frequency and distribution of fruit-feeding butterflies in a costa ...€¦ · duong and junger,...

Duong and Junger, 2015 1

Frequency and Distribution of Fruit-Feeding Butterflies in a

Costa Rican Cloud Forest: From Grazeland to Primary Forest

Gabrielle C. Duong & Ashley J. Junger

Abstract

To determine whether the frequency and distribution of fruit-feeding Nymphalid butterflies change through a habitat’s succession from pasture land to primary forest, as well as to determine whether Cloudbridge’s reforestation efforts were expediting the growth of primary forest butterfly populations, a community of fruit-feeding Nymphalid butterflies was sampled daily for 6 weeks by trapping 174 individuals of 27 species in the understory of four habitat types: primary forest, natural secondary regrowth forest, planted secondary regrowth forest, and pastureland. We found the whole study area had a species evenness of 0.5, and a Simpson’s Index of Diversity of 0.88. Planted regrowth had the highest species richness (20), diversity index (0.9), and a relatively high evenness (0.58). Therefore, of the successional habitat types studied, planted regrowth is the most diverse and rich, indicating that the process of planting climax species in secondary forests improves community diversity and richness. This increase in community diversity and richness may lead to higher diversity and richness in the climax community. We also conclude that a large number of species are being found out of their natural elevation range, which could indicate that butterflies in this area are experiencing the effects of climate change. Key words: nymphalidae, butterfly, species abundance distribution, species richness, environmental monitoring, habitat disturbance, tropical, conservation.

INTRODUCTION

Natural habitats in the tropics continue to be globally threatened by habitat loss and climate change, leading to the massive loss of species. Remediation efforts are being undertaken globally in an effort to reduce and reverse the effects of habitat loss and climate change. In order to focus these efforts and to determine their effects on biological diversity, reliable monitoring programs that assess changes in biodiversity and ecosystem function are needed. The choice of organism investigated is crucial to this process due to overall lack of funds and available expertise.

Trapping butterflies is often the method of choice in tropical forests (Aduse-Poku et al., 2012). Advantages of using butterflies (Lepidoptera) as a target species include: their relatively large size, colorful appearance, relative ease of identification to species level, their presence in all terrestrial

habitats, and sensitivity to microclimate heterogeneity and disturbance (New, 1997; DeVries et al., 1997). Butterflies are the best-known group of insects (DeVries et al., 1997), giving them great potential to provide understanding of insect diversity and conservation. The study of fruit feeding butterflies has additional advantages, including their ability to be vigorously sampled with the use of fruit-baited traps. Therefore, fruit-feeding butterflies provide a standard means for comparing species diversity within and among tropical insect communities (DeVries et al., 2012).

Bait trapping is an inherently biased method for assessing butterfly fauna. Issues include: some butterflies are never captured in traps, and some butterflies are more strongly attracted than others, thus relative abundances captured do not necessarily reflect the relative


abundances of fruit feeding species in the region (Hughes et al., 1998). Despite these drawbacks, bait trapping provides the most effective and efficient method for monitoring changes in species abundances, and measuring diversity of tropical butterfly communities.

Reforestation is an essential step in restoring forest health. Monitoring and assessment of the effects of reforestation on communities within remediated areas is essential to gaining an understanding of its short- and long-term effects. Few studies investigate the changes in species abundance and diversity through various levels of succession in tropical forests. Most studies in this area focus on the differences between disturbed and undisturbed habitats. Disturbed habitats have been found to have higher species richness and more unique species (DeVries et al., 1997). Additionally, vertical stratification is reduced in disturbed forests, trapping canopy species in the understory, leading to overestimates of species richness in understory trapping in disturbed areas (DeVries & Walla, 2001; Fermon et al., 2005; Aduse-Poku et al., 2012). Rapid monitoring programs will allow assessments of the changes in diversity and abundance within different stages of succession, allowing for more effective and focused remediation efforts.

