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File - UC Berkeley Urban Bee Lab
Relationships of Bees to Host Ornamental and Weedy Flowers
in Urban Northwest Guanacaste Province, Costa Rica
Author(s): G. W. Frankie , S. B. Vinson , M. A. Rizzardi , T. L. Griswold , R. E.
Coville , M. H. Grayum , L. E. S. Martinez , J. Foltz-Sweat , and J. C. Pawelek
Source: Journal of the Kansas Entomological Society, 86(4):325-351. 2013.
Published By: Kansas Entomological Society
DOI: http://dx.doi.org/10.2317/JKES121222.1
URL: http://www.bioone.org/doi/full/10.2317/JKES121222.1
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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
86(4), 2013, pp. 325–351
Relationships of Bees to Host Ornamental and Weedy Flowers in
Urban Northwest Guanacaste Province, Costa Rica
G. W. FRANKIE,1 S. B. VINSON,2 M. A. RIZZARDI,3 T. L. GRISWOLD,4 R. E. COVILLE,5
M. H. GRAYUM,6 L. E. S. MARTINEZ,7 J. FOLTZ-SWEAT,1 AND J. C. PAWELEK1
ABSTRACT: Ecological studies on native bees in urban tropical environments are rare,
however, ever-increasing urban areas world-wide necessitate study on how many of these bees
can and have adjusted to human constructs. Predictable ecological patterns that emerge from
these studies can provide guidance on how future urban constructs can be designed to provide
habitat for conserving and protecting native bees. These patterns can also be used for bee
habitat restoration in natural and agricultural environments. An extensive survey of native
bees and honey bees and their relationships to a community of 102 plant types in urban
residential environments of Bagaces and Liberia in northwestern Costa Rica was conducted
from 2003–2012. Bees were attracted and recorded at measurable frequencies to 82 plant
genera in 41 families, the most common of which was Fabaceae. Forty-two plant types were
native ornamentals; 39 were non-natives; and 21 were native weed species. Standardized bee
visitation (frequency) counts, 17,000+, were used to record relationships between bees and
flowers. The following data were recorded for each plant type: flowering phenology in months,
type of floral reward(s) (pollen, nectar, and/or oil), main daily attraction period, and most
frequently visiting bee taxa. Plant life forms included trees, shrubs, lianas/vines, herbs, and
palms. Each plant group had a different seasonal flowering phenology with native ornamentals
and native weeds having patterns that closely resembled the general patterns for wild plants in
the dry forest. Predictable associations of certain bee taxa with each plant type emerged from
the count data, which allowed for categorizing relationships into four types: small bee, diverse
bee, specialized bee, and nocturnal pollination systems. Intraspecific variations in bee
attraction to several plant types were also noted. Honey bees (Africanized) did not figure
prominently in most pollination relationships, especially with regard to native plants. Most
native bee species were generalized foragers. Beyond the urban environment, it is suggested
that knowledge of predictable bee-flower relationships can also be used to restore bee habitat
in disturbed environments such as deforested areas. With some imagination and outreach
education, bee habitats could also be installed for some agricultural crops. Outreaching
information on native bee-flower relationships at local, regional, and state levels is important
for short and long-term propagation of urban (and agricultural) plants. Yet, very few outlets
for transferring this knowledge currently exist in Costa Rica. A few limited options for sharing
this information are discussed, including collaborative partnerships with local NGOs.
KEY WORDS: Bee-flower relations, community pollination, Costa Rican ecology, ecological
restoration, native bee ecology, pollen/nectar resources, pollination ecology, tropical flower
phenology, urban ecology
Urban environments world-wide are well known to provide habitat for a variety
of animals (Tallamy, 2009). An increasing number of habitat relationships are
currently being investigated by several research groups in the Old and New
1
2
3
4
5
6
7
University of California Berkeley, California 94720
Texas A & M University College Station, Texas 77843
Humboldt State University, Arcata, California 95521
USDA-ARS Bee Biology and Systematics Lab, Logan, Utah 84322
Professional bee biologist, photographer, El Cerrito, California 94804
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166
Bagaces, Guanacaste, Province, Costa Rica
Accepted 25 May 2013; Revised 16 July 2013
E 2013 Kansas Entomological Society
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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
World, with a focus on their biodiversity, ecosystem services, and conservation
values. Many of these investigations are reported in a large, newly edited volume,
Urban Biodiversity and Design by Müller et al. (2010). Plant-pollinator relationships, and especially bees and flowers, are also receiving attention as
biologists, conservationists, civic leaders, politicians, and the general public are
becoming aware of the important roles they play now and in the future of our
lives (Buchmann and Nabhan, 1996; Allen-Wardell et al., 1998; Kearns et al.,
1998; Cane and Tepedino, 2001; NAS 2007). Developing human populations in
cities around the world (2/3 of world’s population will be in cities by 2050) bring
an urgency to know more about the new novel relationships that are being
created, many of which are dynamic owing to anthropogenic activities and
impacts. As urban areas increase, impacts on surrounding areas are inevitable,
and these will also require study so they may be addressed within larger
community and landscape frameworks.
