of the lagoon and river data show that the major contributors of variation on the
first axis were salinity and Si-SiO2. Additionally, for the lagoon there was heavy N-NH4+ loading
and temperature was important for rivers. Si-SiO2 was negatively correlated with salinity and NNH4+ (Table 2). The ANOVA on the first component extracted from the PCA data from the
lagoon and the rivers indicates that differences among months depended on the characteristics of
the lagoon or rivers (F = 14.37, P < 0.001). Significant differences among consecutive months
(Fig. 3) allow us to classify the lagoon seasonally as follows: October 2002 to December 2002
was the 2002 nortes season, February was the transition from the nortes to the dry season; April
was the dry season; June was the transition from the dry to the rainy season; August was the rainy
season; and October 2003 was the beginning of the 2003 nortes season. For the rivers, climatic
conditions exerted an effect on their characteristics only from December 2002 to April 2003 (the
nortes to the dry season), so seasonal characterization is not as marked as it is for the water
chemistry of the lagoon.
3.2. Species composition
A total of 179 taxa were recorded in both the lagoon and the three rivers draining into it. There
were 148 species in the lagoon, and 123 in the rivers. Species exclusive to each environment are
indicated in Table 3. The phytoplankton assemblages were mainly comprised of
Bacillariophyceae (76% lagoon, 79% rivers), followed by Dinophyceae (14% lagoon, 7% rivers),
Cyanophyceae (5% lagoon, 6% rivers), Chlorophyceae (3% lagoon, 4% rivers), Euglenophyceae
(1% lagoon, 1% rivers) and other phytoflagellates (1% lagoon, 3% rivers).
Diatoms dominated the phytoplankton composition of the lagoon, except in February, April
and June when dinoflagellates dominated (Fig. 4). In October 2002, December 2002 and October
72
2003 (nortes season) the most abundant species were Skeletonema costatum, S. pseudocostatum,
S. subsalsum, and Chaetoceros subtilis var. abnormis f. simplex (Fig. 4a). In February (transition
from the nortes to the dry season) the dinoflagellates Peridinium aff. quinquecorne and
Prorocentrum cordatum dominated the assemblage, then in April (dry season) Ceratium furca
var. hircus and the diatom Thalassiosira cedarkeyensis dominated. June (transition dry-rainy
season) was dominated by Prorocentrum cordatum and the dinoflagellate Scrippsiella sp. was
also abundant (Fig. 4b). In June, solitary diatoms were caught, and in August (rainy season) a
complex of Cyclotella species (Cyclotella cryptica, C. meneghiniana and C. striata),
Chaetoceros simplex and C. holsaticus dominated the assemblage (Fig. 4c). Cyclotella cryptica,
C. meneghiniana and Chaetoceros simplex persisted until October 2003 (beginning of the nortes
season) when Skeletonema spp. dominated again.
3. 3. Cell density
Variation in cell density over time was seasonal. According to the ANOVA, these differences
depended on the environment (F = 5.68, P < 0.001). In the lagoon, two peaks in cell density were
detected: one in December 2002 and the other in August 2003. Cell density in August was
highest and was significantly different from the other months with the exception of December
2002 (P = 0.29) (Fig. 5a). For the rivers, surface cell density in December 2002 was significantly
different from that of October 2003 when the highest cell densities were recorded (P = 0.002)
(Fig. 5). There were no significant differences in cell density between surface and bottom
samples from the lagoon for most months, except in October 2003 (P = 0.015), and there were no
significant differences between levels in the rivers (Fig. 5b).
73
Peaks in cell density were caused by the phytoplankton species that formed blooms (more than
1000 cells ml-1): Skeletonema subsalsum, S. pseudocostatum in the nortes season; Cyclotella spp.,
and Chaetoceros holsaticus in the rainy season. Even in the dry season at their lowest densities,
Peridinium aff. quinquecorne and Prorocentrum cordatum formed blooms.
3.4. Diversity
The diversity indexes calculated for the rivers were higher than those for the lagoon in most
months (Table 4). The diversity index for the lagoon was highest in April (dry season), when cell
density was lowest and the lowest value was recorded in August (rainy season) when cell density
was high (Section 3.3.). Except for the Sabalo River in October 2003, the evenness values for the
rivers were higher than those of the lagoon for all months, indicating that species were equally
abundant in these environments. Evenness for the lagoon never reached 0.5, emphasizing the
dominance of the species that formed blooms in the different seasons.
3.5. Relationship between environmental parameters and phytoplankton
The CCA of the lagoon data set resulted in 27.9% of the variance being explained by speciesenvironment relation for the first axis, and 18.3% for the second. The Monte Carlo test showed
that first axis was significant (R = 5.643, P = 0.005), as were all canonical axes (F = 2.767, P =
0.005). The species-environment plot shows that the species associated with a high concentration
of Si-SiO2, moderate concentration of N-NH4+, N-NO3-, and FPAS, and low salinity, temperature,
and P-PO43- concentrations are in the upper left quadrant. This included species such as
Petrodyctium gemma,
Entomoneis
alata,
Skeletonema
74
subsalsum,
S.
pseudocostaum,
Cylindrotheca closterium, and Bacillaria paxillifera (Fig. 6a). These species occurred in the
nortes season and the nortes-dry season transition (Fig. 6b). In the upper right quadrant are those
species positively related with high salinity, high temperature, and high P-PO43-, N-NH4+, N-NO3and FPAS concentrations. These species included the dinoflagellates Ceratium furca,
Prorocentrum cordatum, Protoperidinium sp., Gonyaulax digitale, Amphidinium sp. 1, and the
diatoms Chaetoceros heterovalvatus, Thalassiosira cedarkeyensis, Paralia sulcata, and
Gyrosigma balticum (Fig. 6a). These species occurred during the dry season and dry-rainy season
transition (Fig. 6b). Species associated with high concentrations of Si-SiO2 and O2, high pH, low
salinity and temperature, low concentrations of P-PO43-, N-NH4+, N-NO3- and FPAS are in the
lower left quadrant. These included Thalassiosira simonsenii, Scenedesmus dispar, Cyclotella
striata and C. meneghiniana. These species occurred in the nortes season (Fig. 6b). In the bottom
right quadrant are the species associated with high temperature, high concentrations of O2, high
pH, moderate concentrations of Si-SiO2, low salinity, and low concentrations of P-PO43-, NNH4+, N-NO3- and FPAS: Chaetoceros holsaticus, C. simplex, Cyclotella striata, Gyrosigma
robustum which were recorded mainly during the rainy season (Fig. 6b).
The CCA on the river resulted in the first axis explaining 24.1% of the variance of the speciesenvironment relationship and the second, 21.7%. The Monte Carlo test returned a significant
value for all canonical axes (F = 1.341, P = 0.04). The species-environment plot shows that
species in the upper left quadrant are positively related to physical parameters such as high
salinity and high temperature, and high concentrations of FPAS, and negatively correlated with
low concentrations of Si-SiO2. These species included Cocconeis scutellum, Prorocentrum
cordatum,
Chaetoceros
simplex,
Cylindrotheca
closterium,
Chaetoceros
holsaticus,
Thalassiosira cedarkeyensis, and Peridinium aff. quinquecorne. Species associated with high
concentrations of Si-SiO2 were Nitzschia hantzschiana, Auliscus sp., Fragilaria ulna var.
75
goulardii, Gomphonema parvulum, F. ulna var. ulna, and N. frustulum (Fig. 6). As also seen in
Section 3.1., the site-environmental biplot showed no clear pattern of seasonal variation (Fig. 6).
4. Discussion
4.1. Environmental parameters
The salt wedge caused by the tidal regime in this zone is a constant characteristic of
Sontecomapan Lagoon. The concentrations of nutrients in samples from the bottom were usually
higher in N compounds, while silica was higher in samples from the surface. This pattern
indicates that the salt wedge may be acting as a recycling mechanism for nutrients from
sediments while Si-SiO2 is supplied by freshwater input from the rivers to the lagoon. The salt
wedge may be an important mechanism for transporting nutrients from the lagoon to the sea (De
la Lanza-Espino and Rodríguez-Medina, 1993). In addition, the high number of marine species
recorded in the lagoon suggests that the transportation of phytoplankton species between the sea
and the lagoon by daily tides has an important effect on the structure of the phytoplankton
community and diminishes evenness as shown in Section 3.4.
The rivers were important sources of nutrients for the lagoon (Section 3.1.) and this is
indicated by the seasonal variation in N-NO3- and Si-SiO2. Both were a function of freshwater
flow, and decreased during the driest period. However, concentrations of P-PO43- and N-NH4+
were highest in the dry season, so these nutrients might have been produced by internal
biogeochemical cycles including sediment-water column exchange and decomposition processes
(Perkins, 1974; Twilley et al., 1999). Together with the peaks in these nutrients, high
concentrations of FPAS were detected in the lagoon. The peaks in the concentrations of P-PO43-,
76
N-NH4+ and FPAS were similar to the peak in mangrove litter fall production reported for this
lagoon from February to March in the same year; with the decomposition rate for leaf litter high
in the dry season (Aké-Castillo et al., 2006). The availability of P and N compounds has been
shown to result from decomposition processes (Davis III et al., 2003) so mangrove litter fall may
be a source of these nutrients in the short term (i.e. seasonally).
Our values for physicochemical parameters were similar to the values reported for the lagoon
in 1992 by Contreras and Castañeda (2004), except for N-NH4+ which was extraordinarily high in
our study (mean annual value = 29.4 vs. 6.85 in 1992). Ammonia can result from the reduction of
N-NO3- by heterotrophic bacteria or the decomposition of organic matter (Gürel et al., 2005), so it
may be possible to attribute the low concentration of N-NO3- in Sontecomapan Lagoon and high
concentration of N-NH4+ to rapid rates of nitrate ammonification and the high concentration of
organic matter in the sediment. Mean Si-SiO2 concentration was high compared to the tropical
coastal lagoons of Yucatan on the Gulf of Mexico (1.8-105.1 µM, Pennock et al., 1999). The
concentration of Si-SiO2 in the streams of the Los Tuxtlas region, where Sontecomapan Lagoon
is located, have been shown to be high (439-979.5 µM; Ramos-Escobedo and Vázquez, 2001), so
the concentrations recorded for Sontecomapan Lagoon and its tributaries fall within this range.
The high Si-SiO2 concentration in the lagoon may in part explain the dominance of diatoms. The
mean concentration of FPAS in the lagoon is in the range reported for a coastal zone in India
(0.060-0.161 mgl-1, Kalesh et al., 2001), but the maximum value reached 0.236 mgl-1, reflecting
the notable input of plant organic matter to the lagoon.
4.2. Phytoplankton dynamics
77
Phytoplankton assemblage dynamics were characterized by the dominance of a few species
through the seasonal cycle (Sections 3.2., 3.3. and 3.4.). During the nortes season, an assemblage
of Chaetoceros subtilis var. abnormis f. simplex and Skeletonema spp. with affinities for
freshwater, brackish water, and marine salinities (Aké-Castillo et al., 1995, 2004), dominated the
assemblage. Blooms of Skeletonema species have been recorded elsewhere (Nikulina, 2003). The
dry season was characterized by a succession of dinoflagellates with affinities for a wide range of
salinity. The dinoflagellates P. aff. quinquecorne and Prorocentrum cordatum have been reported
for brackish water environments and forming blooms in coastal systems (Barón-Campis et al.,
2005, Phlips et al., 2002). Moreover, the latter species has been recorded as toxic (Grzebyk et al.,
1997) and has spread worldwide (Hajdu et al., 2000). The dinoflagellate Ceratium furca var.
hircus seems to be a resident microalga in Sontecomapan Lagoon which has grown best in the
dry season since 1991 (Guerra-Martínez and Lara-Villa, 1996). In the rainy season freshwater to
brackish water species of Cyclotella were found (Reimann et al., 1963) with brackish water
species of Chaetoceros (Hasle and Syvertsen, 1997). To our knowledge Chaetoceros holsaticus
is recorded here for the first time as causing blooms. Owing to the high cell densities throughout
the seasons and the records of all these species, Sontecomapan Lagoon can be considered a
eutrophic aquatic system (Livingstone, 2001).
4.5. Relationship of phytoplankton to physicochemical parameters
The dynamics of community structure among the diatoms and dinoflagellates is similar to that
reported for estuaries with a strong relationship to the salinity gradient and changes in
temperature (Trigueros and Orive, 2001). However, in addition to the changes in salinity,
temperature and nutrient availability resulting from the influence of seasons, the pattern observed
78
in Sontecomapan Lagoon seems to be related to the interaction of these factors with FPAS. The
ordination of species along the gradient of the FPAS vector on the species biplot of CCA shows
that the species associated with high values of these substances were, in this order, C. furca, P.
aff. quinquecorne, Thalassiosira cedarkeyensis and P. cordatum; all species that dominated
assemblages during the dry season. Species associated with the middle part of the FPAS gradient
were Skeletonema subsalsum, Sccripssiella sp. and Nitzschia amphibia, which were recorded
during the nortes season, and finally, species associated with low concentrations of FPAS were
Cyclotella meneghiniana and C. cryptica, C. striata, Chaetoceros holsaticus, C. simplex,
Scenedesmus dispar and Gyrosigma robustum which were present in the rainy season.
