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Dispersin espacial de las frutas y optimizacin de forrajeo de los murcilagos frugvoros
Spatial dispersion of fruits and foraging optimization of frugivorous bats
Optimal foraging helps maximize fitness of the disperser and corresponding plant. Fruiting strategies may influence foraging success in order to increase seed dispersal rate. This study examines the spatial dispersion of fruits and its influence on foraging time of frugivorous bats. Five bat species in captivity at the Bat Jungle in Monteverde, Costa Rica, including Carollia brevicauda and Artibeus toltecus, are used to test the foraging time on three spatial
arrangements, uniform, random and clumped, using a natural food source, Solanum umbellatum (Solanaceae). Each of the three arrangements were tested for fruit removal rate during one day and two of the trials that were not tested in the morning of the first day were preformed the two following mornings. The bats were able to forage the
quickest on the clumped arrangement of fruits (15:27min) suggesting that it is most advantageous for plants to ripen their fruits in clusters to maximize fruit removal rates. However, the foraging time for random arrangement was only one minute more than for clumped in the morning trial, suggesting that the bats may be able to adopt different
foraging strategies to optimize search time.
Optimizar el forrajeo ayuda a maximizar el xito reproductivo del dispersor y su planta correspondiente. Las estrategias de fructificacin pueden influenciar el xito de forrajeo mientras incrementan la tasa de dispersin de las semillas. Este estudio examin la dispersin espacial de las frutas y su influencia en el tiempo de forrajeo de los murcilagos frugvoros. Cinco especies de murcilagos en cautiverio en el Bat Jungle de Monteverde, Costa Rica, incluyendo Carollia brevicauda y Artibeus toltecus fueron usados para probar el tiempo de forrajeo en tres distribuciones espaciales, uniforme, azar y agregada usando una fuente natural de alimento, solanum umbellatum (Solanaceae). Cada una de las distribuciones espaciales fue probada para la tasa de remocin de las frutas. Los murcilagos fueron capaces de forrajear mas rpidamente en la distribucin agregada, lo que sugiere que es lo ms ventajoso para las plantas es madurar las frutas agrupadas para maximizar la remocin de los frutos. De cualquier forma, el patrn de distribucin al azar fue solamente un minuto ms que el tiempo de forrajeo que para el patrn agregado que en la sesin de la maana, lo que sugiere que los murcilagos son capaces de adoptar diferentes estrategias por optimizar el costo de bsqueda.
Text in English.
Costa Rica--Puntarenas--Monteverde Zone
Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology Fall 2009
Ecologa Tropical Otoo 2009
t Monteverde Institute : Tropical Ecology
Spatial dispersion of fruits and foraging optimization of frugivorous bats Kristen Omori College of Aquatic and Fishery Science and Environmental Science, University of Washington ABSTRACT Optimal foraging helps maximize fitness of the disperser and c orresponding plant. Fruiting strategies may influence foraging success in order to increase seed dispersal rate. This study examines the spatial dispersion of fruits and its influence on foraging time of frugivorous bats. Five bat species in captivity at t he Bat Jungle in Monteverde, Costa Rica, including Carollia brevicauda and Artibeus toltecus , are used to test the foraging time on three spatial arrangements, uniform, random and clumped, using a natural food source, Solanum umbellatum (Solanaceae). Each of the three arrangements were tested for fruit removal rate during one day and two of the trials that were not tested in the morning of the first day were preformed the two following mornings. The bats were able to forage the quickest on the clumped arra ngement of fruits (15:27min) suggesting that it is most advantageous for plants to ripen their fruits in clusters to maximize fruit removal rates. However, the foraging time for random arrangement was only one minute more than for clumped in the morning tr ial, suggesting that the bats may be able to adopt different foraging strategies to optimize search time. RESUME Optimizar el forrageo ayuda a maximizar el Ã©xito reproductivo del dispersor y su planta correspondiente. Las estrategias de fructificaciÃ³n p uen influenicar el Ã©xito de forrageo mientras incrementan la tasa de dispersion de semillas. Este estudio examinÃ³ la dispersion espacial de frutas y su influencia en el tiempo de forrageo de murcielagos frugivoros. Cinco especies de murcielagos en cautiver io en el Bat Jungle de Monteverde, Costa Rica, incluyendo Carollia brevicauda y Artibeus toltecus fueron usados para probar el tiempo de forrageo en tres distribuciones espaciales, uniforme, azar y agregada usando una fuente natural de alimento, solanum um bellatum (Solanaceae). Cada una de las distribuciones espaciales fueron probadas para la tasa de remociÃ³n de frutas. Los