The encroachment of urban areas into rural environments often creates
interconnected habitats that are important as refuges for native species (Goddard
et al., 2009). Urban habitats are comprised of a mosaic of gardens, parks,
buildings (Cane, 2005; Colla et al., 2009; Werner and Zahner, 2010), built spaces,
and semi natural remnant land. The mosaic can be used for nesting,
overwintering, and forage for bees that have flight ability to move between
widely spaced patches within the larger matrix (Bates et al., 2011). Cane (2005)
and Hernandez et al., (2009) provide reviews of bee diversity studies in urban
areas, most of which are in temperate regions. The reviews indicate that urban
areas can harbor a subset of bee fauna found in surrounding natural habitat
(Fetridge et al., 2008; Matteson et al., 2008). A recent study by Bates et al. (2011)
states that as urbanization rates are predicted to increase it is important to study
bees in urban habitats because they have intrinsic conservation value, they
contribute to ecosystem services, and we can use the information to predict bee
responses to future urbanization. With the exception of a few studies in Brazil
(Alvos-Dos-Santos, 2003; Zanette et al., 2005; Viana et al., 2006; Nemésio and
Silveira, 2007) and Columbia (Nates-Parra et al., 2006), research surveys on the
ecology of tropical urban bees are rare.
Griswold et al. (2000) have documented more than 800 species of bees in Costa
Rica, demonstrating that relatively small diverse landscapes such as Costa Rica can
support highly diverse populations of native bees. Despite this impressive number of
bee species, recent and rapid developments of human activity throughout the
country have negatively impacted bee populations. This is especially noticeable in
lowland areas such as the northwestern Guanacaste region where ‘‘dry forests’’ and
other vegetation types have been disappearing at alarming rates since the late 1960’s
(Janzen, 1974, pers. comm.; Frankie et al., 2009a).
The current study is part of a series of papers documenting native bee diversity/
abundance and bee-flower relationships over a period of 40 yrs (1972–2012) in a
lowland dry forest in northwestern Costa Rica. The work began in 1972 along the
Pan American Highway just outside the city limits of Liberia, Guanacaste Province
in an area surrounded by mostly forested wildlands. Goal of the first study was to
investigate inter-tree movement patterns of marked native bees among individuals of
the obligate out-crossing leguminous tree, Andira inermis (Bawa, 1974). Results of
that study demonstrated that large numbers of diverse bee species were visiting A.
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327
inermis, and the few individual bees that moved between trees were enough to
account for the observed fruit set (Frankie et al., 1976).
Subsequent studies of bee populations on A. inermis at the same Liberia site
documented significant decline in bee diversity and abundance through time
(Frankie et al., 1997, 2005a, and 2009a), associated with progressive changes in land
use around Liberia. These changes included extensive forest clearing for agriculture;
frequent and extensive wildfires (not natural to this forest environment);
introduction of an invasive fire-prone grass species, Hyparrhenia rufa (locally called
jaragua) from Africa for cattle forage; and natural revegetation by native plants of
some cleared areas that required several years to produce diverse and abundant
pollen and nectar resources for native bees.
A final land-use change has been the slow expansion of urban areas into
wildlands, especially around the A. inermis- Liberia site. In our last monitoring study
(2004) on A. inermis at this site, we called attention to diverse native bee species in
nearby urban Liberia (Frankie et al., 2009a). We suggested that there was sufficient
bee habitat (i.e., with floral and nesting resources) in urban Liberia to support
relatively diverse bee populations, but much more sparsely compared to numbers
recorded in the 1972 study. We also made the same observation in nearby, but
smaller, urban Bagaces.
Here we report on 10 yrs of survey research (2003–2012) on flowering plant
resources in urban Liberia and Bagaces that are supporting native bee species and
honey bees, mostly Apis mellifera scutellata (Schneider, 1995). The specific goals
were to: a) evaluate bee preferences among native and non-native plant species found
in urban gardens; b) in a community context, record differences in monthly
flowering periods (phenology) and daily times of floral-resource presentation of bee
plants; c) assess predictability of plant species to attract selected taxonomic groups of
bee species/genera; d) conduct preliminary comparisons of bee species diversity
visiting selected conspecific plants in urban and nearby wildlands.
Site Descriptions
LIBERIA: Liberia is the fastest growing city of its size in Costa Rica (Frankie et al.,
2009a). It is the capital city of Guanacaste Province and an important modern hub of
human occupation and activity in the northwestern region of the country (Fig. 1).
From 1972 to 2006 the population grew from 16,260 to ,47,000 people. Currently, it
is believed to exceed 50,000 inhabitants. A wide variety of ornamental plants are
commonly used in city gardens; many are perennials native to the Guanacaste region
(Appendix I). Diverse native weed species are common and are part of the plant
community of urban Liberia. Agriculture and tourism are the most important
economic activities in and around the city. The newly expanded airport at Liberia
receives more than 30 international flights daily, adding significantly to the tourism
industry. Liberia serves as a gateway to many Pacific Coast beach resorts, Volcán
Rincón de la Vieja National Park, and Santa Rosa National Park.
BAGACES: Bagaces is located 25 km SE of Liberia along the Pan American Highway.
It is a small town of some 5,000+ inhabitants and is one of the oldest in the Guanacaste
region with a history of some 300+ yrs. In contrast to Liberia its population growth is
relatively slow. Despite its size, the town serves as a municipal center for several nearby
small pueblos. Like Liberia, a wide variety of ornamental plants are used in home
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Fig. 1. The main study area in Costa Rica is shown in the left map. Studies were conducted in two major
urban areas (Liberia and Bagaces) and in wildland areas (D 5 Hacienda Monteverde, E 5 Hac. Ciruelas,
and F 5 Hac. Tamarindo). A few studies were conducted in Reserva Biologica Barbudal (*). Other
reference features: Pueblos: A - Salto, B - Pijie, C - Guayabo. Rivers: 1 5 Rio Colorado, 2 5 R. Liberia,
3 5 R. Salto, 4 5 R. Potrero, 5 5 R. Piedras.
gardens; many are native perennials (Appendix I). Diverse native weed species are also
common in Bagaces. Bagaces is largely an agricultural community with developing
modern features. It also serves as a gateway to Palo Verde National Park, Lomas
Barbudal Biological Reserve, and Volcán Miravalles National Park.