A response to substances derived from plant organic matter has been observed in different
microalgae, and both negative and positive effects on growth have been reported (Prakash and
Rashid, 1968; Prakash et al., 1973; Herrera-Silveira and Ramírez-Ramírez, 1996; Klug, 2002).
Response to these kinds of substances seems to depend entirely upon the physiology of the
species. Granéli et al. (1985) have demonstrated that humic substances, together with the addition
of phosphates, promoted the growth of P. minimum (= P. cordatum), and this coincides with our
observations when FPAS and P-PO43- increased in the dry season. Herrera-Silveira and RamírezRamírez (1996) demonstrated that the growth of Skeletonema costatum was inhibited at high
concentrations of tannic acid, while at low concentrations growth was promoted. In
Sontecomapan Lagoon, Skeletonema spp. caused blooms when FPAS concentrations were
moderate with respect to the range detected for this lagoon.
5. Summary and conclusion
79
Sontecomapan Lagoon can be characterized as a seasonal system with a high concentration of
nutrients. In the nortes season the concentrations of nutrients and FPAS, as well as salinity,
varied widely depending on the intensity of rainfall and hurricane events; but generally,
concentrations of Si-SiO2 were high and salinity and temperature were low in the lagoon. In the
dry season the lagoon’s concentrations of P-PO43-, N-NH4+ and FPAS were high, as were values
for salinity and temperature. In the rainy season the lagoon was characterized by high Si-SiO2
concentrations, low N-NO3- concentrations, low salinity, and warm temperatures. Variation in SiSiO2 seems to depend entirely on supply by the rivers, while variation in the other nutrients
depends on the internal biogeochemical processes of the lagoon. Variations in the concentration
of FPAS indicate that nutrient regeneration from the decomposition of plant organic matter, i.e.
litterfall from mangrove community, could play an important role in making nutrients available
to the phytoplankton community and shape its composition. The dynamics of the phytoplankton
assemblages followed the variations in nutrient concentration over the seasons with changes in
species composition reflecting changes in salinity. Variations in the phytoplankton community
can be characterized by season: Skeletonema spp. (nortes) – dinoflagellates and tychoplanktonic
diatom Thalassiosira cedarkeyensis (dry) – Cyclotella spp. and Chaetoceros spp. (rainy) are
dominant species in succession. Tolerance to FPAS seemed to favour the growth of certain
species. In the nortes season, freshwater species, brackish water species and marine species with
moderate tolerance to FPAS were present. In the dry season brackish water-marine species of
dinoflagellates and a solitary diatom tolerant to high concentrations of FPAS succeeded, while
freshwater-brackish water species with a low tolerance to FPAS characterized the rainy season.
Acknowledgements
80
The Instituto de Ecología, A. C. (projects 902-17 and 902-11-280) and CONACYT (32732-T)
provided financial support. We thank Ricardo Madrigal, Javier Tolome and Olivia Hernández for
providing support in the field. Ariadna Martínez helped with the laboratory analyses of water
samples. E. Philps, Edna Granéli and Susana Hajdu kindly provided basic literature. Angélica
Hernández made valuable suggestions regarding the statistical analyses. M. Favila kindly read
and improved an earlier manuscript. We thank B. Delfosse for helping with the English. The first
author gratefully acknowledges the support of CONACYT (scholarship 90031) during his
doctoral studies as this study is part of his Ph.D. thesis.
References
Aké-Castillo, J. A., Meave, M. E., Hernández-Becerril, D. U., 1995. Morphology and distribution
of species of the diatom genus Skeletonema in a tropical coastal lagoon. European Journal of
Phycology 30, 107-115.
Aké-Castillo, J. A., Guerra-Martínez, S. L., Zamudio-Reséndiz, M. E., 2004. Observation on
some species of Chaetoceros (Bacillariophyceae) with reduced number of setae from a
tropical coastal lagoon. Hydrobiologia 524, 203-213.
Aké-Castillo, J. A., Vázquez, G., López-Portillo., J., 2006. Litterfall and decomposition of
Rhizophora mangle L. in a coastal lagoon in the southern Gulf of Mexico. Hydrobiologia 559,
101-111.
APHA, 1998. Standard methods for the examination of water and wastewater. APHA, AWWA,
WPCF, USA, 1193 pp.
81
Barón-Campis, S. A., Hernández-Becerril, D. U., Juárez-Ruíz, N. O., Ramírez-Camarena, C.,
2005. Red tide produced by the dinoflagellate Peridinium quinquecorne in Veracruz, Mexico
(Oct-Nov. 2002): morphology of the causative agent. Hidrobiológica, 15, 73-78.
Contreras, F., Castañeda, O., 2004. Las lagunas costeras y estuarios del Golfo de México. In:
Caso, M., Pisanty, I., Excurra., E. (Eds.), Diagnóstico ambiental del Golfo de México.
Instituto Nacional de Ecología (INE_SEMARNAT). Mexico, pp. 373-415.
Conzonno, V. H., Fernández, A., 1996. Humic substances and phytoplankton primary production
in Chascomus pond (Argentina). Facts and speculations. Revista de la Asociación de Ciencias
Naturales del Litoral 27, 35-42.
Cupp, E. F., 1943. Marine plankton diatoms of the west coast of North America. University of
California Press. Bulletin Scripps Institute of Oceanography 5, 1-128.
Danilov, R. A., Ekelund, N. G. A., 2001. Effects of solar radiation, humic substances and
nutrients on phytoplankton biomass and distribution in lake Solumsjö, Sweden.
Hydrobyologia 444, 2003-212.
Davis III, S. E., Corronado-Molina, C., Childers, D. L., Day Jr., J. W., 2003. Temporally
dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter
in oligotrophic mangrove wetlands of the Southern Everglades. Aquatic Botany 75, 199-215.
De la Lanza-Espino, G., Rodríguez-Medina, M. A., 1993. Nutrient exchange between subtropical
lagoons and the marine environment. Estuaries 16, 273-279.
Dodge, J. D., 1985. Marine dinoflagellates of the British Isles. HSMO. London, 303 pp.
Emery, K. O., Stevenson., R. E., 1957. Estuaries and lagoons. In: Hedgpeth, J. W. (Ed.). Treatise
on Marine Ecology and Paleoecology. Geol. Soc. Amer. Mem. 67. New York, pp. 673-750.
Granéli, E., Edler, L., Gedziorowska, D., Nyman, U., 1985. Influence of humic and fulvic acids
on Prorocentrum minimum (Pav.) J. Schiller. In Anderson, D.M., White, A. W., Baden, D. G.
82
(Eds), Toxic dinoflagellates. Elseviere Science Publishing Co. Inc., North-Holland, pp. 201206.
Grzebyk, D., Denardou, A., Berland, B., Pouchus, Y. F., 1997. Evidence of a new toxin in redtide dinoflagellate Prorocentrum minimum. Journal of Plankton Research 19, 1111-1124.
Guerra-Martínez, S. L., Lara-Villa, M. A., 1996. “Florecimiento” de Ceratium furca
(Peridiniales: Ceratiaceae) en un ambiente salobre: Laguna de Sontecomapan, México.
Revista de Biologia Tropical 44, 23-30.
Guildford, S. J., Healey, F. P., Hecky, R. E., 1987. Depression of primary production by humic
matter and suspended sediment in limnocorral experiments at Southern Indian Lake, northern
Manitoba. Canadian Journal of Fisheries and Aquatic Sciences 44, 1408-1417.
Gürel, M., Tanik, A., Russo, R. C., Gönenç, I. E., 2005. Biogeochemical cycles. In: Gönenç, I.
E., Wolflin, J. P. (Eds.). Coastal lagoons. Ecosystem processes and modelling for sustainable
Hajdu, S., Edler, L., Olenina, I., Witek, B., 2000. Spreading and establishment of the potentially
toxic dinoflagellate Prorocentrum minimum in the Baltic Sea. International Review of
Hydrobiology 85, 561-575.
Hasle, G. R., 1978a. The inverted-microscope method. In: Sournia, A. (Ed.), Phytoplankton
manual, UNESCO, Paris, pp. 88-96.
Hasle, G. R., 1978b. Diatoms. In: Sournia, A. (Ed.), Phytoplankton manual, UNESCO, Paris, pp.
136-142.
Hasle, G. R., & Syvertsen, E. E., 1997. Marine diatoms. In: Tomas, C. R. (Ed.), Identifying
marine phytoplankton, Academic Press, USA, pp. 5-385.
Herrera-Silveira, J. A., Ramírez-Ramírez, J., 1996. Effects of natural phenolic material (tannins)
on phytoplankton growth. Limnology and Oceanography 41, 1018-1023.
83
Horwitz, E., 1980. Official methods of analysis of the Association of Official Analytical
Chemists. 13th Edition. Washington, USA, 1018 pp.
Jackson, T. A., Hecky, R. E., 1980. Depression of primary productivity by humic matter in lake
and reservoir waters of the boreal forest zone. Canadian Journal of Fisheries and Aquatic
Sciences 37, 2300-2317.
Jongman, R. H. G., Ter Braak, C. J. F., van Torengen, O. F. R., 1987. Data analysis in
community and landscape ecology. Cambridge University Press, UK, 299 pp.
Kalesh, N. S., Sujatha, C. H., Nair, S. M., 2001. Dissolved folin phenol active substances (tannin
and lignin) in the seawater along the west coast of India. Journal of Oceanography 57, 29-36.
Klug, J. L., 2002. Positive and negative effects of allochthonous dissolved organic matter and
inorganic nutrients on phytoplankton growth. Canadian Journal of Fisheries and Aquatic
Sciences 59, 85-95.
Krammer, K., Lange-Bertalott, H., 1991a. Bacillariophyceae. 3. Teil: Centrales, fragilariaceae,
Eunotiaceae. 166 tafeln mit 2180 figuren. Gustav Fischer Verlag Stuttgart. Germany, 576 pp.
Krammer, K., Lange-Bertalott, H., 1991b. Bacillariophyceae. 4. Teil: Achnanthaceae, Kritische
Ergänzungen zu Navicula (Lineolatae) und Gomphonema Gesamliteratuverzeichnis Teil 1-4.
88 tafeln mit 2048 figuren. Gustav Fischer Verlag Stuttgart. Germany, 437 pp.
Krammer, K., Lange-Bertalott, H., 1999. Bacillariophyceae. 1. Teil: Naviculaceae. 206 tafeln mit
2976 figuren. Spektrum Akademischer Verlag. Germany, 876 pp.
Lankford, R. R., 1977. Coastal lagoons of Mexico, their origin and classification. In: Wiley, M.
(Ed.), Estuarine Processes, Academic Press, Inc. USA, pp. 182-215.
Livingstone, R. J. 2001. Eutrophication processes in coastal systems. Origin and succession of
plankton blooms and effects on secondary production in gulf coast estuaries. CRC Press,
USA. 327 pp.
84
Nikulina, V. N., 2003. Seasonal dynamics of phytoplankton in the inner Neva Estuary in the
1980s and 1990s. Oceanologia 45, 25-39.
Pennock, J. R., Boyer, J. N., Herrera-Silveira, J. A., Iverson, R. L., Whitledge, T. E., Mortazavi,
B., Comín, F. A., 1999. Nutrient behavior and phytoplankton production in the Gulf of
Mexico estuaries. In: Bianchi, T. S., Pennock, J. R., Twilley R. R., (Eds.), Biogeochemistry of
Gulf of Mexico Estuaries, John Wiley & Sons, Inc. USA, pp. 109-162.
Perkins, E. J., 1974. The marine environment. In: Dickinson, C. H., Pugh, G. J. F. (Eds.), Biology
of plant litter decomposition, Academic Press, London, pp. 683-721.
Phlips, E. J., Badylak, S., Grosskopf, T., 2002. Factors affecting the abundance of phytoplankton
in a restricted subtropical lagoon, the Indian River lagoon, Florida, USA. Estuarine and
Coastal Shelf Science 55, 385-402.
Prakash, A., Rashid, M. A., 1968. Influence of humic substances on the growth of marine
phytoplankton: Dinoflagellates. Limnology and Oceanography 13, 598-606.
Prakash, A., Rashid, M. A., Jensen A. & Subba Rao. D. V., 1973. Influence of humic substances
on the growth of marine phytoplankton: Diatoms. Limnology and Oceanography 18, 516-524.
Prasad, A. K. S. K., Fryxell, G. A., Livingston, R. J., 1993. The genus Thalassiosira
(Bacillariophyta): T. cedarkeyensis, a new marine benthic diatom from the Florida Coast of
the Gulf of Mexico. Phycologia 32, 204-212.
Reimann, B. E. F., Lewin, J. M. C., Guillard, R. R. L., 1963. Cyclotella cryptica, a new brackishwater diatom species. Phycologia 3, 75-84.
