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Lunar phobia in a neotropical fruit bat, Artibevs jamaicensis (Chiroptera: Phyllostomidae)
Anim. Behav ., 1978, 26, 8 5 2-855
LUNAR PHOBIA IN A NEOTROPICAL FRUIT BAT, ARTIBEUS JAMAICENSIS (CHIROPTERA : PHYLLOSTOMIDAE) BY
DOUGLAS W . MORRISON*
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853
Abstract. A radio-tracking study of the foraging behaviour of the Jamaican fruit bat (Artibeus jamaicensis) in a Panamanian forest revealed that searching and feeding flights were timed as if to minimize flying in bright moonlight . On nights I week before and after the new moon, foraging activity was continuous from dark to dawn . In contrast, on nights 1 week before and after the full moon radio-tagged individuals interrupted their feeding activity to return to their day roosts for the 1 to 7 h of the night when the moon was highest, even on nights when the moon was obscured by heavy clouds . Long flights in search of new fruit trees were observed only during the new moon half of the lunar month . Lunar phobia may have both endogenous and exogenous components that evolved to reduce losses to visually orientated predators . and continuous observations of foraging . A .
Moonlight has an inhibitory effect on the activity of certain nocturnal animals . In some species, such as Merriam's kangaroo rat Dipodomys merriami, moonlight avoidance behaviour takes the form of a shifting in foraging activity to areas of heavy cover during moonlight (Schwab 1966). In other species, such as the bannertail kangaroo rat (D. spectabilis), activity tends to be restricted to that part of the night when the moon is down (Lockard & Owings 1974) . In their review of moonlight avoidance in rodents, Lockard & Owings argue that moonlight avoidance probably reduces losses to visually orientated predators, and they cite the marked effects of nocturnal illumination on the hunting success of foxes (Vulpes vulpes) reported by Kruuk (1964) . Most of what is known about the foraging activity of bats has been deduced from data gathered by mist-netting. The common finding is that fewer bats are netted on moonlit nights . This is generally thought to mean that moonlight reduces foraging activity. It is not clear, however, whether the reduced capture rates reflect decreased activity or whether they are due to the bats' enhanced ability to avoid illuminated mist nets . In reduced light, deafened bats can avoid fine wires using vision alone (Bradbury & Nottebaum 1969) . The data presented here were gathered as part of a radio-tracking study of the Jamaican fruit bat (Artibeus jamaicensis) in Panama (Morrison 1975) . Fitting individual bats with miniature radio transmitters made it possible to make direct
jamaicensis was found to have a lunar phobia
similar to that of the bannertail kangaroo rat . Methods The Study Animal Artibeus jamaicensis is one of the larger species (45 to 50 g) of the family Phyllostomidae . Throughout Central America, the species is primarily frugivorous, showing a strong preference for figs (Ficus spp .) (Bonaccorso 1975 ; Heithaus et al . 1975) . In the semi-evergreen, moist tropical forest of Barro Colorado Island, Panama Canal Zone, where this study was conducted, A . jamaicensis roosted during the day in hollow trees or under broadleaf foliage .
