1 Pollen diversity on male Hylonycteris underwoodi Glossophaginae Julia Hoeh Department of Zoology, University of Wisconsin ABSTRACT Nectivorous bats play important roles in pollination systems in the tropics, by transferring pollen carried on their bo dies between the plants that they visit for nectar. The purpose of this study was to evaluate diversity indices of pollen loads found on individuals of Hylonycteris underwoodi Glossophaginae. It was conducted in the Selvatura Adventure Park in Monteverd e, Costa Rica during the rainy season, and related pollen load diversity to aspect ratio, wing tip index, and mass of individuals N = 30 males. The pollen load on individuals had low richness 2.20 Â± 0.81, diversity 0.09 Â± 0.16, and evenness 0.09 Â± 0.15 due to the large abundance of Markea sp. pollen grains. Markea sp. was present on every individual, suggesting a specialization by H. underwoodi . Neither the variation of the overall pollen load nor the variation in the abundance of Markea sp. poll en grains could be explained by aspect ratio, wing tip ind ex, or mass of the individuals . RESUMEN Los murciÃ©lagos nectarÃvoros juegan un papel importante en los sistemas de polinizaciÃ³n en los trÃ³picos, transfiriendo polen continuamente en sus cuerpos e ntre las plantas que visitan. El propÃ³sito de este estudio fue el de evaluar la diversidad de carga de polen encontrada en los individuos de Hylonycteris underwoodi Glossophaginae. Fue realizado en Selvatura, Monteverde, Costa Rica, durante la estaciÃ³n l luviosa. Se relacionÃ³ la diversidad con la carga de polen, la proporciÃ³n del aspecto, el Ãndice de punta del ala, y a la masa de individuos N = 30 machos. La carga del polen en individuos tuvo una riqueza 2,20 Â± 0,81, diversidad 0,09 Â± 0,16 y uniform idad 0,09 Â± 0,15 baja debido a la gran abundancia de Markea. Markea fue encontrada en todos los individuos, sugiriendo una especializaciÃ³n de H. underwoodi . Ni la variaciÃ³n de la carga general de polen ni la variaciÃ³n en la abundancia de sp de Markea pod rÃan ser explicadas por la proporciÃ³n de aspecto, ni por el Ãndice de punta del ala, ni por la masa de los individuos . INTRODUCTION Hylonycteris underwoodi Glossophaginae, a common Neotropical bat Arita 1993 found in Monteverde, Costa Rica, visits man y flower species each night. They feed on nectar LaVal and Rodriguez H 2002 and in the process disperse pollen. In many populations, nectar is the main source of energy for H. underwoodi year round in Costa Rica Tschapka 2003. Species diversity of b ats increases toward the equator, as well as, in lower elevations due to the increased variety of food resources LaVal and Rodriguez H 2002. This is possibly in part because flowers specialized for bat pollination are restricted primarily to the tropics LaVal and Rodriguez H 2002. Though this pollination system is important to the diversity of the tropics, the bats within this nectar feeding guild are understudied. Tschapka 2003 preformed a study analyzing niche partitioning of nectar resources b etween four Glossophaginae species. He examined how bat species differ in
2 the number and kinds of flowers they visit, and how that correlates to the variation in size and wing morphology between these four species. However, little is known about the vari ation within each of these species. As a generalist nectivore, H. underwoodi has been found to carry an assortment of pollen types in varying abundance. However, specialization may occur for certain seasons, times of the night, or foraging bouts. My study examines individual H. underwoodi and how they differ in the number and kinds of plant species they visit. Variation in body mass was shown as one of the factors that influence nectar partitioning between species of Glossophaginae Tschapka 2002. Mass variation within H. underwoodi is expected to correspond to flower choice based on nectar quality or quantity. Larger individuals may have higher absolute energy requirements and may seek more nectar productive plants. Larger bats, in this study assumed to be older, may have learned the location and species of the most nectar productive plants and specialized on those nectar rich flowers. Smaller or younger individuals may either have lower absolute energy needs, or may not have the experience to speciali ze on more productive flowers. Bat size should therefore correspond to the diversity or abundance of pollen based on nectar productivity of the flower. Diversity and abundance of pollen is also influenced by the foraging strategy of the bat. As outlined by Findley et al . 