NATURAL WILDLANDS: To assess bee visitation at target native plant species
(conspecifics with urban plants) in wildland environments, bee diversity/abundance
was recorded on these species along rural roads within the vicinities of Hacienda
Monteverde, Hacienda Ciruelas, and Hacienda Tamarindo (Fig. 1). Target plants in
these locations were mostly along forest edges. All three Haciendas are private
properties (Costa Rican topographic map series).
Methods and Materials
We occasionally called upon earlier work to form a context for evaluating current
results. For example, we have studied bee foraging behavior for pollen and nectar
from native Guanacaste plants (Frankie and Haber, 1983; Frankie et al., 1976, 1982,
1983, 2005a). At that time we also observed many of the same bee species visiting
flowers in nearby urban areas. In 2003 we began surveying bees in urban Liberia and
Bagaces to characterize bee-flower relationships on both native and non-native
ornamental plant species. The work continues and involves conducting numerous
standardized visitation (frequency) counts of bees.
We selected plant types for study by conducting extensive and regular walks
through city residential blocks of Bagaces (60) and Liberia (,90), especially during
2003–2004. Plant types that attracted bees were recorded from urban gardens that
could be accessed from sidewalks or in some cases streets. Notes were made on
locations of most plants so they could be followed over several years. Once plants
VOLUME 86, ISSUE 4
329
were selected, a year-long schedule of dates was made to gather data. Sometimes
observations were conducted weekly; more often monthly. There was not a set
number of replications of each plant type as there were variable numbers of each
type.
The visitation or frequency recording method, also employed successfully in
California (Frankie et al., 2005b, 2009b), consisted of randomly selecting ,1.5 m2
patches of flowers on a vigorously flowering plant of a targeted plant type, and
counting bee taxa that enter the space during 3 minute periods. Once a bee entered
the space, and touched the reproductive parts of a flower, it was counted once
regardless of the number of subsequent flowers it visited. This was done to be able to
observe subsequent visits by other bees to the same patch. If a bee left the space and
returned, it was counted as a second visit. Counts were repeated numerous times on
the same and several different individuals of a given plant type for several flowering
seasons. For some we mapped individual plants and returned to the same individuals
over several years. Wide-angle binoculars were used to view bees on flowers of tall
trees. More than 17,000 counts were recorded over the duration of the survey.
For purposes of this paper we used the term plant types to refer to all the different
plant elements, that is, each species, each sex of dioecious species, and different
varieties/cultivars of the same species. Males and females of dioecious species were
considered as separate entities as male plants usually attracted more bees than
females, and males often flowered for longer periods.
Most large bees could be identified to species on the wing or on flowers, but
smaller bees had to be collected for identification; some collections were made with
long-handled nets. These counts provided frequency and abundance data on each
bee taxon. All bee collections were initially identified by one of us (TG), with follow
up identifications by RC and GF. Most collections are curated at the University of
California, Berkeley and are currently in the Frankie lab with eventual deposition at
the UC Berkeley Essig Museum of Entomology. A few selected specimens were kept
at the USDA-ARS Bee Lab in Logan, Utah.
Many of the native plants were identified through earlier studies (Frankie et al.,
1974, 1983), however, all plants were rechecked by one of us (MG) to ensure the
names would be consistent with those appearing in the new Manual de Plantas de
Costa Rica (Hammel et al., 2004; Hammel, Grayum et al., in preparation)
Results
Surveys from 2003 to 2012 revealed that there were 102 plant types that attracted
bees at measurable levels in Liberia and Bagaces (Appendix I). These plants belong
to 82 genera in 41 families. The most commonly used host plant flowers belonged to
the Fabaceae. Another important family for native bees was Bignoniaceae, which
also has numerous attractive species in adjacent wildlands.
Plants native to Costa Rica were common in gardens and accounted for 63 of 102
types; 39 non-natives to the country were also recorded attracting bees (Appendix I).
The 102 types could be divided into two groups: a group of 80 was considered
ornamental; these types were either planted or volunteered (self-seeded) and
subsequently managed by homeowners. These consisted of 44 tree types, 16 shrubs,
nine vines/lianas, eight herbaceous/woody herbs, and three palms. The second group
of 22 was considered weedy volunteers that were found scattered and unattended
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throughout both urban areas and sometimes in large patches (e.g., Ipomoea trifida
and Tridax procumbens). They were included in the study because they are an
essential component of the urban plant community utilized by bees (Geber and
Moeller, 2006). Further, 21 of the 22 weedy types were native to Costa Rica, and
natives are generally known to be attractive to native bees (Frankie et al., 2005a;
Frankie, pers. obs.). Most plants listed in Appendix I were found in both Bagaces
and Liberia.
Flowering phenological patterns were highly variable among the 80 ornamentals
and 22 weedy types, however, they were consistent for a given plant type (Frankie
et al., 1974). Some flowered all year or most of the year (Ipomoea carnea, Muntingia
calabura, Thevetia peruviana, and Thunbergia grandiflora); some for periods of two
or more months (Cordia dentata, Couepia polyandra, and Cryptostegia grandiflora);
and some for briefly a month or less (Andira inermis, Bixa orellana). Individuals of
some species flowered for just a few days (Pterocarpus michelianus and Tabebuia
ochracea), and some individuals more than once during the year (Crescentia alata,
Diphysa americana, and Tabebuia spp.). Individuals of some types such as Andira
inermis, Dalbergia retusa, and Piscidia carthagenensis, may not flower during a given
year (Frankie et al., 1974), however, even during ‘‘off years’’ some individuals of
these types could produce a few flowers.
