Diversity and composition of insects in a regenerated premontane tropical forest


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Diversity and composition of insects in a regenerated premontane tropical forest
Translated Title:
Diversidad y composición de insectos en un bosque tropical premontano
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Sanko, Katelyn
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Tropical forests, the richest ecosystems on earth, are rapidly disappearing. This is causing the loss of species at an unprecedented rate. However, there is hope to regain lost biodiversity through the process of forest regeneration. Insects, the most specious class of animals, are concentrated in the tropics. I examined the effects of reforestation on insect species composition and diversity in the canopy and understory of a premontane tropical forest in Monteverde, Costa Rica: La Calandria. I collected insects with flight interception traps and analyzed the composition and diversity of orders and hymenopteran morphospecies. I found that species composition varies with reforestation status and between the forest canopy and understory. Although the species composition is different, I found diversity between less disturbed and regenerated forest to be similar. ( , )
Abstract:
Los bosques tropicales son los ecosistemas más ricos de la tierra, pero están desapareciendo rápidamente. Esto está causando una pérdida de especies a un ritmo sin precedentes. Sin embargo, hay esperanza de recuperar la biodiversidad perdida a través del proceso de regeneración de los bosques. Los insectos, la clase más especiosa de animales, se concentran en los trópicos. Examiné los efectos de la reforestación en la composición y diversidad de las especies de insectos en el dosel y el sotobosque de un bosque tropical premontano en Monteverde, Costa Rica: La Calandria. Recolecté insectos con trampas de intercepción de vuelo y analicé la composición y diversidad de órdenes y de morfospecies de himenópteros. Descubrí que la composición de las especies varía según el estado de reforestación y entre el dosel del bosque y el sotobosque. Aunque la composición de las especies es diferente, encontré que la diversidad entre bosques poco perturbados y regenerados es similar.
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Student affiliation : Department of Environmental Science, Policy and Management, College of Natural Resources; University of California, Berkeley
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Monteverde Institute
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Monteverde Institute
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Diversity and Composition of Insects in a Regenerated Premontane Tropical Forest Katelyn A. Sanko Department of Environmental Science, Policy and Management, College of Natural Resources Univ ersity of California, Berkeley UCEAP Tr opical Biology and Conservation Spring 2019 7 June 2019 ABSTRACT Tropical forests, the richest ecosystems on earth, are rapidly disappearing. This is causing the loss of species at an unprecedented rate. However, there is hope to regain lost biodiversity through the proc ess of forest regeneration. Insects, the most specious class of animals, are concentrated in the tropics. I examined the effects of reforestation on insect species composition and diversity in the canopy and understory of a premontane tropical forest in Monteverde, Costa Rica : La Calandria. I collected insects with flight interception traps and analyzed the composition and diversity of orders and hymenopteran morphospecies. I found that species composition varies with reforestation status and between the fo rest canopy and understory. Although the species composition is differe nt, I found diversity between less disturbed and regenerated forest to be similar. Diversidad y composicin de insectos en un bosque tropical premontano RESUMEN Los bosques tropicales son los ecosistemas ms ricos de la tierra, pero estn desapareciendo rpidamente. Esto est causando una prdida de especies a un ritmo sin precedentes. Sin embargo, hay esperanza de recuperar la biodiversidad perdida a travs del proceso de re generacin de los bosques. Los insectos, la clase ms especiosa de animales, se concentran en los trpicos. Examin los efectos de la reforestacin en la composicin y diversidad de las especies de insectos en el dosel y el sotobosque de un bosque tropical premontano en Monteverde, Costa Rica: La Calandria. Recolect insectos con trampas de intercepcin de vuelo y analic la composicin y diversidad de rdenes y de morfospecies de himenpteros. Descubr que la composicin de las especies vara segn el estado de reforestacin y entre el dosel del bosque y el sotobosque. Aunque la composicin de las especies es diferente, encontr que la diversidad entre bosques poco perturbados y regenerados es similar.