murcielagos fueron capaces de forragear mas rapidamente en la distribuciÃ³n agregada, lo que sugiere que es lo mas ventajoso para las p lantas es madurar las frutas agrupadas para maximizar la remociÃ³n de frutos. De cualquier forma, el patrÃ³n de distribuciÃ³n al azar fue solamente un minuto mas que el tiempo de forrageo que para el patrÃ³n agregado que en la session de la maÃ±ana, lo que sugi ere que los murcielagos son capaces de adoptar diferentes estrategias por optimizar el costo de busueda. INTRODUCTION The relationship between plants and dispersers has been shaped by natural selection to maximize ted to provide fruits that maximize dispersal, catering to dispersers that are capable of moving fruits away from the parent and to desirable sites. Dispersers have evolved to optimally balance the costs of foraging with the benefits of food and nutrient intake. Optimal foraging theory states that through natural selection, organisms have evolved to optimize net energy yield, thereby improving individual fitness (Schoener 1971). Dispersers use a variety of foraging strategies to optimize net energy intake depending on the distribution of plants. For instance, dispersers that forage over a large area travel in a relatively straight line and once a patch of fruit is located, foraging strategy may change to better optimize
energy expenditure (Scharf et al. 2 009). Therefore, smaller spatial scales, including patch distribution and fruiting on individual plants, affects the foraging behavior of dispersers. There are many factors that influence the foraging strategies of bats.Canopy density in combination with conditions of lunar lighting and/or large openings impact bat flight and foraging due to varying levels of predation risk (Esperard 2007). One study documented 14 species of birds that prey on bats (Chacon Madrigal and Barrantes 2004). Thus bats may selec t fruits in large clusters in order to minimize exposure time to predators. Another aspect affecting foraging is the seasonal patterns. Due to the relative sparsity of food in the dry season, some bats are known to fly longer distances in search of more h ighly concentrated resource patches (Fleming and Heithaus 1986). It is then ideal for a fruiting plant in the dry season to produce large amounts of ripe fruits along with its neighbors to attract the frugivorous bats. Likewise, the fruiting phenology of p lants influences bat foraging. Bats favor plants such as Piper spp . that fruit year around because they are reliable sources of food. These bats also tend to forage on other species of fruiting plants that are within close proximity to Piper (Fleming et al . 1977). In each of the factors above, dispersion of the fruit on a plant plays an important role in the foraging response and change in strategy of the bat. There are several theories on the mechanisms by which individual plants maximize their fruit disp ersal. The fruit crop size hypothesis states that plants with large fruit crop size will attract more dispersers compared to those with small crop, size resulting in higher seed dispersal (Ortiz Polido et al. 2007). Many studies have demonstrated that lar ger crop sizes do influence seed dispersal, increasing the fitness of the plant (e.g. Garcia and Ortiz Polido 2004). Furthermore, the arrangement of fruits on a plant can also influence dispersal success. Dispersion can be divided into three basic categori es: uniform, clumped and random. Fruits in a uniform distribution are arranged evenly on the plant, clumped fruits are arranged in large bunches, and random distribution describes fruits that are in clumps of various sizes. Plants are also able to strategi cally ripen fruits within an infructescence to optimize visitation, ripening a few fruits from each infructescence (uniform), randomly ripening fruits on some infructescences (random), or ripening all the fruit in one cluster (clumped). Plants may ripen fr uits in the arrangement that best attracts their specific dispersers, therefore increasing their own fecundity via successful seed dispersal. Few studies have been conducted with a focus on fruit dispersion, but flower arrangement is relatively well studi ed and is perhaps indicative of similar trends. It has been shown that with pollinators, visits to areas with higher densities of flowers in patchy arrays were more frequent than those arranged in a more uniform distribution (Cresswall 2000; Pyke 1981). Fo r example, bumblebees revisit areas with higher aggregated flower arrangement twice as much as areas with flowers in a more uniform array (Cresswall 2000). Hummingbirds have also demonstrated a preference for patchy arrangement of flowers and, as with bats , their foraging technique varies depending on the available resources (Baum and Grant 2001). This suggests that these pollinators may optimize their foraging behavior by searching for the largest densities of flowers in one patch, thereby decreasing energ y is spent searching for nectar. Dispersers may have similar foraging patterns, searching for high return sites that have clumped arrays of fruits. In the case of frugivorous bats, species such as Carollia perspicillata may commute as far as 2.7 km before feeding at the optimal location (Fleming et al. 1977). However, bats may travel far at the beginning of the night, but once a good foraging area is located, the travel time for food is reduced, thus lessening the energy needed for foraging (Presley et al. 2009). Given that Carollia sp. consume 100 120% of their body weight in fruit pulp and Artibeus eat twice their body mass