Seasonal Flowering in Urban Bagaces and Liberia
As a group, the 102 plant types constitute a novel community of year-round floral
resources for bees. Seasonal flowering phenology of all plant types was separated
into three main groups based on early observations that each plant group had a
different general pattern: A) native trees, shrubs, vines, etc. (42 types); B) non-native
ornamentals, including one non-native weed species (39); and C) native weedy
species (21) (Fig. 2). In group A there was a substantial number of plant types in
flower during the dry forest months of February and March, a well known flowering
pattern for natives in Guanacaste wildlands (Janzen, 1967; Frankie et al., 1974,
1976). As summer heat and dryness intensified, flowering declined in April and May,
continuing into June of the first wet season (Frankie et al., 1974). A slight increase in
flowering occurred in July (short dry season), followed by a noticeable decline in
flowering during the remainder of the year. Median flowering period for plants in
this group was 3.0 months (25% 5 2.0; 75% 5 4.3 months).
In contrast to native plants of group A, non-natives in group B displayed a
different pattern with a relatively consistent level of flowering during the year
(Fig. 2). In each month there were 15–20 plant types in flower. Median flowering
period for group B plants was 3.0 months (25% 5 2.0; 75% 5 7.0 months). The
relative constancy of monthly flowering reflected interest of urban residents to have
some plants in flower year round.
Native weed types in group C flowered prominently from July through December
taking advantage of the long wet period in the dry forest (Fig. 2). Flowering dropped
off during the main part of the dry season and especially during the hottest, driest
months of April and May. Median flowering period for group C plants was
5.0 months (25% 5 3.0; 75% 5 7.5 months).
Periods of flowering for each plant type of the three plant groups were sorted from
1 to 12 months (Fig. 3). In native ornamentals (Group A) most flowering periods
VOLUME 86, ISSUE 4
331
Fig. 2. Graph of number of plant types in flower each month for native ornamentals, non-natives, and
native weeds.
were somewhat shorter compared to non-natives and weeds (Groups B and C), when
both the medians and 25/75 percentiles were considered together. There was also a
wide variety of flowering periods among weed types.
Pollen and Nectar and Main Attraction Period
All bee-adapted plants in both Bagaces and Liberia attracted bees primarily
during morning hours; however, rare and scattered visits were also recorded on most
types after 12 P.M. (Appendix I). To determine more precisely the periods when
pollen and nectar were available and attracting bees, we conducted more than 17,000
bee frequency counts over several years on all plant types. The most common
visitation period was a continuous one from about 6 A.M.–12 P.M., and 34 types were
recorded in this group including Caesalpinia pulcherrima (red/yellow flower types),
Spondias purpurea, Tabebuia rosea (Fig. 4), Tamarindus indica, and Tecoma stans. A
second group of 27 types attracted bees for about two hours or less; examples
included: Cordia dentata, Jatropha integerrima, Murraya paniculata, and Thevetia
peruviana. Within this second group were five that were attractive for about one hour
only in the morning: Byrsonima crassifolia, Cassia fistula, two Cosmos species,
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Fig. 3. Numbers of plant types versus numbers of months in flower for native ornamentals, non-natives,
and native weeds.
and Melampodium divaricatum. This brief period was especially noticeable in C.
crassifolia and C. fistula, which attracted medium to large size bee species.
There were other morning patterns in the list of 102 plant types, with most of these
attractive for 2 1/2 to 4 hr periods. A few of these started later in the morning such as
Baltimora recta, Bunchosia nitida, Pereskia bleo, Senna alata, Sida rhombifolia, and
Tridax procumbens. Two plants, Moringa oleifera and Terminalia catappa attract
infrequent visitation all day.
An atypical pattern of visitation, nectar robbing, was observed in two non-natives:
Thevetia peruviana (Apocynaceae) and Thunbergia grandiflora (Acanthaceae). In T.
grandiflora stingless bees have learned to visit flowers for pollen, but for nectar they
spend most of the day chewing holes in the bases of corollas to eventually reach the
nectar, which they cannot reach with their short mouth parts by going straight into
the throat of the corolla. In T. peruviana diverse orchid bees, Euglossa spp. and
Eulaema spp., primarily visit flowers with their long mouth parts early in the
morning for nectar, which small stingless bees cannot gain access to ‘‘legitimately’’.
VOLUME 86, ISSUE 4
Fig. 4.
333
Flowering Tabebuia rosea in Liberia. Photo by G. Frankie.
These small short-tongue bees instead also chew holes in the corolla bases to
eventually reach the sugary reward, an activity that takes most of the morning
(Inouye, 1983).
Some pollen and nectar resources used by the bees were from plants adapted for
nocturnal pollinators such as bats and moths: Brugmansia sp. (Solanaceae),
Crescentia alata and C. cujete (Bignoniaceae), and Calliandra sp., Enterolobium
cyclocarpum, Hymenaea courbaril, and Samanea saman (Fabaceae) (Equiarte et al.,
1987; Roubik, 1989). All but Brugmansia sp. are native to Costa Rica. Pollen and/or
nectar collections were made by bees in late afternoon on Crescentia spp. and H.
courbaril as flowers were beginning to open for attraction to evening visitors. In
contrast, bees visited Brugmansia sp., Calliandra sp., E. cyclocarpum, and S. saman
during early morning to forage on residual pollen and/or nectar from previous night
flowering.