Between the 1940s and 1980s deforestation in Costa Rica was caused by government-sponsored land colonization schemes, expansion of the agricultural frontier, cattle ranching to support the beef

industry, and both legal and illegal timbering (Borges-Méndez, 2008). During this period the national area covered with forests dropped from about 70% to about 10% (United States Agency for International Development [USAID], 1996). In fact, between 1950 and 1994, the pace of deforestation in Costa Rica was one of the fastest in the western hemisphere, with a decrease of 40,000-50,000 hectares annually (Watson et al., 1998; Borges-Méndez, 2008). Given this rapid and drastic loss of forested areas throughout the country, reforestation programs will be essential to restoring the country’s former biodiversity.

Costa Rican forests have sufficiently diverse fruit-feeding butterfly fauna to warrant their use as target organisms for monitoring changes in biodiversity. There are approximately 543 butterfly species present in Costa Rica (DeVries, 1987). Of these, at least 40% feed exclusively upon rotting fruits as adults (DeVries, 1987).

The aim of this study is to quantify the differences in diversity and abundance of fruit-feeding butterflies within habitats at different stages of succession. We performed a butterfly trapping study on the Cloudbridge Nature reserve in Costa Rica during the onset of the rainy season, studying four habitat types (grazeland, natural regrowth, planted regrowth, and primary forest). In each of these habitat types three traps were established in the understory.

MATERIALS AND METHODS

Study Site

This research was conducted at the Chirripó Cloudbridge Nature Reserve, San Isidro de General, south central Costa Rica. Located in a cloud forest on one of the tallest mountains of Central America, Cloudbridge is a 700 acre nature reserve on the northern end of one of the most important biological zones of all Central America, and lies within a designated “biological hot spot” on the Meso-American Biological Corridor. Cloudbridge is part of an area of forested land that includes

over a million hectares spanning northern Costa Rica and southern Panama. Together with the adjoining La Amistad International Park, Chirripó National Park is comprised of the largest unspoiled forest in the country.

Cloudbridge started off as privately owned land in 2002, owned by Ian Giddy and Genevieve (Jenny) Giddy, who made the first of many subsequent purchases of cattle farms bordering the Chirripó National Park to impede the appalling denuding and erosive effects that cattle grazing has had on the land.


Since then, their reserve has grown to encompass 700 acres of reclaimed pasture land and is used to re-build a corridor where deforestation has left a gap between the large Chirripó National Park, and the smaller nature reserve of 4,000 acres on the other side of the river. Our study was conducted within a contiguous patch of the Cloudbridge reserve that formed a disturbance gradient composed of 3 contiguous habitat types: primary forest, natural secondary regrowth forest, and planted secondary regrowth forest, as well as the pasture of a nearby cow farm. Trap Sites

Each habitat type was fitted with 3 butterfly traps, whose locations were selected based on elevation, walking distance, and accessibility (Appendix B). In steeper hiking areas, such as in the primary forest (PF) and planted regrowth (PR) forest, traps were spaced, on average, 117 meters apart in elevation. In flatter and lower areas, such as on the grazeland (GL) and along the natural regrowth (NR) forest, traps were spaced, on average, 14 meters apart in elevation. All latitude, longitude, and elevation measurements were taken using GIS with an accuracy of ± 15 meters. Primary Forest Also known as an old-growth forest, a primary forest is one that has remained essentially unmodified by human activity. Additionally, they are generally comprised of climax species, a composition achieved as a result of unrestrained ecological processes. We chose to place our traps along the primary forest areas of the El Jilguero and El Hectare Trails. Natural Regrowth Forest A natural regrowth, or secondary, forest is defined here as one that has naturally re-grown after a major disruption, natural or man-made, such as the deforestation efforts in Costa Rica between the 1940’s and 1980’s. A secondary forest has regrown for a long enough period of time such that the effects of the disturbance are no longer evident. It is distinguished from a primary forest by species composition; a secondary regrowth forest has not yet reached a climax community.

