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Variation in the abundance and diversity of Hymenoptera as an indicator of biodiversity across three tropical habitats in Monteverde, Costa Rica
Translated Title:
Variación en la abundancia y diversidad de himenópteros como un indicador de la biodiversidad a través de tres hábitats tropicales en Monteverde, Costa Rica ( )
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Ramsel, Jessica
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Hymenoptera   ( lcsh )
Fragmented landscapes   ( lcsh )
Hymenoptera
Paisajes fragmentados
Tropical Ecology 2007
Ecología Tropical 2007
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Reports   ( lcsh )
Reports

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Abstract:
Loss of biodiversity is becoming increasingly evident and is receiving much attention. Fragmentation and conversion of natural forest into agricultural land in particular are increasingly detrimental to biodiversity. It has been stated that agroecosystems such as agroforestry provide a valuable contribution to the overall biodiversity of the landscape and may even be suitable for conservation efforts (Tylianakis et al. 2005; Klein et al. 2002). This study examined the relative abundance and diversity of Hymenoptera within three habitats: primary forest, an agricultural area, and an open area. This was done by placing yellow plates with honey and soap water in each of the three areas. The plates were left out for five hours and then all Hymenoptera were collected and analyzed to find relative abundance and diversity. It was found that there was no significant difference in the number of individuals or species between primary forest and the agricultural area (Student t-test: t = 3.04, df = 275, p = 0.164). In contrast, there was a significant difference between primary forest and the open area (Student t-test: t = 5.83, df = 53, p < 0.001) and the agricultural area and the open area (Student t-test: t = 7.80, df = 51, p = 0.009). The greatest numbers of individuals were found in the primary forest and the greatest number of species in the agricultural area. The fewest species and individuals were found in the open area. That there was no significant difference between numbers of species or individuals in primary forest versus agroforest may suggest that agroforest could be a suitable area in which to focus a conservation effort.
Abstract:
La perdida de biodiversidad es cada vez mas evidente y ahora esta recibiendo mucha atención. La fragmentación y la conversión de los bosques naturales en tierras agrícolas son particularmente degradantes para la biodiversidad. Se sugiere que los agro-ecosistemas como los sistemas agro-forestales se puede usar para la conservación (Klein et al. 2002). Este estudio examino la abundancia relativa y la diversidad de Hymenoptera en tres lugares: bosque primario, un area agrícola y un area abierta.
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Text in English.
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Born Digital

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Loss of biodiversity is becoming increasingly evident and is receiving much attention. Fragmentation and conversion of natural forest into agricultural land in particular are increasingly detrimental to biodiversity. It has been stated that agroecosystems such as agroforestry provide a valuable contribution to the overall biodiversity of the landscape and may even be suitable for conservation efforts (Tylianakis et al. 2005; Klein et al. 2002). This study examined the relative abundance and diversity of Hymenoptera within three habitats: primary forest, an agricultural area, and an open area. This was done by placing yellow plates with honey and soap water in each of the three areas. The plates were left out for five hours and then all Hymenoptera were collected and analyzed to find relative abundance and diversity. It was found that there was no significant difference in the number of individuals or species between primary forest and the agricultural area (Student t-test: t = 3.04, df = 275, p = 0.164). In contrast, there was a significant difference between primary forest and the open area (Student t-test: t = 5.83, df = 53, p < 0.001) and the agricultural area and the open area (Student t-test: t = 7.80, df = 51, p = 0.009). The greatest numbers of individuals were found in the primary forest and the greatest number of species in the agricultural area. The fewest species and individuals were found in the open area. That there was no significant difference between numbers of species or individuals in primary forest versus agroforest may suggest that agroforest could be a suitable area in which to focus a conservation effort.
La perdida de biodiversidad es cada vez mas evidente y ahora esta recibiendo mucha atencin. La fragmentacin y la conversin de los bosques naturales en tierras agrcolas son particularmente degradantes para la biodiversidad. Se sugiere que los agro-ecosistemas como los sistemas agro-forestales se puede usar para la conservacin (Klein et al. 2002). Este estudio examino la abundancia relativa y la diversidad de Hymenoptera en tres lugares: bosque primario, un area agrcola y un area abierta.