In addition to daily pollen and nectar patterns described above there are subtle
biological patterns that are basic to the expression of pollen and nectar. Many of
these were investigated years ago and are believed to be related to plant reproductive
strategies at the individual and community levels (Janzen, 1967, 1971; Bawa, 1974;
Gentry, 1974; Heithaus, 1974; Frankie et al., 1974, 1976, 1983; Baker and Baker,
1983). These studies also indicate there is considerable inter and intraspecific variation
in presentation of floral rewards, and examples of this variation can be observed in
urban areas for some plants. Timing of the main attraction period (Appendix I) and
foraging behavior of visiting bees through frequency counts provides clues to these
subtle plant characteristics, some of which are presented below.
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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
Pollen
Flower opening time (FOT) for most native and non-native ornamental plant
types (Appendix I) was before or right after sunrise (Frankie et al., 1983). Some
pollen expression patterns could be readily observed in urban gardens. For example,
FOT was progressive during the morning in Gliricidia sepium and Piscidia
carthagenensis. In Dalbergia retusa and Poincianella eriostachys anther dehiscence
was gradual on open flowers during the morning. In some native ornamentals, pollen
could only be removed by native bees buzzing or vibrating the anthers, which have
apical pores (Wille, 1963; Buchmann, 1974; Roubik, 1989); honey bees cannot buzz
flowers. Bees were easily observed and heard buzzing ornamental flowers of Cassia
alata, C. fistula, Senna alata, S. pallida, and Solanum wendlandii.
Nectar
Regarding the nectar resource, bee attraction periods listed in Appendix I suggested a
starting point for understanding relationships between bees and nectar flow. Nectar
monitoring with precalibrated micropipettes (Frankie and Haber, 1983) combined with
extensive bee frequency counts provided more specific information, especially with
regard to intraspecific variations. One pattern to emerge from the counts is the difference
in bee attraction among individuals of a given plant population. That is, some conspecific
tree types (and shrubs) were noticeably more or less attractive to bees than others, even if
they occurred in close proximity. Even without the counts, this variation could be easily
observed in such trees as Andira inermis, Gliricidia sepium, Poincianella eriostachys,
Piscidia carthagenensis, Pterocarpus michelianus, Tabebuia ochracea, Tabebuia rosea, and
Tamarindus indica (Frankie et al., 1982, 2009a; see also Pleasants, 1979; Brink and Wet,
1980; Southwick and Southwick, 1983; Corbet et al., 1984; Comba et al. 1999).
In bee-attractive Andira inermis individuals two periods of peak bee abundance
were recorded; one from 0730-0830 and a second from ,1130–1330 (Frankie et al.,
2009a; Frankie and Haber, 1983). Once we were familiar with this pattern it was
common to observe a short early burst of bee activity followed by a second one three
to four hours later. Two periods of bee activity were also recorded on some
individuals of Gliricidia sepium and Tabebuia rosea (Frankie and Haber, 1983;
Frankie et al., 1983). In G. sepium, Xylocopa species regularly visited flowers in early
morning and again in mid afternoon.
Pollination Systems
Frankie et al., (1983) placed native Guanacaste tree species into large and small/
bee generalist categories in wild sites near Bagaces. Here we categorized each plant
type using an expanded set of pollination systems (relationships) based on
characteristics of the plant and taxonomic group of bees that visit it. The following
four categories are recognized (Appendix I).
N
N
N
Sm-B: Small bee. Flowers adapted for visits by small bee taxa such as halictids,
stingless bees, and some megachilids; 54 plant types (29 natives, 25 non-natives).
Div-B: Diverse bee. Flowers adapted for visits by diverse large bee taxa such as
Centris, Epicharis, Euglosini, and Xylocopa and small bee taxa; 31 plant types (22
natives, 9 non-natives).
Spec: Specialized flowers having morphological characteristics that make them
specialized for selected bee taxa. For example nectar in flowers such as Thevetia
VOLUME 86, ISSUE 4
N
N
335
species that can only be reached by bees with long tongues (Euglossa, Eulaema), or
flowers that are designed for buzz pollination such as Cassia and Senna species; 7
plant types (4 natives, 3 non-natives).
Noct/NP: Plants that are pollinated at night by moths and/or bats that also
provide pollen and nectar for bees for brief periods in late afternoons at flower
anthesis, or in early morning when there are residual floral resources from the
previous night; 7 plant types (6 natives, 1 non-native).
Combination Div-B/Spec: These included three plant types (2 natives, 1 nonnative) that have both diverse bee characteristics and specialized floral traits.
These were buzz flowers of Cassia fistula and Senna pallida. The third, Gliricidia
sepium, requires large bee taxa needed to open the ‘‘tight flowers’’, which then
makes them available to other bee taxa (Roubik, 1989).
Extensive bee visitation (frequency) counts were made on all bee taxa that visited
each plant type (Appendix I). These are ordered from left to right from most to
least frequently recorded for each plant. Listing for bee taxonomic groups
represents a summary of all counts done on a given plant type from both cities
through time. Some interpretation was necessary when there was variation in bee
composition and abundance from year to year (Roubik, 2001). An expanded list of
the bee taxa is found in Appendix II (See bee images, Figs 5–7). Variations in
composition and abundance of longitudinal bee data will be examined in a later
paper.
One distinct pattern to emerge from the frequency counts was the predictability of
specific bee-plant type associations. That is, each plant type could be expected to
generally attract certain bee taxa and only rarely others. For example, the two
Tabebuia species and Tecoma stans attract primarily Centris species and a wide variety
of other bee taxa. Brysonima crassifolia attracts low levels of Centris species foraging
for oil very early in the morning (5:30–6 A.M.) followed later by stingless bees and
honey bees seeking pollen. Male and female Bursera simaruba and Simarouba glauca
consistently attract only stingless bees and honey bees. Male plants of each of these
two species were more attractive than females. Thevetia species attract primarily
Euglossa and Eulaema species for nectar at low but consistent levels.
