Island Bats: Evolution, Ecology, and Conservation

Island Bats

Island Bats Evolution, Ecology, and Conservation

Edited by

Theodore H. Fleming and Paul A. Racey

The University of Chicago Press Chicago and London

Theodore H. Fleming is professor emeritus of biology at the University of Miami in Coral Gables, Florida. Paul A. Racey is the Regius Professor of Natural History (emeritus) in the School of Biological Sciences at the University of Aberdeen, Scotland.

The University of Chicago Press, Chicago 60637 The University of Chicago Press, Ltd., London © 2009 by The University of Chicago All rights reserved. Published 2009 Printed in the United States of America 18 17 16 15 14 13 12 11 10 09   1 2 3 4 5 ISBN-13: 978-0-226-25330-5   (cloth) ISBN-10: 0-226-25330-9   (cloth) Library of Congress Cataloging-in-Publication Data Island bats: evolution, ecology, and conservation / edited by Theodore H. Fleming and Paul A. Racey.    p. cm.   Includes index.   ISBN-13: 978-0-226-25330-5 (cloth : alk. paper)   ISBN-10: 0-226-25330-9 (cloth: alk. paper)  1. Bats.  2. Bats—Ecology. 3. Bats—Conservation.  4. Bats—Islands of the Pacific.  5. Bats—West Indies. 6. Island Animals­  I. Fleming, Theodore H.  II. Racey, P. A.   QL737.C5185 2009   599.4’1752­—dc22 2009028840 a The paper used in this publication meets the minimum requirements of the American National Standard for Information Sciences—Permanence of Paper for Printed Library Materials, ANSI Z39.48-1992.

C O NT E NTS

1

An Introduction to Island Bats 1

Theodore H. Fleming and Paul A. Racey

P A R T

2

1 .

E V O L U T I O N

O F

I SLAND

B ATS

New Perspectives on the Long-Term Biogeographic Dynamics and Conservation of Philippine Fruit Bats 17

Lawrence R. Heaney and Trina E. Roberts

3

Crossing the Line: The Impact of Contemporary and Historical Sea Barriers on the Population Structure of Bats in Southern Wallacea Lincoln H. Schmitt, Susan Hisheh, Agustinus Suyanto, Maharadatunkamsi, Christopher N. Newbound, Darrell J. Kitchener, and Richard A. How

4

Earth History and the Evolution of Caribbean Bats 96

Liliana M. Dávalos

5

Phylogeography and Genetic Structure of Three Evolutionary Lineages of West Indian Phyllostomid Bats Theodore H. Fleming, Kevin L. Murray, and Bryan Carstens

P A R T

6

2 .

E C O L O G Y

O F

I SLAND

116 B ATS

Physiological Adaptation of Bats and Birds to Island Life 153

Brian K. McNab

7

59

The Role of Pteropodid Bats in Reestablishing Tropical Forests on Krakatau Louise A. Shilton and Robert J. Whittaker

176

8

Macroecology of Caribbean Bats: Effects of Area, Elevation, Latitude, and Hurricane-Induced Disturbance Michael R. Willig, Steven J. Presley, Christopher P. Bloch, and Hugh H. Genoways 216

9

Bat Assemblages in the West Indies: The Role of Caves 265

Armando Rodríguez-Durán



Contents

vi

10 Island in the Storm: Disturbance Ecology of Plant-Visiting Bats on the Hurricane-Prone Island of Puerto Rico Michael R. Gannon and Michael R. Willig 281 11 Bats of Montserrat: Population Fluctuation and Response to Hurricanes and Volcanoes, 1978–2005 Scott C. Pedersen, Gary G. Kwiecinski, Peter A. Larsen, Mathew N. Morton, Rick A.

302

Adams, Hugh H. Genoways, and Vicki J. Swier

12 Flying Fox Consumption and Human Neurodegenerative Disease in Guam 341

Sandra Anne Banack, Paul Alan Cox, and Susan J. Murch

P A R T

3 .

C O NS E R V AT I O N

O F

I SLAND

B ATS

13 The Ecology and Conservation of Malagasy Bats Paul A. Racey, Steven M. Goodman, and Richard K. B. Jenkins

369

14 Conservation Threats to Bats in the Tropical Pacific Islands and Insular Southeast Asia Gary J. Wiles and Anne P. Brooke 405 15 The Ecology and Conservation of New Zealand Bats Colin F. J. O’Donnell

460

16 Global Overview of the Conservation of Island Bats: Importance, Challenges, and Opportunities Kate E. Jones, Simon P. Mickleburgh, Wes Sechrest, and Allyson L. Walsh

496



List of Contributors

531



Subject Index

535



Species Index

539



Color gallery follows page 314

Chapter 1

An Introduction to Island Bats Theodore H. Fleming and Paul A. Racey

Introduction One of us (THF) recently polled colleagues in his department about their immediate visual response to the phrase “tropical islands.” In addition to the usual images of aquamarine seas, turquoise lagoons, white sandy beaches, and lush green vegetation, people mentioned coral reefs, volcanoes, basalt, palm trees, and hammocks. By and large most of these respondents pictured benign scenes of tranquility and beauty—scenes that you would typically see in tourist brochures. But, as will become abundantly clear in this volume, the biological reality of island life is far from benign and tranquil. Ask these same people to describe “tropical islands” in less visual and more biological terms, and their responses might include such terms as “limited species diversity,” “limited space and resources,” “fewer predators,” “physiologically harsh environments,” “frequent disturbances caused by tropical storms, earthquakes, and erupting volcanoes,” and, with increasing frequency and intensity, “human disturbance.” For the organisms that have successfully colonized them, isolated oceanic islands worldwide can be anything but benign and Eden-like places to live. Despite, or perhaps because of, their isolation, and limited space, resources, and species richness, islands and their species have long fascinated biologists. With their reputation as being living laboratories, islands have provided ecologists and evolutionary biologists with a much greater number of fundamen­ tal concepts than their total area (about 3% of Earth’s surface; Whittaker 1998) might suggest. Beginning with Darwin’s and Wallace’s seminal idea of organic evolution via natural selection (Darwin and Wallace 1858), these con­ cepts include adaptive radiation, Sewall Wright’s (1931) island and stepping stone models of population genetics, Ernst Mayr’s (1942) concept of allopatric speciation and the importance of founder effects, Edward O. Wilson’s (1961) taxon cycle, Robert MacArthur and E. O. Wilson’s (1963, 1967) equilibrium theory of island biogeography and r and K selection, Jared Diamond’s (1975) community assembly rules, Graeme Caughley’s (1994) small-population paradigm in conservation biology, and Ilka Hanski and Michael Gilpin’s (1997) recent versions of metapopulation theory (table 1.1). Collectively, these concepts





T. H. Fleming and P. A. Racey

Table 1.1.  Major concepts or theories in evolution and ecology resulting from or inspired by islands and their biogeography (modified from Whittaker 1998). Concept or Theory

Authors and/or examples

Evolution by natural selection

C. Darwin (Galapagos), A. Wallace (Indonesia)

Adaptive radiation

Galapagos finches, Hawaiian honeycreepers, Hawaiian Drosophila, New Guinea birds of paradise, Caribbean Anolis, Madagascan lemurs and tenrecs, Galapagos Scalesia, Hawaiian silverswords

