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Composicin de las especies de murcilagos (Chiroptera) en diferentes usos de la tierra sobre los ecosistemas
Species composition of bats (Chiroptera) in different land- use mosaics
Bats are an abundant and diverse group of species that can be used as indicators of habitat disturbance and to test the effects of land-use mosaics on an ecosystem. For 11 nights I used mist-nets to sample the bat assemblages in pastures, forest fragments, banana fields and coffee fields on the Finca Santamara in Caitas, Monteverde, Costa Rica. The differences between the land-use areas were not significant in the abundance of bats, species richness, species diversity or trophic diversity. However the species that were found, such as Glossaphaga commissarisi and Sturnia ludovici could be considered indicators of disturbed habitats suggesting the entire area is degraded to a point that only generalist species persist.
Los murcilagos son un grupo diverso y abundante de especies que pueden ser utilizados como indicadores de la perturbacin del hbitat y para probar los efectos de los diferentes usos de la tierra sobre los ecosistemas. Por 11 noches yo utilice redes de niebla para muestrear comunidades de murcilagos en los pastos, en los fragmentos del bosque, en las plantaciones de banano y de caf en la finca Santamara en Caitas, Monteverde, Costa Rica.
Text in English.
Tropical Ecology 2006
Ecologa Tropical 2006
t Monteverde Institute : Tropical Ecology
Species composition of bats (Chiroptera) in different landuse mosaics Samantha Carter Department of Geography, The George Washington University ABSTRACT Bats are an abundant and diverse group of species that can be used as indicators of habitat disturbance and to te st the effects of land-use mosaics on an ecosystem. For 11 nights I used mist-nets to sample the bat a ssemblages in pastures, forest fragments, banana fields and coffee fields on the Finca Santamara in Caitas, Monteverde, Costa Rica. The differences between the land-use ar eas were not significant in the abundance of bats, species richness, species diversity or trophic diversity. However the species that were found, such as Glossaphaga commissarisi and Sturnia ludovici could be considered indicators of disturbed habitats suggesting the entire area is degraded to a point that only generalist species persist. RESUMEN Los murcilagos son abundantes y diversos y pueden ser utilizados como indicad ores de la alteracin del hbitat y para probar los efectos de los diferentes usos de la tierra sobre los ecosistemas. Por 11 noches yo utilic redes de niebla para muestrear com unidades de murcilagos en pastos, fragmentos de bosque, cultivos de pltano y caf en la Finca Sant amara en Caitas, Monteverde, Costa Rica. Los sitios muestreados no difirieron en la abundancia de mu rcilagos, la riqueza de especies, la diversidad de las especies y la diversidad de los grupos troficos. Sin embargo, Glossaphaga commissarisi y Sturnia ludovici podran ser considerados como indicadores de hbitats pe rturbados lo que sugiere que el rea entera est degradada a un punto que so lamente los especies ge neralistas persisten. INTRODUCTION Each year the planet loses 13 million hectares of forest and the majority of this forest is being converted into row crops and past ure land (2005 FAO Globa l Forest Resource Assessment). Some estimates suggest that be tween 40 and 50% of the Earths surface has been altered or degraded in some way by humans (Vitousek et al. 1997). Crop lands and pastures create a vast biome that is equal in area to the remaining forests of the world (Foley et al. 2005). If deforest ation trends continue at their current rates, many organisms will no longer be able to depend solely on pristine-primary forest. The long term survival of many species will largely depend on their ability to adapt to converted landscapes (Medelln et al. 2000). The impact of tran sformed land on the natural diversity will become increasingly more important for future conservation efforts. Certain species or groups of species can be very useful i ndicators of the effects of different land-use areas on the ecosystem health. To be a good indicator these taxa should 1
be abundant, as well as trophical ly, geographically and ecologically diverse. They should also have an important role in the ecosyste m and respond to changes in that ecosystem in a measurable way (Medelln et al. 2000). In the Neotropics, bats are more abundant than any other group of mammals and are extremel y diverse. There are around 220 species of bats in the New World Tropics and they o ccupy a wide array of niches ranging from primary to tertiary consumers (Medelln et al. 2000). They are also important seed dispersers and pollinators and are thought to be key players in forest regeneration (Nowak 1994). Insectivorous bats control popu lations of many insects including those that are vectors for disease and that ca use agricultural problems (Altringham1996). It is due the high level of diversity a nd abundance of bats almost everywhere