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Insect Diversity and Composition in Regenerated Forest Sanko 2 Tropical forests are the most speciose ecosystems on earth, supporting more than half of all extant species (Gentry, 1992). Most “biodiversity hotspots” are located in tropical forests ( Myers et al., 2000) . Hotspots are ecosystems with particularly high concentrations of endemic species undergo ing rapid habitat loss (Myers et al., 2000). Arthropods, specifically insects, are concentrated in tropical forests ( Wilson, 1989). Although close to 900,000 species of insects have been described, thee total number of insect species is estimated to be aro und 10,000,000 (Gaston, 1991). As the “last biological frontier,” the forest canopy is a relatively untapped source of tropical biodiversity. Specifically, arthropods in the canopy remain widely understudied (Erwin, 1983). Many undescribed insect species are suspected to exist in the canopies of tropical forests (Erwin, 1983). Additionally, the species composition of the forest canopy is often strikingly different from the understory (Longino & Nadkarni, 1990). However, despite the richness of tropical for ests, we are currently in the midst of a “biodiversity crisis” (Wilson, 1989). Species are disappearing far faster than we are able to describe them. Because the planet’s insect species are largely undescribed and unstudied, biodiversity loss is a threat w ith unpredictable consequences (Wilson, 1989). Deforestation is a major cause of the rapid loss of species in the tropics (Wilson, 1989). Agricultural production is one of the most significant causes of deforestation, as growing urban populations require i ncreasing amounts of food produced in rural tropical areas (DeFries et al., 2010). Population growth is projected to occur in mostly urban areas, which counterintuitively has a larger impact on tropical deforestation than rural growth (DeFries et al., 2010). Urban populations consume more processed food and animal products than their rural counterparts, placing more agricultural pressure on tropical forests (DeFries et al., 2010). In response to biodiversity loss, reforestation and reclamation of agricultur al sites is becoming more common. DellaSala et al., (2003) define the core principle of forest restoration, ecological integrity, as “the ability of an ecosystem to support and maintain a balanced, adaptive community of organisms having a species compositi on, diversity, and functional organization comparable to that of natural habitats within a region.” Insect community structure is an overall indicator of forest biodiversity, ecosystem integrity, and the recovery of ecosystems following human disturbance ( Maleque et al., 2006). However, reforested areas are often novel in terms of species composition, species interactions, and ecosystem functions (Aerts & Honnay, 2001). I investigated insect composition and diversity in an undisturbed secondary forest as w ell as two reforested plots in a premontane forest in Monteverde, Costa Rica. I examined the effects of reforestation on the understory and canopy of a plot that was reforested by tree planting and a former agricultural plot allowed to regenerate naturally . The central question addressed by this study is as follows: how does reforestation affect insect composition and diversity in the tropical forest understory and canopy?

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Insect Diversity and Composition in Regenerated Forest Sanko 3 MATERIALS AND METHODS Study Site This study took place at La Calandria Res erv e in Los Llanos, Costa Rica, from 13 18 May, 2019. La Calandria is mid elevation (1200 1250m) and is on the border between premontane moist and premontane wet forest. I collected insect samples from three plots: one undisturbed secondary forest (>50 years old) and two reforested plots. One plot was reforested by planting in 2001. The other plot is a former coffee plantation that has been re colonized by natural revegetation, beginning in the 1990s. Insect Trapping I collected flying insects with simple flightinterception traps based on those used by Barbier, 2019 and Steininger et al, 2015. These traps consist of twoliter soda bottles with window cutouts, filled with water, unscented soap and ethanol and suspende d f rom tree branches with nylon (Figure 1). I colored the traps yellow to attract Hymenoptera, my focal order. Disposable plastic plates were placed over the top to prevent flooding from rainfall (Figure 1) . I installed four traps in the understory of each pl ot, suspended 0.5m from the ground. Two traps were placed in the canopy of each plot. Traps were active for approximately five days, wherein they were checked and emptied twice. Figure 1. Flight interception trap model. Insects entered through the window and made contact with the smooth plastic interior, causing them to fall into the water.