Rivera-Monroy, V. H., Day, J. W., Twilley, R. R., Vera-Herrera, F., Coronado-Molina, C., 1995.
Flux of nitrogen and sediment in a fringe mangrove forest in Terminos lagoon, Mexico.
Estuarine, Coastal and Shelf Science 40, 39-160.
85
Rivera-Monroy, V. H., Madden, C. J., Day Jr., J. W., Twilley, R. R., Vera-Herrera, F., AlvarezGuillén H., 1998. Seasonal coupling of a tropical mangrove forest and an estuarine water
column: enhancement of aquatic primary productivity. Hydrobiologia 379, 41-53.
StatSoft, Inc., 2004. STATISTICA (data analysis software system), ver. 7.0 www.statsoft.com.
Steidinger, K. A., Tangen, K., 1997. Dinoflagellates. In: Tomas, C. R. (Ed.), Identifying marine
phytoplankton, Academic Press, USA, pp. 387-589.
Strickland, J. D. H., Parsons, T. R., 1977. A practical handbook of seawater analysis. Bulletin
167. Second Edition. Fisheries Research Board of Canada. Ottawa, 310 pp.
Tam, N. F. Y., Vrijmoed, L. L. P., Wong, Y. S., 1990. Nutrient dynamics associated with leaf
decomposition in a small subtropical mangrove community in Hong Kong. Bulletin of Marine
Science 47, 68-78.
Ter Braak, C. J. F., 1986. Canonical Correspondence Analysis: A new eigenvector technique for
multivariate direct gradient analysis. Ecology 67, 1167-1179.
Ter Braak, C. J. F., Smilauer, 1998. CANOCO reference manual and user’s guide to Canoco for
Windows: software for canonical community ordination (version 4) Microcomputer Power,
USA, 352 pp.
Toledo, A. P. P., Tundisi, J. G., D’Aquino, V. A., 1980. Humic acid influence on the growth and
copper tolerance of Chlorella sp. Hydrobiologia 71, 261-263.
Toledo, A. P. P., D’Aquino, V. A., Tundisi, J. G., 1982. Influence of humic acid on growth and
tolerance to cupric ions in Melosira (subsp. subartica). Hydrobiologia 87, 247-254.
Trigueros, J. M., E. Orive., 2001. Seasonal variations of diatoms and dinoflagellates in a shallow,
temperate estuary, with emphasis on neritic assemblages. Hydrobiologia 444, 119-133.
Troccoli, L., Herrera-Silveira, J. A., Comín, F. A., 2004. Structural variations of phytoplankton in
the coastal seas of Yucatan, Mexico. Hydrobiologia 519, 85-102.
86
Twilley, R. R., Cowan, J., Miller-Way, T., Montagna, P. A., Mortazavi, B., 1999. Benthic
nutrient fluxes in selected estuaries in the Gulf of Mexico. In: Bianchi, T. S., Pennock, J. R.,
Twilley., R. R., (Eds.), Biogeochemistry of Gulf of Mexico Estuaries, John Wiley & Sons,
Inc. USA, pp. 163-209.
Wafar, S., Untawale, A. G., Wafar, M., 1997. Litterfall and energy flux in a mangrove ecosystem.
Estuarine, Coastal and Shelf Science 44, 111-124.
Weber, J., 2005. Definition of soil organic matter and humic acids based products.
http://www.humintech.com/01/articles/articles_definition_of_soil_organic_matter3.html
Wetzel, R. G., 2001. Limnology. Lake and river ecosystems. Academic Press, USA, 1006 pp.
Zar, J. H., 1999. Biostatistical analysis. Prentice-Hall, Inc. USA, 662 pp.
87
Figure captions
Figure 1. The Sontecomapan Lagoon with sampling stations.
Figure 2. Variation in physicochemical parameters measured from October 2002 to October
2003. a) salinity, b) O2, c) temperature, d) pH, e) N-NH4+, f) N-NO3-, g) P-PO43-, h) Si-SiO2, i)
FPAS. Middle points represent the mean, whiskers are 95% confidence intervals. L indicates
lagoon and R rivers. The continuous line represents the surface level and the dotted line is the
bottom level.
Figure 3. Variation in the mean of the first axis extracted from PCA. Whiskers are 95%
confidence intervals. The continuous line represents the lagoon and the dotted line is the rivers. L
indicates lagoon and R rivers. Different letters indicate significant differences (P < 0.05).
Figure 4. Dynamics of dominant phytoplankton species. a) nortes season, b) dry season, c)
rainy season. Middle points represent the mean, whiskers show the minimum and maximum
values. Note Y scale is logarithmic.
Figure 5. Cell density for each month in the (a) lagoon and (b) rivers. The middle point
represents the mean and whiskers are 95% confidence intervals. The continuous line represents
the surface level and the dotted line is the bottom level. Note Y scale is logarithmic.
Figure 6. Correlation biplot based on CCA analyses. a) Environmental-species biplot of the
lagoon. b) Environmental-site biplot of the lagoon. c) Environmental-species biplot of the rivers.
d) Environmental-site biplot of the rivers. Environmental variables are indicated by arrows.
Environmental scores were multiplied by 2 to fit the coordinate system. Abbreviations of species
are given in Table 3. In figures (a) and (c), the dominant species are marked as follows: solid
rhombus nortes season, solid circles dry season, and solid triangles rainy season. In figures (b)
and (d), solid circles represent samples from October 2002; plus symbol December 2002; empty
88
triangle February 2003; solid rhombus April 2003; solid triangle June 2003; solid square August
2003; and empty circle October 2003.
89
Figure 1
90
Figure 2
91
Figure 3
92
Figure 4
93
Figure 5
94
Figure 6
95
Table 1. Annual mean values and concentrations of physicochemical characteristics of the
Sontecomapan Lagoon and three rivers. Standard deviation in parenthesis. * Significantly greater
(P < 0.015)
Parameter
Lagoon
Rivers
Salinity
12.68 (10.5)*
7.90 (10.8)
Temperature ºC
28.69 (2.7)*
26.63 (3.0)
O2 %
7.04 (1.5)*
5.59 (1.8)
pH
7.44 (0.4)*
7.06 (0.3)
N-NH4+ µM
29.40 (29.9)
29.67 (27.5)
N-NO3- µM
3.28 (3.8)
5.07 (4.9)*
P-PO43- µM
1.03 (0.9)
1.40 (1.0)*
Si-SiO2 µM
412.92 (243.8)
499.46 (249.6)*
FPAS mg L-1
0.10 (0.06)*
0.06 (0.06)
96
Table 2. Factor loadings from the first axis extracted from the PCAs on data sets for the
Sontecomapan Lagoon and three rivers. Numbers in bold indicate major loading
Variable
Lagoon
Rivers
Factor 1
Factor 1
Salinity
0.90
-0.89
O2 %
-0.22
0.52
Temperature
0.34
-0.68
pH
-0.04
-0.06
N-NH4+
0.77
-0.63
N-NO3-
-0.31
0.53
P-PO43-
0.32
-0.43
Si-SiO2
-0.89
0.83
FPAS
0.25
-0.58
eigenvalue
2.67
3.48
% total variance
29.72
38.69
97
Table 3. List of species found in the Sontecomapan Lagoon and the three rivers draining into it. *
indicates a species is present, and ** indicates the species that were used in the CCA analyses.
BACILLARIOPHYCEAE
Achnanthes cf. curvirostrum J. Brun
Achnanthes exigua Grunow in Cleve & Grunow
Achnanthes sublaevis Hustedt
Achnanthes sp.
Amphipleura sp.
Amphora sp.
Asterionellopsis glacialis (Castracane) Round
Azpeitia nodulifera (Schmidt) Fryxell et Sims
Bacillaria paxillifera (O. F. Müller) Hendey
Bacteriastrum elegans Pavillard
Bacteriastrum elongatum Cleve
Biddulphia pulchella S. F. Gray
Biddulphia sp.
Caloneis sp.
Chaetoceros affinis Lauder
Chaetoceros curvisetus Cleve
Chaetoceros danicus Cleve
Chaetoceros diversus Cleve
Chaetoceros heterovalvatus Proschkina-Lavrenko
Chaetoceros holsaticus Schütt
Chaetoceros laciniosus Schüt
Chaetoceros lorenzianus Grunow
Chaetoceros mulleri var subsalsum (Lemmermann)
Johansen et Rushforth
Chaetoceros peruvianus Brightwell
Chaetoceros simplex Ostenfeld
Chaetoceros subtilis var. abnormis f. abnormis ProschkinaLavrenko
Chaetoceros subtilis var. abnormis f. simplex ProschkinaLavrenko
Chaetoceros throndsenii var. throndsenia (Marino,
Montresor & Zingone) Marino, Montresor & Zingone
Chaetoceros throndsenii var. trisetosa Zingone in Marino et
al.
Cocconeis scutellum Ehrenberg
Coscinodiscus concinnus Wm. Smith
Coscinodiscus granii Gough
Coscinodiscus radiatus Ehrenberg
Cyclotella cf. austriaca (M. Peragallo) Hustedt
Cyclotella cryptica Reimann Lewin et Guillard
Cyclotella meneghiniana Kützing
Cyclotella striata (Kützing) Grunow
98
CODE
Achsu
Amphi
Asgla
Bapa
Chhet
Chhol
Chsim
Lagoon Rivers
*
*
*
**
*
*
**
*
*
*
*
**
**
*
*
*
*
*
*
*
*
*
*
*
**
*
**
**
*
*
*
*
*
**
*
**
*
Chabsim
**
**
*
Coscu
Cossp1
Cyaus
Cycplx
Cycplx
Cystr
*
*
**
*
*
*
**
**
**
**
*
**
**
**
**
Cylyndrotheca closterium (Ehrenberg) Reimann et Lewin
Cymatopleura sp.
Cymatosira sp.
Cymbella sp.
Diploneis bombus Ehrenberg
Diploneis sp.
Ditylum brightwelli (West) Grunow
Entomoneis alata (Ehrenberg) Ehrenberg
Eucampia zodiacus Ehrenberg
Fragilaria counstruens f. counstruens (Ehrenberg) Hustedt
Fragilaria ulna var. goulardii (Bréb. Ex Cleve et Grunow)
Lange-Bertalot
Fragilaria ulna var. ulna (Nitzsch) Lange-Bertalot
Fragilaria sp.
Gomphoneis olivacea (Lyngbye) Dawson
Gomphonema parvulum (Kützing) Kützing
Guinardia flaccida (Castracane) Peragallo
Guinardia striata (Stolterfoth) Hasle
Gyrosygma balticum (Ehrenberg) Rabenhorst
Gyrosygma fasciola (Ehrenberg) Griffith & Henfrey
Gyrosygma robustum (Grunow in Cleve & Grunow) Cleve
Gyrosygma cf. terryanum (H. Peragallo) Cleve
Gyrosygma sp.
Hemiaulus sinensis Greville
Hyalodiscus sp.
Leptocylindrus danicus Cleve
Licmophora sp.
Lithodesmium undulatum Ehrenberg
Luticula mutica (Kützing) D. G. Mann in Round et al.
Luticula sp.
Lyrella impercepta (Hustedt) Moreno
Lyrella sp.
Melosira nummuloides Agardh
Minidiscus comicus Takano
Navicula cryptocephala Kützing
Navicula soehrensis Krasske
Navicula pelliculosa (Kützing) Hilse
Navicula cf. pennata Schmidt in Schmidt
Navicula cf. peregrina (Ehrenberg) Kützing
Navicula cf. takoradiensis Hendey
Navicula sp. 1
Navicula sp. 2
Neidium cf. Iridis (Ehr.) Cleve
Neidium sp.
Neocalyptrella robusta (Norman ex Ralfs) HernándezBecerril & Meave
Nitzschia amphibia Grunow
99
Cylclos
Cymsp1
**
*
*
Enala
*
*
**
*
*
**
**
*
*
*
**
*
Fugou
Fuuln
Gooli
Gopar
Gybal
Gyrob
Gyterr
Hyasp
**
**
*
**
*
*
**
*
**
**
*
*
**
*
*
*
Menum
Navpe
Nitamp
**
*
*
*
*
*
**
*
*
*
*
*
*
**
**
**
*
**
**
*
*
*
*
*
*
*
*
*
*
*
*
*
**
*
*
*
**
*
*
*
*
*
Nitzschia constricta (Kützing) Ralfs
Nitzschia frustulum (Kützing) Grunow
Nitzschia hantzschiana Rabh
Nitzschia longissima (Brébisson in Kützing) Ralfs in
Pritchard
Nitzschia ovalis Arnott
Nitzschia palea (Kützing) Wm. Smith
Nitzschia sigma (Kützing) Wm. Smith
Nitzschia triblyonella Hantzsch
Nitzschia cf. Linearis W. Smith
Nitzschia sp.
Odontella longicruris (Greville) Hoban
Opephora martiyi Héribaud
Paralia sulcata (Ehrenberg) Cleve
Petrodyction gemma (Ehr.) D. G. Mann
Petroneis humerosa (Breb. Ex Smith) Stickle & Mann
Pinnularia sp.
Plagiotropis sp.