Radio-tracking After being captured in nylon mist nets set across forest flyways, individual bats were fitted with miniature, 148-MHz radio transmitters (AVM Instrument Company model SM-1 with a Mallory WH-3 watchcell battery) fixed to the fur of the back with silicon adhesive (GE `Silastic' brand) . The weight of the entire transmitter package (3 .5 to 4 . 5 g) was less than 10% of body weight, the limit recommended for minimal behavioural distortion (Brander & Cochran 1969) . The attachment technique allowed the bats to scratch off the transmitters in 8 to 22 days. The location of a radio-tagged individual at night was determined by triangulation : bearings on the signal were taken regularly from several mapped points along the island's trail network using a hand held yagi antenna (modified Cushcraft A147-4) and portable receiver (AVM
*Present address : Department of Zoology and Physiology, Rutgers University, Newark, New Jersey 07102, U .S .A. 852
MORRISON
model LA-12) . In addition to position, the radio signal provided an indication of the bat's activity . When the bat was roosting, the signal pulses were of equal amplitude . During flight, the trailing 30 cm antenna wire whipped up and down, causing the relative volumes of the pulses to become distinctly variable . Signal variability was used to detect and count short feeding flights and to time longer searching flights . During the 8-month study (April to November 1973) observations were made on the nocturnal movements of 10 radio-tagged females and five radio-tagged males . The data presented here are drawn from over 650 h of observation made on over 100 nights of tracking . On 36 of these nights, radio contact was maintained unbroken from the time the bat left its day roost at dark until it returned at dawn . Results The basic foraging pattern of Artibeus jamaicensis each night was to emerge from the day roost as soon as it was dark (30 to 40 min after local sunset), fly (5 to 10 min) to a previously located fruit tree (up to 1 km from the day roost), establish a feeding roost in a second tree nearby (25 to 250 m), and make 10 to 15 feeding passes into the fruit trees to bring fruit back to the feeding roost (2 to 7 min each) before returning to the day roost at dawn (30 to 40 min before sunrise) . Flying time appeared to be kept to the minimum necessary to feed, with over 80% of the night spent roosting at various sites . Variations on this basic pattern were correlated with the phase of the moon . On nights during the `dark moon' half of the lunar month (one week before and after the new moon), when the face of the moon is less than half illuminated and does not cast much light, foraging activity was continuous from dark to dawn . On these `dark moon' nights a bat typically visited three to five different fruit trees . In contrast, during the `bright moon' half of the lunar month, the number of fruit trees visited per night was reduced to one or two and the bat suspended foraging activity to return to its day roost for the 1 to 7 h when the moon was nearest its zenith . Figure 1 shows 36 nights of tracking observations made on eight females (28 nights) and three males (eight nights) . Each line is placed according to the day of the lunar month on which the observation was made . For the sake of clarity, all emergence times and final return
853
LUNAR PHOBIA
times are shown equal to their approximate average values of 0 . 5 h after an 18 .00 hours (E.S.T .) local sunset and 0 .5 h before an 06.00 hours sunrise respectively . Figure 1 shows clearly that foraging activity is interrupted only on nights between the first and last quarter moon, when the face of the moon is relatively full . From first quarter to full moon, despite the presence of a relatively bright moon at sunset, A. jamaicensis left the day roost at the usual time, but stayed away long enough to complete only two or three feeding passes before returning to the day roost . At moonset these individuals re-emerged and foraged until dawn . From full moon to last quarter, the moon rises after sunset . On these nights A. jamaicensis began foraging at dark, returned to the day roost at moonrise, and usually re-emerged for a second bout of feeding just before dawn . Of the 14 nights of tracking observations made one week before and after the new moon, none was interrupted by a return to the day roost. In contrast, all of the 22 nights one week before and after the New
First
4
Last 14
J, I c
18.00
M
06 .00
TIME ACTIVE (Hours E .S .T .)
Fig. 1 . Foraging activity of radio-tagged A . jamatcensis relative to the phase of the moon . Each horizontal line represents time spent away from the day roost by a single bat on one night . Shaded areas cover those hours of the night when the moon is either set (upper right) or not yet risen (lower triangle) .