Island and stepping stone models of population genetics

S. Wright

Allopatric speciation and founder effects

E. Mayr (New Guinea, Pacific islands)

Taxon cycle

E. Wilson (ants, Melanesia), R. Ricklefs (birds, Lesser Antilles)

Equilibrium theory of island biogeography

R. MacArthur, E. Wilson (Pacific and Caribbean islands)

r and K selection

R. MacArthur, E. Wilson

Community assembly rules

J. Diamond (birds, New Guinea and surrounding islands)

Small-population paradigm in conservation biology

G. Caughley (small island populations)

Metapopulations

R. Levins, I. Hanski, M. Gilpin

represent many of the basic cornerstones of modern evolutionary, ecological, and conservation thinking. In addition to inspiring many important biological concepts, islands and their faunas and floras have been endlessly fascinating to biologists because of their intrinsic physical and biological features, many of which are summa­ rized in table 1.2. The important physical features associated with islands are generally well-known. Two of those features—geological substrates and degree of natural disturbance—are particularly important for bats, the major subject of this book. Like their continental relatives, many island-dwelling bats use caves for their day roosts, and basic island geology can determine the extent and physical nature of caves. Many islands lie on the boundaries of crustal plates or above crustal “hot spots” and hence occur in areas of intense seismic activity. This activity can have strong negative effects on island floras and faunas. Additionally, many tropical islands occur in hurricane or typhoon zones, whose storms can also have devastating effects on populations of plants and animals. Biological features of islands include reduced species richness (impoverishment) and taxonomically and ecologically skewed (disharmonic) faunas and floras favoring organisms with excellent over-water dispersal abilities (table 1.2). Interesting ecological features of island endemics often include



An Introduction to Island Bats



Table 1.2.  What’s so special or interesting about islands? Topic

Details

Physical features

Size, number or habitats, geological substrates, isolation, disturbance prone (nonanthropogenic)

Biological features

Impoverishment, disharmony, dispersal, loss of dispersal ability, reproductive changes, body-size changes, broad ecological niches, high population density, tameness, extinction prone

Biodiversity features

Disproportionately high number of species overall occur on islands. Plants: about 1/6 of all species occur on islands; birds: about 1/6 of all species occur on islands; bats: 3/17 families occur only on islands; reptiles: 1/2 of all species of Anolis lizards occur on islands

Conservation concerns

Disproportionately high number of extinctions occur on islands. Birds: 40× higher extinction rate in island species than continental species; mammals: except for bats (~14%), 83–100% of West Indian land mammals are extinct; reptiles: “majority of extinctions have occurred on islands”

Sources: Based on Grant 1998; Whittaker 1998; Williamson 1981.

reduced fecundity and dispersal ability (e.g., loss of flight), higher population densities, broader ecological niches, reduced fear of predators, larger or smaller body sizes, and elevated rates of extinction compared with their continental relatives. Island faunas and floras are also notable for harboring high proportions of endemic species such that islands contribute (or contributed) a disproportionately high number of species to Earth’s biodiversity. Levels of endemism are uniformly high in flowering plants, birds, and bats on islands. In terms of numbers of endemic families or subfamilies and their genera and species, island birds are more diverse than island bats (tables 1.3 and 1.4). Fourteen families or subfamilies of birds containing 47 genera and 86 species are island endemics, compared with only 5 families or subfamilies of bats containing 7 genera and 25 species. With 5 endemic families, Madagascar has the greatest number of endemic bird families. With 2 endemic subfamilies of phyllostomid bats, the West Indies is the site of greatest endemism at higher taxonomic levels in bats. Two other groups of West Indian bats—family Natalidae and the phyllostomid tribe Stenodermatina of subfamily Stenodermatinae—evolved in the Caribbean and then colonized the mainland of Mexico and Central and South America (Dávalos, chapter 4, this volume) and hence are not strictly endemic to those islands. Finally, island faunas and floras are notable because of their high conservation concerns. About one-quarter of the 25 global biodiversity hot spots identified by Myers et al. (2000) because of their exceptional conservation concern, for example, are island systems. These areas include the Caribbean, Madagascar, Sundaland, Wallacea, the Philippines, Polynesia/Micronesia, and New Zealand. Each of these areas contains endemic species of island-dwelling bats,

Apterygidae Rhynochetidae Mesitornithidae Todidae Brachypteraciidae Leptosomatidae Acanthisittidae Philepittidae Callaeidae Vangidae Dulidae Rhabdornithidae Drepanidinae Emberizidae, Geospizinae 14

Dinornithoiformes Gruiformes Gruiformes Coraciiformes Coraciiformes Coraciiformes Tyranni Tyranni Passeres Passeres Passeres Passeres Passeres Passeres   Total

Sources: Gill 1990; Craycraft et al. 2003.

Family or subfamily

Order or suborder

Name Kiwis Kagu Mesites Todies Ground rollers Cuckoo rollers N Z wrens Asities Wattlebirds Vangas Palmchat Philippine creepers Hawaiian honeycreepers Galápagos finches

Table 1.3.  Extant endemic families and subfamilies of island birds

N Zealand N Caledonia Madagascar W Indies Madagascar Madagascar N Zealand Madagascar N Zealand Madagascar W Indies Philippines Hawaii Galápagos

Island 1 1 2 1 4 1 2 2 3 15 1 1 10 3 47

N genera

3 1 3 5 5 1 4 4 3 22 1 2 23 13 90

N species



An Introduction to Island Bats



Table 1.4.  Extant endemic families and subfamilies of island bats Family or subfamily

Name

Islands

N genera

N species

Pteropodidae, Nyctimeninae

Tube-nosed bats

New Guinea, Philippines (and Australia)

2

15

Myzopodidae

Old World sucker-footed bats

Madagascar

1

2

Mystacinidae

New Zealand short-tailed bats

New Zealand

1

2

Phyllostomidae, Phyllonycterinae

West Indian flower bats

Greater Antilles

2

5

Phyllostomidae, Brachyphyllinae

West Indian fruit bats

Greater and Lesser Antilles

1

2

7

26

  Total

5

Source: Simmons 2005.

many of which are considered to be “threatened” by the IUCN. More generally, extinction rates of island plants and animals are considerably higher than those of their continental relatives. In birds, for example, extinction rates on islands are 40 times higher than they are elsewhere in the world. Similarly, in the West Indies, 83–100% of nonvolant mammals, depending on family, are extinct, although only 14% of West Indian bats are known to be extinct. Likewise, most known extinctions of reptiles have occurred on islands. Most, but not all (e.g., West Indian bats; Morgan 2001), of these extinctions have an anthropogenic cause resulting from habitat destruction, overhunting, and the introduction of exotic species (including pathogens).