Pleurosigma acuminatum (Kützing) Grunow
Pleurosigma angulatum (Quekett) W. Smith
Pleurosigma formosum W. Smith
Pleurosira laevis (Ehr.) Compère
Proboscia alata (Brightwell) Sundström
Psammodictyon constrictum (Gregory) D. G. Mann
Pseudonitzschia sp.
Pseudosolenia calcar-avis (Schultze) Sundström
Rhizosolenia imbricata Brightwell
Rhizosolenia setigera Brightwell
Rhizosolenia sp.
Sellophora pupula (Kützing) Mereschkowsky
Skeletonema costatum (Greville) Cleve
Skeletonema pseudocostatum Medlin
Skeletonema subsalsum (A. Cleve) Bethge
Surirella biseriata Brébisson
Surirella fastuosa Ehrenberg
Surirella febigerii Lewis
Surirella linearis W. Smith
Surirella robusta Ehrenberg
Terpsinoe musica Ehrenberg
Thalassionema nitzschiodez (Grunow) Mereschkowsky
Thalassiosira cedarkeyensi A. K. S. K. Prasad
Thalassiosira eccentrica (Ehrenberg) Cleve
Thalassiosira lineata Jousé
Thalassiosira oestrupii (Ostenfeld) Hasle
Thalassiosira simonsenii Hasle & Fryxell
Thalassiosira decipiens (Grunow) Jörgensen
Thalassiosira weissflogii (Grunow) G. Fryxell & Hasle
100
Nitcon
Nitfru
Nithan
Nitlo
Nitsig
Nittry
Pasul
Pegem
Plfor
**
**
*
**
**
**
*
*
**
**
*
*
*
*
**
**
*
**
*
*
**
*
*
*
**
*
*
*
*
*
Skcos
Skpse
Sksub
*
**
**
**
Sufas
Sufeb
*
**
Tmanit
Thace
*
*
**
**
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
**
**
**
*
**
*
*
*
*
**
**
*
*
Thasim
**
*
*
Thalassiotrhirx longissima Cleve & Grunow
Trachyneis aspera (Ehrenbegr) Cleve
Tryblionella cocconeiformis (Grunow) D. G. Mann
Tryblionella parvula (W. Smith) Ohtsuka & Fujita
Tryblionella punctata Wm. Smith
Tryblionella cf. calida (Grunow) D. G. Mann
*
Traas
Trypun
*
*
**
*
**
*
*
*
CLOROPHYCEAE
Scenodesmus armatus Chad
Scenodesmus dispar (Breb.) Rabenhorst
Scenedesmus cf. pecsensis Uherk.
Closterium sp.
Cosmarium sp. 1
Cosmarium sp. 2
Mougeotia sp.
Ocystis sp.
Scedis
*
**
*
*
*
EUGLENOPHYCEAE
Lepocinclis acus Ehrenberg
Phacus caudatus Huebner
Lepacu
*
*
*
*
*
**
*
CIANOPHYCEAE
Chroccocus sp.
Komovophoron sp.
Merismopedia tenussima Lemmermann
Nostoc sp.
Oscillatorial nigro-viridis Thwaites in Harvey
Oscillatoria cf. limosa Agardh ex Gomant
Oscillatoria sp.
Planktolyngbya sp.
Synechococcus sp.
*
*
*
*
*
*
*
*
*
*
*
*
*
*
DINOPHYCEAE
Amphidinium sphenoidesWulff
Amphidinium sp.1
Amphidinium sp. 2
Ceratium furca var hircus (Schöder) Margalef ex Sournia
Dinophysis caudata Saville-Kent
Gonyaulax digitale (Pouchet) Kofoid
Gymnodinium sp.
Heterocapsa sp.
Noctiluca scintillans (Macartney) Ehrenberg
Oxytoxum sp.
Peridinium aff. quinquecorne
Peridinium sp. 1
Peridinium sp. 2
101
Amsph
Cefuhir
Godig
Pequi
Pesp1
Pesp2
**
*
*
**
*
**
*
*
*
*
**
**
**
*
**
**
*
**
Prorocentrum cordatum (Ostenfeld) Dodge
Prorocentrum gracile Schütt
Prorocentrum lima (Ehrenberg) Dodge
Prorocentrum micans Ehrenberg
Protoperidinium crassipes (Kofoid) Balech
Protoperidinium sp.
Scrippsiella sp.
Procor
Progra
Prolim
Scrsp
OTHER FLAGELLATES
Chlamydomonas sp.
Pyramimonas sp.
Phytoflagellate sp. 1
Phytoflagellate sp. 2
**
**
**
*
*
*
**
**
*
*
*
*
*
*
*
Table 4. Shanon-Wiener Diversity Index (H) and evenness by month. Letters a, b, c, d show
significant differences between sites for a given month (P < 0.05)
Month
Oct 2002
Dec
Feb
Apr
Jun
Aug
Oct 2003
Lagoon
Coscoapan
River
Sabalo River
La Palma
River
H’
0.68a
1.54b
1.09c
1.78b
evenness
0.17
0.67
0.56
0.85
H’
0.56a
1.96b
0.38c
0.62ac
evenness
0.15
0.85
0.19
0.34
H’
0.97a
1.74b
0.91a
1.61b
evenness
0.24
0.72
0.41
0.69
H’
1.50a
2.09b
1.25a
2.25b
evenness
0.39
0.68
0.50
0.64
H’
1.31a
1.82b
1.09a
1.68b
evenness
0.32
0.53
0.41
0.49
H’
0.52a
1.69b
1.07c
0.64a
evenness
0.13
0.62
0.39
0.25
H’
1.27a
2.30b
0.67c
1.16d
evenness
0.29
0.62
0.25
0.42
102
CAPÍTULO 5
Effect of the products of mangrove leaf litter decomposition on primary productivity and
phytoplankton growth
En preparación
103
EFFECT OF THE PRODUCTS OF MANGROVE LEAF LITTER DECOMPOSITION ON
PRIMARY PRODUCTIVITY AND PHYTOPLANKTON GROWTH
Abstract. The relationship between dissolved organic matter and phytoplankton function has
either a positive or a negative effect on primary productivity and phytoplankton growth.
Sontecomapan is a coastal lagoon bordered by a mangrove forest where Rhizophora mangle is
the dominant species. In the lagoon, the concentrations of folin phenol active substances (FPAS)
are indicative of the high input of plant organic matter. Because of the different effects that
organic matter can have on phytoplankton function, we experimented with the effects of extracts
of mangrove leaf litter on primary productivity and phytoplankton growth in different seasons.
The inhibitory and stimulatory effects observed on primary productivity and phytoplankton
growth, are indicative that mangrove leachate is made up of a mixture of stimulatory as well
inhibitory substances. The different effect on primary productivity and phytoplankton growth
suggest that the tolerance of the species to concentrations of folin phenol active substances in the
extracts is important in the response. Chaetoceros muelleri var. subsalsum, Cyclotella cryptica,
and C. meneghiniana were species sensitive to high concentrations of FPAS. Skeletonema
subsalsum was a species able to tolerate moderate concentrations of FPAS. These responses
support the idea that tolerance to organic compounds in natural systems can determine the
dynamics of phytoplankton communities.
Keywords: bioassay, organic matter, phytoplankton, phytoplankton growth, primary
productivity
104
INTRODUCTION
Plant organic matter represents a source of nutrients and humic substances that affects primary
production and determines phytoplankton dynamics in both marine and freshwater environments
(Rivera-Monroy et al. 1998, Herrera-Silveira and Ramírez-Ramírez 1996, Danilov and Edlund
2001, Klug 2002). The relationship between dissolved organic matter and phytoplankton function
can have a positive or a negative effect on primary productivity and phytoplankton growth, so the
net effect of dissolved organic matter is under debate (Klug 2002)
In evaluating the effect of dissolved organic matter on primary productivity, Jackson and
Hecky (1980) found an inverse relationship between primary productivity and dissolved organic
carbon in a lake and reservoirs in Canada, and inferred that depression of primary productivity
was the result of humic substances making iron unavailable. In contrast, Rivera-Monroy et al.
(1998) demonstrated the stimulatory effect of runoff from a fringe mangrove forest on primary
productivity in water from the Terminos Lagoon, Mexico.
The response of phytoplankton growth has been tested using specific humic compounds such
as humic acid, fulvic acid and tannins on different microalgae species. These studies show that
the stimulatory effect of humic substances results from its capacity to chelate damaging metalic
ions such as copper (Toledo et al. 1980, 1982), possibly to sensitize cell, to chelate essential ions
that penetrate the cell (Prakash et al. 1973), and to supply nitrogen as a nutrient (Graneli et al.
1985). The inhibitory effect is mainly due to humic substances decreasing the availability of trace
minerals, such as iron (Imai et al. 1999).
Tropical coastal lagoons and estuaries are characterized by a high input of terrestrial organic
materials from surrounding mangrove communities (Flores-Verdugo et al. 1987, Tam et al.
1990). Mangrove leaves have a high concentration of tannins which are liberated rapidly in the
early stages of decomposition (Cundell et al. 1979). In coastal systems, the concentration of these
105
substances can be high (Kalesh et al. 2001). Sontecomapan is a coastal lagoon bordered by a
mangrove forest where Rhizophora mangle L. is the dominant species. In the lagoon, the
concentration of folin phenol active substances varies seasonally from 0.0 to 0.236 mg l-1 (AkéCastillo and Vázquez, in revision; see Chapter 3). These concentrations are indicative of the high
input of plant organic matter. In the lagoon the phytoplankton dynamics are characterized by
blooms of diatoms and dinoflagellates that dominate the species composition seasonally.
Because of the different effects that organic matter can have on phytoplankton function, we
experimented with the effects of extracts of mangrove leaf litter on primary productivity and
phytoplankton growth in different seasons. We investigated whether mangrove leaf litter was a
source of nutrients throughout the decomposition process. Then, to test the effect of substances
from mangrove leachate, the products from different lengths of decomposition time were used to
test their effect on the primary productivity and phytoplankton growth of a natural community
from Sontecomapan Lagoon.
METHODS
Site description
Sontecomapan Lagoon is a shallow coastal lagoon permanently connected to the Gulf of
Mexico. It is located in the Los Tuxtlas Biosphere Reserve between 18º 30’-18º 34’ N and 94º
59’-95º 04’ W (Fig. 1). This region is characterized by three climatic seasons: dry from March to
May, rainy from June to September, and “nortes” from October to February. The latter is
characterized by strong winds coming from north and sporadic rain fall. This lagoon is bordered
by a mangrove forest where Rhizophora mangle is the dominant species in the system (AkéCastillo et al. 2006). The lagoon is a brackish water system where salinity varies spatially and
temporally from 0 to 35 ups. Variation in the phytoplankton community is reflected by the
106
dominant species in each season: in the nortes season, the diatoms Skeletonema subsalsum, S.
pseudocostatum and S. costatum; during the dry season, the dinoflagellates Peridinium aff.
quinquecorne, Prorocentrum cordatum, Ceratium furca var. hircus, Scrippsiella sp. and the
diatom Thalassiosira cedarkeyensis; and during the rainy season, the diatoms Cyclotella cryptica,
C. meneghiniana, C. striata , Chaetoceros holsaticus and C. simplex (Aké-Castillo and Vázquez,
in revision; see Chapter 3).
Extracts obtained from decomposing Rhizophora mangle leaves
Senescent Rhizophora mangle leaves were collected by hand from the water’s edge in
Sontecomapan Lagoon in February 2003 and taken to the laboratory. Substances from the
decomposing leaves were obtained by incubating known weights (10 g) of the wet fresh leaves in
3 l of fresh water in 3 plastics bottles. Three bottles without leaves were used as controls. These
bottles were maintained at laboratory temperatures, under natural light-dark day conditions and
were aerated using aquarium pumps.
As wet fresh leaves were used for the incubations, initial dry weight was estimated by
weighing 3 samples of the fresh leaves and drying them to constant weight at 60 ºC in a muffle
furnace (Davis III et al. 2003).
On days 0, 2, 5, 10, 25 and 45 a sample of 160 ml of water was taken from each bottle for the
chemical analyses. Ammonium (N-NH4+), nitrate (N-NO3-), orthophosphate (P-PO43-) and folin
phenol active substances (FPAS, i.e tannins and lignins) were determined using colorimetric
techniques following the methods of Strickland and Parsons (1977), Horwitz (1980) and APHA
(1998). Each day a 20 ml sample was frozen for later use in primary productivity and
phytoplankton growth experiments.
107
A two-way repeated measures analysis of variance (ANOVA) was done to test the difference
between the incubating leaves and the control. Factors were the treatment and day. Data were
log10 (x+1) transformed to achieve normality (Zar 1999).
Effect on primary productivity
Experimental design.-The effect of mangrove leaf extract on primary productivity (PP) was
evaluated during 2003 in three different months representing the three climatic seasons: May (dry
season), August (rainy season) and October (nortes season).