We chose to place our traps along the natural regrowth areas of the River Trail. Trap 1 was located near the bench by the river, and next to a very small, narrow stream that crossed over the trail. Traps 2 and 3 along the River Trail were farther from the river and did not have any streams of water flowing past them. Trap 2 was placed in an open pocket of forest under a tree surrounded by plants that produced fruit. Trap 3 was placed in a more open section of forest under a tree; no fruit-growing species were observed. Planted Regrowth Forest A Planted regrowth, or secondary, forest is defined here as one that, in addition to having naturally regrown after a major disturbance, is replenished through reforestation efforts. During reforestation, climax species are manually planted to facilitate the transition of a secondary forest into what more closely resembles a primary forest. We chose to place our traps along the planted regrowth areas of the El Jilguero Trail. Grazeland

A grazeland is a grassy field suitable for grazing by livestock. In our study, the grazeland is the state of disturbance from which secondary regrowth forests are recovering. We chose to utilize farmer Marcos Romero’s land, located just down the road from the Cloudbridge Nature Reserve. The grazeland shared one of its borders with a coffee bean plantation; it is along this border that some of our traps were located.

Trap number 1 was located by the road, just within the gate that fenced off the grazeland, and was suspended from a lime tree. Trap number 2 was located farther into the grazeland and was suspended from a tree located just past a narrow stream that ran through the land. Trap number 3 was suspended from a tree located at the top of the hill. Study Community: Fruit-feeding Nymphalids Adult butterflies can be divided into two main feeding guilds. One guild obtains all nutritional requirements by feeding on the nectar of flowers; this guild includes most species of Papilonidae, Pieridae, Lycaenidae, Riodinidae, and some groups within


Nymphalidae. (DeVries, Murray, & Lande, 1997). The other guild meets all nutritional requirements by feeding on the juices of rotting fruits or plant sap; this guild is comprised of certain subfamilies of the Nymphalidae, such as Charaxinae, Morphinae, Brassolinae, Satyrinae, and Nymphalinae (DeVries et al, 1997). It is this second butterfly guild, which we call fruit-feeding nymphalids, that can be easily baited and trapped by exploiting their feeding habits and escape mechanism. For completeness, we note that some species in the subfamily Ithomiinae, Limenitidinae, and Apaturinae can occasionally be found in fruit-traps, although they typically feed on flower nectar. Additionally, some species in the Hespieriidae family of skippers can also be occasionally found in fruit-traps; however, because they are not strictly butterflies, they are excluded from the data analyzed here. Butterfly Trap Design and Construction

Loosely following the trap dimensions and construction instructions outlined by George Austin and Thomas Riley, 1995, we constructed our traps to be approximately 80 cm tall and 13 inches in diameter, with the base hanging 1 inch below the bottom of the trap netting. Each trap was constructed using the following materials and procedures:

• Two wire hoops: 13-inches in diameter. Bend wire into circle and connect the ends by hooking them together. Clamp the loop shut with pliers.

• For body of the trap, cut a piece of mosquito netting 42-inches wide and 34-inches tall; sew ends together along the 42-inch edges to produce a “tube” of netting. Then sew one end of the tube such that this end is 2 inches narrower in diameter with respect to the wire hoops you just made. (Illustration 1.B)

• For the top of the trap, cut a sheet of plastic tarp approximately 4 inches larger in diameter than the wire hoops you made. Wrap and tape this over the wire hoop. (Illustration 1.B)

A

B

C

D

Illustration 1. Trap design and construction


• For the top of the trap, cut a sheet of plastic tarp approximately 4 inches larger in diameter than the wire hoops you made. Wrap and tape this over the wire hoop. (Illustration 1.B)

• Fit the plastic covered hoop into the narrow end of the tube and secure in place by placing two 30-inch lengths of wire in an “x” pattern under the plastic-covered hoop; the wires should support the plastic-covered hoop, and the plastic-covered hoop should support the body of the netting. The ends of the wire should meet near the center of the upper side of the plastic-covered hoop. Fashion the ends into a hoop or hook, to which you will tie the suspending rope. Plastic across the top should be flat. (Illustration 1.C)

• For trap base, sew the second wire hoop directly onto the bottom end of the tube. When hung, hoops should lay parallel to one another and to the ground. (Illustration 1.A)

• Attach four hooks fashioned out of metal wire to the base, leaving approximately 1 inch of space between the base and the bottom edge of trap netting (Illustration 1.A).