Some plant types were noteworthy for the highly diverse and abundant bee species
they attracted. This group (Div-B) included Andira inermis, Antigonon leptopus, Bixa
orellana, Dalbergia retusa, Piscidia carthagenensis, Poincionella eriostachys, Pterocarpus michelianus, Senna pallida, Tabebuia rosea, Tamarindus indica, and Tecoma
stans (Silva et al., 2007). A relatively high number of plant types (22 or 71%) in the
Div-B system were natives to Costa Rica (Appendix 1).
In 19 of 22 weed types (native and non-native), the small-bee pollination system
(Sm-B) was recorded with three in the diverse (Div-B) group (Appendix I). The Sm-B
group can be further divided into plant types having diverse (7 types) and less diverse
(12 types) small bee taxa. Diverse Sm-B types such as Baltimora recta, Ipomoea
trifida, Sida rhombifolia, and Tridax procumbens attracted a wide diversity of small
bee species in several genera.
Most bee species visiting urban plants, as well as conspecific plants in the wild, are
generalist foragers. In Table 1 we list examples of some of the generalist taxa.
Stingless bees and halictids stand out prominently, however, other diverse groups
such as Euglossa spp. and Exomalopsis spp. also foraged from a wide selection of
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Fig. 5. Male Centris flavifrons perched. Photo by R. Coville.
Fig. 6. Male Euglossa sp. visiting Securidaca sylvestris (Polygalaceae). Only 2/3 of long mouth parts are
exposed. Photo by R. Coville.
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Fig. 7. Trigona fulviventris foraging for pollen. Photo by R. Coville.
urban plant types. Honey bees (generalists) were dominant visitors on only 11 plant
types (6 natives; 5 non-natives). Four of the six natives were nocturnal flowering in
which honey bee foraging occurred either at FOT or on residual resources the
following day. A few species, Centris lutea, Peponapis sp. and Ptiloglossa sp. had
more selective host flower preferences.
Comparison of Bee Composition on Native Plants in Urban Versus Wildlands
Preliminary survey results indicated similar bee diversity and abundance on some
types such as Dalbergia retusa, Tabebuia spp., and Thevetia ovata in urban and
wildland areas. Diversity, but not abundance, appears higher on wild Andira inermis,
Cleome viscosa, Gliricidia sepium, Muntinga calabura, and Poincianella eriostachys.
The case for Bonellia nervosa (siempre verde) is in contrast as we have never observed
bees visiting flowers in wild individuals, yet the plant sets fruit at low levels. In urban
Bagaces flowers are commonly visited by at least two halictid and two stingless bee
species, and the plants commonly set fruit. This comparative work is in progress and
will be published in a future paper.
Discussion
Results of this study indicate that diverse native bee species of the Guanacaste
region of Costa Rica are readily using a novel composition or community of floral
resources in urban Bagaces and Liberia for their reproduction and year-round
survival. That is, humans have unknowingly created habitat for the bees in these two
cities. We have seen similar diverse native bee activity on flowers during occasional
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Table 1. Numbers of host plant families, genera, and species for selected native bee species/genera that
were considered generalist foragers in Bagaces and Liberia.
Bee species
Plant families
Plant genera
Plant species
Centris adani
Centris aethyctera
Ceratina spp.
Euglossa spp.
Epicharis elegans
Exomalopsis spp.
Gaesischia exul
Stingless bees (all genera)
4
4
10
7
3
14
1*
25
6
12
11
10
4
18
7
37
6
12
11
12
5
18
7
38
15
20
18
17
29
26
18
31
27
4
7
7
Apidae
Halictidae
Agapostemon nasutus
Augochorini
Halictus lutescens
Megachilidae
Megachile otomita
* (Family Fabaceae).
sampling in several other urban areas of Costa Rica, including communities around
the country’s capital city of San José. Current increases in development and
urbanization in Guanacaste and elsewhere in the country suggest that opportunities
for the creation of more habitats for bees and other flower visitors will increase.
The urban environment of Bagaces and Liberia can be considered a dynamic
habitat for bees for at least two reasons. First, urban residents are continually
manipulating their ornamental plants by either pruning the perennials or sometimes
taking them out entirely, which we have observed on our marked plants. Some
residents provide water and fertilizer to their plants, which can increase and extend
flowering for some species. Second, new ornamental species are occasionally
introduced, and this occurred primarily in Liberia, which has a larger and more
diverse population of people. Some of these new introductions (new species) are
currently being evaluated for their potential to attract bees. Finally, there are
undoubtedly a few more plant types attractive to bees in some residences, which
are found in enclosed Spanish-type gardens (courtyards). We were able to examine
only two of these enclosed gardens in Liberia.
Generalist native bees, such as those visiting Bagaces and Liberia, work well under
dynamic urban garden conditions. Being a generalist is advantageous as some native
and non-native host plants do not flower every year with the same regularity or
intensity. Thus, being able to use a variety of host flowers in this environment
ensures survival. In his large treatment of bees in Panama, Michener (1954) refers to
many Panamanian bee species as generalist foragers.