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Variation in the abundance and diversity of Hymenoptera as an indicator of biodiversity across three tropical habitats in Monteverde, Costa Rica Jessica Ramsel Department of Biology, University of Wisconsin-Madison ______________________________________________________________________________ ABSTRACT: Loss of biodiversity is becoming increasingly evident and is receiving much attention. Fragmentation and conversion of natural forest into agricultural land in pa rticular are increasingly detrimental to biodiversity. It has been stated that agroecosystems such as agroforestry provide a valuable contribution to the overall biodiversity of the landscape and may even be suitable for conservation efforts (Tylianakis et al. 2005; Klein et al. 2002). This study examined the relative abundance and diversity of Hymenoptera within three habitats: primary forest, an agricultural area, and an open area. This was done by placi ng yellow plates with honey an d soap water in each of the three areas. The plates were left out for five hours and then all Hymenoptera were collected and analyzed to find relative abundance and diversity. It was found that there was no significant difference in the number of individuals or species between primary forest and the agricultural area (Student t-test: t = 3.04, df = 275, p = 0.164). In contrast, there was a significant difference between primary forest and the open area (Student t-test: t = 5.83, df = 53, p < 0.001) and the agricultural area and the open area (Student t-test: t = 7.80, df = 51, p = 0.009). The greatest numbers of individuals were found in the primary forest and the greatest number of species in the agricultural area. The fewest species and individuals were found in the open area. That there was no significant difference between numbers of species or individuals in primary forest versus agroforest may suggest that agroforest could be a suitable area in which to focus a conservation effort. RESUMEN: La prdida de biodiversidad es cada vez ms evidente y a hora esta recibiendo mucha at encin. La fragmentacin y conversin de bosques naturales en tierra agrcolas son particularmente degradantes para la biodiversidad. Se sugiere que los agro-ecosistemas como los sistemas agro-fore stales se puede usar para la conservacin (Klein et al 2002). Este estudio examin la abundancia relativa y diversidad de Hymenoptera en tres lugares: bosque primario, un rea agrcola y un rea abierta. Se hizo este estudio poniendo pl atos amarillos con miel, jabn, y agua en cada una de las tres reas. Se dejaron los platos por cinco horas y despus todos los himenpteros fueron recolectados e identificados para saber su abundancia relativa y diversidad No hubo diferencia significante entre la cantidad de individuos ni especies entre el bosque primario y el rea agrcola. En cambio, si hubo una diferencia entre bosque primario y el rea abierta, y entre el rea agrcola y la abierta. Se encontr la cantidad ms grande de individuos en el bosque primario y la mayor cantidad de especies en el rea agrcola. La menor cantidad de especies e individuos fueron encontrados en el rea abierta. El que no hubiera diferencias significativas entre nmero de especies ni individuos en bosque primario contra agro-silvestre sugiere que las tierras agro-silvestres pueden ser un lugar donde se debe enfocar las fuerzas de conservacin. INTRODUCTION: Changes to the forests of the world are receiving increasing attention at the highest scientific and governmental levels. The most notable changes fa ll into three categories including: reduction in total forest acreage; conversion of naturally st ructured and regenerated forest to monoculture plantations; and fragmentation of remaining natural forests into progressively smaller patches isolated by plantations or by ag ricultural, industrial, or ur ban development (Harris 1984). Conversion of natural ecosystems to agroecosyst ems continues to accelerate in many tropical countries, resulting in the degradation of tropical rain forests (Klein et al. 2006). The loss of 1

