1 The Effects of Predator Presence on Nectarivorous Bat Foraging Behavior Rachael Heuer Department of Zoology, University of Florida ABSTRACT For many species, predator avoidance changes normal foraging behavior, altering optimal foraging strategies. In this study, foraging behavior of bats was examined by observing the number of feeding visits to control feeders in comparison to feeders with an artificial snake or owl in close proximity. Trials were also performed between snake and owl treatments to det ermine if one predator was more strongly avoided during feeding. Nectarivorous bats were found to exhibit predator avoidance behaviors for both snake and owl predators (P < 0.0001, P < 0.0001). There was no significant difference in trials comparing owl an d snake avoidance, suggesting that bats do not fear one more than the other (P = 0.947). This study shows that predator presence must be taken into account along with search time, handling time, and caloric reward when evaluating optimal foraging models wi th necatarivorous bats. RESUMEN Para muchas especies, evitar al depredador cambia el comportamiento normal para forrajear, alterando las estrategias Ã³ptimas para forrajear. En este estudio, se examinÃ³ el comportamiento para forrajear de murciÃ©lagos obse rvando el nÃºmero de visitas al alimentarse en los comederos control en comparciÃ³n con los comederos con una serpiente o un bÃºho artificial cerca en proximidad. Se realizaron ensayos tambiÃ©n entre los tratamientos con serpiente y con bÃºho para determinar si un depredador fue evitado mÃ¡s fuertemente durante la alimentaciÃ³n. Se encontrÃ³ que los murciÃ©lagos nectarÃvoros exhibieron comportamientos para evitar los despredadores tanto para el depredador serpiente y el bÃºho ( P < 0.0001, P < 0.0001). No hubo difere ncia significativa en los ensayos que comparaban el evitar el bÃºho y la serpiente, sugiriendo que los murciÃ©lagos no temen a uno mÃ¡s que al otro (P = 0.947). Este estudio demuestra que la presencia del despredador se debe tomar en cuenta junto con tiempo d e bÃºsqueda, manejando el tiempo, y la recompensa calÃ³rica cuando se evalÃºa los modelos Ã³ptimos con los murciÃ©lagos nectarÃvoros. INTRODUCTION The impacts of predator prey interactions on population structure and dynamics have been examined for years. Nu merous studies have observed the effects of predator presence on the foraging efficiency of prey species (Krebs and Davies 1981). Optimal foraging models have attempted to predict foraging strategies based upon search time, handling time, and caloric rewar d (Krebs and Davies 1981). It is likely that the presence of predators creates another variable in optimal foraging behavior. The foraging strategies of hummingbirds, birds, and insects have been found to be affected by predator presence. In a previous s tudy, it was found that hummingbirds visited feeders less frequently if there was an artificial predator in the vicinity, even if higher caloric rewards were found near the predator feeder (Flowers 1998). In another study, small birds were found to decreas e their feeding rates after a hawk predator was flown overhead (Alcock 1984). Insect species have also exhibited predator avoidance
2 behaviors while feeding. In one study, the presence of artificial predators reduced the overall number of insect visitation s to Clibadium leiocarpum (Asteraceae) (Tomon 1995). There appears to be a lack of information about the effects of predator presence on the feeding behavior of bat species. Bats have highly developed olfactory and echolocation sensory systems for foragi ng, allowing them to detect objects as thin as a mist net (Janzen 1983). The complexity of bat sensory systems suggest acute predator sensing ability. If predator presence affects foraging behavior of such a variety of organisms it is possible that bats mi ght exhibit similar behavior. This study attempted to determine if bats exhibit predator avoidance behavior while foraging, and whether avoidance was stronger with a certain type of predator. An artificial snake and owl were used as predators in this study because they are known to prey upon bats (Altringham 1996). It was hypothesized that higher numbers of bats will feed at control feeders rather than feeders with predators nearby. It was also hypothesized that there would be different responses to each ty pe of predator. METHODS Data were collected at feeders located at Selvatura near the Santa Elena Cloud Reserve between the dates of July 14 th and August 1 st in Santa Elena, Monteverde, Puntarenas province. Data collection occurred between 6:50 p.m. 9 p.m. for eight evenings. Selvatura contains 90% primary forest, 3% pasture, and 7% secondary forest and it is located on the Atlantic side of the TilirÃ¡n Mountain Range at 1612 meters (Solano pers. comm.). To imitate a snake both visually and olfactori ly, a rubber snake (1.55 m long, 0.03 m thick) was rubbed with snake scent obtained from the Serpentarium in Santa Elena, on July 19th, 22nd, and 29 th , 2004. An artificial owl (0.25 m long, 0.10 m wide) was constructed out of clay, chicken wire, and brown felt material in order to imitate the approximate size and shape of an average owl. Bird feathers from wild birds were obtained on July 16 th and 29 th , 2004 and attached to the artificial owl in order to imitate bird scent. For each time trial, two feeders six meters apart were monitored. Three types of treatments were used: snake versus control, owl versus control, and snake versus owl. Artificial predators were hung in the same horizontal level as feeder holes, approximately 0.25 meters from feeders. Othe r area feeders were removed to increase bat visitation at experimental feeders. Mag lights were used to spotlight feeders in order to view feeding. Control, snake, and owl feeders were rotated between trials to control for preset feeder preferences or effe cts of surrounding objects. The order of treatments was also rotated nightly to avoid patterns based upon feeding times. Eighteen ten minute observation periods were conducted for each treatment. The number of bats visiting each feeder was recorded over the ten minute intervals. Within each observation period, monitoring was alternated by ten second intervals between the two feeders. A feeding visit was counted as a pause in front of any one of the four feeder holes. Any bats that appeared to revisit a fe eder were counted as a new bat. Moonlight conditions were also recorded for each interval.