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Insect Diversity and Composition in Regenerated Forest Sanko 4 Insect Sorting I combined trap samples from each plot into the categories “Planted,” the plot reforested by tree planting, “Abandoned,” the abandoned coffee plantation reforested by natural regeneration, and “>50,” or the plot of undisturbed secondary forest. From there, samples were split into canopy and understory specimens. Within each of the six categories, I identified specimens to order and recorded the number of individuals and morphospecies. Furthermore, I selected all hymenopterans from each category and recorded which morphospecies were present. Analysis I analyzed the composition of the understory and canopy of each plot on two taxonomic levels, arthropod orders and morphospecies of Hymenoptera. I compared the abundance of each order within each of the six ca tegories and identified which were dominant, or most abundant. To assess diversity, I used a true diversity test with three levels of analysis. q=0 is a equal to richness, q=1 (Shannon index exponent) weighs common species more heavily, and q=2 gives more weight to rare species. True diversity indices were calculated for the canopy and understory of each plot with regards to order richness (number of morphospecies/order) and hymenoptera morphospecies richness. I also compared the number of morphospecies of each order within the understory and canopy of each plot. Order Composition I collected 521 total individuals over the course of five days. Relative abundance of arthropod orders varied between plots and within plots between canopy and understory (Figure 2). In the understory of all three plots, the significantly dominant order (by abundance of individuals) was Coleoptera, followed by Diptera and Hymenoptera respectively. However, in the canopy, Coleoptera was only dominant in the planted plot. In the >50 year undisturbed plot, Hymenoptera dominated, followed by Coleoptera and Diptera. In the abandoned pasture, Diptera and Hymenoptera were the most dominant, followed by Coleoptera.

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Insect Diversity and Composition in Regenerated Forest Sanko 5 A B C D 0 5 10 15 20 25 30 35 40 Coleoptera Diptera Hemiptera Hymenoptera Blattodea Collembola Thysanoptera Pscoptera Orthoptera Lepidoptera Relative Abundance (% Individuals) Order 0 5 10 15 20 25 30 35 40 45 50 Relative Abundance (% Individuals)Order 0 5 10 15 20 25 30 35 40 45 50 Relative Abundance (% Individuals)Order 0 10 20 30 40 50 60 Relative Abundance (% Individuals)Order

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Insect Diversity and Composition in Regenerated Forest Sanko 6 E F Figure 2. Order composition of each plot, separated into understory and canopy. Measured by relative abundance of each order. (A) Planted, Understory (B) Planted, Canopy (C) >50, Understory (D) >50, Canopy (E) Abandoned, Understory (F) Abandoned, Canopy. Table 1. Chi Square values of order abundances. Numbers of individuals from each order were compared within each of the six categories. Understory Canopy Planted 95.691, p<0.01 176.429, p<0.01 >50 201.026, p<0.01 24.548, p<0.01 Abandoned 135.985, p<0.01 20.923, p<0.01 Morphospecies Composition When comparing Hymenoptera between all six categories, I identified 54 distinct morphospecies. I compared the morphospecies found in the understory and the canopy of each plot (Figure 2). The abandoned pasture had significantly more morphospecies in common between the canopy and understory than did the planted plot or the undisturbed forest (X2=7.0, p<0.05). 0 5 10 15 20 25 30 35 40 45 Coleoptera Diptera Hemiptera Hymenoptera Blattodea Collembola Thysanoptera Orthoptera Relative Abundance (% Individuals)Order 0 5 10 15 20 25 Coleoptera Diptera Hemiptera Hymenoptera Collembola Psocoptera Thysanoptera Relative Abundance (% Individuals) Order