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biodiversity is becoming increasingly evident along with the loss of services that those organisms provide (Tylianakis et al. 2005). These services include things such as soil nutrient supply, soil carbon storage, and biodiversity re lated services such as decomposition, natural control of pests and invasive species and pollina tion (Klein et al. 2006). In addition to habitat degradation, fragmentation of natural habitats ma y cause particular species to flourish, decline, or disappear entirely as a result of direct ch ange or through edge effects. Furthermore, if fragmentation affects certain species participating in mutualistic interactions, the effects could magnify to include other speci es as well (Aizen et al. 1994). Insects which act as pollinators, especially, could have a large e ffect if their numbers were lim ited due to fragmentation. Members of Hymenoptera are abundant in mo st ecosystems and are involved in many such mutualistic interactions with other taxa. They can therefore be used as an indicator species as they respond rapidly in numbers to environm ental change because of their high reproductive capacity and short life span (Vinson et al. 2004 ). Van Nouhuys (2005) de scribes how species at higher trophic levels, including parasitoid wasps, are more sensitive to habitat fragmentation. This is because food/prey/host sp ecies are limited to a subset of suitable locations and changes in their population can make them an unstable reso urce for the dependant species. Klein et al. (2006) has suggested that divers ity and parasitism are enhan ced by improved connectivity of agroecosystems with natural ha bitats. In contrast, after converting natural habitats to agroecosystems, populations of para sitoids are typically low (Klein et al. 2006) This can give an advantage to a number of pests, as parasitoids ar e known to control insect pests in addition to the populations of many beetles a nd moths (Arnett et al. 1981). Conservation efforts to save biodiversity generally focus on remaining areas of natural ecosystems. However, only a small amount of th e terrestrial environment is unmanaged and uninhabited by humans, and most species that survive in fore st remnants interact with agricultural systems. Despite this, the potential value of agroecosystems for conservation is often overlooked. Agroforestry is characterized by high diversity of vegetation and thus can maintain surprisingly high levels of biodi versity. Shade coffee, especiall y, is able to support relatively high biodiversity (Klein et al. 2002 ). This study, therefore, looked at three different habitats within the Monteverde Cloud fore st, using Hymenoptera diversity and abundance as an indicator of biodiversity. The three habitats included prim ary forest, agricultural land and an open area. The results of this study may i ndicate their relative potential as a conservation site. I expected that there would be a difference in the number of individuals and speci es between the three habitats. Ricketts (2004) has de scribed how bee richness and pollen deposition rate were higher in [coffee plantation] sites within 100m of forest fragments than in sites farther away. Therefore, I predicted that there would be the most sp ecies and individuals in primary forest. MATERIALS AND METHODS: Site Location: This study was carried out in three different habitats; primar y forest, agroforest, and an open area. The primary forest is located within the Monteverde Biological Station, classified as lower montane cloud forest. It is located near the continental divide of Costa Ricas Cordillera de Tilarn mountain range. The study site includes th e first 250 m of the fore st, although the actual forest is considerably larger. The agroforest is located near Karen Masters property and includes shade coffee, banana trees and citrus trees. The area is approximately 1000 m2. The open area is an open field located near the agro forest, and is approximately 1000 m2. It contains mostly grasses with some small shrubs. 2