Weeds are common in urban Bagaces and Liberia, and at least 22 types provide
pollen and nectar for bee forage for diverse native bee taxa. They are considered an
important community floral resource for bees. Further, most listed species (21 of 22
types) are natives; and native bees generally prefer native plants in Guanacaste and
in temperate areas as well (Frankie et al., 2005a). Bagaces and Liberia weeds are
VOLUME 86, ISSUE 4
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found in residential gardens, in vacant lots, small parks, along roadsides,
surrounding public structures such as football stadiums, and creeksides. With a
few exceptions (e.g., Owen, 1991, 2010) urban bee-plant inventories world-wide
usually do not include adequate treatment of weeds. This lack may also be due, in
part, to studies that are mostly done in highly managed, urban garden
environments. Weeds in urban areas definitely need more attention in future
studies everywhere.
Each plant type had predictable bee taxa associated with it. Relationships between
plants and bee species/genera visiting them were consistent over the 10-yr study
period based on extensive frequency counts conducted. The same kind of predictable
relationships have been documented for urban plant types and bees in California using
the same frequency count method (Frankie et al., 2009b). Further, many experienced
bee biologists are familiar with these predictable bee-flower relationships.
The counts provided mostly bee diversity data and to a lesser extent bee
abundance records. It is believed that climatic patterns can greatly influence bee
abundance levels from year to year ( Roubik, 2001; Frankie et al., 2005a; Geber
and Moeller, 2006; Bartomeus et al., 2011). The relatively low-rainfall wet seasons
of 2006 through 2008 and subsequent drought periods, followed by high-rainfall
wet seasons of 2009/2010 probably greatly reduced bee abundance levels based on
our long-term monitoring records on individuals of selected plant species (eg.,
Andira inermis, Tabebuia rosea) in Bagaces and Liberia (unpubl.; see also Bawa,
2004).
The combination of native and non-native host plants in Bagaces and Liberia
provides a novel floral habitat (Marris, 2011) for native bee species. Resulting
relationships between the bees and flowers open up new avenues for questioning
and research. For example, a high number of ornamental plant types attracting
bees in Bagaces and Liberia were native to Costa Rica, and many were locally
native. This suggests that bee-flower relationships between urban native plants and
conspecific plants in nearby wildlands can be compared for a measure of the
potential of urban areas to provide habitat for bees (and other flower visitors).
That is, how much bee diversity and abundance can urban areas in Guanacaste be
expected to support? In this regard, preliminary results of a comparison of bee
species diversity and abundance on selected conspecific native plant types in urban
and nearby wildland indicate that a considerable diversity of native bees are using
urban floral resources.
At the opposite end of native ornamental plant use by native bees is the reality that
urban Guanacaste residents also use and enjoy a substantial number of non-native
plant types, with the desirable characteristic of flowering almost continuously during
the year (Fig. 2). Although native bees generally prefer native plant species (Frankie
et al., 2005b), they will also forage from non-natives if they provide attractive
(acceptable) pollen and nectar. Knowing predictable facts such as preferred floral
rewards (pollen, nectar, and oil plant types), reward presentation patterns, and
seasonal flowering periods can provide ecological understanding of what leads to
good pollinator habitat gardens (Frankie et al., 2009b). This kind of information
may also prove useful for designing habitat gardens in the future as local NGOs such
as Fundarbol (www.fundarbol.or.cr/) and Pronativas (www.pronativas.org/) of
Costa Rica are currently and aggressively promoting the use of native plants (and
some non-natives) in private gardens and public spaces in Guanacaste (Hunter and
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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
Hunter, 2008; Corbett et al., 2001). Findings from our bee-flower relationship
studies can also be extended beyond the urban environment for restoring bee habitat
in highly disturbed (deforested) natural environments (Frankie and Vison, in prep.)
and for some agricultural crops (see ‘‘Farming for Native Bees’’ in helpabee.org).
Does the Africanized honey bee (AHB) negatively impact native bee species in
Guanacaste gardens? This question emerged continually during our urban field
work, and the short answer, based on several lines of evidence, is probably not. The
African honey bee (Apis mellifera scutellata) first entered Costa Rica in 1983 and
proceeded to quickly Africanize the resident honey bee (A. m. mellifera) (Schneider,
1995). Although the AHB is considered a generalist forager on many plant types
(Appendix I), in most cases it was not the dominant bee.
Extensive land use changes since the early 1970’s, rather than possible AHB
competition, are believed responsible for general native bee decline in lowland
Guanacaste (Janzen, 1974). A brief history of these changes and bee responses is
presented in Frankie et al. (2009a). More changes in land use can be expected in the
future as human population growth increases in Guanacaste. Urbanization is also
expected to increase in several cities such as Bagaces, Canas, and Liberia (see also
Zanette et al., 2005).
Some urban areas can be viewed as refugia for beneficial organisms such as bees,
which we know can survive and reproduce in this novel environment. Other
beneficial and aesthetically pleasing flower visitors such as butterflies, some moths,
certain fly and wasp taxa can also benefit from suitable urban habitat. One of the
first persons to suggest that urban areas can serve as refugia (for genetic material)
was Jennifer Owen in Great Britain (1991, 2010; see also Watts and Lavriviere, 2004;
Zanette et al., 2005). The missing part of this scenario is the urban human
population that must become aware of this resource and the need to conserve,
protect, and encourage it if it is to continue. Costa Rica has over 800 species of
native bees (Griswold et al., 2000). Native bees are also pollinators of some
important crop plants of Costa Rica, such as squash and watermelon (GF, pers.
obs.), but more importantly they have coevolved with the magnificent and diverse
angiosperms of the country, and as such the plant-bee relationships should be
regarded a part of the natural heritage of the land along with the plants and the wild
places where they live (Kearns et al., 1998).
