Higher abundance and species richness at lower elevations in Monteverde altitudinal survey on euglossine bee diversity


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Higher abundance and species richness at lower elevations in Monteverde altitudinal survey on euglossine bee diversity

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Higher abundance and species richness at lower elevations in Monteverde altitudinal survey on euglossine bee diversity
Translated Title:
Mayor abundancia y riqueza de especies de abejas euglosinas en las elevaciones más bajas de Monteverde
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Huebner, Liora
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Bees--Behavior ( lcsh )
Abejas--Comportamiento ( lcsh )
Bees ( lcsh )
Abejas ( lcsh )
EAP Spring 2017
EAP Primavera 2017
Costa Rica--Puntarenas--Monteverde Zone
Costa Rica--Puntarenas--Zona de Monteverde
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In many Neotropical areas, Orchid bees are the primary bee pollinators, so knowing their biogeographical and altitudinal distribution in Monteverde, Costa Rica could be useful for understanding ecosystem health. The Orchid bees’ optical uniqueness, large biodiversity and accessibility serve as useful and easily identifiable bioindicators of farm and ecosystem health. The biogeographical distribution of Orchid bees has been thoroughly researched, but there are few scientific papers conducting surveys on their altitudinal distribution. I caught a total of 138 bees from six different species: Euglossa viridissima, Euglossa imperialis, Euglossa mixta, Euglossa maculilabris, Exaerete smaragdina and Eulaema bombiformis using methyl salicylate, cineole and eugenol in four different locations of altitudes ranging from about 1200 m to 1800m. I spent two mornings and three hours each day at Bajo del tigre, the Crandell reserve, la Estación Biológica and the TV towers. The region of lowest elevation had the highest abundance and species richness. I found five species and 66 individuals at Bajo del Tigre and only two species and six individuals at the TV towers. Surprisingly, a site at medium elevation, la Estación Biológica had the highest Shannon diversity due to possessing the most heterogeneous species composition and a presence of four species. Since my results show that bee biodiversity does vary with altitude, they would make useful indicators of ecosystem change over time as climate change causes locations of lower elevations to heat up and become less habitable. ( ,, )
Abstract:
En muchas áreas Neotropicales, las abejas de las orquídeas o euglosinas son los polinizadores primarios de este grupo de insectos. Por lo tanto conocer su distribución biogeográfica y altitudinal en Monteverde, Costa Rica podría ser útil para entender el salud del ecosistema. La singularidad óptica de las abejas euglosinas, su gran biodiversidad y su accesibilidad, les permiten servir como bioindicadores útiles y identificables fáciles de la salud de las granjas y de la salud del ecosistema. La distribución biogeográfica de las abejas de la orquídea ha sido investigada a fondo, pero hay pocos documentos científicos que realizan encuestas sobre su distribución altitudinal. Se capturaron un total de 138 abejas de seis especies diferentes: Euglossa viridissima, Euglossa imperialis, Euglossa mixta, Euglossa maculilabris, Exaerete smaragdina y Eulaema bombiformis usando salicilato de metilo, cineol y eugenol en cuatro ubicaciones diferentes de altitudes de aproximadamente 1200 m a 1800 m. Pasé dos mañanas y tres horas cada día en Bajo del tigre, la reserva de Crandell, la Estación Biológica y las torres de TV. La región de menor elevación tuvo la mayor abundancia y riqueza de especies. Encontré 5 especies y 66 individuos en Bajo del Tigre y sólo dos especies y seis individuos en las torres de TV. Sorprendentemente, un sitio en la elevación media, la Estación Biológica tenía la diversidad más alta del Shannon debido a poseer la composición más heterogénea de la especie y una presencia de cuatro especies. Como mis resultados muestran que las abejas tienen una preferencia altitudes menores. Este grupo de especies pueden resultar indicadores útiles de la salud del ecosistema. El cambio climático podría provocar que a raíz del calentamiento global, estas abejas suban a altitudes mayores como respuesta.
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Student affiliation: Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz
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Euglossine bee Altitudinal Distribution Huebner 1 Higher abundance and species richness at lower elevations in Monteverde Altitudinal Survey on Euglossine bee diversity Liora Huebner Department of Molecular, Cell and Developmental Biology University of California, Santa Cruz EAP Tropical Biology and Conservation Program, Spring 2017 June 10, 2017 ABSTRACT In many neotropical areas, Orchid bees are the primary bee pollinators, so knowing their biogeographical and altitudinal distribution in Monteverde, Costa Rica could be useful for understanding ec osystem health. The Orchid bees' optical uniqueness, large biodiversity and accessibility serve as useful and easily identifiable bioindicators of farm and ecosystem health. The biogeographical distribution of Orchid bees has been thoroughly researched, b ut there are few scientific papers conducting surveys on their altitudinal distribution. I caught a total of 138 bees from six different species: Euglossa viridissima, Euglossa imperialis, Euglossa mixta, Euglossa maculilabris, Exaerete smaragdina and Eul aema bombiformis using methyl salicylate, cineole and eugenol in four different locations of altitudes ranging from about 1200 m to 1800 m. I spent two mornings and three hours each day at Bajo del tigre, the Crandell reserve, la Estacion Biologica and the TV towers. The region of lowest elevation had the highest abundance and species richness. I found five species and 66 individuals at Bajo del Tigre and only two species and six individuals at the TV towers. Surprisingly, a site at medium elevation, la Est acion Biologica had the highest Shannon diversity due to possessing the most heterogenous species composition and a presence of four species. Since my results show that bee biodiversity does vary with altitude, they would make useful indicators of ecosyste m change over time as climate change causes locations of lower elevations to heat up and become less habitable. Mayor abundancia y riqueza de especies de abejas euglosinas en las elevaciones m‡s bajas de Monteverde RESUMEN En muchas ‡reas neotropicales, las abejas de las orqu’deas o euglosinas son los polinizadores primarios de este grupo de insectos. Por lo tanto conocer su distribuci—n biogeogr‡fica y altitudinal en Monteverde, Costa Rica podr’a ser œtil para entender el s alud del ecosistema. La singularidad —ptica de las abejas euglosinas su gran biodiversidad y su accesibilidad, les permiten servir como bioindicadores œtiles y identificables f‡ciles de la salud de las granjas y de la salud del ecosistema. La distribuci—n biogeogr‡fica de las abejas de la orqu’dea ha sido investigada a fondo, pero hay pocos documentos cient’ficos que realizan encuestas sobre su distribuci—n altitudinal. Se capturaron un total de 138 abejas de seis especies diferentes: Euglossa viridissima, Euglossa imperialis, Euglossa mixta, Euglossa maculilabris,