• Punch four holes into a plastic plate. This will serve as the trap base.

• Tape a bait container in the center of the trap base, and hang the base to the trap via the four hooks. For bait containers, we repurposed cream cheese containers and tuna cans.

Field Methods Within the study areas, each of the

four habitat types was fitted with three traps, providing a total of twelve traps. These understory traps were suspended such that the bottom of the traps were approximately 1.3 meters above the ground, with the exception of the pastureland traps, whose bottoms were approximately 1.8 meters above the ground to keep the curious residential cows from destroying them. Traps in the pastureland were suspended from thin ropes run over branches of an emergent tree, such that the traps could be raised and lowered from the ground without disturbance. The free end of the rope was

fastened to a branch at least 2 meters high with all excess rope either wrapped around the branch or tucked away to prevent the cows from chewing through the ropes. All other traps were suspended from lower tree branches and could be serviced directly.

Each Monday morning, traps were baited with rotting bananas obtained free-of-charge from the local village store. Bananas were sprinkled with 1 teaspoon of dry yeast and 1 teaspoon of sugar, mixed and mashed, and fermented for 24 hours in one large container prior to use. On the last day of the weekly four-day sampling period, bait was removed from all traps, and traps were tied shut over the weekend. New bait was made prior to the subsequent sampling interval, and this protocol repeated throughout the study, which extended from 15 June 2015 to 24 July 2015.

When checking each trap, we first cinched the middle section shut with string to prevent any butterflies from escaping. Trapped butterflies were then individually extracted via a plastic bag and photographed within the bag. Then, butterflies were handled so they could be photographed outside of the bag; both dorsal and ventral sides were photographed for identification. Butterflies were then released to the area in which they were found. Information was first recorded in a field notebook, and later transferred to a spreadsheet to perform data analyses.

All butterflies were identified using the DeVries butterfly field book, which follows the more conservative estimates of Ackery, is based upon the work of Ehrlich, and represents a widely used, functional classification of nymphalid subfamilies (DeVries et al, 1997). Bait Recipes Different butterfly species use different kinds of food sources to obtain the nutrients they require to survive. Some species are attracted to what is called stinky bait, which includes rotting fish and other carrion. Nymphalids, however, are attracted to sweet bait, which includes overripe or rotting bananas, mangos, and other fruit. More specifically, Nymphalid butterflies are attracted to the alcohol in sweet baits. We tried


two different sweet bait recipes: (1) Beer bait and (2) Yeast bait.

1. Beer Bait o 4 overripe/rotting bananas,

peeled and mashed o Add 1 tablespoon sugar o Add ⅓ cup beer o Mix well o Let ferment for 7 days

2. Yeast Bait o 4 overripe/rotting bananas,

peeled and mashed o Add 1 teaspoon sugar

o Add 1 teaspoon yeast o Mix well o Let ferment for 24 hours

On June 26th, 11 days into our study, we switched from using the beer bait to using the yeast bait for a few reasons: it was easier to prepare, cheaper, and took less time to ferment. We also found that the yeast bait attracted slightly more butterflies than the beer bait, as we started finding butterflies in traps in which we had never before found butterflies.

RESULTS

Over the course of 27 data collection

days, 174 individual butterflies were collected (Figure 1). These individuals were represented by 27 different species. All species captured were members of the Nympalidae family; 44.4% of species captured belonged to the Satyrinae subfamily, followed by the subfamily Charaxinae (22.2%). Other subfamilies captured include: Brassolinae (14.81%), Nymphaline (7.4%), Ithomiinae (3.7%), Opoptera (3.7%), and Pycina (3.7%). Of the Satyrinae butterflies captured, 36.6% were Cissia satyrina, which represented 25.28% of all individuals captured.

