Going batty: response of foraging glossophagine bats to auditorily perceived predator presence


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Going batty: response of foraging glossophagine bats to auditorily perceived predator presence

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Title:
Going batty: response of foraging glossophagine bats to auditorily perceived predator presence
Translated Title:
Ir batty: respuesta de forrajeo de los murciélagos con la presencia de depredadores percibidos auditivamente
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Frank, Hannah Kim
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Bats--Behavior ( lcsh )
Murciélagos--Comportamiento ( lcsh )
Bats ( lcsh )
Murciélagos ( lcsh )
Predation (Biology) ( lcsh )
Depredación (Biología) ( lcsh )
Costa Rica--Puntarenas--Monteverde Zone
Costa Rica--Puntarenas--Zona de Monteverde ( lcsh )
CIEE Summer 2007
CIEE Verano 2007
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Reports

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Abstract:
Predator presence is known to alter the foraging behavior of many species leading to decreased resource acquisition and lowered reproductive rate (Werner 1994). Previous studies have examined the effect of predator presence on the emergence of roosting bats and the effect of predator models on foraging bats (Baxter et al. 2006). Only one study, however, has examined the importance of auditory cues in alerting foraging bats to the presence of predators (in this case, owls; Baxter et al. 2006). The study concluded that bats not only avoid perceived owls but also the call of a diurnal woodpecker, leading the authors to question whether the latter finding was the result of novel sound avoidance or acoustic interference. This study, conducted in Monteverde, Costa Rica, investigated whether the findings of the earlier study were due to the effects of a novel sound or acoustic interference. Predator avoidance was quantified by counting number of visits to a hummingbird feeder after playing an owl call, a frog call or no call (a silent control). Significantly fewer visits were detected after the owl call than either the frog call or silence (ANOVA, F = 11.0203, p = 0.0001, df = 2) indicating the results of the previous study were due to novel sound avoidance. This study also reaffirmed the importance of auditory cues as a technique for predator detection in foraging bats, demonstrating a globally significant trait of bats. ( ,, )
Abstract:
Se sabe que la presencia de depredadores puede cambiar el comportamiento de forrajeo de muchas especies, llevando a una reducción en la adquisición de recursos y bajando la tasa reproductiva (Werner 1994). Estudios anteriores examinaron el efecto de la presencia de depredadores afuera de los sitios de descanso de los murciélagos y el efecto de los modelos de los depredadores en los murciélagos que forrajean (Baxter et al. 2006). Sin embargo, solamente un estudio examino la importancia de las señales auditivas como alerta ante depredadores sobre los murciélagos que forrajean (búhos en este caso; Baxter et al 2006). En este estudio se concluyo que los murciélagos no solo evitan a los búhos que perciben sino que también el canto de un carpintero diurno, lo que llevo a los autores a cuestionar si lo encontrado es el resultado de evasión de un nuevo sonido o de evitar la interferencia acústica. En este estudio, realizado en Monteverde, Costa Rica se investigo si los resultados del estudio anterior se deben a los efectos de un sonido nuevo o la interferencia acústica.