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Euglossine bee Altitudinal Distribution Huebner 2 Exaerete smaragdina y Eulaema bombiformis usando salicilato de metilo, cineol y eugenol en cuatro ubicaciones diferentes de altitudes de aproximadamente 1200 m a 1800 m. PasŽ dos ma–anas y tres h oras cada d’a en Bajo del tigre, la reserva de Crandell, la Estaci—n Biol—gica y las torres de TV. La regi—n de menor elevaci—n tuvo la mayor abundancia y riqueza de especies. EncontrŽ 5 especies y 66 individuos en Bajo del Tigre y s—lo dos especies y seis individuos en las torres de TV. Sorprendentemente, un sitio en la elevaci—n media, la Estaci—n Biologica ten’a la diversidad m‡s alta del Shannon debido a poseer la composici—n m‡s heterogŽnea de la especie y una presencia de cuatro especies. Como mis res ultados muestran que las abej as tienen una preferencia altitudes menores. Este grupo de especies pueden resultar indicadores œt iles de la salud del ecosistema. El cambio clim‡tico podr’a provocar que a ra’z del calentamiento global, estas abejas suban a al titudes mayors como respuesta. INTRODUCTION A critical aspect of ecological restoration and conservation is understanding species distributions and abundance over biogeographical boundaries. In many neotropical forests, the Euglossine tribe comprises the main bee component. Therefore, having knowled ge of their population's distribution is essential for the preservation of their role as pollinators (Roubik and Hanson, 2004). It is predicted that insects will be very important bioindicators of ecosystem changes along the altitudinal gradient as climate change variably affects these regions (Morochz, 2015). For example, global warming will cause many species to migrate to higher altitudes in search of cooler conditions. This has been seen with Grassland Butterflies of the Sierra de Guadarrama, where the average occupancy of elevation increased by about 150 meters over 31 years (Gutierrez, 2005). Euglossine bees are also accurate bio indicators of farm health (Hedstrom, 2005). For example, the number of euglossine bees on organic farms is on average 3 time s higher than on conventional farms. The biogeography of Euglossine bees has been studied latitudinally and grouped into six geographical zones, including Mexico to Nicaragua and Panama to Costa Rica. Despite widespread knowledge of their latitudinal spec ies distribution, little is known about their altitudinal species distribution and abundance in each region. However, research was conducted on the pacific and atlantic slopes of Costa Rica and in San Luis by UCEAP students showing that the bees' biodiver sity is higher at lower elevations (Christie, 2008) The bees' geographical distribution is affected by climate, vegetation and intraspecific and interspecific competition (Roubik and Hanson, 2004). Similar factors could also contribute to species diversi ty and abundance distribution changes across elevation, such as temperature, resources and floral distribution (Uehara Prado, 2006). Costa Rica has 70 species of orchid bees, but their altitudinal distribution is unknown (Roubik and Hanson, 2004). One stu dy determined that species abundance of Eufriesea violacea varies between 700 and 1,100 meters in Pindamonhangaba, Brazil (Uehara Prado, 2006). If one species of orchid bees has a preference, it is likely that other species will exhibit a similar behavior. To pursue this idea further, I did a