There were three treatments with extracts from mangrove leaves in different stages of
decomposition and two controls without them. For one control no extract was added, and for the
other control the freshwater used for incubating the leaf litter was added. The extracts tested were
those obtained on days 2, 10 and 45. The treatments for the experimental design and the
characteristics of the extracts are shown in Table 1. The treatments and controls were tested in
triplicate.
The treatments and controls were tested using water samples from two sites with different
marine influences: one site in the interior of the lagoon and another close to the channel
connection to the sea (Fig. 1).
Primary productivity experiment.- In each month, PP was determined using the light-dark
BOD bottle method, and oxygen concentration was evaluated using the Winkler method
(Vollenweider 1974). BOD bottles were filled with the water collected from the two sites. Except
for treatment 1, BOD bottles were inoculated with 1 ml of each extract (0.3% of volume of BOD)
and were hung to a depth of 20 cm in the lagoon to incubate for 4 hours. The results are
expressed as gross primary productivity (GPP) transformed to mg C L-1hr-1 with a conversion
108
factor of 0.375 of mol carbon production and a photosynthetic coefficient of 1.2 (Wetzel and
Likens 1974).
Statistical analysis.-Differences in GPP between treatments were analyzed with a nested
factorial analysis of variance (ANOVA). Factors were treatment, month, and site nested in
month. Data were log10 (x+1) transformed to achieve normality (Zar 1999). The Statistica ver
7.0 software package was used for the analysis (StatSoft 2004).
Effect on phytoplankton growth
Experimental design.-The effect of mangrove leaf extract on phytoplankton growth was
evaluated in phytoplankton cultures from water samples taken in May, August and October 2003
from site 1 in Sontecomapan Lagoon (Fig.1). The phytoplankton cultures represented the three
climatic seasons: dry, rainy and nortes.
The treatments and controls tested in the PP experiment were tested on phytoplankton growth
either (Table 1). The were five replicates of each treatment and control.
Phytoplankton cultures.-The culture medium was prepared by collecting 3 l water from the
Sontecomapan Lagoon at site 1 (Fig. 1) a month before May, August and October when the
inoculations of phytoplankton were done. The water collected was transported to the laboratory
and filtered using a Millipore membrane of 1.2 µm and sterilized in an autoclave at 120 ºC for 15
minutes. Pyrex culture tubes were filled with the medium (20 ml).
Each month, the culture tubes were transported to the field for the phytoplankton inoculations.
Water with phytoplankton was collected from the lagoon and a 1 ml sample was inoculated in the
tubes. The tubes for each treatment were inoculated with 0.2 ml (1% of the total volume of
cultures) of the mangrove extracts and tubes for one of the controls with 0.2 ml of freshwater
109
used for decomposing leaf litter. A 125 ml water sample from the lagoon was fixed with acetatelugol to count the initial number of phytoplankton cells and to study the species composition at
the beginning the experiment.
The tubes were transported to the laboratory and placed in a culture chamber (LAB-LINE) at
26ºC with a 12/12 light-dark cycle. All the tubes were gently shaken daily, and every 2 or 3 days
a sub-sample was extracted from one tube of each treatment to check phytoplankton growth. On
days 7, 14, 21, 28, 35, 42, and 49 a 1 ml sample from each tube was fixed with acetate-lugol to
count cells and identify the species. This was done in a Neubauer chamber (Semina 1978) using a
light microscope (LEICA).
Statistical analysis.-Differences in phytoplankton growth among treatments were analyzed
with a two-way repeated measures ANOVA. Factors were treatment and day. Data were log10
(x+1) transformed to achieve normality (Zar 1999). The Statistica ver. 7.0 software package was
used for the analysis (StatSoft 2004).
RESULTS
Extract obtained from decomposing Rhizophora mangle leaves
The differences between incubated bottles with leaf litter and controls show that the
decomposition of leaf litter produced N-NH4+ (ANOVA: F = 459.81, P < 0.001), N-NO3(ANOVA: F = 55.47, P < 0.001), and FPAS (ANOVA: F = 459.81, P < 0.001). The concentration
of P-PO43- in the extract was not significantly different from the control (ANOVA: F = 4.8, P =
0.09), so no differences in the concentration of this nutrient resulting from decomposition were
detected.
During the first two days of decomposition there was a rapid increase in the concentrations of
N-NH4+, N-NO3-, and FPAS (Figs 2a, 2b, and 2d). After the 5th day there were changes in the
110
concentrations of nitrogen compounds, but the tendency was for these to decrease (Figs 2a, 2b).
Variation in the concentration of P-PO43- did not differ over time (Fig. 2c). After the 5th day, the
concentration of FPAS increased slowly until the end of the experiment (Fig. 2d).
The different treatments had an effect on PP (ANOVA: F = 12.52, P < 0.001). However
significant differences in the effect of treatments were only detected in the experiments carried
out in May and August.
In May, treatment 5 inhibited PP compared to controls and to the extracts of leaf litter from
days 2 and 10 (P-values < 0.001) at site 1 (Fig. 3). At site 2 the effect was similar but no
significant differences were detected. In August, although no significant effect was detected at
site 1, treatment 3 stimulated PP. At site 2, the effect of treatment 3 differed significantly from
treatment 5 (P = 0.01). This difference resulted from treatment 3 stimulating PP while treatment 5
inhibited it (Fig.3). In October there were no differences among treatments within the sites, but
treatment 3 stimulated GPP at site 2 (Fig. 3).
All phytoplankton cultures began with at least 4 species in each month evaluated (Table 2),
but at the end of the experiments all cultures were dominated by only one species. In May,
Chaetoceros muelleri var. subsalsum accounted for more than 80% of total cell density. In the
experiment carried out on phytoplankton collected in August, a complex of two Cyclotella
species (C. cryptica and C. meneghiniana) accounted for more than 95% of the total cell density.
In the experiment on phytoplankton collected in October, Skeletonema subsalsum accounted for
more than 92% of total cell density. The rest of the species did not survive or their cell density
111
did not increase significantly, so only the effect of the treatments in the growth of the dominant
species is presented.
Treatments affected the growth of Chaetoceros muelleri var. subsalsum (ANOVA: F= 4.46, P
= 0.01) and the cell density was different among days (ANOVA: F= 57.24, P < 0.001). The
differences among treatments did not depend on day (ANOVA: F= 0.69, P = 0.84). Treatment 5
(leaf litter extract obtained on day 45) inhibited growth compared to treatments 1, 2 and 4
(controls and other extracts; P < 0.05). Cell growth under this treatment was always lower than
the growth recorded in the other treatments (Fig. 4a). Although the cell growth in treatment 3
stayed below the growth of treatments 1, 2 and 4, the difference was not significant (P values >
0.05).
The effect of the treatments on the growth of Cyclotella spp. depended on the day on which
the effect was evaluated (ANOVA: treatments: F= 3.11, P = 0.05; day: F= 47.1, P < 0.001;
treatment x day: F= 3.10, P < 0.001). Differences in cell growth were detected on day 14, when
treatment 5 inhibited the growth compared to treatments 1, 2, and 4 (P values < 0.02). Even
though no significant differences were detected on the following evaluation days, the treatments
with leaf litter extract had lower cell densities than the controls after day 35 (Fig 4b).
Treatments did not significantly affect the growth of Skeletonema subsalsum (ANOVA: F=
2.59, P = 0.09) and this not depended on day also (ANOVA: F= 0.36, P = 0.99). In spite of this,
on day 42 cell growth in treatment 3 (extract from day 2) was higher than that of treatments 1 and
2 (controls). On day 49, cell growth in treatments 3 and 4 was also higher (Fig. 4c). Cell density
in treatment 5 (extract from day 45) was always lower than that of the other treatments.
DISCUSSION
Extract obtained from decomposing Rhizophora mangle leaves
112
Leaching has been identified as the main way nutrients are released during the early stages of
decomposition (Davis III et al. 2003). The high concentration of N compounds recorded during
this experiment show that rapid mineralization was occurring, so microbial action was very
important right from the beginning of decomposition (Cundell et al. 1979).
The concentration of FPAS was the result of leaching which continued during the entire
decomposition process. Although FPAS are comprised of different phenolic compounds (APHA,
1998), the high concentrations of tannins in leaf mangrove litter show their importance in the
FPAS analyzed in water.
P-PO43- concentrations could not be attributed to the dynamics of the nutrient from the
decomposing litter. The dynamics of this nutrient indicated that this nutrient could have been
used by increasing microbial activity in litter (Davis III et al., 2003) or rapidly cycling (Gürel et
al. 2005).
The inhibitory effect of decomposing leaf litter extracts on PP in May, the stimulatory and
inhibitory effects in August, and the lack of an effect in October indicate that mangrove leachate
is made up of a mixture of stimulatory as well inhibitory substances. An increase in the PP on
phytoplankton with the addition of runoff from mangrove forest to a water lagoon has been
observed in Terminos Lagoon (Rivera-Monroy et al. 1998), although when highly concentrated
runoff was added, PP was inhibited. Similar responses have been found in experiments on the
photosynthetic activity of some dinoflagellates and diatoms (Prakash and Rashid 1968, Prakash
et al. 1973). The inhibitory effect of humic substances contained in water with a high
concentration of organic matter can be attributed to its ability to chelate trace metals and
phosphate (Jackson and Heckey 1980).
113
In addition, the stimulatory-inhibitory effect on PP detected in experiments suggests that the
metabolism of the phytoplankton species present during the months when the experiments were
carried out (Table 2) affected the responses. Each species has a different threshold for carrying
out biological functions such as photosynthetic activity and growth (Bonilla et al. 1998).
The results of the PP experiments indicate that in May the phytoplankton community was
composed of species sensitive to high concentrations of FPAS which inhibited PP. In August,
species were more sensitive to the addition of the nutrients that stimulated PP and it decreased
when the concentration of FPAS was high. In October species had a high tolerance to high
concentrations of FPAS.
Although the only significant effect of leaf litter extract on growth was detected as the
suppression of growth caused by the extract with a high concentration of FPAS, the following
conclusions can be drawn from the experiments.
A suppression of phytoplankton growth indicated that Chaetoceros muelleri var. subsalsum is
more sensitive to high concentrations of FPAS than Cyclotella cryptica, C. meneghiniana or
Skeletonema subsalsum is. Cyclotella spp. was sensitive to high concentrations of FPAS in its
early stage of growth, but later was able to tolerate them. The growth of Skeletonema subsalsum
was not affected by any treatment, and although the mangrove extracts did not significantly
stimulate growth in all experiments, the positive response of Skeletonema subsalsum in
treatments 3 and 4 indicate that this species might be able to tolerate moderate concentrations of
FPAS. These responses support the idea that tolerance to organic compounds in natural systems
can determine the dynamics of phytoplankton communities (Herrera-Silveira and RamírezRamírez 1996, Aké-Castillo and Vázquez, in revision; see Chapter 3).
114
Experiments carried out on phytoplankton primary productivity and growth showed the effects
of mangrove extract on two different metabolic functions acting on two different time scales:
photosynthetic rate in the short term, and growth in the long term.
Photosynthetic activity is a basic function that determines growth, so the stimulatory and
inhibitory effects on this process are reflected in the species’ growth. Extracts of leaf litter can
enhance PP by supplying nutrients, but if the concentration of FPAS is too high there are no
stimulatory effects and growth can even be suppressed. The negative effect of the extract on PP
in May affected growth, as observed in the negative effect it had on Chaetoceros. The
stimulatory-inhibitory effect on PP in August may be reflected in the adjustment of Cyclotella’s
metabolism observed during its growth. The lack of a significant effect on PP for October may be
indicated by the lack of significant effect on the growth of Skeletonema.
These results support the observation made during a one year study of phytoplankton
dynamics in Sontecomapan Lagoon, where Cyclotella cryptica and C. meneghiniana were
associated with a gradient of low concentrations of FPAS, while Skeletonema subsalsum was
associated with moderate concentrations of FPAS (Aké-Castillo and Vázquez, in revision; see
Chapter 3). Although Chaetoceros muelleri var. subsalsum did not account for more than 3% of
the total cell density in that study, this species can potentially grow in moderate concentrations of
FPAS.
LITERATURE CITED
Aké-Castillo, J. A., G. Vázquez and J. López-Portillo. 2006. Litterfall and decomposition of
Rhizophora mangle L. in a coastal lagoon in the southern Gulf of Mexico. Hydrobiologia
559: 101-111.
115
APHA, 1998. Standard methods for the examination of water and wastewater. APHA,
AWWA, WPCF, USA, 1193 pp.
Bonilla, S., D. Conde and H. Blanck. 1998. The photosynthetic responses of marine
phytoplankton, periphyton and epipsammon to herbicides paraquat and simazine.
Ecotoxicology 7: 99-105.
Cundell, A. M., M. S. Brown, R. Standford, and R. Mitchell. 1979. Microbial degradation of
Rhizophora mangle leaves immersed in the sea. Estuarine, Coastal and Shelf Science 9:
281-286.
Danilov, R. A. and N. G. A. Ekelund. 2001. Effects of solar radiation, humic substances and
nutrients on phytoplankton biomass and distribution in Lake Solumsjö, Sweden.