each night, it would be ideal for the bats to consume the most amount of fruit with the least amount of time spent foraging (Charles D ominique 1991). Therefore, in order for a plant to most effectively attract its bat dispersers, it may be advantageous to produce more ripe fruit within in a shorter time frame to signal to bats that the fruits are ready to be consumed. Bats expend the mos t energy on searching for this large cluster of fruits, but once the cluster is located the bat can forage directly off of this patch without spending more energy on locating more singly placed fruits. With a more random arrangement, bats may have to spend more time foraging to locate as many fruits found in a clumped arrangement. Similarly, the energy return when searching for one fruit is smaller than the reward of many fruits in a clumped dispersion. A common plant consumed by some frugivorous bats, incl uding Carollia and Artibeus species, is Solanum (Dinerstein 1983; LaVal and Rodriguez H 2002; Lopez and Vaughan 2007). One studied species, S. umbellatum , produces two mass fruiting, one from August to November and another from March to May (Dinerstein 198 3) and fruits are arranged in clumps ( pers. obs. ). to increase dispersal rates. This then benefits the fitness of the individual bats by helping them for age more effectively. This study examines the foraging time for two native frugivorous bats, Artibeus toltecus and Carollia brevicauda , on Solanum umbellatum using different spatial dispersion patterns of fruits. Uniform, clumped and random distributions were tested to examine which one was most energetically advantageous for the bats, thus increasing the dispersal rate of the plant. Based on optimal foraging theory, it is hypothesized that the two species of bats will consume the natural fruit in the clu mped arrangement the quickest because fruits in a cluster are easier to locate and involve less search time after being found. Therefore, bats can increase the foraging efficiency by spending less time searching on a small spatial scale. METHODS Study Site and Species This study was conducted in November, 2009 at the Bat Jungle in Monteverde, Costa Rica. The Bat Jungle contains a large, L shaped flight cage with glass on one side for viewing. The room is dimly lit with artificial branches and trees for the bats to hang from. Inside the enclosure, there are three artificial hanging branches with a total of 13 feeding dishes distributed along the glass side with five feeding dishes on two of the branches and three on the remaining. There are a total of 8 5 free flying nectarivorous and frugivorous bats, comprising of eight different species. This study focused on the five frugivorous bat species, Carollia brevicauda , Artibeus toltecus , A. jamaicensis, A. lituratus, Platyrrhinus vittatus each of those speci es have 8, 40 45, 5, 2, and 3 individuals, respectively. Most bats were captured by mist netting between May and November 2006. Since then some A. toltecus individuals have been born in captivity. The two most abundant frugivorous batsin the Bat Jungle, C. brevicauda and A. toltecus , are smaller and seem to consume eat more regularly (Richard LaVal pers. obs. ) Carollia brevicauda are known to focus on Piper spp ., but are also prime seed dispersers of other fruits in Costa Rica, including Cecropia (Cecropiac eae), Vismia (Hypericaceae) and Solanum (Solanaceae) (LaVal and Rodriguez H 2002). Artibeus toltecus have been reported to eat fruits of 17 species of plants, specializing on Solanum , a Myrtaceae canopy tree, figs and Cepropia (LaVal and Rodriguez H
2002; Dinerstein 1983). At the Bat Jungle, the frugivorous bats are provided with watermelon, papaya, banana, apples, mangos, and occasionally guayaba by caretakers. Experimental Design The fruits from Solanum umbellatum , which are naturally consumed, were use d as the experimental fruit, because previous observations demonstrated that the bats preferred Solanum over fruits regularly feed to them. The three tests include clumped, random and uniform dispersion patterns to represent different fruiting techniques i n nature. For the clumped trials, 40 Solanum fruits were placed into one dish. The remaining nine dishes were filled with fruit that are normally fed to the Bat Jungle bats including watermelon, banana, apples, papaya and mangos. The random arrangement tes top of five of the ten feeding dishes. The five dishes containing 