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Euglossine bee Altitudinal Distribution Huebner 3 survey of most orchid bee species present in Monteverde between 1,100 and 1,800 meters, providing a biogeographical overview of the tribe Euglossini that is more general than Uehara Prado's research. Monteverde, spec ifically the area between Bajo del Tigre and the TV towers, is an ideal place to conduct a survey on the species distribution of Euglossine bees across the altitudinal gradient because of the steep rise in altitude within a small area. The latitudinal line ar distance between the TV towers an d my area of study in Bajo del T igre is around 3,800 meters while the altitudinal difference in distance was 617 meters. Since altitude changes rapidly relative to latitude between the locations tested, changes in specie s distribution and abundance can be attributed to altitudinal variation and potentially habitat fragmentation instead of latitudinal variation. I addressed: how does Euglossine bee distribution and abundance vary with altitude? METHODS My research was con ducted in Monteverde, Costa Rica between May 18 and May 26, 2017. I spent two mornings doing bee surveys from 7:30 am to 10:30 am for each of the locations. My locations were Bajo del tigre at 1,216 meters, the Crandell Memorial Reserve at 1,378 meters, la Estacion Biologica, at 1,517 meters, and the TV towers at 1,833 meters. Bajo del tigre is a drier variety of forest, called rain shadow forest, while the TV towers, the Crandell Memorial reserve and la Estacion Biologica are cloud forest. I used the attra ctants Cineole, Eugenol and Methyl Salicylate to pipette 0.5 ml of each fragrance on one paper towel sheet hung 1.5 meters from the ground and one meter apart from each other using string. I reapplied with 0.25 ml of fragrance every 30 minutes. I captured bees using a butterfly net and identified them in the field using the book The Orchid bees of Tropical America Biology and Field Guide (Roubik and Hanson, 2004) I marked specimens by painting a dot of white out on their scut el um so that I would not count them twice if re captured. RESULTS A total of 138 bees were captured and identified. Species were found in the genera Euglossa, Eulaema and Exaerete Species richness and abundance at every site My Euglossine bee survey showed that there is a slight shift in the species present and a large shift in the abundance between locations of different altitudes. I found 11 times as many individuals in Bajo del Tigre than TV towers (Table 1 Fig. 1 ). Bajo del Tigre had 5 species pr esent including Euglossa viridissima, Eulaema bombiformis, Euglossa imperialis, Euglossa mixta, Exaerete smaragdina, and Euglossa maculilabris The Crandell reserve had 3 species present, including Euglossa viridissima, Eulaema bombiformis and Euglossa imp erialis La Estacion Biologica had 4 species, including Euglossa viridissima, Eulaema bombiformis, Euglossa imperialis and Euglossa mixta TV towers had 2 species, including Eulaema bombiformis and Exaerete smaragdina (Table 1). Eulaema bombiformis was t he only species