8 54
ANIMAL BEHAVIOUR, 26, 3
full moon were so interrupted, even those five when the moon was obscured by heavy clouds . Feeding flights were not the only aspect of foraging affected by the phase of the moon . New fruit trees were apparently located during unusually prolonged bouts of flying lasting 20 to 45 min (Morrison 1975) . These long searching flights were noted on only six nights, all of them `dark moon' nights . Discussion The moonlight avoidance response of A . jamaicensis is not cued simply to ambient light level . A . jamaicensis left the day roost after sunset even on nights when a bright moon was already present, and the bats returned to their day roosts even on nights when the moon was clouded over. At sunset hunger may be an overriding factor, causing the bats to emerge for a short bout of feeding despite the full moon . Unlike some smaller species of bats, A . jamaicensis does not go torpid during the day but maintains its body temperature at 38 ± 1 C (McManus & Nellis 1972). In their return to the day roost at moonrise, it is unlikely that the bats were simply mistaking moonrise for a premature sunrise . Artibeus jamaicensis begins feeding flights at 50 lux (Jimbo & Schwassman 1967) and the light of a full moon at its zenith is less than 0 .1 lux (Wells 1976). On heavily overcast nights the return time may have been determined in part by endogenous factors . A combination of endogenous and exogenous factors has been implicated in the sunset emergence and sunrise return of the insectivorous bat Myotis dasycneme (Voute et al . 1974) . Endogenous rhythms keyed to solar light-dark cycles have been known in bats for some time (Griffin & Welsh 1937), but a similar entrainment to lunar light-dark cycles has not yet been demonstrated . Lunar phobia is probably an adaptation for reducing losses to nocturnal predators that are at least partially visually orientated. Lockard & Owings (1974) argue that the sharp shadows cast by kangaroo rats in bright moonlight make their movements more conspicuous . This argument might also hold for A . jamaicensis that must forage in relatively open habitats . On Barro Colorado Island A . jamaicensis did most of its flying under the cover of the forest canopy . Here the shadows of the bats themselves did not seem to be as important as the patchwork of
light and shade cast by the moonlight coming through the canopy foliage . I found that the movements of the bats were much easier to detect when they could be viewed against this patchwork . Spectacled owls (Pulsatrix perspicillata) and black and white owls (Ciccaba nigrolineata) are two species of tropical wood owls known to take bats (Mikkola 1973). In general, large owls are opportunistic sit-and-wait predators . A bat flying in moonlight beneath a perched and waiting owl might be a particularly conspicuous target. The owl's strike would have to be quick, however, as large owls are not capable of sustained pursuits (Burton 1973) . Both the common opossum (Didelphis marsupialis) and the `four-eyed' opossum (Philander opossum) attack and feed on live bats caught in mist nets (Fleming 1972). A four-eyed opossum was apparently able to catch an A . jamaicensis coming to roost near it on a tree branch (Morrison 1975) . Selection pressure from stalking predators may explain why A . jamaicensis, and Artibeus species in general (Janzen et al. 1976), carry fruits away to relatively remote feeding roosts rather than consume them in the canopy of the fruit tree . Another possible source of predation is other species of bats. Trachops cirrhosus are known to eat lizards (Goodwin & Greenhall 1961) and will attack Carollia perspicillata cage mates (S . Graetz, personal communication) . Trachops were attracted by the alarm vocalizations of mist-netted A . jamaicensis (Morrison 1975) . Predation by larger carnivorous bats like the 80 to 100 g Phyllostomus hastatus and the 150 to 180-g Vampyrum spectrum may also be significant in the evolution and maintenance of lunar phobia . The hunting methods of these bats are not known, but may be similar to those of the large, carnivorous African false vampire bat (Cardioderma cor) which hangs in wait along forest trails and swoops down on large beetles and small bats passing by (Vaughn 1976) . A listing of probable predators does not constitute proof that lunar phobia evolved in response to predation pressure. Nevertheless, predation pressure seems to be the most reasonable explanation for the evolution of such energetically inefficient behaviour as limiting searching flights to nights with minimal moonlight, carrying away fruits to a feeding roost, and returning to the day roost in the midst of feeding.