Davis III, S. E., C. Corronado-Molina, D. L. Childers, and J. W. Day, Jr. 2003. Temporally
dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf
litter in oligotrophic mangrove wetlands of the Southern Everglades. Aquatic Botany, 75:
199-215.
Flores-Verdugo, F. J., J. W. Day Jr. and R. Briseño-Dueñas. 1987. Structure, litterfall,
decomposition, and detritus dynamics of mangroves in a Mexican coastal lagoon with an
ephemeral inlet. Marine Ecology Progress Series 35: 83-90.
Graneli, E., L. Edler, D. Gedziorowska, and U. Nyman. 1985. Influence of humic and fulvic
acids on Prorocentrum minimum (Pav.) J. Schiller. Pages 201-206 in D.M. Anderson, A.
W. White and D. G. Baden, editors. Toxic dinoflagellates. Elsevier Science Publishing Co.
Inc., North-Holland.
116
Gürel, M., A.Tanik, R. C. Russo y I. E. Gönenç. 2005. Biogeochemical cycles. In: I.
E.Gönenç and J. P. Wolflin, editors. Coastal lagoons. Ecosystem processes and modelling
for sustainable use and development. CRC Press. USA.
Herrera-Silveira, J. A. and J. Ramírez-Ramírez. 1996. Effects of natural phenolic material
(tannins) on phytoplankton growth. Limnology and Oceanography 41: 1018-1023.
Horwitz, E., 1980. Official methods of analysis of the Association of Official Analytical
Chemists. Association of Official Analytical Chemists. USA, 1018 pp.
Imai, A., T. Fukushima and K. Matsushige. 1999. Effects of iron limitation and humic
substances on the growth of Mycrocystis aeruginosa. Canadian Journal of Fisheries and
Aquatic Sciences 56: 1929-1937.
Jackson, T. A. and R. E. Hecky. 1980. Depression of primary productivity by humic matter in
lake and reservoir waters of the boreal forest zone. Canadian Journal of Fisheries and
Aquatic Sciences 37: 2300-2317.
Kalesh, N. S., C. H. Sujatha and S. M. Nair. 2001. Dissolved folin phenol active substances
(tannin and lignin) in the seawater along the west coast of India. Journal of Oceanography
57: 29-36.
Klug, J. L., 2002. Positive and negative effects of allochthonous dissolved organic matter and
inorganic nutrients on phytoplankton growth. Canadian Journal of Fisheries and Aquatic
Sciences 59: 85-95.
Prakash, A. and M. A. Rashid. 1968. Influence of humic substances on the growth of marine
phytoplankton: Dinoflagellates. Limnology and Oceanography 13: 598-606.
Prakash, A., M. A. Rashid, A. Jensen and D. V. R. Subba. 1973. Influence of humic
substances on the growth of marine phytoplankton: Diatoms. Limnology and
Oceanography 18: 516-524.
117
Rivera-Monroy, V. H., C. J. Madden, J. W. Day Jr., R. R. Twilley, F. Vera-Herrera and H.
Alvarez-Guillén 1998. Seasonal coupling of a tropical mangrove forest and an estuarine
water column: enhancement of aquatic primary productivity. Hydrobiologia 379: 41-53.
Semina, H. J. 1978. Using the standard microscope, Treatment of an aliquot sample. Pages
181-189 in A. Sournia, editor. Phytoplankton manual. UNESCO, UK.
StatSoft,
Inc.
2004.
STATISTICA
(data
analysis
software
system),
ver.
7.0
www.statsoft.com.
Strickland, J. D. H. and T. R. Parsons. 1977. A practical handbook of seawater analysis.
Bulletin 167. Second Edition. Fisheries Research Board of Canada. Ottawa, 310 pp.
Tam, N. F. Y., L. L. P. Vrijmoed, and Y. S. Wong. 1990. Nutrient dynamics associated with
leaf decomposition in a small subtropical mangrove community in Hong Kong. Bulletin of
Marine Science 47: 68-78.
Toledo, A. P. P., J. G. Tundisi and V. A. D’Aquino. 1980. Humic acid influence on the
growth and copper tolerance of Chlorella sp. Hydrobiologia 71: 261-263.
Toledo, A. P. P., V. A. D’Aquino and J. G. Tundisi. 1982. Influence of humic acid on growth
and tolerance to cupric ions in Melosira (subsp. subartica). Hydrobiologia 87: 247-254.
Vollenweider, B. A. 1974. Manual on methods for measuring primary production in aquatic
environments. IBP-Handbook No. 12, Blackwell Oxford.
Wetzel, R. G. and G. E. Likens. 1994. Limnological analyses. Springer-Verlag. 391 pp.
Zar, J. H. 1999. Biostatistical analysis. Prentice-Hall, Inc. USA, 662 pp.
118
Figure legends
Figure 1. Location of Sontecomapan Lagoon with primary productivity experiment study sites.
Figure 2. Mean concentration of a) N-NH4+, b) N-NO3-, c) P-PO43- and d) FPAS released from
the decomposition of 1 g of leaf litter in 1 l of water over time. Dotted line represents the
treatment with leaf litter; continuous line represents the control without litter. Whiskers are 95%
confidence intervals.
Figure 3. Mean gross primary productivity for two sites on Sontecomapan Lagoon for three
different months in 2003. Treatments tested are given in Table 1. Whiskers are 95% confidence
intervals. Empty circles are controls without extract, squares are controls without extract but with
incubating medium, the rhombus are treatments with extract from day 2, triangles are treatments
with extract from day 10, and the filled circles are treatments with extract from day 45.
Figure 4. Mean cell density during phytoplankton growth: a) Chaetoceros muelleri var.
subsalsum, b) Cyclotella spp., and c) Skeletonema subsalsum subjected to different treatments
(see Table 1). Whiskers are 95% confidence intervals. Empty circles are controls without extract,
squares are controls without extract but with incubating medium, the rhombus are treatments with
extract from day 2, triangles are treatments with extract from day 10, and the filled circles are
treatments with extract from day 45.
119
Figure 1
120
Figure 2
121
Figure 3
Figure 4
122
123
Table 1. Characteristics of extracts obtained from decomposing mangrove leaf litter and used in
experiments on primary productivity and phytoplankton growth.
inoculums
N-NH4+ µM
N-NO3- µM
P-PO43- µM
FPAS mgL-1
1
No extract (control)
-
-
-
-
2
Incubating medium
Treatment
0
0.58
13.54
0
from day 0 (control)
3
Extract from day 2
171.52
2.43
8.32
7.30
4
Extract from day 10
104.88
1.59
11.52
8.49
5
Extract from day 45
110.70
1.27
5.8
12.50
Table 2. Species composition and cell density (cell ml-1) at the beginning of the experiments on
phytoplankton growth.
Species
May
August
October
Chaetoceros muelleri var. subsalsum
Thalassiosira cedarkeyensis
Scrippsiella sp.
Chaetoceros simplex
Cylindroteca closterium
Scenedesmus armatus
Chaetoceros subtilis var. abnomis f. simplex
Cyclotella spp.
Skeletonema pseudocostatum
Skeletonema subsalsum
Skeletonema costatum
Fragilaria ulna
174
166
6
863
2
0
0
0
0
0
0
16
0
0
0
964
2
19
2
2540
0
0
0
8
0
0
0
0
0
0
0
225
9938
3403
0
23
Total
1227
3534
13589
124
CAPÍTULO 6
Conclusión general
125
CONCLUSIÓN GENERAL
Es indudable el hecho de que la dinámica de las comunidades fitoplanctónicas en sistemas
lénticos, por tratarse de productores primarios, depende en gran parte a su relación con los
nutrientes disueltos en la columna de agua. Estas concentraciones pueden variar en función de
factores tales como: 1) los aportes de los ríos y escurrimientos de agua dulce, 2) las
características hidrológicas, 3) los ciclos biogeoquímicos internos propios del sistema
relacionados con la columna de agua, los sedimentos y otros productores primarios, y 4) el aporte
de la materia orgánica como la hojarasca de la zona circundante.
A través de los capítulos de este trabajo se obtuvo información de tales factores que
contribuye al entendimiento de la dinámica fitoplanctónica de la laguna de Sontecomapan
relacionada con la variación de nutrimentos y la hojarasca producida por Rhizophora mangle. A
continuación se resumen los resultados más importantes de esta investigación que permiten
integrar estos aspectos.
La producción de hojarasca de Rhizophora mangle en Sontecomapan fue uno de los valores
más altos registrados para la especie en sistemas de manglar de América. La variación de la
producción de hojarasca siguió un patrón estacional con los picos de producción más altos en la
época de secas y uno bajo en la época de lluvias. La velocidad de descomposición de hojarasca
estimada a través de las constantes de descomposición (k) fue diferente para las tres épocas
siendo más rápidas en la época de lluvias. En esta época, la velocidad de descomposición estuvo
relacionada con la presencia del molusco Neritina reclivata en alta densidad (Capítulo 2). De
acuerdo a estos resultados, no se rechaza la primera hipótesis planteada en este trabajo.
126
El contenido de nutrientes y taninos en la hojarasca producida también varió estacionalmente.
Sin embargo, la dinámica de su concentración durante la descomposición varió estacionalmente
solo para alguno de los nutrientes. El fósforo sufrió fases de acumulación y liberación en las tres
épocas. En la época de nortes y lluvias la hojarasca representó una fuente de este nutriente,
mientras que en la época de secas funcionó como una trampa. La dinámica del nitrógeno fue
similar en las tres épocas y éste fue acumulado durante todos los tiempos evaluados. La
proporción C:N:P al inicio de los experimentos de descomposición fue de 228:2:1, 595:5: y
358:3:1 en las épocas de nortes, secas y lluvias respectivamente. Estas proporciones fueron
menores a la proporción de Redfield de 106:16:1 (Atkinson y Smith, 1983) lo que explica en
parte la acumulación de N y P durante la descomposición. Por lo tanto, la hojarasca representó
una trampa para este nutriente. No obstante, se puede inferir una relación indirecta entre la
hojarasca como fuente de nitrógeno y el fitoplancton por medio de los detritívoros que reciclan
este nutriente a través de sus excretas y su interacción trófica con otros organismos (Harmon et
al., 1999. Gürel et al., 2005). Los taninos fueron liberados constantemente, por consiguiente la
hojarasca representó una fuente continua de estas sustancias (Capítulo 3). Estos resultados
conducen a rechazar parcialmente la segunda hipótesis de este trabajo, ya que la hojarasca no
representó una fuente de nitrógeno liberado directamente al medio.
Los valores de concentración de sustancias activas al folín fenol en la laguna fueron una
evidencia de la alta cantidad de materia orgánica de origen vegetal que entra a la laguna como lo
es la hojarasca de Rhizophora mangle. La variación estacional de las sustancias activas al folín
fenol coincidió con los picos de producción de hojarasca.
La estructura y dinámica de la comunidad fitoplanctónica de la laguna se caracterizó por
cambios en la composición y dominancia de especies que estuvieron asociadas con las diferentes
concentraciones de nutrientes y sustancias fenólicas. El análisis de la relación de las especies con
127
tales concentraciones permitió caracterizar los cambios de la comunidad fitoplanctónica
estacionalmente con especies con diferentes tolerancias a las sustancias activas al folin fenol. De
acuerdo a estos resultados, la tercera hipótesis se rechaza parcialmente, ya que solo la dinámica
de concentración de sustancias fenólicas fue similar al patrón de producción de hojarasca. Como
se presenta en el Capítulo 3, la dinámica de acumulación de nitrógeno y de fósforo durante la
descomposición de hojarasca sugiere que las concentraciones de amonio, nitratos y fosfatos en la
laguna no pueden ser resultado de la mineralización de la hojarasca de este mangle. Por lo tanto,
la fuente de nutrientes inorgánicos para el fitoplancton pueden ser otras fuentes alternas como
otros organismos en descomposición y los procesos de mineralización en la columna de agua y
en los sedimentos (Gürel et al., I. E. 2005).
Por otra parte, la dinámica registrada en la comunidad fitoplanctónica (dominancia de las
diatomeas del género Skeletonema en la época de nortes, los dinoflagelados Peridinium aff.
quinquecorne, Ceratium furca var. hircus, Prorocentrum cordatum, Scrippsiella sp., la diatomea
Thalassiosira cedarkeyensis en la época de secas, y las diatomeas Cyclotella spp, Chaetoceros
simplex y C. holsaticus en la época de lluvias) sugiere que la composición fitoplanctónica puede
estar modulada por la tolerancia a las sustancias fenólicas derivadas de la materia orgánica de
origen vegetal por lo que no se puede rechazar la tercera hipótesis totalmente.
Una consideración importante que resulta del Capítulo 4, es la necesidad de determinaciones
taxonómicas precisas que pueden tener implicaciones ecológicas. Tal es el caso de los
dinoflagelados Prorocentrum cordatum y Peridinium aff. quinquecorne que fueron abundantes
en Sontecomapan y que estuvieron asociadas con altas concentraciones de sustancias fenólicas.