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Euglossine bee Altitudinal Distribution Huebner 4 that I found at every location. I found that two species were specific to one location; I only found Euglossa maculilabris at 1833 m and I only found Exaerete at 1216 meters (Table 1). However, many more mornings of research would have to b e done at the TV towers and Bajo del Tigre to definitively determine this. The Shannon diversities were H= 0.83 at Bajo del Tigre, H= 0.62 at the Crandell Reserve, H=1.01 at la Estacion Biologica and H=0.64 at the TV towers Table 1 : The number of indivi duals per Euglossine bee species present at each location. Bajo del Tigre Crandell Reserve Estacion Biologica TV towers Altitude (m) 1216 1378 1517 1833 Euglossa viridissima 55 37 12 0 Eulaema bombiformis 3 6 4 4 Euglossa imperialis 3 3 1 0 Euglossa mixta 5 0 2 0 Exaerete smaragdina 1 0 0 0 Euglossa maculilabris 0 0 0 2 TOTAL 67 46 19 6

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Euglossine bee Altitudinal Distribution Huebner 5 Fig. 1 : The number of individuals per species present at each location. Altitudinal range of my species compared with the literature According to my results, the guide's altitudinal population limits for Euglossa viridissima, Euglossa maculilabris and Eulaema bombiformis are too low. For example, I found the species Euglossa maculilabris 833 meters hi gher than the guide suggested (T able 2). Table 2: The altitudinal distribution of Orchid bee species I found according to the Orchid bees of tropical America Biology and field guide vs. the distribution I found during my research. Species Published altitudinal range Project's range Euglo ssa viridissima Lowlands 1200 m 1215 m 1517 m Eulaema bombiformis Lowlands 1700 m 1215 m 1833 m Euglossa imperialis Lowlands 1700 m 1216 m 1517 m Euglossa mixta Lowlands 1700 m 1216 m 1517 m Exaerete smaragdina Lowlands 2600 m 1216 m Euglossa maculilabris Lowlands 1000 m 1833 m