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Experimental Setup: Five yellow plates were placed in each of the three habita ts approximately 50 m apart. A ring of honey was placed at the bottom of each plate. The plate was then filled with a mixture of soap and water. A rock was placed at the center of each plate to prevent the plates from blowing over. Each day the first plate was set out around 7: 00 am in the primary forest and the last plate was set out by 8:00 or 9:00 am in the open area. The plates were th en collected in the same order they were set out to standardize data collection time, beginning in the prim ary forest at 1:00 pm. During collection, any insects found on the plates were placed in a plastic vial marked according to the habitat location, plate number and day. Once all plates had been collected, a small amount of ethanol was poured into each vial in order to preserve the sample. This procedure was repeated over four days. Data Analysis: The data from each day and site were grouped together for analysis. The insects from this group of five plates were then placed on a Petri dish and inspected under a dissecting microscope. Any insects found that were not hymenoptera were discarded, as well as any wingless ants. Remaining insects included bees, wa sps, parasitoid wasps and winged ants. These were then separated into morpho species. The first day morpho species were identified and verified by Pablo Allen. This process was then rep eated with the next group of five plates from another habitat on a different day. Petri dishes and morpho species were then compared to identify which morpho species occurred across habitats. Statistical Analysis: After all morpho species were id entified, the results were analyzed finding S, H, E, N, and Smarg. The H values were then compared using a t-test. An ANOVA was run to determine if there was any difference in the num ber of individuals between sites. Finally, a Post Hoc LSD test was run to see if there was a difference between the habitats. RESULTS: The data partially supported my hypothesis and prediction. There was a difference in number of species and individuals between primary forest, agricultural land, and the open area. The greatest number of individuals were f ound in primary forest (163 of 314), as predicted, however the greatest number of species was found in the agri cultural area (52 of 93, Table 1, Figure 1). 160 180 0 20 40 60 80 100 120 140 PrimaryAgriculturalOpen number of individuals number of species TABLE 1. Number of Individuals and Species by Habitat Habitat # Individuals # Species Primary 163 46 Agricultural 118 52 Open 33 16 FIGURE 1. Number of Indi viduals and Species by Habitat 3

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Although the original goal of this project was to look prim arily at bees and wasps within the three habitats, very few were found in each, t hus parasitoid wasps were also included. Two bees were found, both in the agricultural area. Any wasps found were more or less evenly distributed between the three hab itats, however, slightly more we re found in the open area. There was some crossover between habitats, mostly between agricultural areas and primary forest. Notably, there were 10 individuals of morpho sp ecies 15 in primary forest, and nine in the agricultural area (see appendix). One was al so found in the open area. Additionally, 18 individuals of morpho species 24 were found in primary forest and nine were found in the agricultural area. None were f ound in the open area. There was also some cross over between agricultural area and op en area. Five indivi duals of morpho species 61 were found in the agricultural area and seven in the open area. Morpho species 24 was found to be the most abundant in primary forest with 18 indivi duals, followed by morpho species 23 with 14 individuals and morpho species 54 with 12 individuals. In total, there were 163 individuals and 46 morpho species in primary fore st. The most abundant morpho speci es in the agricultural area was morpho species 16, 17, and 25, each with nine individuals. In total there were 118 individuals and 52 morpho species in the agricultural area. Fi nally, the most abundant morpho species in the open was morpho species 61 and 94, both with seven individuals. The open area had a total of 33 individuals and 16 morpho species All habitats together, there were 93 morpho species and 314 individuals. I found that there was a signi ficant difference in number of species and individuals between primary forest and open area (t -test: t = 5.83, df = 53, p < 0.001), and between agricultural land and the open area (t-test: t = 7.80, df = 51, p = 0.009). However, the difference in number of species and individuals was not significant between primary forest and agricultural land (t-test: t = 3.04, df = 275, p = 0.164, Table 2). A dditionally, the data were analyzed to find