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Student affiliation: Department of Organismic and Evolutionary Biology, Harvard University
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1 Going Batty: Response of foraging glossophagine bats to auditorily perceived predator presence Hannah Kim Frank Department of Organismic and Evolutionary Biology, Harvard University ABSTRACT Predator presence is known to alter the foraging behavior of many species leading to decreased resource acquisition and lowered reproductive rate Werner 1994. Previous studies have examined the effect of predator presence on the emergence of roosting bats and the effect of predator models on foraging bats Baxte r et al. 2006. Only one study, however, has examined the importance of auditory cues in alerting foraging bats to the presence of predators in this case, owls; Baxter et al. 2006. The study concluded that bats not only avoid perceived owls but also th e call of a diurnal woodpecker, leading the authors to question whether the latter finding was the result of novel sound avoidance or acoustic interference. This study, conducted in Monteverde, Costa Rica, investigated whether the findings of the earlier study were due to the effects of a novel sound or acoustic interference. Predator avoidance was quantified by counting number of visits to a hummingbird feeder after playing an owl call, a frog call or no call a silent control. Significantly fewer visit s were detected after the owl call than either the frog call or silence ANOVA, F = 11.0203, p = 0.0001, df = 2 indicating the results of the previous study were due to novel sound avoidance. This study also reaffirmed the importance of auditory cues as a technique for predator detection in foraging bats, demonstrating a globally significant trait of bats. RESUMEN Se sabe que la presencia de depredadores puede cambiar el comportamiento de forrajeo de muchas especies, llevando a una reducción en la adq uisición de recursos y bajando la tasa reproductiva Werner 1994. Estudios anteriores examinaron el efecto de la presencia de depredadores afuera de los sitios de descanso de murciélagos y el efecto de modelos de depredadores en los murciélagos que forra jean Baxter et al. 2006. Sin embargo, solamente un estudio examinó la importancia de señales auditivas como alerta ante depredadores sobre murciélagos que forrajean búhos en este caso; Baxter et al. 2006. En este estudio se concluyó que los murciélag os no solo evitan los búhos que perciben sino que también el canto de un carpintero diurno, lo que llevo a los autores a cuestionar si lo encontrado es el resultado de evasión de un nuevo sonido o de evita interferencia acústica. En este estudio, realizad o en Monteverde, Costa Rica, se investigó si los resultados del estudio anterior se deben a los efectos de un sonido nuevo o a interferencia acústica. La evasión de depredadores se cuantificó contando el número de visitas a un comedero artificial después del canto playback de un búho, una rana y silencio como control. Había menos visitas después del canto del búho que después del canto de la rana y el silencio, indicando que los resultados de Baxter et al. 2006 fueron debido a la evasión de un sonid o nuevo. Este estudio también reafirma la importancia de señales auditivas como una técnica para la detección de depredadores por parte de murciélagos que forrajean. INTRODUCTION Glossophagine bats are in the family Phyllostomidae, also known as the Amer ican leaf nosed bats Nowak 1994. Members of the subfamily Glossophaginae, these bats exhibit similar behaviors to hummingbirds, pollinating many tropical plants. They are specialized to extract nectar from flowers with elongated tongues, a narrow snout with sensory hairs and the ability to hover LaVal and Rodríguez H 2002. Still, many species have more

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2 generalized diets that include fruit and insects Findley 1993. Because of this nectarivorous diet, glossophagine bats are attracted to hummingbird f eeders at night, where they can be observed in large numbers Heuer 2004. The presence or absence of predators near the feeding site is very important since predation is a major factor in bat mortality. In fact, predator avoidance has been offered as t he reason for why bats roost colonially, emerge from these roosts in groups and are nocturnal Baxter et al. 2006. Risk of predation is especially high during foraging since with increased activity bats are more likely to encounter predators and because predators are often better at detecting moving prey. Still, level of activity is positively related with resource acquisition and it is this tradeoff between obtaining food and the risk of mortality that defines the behavior of many species. Bats general ly avoid predators and will avoid food if the predator is nearby Baxter et al. 2006. This predator presence therefore hinders the foraging success of many species, leading to a lower reproductive rate, making the organism less evolutionarily fit Werner 1994. Therefore predator presence is a powerful factor in determining not only a bat s short term feeding but also its lifetime fitness. A variety of studies have been conducted to determine how roosting bats respond