Overview of Bats on Islands Because they can fly, bats often represent most or all of the extant mammals on isolated oceanic islands. They are the only native land mammals on Hawaii, New Zealand, and many Pacific islands, for example. Island bats also contribute significantly to the overall species richness of bats. Jones et al. (chapter 16, this volume) report that fully 60% of all bat species live on islands (n = 925) and that 25% of all bats are island endemics; 8% of all bats are single-island endemic species. Thus islands have played an especially important role in the overall evolution of bats. In addition to being of considerable evolutionary interest, plant-visiting bats are particularly important as pollinators and seed dispersers in tropical island ecosystems (e.g., Cox et al. 1991; Cox et al. 1992; Elmqvist et al. 1992; Rainey et al. 1995). Banack’s work (1998) in American Samoa, for example, indicates that two species of Pteropus flying foxes feed on flower and fruit resources of 78 plant species throughout their ranges and on



T. H. Fleming and P. A. Racey

69 plant species on Samoa alone. Many of their food resources are produced by canopy trees in primary forests, and bats are likely to be their sole dispersers. Although fruit-eating bats appear to play a more important role in the early stages of ecological succession in the Neotropics than in the Paleotropics (Muscarella and Fleming 2007), pteropodid bats have played an important role in the recolonization of Krakatau by plants (e.g., Whittaker and Jones 1994). The ability to retain seeds in viable condition in their guts for up to 19 hours makes pteropodid bats especially important as long-distance dispersers of the seeds of island plants (Shilton et al. 1999). Finally, island bats are the source of considerable conservation concern. Jones et al. (chapter 16, this volume) indicate that nearly 50% of threatened bats worldwide (i.e., species designated as VU, EN, or CR in IUCN 2006) are island endemics; an additional 22% of threatened bats are single-island endemics. Not only will the loss of these bats contribute to a decrease in global biodiversity, but it also represents the loss of important ecological services such as predation on insects as well as pollination and seed dispersal. McConkey and Drake (2006), for instance, reported that seed dispersal by flying foxes declined nonlinearly with a decline in relative bat abundance on Vava’u (Tonga, Polynesia). Below a threshold abundance value, bats moved 0.99, table 3.3), which is unexpected if there had been recent gene flow between islands that are genetically distinct.

A

B

Figure 3.8.  Cynopterus nusatenggara. A, Position of islands on the first two axes from ordination of the arc genetic distance matrix. B, Plot of mean island heterozygosity on longitude (degrees east) with the estimated regression line (solid ) and a broken line drawn at 4.4%, an estimate of the mammalian average. See figure 3.3 for further explanation.

A

B

Figure 3.9.  Macroglossus minimus. A, Position of islands on the first two axes from ordination of the arc genetic distance matrix. B, Plot of mean island heterozygosity on longitude (degrees east) with the estimated regression line (solid ) and a broken line drawn at 4.4%, an estimate of the mammalian average. See figure 3.3 for further explanation.



The Impact of Sea Barriers on Bats in Southern Wallacea

79

Allozyme variation in M. minimus in the Philippine archipelago was reported by Heaney et al. (2005), and this provides some interesting similarities and differences. They reported rather low levels of interpopulation differentiation, probably similar to our observations if we exclude Nusa Penida, Bali, and Sumba, and they concluded this was consistent with high colonizing ability. One is tempted to conclude, therefore, where we observe strong genetic differentiation, across Selat Lombok, Selat Sumba, and the Sawu Sea, that these straits mark ecological factors inhibiting gene flow and stimulating local adaptation. Heterozygosity in this species is generally low by mammalian standards, and there is a statistically significant decline from east to west (fig. 3.9B, table 3.4). Suyanto (1994) found heterozygosity, on average, was higher in Australia and New Guinea (5.4% and 6.2%, respectively) than the populations sampled here, and Heaney et al. (2005) reported 4.6% in the Philippines. While these regional values suggest the Banda Arc islands may maintain lower effective population sizes, in the islands reported here heterozygosity is not associated with island area (table 3.4). Eonycteris spelaea The cave fruit bat, Eonycteris spelaea, is widespread in mainland Southeast Asia and Wallacea, with Timor being the southeast limit of its distribution. It roosts in large colonies and travels long distances to feed on fruit and nectar. The F statistics for this species are small, but three are statistically greater than zero (table 3.3). FRT is the largest statistic at 0.06, indicating a modest level of population structure associated with Pleistocene islands. There is no genetic differentiation across Wallace’s line but moderate differentiation across Muller’s line, with the islands to the west of this line clustered together (fig. 3.10A). There is also quite strong differentiation across Selat Alor. The two Outer Banda Arc islands sampled, Timor and Sumba, while quite different from each other, are similar to Inner Banda Arc islands, Timor to Alor and Sumba to the western groups. mtDNA RFLP diversity in E. spelaea does not show concordance with allozyme patterns (Hisheh et al. 1998). There is quite strong structure associated with Selat Ombai, which is less evident in the allozyme markers. Of the Inner Banda Arc islands, Flores shows the most differentiated mtDNA, which also is not evident in allozymes and makes little biogeographic sense. Allozyme heterozygosity in this species is high by mammalian standards and shows no evidence of a longitudinal trend (fig. 3.10B) or an association with island area (table 3.4). Dobsonia peronii Dobsonia peronii, the western naked-backed fruit bat, is endemic to southern Wallacea, occurring between Bali and Babar, east of Timor. It roosts almost exclusively in caves. All F statistics were nonsignificant (table 3.3), and

A

B

Figure 3.10.  Eonycteris spelaea. A, Position of islands on the first two axes from ordination of the arc genetic distance matrix. B, Plot of mean island heterozygosity on longitude (degrees east) with the estimated regression line (solid ) and a broken line drawn at 4.4%, an estimate of the mammalian average. See figure 3.3 for further explanation.

A

B

Figure 3.11.  Dobsonia peronii. A, Position of islands on the first two axes from ordination of the arc genetic distance matrix. B, Plot of mean island heterozygosity on longitude (degrees east) with the estimated regression line (solid) and a broken line drawn at 4.4%, an estimate of the mammalian average. See figure 3.3 for further explanation.

A

B

Figure 3.12.  Rousettus amplexicaudatus. A, Position of islands on the first two axes from ordination of the arc genetic distance matrix. B, Plot of mean island heterozygosity on longitude (degrees east) with the estimated regression line (solid) and a broken line drawn at 4.4%, an estimate of the mammalian average. See figure 3.3 for further explanation.



The Impact of Sea Barriers on Bats in Southern Wallacea

83

genetic distances between island populations of this species are small, with all specimens lying within a small range of less than 0.1 units (fig. 3.11A). Two of the Outer Banda Arc islands, Timor and Sumba, are at the margins of all three axes, but the other Outer Banda Arc islands, Roti, Savu, and Semau, are not differentiated from those on the Inner Banda Arc. Alor and Pantar lie at one end of the first dimension. The differentiation of Timor, but not Roti or Semau, makes little biogeographic sense given their close geographic proximity and the lack of the latter pair’s genetic separation from Savu and Inner Banda Arc islands. In this species, only 6 of 36 loci showed variation, and heterozygosity was very low at less than 2% in all islands. There was no association between heterozygosity and longitude (fig. 3.11B), but this is the only species where heterozygosity was associated with island area (table 3.4), although the regression coefficient only just reached statistical significance ( p = 0.038). Rousettus amplexicaudatus Geoffroy’s rousette fruit bat, Rousettus amplexicaudatus, is widespread in the Malay Peninsula and Wallacea, where it is essentially an obligate cave bat. F statistics indicate little differentiation (table 3.3), but an initial ordination indicated that two islands, Rinca and Adonara, were quite separate from the rest. Both of these islands were represented by only one sampled individual, and for clarity in the plot they were eliminated prior to the ordination presented here (fig. 3.12A). The estimates, to two decimal places, and significance of the F statistics, were the same whether or not these two islands were included. As expected from these F statistics, the ordination plot reveals little in the way of population structure, although the Outer Banda Arc islands are located in the same region of the plot and in the same region as Alor and Pantar. The second axis separates these islands from those on the Inner Banda Arc west of Selat Alor, and although the separation is modest indeed, it implies Selat Alor may be associated with a restriction in gene flow. Heterozygosity is high in this species and is not associated with longitude (fig. 3.12B) or island area (table 3.4). These observations of high heterozygosity and low genetic differentiation at all population levels are similar to the observations of Heaney et al. (2005) in Philippine populations.