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Euglossine bee Altitudinal Distribution Huebner 6 Orchid bee presence varies between open and forested areas There was a surprisingly large disparity in the abundance and richness between the open and forested areas. Five bee species were present in the forested area, whereas only two were present in the open area (Table 3). Also, more than twice as many total individuals were caught in the forested area than in the open area. These locations were very close to each other bio geographically and only one meter apar t in altitude (Table 3). The only environmental factors that varied between the two locations is that the open area had more wind and sun and was not under tree cover. Table 3: Number of individuals of each species in two different habitats within the sam e reserve: a sunny, open, windy lookout spot and a forested area. Bajo del Tigre Euglossa viridissima Eulaema bombiformis Euglossa imperialis Euglossa mixta Exaerete smaragdina Euglossa maculilabris TOTAL Forested 35 3 3 3 1 0 45 Open 20 0 0 2 0 0 22 DISCUSSION Species richness and abundance at every site A previous UCEAP study on Euglossine bee biodiversity was conducted in San Luis, Costa Rica which is only a couple miles away from the sites I sampled. 13 species of orchid bees were found with an approximate Shannon diversity index H= 2.04 between 1,100 and 1240 meters (Asarian, 1999). In my study, at an elevation of 1517 meters, H= 1.01 and at 1833 m, H= 0.64. Comparing my diversities of highest elevation with Asarian's data gives some indication that regions of low elevation have higher diversity than higher regions when comparing similar habitats. Also, at all of my sites combined, I was able to find six species total, whereas 13 species were found in San Luis. Since San Luis is only about 100 me ters lower than Bajo del Tigre and seven more species were found in San Luis, it is unlikely that altitude was the only contributing factor. Forest fragmentation, such as roads separating habitats, types of forest and time sampling was also likely a factor The relatively similar species composition coincides with the short distance between my and Asarian's sampling locations. In San Luis, the most common species was Euglossa imperialis and Euglossa viridissima was the second most common. Furthermore, in Mo nteverde I found Euglossa viridissima to be the most common species and Euglossa imperialis to be the third most common species. There is a limitation to comparing my data with Asarian's data because he performed his tests 18 years ago and did not compare species along an altitudinal gradient within San Luis. It is more accurate to compare my results with an elevational study of one region at a certain time. Another UCEAP student found higher abundance and richness, or number of species in low regions when she measured eight species at 800 m and one species at 1450 m along the pacific

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Euglossine bee Altitudinal Distribution Huebner 7 slope of the Tilaran mountains(Christie, 2008). T his pattern is apparent not just in tropical regions but temperate regions as well. When the species distribution of bees was tested along the altitudinal gradient in the German Alps, only seven species were found above 1500 m and 34 species were found bel ow 1000 m (Hoiss, 2012). Christie also found that Euglossa imperialis and Euglossa viridissima were in the top three most abundant species on the Pacific slope. Other species we both found are Euglossa mixta and Exaerete smaragdina It is evident that alt itude is correlated with species distribution when comparing my own data from the elevational extremes in Table 1. In Bajo del Tigre, 5 species and 66 individuals were found and only two species and six individuals at the TV towers. Despite there being 11 times as many individuals in Bajo del Tigre than TV towers, Bajo del tigre had a Shannon diversities that was only a 0.19 higher than that of the TV towers. I expected that the Shannon diversities would increase linearly with an increase in elevation but this was not the case. The Shannon diversities show that there was higher diversity at la Estacion Biologica (H=1.01) than at Bajo del Tigre (H=0.83), even though the lower elevation had more than three times as many individuals and 1 more species present. This was a species specific to Bajo del Tigre, Exaerete smaragdina (Table 1). These unexpected Shannon diversities are explained by the relative abundance of species; my sampling from 1517 meters and 1833 meters was much more heterogenous than my sampling from 1216 m. A more heterogenous population is one with similar abundances of the different species. Specifically, at 1216 meters 82% of the population was comprised of Euglossa viridissima whereas at 1517 meters only 63% of the population was comprised o f E. viridissima The Shannon diversity preferentially measures for heterogeneity as an indicator of biodiversity, rather than species richness and total population number. There are many potential ecological causes for differential biodiversity and abun dance along the altitudinal gradient, such as temperature, radiation, precipitation, wind and niche breadth (Hodkinson, 2005). Temperature usually decreases by about six degrees celsius for every 1000 meters of ascent. Short wave radiation, wind speed and precipitation increases with altitude. This can lead to nutrient leaching where rainfall rates are high. The atmospheric partial pressure decreases with an increase in elevation, which can affect flight performance and slow down energy processing in insect s. Orchid bees are species specifically dependent on orchids. They harvest nectar, pollen and perfumes and consequently the bees' distribution is affected by the biogeographical and elevational spread of orchids. I could not find data on altitudinal orch id diversity in Costa Rica but studies have been done about this around the world. In one study in Nepal, no correlation between species richness and elevation was found between 900 m and 2500 m (Rai,2015). Alternatively, in Yunnan, China, a bell curve of species richness along the altitudinal gradient was found, with the highest species richness at medium elevations (Zhang, 2015). Zhang deduced that the mid domain effect and climate were two of the largest contributing factors to this gradient. A study fro m Colombia agrees that orchid distribution is dependent on climate and studies from Peru, Venezuela and Colombia predict that due to climate change there will be an increase in altitudinal distribution of 378 m by 2050 for 12 focal species of orchids (Rein a