1972 aspect ratio and wing tip index are related to foraging choices between bat species. Aspect ratio and wing tip index are defined as: Aspect Ratio Index = Length of forearm mm + Length of 3 rd finger mm Length of 5 th fin ger mm Wing Tip Index = Length of 3 rd finger mm / Length of forearm mm A low aspect ratio has been found in forest dwelling bats, while high aspect ratio is found in migrants and open air feeders. Wing tip corresponds to hovering ability of intersp ecific bats. Both indices correlate with foraging strategies and differences in bat energetic requirements. Intraspecific wing variation of H. underwoodi has not been evaluated to determine if the differences are great enough to correlate with foraging b ehaviors. If the intraspecific differences do influence foraging strategies then amount and variety of pollen found on the individuals should correspond to varying aspect ratio and wing tip indices. I analyzed richness, diversity, and evenness of pollen s amples from individual H. underwoodi males to investigate proposed ideas of intraspecific niche partitioning and nectar specialization. I was interested in seeing if the range of these indices could be explained by the morphological characteristics of mas s, aspect ratio and wing tip index. MATERIALS AND METHODS The study was conducted at Selvatura Adventure Park in Monteverde, Costa Rica, from October 21 to November 16, 2007. Bats were captured using a mist net positioned near the nectar feeders in the hummingbird garden of Selvatura. Mist nets were tended from 1800 till 1900 hr when capture was not impeded by weather. Thirty male individuals of H. underwoodi were collected, and they were individually placed in cloth bags. The mass of the individual was determined with a Pesola 50g scale. Scotch tape was used to remove pollen from the forehead, the snout, the venter, the back, and the uropatangium.
3 Pollen samples were affixed to a microscope slide, labeled and later counted and identified in the lab . Following the removal of the pollen, the length of the forearm, third, and fifth digit were measured with calipers. Length measurements were used to calculate, for each individual, the Aspect Ratio Index and the Wing Tip Index as described in the prev ious section. Once the length and weight measurements were taken and the pollen samples were collected the individual was released. In the lab, pollen from each individual and body section was counted and identified using a compound microscope to genus or morphospecies based on descriptions by Roubik and Moreno 1991 and Jost 2004. The pollen richness, diversity and evenness per individual were estimated using the Shannon Weiner Index. Pollen indices were analyzed using regressions for each of the mo rphological measurements, as well as the aspect ratio index and wing tip index. The location of pollen on the body was compared using a Chi squared Test of Independence. RESULTS A range of sizes was found for male H. underwoodi for all of the morphologi cal measurements gathered Table 1. The greatest variability in a single parameter was found in the third digit length. TABLE 1. Averages with standard deviations and ranges for morphological measurements and pollen data from Hylonycteris underwoodi N = 30 in Selvatura Adventure Park, Monteverde . Average S.D. Range Mass of Body g 8.00 Â€ 0.59 6.5 9.5 Forearm Length mm 34.00 Â€ 2.05 30 40 3rd Digit Length mm 70.47 Â€ 2.83 68 80 5th Digit Length mm 45.93 Â€ 2.13 42 50 Aspect R atio 2.28 Â€ 0.13 2.06 2.64 Wing Tip Index 2.08 Â€ 0.11 1.89 2.29 Total Pollen Load N 421.80 Â€ 337.93 4 1476 Pollen richness S 2.20 Â€ 0.81 1.0 4.0 Pollen diversity H' 0.09 Â€ 0.16 0.00 0.82 Pollen evenness E 0.09 Â€ 0.15 0.00 0.7 5 Intraspecific variation was found for pollen load, richness, diversity and evenness Figure 1. Pollen was identified from eight different plant species in varying abundance. The diversity values and evenness for individual bats is low Figure 1 du e to the overwhelming abundance of one species Markea sp. of pollen. Markea sp. was present on all individuals sampled, yet the range in abundance of pollen found on individuals extends from four grains to over 1,000. The frequency of bats with greater amounts of pollen grains was also more evenly distributed for Markea sp. than other common pollen samples, such as Vriesea sp. and Mucuna sp. Figure 2a.