3 Means over ten minute time intervals were compared in order to test for preferred feeding times Paired t tests were used to compare feeder visitation at control ver sus owl, control versus snake, and owl versus snake treatments. An unpaired t test was used to compare feeder visitations in nights with full moon versus nights with partial moon cover. RESULTS Feeding activity was highest between 8:11 8:21 p.m. and the lowest between 6:54 7:04 p.m. (x: 188.5 and 65.056) (Figure 1). Lunar cycles were also found to effect bat feeding behavior, with a significantly lower number of overall feeder visits during full moon nights versus partial moon nights (Unpaired t test: t = 6.465, P < 0.0001) (Figure 2). The number of bat visits was significantly higher at control feeders when compared to both owl feeders and snake feeders (Paired t test: t = 5.115, P < 0.0001; t = 5.446, P < 0.0001) (Figure 3). Bats were not found to avo id one predator more than the other (Paired t test: t = 0.067, P = 0.9472; Figure 3). DISCUSSION As predicted, bats were found to exhibit less frequent feeding activity in the presence of both owl and snake artificial predators when compared to contro l treatments. It is clear that predator presence must be taken into account along with search time, handling time, and caloric reward when evaluating optimal foraging models. In order to better understand how predator avoidance fits into foraging strategy, manipulations of feeder sucrose concentrations may be necessary to test for trade offs between greater caloric rewards and predator avoidance. Comparisons of behavior at feeders and in natural habitats may also determine differences in predator avoidance behavior and optimal foraging strategy. The lack of a significant difference between avoidance of owl and snake predators suggests that bats do not find one of the predators more threatening than the other. Comparing bat response to predators with response to random objects would be useful to determine if bats avoid specific predators or if foreign objects of any kind near their food source produce a response. Outside factors could have affected the observed bat foraging behavior. Feeding times were the hig hest between 8:11 8:21 p.m., suggesting that bats may have an optimal feeding time. There was a decrease in overall feeding behavior with increases in lunar light. This is consistent with a study on frugivorous bats in Mexico where it was found that the nu mber of feeding visits was negatively correlated with percent moonlight (Elangovan and Marimuthu 2001). Throughout data collection, numerous bat vocalizations were heard. Bats are known to make food calls in order to increase group foraging behavior (Altri ngham 1996). These communications could have contributed to foraging behaviors in the presence of treatment feeders. Bats have been shown to have some memory capacity so it is possible that with successive nights there was less feeding activity due to avo idance of feeding disturbances (Janzen 1983). In addition to predator and control manipulations, mag lights could have caused overall reduced feeding rates.
4 Further studies are needed to determine more precise effects of predator presence on optimal fora ging strategies. Incorporating a measure of movement into predator treatments may be helpful in more closely mimicking real predators. It is unknown whether predator behavior is learned or a result of previous close encounters. A study on bat memory of pre dator locations may help further explain the importance of choice in optimal foraging strategy. Furthermore, it is possible that predator avoidance during foraging behavior may be population or geographically specific, and that certain populations may beco me habituated to different stimuli at the microhabitat level. To fully understand bat foraging behavior, studies on other aspects of feeding would be beneficial. Predator avoidance appears to be one of many complex factors that influence feeding behavior. ACKNOWLEDGEMENTS First of all, thanks to Carlos for supporting my bat project obsession, and for all the help along the way with the science and the logistics of the project. I have been so inspired by your passion for your work. Carmen Rojas, you were my hero numerous times, thank you for always arranging all of my visits and putting up with my last minute changes! Ollie and Maria, I am terribly sorry if you all get rabies, at least we will all be in d for overall making this trip an awesome experience for us. Thanks to Emily for making my trips much more bearable, and to Sean for inviting me to my very first mist net experience and Leah for providing me with bird feathers. Thanks to the Selvatura for the use of their hummingbird feeders, and to the Serpentarium for allowing me to get snake scent. Finally, to all of my new friends at CIEE, you have impacted me in more ways than you can ever imagine. I feel lucky to have gotten to spend time with such an stopped laughing since the first day in San Jose. LITERATURE CITED Alcock, J. 1984. Animal behavior: An evolutionary approach. pp. 270. Sinaur Associates, Inc. Sunderland, Massachusetts. Altringham, J. D. 1996. Bat s: biology and behavior. pp. 182 183, 219 221. Oxford University Press. New York, New York. Elangovan V. and Marimuthu G. 2001. Effect of moonlight on the foraging behaviour of a megachiropteram bat Cynopterus sphinx . Journal of Zoology. 253: 347 350. Flowers, T. 1998. Trade offs between caloric gain and anti predator defense in hummingbirds (Tochilidae). Tropical Ecology and Conservation. CIEE, Spring, pp. 150 162.