Discussion Population Structure The F statistics reveal clear patterns in population structure across the species, with differentiation largely focused at the interisland level. There is little evidence of inbreeding within localities (i.e., inbreeding in the classical sense), with none of the FID values being statistically significantly greater than zero

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L. H. Schmitt, S. Hisheh, A. Suyanto, Maharadatunkamsi et al.

(table 3.3). FID for Dobsonia peronii is high at 0.25, but in this species there is very limited genetic variation, with only 6 of 36 loci showing polymorphism. The rather low values of FDS across the ten species indicate that there is, generally, considerable gene flow between localities within islands. Nonetheless, there is some evidence of modest structuring within island populations of Myotis muricola, Cynopterus nusatenggara, Eonycteris spelaea, and Rousettus amplexicaudatus. These species have FDS values that are significantly greater than zero at the 5% level, but all four of the estimates are rather small at 0.05 or less. Three of the four significant values are in fruit bats, perhaps indicating that intraisland gene flow may be a little more restricted in this group. While fruit bats are often fast fliers and may travel large distances to feed, they often congregate in large centralized roosts, which may facilitate the exchange of information on locations of seasonal food supplies: an adaptation for foraging success (Marshall 1983). This requirement may constrain their capacity to disperse and may lead to greater roosting fidelity than the microchiropteran species. The fruit bat E. spelaea demonstrated evidence of roost fidelity within Lombok Island with some mtDNA lineages confined to specific cave roosts (Hisheh et al. 1998). The fourth species with a significant FDS value is the microchiropteran M. muricola. This species roosts in small groups (up to eight individuals) in rolled leaves of banana plants, behavior that may promote local differentiation (Hisheh et al. 1998). On the other hand, many values of FSR and FRT are large and statistically significant, revealing extensive population structure associated with island geography. Seven species have large and significant values of FRT, indicating that the straits that persisted throughout the Pleistocene are the ones most strongly associated with this structure. With the exception of Rhinolophus affinis, these seven FRT values are all much larger than the corresponding FSR values. Why do species that are seemingly able to move readily within islands show restricted movement across the straits? Most, if not all, are physically capable of crossing between islands. Indeed, they must have made several sea crossings, initially to colonize the islands and subsequent ones to maintain genetic integrity between the island populations. One factor contributing to restricted movement may be natural selection for behaviors to avoid extensive water gaps. Undertaking flights across the sea may carry considerable risks for some species, especially those that are weak fliers, susceptible to predation as they cross alien habitat with limited refuge, or require patchy habitats. The effect of this selection could be behavior to avoid making sea crossings across substantial gaps, with its consequent effects on population structure. This form of natural selection has been proposed to explain why the Australian bush rat, Rattus fuscipes, seems reluctant to cross between two islands that are occasionally joined at spring low tides by an isthmus only a few meters wide (Schmitt 1975).



The Impact of Sea Barriers on Bats in Southern Wallacea

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How have the more persistent straits imposed a greater effect on population structure than those that disappeared during the Pleistocene glaciations? One explanation is that the straits act directly by imposing restrictions on the movement of some species of bats, resulting in population structure. This structure intensifies over time, and the straits that exist the longest, for example those persisting throughout the Pleistocene, develop the strongest interisland differences. However, the Pleistocene-persistent straits are also the largest ones, and this association between strait width and longevity confounds our explanation. The association is obvious in the distances between adjacent islands of the Outer Banda Arc, but it is also the case on the Inner Banda Arc. Selat Lombok, Selat Sape, and Selat Alor are today 21, 18, and 11 km wide, respectively. All other contemporary straits between adjacent islands on the Inner Banda Arc are less than these, with the exception of those separating Lombok and Sumbawa (13 km), and Bali and Nusa Penida (11 km). It is possible that the primary determinant of population structure is the width of the sea crossing between islands rather than its longevity. One observation mitigating against width per se as an explanation is Selat Ombai, which is 30 km wide but, as discussed later, is not as strongly associated with population structure as some of the narrower Pleistocene straits. Irrespective of whether it is the dimensions or longevity of straits that impose on population structure, the sea appears to act as a substantial barrier to movement in seven of the ten bat species we have examined here. Consequently, large or persistent straits have stimulated evolutionary divergence and have played a substantial causative role in the development of the high level of chiropteran diversity in the region. Are sea barriers a primary determinant of the high rates of endemicity in the region? It is expected that endemic species are more likely than widespread species to demonstrate marked geographic structuring due to their in situ evolution and the length of time they have inhabited a region (e.g., Heaney et al. 2005; Roberts 2006). Those species adapted to primary rain forest, as are many Indonesian chiropterans, are susceptible to habitat fragmentation that can give rise to population differentiation. The most significant FRT values ( p < 0.001) were observed in two of the three endemics we examined, Rhinolophus simplex and Cynopterus nusatenggara. Results indicate that the extent of Pleistocene sea crossing was the most important regulator of gene flow in these species. Both species tend to forage locally and are adapted to foraging in cluttered air spaces rather than open spaces (McKenzie et al. 1995) and may therefore be reluctant to cross significant sea barriers. The third endemic examined, Dobsonia peronii, did not show a significant FRT value, but this species possesses traits that would override the influence of geography. D. peronii is a large megabat, weighing over 200 g and with a forearm length of about 120 mm (Kitchener et al. 1990; Kitchener et al. 1997), that is capable of very fast flight and forages in unobstructed air spaces over large areas. An

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L. H. Schmitt, S. Hisheh, A. Suyanto, Maharadatunkamsi et al.