Actualmente la identidad taxonómica de Prorocentrum cordatum está en debate debido a que se
ha planteado su conespecíficidad con Prorocentrum minimum (Pavill.) Schiller (Velicova y
Larsen, 1999, Krakhmalny et al. 2004). Su toxicidad potencial y la rápida ampliación en su
128
distribución en los mares del planeta han atraído la atención de la comunidad científica (Heil et
al. 2005). En el caso del dinoflagelado denominado Peridinium affine quinquecorne, sus
características morfológicas concordaron con las de la especie nomenclatural, sin embargo
presentó una variación importante que nos condujo a proponer una variedad nueva que se
presenta como Apéndice en esta tesis.
Los experimentos del efecto de los extractos obtenidos de la descomposición de hojarasca de
R. mangle en la productividad primaria y en el crecimiento del fitoplancton (Capítulo 5),
evidenciaron la tolerancia de las especies a las sustancias fenólicas que acompañan a los
nutrientes producidos por los procesos de descomposición. Esta tolerancia se observó en dos
diferentes escalas de tiempo: en las tasas de fijación de carbono (en corto tiempo) cuyo efecto
repercutió en el crecimiento celular (en largo tiempo). Los resultados de estos experimentos
apoyan las observaciones de las especies dominantes relacionadas con el gradiente de sustancias
activas al folín fenol presentadas en el Capítulo 4. Asimismo, el experimento correspondiente al
efecto en el crecimiento evidenció la potencialidad de especies de desarrollarse en diferentes
concentraciones de tales sustancias, como en el caso de Chaetoceros muelleri var. subsalsum. Por
lo tanto estos resultados no permiten rechazar la última hipótesis planteada en este trabajo.
En conclusión, la hojarasca derivada de Rhizophora mangle en Sontecomapan representa una
fuente de fósforo que a través de la descomposición es liberado al sistema. En cambio, representa
una trampa de nitrógeno que puede ser reconstituido al sistema a través de los organismos
detritívoros como Neritina reclivata. A partir de estas rutas y del proceso de mineralización, estos
nutrientes pueden ser potencialmente utilizadas por el fitoplancton. El alto contenido de taninos
en Rhizophora mangle es liberado a la laguna continuamente durante su descomposición, y la
relación encontrada con las diferentes especies fitoplanctónicas, su productividad primaria y su
129
crecimiento, sugieren que las concentraciones de las sustancias fenólicas en la laguna contribuyen
en la modulación de la dinámica del fitoplancton estacionalmente.
En la figura 1, se presenta un esquema que resume la relación existente entre la producción de
hojarasca de Rhizophora mangle y el fitoplancton en la laguna de Sontecomapan inferida a través
de los procesos de descomposición, la dinámica de nutrientes de la laguna y su relación con la
composición fitoplanctónica, y la productividad primaria estudiados en este trabajo.
LITERATURA CITADA
Atkinson, M. J. y S. V. Smith. 1983. C:N:P ratios of benthic marine plants. Limnology and
Oceanography 28: 568-574.
Gürel, M., A.Tanik, R. C. Russo y I. E. Gönenç. 2005. Biogeochemical cycles. In: I. E.Gönenç y
J. P. Wolflin, editores. Coastal lagoons. Ecosystem processes and modelling for sustainable
Harmon, M. E., K. J. Nadelhoffer y J. M. Balir. 1999. Measuring decomposition, nutrient
turnover, and stores in plant litter. Páginas 202-240 in G. P. Robertson,.D. C. Coleman, C. S.
Bledsoe y P. Sollins, editors. Standard Soil Methods for Long-term Ecological Research.
Oxford University Press, Inc. USA.
Heil, C. A., P. M. Glibert y C. Fan. 2005. Prorocentrum minimum (Pavillard) Schiller a review of
a harmful algal species of growing worldwide importance. Harmful Algae 4: 449-470.
Krakhmalny, A. F., Tishaeva, M. V., Panina, Z. A. & Krakhmalny, M. A. 2004. A problem on
identity Prorocentrum cordatum (Ostf.) Dodge and P. minimum (Pavill.) Schiller (Dinophyta).
Internacional Journal on Algae 6: 331-340.
Velikova, V. y J. Larsen. 1999. The Prorocentrum cordatum/Prorocentrum minimum taxonomic
problem. Grana 38: 108-112.
130
Pies de figura
Figura 1. Contribución y efecto de la hojarasca derivada de Rhizophora mangle en la
productividad primaria y composición del fitoplancton en la Laguna de Sontecomapan. La figura
muestra la entrada de nutrientes por los ríos y la hojarasca, los ciclos biogeoquímicos del P y N,
los procesos de acumulación y liberación de nutrientes y taninos por la descomposición de
hojarasca y su relación con los detritívoros, y la dinámica fitoplanctónica caracterizada por las
especies dominantes en cada época climática. Las líneas verticales separan las épocas climáticas:
nortes, secas y lluvias. En la parte de abajo se presentan las constantes de descomposición (k) de
la hojarasca en cada época. Se presentan las especies fitoplanctónicas dominantes a) Skeletonema
subsalsum, b) S. pseudocostatum, c) S. costatum, d) Chaetoceros subtilis var. abnormis f.
simplex, e) Peridinium aff. quinquecorne, f) Ceratium furca var. hircus, g) Thalassiosira
cedarkeyensis, h) Prorocentrum cordatum, i) Scrippsiella sp., j) Cyclotella meneghiniana, k) C.
cryptica, l) C. striata, m) Chaetoceros holsaticus, n) C. simplex, la diatomea o) Chaetoceros
muelleri var. subsalsum, que puede crecer potencialmente y el molusco p) Neritina reclivata
asociado a la descomposición de hojarasca. C = carbono, P = fósforo, N = nitrógeno, SAFF =
sustancias activas al folín fenol. Las letras en negritas representan mayor concentración de estos
nutrientes. Las flechas con O2 en el interior representan la productividad primaria y su tamaño la
intensidad del proceso.
131
Figura 1
132
APÉNDICE
Peridinium quinquecorne var. trispinifera var. nov. (Dinophyceae) from a brackishwater
environment
En preparación para enviar a Botanica Marina
133
Peridinium quinquecorne var. trispinifera var. nov. (Dinophyceae) from a brackishwater
environment
J. A. AKÉ-CASTILLO∗ and G. VÁZQUEZ
Instituto de Ecología, A. C. Departamento de Ecología Funcional. Carretera antigua a Coatepec
Km. 2.5 No. 351, C.P. 91070. Congregación El Haya, Xalapa, Veracruz, México.
Fax: +52 (228) 8421800 ext. 4222.
Suggested running title: Peridinium quinquecorne var. trispinifera var. nov.
Key words: coastal lagoon, dinoflagellate, Gulf of Mexico, microalgae bloom.
Abstract
Peridinium quinquecorne is a marine dinoflagellate characterized by the possession of four thick
spines at hypotheca. In Sontecomapan Lagoon, Mexico, a dinoflagellate whose characteristics of
shape, number and arrangement of plates fitted to those of P. quinquecorne, was recorded for
some months in phytoplankton samples which represented a one year period of study in this
lagoon connected to the Gulf of Mexico. However, the number of the spines at hypotheca of this
dinoflagellate differed from P. quinquecorne, being three in specimens found in this lagoon. The
presence of three spines was a consistent character found in the populations of this dinoflagellate,
and high densities of cells were related to salinities lower than 21 ‰ and temperatures higher
than 24.5 °C. Based on observations from light and electron microscopes, we proposed the new
∗
Corresponding author ([email protected]; [email protected])
134
variety Peridinium quinquecorne var. trispinifera for this taxon which caused a bloom in this
tropical brackishwater system.
INTRODUCTION
Peridinium quinquecorne Abé is a marine thecate dinoflagellate characterized by the possession
of four thick spines at hypotheca (Abé 1927; Horiguchi & Pienaar 1991). Its thecal plate
arrangement is pp, x, 3’, 2a, 7´´, 5c, 5’’’, 2’’’’ 4s, with the distinction of the second intercalary
plate being large. Diamond to ovoidal shape have been pointed out as variation in cell form by
Horiguchi & Pienaar (1991), and variation of the length between the sulcus and the antapex exists
in this species depending on the degree of development of intercalary bands. Number and pattern
of plates, left-handed cingulum slightly displaced and possession of the four antapical spines are
consistent characteristics in this species (Madariaga et al. 1989; Horiguchi & Pienaar 1991;
Trigueros et al. 2000).
Ecologically, Peridinium quinquecorne have shown to be a significant component of estuarine
phytoplankton causing blooms at Philippines (Horstmann 1980), North Spain (Madariaga et al.
1989; Trigueros et al. 2000) and regional seas of China (Shen et al. 2001). In the Gernika estuary
(Northern Spain) this species has been responsible for the most of the primary production during
summer period, and in the same region (Urdaibai estuary) cell densities reached 450 cells ml-1
with best growth at temperatures higher than 20 °C and salinities of 29 ‰ (Madariaga et al. 1989;
Trigueros et al. 2000).
In some samples collected during a period of one year (2002-2003) in Sontecomapan Lagoon,
a tropical coastal lagoon located at the south of Gulf of Mexico, the presence of a dinoflagellate
in high densities was noticed. Cell form and number and arrangement of thecal plates fitted with
135
that of Peridinium quinquecorne, as well as the possession of spines at hypotheca but not its
number. This last difference was consistent in the populations from Sontecomapan Lagoon, and
as a consequence, we provide the description of a new variety with some ecological remarks.
MATERIAL AND METHODS
Net and bottle samples were collected bimonthly from October 2002 to October 2003 in
Sontecomapan Lagoon (18º 30’ and 18º 34’ N and 94º 59’ and 95º 04’ W), a tropical coastal
lagoon permanently connected to the sea. Characteristics of this lagoon are provided by AkéCastillo et al. (2004). Bottle samples were collected at two depths: surface and close to the
bottom (mean depth of the lagoon is 1.5 m).
Net samples were fixed with formalin to a final concentration of 4 %. Bottle samples were
fixed with Lugol-acetate solution. Water mounts were studied using a light microscope Nikon
Eclipse 80i and cell countings were made following Utermöhl method with an inverted
microscope Leica DMIL (Hasle 1978). Following Lebour (1925), water mounts with the
dinoflagellate were stained with trypan blue to make evident the plate pattern. Samples with the
dinoflagellate were prepared for the critical point drying (Lewis et al. 2001) and were observed in
a scanning electron microscope JEOL-5600. Measurements of length and width of 30 cells were
made using a micrometric ocular at 1000x. Drawings were made using a camera lucida and
pictures were taken using a digital camera Nikon COOLPI4300. Terminology of plate tabulation
followed the same used by Horiguchi & Pienaar (1991).
RESULTS
136
Diagnosis
Peridinium quinquecorne var. trispinifera Aké-Castillo var. nov.
Cellula solitaria, 17.5-42.5 µm longum, 15-35 µm latum. Tres spinas conspicuae in hypotheca.
Chromatophoris parvi rotundi virides sufflavi numerosi. Formula laminarum pp, x, 3’, 2a, 7’’,
5c, 5’’’, 2’’’’.
Cells Solitary, 17.5-42.5 µm long, 15-35 µm wide. Three conspicuous spines at hypotheca, which
distinguish it from the type variety. Numerous small yellow-greenish chloroplasts. Plate formula
pp, x, 3’, 2a, 7’’, 5c, 5’’’, 2’’’’.
Holotype: Figs1-4.
Type locality: Sontecomapan Lagoon, Veracruz, Mexico (18º 30’ and 18º 34’ N and 94º 59’ and
95º 04’ W).
Date: 19 February 2003
Collector: Aké-Castillo J. A.
Etymology: The variety name refers to the three thick spines at hypotheca.
Habitat: Planktonic, brackishwater environment.
Observations
The general shape of the cell body is ovoid divided close to the middle by the cingulum (Fig. 5).
The epitheca is conical with an evident apical pore (Figs 5, 6) whereas the hypotheca is rounded
137
with three long spines (Figs 7, 8). Short spines can occur at precingular plates as well as
postcingular plates (Fig. 8). The 1a plate is pentagonal located among plates 1’’, 2’’, 3’’, 2’ and
2a (Fig. 9). The 2a plate is large with seven sides of unequal size and the vertices of the sides
opposite to the apical pore may not evident resulting in a curved appearance (Fig. 10). Intercalary
bands can be well developed. Precingular plates are unequal in form and size (Fig. 10). The
cingulum is formed by five plates and is slightly displaced to the epitheca. The sulcus does not
penetrate into the epitheca and does not reach the antapex (Fig. 11). The three spines of the
hypotheca are prominent. One spine arises from one edge of plate 1’’’’ and two from opposite
edges of plate 2’’’’ (Figs 11, 12). Chloroplasts are discoid and numerous and are greenyellowish.
Ecological remarks
In all the period studied, Peridinium quinquecorne var. trispinifera was detected only in samples
from February and June. It reached the highest densities during February while in June was low
and occurred in few samples. Densities ranged from 12 to 4515 cells ml-1 in February, and from 4
to 282 cells ml-1 in June (Table 1). The maximum cell density (4515 cells ml-1) was recorded at
salinity of 10 ‰ and temperature of 28.4 °C.