4 0 2 4 6 8 10 12 14 0.1-1.0 1.1-2.0 2.1-3.0 3.1-4.0 Pollen species richness S Frequency of bats a. 0 2 4 6 8 10 12 14 16 18 < 0.01 0.01-0.10 0.11-0.20 0.21-0.30 0.31-0.40 > 0.41 Pollen species diversity H' Frequency of bats b. 0 2 4 6 8 10 12 14 16 18 < 0.01 0.01-0.10 0.11-0.20 0.21-0.30 0.31-0.40 > 0.41 Pollen species evenness E Frequency of bats c. FIGURE 1. Frequency of Hylonycteris underwoodi individuals N = 30 carrying loads of pollen of different species richness a, diversity b, and evenness c at Selvatura Adventure Park in Monteverde.
5 0 1 2 3 4 5 6 7 8 9 <101 101-200 201-300 301-400 401-500 501-600 601-700 701-800 >800 Number of Markea grains N Frequency of bats a. 0 2 4 6 8 10 12 14 16 18 20 < 1.0 1.0-1.9 2.0-2.9 3.0-3.9 4.0-4.9 5.0-5.9 >5.9 Number of Vriesea grains N Frequency of bats b. 0 2 4 6 8 10 12 14 16 18 20 < 1.0 1.0-1.9 2.0-2.9 > 2.9 Numbers of Mucuna grains N Frequency of bats c. FIGURE 2. Frequency of Hylonycteris underwoodi individuals N = 30 carrying different intervals of three types of pollen, Markea sp. a, Vriesea sp. b, and Mucuna sp. c at Selvatura Adventure Park in Monteverde. Pollen grains were found mostly in the uroptangium for Markea sp. Figure 3 and other pollen types Figure 4. No clear trends were found between the amount of pollen per ba t and the mass of the bat p = 0.80, n = 30, F = 0.07, the aspect ratio p = 0.10, n = 30, F = 2.96, or wing tip index p = 1.18, n = 30, F = 1.94, though the trend is best fit
6 for aspect ratio Figure 5. Also, no trend was found for mass p = 0.88, n = 30, F = 0.024, aspect ratio p = 0.11, n = 30, F = 2.75, or wing tip index p = 0.17, n = 30, F = 1.99 when compared with Markea sp. pollen loads Figure 6. 0 1000 2000 3000 4000 5000 6000 7000 8000 Head Back Uropatangium Venter Body region Number of Markea grains FIGURE 3. Placement of pollen grains of Markea sp. on Hylonycteris underwoodi males coll ected at Selvatura Adventure Park in Monteverde. 0 5 10 15 20 25 30 35 Head Back Uropatangium Venter Body region Number of pollen grains Mucuna Vriesea Burmeistera Morphospecies A Morphspecies B Morphospecies C Morphospecies D FIGURE 4. Placement of pollen grains of Mucuna sp., Vriesea sp., Burmeistera, and Morphospecies A D on Hylonycteris underwoodi males collected at Selvatura Adventure Park, Monteverde.
7 0 200 400 600 800 1000 1200 1400 1600 6 7 8 9 10 Mass of Bat g Number of Pollen Grains 0 200 400 600 800 1000 1200 1400 1600 2.00 2.20 2.40 2.60 2.80 Aspect Ratio Number of Pollen Grains 0 200 400 600 800 1000 1200 1400 1600 1.85 1.95 2.05 2.15 2.25 2.35 Wing Tip Index Number of Pollen Grains FIGURE 5. Re gression analyses of the number of pollen grains with respect to mass R 2 0.0023, y = 27.8x + 199.4, aspect ratio R 2 0.0958, y = 825.86x + 2303.4, and wing tip index R 2 0.0647, y = 747.39x 1131 of Hylonycteris underwoodi collected at Selvatura Adve nture Park, Monteverde.