in the tropics that they are useful indicators of the effects that different land use activities have on the ecosystem. Some species will be sensitive to changes and other opportunistic species will become more abundant, depending on the land use activity (Medelln et al. 2000). Studies conducted in Guatemala, Mexico and Costa Rica showed that many Phyllostomid bats species declined in species richness and abundance after land transformation, however, other species of Phyllostomids such as Sturnia lilium Carollia perspicillata / brevicauda and Desmodus rotundus tend to become more abundant in disturbed areas (Schulze et al. 2000, Medelln et al. 2000, LaVal 2004). In this study I aim to examine the species assemblages of bats in different land use areas in Caitas, Monteverde, Costa Rica. Specifically, to compare the bat communities that frequent banana fields, coffee fields, pastures and forest fragments. I hypothesized that there would be a difference in the community assemblages of bats in the different land-use areas. I predicted that the bat communities in the forest fragment would be more numerous and diverse in co mparison to the other land-use types. METHODS Study Sites I conducted this study at the Finca Santamara in Caitas, Monteverde, Costa Rica at an elevation of about 1300 m. The Finca Santamara is a farm that contains areas of open pasture, coffee, banana and other small cr op fields bordering several secondary forest fragments. Theses regenerating fragment s have been left standing since 1989. Procedure I used the forest fragments, coffee, banana, and pasture fields to conduct the experiment. Mist nets were set up during the day in each of the land-use areas, but left closed until dark. Nets for the coffee, banana and past ure were 12 m long and the forest fragments contained two 6 m long nets. The nights for data collection were chosen according to what time the moon is high in the sky (three hours after moonrise un til three hours before moonset) and the phase of the moon. Nets were also moved for each night so that the bats would not learn to avoid them. Just before dark, at around 5:30pm the nets were opened and checked continuously for two hours, by walking between the four sites and observing what was caught. They were identified to species and sex, and marked by cutting a small patch of hair on their back to notice in the event of a recapture. The nets were usually closed around 8:00pm each night; data were collected on 11 nights over the course of four weeks. Statistical Analyses 2
The Shannon Wiener index for diversity was used to compare the four different landuse areas. A Chi-Squared test was used to compare the differences in trophic groups between the land-use areas. A Chi-Squared test was also used to compare the differences in over-all abundance of bats between the land-use areas. Due to the overall low number of bats caught, recaptures were included in all calculations and statistics. RESULTS Habitat Use by Bats I caught a total of fi ve species of bats: Glossaphaga commissarisi, Sturnia ludovici, Carollia brevicauda, Micronycteris microtis and Myotis keaysi. Four of the five species found were of the largest family in Costa Rica, Phyllostomidae, the leaf-nosed bats. These four species are all found in a wide vari ety of habitats, including disturbed areas. G. commissarisi is often associated with agricultura l land-use areas in addition to being common to various habitat types. Both S. ludovici and C. brevicauda are found in a wide variety of habitats but are especially comm on in early successional forests. Each of the four species of phyllostomid bats belong to different subfamilies. The fifth species, M. keaysi is in the family Vespertilionidae, the worlds largest and most widely distributed family of bats (Laval and Rodrguez-H 2002). This species is also found in both disturbed and undisturbed habitats (Table 1). All except for one of the species capture d in this study was listed as either common or abundant for Monteverde (LaVal and Timm 2000). The species M. microtis was reported as uncommon to the Montev erde area but can re ach elevations of at least 2600 m (Laval and Rodrguez-H 2002). Patterns of Species Abundance There were 32 total mist-net captures incl uding five recaptures within the land-use mosaic on the farm. The most bats were cap tured in the banana field, followed by the forest fragments, then the pasture an d finally the coffee field (Table 2). There was no significant difference in the number of bats caught in the four landuse types when including the re captures (Chi-squared test, X2 = 10.25; df = 3; P > 0.05). The differences were not significant when excl uding recaptures as well (Chi-squared test, X2 = 9.15; df = 3; P > 0.05). Patterns in Species Richness The greatest numbers of species were captu red in the forest fragments (Figure 2). G. commissarisi and S. ludovici were caught in all four th e different land-use areas. C. brevicauda was captured in both the pasture and banana fields. In the forest fragments two species, M. keaysi and