MORRISON : LUNAR PHOBIA
Acknowledgments I greatly appreciate the assistance in radiotracking provided by Sally Graetz, Michael Perrone, Clark Sanford, and Julie Wiatt. I thank Jack Bradbury for his many helpful suggestions throughout this study, and James Anderson, Keith Hawthorne, Robert Lederhouse, Egbert Leigh, Michael Ryan, and Don Wilson for their comments and criticisms of the manuscript. This study was supported by N.S .F . Grant GB 32234X to J . Bradbury, N.S .F. Grant for the Improvement of Doctoral Dissertations GB 39708, a Sigma Xi Grant-in-Aid of Research, and the Smithsonian Tropical Research Institute . REFERENCES Bradbury, J. W . & Nottebaum, F . 1969 . The use of vision by the little brown bat, Myotis lucifugus, under controlled conditions . Anim. Behav., 17, 480-485 . Brander, R . B. & Cochran, W . W. 1969 . Radio-location telemetry . In : Wildlife Management Techniques (Ed . by R . H. Giles), pp. 95-103 . Washington, D .C. : Wildlife Society. Bonaccorso, F. 1975 . Foraging and reproductive ecology of a community of bats in Panama . Unpublished Ph .D . dissertation, University of Florida, (Univ . Microfilm No. 76-12,045) . Burton, J. A . 1973 . Owls of the World. New York : Dutton . Fleming, T . H. 1972. Aspects of the population dynamics of three species of opossums in the Panama Canal Zone. J. Mammal., 53, 619-623 . Goodwin, G . C. & Greenhall, A . M . 1961 . A review of bats of Trinidad and Tobago . Bull. Am . Mus. nat. Hist., 122, 187-302 . Griffin, D. R. & Welsh, J . H . 1937 . Activity rhythms in bats under constant external conditions . J. Mammal., 18, 337-342 . Heithaus, E. R ., Fleming, T . H . & Opler, P. A . 1975 . Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest . Ecology, 56, 841-854 .
855
Janzen, D. H ., Miller, G . A ., Hackforth-Jones, J., Pond, C . M ., Hooper, K. & Janos, D . P. 1976 . Two Costa Rican bat-generated seed shadows of Andira inermis (Leguminosae). Ecology, 57, 1068-1075 . Jimbo, S . & Schwassman, H. O . 1967 . Feeding behavior and daily emergence pattern of Artibeus jamaicensis. Atas do Simposio sobre a Biota Amazonica, 5, 239-253 . Kruuk, H. 1964 . Predators and anti-predator behavior of the black-headed gull (Larus ridibundis L .) Behaviour, Suppl . XI . Lockard, R. B. & Owings, D. H . 1974 . Moon-related surface activity of bannertail (Dipodomys spectabilis) and Fresno (D. nitratoides) kangaroo rats . Anim . Behav., 22, 262-273 . McManus, J . J. & Nellis, D . W. 1972 . Temperature regulation in three species of tropical bats . J . Mammal., 53, 226-227 . Mikkola, H. 1973 . Wood owls . In : Owls of the World. (Ed . by J . A . Burton), pp . 116-146 . New York : Dutton. Morrison, D . W . 1975 . Foraging behavior and feeding ecology of a neotropical fruit bat, Artibeus jamaicensis . Unpublished Ph.D . dissertation, Cornell University . (Univ . Microfilm No . 7612,879) . Schwab, R. G . 1966 . Environmental factors affecting surface activity of the kangaroo rat (Dipodomys merriami) . Unpublished Ph.D . dissertation, University of Arizona . (Univ. Microfilm No . 66-5139) . Vaughn, T. H . 1976 . Nocturnal behavior of the African false vampire bat (Cardioderma cor) . J. Mammal., 57, 227-248 . Voute, A . M., Sluiter, J . W . & Grimm, M . P. 1974 . The influence of the natural light-dark cycle on the activity rhythm of pond bats (Myosis dasycneme Boie, 1825) during summer. Oecologia, 17, 221243 . Wells, K . D. 1976 . Territorial behavior of the green frog Rana clamitans) . Unpublished Ph .D . dissertation, Cornell University . (Univ . Microfilm No . 7618,213) . (Received 27 February 1977 ; revised 18 May 1977 ; MS. number : A2005)
LUNAR PHOBIA IN A NEOTROPICAL FRUIT BAT, ARTIBEUS JAMAICENSIS (CHIROPTERA : PHYLLOSTOMIDAE) BY
DOUGLAS W . MORRISON*
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853
Abstract. A radio-tracking study of the foraging behaviour of the Jamaican fruit bat (Artibeus jamaicensis) in a Panamanian forest revealed that searching and feeding flights were timed as if to minimize flying in bright moonlight . On nights I week before and after the new moon, foraging activity was continuous from dark to dawn . In contrast, on nights 1 week before and after the full moon radio-tagged individuals interrupted their feeding activity to return to their day roosts for the 1 to 7 h of the night when the moon was highest, even on nights when the moon was obscured by heavy clouds . Long flights in search of new fruit trees were observed only during the new moon half of the lunar month . Lunar phobia may have both endogenous and exogenous components that evolved to reduce losses to visually orientated predators . and continuous observations of foraging . A .