Outreach
The information presented in this paper will be published as a scientific study and
will be mostly available to biologists and some agency people, all of whom read
English. But what about outreaching the information to Spanish-speaking people of
Guanacaste and Costa Rica in general who we believe should be made aware of it
(Dicks et al., 2010)? We believe that researchers are the best outreach agents (Kearns
et al., 1998), yet we have only a few options for outreach at this time, and they are all
untested as to their effectiveness. First, we have partnered with two local NGOs to
share information of mutual interest. We are currently collaborating with Fundarbol
and Pronativas to provide both of these native plant organizations with native beenative plant information. We also have put both organizations on our website
(http://helpabee.org) in English and Spanish. In addition we have already
collaborated with both organizations in June 2011 at a local Guanacaste conference
VOLUME 86, ISSUE 4
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they organized on native plants of the lowland dry forest of Costa Rica. One of us
(GF) presented a paper in Spanish on native bee species associated with native
plants.
A second option is the presentation of high quality color photos of bees that we
can produce and distribute in the form of large posters (60.96 cm 3 91.44 cm). We
have just begun distributing posters of a collage of diverse native bee images (by one
of us, RC) to selected locations in Guanacaste such as souvenir shops, hotels, and
national park service sites so that local people can see enlarged images of bees with
their various sizes, shapes, and colors. The posters also have NGO websites for
further information. We have already used the posters as an outreach tool in
California with considerable success (GF and RC unpubl.). We plan to investigate
other potential distribution locations, such as local garden clubs and nurseries, as
our Costa Rican work continues.
Acknowledgements
We thank the California and Texas Agricultural Experiment Stations for their
support of the research. Partial support was also provided by the National
Geographic Society of Washington, DC. Peter Ronchi, Marvin Duarte, Marissa
Ponder, and Mary Schindler assisted with collections of bee-flower frequency data in
Bagaces and Liberia. David and Gary Stewart provided logistic support to conduct
research on their respective properties in Guanacaste. The Hilda Sandoval family in
Bagaces offered logistic and moral support for the project. Jim Cane, Robbin Thorp
and Jerry Rozen kindly read an early draft of the paper.
Paper contributions. Frankie: designed and organized survey, field data collections,
data analysis/interpretations, wrote ms. Vinson: field data collections. Rizzardi:
statistical analysis/interpretations. Griswold: bee identifications/editing. Coville:
photography, bee identifications. Grayum: plant identifications. Martinez: field data
collections. Foltz-Sweat: field data compilations. Pawelek: field data collections.
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Appendix I. Flowering plants in urban Bagaces and Liberia and their relative attraction to native
Guanacaste bees and honey bees.
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Appendix I. Continued.
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Appendix I. Continued.
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Appendix I. Continued.
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Appendix II. List of bee taxa collected from plants in urban Bagaces and Liberia, 2003–2012.
Apidae
Apis mellifera scutellata Lepeletier, 1836
Ancyloscelis spp.
Ceratina spp.
Centris adani Cockerell, 1949
Centris analis (Fabricius, 1804)
Centris aethyctera Snelling, 1974
Centris bicornuta Mocsáry, 1899
Centris flavifrons (Fabricius, 1775)
Centris heithausi Snelling, 1974
Centris lutea Friese, 1899
Centris nitida Smith, 1874
Centris trigonoides Lepeletier, 1841
Centris varia (Erichson, 1848) (5C. inermis and C. segregata)
Euglossa spp.
Eulaema spp.
Epicharis elegans Smith, 1861
Epicharis lunulata Mocsáry, 1899
Exomalopsis mellipes Cresson, 1878
Exomalopsis spp.
Gaesischia exul Michener, LaBerge and Moure, 1955
Melipona beecheii Bennett, 1831
Melissodes tepaneca Cresson, 1878
Undetermined Eucerini
Mesoplia decorata (Smith, 1854)
Mesoplia rufipes (Perty, 1833)
Mesochiera bicolor (Fabricius, 1804)
Melitoma spp.
Paratetrapedia apicalis (Cresson, 1878)
Paratetrapedia moesta (Cresson, 1878)
Peponapis spp.
Cephalotrigona spp.
Nannotrigona perilampoides (Cresson, 1878)
Plebia frontalis (Friese, 1911)
Scaptotrigona pectoralis (Dalla Torre, 1896)
Tetragonisca angustula (Latreille, 1811)
Trigona fulviventris Guérin-Méneville, 1844
Trigona spp.
Triepeolus spp.
Xylocopa fimbriata Fabricius, 1804
Xylocopa gualanensis Cockerell, 1912
Xylocopa spp.
Colletidae
Ptiloglossa spp.
Hylaeus spp.
Halictidae
Augochlora nigrocyanea Cockerell, 1897
Augochloropsis ignita (Smith, 1861)
Augochloropsis metallica (Fabricius, 1793)
Caenaugochlora costaricensis (Friese, 1917[‘‘,1916’’])
Pseudaugochlora graminea (Fabricius, 1804)
Undetermined Augochlorini
Agapostemon nasutus Smith, 1853
Halictus lutescens (Friese, 1921)
Halictus hesperus Smith, 1862
Lasioglossum spp.
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Appendix II. Continued.
Megachilidae
Coelioxys spp.
Anthidiellum apicale (Cresson, 1878)
Anthodioctes calcaratus (Friese, 1921)
Stelis costaricensis Friese, 1921(5Dolichostellis costaricensis)
Megachile abacula Cresson, 1878
Megachile axyx (Snelling, 1990)
Megachile chichimeca Cresson, 1878
Megachile exaltata Smith, 1853
Megachile otomita Cresson, 1878
Megachile toluca Cresson, 1878
Megachile spp.

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