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Euglossine bee Altitudinal Distribution Huebner 8 Rodriguez, 2017). If this pattern is true for species that Orchid bees pollinate then we can also predict that bee populations would shift upwards in altitude as well. In Reunion island, there was a decrease of orchid species with an increase in altitude and a large difference in species composition between low and high regions (Jacquemyn, 2006). If Reunion island's orchid distribution reflected that of Monteverde's, I would not have seen such similar species compositions among my sites. Orchid bee specie s turnover would have been higher, since orchid preferences are species specific (Roubik and Hanson, 2004). Even though altitudinal patterns of orchid richness have been observed around the world, there are many contradicting patterns of distribution and t here is no such information about the orchid species pollinated by orchid bees in Monteverde and therefore I cannot deduce how orchid distribution affects the range of the bees I sampled. Altitudinal range of my species compared with the literature The Orchid Bees of Tropical America Biology and Field guide is one of the only guides for identifying and understanding Orchid bee. The altitudinal distribution it depicts for three out of the six species I identified is different than the altitudinal range I observed. According to my results, the guide's altitudinal population limits for Euglossa viridissima, Euglossa maculilabris and Eulaema bombiformis are too low (Table 2). This shows that either the authors of this book simply did not analyze the altitudin al distribution of these species thoroughly enough or that due to environmental changes, such as climate change, bees have migrated to higher elevations since the publishing of this book 21 years ago. For example, a study from Colorado concluded that clima te change caused an average altitudinal increase of 317 meters for queen and worker Bumblebees between the years 1974 and 2007 (Pyke, 2016). It is important to know what species are present at which elevations now so that in the future the same studies can be continued in order to measure ecosystem health and changes over time. Understanding the biogeographical and altitudinal distribution of bees is important for maintaining their population levels. Bees, particularly Orchid bees in tropical rainforests ar e significant contributors to ecosystem diversity since they are the main pollinators of many plants (Morochz, 2015). It is important to monitor Euglossine population levels and their overall distributions closely since they are likely to change in the fut ure with current orchid extinction rates being 1,000 times higher than background rates (Reina Rodriguez, 2017, Swarts, 2009). Orchid bee presence varies between open and forested areas When taking samples from the same biogeographical region it is impor tant to choose locations with the same environmental conditions. A previous study discovered that the abundance of many species is lower in cleared areas than forested areas and that species biodiversity is directly proportional to forest fragment size eve n if the spaces between fragments are very narrow (Powell and Powell, 1987). In Powell's study, Eulaema bombiformis was not affected by fragment size, which may explain why I found this species in all the habitats I surveyed. I sampled two different spots in Bajo del Tigre and found a much higher abundance of