N, S, Smarg, H, and E (Table 3). This showed that primary forest has the greatest number of individuals (N = 163) and the ope n area has the fewest (N = 33). Agroforest has the greatest species richness (S = 52) and the open area the lo west (S = 16). Similarly, agroforest has the highest diversity (H = 3.62) a nd the open area has the lowest (H = 1.03). Finally, agroforest shows the highest evenness (E = 0.92), and the open area has the lowest (E = 0.37). ______________________________________________________________________________ TABLE 2. Results of t-test. TABLE 3. N, S, Smarg, H and E by Habitat Test df t-test p-value primary vs. agricultural 275 3.04 p = 0.164 Primary vs. open 52 5.83 p < 0.001 agricultural vs. open 51 7.8 p = 0.009 _____________________________________________________________________________ Primary Agricultural Open N 163 118 33 S 46 52 16 Smarg 8.83 39.64 536.01 H' 3.32 3.62 1.03 E 0.87 0.92 0.37 Lastly, an ANOVA was run on the data to de termine p-value and significance (Figure 2). The p-value was found to be .00295, meaning the data are statistically si gnificant. See appendix for the complete list of morpho speci es and individuals by habitat. 4

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Std. Dev. Std. Err. Mean# individuals -3 -2 -1 0 1 2 3 4 5 6 ForestAgriculturalOpen FIGURE. 2. Results of ANOVA performed on number s of species and indi viduals found in each habitat type (p-value = .00295, F = 8.372, df effect = 2, df error = 276). ______________________________________________________________________________ DISCUSSION: Diversity varied greatly between primary forest and the open area and between the agricultural and open areas. However, there was no signifi cant difference between pr imary forest and open areas. Although there were more individuals f ound in the primary forest, more species were found in the agricultu ral area. This could be because while the primary forest is predominantly uniform in habitat type, the open area included nu merous crops, such as coffee, bananas, and mango, which could attract a greater variety of species. However, evenness was found to be greater in the agricu ltural area (E = 0.92) than in the primary forest (E = 0.87), suggesting that the inclusion of various microhabitats within the agroforest is not necessarily what accounts for the greater species richness. The largest number of bees and wasps were found in the open area, while primary forest and agroforest included mainly parasitoid wasp s. This could be because wasps and bees are found primarily in the canopy, however only the understory was incl uded in this study. It is possible that if plates were set higher up, more bees and wasps could be found, adding to the species richness of primary forest and agroforest. It could serve to further differentiate between the abundance and species richness of primary forest versus agroforest. Additionally, it is also possible that there were more b ees and wasps in the open area b ecause it would have been easier to see the yellow plates as they were not c overed by trees. Finally it is also possible that abundance of parasitoid wasps was lower in the open area because they are more sensitive to habitat fragmentation and could have responded to the open area as if it were a fragmented or degraded habitat. Another factor that could have influenced th e results is the size of the habitat studied. Although plates were placed in the same size area, the overall habitats were very different in size. The primary forest is considerably larger th an either of the other sites, meaning that the overall evenness may be higher, but due to th e size of the forest and time constraints on 5

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collection, fewer individuals and species were caught than may actually be in the area. Accordingly, a longer collection time may result in a greater numb er of individuals or greater species richness. However, it should be noted th at this is true across all habitats; a greater collection time could lead to a greater number of species and individua ls. Further study is therefore necessary to gain more accurate results. With the rapid population growth in many c ountries, and especially tropical countries, primary forests are increasingly stressed. Th e human population has already removed between 35% and 