5 Janzen, D. 1983. Costa Rican natural history. pp. 431 435. University of Chicago Pr ess. Chicago, Illinois. Krebs J. R. and Davies, N. B. 1984. Behavioural ecology: An evolutionary approach. pp. 95 110. Sinauer Associates, Inc. Sunderland, Massachusetts. Tomon, T. J. 1995. Predator recognition by insects foraging at flowers of Clibadi um leiocarpum (Asteraceae). Tropical Ecology and Conservation. CIEE, Summer, pp. 236 244.
6 Figure 1: Mean number of bat visits per ten minute interval at hummingbird feede rs. Includes total number of treatments for each time interval averaged over 8 nights.
7 Figure 2: Comparison of mean number of bat visits at hummingbird feeders during full moonlight (x = 39.899 Â± 51.57) (N = 28) and partial moonlight (x = 199.643 Â± 114.284) (N = 28) (Unpai red t test: t = 6.465, P<0.0001). Error bars represent one standard deviation.
8 A B C Figure 3: Comparing the mean number of bat visits in treatments of A: owl (x = 80.333 Â± 67.973) versus control (x = 173.833 Â± 116.662) (Paired t test: t = 5.115, P < 0.0001) B: snake (x = 94.158 Â± 82.614) vers us control (x = 164.053 Â± 127.724) (Paired t test: t = 5.446, P < 0.0001P<0.0001) and C: owl (x = 113.474 Â± 94.306) versus snake (x = 113.947 Â± 94.341) (Paired t test: t = 0.067, P = 0.9472). Means were taken over 18 ten minute observation periods for eac h treatment. Error bars represent one standard deviation.
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Los efectos de la presencia de depredadores en el comportamiento de forrajeo de los murcilagos nectarvoros
The effects of predator presence on nectarivorous bat foraging behavior
For many species, predator avoidance changes normal foraging behavior, altering optimal foraging strategies. In this study, foraging behavior of bats was examined by observing the number of feeding visits to control feeders in comparison to feeders with an artificial snake or owl in close proximity. Trials were also performed between snake and owl treatments to determine if one predator was more strongly avoided during feeding. Nectarivorous bats were found to exhibit predator avoidance behaviors for both snake and owl predators (P < 0.0001, P < 0.0001). There was no significant difference in trials comparing owl and snake avoidance, suggesting that bats do not fear one more than the other (P = 0.947). This study shows that predator presence must be taken into account along with search time, handling time, and caloric reward when evaluating optimal foraging models with necatarivorous bats.
Para muchas especies, evitar al depredador cambia el comportamiento normal para forrajear, alterando las estrategias ptimas para forrajear. En este estudio, se examin el comportamiento para forrajear de murcilagos observando el nmero de visitas al alimentarse en los comederos control en comparacin con los comederos con una serpiente o un bho artificial cerca en proximidad. Se realizaron ensayos tambin entre los tratamientos con serpiente y con bho para determinar si un depredador fue evitado ms fuertemente durante la alimentacin. Se encontr que los murcilagos nectarvoros exhibieron comportamientos para evitar los depredadores tanto para el depredador serpiente y el bho (P < 0.0001, P < 0.0001). No hubo diferencia significativa en los ensayos que comparaban el evitar el bho y la serpiente, sugiriendo que los murcilagos no temen a uno ms que al otro (P = 0.947). Este estudio demuestra que la presencia del depredador se debe tomar en cuenta junto con tiempo de bsqueda, manejando el tiempo, y la recompensa calrica cuando se evalan los modelos ptimos con los murcilagos nectarvoros.
Text in English.
Costa Rica--Puntarenas--Monteverde Zone--Santa Elena
Costa Rica--Puntarenas--Zona de Monteverde--Santa Elena
Tropical Ecology Summer 2004
Ecologa Tropical Verano 2004
t Monteverde Institute : Tropical Ecology