Moonlight has an inhibitory effect on the activity of certain nocturnal animals . In some species, such as Merriam's kangaroo rat Dipodomys merriami, moonlight avoidance behaviour takes the form of a shifting in foraging activity to areas of heavy cover during moonlight (Schwab 1966). In other species, such as the bannertail kangaroo rat (D. spectabilis), activity tends to be restricted to that part of the night when the moon is down (Lockard & Owings 1974) . In their review of moonlight avoidance in rodents, Lockard & Owings argue that moonlight avoidance probably reduces losses to visually orientated predators, and they cite the marked effects of nocturnal illumination on the hunting success of foxes (Vulpes vulpes) reported by Kruuk (1964) . Most of what is known about the foraging activity of bats has been deduced from data gathered by mist-netting. The common finding is that fewer bats are netted on moonlit nights . This is generally thought to mean that moonlight reduces foraging activity. It is not clear, however, whether the reduced capture rates reflect decreased activity or whether they are due to the bats' enhanced ability to avoid illuminated mist nets . In reduced light, deafened bats can avoid fine wires using vision alone (Bradbury & Nottebaum 1969) . The data presented here were gathered as part of a radio-tracking study of the Jamaican fruit bat (Artibeus jamaicensis) in Panama (Morrison 1975) . Fitting individual bats with miniature radio transmitters made it possible to make direct
jamaicensis was found to have a lunar phobia
similar to that of the bannertail kangaroo rat . Methods The Study Animal Artibeus jamaicensis is one of the larger species (45 to 50 g) of the family Phyllostomidae . Throughout Central America, the species is primarily frugivorous, showing a strong preference for figs (Ficus spp .) (Bonaccorso 1975 ; Heithaus et al . 1975) . In the semi-evergreen, moist tropical forest of Barro Colorado Island, Panama Canal Zone, where this study was conducted, A . jamaicensis roosted during the day in hollow trees or under broadleaf foliage .