17, 10, 8, 3, and 2 pieces of Solanum fruit. The uniform test consisted of supplementing each of the ten normal food dishes with four pieces of Solanum . The dishes containing the Solanum in each trial were randomly placed in the hanging branches with dish holders to avoid bats memorizing the placement of the preferred, natural fruit. On day 1, random, clumped and uniform arrangement trials were performed during the three feeding times, 8:45 (morning), 12:00 (midday), and 15:00 (afternoon) respectively. To determine whether time of day was a factor in the amount of time foraging on Solanum fruits, the clumped and uniform trials were t ested the two subsequent mornings. Fruit Removal Rates and Behavioral Observations Time was started once all the dishes were placed inside the flight cage and when a bat ate the first piece of food. For each dish, the length of time it took for the bats to consume all of the Solanum was recorded. These times from day 1 and morning trials were compared to one another to find trends. RESULTS On day 1, frugivorous bats in the Bat Jungle consumed the f ruits the quickest when Solanum umbellatum fruits were placed in a clumped arrangement, followed by random and lastly uniform (Table 1). The general trend of forage times during the morning, however, showed that the foraging time for random arrangement was only a minute more than the clumped morning trial (Table 1). During the uniform distribution trial in the afternoon, two pieces of experimental fruit were left untouched after two hour. One of the pieces seemed to be unripe and the other was TABLE 1. Total forage time (minutes:seconds) of C. brevicauda and A. toltecus on varing distributions of S. umbell atum fruits during morning (8:45), midday (12:00), and afternoon (15:00). Distribution Uniform Random Clumped Morning 38:29 16:36 15:27 Midday ----12:34 Afternoon 27:36 ----
overripe, in which it was assumed that the bats were not going to consume those pieces, and therefore discarded from the forage time. The time recorded for the afternoon uniform arrangement trial was the last dish containing Solanum , which excluded the two undesirable fruits. Additional Observations Roughly 40 60% of the frugivorous bats that were eating were consuming Solanum umbellatum . The Solanum fruits appeared to disappear before any other bowls were emptied. DISCUSSION There is weak evidence that it is most a dvantageous for Solanum umbellatum to ripen their fruits in clumps rather than randomly or uniformly, though the random trial was nearly equal in time and contained small clumps. Time of day may have influenced the foraging time slightly, but the trends st ill suggests the bats are more likely to select fruits from larger clusters than other spatial dispersion strategies. Ripening the fruits all in one cluster not affect the larger spatial scale foraging behavior, but can help reduce the small scale foraging energy output. Therefore, to optimize the dispersal of seeds, S. umbellatum plants should put energy into ripening fruits in clusters at the same time. Bats are able to disperse seeds far from the parent plant, thus plants would want all their fruits to b e consumed, not worry about dense seed clumps near the parent, and there is also a better chance for more of their fruit to be eaten when presented in a clump formation. Once the frugivores are able to locate the fruit clusters, they can consume all the fo od presented without searching for other pieces individually. As a result, this ensures that the fruits al success as well as optimizing the foraging efficiency of their dispersers. Frugivorous bats appeared to show preference toward Solanum fruits over the other unnaturally foraged fruits in the Bat Jungle based on personal observations. This suggests tha t the frugivorous bats are able to locate and specifically select the S. umbellatum fruits, supporting the theory that these bats are able to distinguish among the preferred and less desirable fruits. For example, bats are able to differentiate between rip e and unripe fruits and species (Fleming et al. 1977) mostly based off olfactory cues ( Hodgkison et al. 2007), thus it is possible for them to find and select food that is edible and provides some nutrients. Foraging strategies are often adapted to diffe rent fruiting patterns. In random spatial distribution compared to clumped or uniform, foraging techniques need to be altered to be the most efficient, meaning the energy spent searching is minimized. In more uniform arrangement patches, a directional and more methodological foraging system is more efficient than random approach for hummingbird foraging, whereas in random patches, it was more advantageous for these pollinators to forage randomly (Baum and Grant 2001). This study also demonstrated that forag ing by area restriction meaning that the hummingbird can visit any flower directly adjacent to the current flower, is the most beneficial strategy for clumped flower patches. Possibly for similar reasons, the frugivorous bats most efficiently forage on the Solanum when presented in a clump, but can possibly change its foraging techniques for the other arrangements. In the random arrangement, there are still clusters of ripe fruits in which dispersers may demonstrate a foraging behavior similar to when forag ing for clumps of fruits by searching randomly and using olfactory