to the presence of predators. These studies have used methods that include using actual predators, visual models of predators and models with playbacks of predator calls near bat roosts with mixed results. However, few researchers have examined the behavior of foraging, not roosting, bats i n response to predators Baxter et al. 2006. Heuer 2004 examined the response of foraging nectarivorous bats to a model snake or owl, known and important predators of bats, positioned at their feeder sites Altringham 1996. She noted that bats avoid ed feeders with either model present but not a control without a model. As a follow up, Díaz 2005 tested the hypothesis that bats were avoiding a novel object and not a predator by comparing bats reactions to a snake model, a novel object a shoe and a control, which lacked any object. She found that bats avoided the snake model but not the shoe and concluded that bats only respond to the threat of a recognizable predator. However, bats do not only use visual and olfactory signals. Bats also use echo location, which involves the transmittance of sound Nowak 1994. Additionally, studies with bats and other prey animals have demonstrated that auditory cues are very important in predator detection Baxter et al. 2006; Berger 1999; Schnitzler and Kalko 1 998. Only one study, however, has looked at foraging bats detection of predators using auditory cues. Baxter et al. 2006 used playbacks of owls, woodpeckers and silence at spatially separated stations to determine whether bats avoid owl calls. The b ats they studied did avoid owl calls but also avoided the woodpecker calls. The researchers theorized that the avoidance of woodpeckers was likely due to an avoidance of novel sounds or acoustic interference since the bats of their study were insectivorou s bats, which rely heavily on echolocation Nowak 1994. The woodpecker would indeed be a novel sound because the bats of their study, genus Myotis , tend to roost in caves and very rarely in hollow trees where they would be likely to encounter the diurnal woodpecker Nowak 1994. This study attempted to clarify the results of Baxter et al. 2006 and to determine whether bats avoid a novel sound or acoustic interference by using playbacks of owl and frog calls. Also, if the bats avoid predator song owl, it further reinforces the conclusion of Baxter et al. 2006 that acoustic cues are important in detecting predator presence during foraging. This study expected a difference in the number of bat visits to the feeder after the various calls. Also, it was predicted that there would be fewer visits to the

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3 feeder immediately after the predator call than after either the familiar call or silence, as bats should avoid the perceived predator. Since the bats are familiar with the frogs and know they are not har mful, the bats would not avoid the feeder after the frog call unless it is indeed the noise that bothers them. MATERIALS AND METHODS Bats were observed on 11 nights between July 14 and July 31, 2007, between 6:40 pm and 9:00 pm. They were observed visi ting a hummingbird feeder in the garden at Selvatura Adventure Park, located at 1612 m on the Caribbean slope of the Tilarán mountain range Millard 2004. The garden contains six feeder stands, each with four feeders. For this experiment, all feeders bu t the one observed feeder were removed to concentrate the bats and accurately monitor all bat activity. Three treatments were used in the experiment: the call of the Bare shanked Screech Owl, the call of the Common Tink Frog Eleutherodactylus diastema a nd a silent control. These species were chosen because they are known to live in the region of the study site; this ensures bats would be familiar with both calls Fogden 1993; Leenders 2001. The silent control trials replaced the call with silence but were otherwise identical. Treatments were performed in a random order by sampling without replacement to control for the variation in visits with time of night. All treatments were run an equal number of times per night, twice a night except for one night in which trials were only once, for nine nights the first two nights utilized a different procedure. Trials were run a total of 17 times for each call type. Only 15 trials were used in data analysis, however, since the data from July 21 were excluded based on abnormal activity possibly due to aberrant weather and the presence of a screaming animal. For each trial the call was played and then the numbers of visits were recorded for a five minute period following the call or silence. Calls were played , from various locations, for roughly one minute each to allow the bats time to hear the call and react. The frog call lasted 52 seconds, the owl 55 seconds and silence for approximately one minute. A visit was defined as a pause in front of the feeder; repeated visits by the same bat were counted as separate visits as described in Heuer 2004 and Díaz 2005. Visits were observed using a headlamp and small flashlight, both covered in red cellophane to minimize disturbance to the bats. Trials were space d 20 minutes apart to allow bats to forget the previous call. This period was chosen based on observations of the bats on the