Planted Regrowth had a species evenness of 0.58, and a Simpson’s Index of Diversity of 0.9. Of the total individuals captured 44.8% were found in planted regrowth, and 14.81% of species captured were found there exclusively (Figure 2). Primary Forest had a species evenness of 0.58, and a Simpson’s Index of Diversity of 0.87. Of the total number of individuals captured 25.9% were found in primary forest, and 7.4% of species captured were found there exclusively (Figure 2).

Natural Regrowth had a species evenness of 0.48, and a Simpson’s Index of Diversity of 0.76. Of the total number of individuals captured 26.4% were found in

natural regrowth, and 11.11% of species captured were found there exclusively (Figure 2).

Grazeland had a species evenness of 0.82, and a Simpson’s Index of Diversity of 0.9. Of the total number of individuals captured 2.9% were found on grazeland. No species were found there exclusively (Figure 2).

The whole study area had a species evenness of 0.5, and a Simpson’s Index of Diversity of 0.88. With respect to relative abundance, 33.3% of species were represented by 1 individual, and 70.37% of species were represented by 5 individuals or fewer (Figure 3). Of the total species captured 11.11% were found in all habitat types (Figure 2).

Figure 1. Distribution of individuals captured in each habitat type


Of the 27 species captured 10 (37%)

were found at least once between 30 m and 819 m out of their elevation range as specified by DeVries in The Butterflies of Costa Rica

and Their Natural History: Volume I. All butterflies found out of their range were found above their specified range; 72.5% were found out of their elevation range by 100 m or more at least once.

Figure 2. A Venn diagram showing the overlap of species in the habitat types

Figure 3. Relative abundance (A) Overall (B) Planted Regrowth (C) Primary Forest (D) Natural Regrowth (E) Grazeland


The number of individuals captured steadily increased as the study continued. 56% of all individuals captured were captured in the last two weeks of the study (Figure 4). In

line with this, as the study continued, the number of unique species captured increased (Figure 5).

DISCUSSION

As with any trapping study, sampling

bias because of microenvironmental variance among traps, as well as because of variance among species in attraction to baits, may have been a source of error. Pooling replicate traps can reduce individual trap variance; however, species attraction to bait can be addressed only by intensive mark/recapture studies and/or by natural history observations (DeVries et al., 1997).

We found that the grazeland had the highest species evenness and the highest diversity index; however, it has the lowest species richness. This is because few species were found in the grazeland, but these species were each represented by only 1 or 2 individuals, making it very even and diverse. We can conclude that the grazeland provides habitat for a small number of highly varied species. This suggests that butterflies may use grazeland as a transitory habitat and that it may act as a habitat corridor. Thereby, grazelands allow butterflies to travel between more suitable fragmented habitats.

The planted regrowth had the highest species richness, highest diversity index, and a relatively high evenness rating. This suggests that of the habitat types studied the planted regrowth forests host the highest number of individuals and the most diverse butterfly population. There are a few explanations as to why planted regrowth is more diverse and rich

than natural regrowth. Firstly, planted regrowth is cleared of invasive species, such as bracken, which shade out and compete with other secondary species as part of the planting process. This clearing may provide more habitat for butterfly host plants that would not have been able to grow otherwise. Secondly, the clearing of the planted regrowth habitat reduces the number of plants shading the habitat. Butterflies often prefer areas that are sunny and warm, so this may explain the butterfly’s higher affinity to planted regrowth habitats. Thirdly, the elimination of bushy and invasive plant species may reduce habitat for organisms that compete with or parasitize butterfly species, giving butterflies in the planted regrowth area a competitive advantage. From the data collected during this study we can conclude that the process of planting trees in secondary forests encourages an increase in butterfly richness and diversity. This suggests that planting secondary forests not only aids in speeding up the reforestation process, but also improves the insect diversity in the area. Further studies are needed to pinpoint exactly how the process of planting improves richness and diversity. All habitat types showed relatively low abundance, as 70.37% of species are represented by 5 individuals or fewer. This low abundance has two possible explanations: (i) many butterfly species undergo seasonal