8 0 200 400 600 800 1000 1200 1400 1600 6 6.5 7 7.5 8 8.5 9 9.5 10 Mass of Bat g Markea Pollen Grains a. 0 200 400 600 800 1000 1200 1400 1600 2.00 2.10 2.20 2.30 2.40 2.50 2.60 2.70 Aspect Ratio Markea Pollen Grains b. 0 200 400 600 800 1000 1200 1400 1600 1.85 1.95 2.05 2.15 2.25 2.35 Wing Tip Index Markea Pollen Grains c. FIGURE 6. Regression analyses of the number of Markea sp. pollen grains with respect to mass a.R2 = 0.0009, y = 16.8x + 278.8, aspect ratio b.R2 = 0.0895, y = 798.09x + 2231.5, and wing tip index c.R2 = 0.0663, y = 756. 44x 1158.4 from Hylonycteris underwoodi males collected at Selvatura Adventure Park, Monteverde.
9 DISCUSSION Pollen load variation was present between Hylonycteris underwoodi individuals. The amount of pollen grains ranged from four to over 1000 found on a single individual. This variation in pollen load was not found to correlate with body mass, aspect ratio, or wing tip Figure 5, though it showed the closest trend with aspect ratio. This shows that the wing morphology and body mass are not the main cause for variation in pollen load. Other intraspecific variations, such as differing olfactory ability, variable feeding morphology adaptations e.g. tongue length, or timing of foraging bouts may play a greater role in the amount of pollen on an indiv idual. Variations could also be caused by differences in roost location relative to bat pollinated plants, length of foraging time before capture, or daily variation in abiotic conditions. Biotic factors could also affect pollen load on individuals. The amount of time the individual spent at the flower could be related to the amount of pollen carried away by the bat. The frequency of visits to a particular plant species is a likely cause for load variation. Lastly, the timing of the visit, a bat could arrive at a flower after it has been visited by another individual which removed most of the pollen. These other causes need to be examined further to understand why such variation of pollen load occurs between individuals of H. underwoodi . The diversity and evenness of pollen grains were also variable among individuals. Eight different pollen grains were identified, showing that the individuals had at least eight potential nectar sources. While both HÂ€ and E had low averages Avg. = 0.09 Table 1, their ranges still show variation. Again this variation was not found to correlate with mass, aspect ratio, or wing tip within H. underwoodi individuals. The composition of pollen grains present in this study differs from that found on H. underwoodi in a stud y performed at the same location in the spring of 2004 Millard, suggesting there may be seasonal causes for the variation in pollen diversity. Perhaps plants that are highly productive in the spring are less productive in the fall. Since the bats were captured early in the evening the composition of pollen may reflect variation in flower timing. The diversity and evenness values were greatly affected by the abundance of one pollen species Markea sp.. When Markea sp. was highly abundant HÂ€ and E were very low, and conversely when Markea sp. was present in low abundance, HÂ€ and E were higher. The influence of Markea sp. pollen on diversity and evenness indices leads to further consideration of why there is such variability in Markea sp. pollen abunda nce. Markea sp. pollen was present on every individual N = 30 in the study with a wide range of pollen grains found range = 4 to 1467 grains per individual. When separated from other pollen data, Markea sp. did not show a correlation to body mass, as pect ratio, or wing tip. Markea sp. pollen abundance may be better explained by temporal or seasonal variation in flower production. A study by Millard 2004, in the dry season found H. underwoodi to carry the greatest abundance of Mucuna sp. with a low er comparable abundance of Markea sp. This suggests that Markea sp. may provide an important nectar resource during the wet season, but be out produced by other bat pollinated flowers during the dry season. Some Markea species have been shown to open cl ose to dusk 1800 hr and be most productive early in the evening Voss et al. 1980. Bats may specialize on certain plant species at different times of the night based on when