first two nights as being adequate recovery time. Also, based on the first two nights of observations, the most reliable predicto r of bat activity appeared to be presence of food in the feeder. On the subsequent nights feeders were refilled with a 20 % sugar solution by volume. Volume of sugar solution in the feeder was measured immediately before the call and after the five minut e period to determine volume eaten by the bats during each trial. Other data was recorded as well. The amount of moonlight was quantified as no moon, slight moon or nearly full. Weather conditions were recorded in regards to the degree of rain and were q uantified as dry, drizzle, rain and downpour. Number of visits per trial was the average of counts by two individuals. Number of visits as a percentage of the nightly average was used in data analysis to control for the fluctuations in numbers of visits each night between 481 and 922 visits per trial. Visits as a percentage of the nightly average was then analyzed with an ANOVA test to determine whether bats selectively

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4 avoid any treatment. ANOVA tests were also used to determine the effect of weather , moonlight and time of night on the number of visits. A regression was used to relate volume eaten with number of visits. On two nights bats were netted with butterfly nets to identify species using a guide by LaVal and Rodríguez H. 2002. RESULTS Th ree species of bats were found to visit the feeders. Anoura geoffroyi , Glossophaga commissarisi and Glossophaga soricina were all caught as they visited the feeder. All three species are common in the Monteverde area LaVal and Rodríguez H. 2002. There were significantly fewer visits to the feeder after the owl call than after either the frog call or the silent control ANOVA, F = 11.0203, p = 0.0001, df = 2; Figure 1. Weather was shown not to affect the number of visits in this experiment ANOVA, F = 1.5309, p = 0.2090, df = 4. Similarly, the time of night did not affect the number of visits during a trial ANOVA, F = 0.3316, p = 0.9593, df = 9. Moonlight was significantly related to number of visits within a trial, showing fewer bat visits with n o moon ANOVA, F = 5.2969, p = 0.0083, df = 2; Figure 2. In addition, volume eaten was compared with number of visits and no correlation was discovered R 2 = 0.0422, p = 0.1483, N = 51; Figure 3. Figure 1. Effect of call type on visits mean ± s. Da ta over all nights except July 21 shows a strong relationship with fewer visits after the owl call Means for frog, owl, silence:1.0212 ± 0.1028; 0.8918 ± 0.1209 and 1.0870 ± 0.1228 % nightly average is the number of visits in a trial divided by the avera ge number of visits per trial for that night. 0.5 0.6 0.7 0.8 0.9 1 1.1 1.2 1.3 frog owl silence call type % nightly visits

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5 0 200 400 600 800 1000 1200 almost full none slight Amount of Moonlight Visits 0 10 20 30 40 50 60 70 80 0 200 400 600 800 1000 1200 Visits Volume Change mL DISCUSSION Trials demonstrated that there were fewer visits after the owl call than the frog call or silence, supporting the hypothesis and predicti on of this study that bats avoid an auditorily perceived predator. The response to the predator call, reduction in number of visits to the feeder, supports the findings of Heuer 2004, Diaz 2005 and Baxter et al. 2006 that bats respond to the detecti on of predators with avoidance and that predator presence is an important factor in foraging activities. This is vitally important since in altering foraging behavior to avoid the predator, bats lose an opportunity to gain food and potentially reduce life time reproductive success Werner 1994. The fact that bats accept these costs to avoid predators indicates the importance of predation to these animals. Also, this study confirms the importance of owls as a predator of bats as was found in Heuer 2004 and Baxter et al. 2006. Finally, the relationship confirms the findings of Baxter et al. 2006, emphasizing that auditory cues are important for bats in the detection of predators. This study also clarifies the conclusions of Baxter et al. 2006 by determining whether their findings of reduced bat activity near woodpecker calls was the result of avoidance of a novel sound or an effect of acoustic interference. Since bats in this study did not avoid the frog call, it can be inferred that the bats in Baxter et al. 2006 were likely avoiding a novel sound and not acoustic interference. There was no novel sound in this trial so if the bats had avoided the feeder after the frog call, it would have been to avoid acoustic interference. Still, since the c alls were not played during the five minute periods in which visits were counted, the role of acoustic interference cannot totally be ruled out. Also, the bats observed in this study are nectarivorous bats in the tropics, visiting a known and consistent f eeding source. These bats likely have very different behavioral ecologies than insectivorous bats in British Columbia, the bats observed in Baxter et al. 2006, for which echolocation may play a more important role in foraging and therefore for which aco ustic interference would be a larger concern. Additionally, this study examined the effect of time of night, weather and moonlight on the number of visits to the feeders. Both time of night and weather did not Figure 2. Effect of moonlight on number of visits. There were significantly less visits in the absence of the moon. Figure 3. Volume change as a factor number of visits. No significant relationship was found. Fit line: Y = 25.3945 + 0.0140 X