illustration of this vagility is the very low recapture rate of D. peronii compared to a suite of chiropteran species examined by McKenzie et al. (1995) on Lombok Island. The microchiropteran Scotophilus kuhlii demonstrates a similar population structure. Despite being insectivorous, like D. peronii and Rousettus amplexicaudatus, it forages in unobstructed air spaces in large clearings and at canopy height and is capable of fast, prolonged flight (McKenzie et al. 1995). As such it has a very different foraging strategy than many other vespertilionids (McKenzie et al. 1995), and it is not surprising that it differs markedly in population structure from the other microbats investigated and has more in common with some of the megabats. The patterns of population structure may reflect ecological factors; indeed Heaney et al. (2005) eloquently point out that both geography and ecology will be important factors. Unfortunately, our understanding of the underlying ecology of bat species in the Banda Arc is poor, making it difficult to develop coherent arguments. Increasing trends in aridity from west to east (Oldeman et al. 1980) influence vegetation structure and floristics and availability of fruit. This trend is reflected in the absence in eastern Indonesia of many Oriental fruit-eating species such as tupai, squirrels, and monkeys. From the ecological viewpoint, the straits are not so much barriers to bat flight but, instead, may mark changes in the availability of suitable habitat, which becomes more restricted to the east, and this lack of habitat may greatly reduce the survival of colonizers on new islands. The majority of the bats we have described here are at or near the extreme margin of their distribution, implying they are close to the limits of suitable habitat, which is likely to become scarcer and patchier to the east. New migrants are likely to find it difficult to locate suitable niches. For most species, islands to the east are drier and have fewer ecological niches than those to the west, making the former more difficult to inhabit and get a “footing.” Some evidence for this may be found in the observation that, apart from Dobsonia peronii, no species showed an association between heterozygosity and island area, possibly because species utilize only small parts of an island’s resources, namely areas of suitable habitat. If it were possible to associate heterozygosity with the extent of their preferred habitat, then perhaps we would detect a significant association. Despite the high levels of FRT observed within several species, each of the ten species we examined supports enough gene flow between islands to maintain their integrity as single species. If we assume between-island allopatry is integral to the generation of endemics, then there must have been periods when movement across some of these straits was so limited that speciation was able to occur. There are two endemic Cynopterus species in this region, C. terminus on Timor and C. nusatenggara. The latter species not only has limited gene flow between Pleistocene islands, but genetic data indicate reduced gene flow between contemporary islands and even between localities within islands. Such restrictions in movement are conducive to speciation events. We speculate



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that speciation in this region may be initiated by isolation on geographically marginal islands, especially those that can maintain a viable isolated population over an extended period. Timor and Sumba would be likely candidates, but others could also be effective in this respect. After sufficient differentiation has accumulated in isolation, dispersal to adjacent islands would eventually lead to a more widespread endemic species. Although a widespread species, Myotis muricola at the eastern limit of its distribution shows a similar pattern in F statistics to the endemic Cynopterus nusatenggara. Findings such as a significant west-to-east decline in withinisland variability and differentiation of the eastern populations, coupled with evidence of a population bottleneck, suggest the possibility of incipient speciation in M. muricola. The populations of this species on Bali and Borneo are genetically differentiated from those on the islands to the east (Hisheh et al. 2004), and the latter group of islands may well be on the way to forming a Banda Arc endemic with Wallace’s line as a demarcation. We also sought to determine the relative effects of the five straits and the Sawu Sea on population structure in the region. We did this by making a subjective assessment of the genetic differentiation between Pleistocene islands adjacent to each strait as seen in the principal coordinates analyses plots. A summary of this assessment is presented in table 3.5. Although necessarily impressionistic, this summary suggests that all of these persistent straits have had profound isolating effects, although Selat Ombai apparently less so than the others. In at least one respect, this is somewhat surprising as the minimum distance across Selat Ombai is 30 km at present, greater than all the Inner Banda Arc straits, and it was little reduced during Pleistocene glacial maxima when it was about 28 km wide. However, this table may underestimate the importance of Selat Ombai as a barrier to gene flow because this strait separates two endemic Cynopterus species, C. nusatenggara and C. terminus. These two species are genetically very similar and probably diverged in situ. Wallace’s line (Selat Lombok) is not associated with population subdivision any more often than the other persistent straits, having a marked impact in only three species, a weak impact on one, and no impact on four. We have allozyme data for several other vertebrate species in the region, although for most of these the geographic distribution is more limited. These data include three species of bats that cross Wallace’s line, Aethalops alecto, Cynopterus horsfieldii, and C. titthaecheilus, none of which show differentiation across Selat Lombok (Kitchener et al. 1993a; Schmitt et al. 1995). Unpublished allozyme data for a fourth bat species, Hipposideros larvatus, indicates quite marked differentiation across Selat Sumba (between Sumbawa and Sumba), across the Sawu Sea (between Sumba and Savu, and between Savu and RotiSemau), but not between Roti and Semau, providing another example of preferential differentiation of Pleistocene islands. The house shrew Suncus murinus does not support differentiation at the level of Pleistocene islands, with Flores

+++ +++a + ++ − +++ − ++ − −

+++

+++ − − −

+++ + −

Selat Sape

Selat Lombok

− + +++ +++ − +++ −

+++ − +++ − +/−

+++

Selat Sumba

− +++a +++ +++

Selat Alor

− −

− +/− ++/− −

−

++ +++/−

− +++ −

Selat Ombai

+++/− +++

Sawu Sea

a

Alor and Lombok-Sumbawa-Moyo are separated by both Selat Sape and Selat Alor.

Note. +, ++ and +++ indicate weak, moderate, and strong differentiation across a barrier; − indicates no differentiation; +/− indicates variable or uncertain differentiation. Unmarked positions indicate no assessment was possible.

Myotis muricola Taphozous melanopogon Rhinolophus simplex Rhinolophus affinis Scotophilus kuhlii Cynopterus nusatenggara Macroglossus minimus Eonycteris spelaea Dobsonia peronii Rousettus amplexicaudatus

Table 3.5.  Summary of the effects of Pleistocene sea barriers on the population structure of 10 bat species



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as different from Adonara and Lembata as it is from Bali (Kitchener et al. 1994b), whereas Crocidura maxi shows differentiation across Selat Lombok and Selat Sape but not across Selat Alor (Kitchener et al. 1994a). Allozyme variation in the skink Lamprolepis smaragdina suggests differentiation across Selat Ombai but not across Selat Alor, Selat Sumba, or the Sawu Sea between Savu and Timor (Schmitt et al. 2000). There is no genetic differentiation in another skink, Mabuya multifasciata, across Selat Sape, Selat Alor, Selat Ombai, or the Sawu Sea, but weak separation was apparent across Selat Lombok (Schmitt et al. 2000). Taken together, these data show that the straits that have persisted through the Pleistocene are often, but not invariably, associated with population structure in vertebrates other than the ten bat species that are the focus of this study.

Genetic Variability within Islands At equilibrium, heterozygosity is expected to be a function of effective population size. We used island area as a proxy for population size, but with the exception of Dobsonia peronii, no species showed an association between heterozygosity and island area, although it is worth noting that the regression coefficient for Rousettus amplexicaudatus approached statistical significance ( p = 0.07). Philippine populations of R. amplexicaudatus also show a positive association between heterozygosity and island area (Heaney et al. 2005). These two species show the least population structure of the megachiropterans, and with this knowledge we would have predicted that they would be the least likely to show an area effect as a marker of genetic drift, based on the assumption that high rates of gene flow would increase effective population size. Four of the ten species show a significant decline in heterozygosity from west to east. These four species are also among those showing the strongest population structuring at the level of Pleistocene islands. For three of these species, Myotis muricola, Taphozous melanopogon, and Macroglossus minimus, these observations are consistent with recurrent gene flow into the western end of the Banda Arc from high-heterozygosity populations on the Greater Sunda island of Java, which is near large source populations on the Asian mainland. In combination with an isolation by distance model of population structure in the Banda Arcs, this could maintain high heterozygosity in the west with a gradual decline to the east. The strong structure exhibited by these three species is therefore consistent with this hypothesis, which requires restrictions in gene flow through the island chain. Such restrictions will also enhance population structuring. As discussed in the case study, this explanation is more problematical for endemic species such as Cynopterus nusatenggara because an immediate, contemporary Southeast Asian source does not exist. One could resort to either a historical phenomenon that preceded speciation or a more recent population expansion from the west. We have observed a similar longitudinal trend in one other vertebrate, the skink Mabuya multifasciata (Schmitt