10 the flower is most productive. The abundance of Markea sp. pollen may therefo re be due to the early evening capture times in the study. Body mass and wing morphology variations were not found to correspond with total pollen abundance, Markea sp. pollen abundance, pollen diversity, nor pollen evenness. Perhaps the energetic differ ences for small and large individuals may not be great enough to cause intraspecific foraging responses. A second possible explanation could be seasonality, Markea sp. may be the most available nectar resource in the wet season of Costa Rica, and regardle ss of size H. underwoodi must get energy from nectar of Markea sp. Specialization between H. underwoodi and Markea sp. was observed in this study performed in the wet season. Markea sp. may provide the main energy resource for this bat during the wet se ason, and without it the pollination system that involves many plants during the dry season may collapse. Future studies looking at the impact of forest fragmentation on the growth of Markea sp. and how this affects the apparent food choose of H. underwoo di may be especially beneficial in an area, like the tropics, where forested areas are continuously disappearing. ACKNOWLEDGEMENTS Thank you Karen Masters for helping me turn my crumbled down project into something IÂ€m pleased to submit. Thanks to Richar d LaVal for his guidance and stories throughout this project, as well as during the field trip. Thank you to Arturo, Kim, Pablo, Taegan, Jaime and Jordan for all of the help collecting bats and providing entertainment during the hours of mist netting and analysis. Thanks to Amy for the revisions and suggestions, we can certainly be in a chiropterophyllic relationship, as long as you specialize. Thank you to the staff at Selvatura Adventure Park and the Monteverde Research Station. Thanks to my fellow CI EE participants, especially my roommates, for making Costa Rica feel like home. Finally, thank you to Rafa for the transportation and conversations. LITERATURE CITED Arita, H.T. 1993. Rarity in Neotropical bats: correlations with phylogeny, diet, and body mass. Ecological Applications. 33: 506 517. Findley, J.S., E. H. Studier, and D.E. Wilson. 1972. Morphologic properties of bat wings. Journal of Mammalogy. 533: 429 444. Jost, M. 2004. The Pollen library. C.I.E.E. Spring 2004 Tropical Ecology and Conservation. LaVal, R. K. and B. Rodriguez H. 2002. Murcielagos de Costa Rica: Bats. Instituto National de Biodiversidad, Santo Domingo de Heredia, Cost Rica. Millard, E. 2004. Foraging strategies and body partitioning of glossophagine bats. C.I.E.E. Spr ing 2004 Tropical Ecology and Conservation: 1 11. Roubik, D.W. and J.E. Moreno. 1991. Pollen and Spores of Barro Colorado Island. Monographs in Systematic Botany, v.36. Missouri Botanical Garden. Tschapka, M. 2003. Energy density patterns of nectar resourc es permit coexistence within a guild of Neotropical flower visiting bats. Journal of Zoology. 263: 7 21. Voss, R., M. Turner, R. Inouye, M. Fisher, and R. Cort. 1980. Floral biology of Markea neurantha Hemsley Solanaceae, a bat pollinated epiphyte. Ameri can Midland Naturalist 103 2: 262 268.
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Diversidad de polen en los machos Hylonycteris underwoodi (Glossophaginae)
Pollen diversity on male Hylonycteris underwoodi (Glossophaginae)
Nectivorous bats play important roles in pollination systems in the tropics, by transferring pollen carried on their bodies between the plants that they visit for nectar. The purpose of this study was to evaluate diversity indices of pollen loads found on individuals of Hylonycteris underwoodi (Glossophaginae). It was conducted in the Selvatura Adventure Park in Monteverde, Costa Rica during the rainy season, and related pollen load diversity to aspect ratio, wing tip index, and mass of individuals (N = 30 males). The pollen load on individuals had low richness (2.20 0.81), diversity (0.09 0.16), and evenness (0.09 0.15) due to the large abundance of Markea sp. pollen grains. Markea sp. was present on every individual, suggesting a specialization by H. underwoodi. Neither the variation of the overall pollen load nor the variation in the abundance of Markea sp. pollen grains could be explained by aspect ratio, wing tip index, or mass of the individuals.
Los murcilagos nectarvoros juegan un papel importante en los sistemas de polinizacin en las zonas tropicales, transfiriendo el polen llevado en sus cuerpos entre las plantas de nctar que visitan. El propsito de este estudio fue evaluar los ndices de diversidad de cargas de polen que se encuentran en los individuos de Hylonycteris underwoodi (Glossophaginae). Este estudio se llev a cabo en Selvatura, Monteverde, Costa Rica durante la estacin lluviosa.
Text in English.
Tropical Ecology 2007
Ecologa Tropical 2007
Cargas de pollen
t Monteverde Institute : Tropical Ecology