Radio-tracking After being captured in nylon mist nets set across forest flyways, individual bats were fitted with miniature, 148-MHz radio transmitters (AVM Instrument Company model SM-1 with a Mallory WH-3 watchcell battery) fixed to the fur of the back with silicon adhesive (GE `Silastic' brand) . The weight of the entire transmitter package (3 .5 to 4 . 5 g) was less than 10% of body weight, the limit recommended for minimal behavioural distortion (Brander & Cochran 1969) . The attachment technique allowed the bats to scratch off the transmitters in 8 to 22 days. The location of a radio-tagged individual at night was determined by triangulation : bearings on the signal were taken regularly from several mapped points along the island's trail network using a hand held yagi antenna (modified Cushcraft A147-4) and portable receiver (AVM
*Present address : Department of Zoology and Physiology, Rutgers University, Newark, New Jersey 07102, U .S .A. 852
MORRISON
model LA-12) . In addition to position, the radio signal provided an indication of the bat's activity . When the bat was roosting, the signal pulses were of equal amplitude . During flight, the trailing 30 cm antenna wire whipped up and down, causing the relative volumes of the pulses to become distinctly variable . Signal variability was used to detect and count short feeding flights and to time longer searching flights . During the 8-month study (April to November 1973) observations were made on the nocturnal movements of 10 radio-tagged females and five radio-tagged males . The data presented here are drawn from over 650 h of observation made on over 100 nights of tracking . On 36 of these nights, radio contact was maintained unbroken from the time the bat left its day roost at dark until it returned at dawn . Results The basic foraging pattern of Artibeus jamaicensis each night was to emerge from the day roost as soon as it was dark (30 to 40 min after local sunset), fly (5 to 10 min) to a previously located fruit tree (up to 1 km from the day roost), establish a feeding roost in a second tree nearby (25 to 250 m), and make 10 to 15 feeding passes into the fruit trees to bring fruit back to the feeding roost (2 to 7 min each) before returning to the day roost at dawn (30 to 40 min before sunrise) . Flying time appeared to be kept to the minimum necessary to feed, with over 80% of the night spent roosting at various sites . Variations on this basic pattern were correlated with the phase of the moon . On nights during the `dark moon' half of the lunar month (one week before and after the new moon), when the face of the moon is less than half illuminated and does not cast much light, foraging activity was continuous from dark to dawn . On these `dark moon' nights a bat typically visited three to five different fruit trees . In contrast, during the `bright moon' half of the lunar month, the number of fruit trees visited per night was reduced to one or two and the bat suspended foraging activity to return to its day roost for the 1 to 7 h when the moon was nearest its zenith . Figure 1 shows 36 nights of tracking observations made on eight females (28 nights) and three males (eight nights) . Each line is placed according to the day of the lunar month on which the observation was made . For the sake of clarity, all emergence times and final return
853
LUNAR PHOBIA
times are shown equal to their approximate average values of 0 . 5 h after an 18 .00 hours (E.S.T .) local sunset and 0 .5 h before an 06.00 hours sunrise respectively . Figure 1 shows clearly that foraging activity is interrupted only on nights between the first and last quarter moon, when the face of the moon is relatively full . From first quarter to full moon, despite the presence of a relatively bright moon at sunset, A. jamaicensis left the day roost at the usual time, but stayed away long enough to complete only two or three feeding passes before returning to the day roost . At moonset these individuals re-emerged and foraged until dawn . From full moon to last quarter, the moon rises after sunset . On these nights A. jamaicensis began foraging at dark, returned to the day roost at moonrise, and usually re-emerged for a second bout of feeding just before dawn . Of the 14 nights of tracking observations made one week before and after the new moon, none was interrupted by a return to the day roost. In contrast, all of the 22 nights one week before and after the New
First
4
Last 14
J, I c
18.00
M
06 .00
TIME ACTIVE (Hours E .S .T .)
Fig. 1 . Foraging activity of radio-tagged A . jamatcensis relative to the phase of the moon . Each horizontal line represents time spent away from the day roost by a single bat on one night . Shaded areas cover those hours of the night when the moon is either set (upper right) or not yet risen (lower triangle) .