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Euglossine bee Altitudinal Distribution Huebner 9 orchid bees in the completely forested area than in the open area (Table 3). The opening was small and still within the depths of the forest but it allowed for much more wind and sun. Perhaps in the op en area the bees had trouble finding the origin of the scent due to the strong wind or due to behavioral preferences, never venture away from under tree cover. It is important to note the huge difference in abundance and species between these areas, becaus e it may have skewed my results. If I had taken data in the forested area twice instead of in the open area once, my Shannon diversity for the lowest elevation would have most likely been higher. I would have captured more bees in the forested area on day two and potentially found more species as well. This change in methods has likely resulted in a greater difference between high and low elevational biodiversities. This more consistent method would have obtained a more accurate estimate of the biodiversity of orchid bees, because every other region I surveyed was within the forest and not in a clearing. According to my results, Euglossine bee biodiversity is specific to altitude in Monteverde and changes over a range of 617 meters, with more species and mo re individuals present at lower elevations Observing the changes of their altitudinal biodiversity over time could indicate ecosystem health and orchid abundance and diversity and may help researchers find ways of maintaining this unique group of bee' s p opulation levels. REFERENCES Asarian, J. E. ( 1999). Comparison of Male Euglossine Bee Abundance, Species Richness and Movements in Fragmented and Continuous Forest in San Luis, Costa Rica. UCEAP winter 1999 Christie, J. M. (2008). Euglossine Species Composition at Different Elevations and on Diff erent Slopes of the Tilar‡n Mountains, Costa Rica. UCEAP Fall 2008 Gutierrez, D., Gutierrez, J., Martinez, D., & Agudo, R. (2005). Changes to the elevational limits and extent of species ranges associated with climate change Authors. Ecology Letters 8 : 1138 1146. Hedstrom, I., Harris, J., & Fergus, K. (2006). Euglossine bees as potential Bio indicators of coffee farms: Does forest access, on a seasonal basis, affect abundance? Revista de Biolog’a Tropical 54: 1189 1195 Hodkinson, I. D. (2005). Terrestrial insects along elevation gradients: species and community responses to altitude. Cambridge Philosophical Society 80: 489 513. Hoiss, B., Krauss, J., Potts, S. G., Roberts, S., & Steffan Dewenter, I. (2012). Altitude acts as an

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Euglossine bee Altitudinal Distribution Huebner 10 environmental filter on ph ylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society 279: 4447 4456. Jacquemyn, H., Honnay, O., & Pailler, T. (2006). Range size variation, nestedness and species turnover of orchid species along an altitudina l gradient on Reunion Island: Implications for conservation. Biological Conservation 136: 388 397. Jacquemyn, H., Micheneau, C., Roberts, D. L., & Pailler, T. (2005). Elevational gradients of species diversity, breeding system and floral traits of orchi d species on RÂŽunion Island. Journal of Biogeography 32: 1751 1761. Morochz, C. (2015). Diversity and evolution of wasps and bees along an altitudinal gradient. Nemesio, A., & Silveira, F. A. (2007). Diversity and distribution of orchid bees (Hymenopter a: Apidae) with a revised checklist of species. Neotropical Entomology 36 : 1678 8052. Powell, H., & Powell, G. V. (1987). Population Dynamics of Male Euglossine Bees in Amazonian Forest Fragments. Biotropica 19: 176 179. Pyke, G. H., Thompson, J. D., I nouye, D. W., & Miller, T. J. (2016). Effects of climate change on phenologies and distributions of bumblebees and the plants they visit. Ecosphere 7: 1267 1284. Rai, A. (2015). Orchid Distribution along the Elevational Gradient in Panchase Protected fo rest, Nepal. (Dissertation). Tribhuvan University. (Registration No. 5254912008). Reina Rodriguez, G. A., Rubiano Mejia, J. E., Castro Llanos, F. A., & Soriano, I. (n.d.). Orchid Distribution and Bioclimatic Niches as a strategy to Climate Change in area s of Tropical Dry forest in Colombia. Lankesteriana 17: 17 49. Roubik, D. W., & Hanson, P. E. (2004). Orchid Bees of Tropical America Biology and field guide Santo Domingo, Heredia: Instituto Nacional de Biodiversidad. Swarts, N. D., & Dixon, K. W. (20 09). Terrestrial orchid conservation in the age of extinction. Annals of Botany 104: 543 556. Uehara Prado, M., & Garofalo, C. A. (2006). Small scale elevational variation in the abundance of Eufriesea violacea (Blanchard) (Hymenoptera: Apidae). Neotrop ical Entomology 35 : 1678 8052.

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Euglossine bee Altitudinal Distribution Huebner 11 Zhang, S., Chen, W., Huang, J., Bi, Y., & Yang, X. (2015). Orchid Species Richness along Elevational and Environmental Gradients in Yunnan, China. Plos One 10


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