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6 affect the number of visits indicating that p redator avoidance was likely responsible for differences in numbers of visits between trials. Diaz 2005 also noted no significant effects in visitation as a result of weather or time of night; however, she noted that bats are discouraged entirely from v isiting the feeder by heavy rain. In contrast, I noted no significant difference in visits over all weather types, recording upwards of 500 visits in the five minute periods in which there was torrential rain. The third effect examined was that of moonl ight. Heuer 2004 found a significant relationship indicating that with more moonlight there are fewer visits to the feeder. My study showed the opposite with significantly less bats on nights with no moon or obscured moon. This finding runs contrary t o findings with many different species of bats including vampires and insectivorous species, which seem to avoid moonlight presumably to avoid predation Altringham 1996. It also runs counter to the findings of Elangovan and Marimuthu 2001 who found th at the number of feeding visits of an Indian fruit bat to a tree was negatively correlated with percent moonlight. The significance of the current study s finding of fewer bats with less moonlight is that moonlight did not affect the number of visits to th e feeder in this experiment. The bats in this experiment may be less affected by the amount of moonlight because of the light conditions of the site. Although the garden is not lit at night and is surrounded by tall trees that block some of the surroundi ng light, there are buildings near the site with lights that may acclimatize the bats that visit these feeders and make the effect of extra moonlight less relevant. Lastly, volume measurements were taken as another way to measure potentially the bat activ ity at the feeder. This variable did not relate to visits, likely the result of a variety of difficulties ascertaining the correct volume of solution in the feeders. As a result, volume measurements were not used in any of the data analysis other than to demonstrate that volume eaten as well as could be measured does not seem to correlate with number of visits. If one were able to ensure that they were measuring the correct volume of sugar water consumed by the bats during the trial, it may tell a diffe rent story about foraging behavior and may be an interesting future study. Overall, this study reinforces the conclusions of previous studies that predator avoidance is a major factor in Chiropteran foraging behavior. It also emphasizes the importance of auditory cues in predator detection and their role in affecting foraging behavior, something only previously examined by one study. This previous study was carried out with insectivorous bats in British Columbia. Because the current study shows similar conclusions, but was with nectarivorous bats in Costa Rica, it demonstrates that avoidance of an auditorily perceived owl is a global trait of bats, emphasizing the importance of auditory cues and the role of owls as bat predators. Still, the high numbers of bats visiting after all treatments demonstrates the importance of these feeders as a food resource in the region. Additionally, this study clarified the findings of Baxter et al. 2006, suggesting that confounding results were the result of novel sou nd avoidance and not acoustic interference. Finally, this study examined the effects of weather and time of night and determined that they were not responsible for the differences in number of visits per trial. The effect of moonlight was also examined w ith unanticipated results. This was interpreted to mean that, contrary to the literature, moonlight did not significantly affect visitation in this particular experiment. Future studies may consider playing the call throughout the experimental period to look at the role of acoustic interference versus predator avoidance. This may also strengthen the differences between treatments since in this study visitation tended to recover quickly with bats only avoiding feeders for a short