Figure 4. Number of individuals captured per week Figure 5. Species accumulation


migrations (DeVries & Walla, 2001), which could have caused more species to be present at low numbers as they travel, (ii) the short study period was not sufficient enough to capture representative numbers of individuals from each species, and with a continuation of the study relative abundance could increase. Despite their low relative abundance, the species that we did capture appear to provide a good representation of the Nymphalidae species. 44.4% of the species captured were from the subfamily Satyrinae. The Satyrinae subfamily represents nearly half of Nymphalidae diversity. Therefore, the species we captured appear to be in proportion to the overall species present. This study was conducted at the close of the dry season and the onset of the rainy season. The first three weeks of the study were relatively dry, receiving little rainfall sporadically. The second three weeks saw the onset of the rainy season, with heavy rains almost every day. This change in weather patterns correlates to a drastic increase in the number and species of butterflies captured. 70.11% of all individuals captured were trapped in the last three weeks of the study, with 56% of all individuals captured trapped in the last two weeks alone. This is consistent with the idea that a seasonal correlation with rainfall is typical of tropical insect communities (Wolda, 1978, 1992; Kato et al., 1995; Novoty & Basset, 1998). This seasonal shift in population size has two possible explanations: (i) butterflies typically undergo seasonal, multi-species migrations at this time of year (DeVries & Walla, 2001), causing more species to be present than would normally be found at other times of year, and (ii) the availability of natural fruit sources may cause differential attraction of butterflies to banana-baited traps (DeVries & Walla, 2001), causing butterflies to be less picky about their food source and more likely to feed from the traps. Further studies that span both the rainy season and dry season and specifically investigate the seasonal components of biodiversity should be undertaken. We found that a large number of the species captured (37%) were found at least once higher than their natural elevation range,

with 72.5% found out of their range by 100 m or more at least once. This large shift in species to higher habitats could indicate that climate change is affecting tropical butterfly species’ ranges. Warming of habitats, along with the affects of shifts in cloud density and precipitation patterns may be forcing butterfly species into higher elevation habitats to combat these changes. This shift represents a large concern for tropical insect communities, as habitat types typically change drastically with increases in elevation. Butterflies may find they are rapidly displaced from suitable habitat, and higher elevation habitats that are suitably wet and cool do not contain suitable plant species. This shift has the potential to cause a drastic decrease in the abundance and diversity of butterfly populations in tropical areas. From this study we can conclude that of the successional habitat types studied, planted regrowth is the most diverse and rich, indicating that the process of planting forests improves community diversity and richness. This increase in community diversity and richness may lead to higher diversity and richness in the climax community. We can also conclude that a large number of species are being found out of their natural elevation range, which could indicate that butterflies in this area are experiencing the affects of climate change, and that, if remediation efforts are not undertaken soon, then a drastic decrease in butterfly populations and diversity may ensue. Improvements and Further Studies

An area this study needs improvement in is studying butterflies on the grazeland. Because grazeland traps were more exposed to the sun, rain, and wind, we frequently found these traps and/or the bait in an ineffective state: dried out, diluted, or dumped out by the wind. We suggest weighing down the base of the trap with a handful of gravel to prevent the wind from tipping the bait out, or using heavier material for the base of the trap. Perhaps stirring in a bit of water to dried out bait may restore the bait to a more suitable condition, and carrying extra bait may be worthwhile in case of diluted bait or an empty bait dish. Further studies may also consider


studying butterfly frequency and diversity on farm land instead of grazeland, as farm land lacks animals that tamper with traps and has more shade to prevent desiccation of bait.

Our study methods provide estimates of species abundance using only the numbers of adult butterflies caught in our traps, but provides no information on the distribution of host plants, roosting areas, courtship sites, or other life history components. Further studies should investigate life history components in correlation with diversity and frequency. Additionally, the type of bait we selected mostly excludes adult butterflies that do not belong to the family Nymphalidae, as we used a sweet bait. Further studies may consider incorporating different types of baits to attract a wider variety of butterfly families.