8 54
ANIMAL BEHAVIOUR, 26, 3
full moon were so interrupted, even those five when the moon was obscured by heavy clouds . Feeding flights were not the only aspect of foraging affected by the phase of the moon . New fruit trees were apparently located during unusually prolonged bouts of flying lasting 20 to 45 min (Morrison 1975) . These long searching flights were noted on only six nights, all of them `dark moon' nights . Discussion The moonlight avoidance response of A . jamaicensis is not cued simply to ambient light level . A . jamaicensis left the day roost after sunset even on nights when a bright moon was already present, and the bats returned to their day roosts even on nights when the moon was clouded over. At sunset hunger may be an overriding factor, causing the bats to emerge for a short bout of feeding despite the full moon . Unlike some smaller species of bats, A . jamaicensis does not go torpid during the day but maintains its body temperature at 38 ± 1 C (McManus & Nellis 1972). In their return to the day roost at moonrise, it is unlikely that the bats were simply mistaking moonrise for a premature sunrise . Artibeus jamaicensis begins feeding flights at 50 lux (Jimbo & Schwassman 1967) and the light of a full moon at its zenith is less than 0 .1 lux (Wells 1976). On heavily overcast nights the return time may have been determined in part by endogenous factors . A combination of endogenous and exogenous factors has been implicated in the sunset emergence and sunrise return of the insectivorous bat Myotis dasycneme (Voute et al . 1974) . Endogenous rhythms keyed to solar light-dark cycles have been known in bats for some time (Griffin & Welsh 1937), but a similar entrainment to lunar light-dark cycles has not yet been demonstrated . Lunar phobia is probably an adaptation for reducing losses to nocturnal predators that are at least partially visually orientated. Lockard & Owings (1974) argue that the sharp shadows cast by kangaroo rats in bright moonlight make their movements more conspicuous . This argument might also hold for A . jamaicensis that must forage in relatively open habitats . On Barro Colorado Island A . jamaicensis did most of its flying under the cover of the forest canopy . Here the shadows of the bats themselves did not seem to be as important as the patchwork of
light and shade cast by the moonlight coming through the canopy foliage . I found that the movements of the bats were much easier to detect when they could be viewed against this patchwork . Spectacled owls (Pulsatrix perspicillata) and black and white owls (Ciccaba nigrolineata) are two species of tropical wood owls known to take bats (Mikkola 1973). In general, large owls are opportunistic sit-and-wait predators . A bat flying in moonlight beneath a perched and waiting owl might be a particularly conspicuous target. The owl's strike would have to be quick, however, as large owls are not capable of sustained pursuits (Burton 1973) . Both the common opossum (Didelphis marsupialis) and the `four-eyed' opossum (Philander opossum) attack and feed on live bats caught in mist nets (Fleming 1972). A four-eyed opossum was apparently able to catch an A . jamaicensis coming to roost near it on a tree branch (Morrison 1975) . Selection pressure from stalking predators may explain why A . jamaicensis, and Artibeus species in general (Janzen et al. 1976), carry fruits away to relatively remote feeding roosts rather than consume them in the canopy of the fruit tree . Another possible source of predation is other species of bats. Trachops cirrhosus are known to eat lizards (Goodwin & Greenhall 1961) and will attack Carollia perspicillata cage mates (S . Graetz, personal communication) . Trachops were attracted by the alarm vocalizations of mist-netted A . jamaicensis (Morrison 1975) . Predation by larger carnivorous bats like the 80 to 100 g Phyllostomus hastatus and the 150 to 180-g Vampyrum spectrum may also be significant in the evolution and maintenance of lunar phobia . The hunting methods of these bats are not known, but may be similar to those of the large, carnivorous African false vampire bat (Cardioderma cor) which hangs in wait along forest trails and swoops down on large beetles and small bats passing by (Vaughn 1976) . A listing of probable predators does not constitute proof that lunar phobia evolved in response to predation pressure. Nevertheless, predation pressure seems to be the most reasonable explanation for the evolution of such energetically inefficient behaviour as limiting searching flights to nights with minimal moonlight, carrying away fruits to a feeding roost, and returning to the day roost in the midst of feeding.