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et al. 2000). This species is essentially an Asian species whose distribution extends east to Yamdena and New Guinea. As previously mentioned it does not show substantial population structure associated with Pleistocene water gaps. Apart from gene flow from a large source population, there are two other explanations for longitudinal clines in heterozygosity that have some circumstantial support. First, if effective population sizes decline from west to east, genetic drift can create a cline without resort to recurrent gene flow from a large source population. Island size does not decline from west to east, but the increasing aridity from west to east may lead to a decline in the extent of suitable habitat for some species. This, in concert with greater seasonal uncertainties toward the east, may result in diminishing population sizes in that direction. With limited gene flow between islands in the Banda Arc, heterozygosity would be expected to decline toward the east. Second, natural selection could also be acting to give a similar pattern, through various ecologically based hypotheses such as niche width and marginal-central (e.g., Hedrick et al 1976). An extensive survey by Nevo et al. (1984) revealed heterozygosity is lower in species occupying arid environments, and this is consistent with the known climatic changes in the Banda Arc and the west to east trends in heterozygosity. Of course, these three hypotheses, gene flow from a source population, differential genetic drift, and differential natural selection, are not mutually exclusive. While the allozyme data for Eonycteris spelaea gives no indication of an association between heterozygosity and longitude, mtDNA haplotype diversity shows a tendency to decline from west to east (Hisheh et al. 1998). Compared to allozymes, mtDNA will be particularly sensitive to recent historical demographic processes, and ongoing analyses of DNA variation in the other species will probably reveal disparities between the two types of genetic markers and will certainly give additional insights into evolutionary and demographic processes. (For further discussion of this topic, see Heaney and Roberts, chapter 2, this volume.) For example, the pattern of mtDNA nucleotide diversity in Cynopterus nusatenggara is virtually the opposite to what we have described for allozymes, being lower in the islands west of Selat Sape than those to the east and high in Sumba (Newbound et al. 2008a). This incongruence between the data sets may reflect sex differences in dispersal or effective population sizes. For species showing a decline in genetic diversity within populations from west to east, the eastern islands, because of lower genetic diversity, may be more prone to extinction than western ones. This phenomenon has implications for conservation strategies in the region, and may have assisted the formation of endemics. For example, isolation of the ancestral population of Cynopterus terminus on Timor for sufficient time for speciation to occur may have been assisted by the temporary extinction of the conspecific populations in the eastern Inner Banda Arc around Selat Alor.



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Also relevant to regional conservation are the general levels of heterozygosity. Island populations tend to have lower heterozygosity than those inhabiting mainland (e.g., Nevo et al. 1984), and on this basis we expected to observe less heterozygosity in the species we studied than in mammals generally. However, heterozygosity is known to be associated with various other ecological factors. For example, species inhabiting the tropics tend to have higher heterozygosity than those in temperate zones (e.g., Nevo et al. 1984), which in this region would act to counterbalance an island effect. In only two of the ten species, the megachiropterans Eonycteris spelaea and Rousettus amplexicaudatus, is island heterozygosity consistently equal to or greater than the mammalian average. The other eight species have at least some islands with genetic variation lower than the mammalian average, often markedly so, and therefore potentially at some risk of extinction. In four of these eight species, almost all islands examined have below-average heterozygosity: Taphozous melanopogon, Scotophilus kuhlii, Macroglossus minimus, and Dobsonia peronii. The four other species, Myotis muricola, Rhinolophus simplex, R. affinis, and Cynopterus nusatenggara, each have several populations below average. Although the effect is less marked in C. nusatenggara, the three islands with lower heterozygosity in this species lie at the periphery of the species’ distribution and are separated from other island populations by persistent straits. It would appear then that the island distribution of these species has been a factor in reducing genetic variation within bat populations in this region, especially in the islands to the east, with consequent impacts on vulnerability to extinction.

Conclusions Volcanic activity and Pleistocene sea-level fluctuations have created a dynamic island geography in southern Wallacea for the past few million years, leading to a series of population colonizations and fragmentations. Together with its location at the junction of the Asian and Australian realms, and considerable environmental diversity and gradients, southern Wallacea is a valuable setting in which to study recent evolutionary events. The region is well known for its biogeographic lines, but in the spirit of G. G. Simpson, we examined genetic diversity within ten bat species that are widespread in the region to assess island affinities and the extent of intraisland diversity. We found that the sea is a potent barrier to gene flow for most species, with genetic differentiation focused at the between-island level and little variation between localities within islands. The majority of species show marked interisland genetic structures concordant with sea barriers that existed throughout the Pleistocene glacial maxima, although Wallace’s line is not any more prominently associated with differentiation than other persistent barriers in the region. The high level of interisland genetic differentiation suggests sea straits, directly or indirectly, have stimulated high levels of chiropteran evolution in the region. Three of

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the ten species are endemics, and two of these have the greatest levels of interisland diversity. We speculate that speciation may be initiated by isolation on marginal islands. As a whole, heterozygosity within islands tends to be below the mammalian average, some markedly so, and four species show a trend for heterozygosity to decline from west to east, indicating the eastern populations are particularly vulnerable to extinction. This synthesis of chiropteran genetic diversity provides further evidence that the geography of southern Wallacea has been conducive to rapid evolution in recent times, leaving high levels of endemism as a legacy.

Acknowledgments The former directors of the Puslitbang Biologi, Bogor, Dr. Kardasan and Dr. Soetikno, and of the Western Australian Museum, John Bannister, provided continuous support and encouragement of the survey of the vertebrate fauna of Bali, Nusa Tenggara, and the Maluka Islands. The collecting would not have been possible without the field assistance of many colleagues, including Ken Aplin, Boeadi, Norah Cooper, John Dell, Ron Johnstone, Dennis King, Ibnu Maryanto, Najamuddin, Laurie Smith, Kirstin Tullis, and Chris Watts. We thank Debra Judge for discussions. Aspects of this work received financial support from the Australian Research Council, the National Geographic Society (USA), and the Australian Nature Conservation Agency.