A number of butterflies, particularly of the larger variety, were excluded from our data because they escaped from our trap and were thus unable to be identified. Many times, these larger butterflies were found sitting

directly on the bait dish and, when approached, flew down and out of the trap. One possible modification to the trap, such that the base can be pulled up and the bottom of the trap sealed from a distance, can prevent such losses. Or, perhaps narrowing the distance between the bottom of the trap, and the base and bait dish of the trap, from 1 inch to less than 1 inch may also help to prevent the loss of specimens; however, such a modification may also inhibit larger butterflies from entering the trap entirely. Further studies should consider the trade off between including larger butterfly species and the rate of butterfly escape from the traps. This study focused on butterfly diversity and abundance in habitat understories. Vertical stratification is essential to community structure (DeVries & Walla, 2001). Therefore, further studies should consider investigating the vertical stratification of communities by incorporating canopy traps into their study.

Acknowledgements

This research internship trip was funded by the Hubbard Center for Student Engagement of DePauw University, whose grant funds were used in the purchase of necessary field equipment and supplies. Additionally, this research project was conducted on and made possible by Cloudbridge Nature Reserve, as well as on the pastureland owned by the farmer Marcos Romero, who opened his land for our research and helped to maintain the butterfly traps set on his land. We would also like to thank Cloudbridge manager Frank Spooner for advising us on this study.


References Aduse-Poku, Kwaku, et al. “Spatial And Temporal Variation In Butterfly Biodiversity In A West

African Forest: Lessons For Establishing Efficient Rapid Monitoring Programmes.” African Journal Of Ecology 50.3 (2012): 326-334. Academic Search Premier. Web. 27 July 2015.

Borges-Méndez, Ramón. “Sustainable Development And Participatory Practices In Community Forestry: The Case of FUNDECOR In Costa Rica.” Local Environment 13.4 (2008): 367-383. Academic Search Premier. Web. 27 July 2015.

Devries, Philip J., and Thomas R. Walla. "Species Diversity and Community Structure in Neotropical Fruit-feeding Butterflies." Biological Journal of the Linnean Society 74.1 (2001): 1-15. Web.

Devries, Philip J., Debra Murray, and Russell Lande. "Species Diversity in Vertical, Horizontal, and Temporal Dimensions of a Fruit-feeding Butterfly Community in an Ecuadorian Rainforest."Biological Journal of the Linnean Society 62.3 (1997): 343-64. Web.

DeVries, Philip J. The Butterflies of Costa Rica and Their Natural History. Princeton, NJ: Princeton UP, 1987. Print.

DeVries, P.J., Alexander, L.G., Chacon, I.A. & Fordyce, J.A. (2012) Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. J. Anim. Ecol. 81, 472–482.

Fermon, H., Waltert, M., Vane-Wright, R.I. & Muhlenberg, M. (2005) Forest use and vertical stratification in fruit-feeding butterflies of Sulawesi, Indonesia: impacts for conservation. Biodivers. Conserv. 14, 333–350.

Hughes, Jennifer B., Gretchen C. Daily, and Paul R. Ehrlich. Use of Fruit Bait Traps for Monitoring of Butterflies (Lepidoptera: Nymphalidae). Publication. Stanford: Stanford U Dept. of Biological Sciences, 1998. Print.

Kato M, Inque T, Hamid AA, Nagamitsu T, Merdek MB, Nona AR, Itino T, Yamane S, Yumoto T. 1995. Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Researches on Population Ecology 37: 59-79.

New, T.R. (1997) Are Lepidoptera an effective ‘umbrella group’ for biodiversity conservation? J. Insect Conserv. 1, 5–12.

Novotny V, Basset Y. 1998. Seasonality of sap-sucking insects (Auchenorrhyncha, Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea. Oecologia 115: 514-522.

Rathbone, Sarah. The Lepidoptera Diversity of a Lower Montane Cloud Forest in Costa Rica. Rep. Cloudbridge Nature Reserve, Aug. 2007. Web.