M. microtis, were found, neither of which was captured anywhere else. Patterns in Species Diversity G. commissarisi and S. ludovici were caught most frequently on the farm and in each of the land-use areas. The only exception was in the forest fragments where M. microtis out numbered S. ludovici (Figure 1). There was no difference in the diversity between the pasture and the forest (t = 1.13; v = 82.61; P > 0.05), the pasture and th e banana field (t = 0.02; v = 13.39; P > 0.05), and the pasture and the coffee field (t = 0.56; v = 91.99; P > 0.05). There was also no difference between the forest and the bana na field (t = 0.44; v = 18.33; P > 0.05) and the forest compared the coffee field (t = 0.57; v = 8.61; P > 0.05). Finally there was no difference between the banana and coffee fi elds (t = 0.19; v = 8.43; P > 0.05) (Figure 1, Table 3). 3
Patterns in Trophic Diversity Three groups of trophic guilds were found on the farm (Altringham 1996). Nectarivorous and frugivorous bats visited all four of the land-use areas test ed. Insectivorous bats were found only in the forest fragments (Figure 2). Although varied in abundance, the difference between the land-use areas in the di versity of trophic guild s is not significant (Chi-squared test, X2= 113.39; df = 6; P > 0.05). DISUSSION Many bats from the suborder Microchiroptera, su ch as all the bats found in this study, can travel up to 10-15 km from their roosts; some can even go as far as 80 km in one night (Nowak 1994). This means that the bats on th e farm can move about freely between the different land-use areas. This is consistent with the results of this study. There was no significant difference between the different land-u se areas in terms of the number of bats, number of species, diversity of specie s and diversity of trophic levels. All of the species found in the nets are habitat generalists (Table 1). S. ludovici and C. brevicauda, which were found on the farm, are particularly common to early stages of successional growth (Laval and Rodrguez-H 2002). The forest on the farm is only about 17 years old and is still in th e early phases of re generation. Both these frugivorous bats specialize on Piper fruits (Laval and Rodrguez-H 2002). This also supports the data because there are 42 species of Piper in the Monteverde area and it is an early succession plant that was prevalent on the farm (Haber 2000). G. commissarisi is a nectivarous bat that forages on the flowers of bananas and Macuna. This is consistent with the fact that there was a fairly large plot of bananas on the farm and G. commissarisi was the most common bat caught and more bats were caught in the banana nets than the other three land-use areas (Table 2, Figure 1). M. keaysi is often abundant in premontane and lower montane habitats, such as the farm. It has been noted that this species forages over trails and openings within the forest (Laval and Rodr guez-H 2002). This is exactly where the mist-nets were set up in the forest sites. M. microtis is noted to specialize on butterflies, specifically Morpho peleides which was obsevered frequently on the farm during the study (Laval and Rodrguez-H 2002). The differences in species abundance, species richness, species diversity and trophic diversity between land-use areas were no t significant. It is po ssible that this is because overall disturbance of the entire ar ea. Phyllostomid species can be used as indicators of disturbance in tropical areas because they are sensitive to habitat changes (Medelln et al. 2000). This c ould explain the absence of other species of phollostomids and the persistence of those found. Medelln et al. (2000) and Schul ze et al. (2000) found that the abundance of Sturnia lilium and Carollia perspicillata was an indicator of disturbance. Closely related are S. ludovici and C. brevicauda respectively, were both found on the farm. This could mean that th e species found on the farm are just the generalist species that pros per in habitat fragmentati on and land-use mosaics. Despite the non-significant differences between the landuse types, the data has some similarities to past st udies that did show significan t differences between land-use types. Medelln et al. (2000) showed that forest nets caught less bats overall than nets set up in agriculture areas. Another parallel between this study and Medel ln et al. (2000) is that the greatest number of species was found in the forest but the greatest number of bats was found in the agricultural areas (Table 2 and Figure 1). Medelln et al. (2000) also observed G. commissarisi in every habitat that they tested, again similar to this study. 4