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Chapter 4

Earth History and the Evolution of Caribbean Bats Liliana M. Dávalos

Introduction Bats are the most species–rich and abundant of Caribbean mammals, the sur­ vivors of a fauna that once included native sloths, monkeys, rodents, and in­ sectivorans, all now extinct or nearly so (Morgan and Woods 1986). There are 64 Recent and late Quaternary species in 32 genera of 6 families (Dávalos 2005, 2006; Koopman 1989; Morgan 2001; Tejedor et al. 2004; Tejedor et al. 2005). The bat fauna of the Antilles is unique: about 50% of the species are endemic to the region, and the proportion of endemics rises when only considering the Greater Antilles (Baker and Genoways 1978; Koopman 1989). How can we explain the diversity and distribution of this fauna? Two main biogeographic hypotheses have been proposed: a temporary land bridge connecting the Greater Antillean Ridge and northwestern South America through the Aves Ridge (Iturralde–Vinent and MacPhee 1999), and dispersal over ocean barriers sometimes mediated by prevailing ocean currents (Hedges 1996). The land–bridge—or Gaarlandia—hypothesis draws on strati­ graphic sections and submarine samples that indicate that land exposure in the Caribbean was at a maximum during the Eocene/Oligocene transition (Haq et al. 1993; Iturralde–Vinent and MacPhee 1999). The dispersal hypothesis, in contrast, is based on the finding that estimates of divergence between Carib­ bean and continental amphibians and reptiles were scattered throughout the Cenozoic for 75 of 77 lineages studied (Hedges 1996). A third alternative, the in­ terconnection of North America and South America through the proto–Antilles in the Cretaceous, has recently been revived by Mesozoic–age divergence esti­ mates for the insectivoran mammal Solenodon, the frog genus Eleutherodactylus, and the xantusiid lizard Cricosaura (Roca et al. 2004). This alternative probably does not apply to bats, in light of the dust clouds, tsunamis, and earthquakes that followed the asteroid impact at nearby Chicxulub (Yucatán) 65 million years ago (Ma) (Alvarez et al. 1980; Grajales et al. 2000), and the subsidence of the West Indies in the Eocene (Iturralde–Vinent and MacPhee 1999). The fossil record and phylogenies of a few Caribbean land mammals (e.g., mega­ lonychid sloths, caviomorph rodents, primates, and one bat lineage) are com­ 96



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patible with the Gaarlandia hypothesis (Horovitz and MacPhee 1999; Wetterer et al. 2000; White and MacPhee 2001), but divergence estimates are available only for nonflying lineages, and their reliability is at best questionable (Dávalos 2004). To date, no analysis has combined the necessary taxonomic and molecu­ lar sampling to examine the land–bridge model, in part because most nonfly­ ing Caribbean mammals are extinct (Morgan and Woods 1986). As the most abundant and diverse of extant West Indian mammals (Griffiths and Klingener 1988), bats are ideally suited for such a study. If the Gaarlandia land bridge enabled bats to reach the islands from the continent, the descendents of colonizing populations would share one common ancestor with mainland relatives as ancient as the Eocene/Oligocene bound­ ary. Conversely, multiple divergences between continental and island species within each lineage, scattered across many different dates, would be consistent with the dispersal scenario. Here I conduct phylogenetic analyses of seven groups of Caribbean bats in the families Natalidae, Mormoopidae, and Phyllo­ stomidae, representing about 40% of all bat species found in the West Indies, to test the Gaarlandia hypothesis. These taxa comprise all West Indian endemic bat genera and subgenera and represent >80% of extant endemic species. To test the monophyly of each lineage and estimate the timing of divergence be­ tween insular and continental species, continental taxa closely related to each Caribbean group were also included.

A Phylogenetic Approach to Caribbean Bat Biogeography Geographic and Taxonomic Scope In this chapter “West Indies,” “Antilles,” and “Caribbean” refer to the islands of the Caribbean Sea that have an insular biota (Morgan 2001; Morgan and Woods 1986). Special attention is devoted to the Greater Antilles: Cuba, Jamaica, His­ paniola, and Puerto Rico. The bat fauna of Grenada and the Grenadines, Trini­ dad, Tobago, Margarita, Aruba, Bonaire, and Curaçao is not discussed here because these islands are characterized by a South American biota. A total of 64 extant and sub–Recent bats have been recorded in the West Indies, in about 30 separate groups. This study examines seven groups in de­ tail: mormoopids (with four West Indian representatives), two phyllostomid groups, and natalids.

Phylogenetic Analyses of Caribbean Bat Lineages DNA was extracted from frozen tissues of relevant taxa using the Qiagen DNeasy kit. DNA was amplified and sequenced to generate a data set of one nuclear gene fragment (Rag2) and one complete mitochondrial gene (cyto­ chrome b). Amplification and sequencing used previously described protocols and primers (Dávalos 2005, 2007; Dávalos and Jansa 2004). ABI 3700 automated

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sequencers (ABI) with Big Dye terminator chemistry (ABI) were used to collect sequences. Mitochondrial cytochrome b and Rag2 sequences not generated as part of this study were obtained from Baker et al. 2000; Hoofer et al. 2003; Lewis–Oritt et al. 2001; and Ruedi and Mayer 2001. The species names and GenBank accession numbers of sequences collected for this study are presented in table 4.1. A data set obtained from GenBank including partial sequences of mitochon­ drial ribosomal subunits 12S and 16S, and the complete sequence of the tRNAval intervening gene, was included in analyses (Baker et al. 2003; Van Den Bussche and Hoofer 2001; Van Den Bussche et al. 2002). These sequences were aligned using CLUSTAL W 1.83 (Thompson et al. 1994) with a gap opening penalty of 10 and a gap extension penalty of 5, transitions weighed 0.5 with respect to transversions. Alignments were examined and corrected manually to en­ sure the reliability of positional homology assessments. Concatenated data–set length was 5,175 bp for natalids and outgroups, and 5,219 bp for mormoopids, phyllostomids, and outgroup. Maximum likelihood (ML) analyses were per­ formed with PAUP* 4.0b10 (Swofford 2002), using heuristic searches with a neighbor joining (NJ) starting tree and subtree pruning–regrafting (SPR) branch swapping. Nonparametric ML bootstrap analyses were performed using 100 heuristic replicates with SPR branch swapping. Settings for the GTR+G+I model of DNA sequence evolution were estimated directly using PAUP* (Swofford 2002) and remained fixed in bootstrap analyses. Parameter settings for each of the two data sets are shown in table 4.2. Bayesian phylogenetic analyses were conducted using the program MRBAYES 3.0b4 (Huelsenbeck and Ronquist 2001) with a GTR+G+I model of DNA sequence evolution for each partition (mitochondrial ribosomal DNA [mtrDNA], mitochondrial cytochrome b, and nuclear Rag2), as described pre­ viously (Dávalos 2005). Model parameters were unconstrained and unlinked between partitions. Two independent runs of 1 million generations using four Markov chains were conducted for each data set. Trees were sampled every 100 generations, and the first 10,000 generations were discarded as burn–in. Bayesian posterior probabilities (BPP) for branches and parameter estimates were concordant in separate runs, with one exception (see below). Table 4.2 summarizes the parameters obtained through Bayesian analyses for each of the two data sets. The majority–rule consensus trees obtained through Bayesian analyses were congruent with the ML trees, with the exception of the position of Pteronotus psilotis (sister to the P. parnellii lineage with 0.54 BPP; or sister to a clade formed by P. quadridens–macleayii and P. davyi with 0.53 BPP in a separate run). Fig­ ure 4.1 shows the phylogenetic relationships of (A) Natalidae and outgroups and (B) Mormoopidae, Phyllostomidae, and outgroup obtained through ML analysis of concatenated sequences using PAUP* (Swofford 2002). The ML trees are congruent with those obtained through Bayesian analysis using MRBAYES,