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Insect Diversity and Composition in Regenerated Forest Sanko 7 Table 2. Hymenoptera morphospecies comparison between canopy and understory of each plot. Abandoned plot has significantly more species in common between canopy and understory. Present in Canopy Present in Understory Present in Canopy and Understory Total Planted 7 11 0 18 >50 13 13 1 26 Abandoned 17 13 5 25 Order Diversity True diversity indices showed no significant difference between the order diversity (morphospecies/order) of each plot in both the canopy and understory (Figure 3). Order richness (q=0) did not vary significantly between any plot (Understory X2=0.05, p >0.70, Canopy X2=1.52, p > 0.40). However, when comparing the number of morphospecies within each order, certain orders were significantly diverse in some plots. Coleoptera was significantly more diverse in the understory of both the abandoned plantation and the >50 year forest (X2=6.14, p<0.05). In addition, Coleoptera and H emiptera were significantly more diverse in the canopy of the planted plot (Coleoptera X2=30.46, p<0.01, Hemiptera X2=7.53, p<0.05). A 0 2 4 6 8 10 12 q=0 q=1 q=2True Diversity Between Plots Planted >50 Abandoned

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Insect Diversity and Composition in Regenerated Forest Sanko 8 B Figure 3. Order true diversity index results for A) Canopy and B) Understory for each plot . Diversity is not significantly different between plots. Hymenoptera Morphospecies Diversity Hymenoptera morphospecies diversity did not significantly differ between any of the plots, with the exception of diversity with weight given to rare species (q=3) in the forest canopy (Figure 4). The undisturbed plot was significantly lower than the other two (X2=6.18, p<0.05). A 0 2 4 6 8 10 12 q=0 q=1 q=2 True Diversity Between Plots Planted >50 Abandoned 0 2 4 6 8 10 12 14 q=0 q-1 q=2 True Diversity Between Plots Planted >50

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Insect Diversity and Composition in Regenerated Forest Sanko 9 B Figure 4. Hymenoptera morphospecies true diversity index results , compared between plots . A) Canopy and B) Understory. DISCUSSION Order composition varied between each category. Certain orders, such as Lepidoptera, were found in only one category. Most noticeable is the variation in the canopy, where the dominant order differed between each plot. While Coleoptera, Hymenoptera, and Diptera were most abundant, this is likely due to the mechanism of the traps. These traps did not include bait and were designed to capture flying insects. For a more complete picture of order composition, tra ps directed towards walking insects would also be needed. Regardless of the most abundant orders, these data demonstrate that differences in composition exist between the canopy and the understory. Furthermore, this result supports the idea that regenerate d forest can be novel in taxonomic composition ( Aerts & Honnay, 2001) . Changes in species composition result in changes to ecological interactions, potentially preventing forests from returning to their previous ecological function. Hymenopteran morphospecies composition also varied between plots and between the canopy and the understory. Relatively few species were shared between the canopy and understory of the planted and undisturbed forests, while the abandoned pasture had significantly more in common between the two layers. This could imply that the abandoned pasture supports more habitat generalists than the other plots. While species composition varied between plots, each plot was largely equal in diversity in both arthropod orders and hymenoptera n morphospecies. This result bodes positively for restoration efforts, implying that reforested plots can hold similar levels of biodiversity as undisturbed plots. When Maeto et al. (2006) examined the effect of forest regeneration on braconid wasps in tropical Asia, they too found varying species composition yet similar levels of diversity between undisturbed and reforested plots. A notable exception to the general trend is the undisturbed secondary forest understory, which had significantly fewer rare spe cies than the reforested plots. There is more than one explanation for this result. As the vegetation regenerates 0 2 4 6 8 10 12 14 16 18 q=0 q=1 q=2 True Diversity Between Plots Planted >50 Abandoned