Uehara-Prado, Marcio, Keith Spalding Brown, and André Victor Lucci Freitas. "Species Richness, Composition and Abundance of Fruit-feeding Butterflies in the Brazilian Atlantic Forest: Comparison between a Fragmented and a Continuous Landscape." Global Ecology and Biogeography Global Ecol Biogeography 16.1 (2007): 43-54. Web.

USAID, 1996. PN-ABS-531. Forestry and the environment: Costa Rica case study. Evaluation Highlights 53 Washington DC, USAID.

Wolda H. 1978. Fluctuations in abundance of tropical insects. The American Naturalist 112: 1017-1045.

Wolda H. 1992. Trends in abundance of tropical forest insects. Oecologia 89: 47-52.


APPENDIX Appendix A- Cloudbridge Map with Trap Locations Appendix B- Site and species information APPENDIX A - CLOUDBRIDGE Map with Trap Locations


APPENDIX B - SITES AND SPECIES INFORMATION This is a list of all the sites where research has been conducted, including a list of species found at each site. PF = Primary Forest (El Jilguero/Hectare) PR = Planted Regrowth Secondary Forest (El Jilguero) NR = Natural Regrowth Secondary Forst (Rio) GL = Grazeland (Marco’s pasture) Habitat Type Trap Number Latitude Longitude Elevation (m)

PF 1 09°28'05.1 083°34'27.6 1857

PF 2 09°27'59.0 083°34'17.7 1970

PF 3 09°27'57.1 083°34'12.9 2030

PR 1 09°28'11.9 083°34'39.0 1519

PR 2 09°28'14.6 083°34'44.1 1662 PR 3 09°28'07.8 083°34'32.5 1813

NR 1 09°28'30.9 083°34'06.8 1672

NR 2 09°28'27.6 083°34'11.8 1681

NR 3 09°28'22.8 083°34'15.4 1704

GL 1 09°28'16.9 083°34'53.8 1536 GL 2 09°28'15.9 083°34'53.4 1563

GL 3 09°28'13.9 083°34'52.9 1561 PF 1

Archaeoprepona demophon centralis Cissia renata Cissia satyrina Cyllopsis argentella Dioriste tauropolis Drucina leonata Memphis arginussa eubaena Opoptera staudingeri Opsiphanes cassina chiriquensis Opsiphanes cassina fabricii PF 2

Catonephele chromis godmani Cissia satyrina Drucina leonata Pycina zamba zelys

PF 3

Catonephele chromis godmani Cissia gigas Cissia satyrina Cyllopsis argentella Dioriste tauropolis Drucina leonata Pedaliodes dejecta PR 1

Caligo eurilochus sulanus Cissia satyrina Consul electra Dioriste tauropolis Drucina leonata Megeuptychia antonoe Memphis beatrix Opsiphanes cassina chiriquensis


Smyrna blomfildia datis

PR 2

Archaeoprepona demophon centralis Cissia gigas Cissia satyrina Cissia similis Dioriste tauropolis Drucina leonata Memphis beatrix Memphis glycerium Opsiphanes cassina chiriquensis Pedaliodes dejecta Pronophila timanthes PR 3

Archaeoprepona demophon centralis Cissia gigas Cissia renata Cissia satyrina Cissia satyrina Dioriste tauropolis Drucina leonata Memphis arginussa eubaena Memphis beatrix Memphis pithyusa Opsiphanes cassina chiriquensis Opsiphanes cassina fabricii Pedaliodes dejecta Pedaliodes perperna

NR 1

Cissia satyrina Dioriste cothonides Dioriste tauropolis Memphis beatrix Smyrna blomfildia datis NR 2

Cissia satyrina Cyllopsis argentella Memphis pithyusa Opsiphanes bogotanus Smyrna blomfildia datis NR 3

Cyllopsis argentella Dioriste tauropolis Drucina leonata Greta polissena umbrana Opsiphanes cassina chiriquensis Pronophila timanthes GL 1

Drucina leonata Memphis glycerium Opsiphanes cassina chiriquensis Smyrna blomfildia datis GL 2: zero GL 3: zero

frequency and distribution of fruit-feeding butterflies in a costa ...€¦ · duong and junger,...

Documents