to guide them in the correct direction, but has to also search more when all the ripe fruits are not all in one place. In conclusion general clumping of ripe fruit may be the most advantage ous spatial arrangement for frugivorous bats, however when arranged differently the bats may be able to adapt and change their foraging strategies to optimize net energy. Foraging strategies for frugivorous bats are difficult to observe in nature. Howev er, the Bat Jungle provided an ideal place to observe foraging behavior and techniques because of its abundance of frugivorous bats and large flight cage, which allows the bats enough room for foraging. This study can be improved by repeating the trials ov er a longer period to collect more data points. Furthermore, it would be interesting to bring this study to a more natural setting, quantifying patches of fruits and ripe fruit abundances that were consumed in the natural forests. Fruit clumps could even b e ripened artificially with ethylene gas and placed on a plant to mimic the three different ripening distributions. ACKNOWLEDGMENTS I thank Alan Masters for providing me with the idea of the project and giving me the support and help during the stressful couple days. I also thank JosÃ© Carlos CalderÃ³ Ulloa (Moncho) for also providing me guidance, light and support during ALL my projects. This project would not have been possible without Dr. Richard LaVal and his endless wisdom on bats and willingness for me to use the Bat Jungle. Special thanks to the people working at the Bat Jungle, Sirlene Marin Carranza, Kelly LaVal Wallace, and Wim De Backer (Vino) for being so accommodating. Lastly, to remaining staff, Anjali Kumar, Pablo Allen Mange and Yimen Araya, and to the students for being so understanding with my frustrations with my project and for the support. LITERATURE CITED Baum, K,A, and W.E. Grant. 2001. Hummingbird foraging behavior in different patch types: simulation of alternative strategies. Eco logical Modelling 137: 201 209. Chacon Madrigal, E. and G. Barrantes. 2004. Blue crowned motmot ( Momotus momota ) predation on a long tongued bat (Glossophinae). Wilson Bulletin 116: 108 110. Charles Dominique, P. 1991. Feeding strategy and activity budget of the frugivorous bat Carollia perspicillata (Chirotera: Phyllostomidae) in French Guiana. Journal of Tropical Ecology 7: 243 256. forage plant. E cological Entomology 25: 19 25. Dinerstein, E. 1983. Reproductive ecology of fruit bats and seasonality of fruit production in a Costa Rican cloud forest. Ph.D. dissertation. University of Washington, Seattle. 136pp. Esberard, C.E.L. 2007. Influence of moo n cycle in Phyllostomid bat capture. Iheringia Serie Zoologia 97(1): 81 85. Fleming, T.H. and E. R. Heithaus. 1986. Seasonal foraging behavior of frugivorous bat Carollia perspicillata . Journal of Mammalogy 67 (4): 660 671. ---------, E. R. Heithaus, and W.B. Sawyer. 1977. An experimental analysis of the food location behavior of frugivorous bats. Ecology 58: 619 627. Garcia, D. and R. Ortiz Pulido. 2004. Patterns of resource tracking by avain frugivores at multiple spatial scales: two case studies on disc ordance among scales. Ecography 27 (2): 187 196. Hodgkison, R., M. Ayasse, E.K.V. Kalko, C. Haeberlein, S. Schulz, W.A.W. Mustapha, A. Zubaid, and T.H. Kunz. 2007. Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two specie s of paleotropical bat dispersed figs ( Ficus hispida and Ficus scortechinii ). Journal of Chemical Ecology 33 (11): 2097 2110. LaVal, R.K. and B. Rodriguez H. 2002. Murcielagos de Costa Rica Bats . Instituto National de Biodiversidad. Costa Rica. Lopez, J.E. and C. Vaughan. 2007. Food niche overlap among neotropical frugivorous bats in Costa Rica. Revista de Biologia Tropical 55 (1): 301 313.
Ortiz Pulido, R., Y.V. Albores Barajas, and A.A. Diaz. 2007. Fruit removal efficiency and success: influence of crop s ize in a neotropical treelet. Plant Ecology 189: 147 154. Presley, S.J., M.R. Willig, I. Castro Arellano, and S.C. Weaver. 2009. Effects of habitat conservation on temporal activity patterns of Phyllostomid bats in lowland Amazonisan Rain Forest. Journal o f Mammology 90 (1): 210 221. Pyke, G.H. 1981. Optimal nectar production in a hummingbird pollinated plant. Theoretical Population Biology 20 (3): 326 343. Sallabanks, R. 1993. Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74: 13 26 1336. Scharf, I. B. Kotler and O. Ovadia. 2009. Consequences of food distribution for optimal searching behavior: an evolutionary model. Evolutionary Ecology 23: 245 259. Schoener, T.W. 1971. Theory of feeding strategies. Annual Review of Ecology and Sy stematics 2:369 404.