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Insect Diversity and Composition in Regenerated Forest Sanko 10 and arthropod species colonize new land, it may take time for once abundant species to regain former population levels. Contrastingly, novel p lant species composition in reforested plots could present a different set of resources for arthropods to exploit, causing species that were once common in these forests to become rare. Diversity within order varied between plots as well as canopy and understory. While Coleoptera was significantly less diverse in the understory of the planted plot, the same order was significantly more diverse in the canopy. Hemiptera was also significantly more diverse in the canopy of the planted plot. As hemipterans a re largely herbivorous, this could indicate higher plant diversity in the canopy of this plot. Alternatively, fast growing plants are often planted during reforestation (Wightman et al., 2001). These trees produce less secondary metabolites than slow growi ng species, and are thus subject to increased levels of herbivores (Coley et al., 1985). Increased diversity of hemipterans may be in response to the tree species chosen for planting in this plot. Overall, this study holds important implications for fore st restoration ecology. It is important to consider that the forest understory and canopy are different with respect to species composition and diversity within arthropod orders. When measuring and describing forest biodiversity, it is imperative to treat each layer as a separate ecosystem. Furthermore, these results indicate that arthropod diversity can be recovered in a relatively short amount of time. Overall, forest restoration is an imperfect, but viable solution to insect biodiversity loss. ACKNOWLEDGEMENTS This project was made possible through the Monteverde Institute and La Calandria Reserve, as well as through the tremendous efforts of Emilia Triana, Federico Chinchilla, F rank Joyce, Sofa Arce, and F lix Salazar. LITERATURE CITED Aerts, R., & Honnay, O. (2011). Forest restoration, biodiversity and ecosystem functioning. BMC ecology , 11, 29. doi:10.1186/147267851129. Anderson, A., McCormack, S., Helden, A., Sheridan, H., Kinsella, A., & Purvis, G. (2011). The potential of parasitoid Hymenoptera as bioindicators of arthropod diversity in agricultural grasslands. Journal of Applied Ecology , 48(2), 382 390. Chazdon, R. (2013) homogenization and differentiation hypotheses. Journal of Ecology , 101(6), 14491458. Barbier, Mallory, "Edge effects and diversity of understory and canopy cloud forest beetles" (2019). H onors Theses. Coley, Phyllis D., John P. Bryant, and F. Stuart Chapin. "Resource availability and plant antiherbivore defense." Science 230.4728 (1985): 895899. DeFries, R. S., Rudel, T., Uriarte, M., & Hansen, M. (2010). Deforestation driven by urban

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Insect Diversity and Composition in Regenerated Forest Sanko 11 population growth and agricultural trade in the twentyfirst century. Nature Geoscience, 3(3), 178. DellaSala, D., Martin, A., Spivak, R., Schulke, T., Bird, B., Criley, M., ... & Aplet, G. (2003). A citizen's call for ecological forest restoration: forest restoration principles and criteria. Ecological Restoration, 21(1), 15. Erwin, T. L. (1983). Tropical forest canopies: the last biotic frontier. Bulletin of the ESA , 29(1), 1420. Gaston, K. J. (1991). The magnitude of global insect species richness. Conservation biology, 5(3), 283296. Gentry, A. H. (1992). Tropical forest biodiversity: distributional patterns and their conservational significance. Oikos , 1928. Longino, J. T., & Nadkarni, N. M. (1990). A comparison of ground and canopy leaf litter ants (Hymenoptera: Formicidae) in a neotropical montane forest. Psyche: A Journal of Entomology , 97(1 2), 81 93. Maeto, K., Noerdjito, W. A., Belokobylskij, S. A., & Fukuyama, K. (2009). Recovery of species diversity and composition of braconid parasitic wasps after reforestation of degraded grasslands in lowland East Kalimantan. Journal of Insect Conservation, 13(2), 245257. Maleque, M. A., Ishii, H. T., & Maeto, K. (2006). The use of arthropods as indicators of ecosystem integrity in forest management. Journal of Forestry , 104(3), 113117. Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Natu re, 403(6772), 853. Nadkarni, N. M., & Longino, J. T. (1990). Invertebrates in canopy and ground organic matter in a neotropical montane forest, Costa Rica. Biotropica , 286289. Steininger, M. S., Hulcr, J., igut, M., & Lucky, A. (2015). Simple and efficient trap for bark and ambrosia beetles (Coleoptera: Curculionidae) to facilitate invasive species monitoring and citizen involvement. Journal of economic entomology , 108(3), 11151123. Wightman, K. E., Shear, T., Goldfa rb, B., & Haggar, J. (2001). Nursery and field establishment techniques to improve seedling growth of three Costa Rican hardwoods. New Forests, 22(1 2), 75 96. Wilson, E. O. (1989). Threats to biodiversity. Scientific American , 261(3), 108116.


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