50% of the original closed canopy tropi cal forests worldwide. In addition, the net loss of tropical forest aver ages between 50,000 and 120,000 km2 per year (Wright 2006). Numerous studies have commented on the role of agroforestry in adding to the overa ll biodiversity of the landscape and have suggested the po ssibility of using agricultural land as an area of biodiversity conservation (Klein et. al 2002; Tylianakis et al. 2005). This study found no significant difference between primary forest and agricultura l land, which may suggest that agricultural land is an acceptable alternative to traditional natural forest conservation efforts. However, in order to further support this, future st udies should include orders other than Hymenoptera to determine true biodiversity across habitats. If with further testing, this proves to be correct then agroforest will become increasingly important in the future. ACKNOWLEGDEMENTS: I thank Tania for her help and advice on this project. I thank Pablo A llen for his assistance throughout the project, including fi nding the only patch of truly shade-grown coffee in all of Monteverde, Karen Masters for the use of her property as well as her encouragement and enthusiasm, and Nick and Maria for helping me sort through morpho species. Thanks to Jess and Beth for reviewing my paper for me. Finally, I thank the Estacin Biolgica de Monteverde and the various landowners that allowed me to work on their property. 6

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7LITERATURE CITED: Aizen, M. A. and P. Feinsinger. 1994. Habitat Fragmentation, Native Inse ct Pollinators, and Feral Money Bees in Arge ntine Chaco Serrano. Ecological Applications 4: 378-392. Arnett, Dr. R. H. and Dr. R. L. Jacques, Jr. 1981. Simon & Schusters Guide to Insects Simon & Schuster Inc., pp. 269. Harris, L. D. 1984. The Fragmented Forest: Island Biogeogr aphy Theory and the Preservation of Biotic Diversity The University of Chicago Press, Chicago. Klein, A., I. Steffan-Dewenter D. Buchori and T. Tschar ntke. 2002. Effects of Land-Use Intensity in Tropical Agroforestry Systems on Coffee Flower-Visiting and Trap-Nesting Bees and wasps. Conservation Biology 16: 1003-1014. Klein, A., I. Steffan-Dewenter and T. Tscharntke. 2006. Rain Forest Promotes Trophic Interactions and Diversity of Trap-Nes ting Hymenoptera in Adjacent Agroforestry. Journal of Animal Ecology 75: 315-323. Ricketts, T. H. 2004. Tropical Forest Fragments E nhance Pollinator Activity in Nearby Coffee Crops. Conservation Biology 18: 1262-1271. Tylianakis, J. M., A. Klein and T. Tscharntke. 200 5. Spatiotemporal Variation in the Diversity of Hymenoptera across a Tropi cal Habitat Gradient. Ecology 86: 3296-3302. Van Nouhuys, S. 2005. Effects of Habitat Fragment ation at Different Trophi c Levels in Insect Communities. Ann. Zool. Fennici 42: 433-447. Vinson, S. B., S. T. OKeefe and G. W. Fra nkie. 2004. The Conservation Values of Bees and Ants in the Costa Rican Dry Forest. In Gordon W. Frankie, Alfonso Mata, S. B. Vinson (Ed). Biodiversity Conservation in Costa Rica pp. 67-79. University of California Press, Berkeley. Wright, S. J. and H. C. Muller-Landau. 2006. The Future of Tropical Forest Species. Biotropica 38: 287-301.

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APPENDIX Data Sheet of Morpho Species by Habitat Morpho Species Primary Agricultural Open 1 0 1 0 2 3 5 0 3 0 1 0 4 0 1 0 5 10 1 0 6 1 1 0 7 0 2 0 8 0 1 0 9 0 5 0 10 0 3 0 11 0 1 0 12 0 1 0 13 6 1 0 14 1 2 0 15 10 9 1 16 2 9 0 17 8 1 0 18 2 1 0 19 8 6 0 20 2 3 0 21 0 2 0 22 0 2 0 23 14 2 0 24 18 9 0 25 1 0 0 26 1 0 0 27 1 2 0 28 5 2 0 29 2 0 0 30 1 0 0 31 6 0 0 32 1 0 0 33 1 0 0 34 1 7 0 35 2 0 0 Morpho Species Primary Agricultural Open 36 1 0 0 37 1 0 0 38 1 0 0 39 6 0 0 40 0 0 0 41 2 0 0 42 1 1 0 43 1 1 0 44 0 0 0 45 0 1 0 46 0 2 3 47 0 0 1 48 0 0 4 49 0 0 1 50 0 0 1 51 0 0 1 52 1 0 1 53 1 0 0 54 12 0 0 55 0 1 0 56 0 2 0 57 1 2 0 58 0 1 0 59 0 1 0 60 0 5 7 61 0 0 0 62 0 0 0 63 2 0 0 64 11 0 0 65 2 0 0 66 0 1 0 67 0 1 0 68 0 1 0 69 1 1 0 8

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Morpho Species Primary Agricultural Open 70 1 0 0 71 1 0 0 72 0 0 0 73 0 0 1 74 0 0 1 75 0 0 1 76 0 2 0 77 1 3 0 78 0 1 0 79 0 2 0 80 0 1 0 81 0 2 0 82 0 1 0 83 6 1 0 84 1 0 0 85 1 0 0 86 1 0 0 87 0 1 0 88 0 1 0 89 0 1 0 90 0 0 1 91 0 0 1 92 0 0 1 93 0 0 7 93 0 0 7 93 0 0 7 9