MORRISON : LUNAR PHOBIA
Acknowledgments I greatly appreciate the assistance in radiotracking provided by Sally Graetz, Michael Perrone, Clark Sanford, and Julie Wiatt. I thank Jack Bradbury for his many helpful suggestions throughout this study, and James Anderson, Keith Hawthorne, Robert Lederhouse, Egbert Leigh, Michael Ryan, and Don Wilson for their comments and criticisms of the manuscript. This study was supported by N.S .F . Grant GB 32234X to J . Bradbury, N.S .F. Grant for the Improvement of Doctoral Dissertations GB 39708, a Sigma Xi Grant-in-Aid of Research, and the Smithsonian Tropical Research Institute . REFERENCES Bradbury, J. W . & Nottebaum, F . 1969 . The use of vision by the little brown bat, Myotis lucifugus, under controlled conditions . Anim. Behav., 17, 480-485 . Brander, R . B. & Cochran, W . W. 1969 . Radio-location telemetry . In : Wildlife Management Techniques (Ed . by R . H. Giles), pp. 95-103 . Washington, D .C. : Wildlife Society. Bonaccorso, F. 1975 . Foraging and reproductive ecology of a community of bats in Panama . Unpublished Ph .D . dissertation, University of Florida, (Univ . Microfilm No. 76-12,045) . Burton, J. A . 1973 . Owls of the World. New York : Dutton . Fleming, T . H. 1972. Aspects of the population dynamics of three species of opossums in the Panama Canal Zone. J. Mammal., 53, 619-623 . Goodwin, G . C. & Greenhall, A . M . 1961 . A review of bats of Trinidad and Tobago . Bull. Am . Mus. nat. Hist., 122, 187-302 . Griffin, D. R. & Welsh, J . H . 1937 . Activity rhythms in bats under constant external conditions . J. Mammal., 18, 337-342 . Heithaus, E. R ., Fleming, T . H . & Opler, P. A . 1975 . Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest . Ecology, 56, 841-854 .
855
Janzen, D. H ., Miller, G . A ., Hackforth-Jones, J., Pond, C . M ., Hooper, K. & Janos, D . P. 1976 . Two Costa Rican bat-generated seed shadows of Andira inermis (Leguminosae). Ecology, 57, 1068-1075 . Jimbo, S . & Schwassman, H. O . 1967 . Feeding behavior and daily emergence pattern of Artibeus jamaicensis. Atas do Simposio sobre a Biota Amazonica, 5, 239-253 . Kruuk, H. 1964 . Predators and anti-predator behavior of the black-headed gull (Larus ridibundis L .) Behaviour, Suppl . XI . Lockard, R. B. & Owings, D. H . 1974 . Moon-related surface activity of bannertail (Dipodomys spectabilis) and Fresno (D. nitratoides) kangaroo rats . Anim . Behav., 22, 262-273 . McManus, J . J. & Nellis, D . W. 1972 . Temperature regulation in three species of tropical bats . J . Mammal., 53, 226-227 . Mikkola, H. 1973 . Wood owls . In : Owls of the World. (Ed . by J . A . Burton), pp . 116-146 . New York : Dutton. Morrison, D . W . 1975 . Foraging behavior and feeding ecology of a neotropical fruit bat, Artibeus jamaicensis . Unpublished Ph.D . dissertation, Cornell University . (Univ . Microfilm No . 7612,879) . Schwab, R. G . 1966 . Environmental factors affecting surface activity of the kangaroo rat (Dipodomys merriami) . Unpublished Ph.D . dissertation, University of Arizona . (Univ. Microfilm No . 66-5139) . Vaughn, T. H . 1976 . Nocturnal behavior of the African false vampire bat (Cardioderma cor) . J. Mammal., 57, 227-248 . Voute, A . M., Sluiter, J . W . & Grimm, M . P. 1974 . The influence of the natural light-dark cycle on the activity rhythm of pond bats (Myosis dasycneme Boie, 1825) during summer. Oecologia, 17, 221243 . Wells, K . D. 1976 . Territorial behavior of the green frog Rana clamitans) . Unpublished Ph .D . dissertation, Cornell University . (Univ . Microfilm No . 7618,213) . (Received 27 February 1977 ; revised 18 May 1977 ; MS. number : A2005)