DISCUSSION
Phytoplankton communities of coastal lagoons are complex as a high diversity of organisms
coming from freshwater and marine environment can co-occur spatial and temporally. As a
consequence, confusion on identification of microalgae may arise. Within the dinoflagellates,
138
some genera are well separated in freshwater or marine organisms, and other can be found in both
environments (Dodge 1985; Popovský & Pfiester 1990). The genus Peridinium Ehrenberg was
split by Gran in 1902 into the genera Peridinium and Protoperidinium Bergh, out coming from
this division a general separation of the freshwater species (Peridinium) from those found in
marine environments (Protoperidinium) (Dodge 1985). Thus, the genus Peridinium is commonly
thought to occur only in freshwater environments, but division in two genera is based in the
number of cingular plates (Peridinium having more than 5 plates) and few species of this genus
have been shown to occur in marine-brackishwater environments, i. e. Peridinium quinquecorne,
P. foliaceum (Stein) Biecheler, and P. aciculiferum Lemmermann (Popovský & Pfiester 1990;
Horiguchi & Pienaar 1991).
In 1927 Abé described P. quinquecorne based in two individuals found in marine plankton
from Mutsu Bay, Japan, and since then, the range extension of distribution of this species has
incremented including Maribago Bay, Philippinnes (Horstmann 1980), Northern Spain
(Madariaga et al. 1989), South Africa (Horiguchi & Pienaar 1991), Mexican Pacific (CortésAltamirano 2002), Gulf of Mexico (Barón-Campis et al. 2005) and Douglas Clay, Belize (Faust
et al. 2005). According to these records, P. quinquecorne is distributed in temperate to tropical
marine waters.
Morphological characters such as shape of the cell, number and arrangement of plates, and
possession of spines at antapical plates of the dinoflagellate found in Sontecomapan lagoon, fitted
perfectly with that of P. quinquecorne. However, the number of spines of our specimens differed
from the characteristically four on P. quinquecorne. The presence of three spines in our
specimens was a consistent character found in populations from the two different months they
were detected. In addition, position of these spines was always the same: one at 1’’’’ plate and
two on opposite edges of 2’’’’ plate. This morphological character, together with some aspects of
139
its ecology, led us to consider we were dealing with a different taxon from the typical P.
quinquecorne, so we proposed the new variety trispinifera. Temperatures higher than 24.5 °C and
salinities lower than 21 ‰ were related to high densities of cells, so Peridinium quinquecorne
var. trispinifera can be characterized as a mesohaline species with affinity to warm waters.
Sontecomapan Lagoon, where P. quinquecorne var. trispinifera was collected is a tropical
brackishwater system where salinity varies temporally and spatially and phytoplankton
community is dominated by diatoms with affinities to freshwater, brackiswater and marine water
(Aké-Castillo et al. 1995; Meave & Lara-Villa 1996; Aké-Castillo et al. 2004). However, from
March to May, the dry season in this region, the dinoflagellate Ceratium furca var. hircus
(Schröder) Margalef may be dominant (Guerra-Martínez & Lara-Villa 1996). During February
2003, the occurrence of P. quinquecorne var. trispinifera in high densities, represented the
beginning of the dinoflagellate bloom expected to occur during the dry season, which for this
year of study was dominated, besides of C. furca var. hircus, by a marine species of the genus
Prorocentrum (unpublished data). Densities of P. quinquecorne var. trispinifera in June were low
and not accounted for important proportion for the phytoplankton composition in this month.
Most of the densities recorded of Peridinium quinquecorne var. trispinifera were similar to that
of maxima for P. quinquecorne in other regions: 400 to 450 cells ml-1 for Northern Spain
(Madariaga et al. 1989; Trigueros et al. 2000), 1200 cells ml-1 for China Region (Shen et al.
2001), and 2500 cells ml-1 for Veracruz Seaport at Gulf of Mexico (Barón-Campis et al. 2005).
However, for one bottom sample in February Peridinium quinquecorne var. trispinifera reached
4515 cells ml-1, which represented a high biomass as this organism is bigger than 20 µm. To our
knowledge P. quinquecorne has not been reported as a toxic microalga elsewhere, but can be
consider as a harmful alga because it may cause fish kills due to depletion of dissolved oxygen
(Shamsudin et al. 1996).
140
The finding of this new taxon in a tropical brackish water system stresses two important facts.
First, it makes evident the necessity of studies on phytoplankton in tropical zones which are
known to harbor a high biodiversity. Variation in morphology of microalgae could hide different
taxa, as suggested for the dinoflagellate Ceratium divaricatum (Lemmermann) Kofoid which was
believed to have a wide distribution and was split in two taxa with different distribution: one
variety with temperate-subtropical distribution and other variety with tropical distribution
(Hernández-Becerril & Alonso-Rodríguez 2004). Second, the study of dynamics of individual
species in complex systems as coastal lagoons or estuaries through a seasonal cycle could lead to
the characterization of brackishwater species which could set up stable populations and may be
important contributors to primary production. In addition, the knowledge of the phytoplankton
population dynamic could lead to the implementation of monitoring programs focusing on
microalgae that can cause harmful blooms.
ACKNOWLEDGEMENTS
Instituto de Ecologia, A. C. provided financial support (projects 902-17 and 902-11-280). The
new taxon resulted from the samples collected for the J. A. Aké-Castillo´s Ph. D. thesis who
acknowledges to CONACYT for scholarship (90031) granted during his doctoral studies. Yuri
Okolodkov made important suggestions to the manuscript and provided basic literature. We
thank Tiburcio Láez for his skilled assistance at Scannig Electron Microscope Unit at INECOL,
A. C., Xalapa.
REFERENCES
141
ABÉ T. H. 1927. Report of the biological survey of Mutsu Bay. 3. Notes on the Protozoan Fauna
of Mutsu Bay. I. Peridiniales. Science Reports of the Tohoku Imperial University. Ser. 4, 2: 383438.
AKÉ-CASTILLO J. A., MEAVE M. E. & HERNÁNDEZ-BECERRIL D. U. 1995. Morphology and
distribution of species of the diatom genus Skeletonema in a tropical coastal lagoon. European
Journal of Phycology 30: 107-115.
AKÉ-CASTILLO J. A., GUERRA-MARTÍNEZ S. L. & ZAMUDIO-RESÉNDIZ M. E. 2004. Observation
on some species of Chaetoceros (Bacillariophyceae) with reduced number of setae from a
tropical coastal lagoon. Hydrobiologia 524: 203-213.
BARÓN-CAMPIS, S. A., HERNÁNDEZ-BECERRIL, D. U., JUÁREZ-RUÍZ, N. O. & RAMÍREZCAMARENA, C. 2005. Red tide produced by the dinoflagellate Peridinium quinquecorne in
Veracruz, Mexico (oct-nov. 2002): morphology of the causative agent. Hidrobiológica, 15: 7378.
CORTÉS-ALTAMIRANO, R. 2002. Mareas Rojas: Biodiversidad de microbios que pintan el mar. In:
Atlas de la Biodiversidad de Sinaloa, (Edited by J. L. Cifuentes-Lemus & J. Gaxiola-López) pp
29-41, México.
DODGE J. D. 1985. Marine dinoflagellates of the British Isles. HSMO. London 303 pp.
142
FAUST M.A., LITAKER R. W., VANDERSEA M. W., KIBLER S. R. & TESTER A. P. 2005.
Dinoflagellate diversity and abundance in two Belizean coral-reef mangrove lagoons: a test of
Margalef´s mandala. Atoll Research Bulletin 534: 103-131
GUERRA-MARTÍNEZ S. L. & LARA-VILLA M. A. 1996. “Florecimiento” de Ceratium furca
(Peridiniales: Ceratiaceae) en un ambiente salobre: Laguna de Sontecomapan, México. Revista de
Biologia Tropical 44: 23-30.
HASLE G. R. 1978. The inverted-microscope method. In: Phytoplankton manual (Ed. by A.
Sournia), pp 88-96. UNESCO, Paris.
HERNÁNDEZ-BECERRIL D.U. & ALONSO-RODRÍGUEZ R. 2004. Study of the marine planktonic
dinoflagellate Ceratium divaricatum (Dinophyceae), a confused and considerable variable
species. Phycological Research 52: 346-354.
HORIGUCHI T. & PIENAAR R. N. 1991. Ultrastructure of a marine dinoflagellate, Peridinium
quinquecorne Abé (Peridiniales) from South Africa with particular reference to its chrysophyte
endosymbiont. Botanica Marina 34: 123-131.
HORSTMANN U. 1980. Observations on the peculiar diurnal migration of a red tide dinophyceae in
tropical shallow waters. Journal of Phycology 16: 481-485.
LEBOUR, M.V. 1925. The Dinoflagellates of Northern Seas. Marine Biol. Assoc. U.K., Plymouth.
250 pp.
143
LEWIS J., ROCHON A., ELLEGAARD M., MUDIE P. J. & HARDING I. 2001. The cyst-theca
relationship of Bitectatodinium tepikiense (Dinophyceae). European Journal of Phycology 36:
137-146.
MADARIAGA I., ORIVE E. & BOALCH G. T. 1989. Primary production in the Gernika Estuary
during a summer bloom of the dinoflagellate Peridinium quinquecorne Abé. Botanica Marina
32: 152-165.
MEAVE M. E. & LARA-VILLA M. A. 1996. Diatomeas planctónicas de la laguna de
Sontecomapan. In: Historia Natural de los Tuxtlas. Los Tuxtlas (Ed. by E. González, R. Dirzo &
R. Vogt), pp. 209-212. UNAM, CONABIO. México.
POPOVSKÝ J. & PFIESTER L. A. 1990. Süswasserflora von Mitteleuropa, Band 6: Dinophyceae
(Dinoflagellida). Gustav Fischer Verlag Jena Stuttgart, 271 pp.
SHAMSUDIN L., AWANG A., AMBAK A.& IBRAHIM S. 1996. Dinoflagellate bloom in tropical fish
ponds of coastal waters of the South China Sea. Environmental Monitoring and Assessment
(Historical Archive) 40: 303-311.
SHEN C., LIEW S. C., KWOH L. K. 2001. Seawifs observation of chlorophyll distribution in
regional seas. Paper presented at the 22nd Asian Conference on Remote Sensing, 5-9 November
2001, Singapore. Centre for Remote Imaging, Sensing and Processing (CRISP), National
University of Singapore: Singapore Institute of Surveyors and Valuers (SISV): Asian Association
on Remote Sensing (AARS).
144
TRIGUEROS J. M., ANSOTEGUI A. & ORIVE E. 2000. Remarks on morphology and ecology of
recurrent dinoflagellate species in the Estuary of Urdaibai (Northern Spain). Botanica Marina 43:
93-103.
145
Figures legends.
Figures 1-4. Plate tabulation of Peridinium quinquecorne var. trispinifera. Fig. 1. Ventral view.
Fig. 2. Dorsal view. Fig. 3. Epitheca. Fig. 4. Hypotheca. Scale bar = 20 µm.
Figures 5-8. Peridinium quinquecorne var. trispinifera LM. Fig. 5. Ventral view. Fig. 6. Plate
pattern of epitheca. Note 1a, large 2a plates and the pore plate (arrow). Fig. 7. View of hypotheca
showing three thick spines (arrows) Fig. 8. View of hypotheca with additional small spines at
postcingular plates (arrows). Scale bars = 10 µm.
Figures 9-12. Peridinium quinquecorne var. trispinifera SEM. Fig. 9. Ventral view. Note 1a
plate (arrow). Fig. 10. Dorsal view showing 1a plate (arrow) and the large 2a. fig. 11. Position of
spines at hypotheca: one spine at 1’’’’ plate and two at 2’’’’. Fig. 12. Detail of spines. Note
position of spines at edges of plates. Scale bars = 5 µm (Figs 9-11) or 2 µm (Fig. 12).
146
147
148
149
Table 1. Descriptive statistics of cell density, salinity and temperature of samples where
Peridinium quinquecorne var. trispinifera occurred.
February (n = 12)
June (n = 7)
Mean Min. Max. Std. error
Mean
Min. Max. Std. error
Cells ml-1
634.5 12
4515 361.62
44.3
0.1
282
39.72
Salinity ‰
11.16 5
21
1.55
19.14
10
32
2.92
Temperature ºC
26.03 24.5
28.4
0.30
30.95
29.1
32.3
0.37
150

contribución y efecto de la hojarasca derivada de mangle en la

Transcription

Similar documents

freaky friday nights!

Spring Island Litter Sweep

Layout Property #14472

Lagoon 400 S2 (3 cab)

Create a Warm Welcome for a New Cat or Kitten

October 2013 Newsletter

Anaerobic lagoons - rowenvironmental

LitterBoss - Industry Surplus Australia

Getting a grip on litter: a charity`s perspective

CATAMARAN SUMMER BLUES BLUE LAGOON, TROGIR AND