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7 period, approximately one minute, after the owl calls. Future studies may also wish to examine how much food is actually consumed by the bats during each trial as a different measure of risk taking. ACKNOWLEDGEMENTS I would like to extend a tremendous thank you to Arturo Cruz f or accompanying me for nine nights, enduring extreme boredom and a lot of rain. I am also grateful to him for helping me net and identify the bats or rather, for identifying the bats. I would also like to thank Tania Chavarría for her guidance and assi stance throughout the entire process and especially with the statistics. I am very grateful to the owners of Selvatura for allowing me to use their site. Thanks to Karen Masters for her advice on improving my project, help with statistics and general gui dance. Thank you to Camryn Pennington and Pablo Allen for their help with statistics, general paper writing and, in Cam s case, for allowing me to bug her with questions while she studies for the GREs. I am very grateful to Nick Fabeck, Jessica Walthew an d Amy Elliott for help with Excel and editing. Lastly, Beth Schlimm has my eternal gratitude for sitting in a thunderstorm to assist me on the wettest data collecting night of them all. LITERATURE CITED Altringham, J.D. 1996. Bats: biology and behavio r. pp. 130, 219 221. Oxford University Press. New York, New York. Baxter, D. J. M., J. M. Psyllakis, M. P. Gillingham and E. L. O Brien. 2006. Behavioural response of bats to perceived predation risk while foraging. Ethology 112: 977 983. Berger, J. 1999. Anthropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose and ravens. Proceedings of the Royal Society of London 266: 2261 2267. Díaz, L. 2005. Effects of nov el object versus predator presence on nectarivorous bat foraging behavior. pp. 123 129. Tropical Ecology and Conservation. CIEE, Summer. Elangovan, V. and G. Marimuthu. 2001. Effect of moonlight on the foraging behaviour of a megachiropteran bat Cynopterus sphinx . Journal of Zoology 253: 347 350. Findley, J. S. 1993. Bats: a community perspective. pp. 25 26. Cambridge University Press. Cambridge, Great Britain. Fogden, M. 1993. An annotated checklist of the birds of Monteverde and Peñas Blancas. pp. 17 30. Michael Fogden. Monteverde, Costa Rica. Heuer, R. 2004. The effects of predator presence on nectarivorous bat foraging behavior. pp. 88 95. Tropical Ecology and Conservation. CIEE, Summer. LaVal, R. K. and B. Rodríguez H. 2002. Murciélagos de Costa Rica/ bats. pp. 134, 140 141, 144 145, 148 149. Editorial INBio. Costa Rica. Leenders, T. 2001. A guide to amphibians and reptiles of Costa Rica. pp. 102. Zona Tropical. Miami, Florida. Millard, E. 2004. Foraging strategies and body partitioning of glossophagine bats. pp. 1 11. Tropical Ecology and Conservation. CIEE, Spring. Nowak, R. M. 1994. Walker s bats of the world. pp. 125 129, 186 190. Johns Hopkins University Press. Baltimore, Maryland. Schnitzler, H. U. and E.K.V Kalko. 1998. How echolocating bats searc h and find food. In H. T. Kunz and P. A. Racey Eds.. Bat biology and conservation. pp. 183 196. Smithsonian Institution Press. Washington, DC. Werner, E. E. 1994. Individual behavior and higher order species interactions. In L. A. Real Ed.. Behavioral mechanisms in evolutionary ecology, pp. 300 301. University of Chicago Press. Chicago, Illinois.


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Predator presence is known to alter the foraging behavior of many species leading to decreased resource acquisition and lowered reproductive rate (Werner 1994). Previous studies have examined the effect of predator presence on the emergence of roosting bats and the effect of predator models on foraging bats (Baxter et al. 2006). Only one study, however, has examined the importance of auditory cues in alerting foraging bats to the presence of predators (in this case, owls; Baxter et al. 2006). The study concluded that bats not only avoid perceived owls but also the call of a diurnal woodpecker, leading the authors to question whether the latter finding was the result of novel sound avoidance or acoustic interference. This study, conducted in Monteverde, Costa Rica, investigated whether the findings of the earlier study were due to the effects of a novel sound or acoustic interference. Predator avoidance was quantified by counting number of visits to a hummingbird feeder after playing an owl call, a frog call or no call (a silent control). Significantly fewer visits were detected after the owl call than either the frog call or silence (ANOVA, F = 11.0203, p = 0.0001, df = 2) indicating the results of the previous study were due to novel sound avoidance. This study also reaffirmed the importance of auditory cues as a technique for predator detection in foraging bats, demonstrating a globally significant trait of bats.
Se sabe que la presencia de depredadores puede cambiar el comportamiento de forrajeo de muchas especies, llevando a una reduccin en la adquisicin de recursos y bajando la tasa reproductiva (Werner 1994). Estudios anteriores examinaron el efecto de la presencia de depredadores afuera de los sitios de descanso de los murcilagos y el efecto de los modelos de los depredadores en los murcilagos que forrajean (Baxter et al. 2006). Sin embargo, solamente un estudio examino la importancia de las seales auditivas como alerta ante depredadores sobre los murcilagos que forrajean (bhos en este caso; Baxter et al 2006). En este estudio se concluyo que los murcilagos no solo evitan a los bhos que perciben sino que tambin el canto de un carpintero diurno, lo que llevo a los autores a cuestionar si lo encontrado es el resultado de evasin de un nuevo sonido o de evitar la interferencia acstica. En este estudio, realizado en Monteverde, Costa Rica se investigo si los resultados del estudio anterior se deben a los efectos de un sonido nuevo o la interferencia acstica.
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