These similarities could imply that the sample sizes in this study are just too small to show significance. For future studies, longe r and more extensive trails should be conducted. To further test the impacts of habitat disturbance and land use mosaics on bat assemblages, areas further and closer to prim ary forest should be studied as well such areas with more extensive agricu ltural productions taking place. ACKNOWLEDGMENTS Thanks to everyone who came out batting with me, I hope that you had fun and glad that you got to see some bats. Thanks to Alan, Karen, Cam and Tom for all their help working out the details, and just being so all around awesome. A big thanks to Tania, whom without I would be lost so mewhere in space trying to figure out the log of some crazy something prime valu e of whatever, and for having the cutest dog and cat in Costa Rica, sorry I mean world. A very special thanks to Norman and everyone at Finca Santamara for letting me run around their farm in the middle of the ni ght catching bats. A super huge thanks to Arturo for running around the farm with me night after night, rain or shine, for lending me his expert knowledge of bats, and for putting up with my shenanigans. I could not have done this with out him. LITERATURE CITED Altringham, J.D. 1996 Bats, biology and behavior. Oxford Universtiy Press Inc., New York Foley, J. A., R. DeFries, G. P. Asner, C. Barford, G. Bonan, S. R. Carpenter, F. S. Chapin, M. T. Coe, G. C. Daily, H. K. Gibbs, J. H. Helkowski, T. Holloway, E. A. Howard, C. J. Kucharik, C. Monfre da, J. A. Patz, I. C. Prentice, N. Ramankutty and P. K. Snyder. 2005. Globa l consequences of land use. Science 309: 570-574 Haber, W. A. 2000. Vascular plants of Monteverde. In N. M. Nadkarni and N. T. Wheelwright (Eds.). Monteverde: ecol ogy and conservation of a tropical cloud forest, pp. 489-490. Oxford University Press, Oxford, England. Kunz, T. H. and A. Kurta.1988. Capt ure methods and holding devices. In T.H. Kunz (Ed.) Ecological and be havioral methods for the study of bats, pp 6-17. Smithsonian Institution Press, Washington, DC. LaVal, R. K. 2004. Impact of global warmi ng and locally changing climate on tropical cloud forest bats. Journal of Mammalogy 85(2): 237-244 _____, and B. Rodrguez-H. 2002. Murcilagos de Costa Rica: Bats. Instituto Nacional de Biodoversidad, Santo Domingo de Heredia, Costa Rica _____, and R. Timm. 2000. Mammals of Monteverde. In N. M. Nadkarni and N. T. Wheelwright (Eds.). Monteverde: ecol ogy and conservation of a tropical cloud forest, pp 553-555. Oxford Universi ty Press, Oxford, England. 5
Medelln, R. A., M. Equihua and M. A. Amin. 2000. Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conservation Biology 14(6): 1666-1675 NA. (2005). Global forest resources a ssessment 2005. FAO. Available (online): http//www.fao.org/forestry/site/fra/en Nowak, R. M. 1994. Walkers bats of the world. The Johns Hopkins University Press, Baltimore, Maryland Schulze, M. D., N. E. Seavy and D. F. Whitacre. 2000. A Comparison of the Phyllostomid bat assemblages in undisturbed Neotropical forest and in forest fragments of slash-and-bu rn farming mosaic in Petn, Guatemala. Biotropica 32(1): 174-184 Vitousek, P. M., H. A. Monney, J. Lubc henco and M. Melillo. 1997. Human domination of the Earths ecosystem s. Science 277: 494-499 Table 1: Bat species found at Finca Santamara in Caitas, Monteverde, Costa Rica, along with family, subfamily and common habitat taken from Laval and Rodrguez-H (2002). Species Family Subfamily Common Habitat Glossophaga commissarisi Phyllostomidae Glossophaginae Found in a variety of habitats, including agricultural lands, lowlands and elevations as high as 3000m Sturnira ludovici Phyllostomidae Stenodermatinae Both primary and various disturbed habitats, very common to early successional growth, mid elevations 600-2600m Micronycteris microtis Phyllostomidae Phllostominae Both forested and disturbed habitats up to a least 2600m Carollia brevicauda Phyllostomidae Carollinae Both primary and various disturbed habitats, very common to early stages of regenerating forest, lowlands up to 1500m Myotis keaysi Vespertilionidae Premontane and lower montane habitats and disturbed areas, 14001800m Table 2: The number of bats captured on the farm including and excluding recaptures for each of the given land-use areas. Land-Use Type Total (n) Total (ex-recaps) Pasture 6 6 Forest 7 5 Bananas 15 13 Coffee 4 3 Total 32 27 6
Table 3: Diversity values (H), Hmax and evenness values (J) for each land-use type. Habitats were tested in pair-wise compar isons using the ShannonWeiner Index for Diversity. There was no significant di fference between the habitats. H' H'max J' Pasture 0.38 0.48 0.79 Forest 0.55 0.60 0.92 Bananas 0.38 0.48 0.8 Coffee 0.30 0.30 1 The Frequency of Different Bat Species in Different Land-Use Areas0 1 2 3 4 5 6 7 8 9 Pasture ForestBananasCoffee Land-Use TypeNumnber of Bats Glosophaga commissarisi Sturnira ludovici Corollia brevicauda Micronycteris microtis Myotis keaysi Figure 1: The number of each species of bat cap tured in the different land-use areas. This data is including the recaptures in the tota ls. There was no significant difference between land-use areas (Shannon Wiener index). 7
0 1 2 3 4 5 6 7 8 9 Pasture Forest Banana CoffeeLand-Use TypeNumber of Bats Nectivores Frugivores Insectivores Figure 2: The frequency of bats belonging to differe nt trophic guilds in the different landuse areas. Recaptures are included in the totals. 8