Table 4.1.  Species, molecular sequences, and geographic distribution Taxon Molossus molossus Myotis velifer Myotis riparius Nyctiellus lepidus Chilonatalus tumidifrons Chilonatalus micropus Natalus mexicanus Natalus jamaicensis Natalus major Natalus tumidirostris Natalus stramineus Noctilio leporinus Pygoderma bilabiatum Ametrida centurio Sphaeronycteris toxophyllum Centurio senex Ardops nichollsi Ariteus flavescens Stenoderma rufum Phyllops falcatus Dermanura cinerea Erophylla sezekornib Erophylla bombifronsb Phyllonycteris aphylla Brachyphylla cavernarum Glossophaga soricina Monophyllus redmani Anoura caudiferb Anoura geoffroyib Pteronotus portoricensis Pteronotus pusillus Pteronotus rubiginosus Pteronotus ribiginosus Pteronotus parnellii Pteronotus davyi Pteronotus fulvus Pteronotus gymnonotus Pteronotus quadridens Pteronotus macleayii Pteronotus psilotis Mormoops megalophylla Mormoops blainvillei

12S tRNAval 16S

cyt b

Rag2

AF263215 AF263237 AF263236

L19724 AF376870 AF376866 AY621006a AY621027a AF345925 AY621013a AY621022a AY621020a AY621008a AF345924 AF330796 AY604437a AY604446a AY604451a AY604442a AY572336a AY604436a AY604431a AY604448a ACU66511

AY141017 AY141033 AY141032 AY604463a AY604464a AY141023 AY604467a AY604466a AY604465a AY604468a AY141024 AF316477 AF316483 AF316430 AF316486 AF316438 AF316434 AF316435 AF316487 AY604453a AF316443 AF316450

AF345925

AF345924 AF263224 AY395826 AY395802 AY395828 AF263227 AY395803 AY395804 AY395829 AY395810 AY395839

AY395806 AY395840 AY395824 AY395835

AY620439a AF187033 AY572365 AF423081

AF316478 AF316436 AF316452 AF316473

L19506 AF316431

AF407180 AF407181 AF407176 AF407177 AF407179 AF407178 AF407182 AF407174 AF407172

AF338665 AY604454a AF330807 AF338667 AY604456a AF338671 AF338672 AF338674 AF338683 AF338700 AY604457 AF330808 AF338685

AF330817

AF338692 AF338693 AF338694 AF338695 AF338700 AY245416 AF330818 AY028169

Geographic distribution CA, SA, GA, LA NA, CA CA, SA GA GA GA NA, CA GA GA SA LA CA, SA, GA, LA SA SA SA CA, SA LA GA GA GA CA, SA GA GA GA GA, LA CA, SA GA SA CA, SA GA GA SAc, EG NA, CA, SAc GA NA, CA LA NA, CA, SA GA GA NA, CA, SAc NA, CA, SA GA

Note: Geographic distribution obtained from Koopman 1994. GenBank accession numbers are given below the gene names. NA = North America; CA = Central America; EG = East Guianas (Surinam and French Guiana); SA = South America; GA = Greater Antilles (includes the Bahamas); LA = Lesser Antilles. a

Generated as part of this study.

b

Concatenated “hybrid” sequences.

c

Distribution of the lineage represented by this population, following Dávalos 2006.

10.065, 16.519, 13.068, 0.175, 71.157, 1.000 2.297, 9.016, 2.398, 0.111, 39.327, 1.000 4.242, 12.183, 2.265, 2.111, 15.136, 1.000

8.268, 15.766, 6.217, 0.140, 73.090, 1.000 0.686, 21.762, 1.780, 1.614, 31.353, 1.000 1.147, 5.172, 0.407, 1.330, 8.173, 1.000

Bayesian

Bayesian

Bayesian

ML

Bayesian

Bayesian

Bayesian

mtrDNA

cyt b

Rag2

Mormoopidae, Phyllostomidae, and outgroup

mtrDNA

cyt b

Rag2

Note: I = proportion of invariant sites; α = shape parameter of the Γ distribution.

4.017, 10.650, 3.531, 0.784, 40.551, 1.000

7.212, 12.307, 7.368, 0.735, 64.041, 1.000

ML

Natalidae and outgroups

R–matrix

Method

Data set

0.298, 0.226, 0.220, 0.256

0.363, 0.378, 0.067, 0.191

0.384, 0.228, 0.164, 0.224

0.352, 0.261, 0.165, 0.221

0.309, 0.214, 0.216, 0.261

0.316, 0.293, 0.118, 0.273

0.382, 0.192, 0.165, 0.258

0.349, 0.216, 0.172, 0.264

Base frequencies

Table 4.2.  Maximum likelihood and Bayesian parameters using the GTR+Γ+I model of nucleotide evolution

0.531

0.497

0.449

0.456

0.484

0.552

0.200

0.179

I

3.24

0.735

0.577

0.469

21.089

1.868

0.453

0.244

α



Earth History and the Evolution of Caribbean Bats

101

with the exception of the position of Pteronotus psilotis, as explained above. Maximum parsimony analyses using PAUP* (Swofford 2002) were conducted as described previously (Dávalos 2005), and the results were consistent with the trees obtained through ML and Bayesian analyses. Because of conflict sur­ rounding the position of P. psilotis, and the resolution among P. davyi, P. gymnonotus, and P. fulvus, the branches resolving these relationships were collapsed for subsequent analyses of geographic distribution and divergence time.

Optimization of Geographic Distribution Geographic distributions for each lineage were coded as a five–state character as shown in table 4.1. Taxa distributed across more than one region were coded as polymorphic for this character. Geographic distributions were mapped onto the ML phylogenies using MacClade 4.0 (Maddison and Maddison 2003). The phylogeny of mormoopids was modified to reflect the uncertain relationships of Pteronotus psilotis and P. davyi, and close relatives, as discussed above. Both accelerated transformation (acctran) and delayed transformation (deltran) were implemented; if results conflicted, the branch was coded as equivocal.

Estimation of Divergence Times The Thorne and Kishino method (Kishino et al. 2001; Thorne et al. 1998) was applied to estimate divergence times. This method accounts for constraints based on unconnected data sources such as the fossil record, while allowing for independent rates of molecular evolution along tree branches. The ML tree topology for each data set (modified slightly for mormoopids) was used to estimate parameters of sequence evolution using PAML 3.14 (Yang 1997). The model of sequence evolution used was F84 (Felsenstein 1984), which al­ lows for a transition/transversion parameter with a gamma rate distribution in four discrete categories. Branch lengths were estimated with the estbranches program of Thorne et al. (1998) for each of the two data sets. Divergence times were estimated using the program multidivtime (Kishino et al. 2001; Thorne et al. 1998). Markov chain Monte Carlo analyses ran for 1 million genera­ tions with a 100,000–generation burn–in, and chains were sampled every 100 generations. The mean of the prior distribution of the root of the ingroup tree of natalids and their sister group (Vespertilionoidea) was set at 50 Ma, accounting for middle Eocene molossid and vespertilionid fossils (McKenna and Bell 1997), with a standard deviation of half the mean. The mean of the prior distribution of the root of the ingroup tree of Mormoopidae and Phyllostomidae was set at 36 Ma, in accordance with the recent discovery of Oligocene mormoopid remains in Florida (Czaplewski and Morgan 2003), with a standard deviation of half the mean. Each of these mean priors matches the node age estimated from 17 nuclear gene sequences, and calibrated with other fossil constraints, for the tree of all bat families (Teeling et al. 2005). The rate of molecular evolution

A

92

0.05 substitutions/site

B

95 99

89 72

0.05 substitutions/site

Palynophil

Phyllodia

island Chilonycteris Mormoops

Legend Genus abbreviation Nat.- Natalus Chi.- Chilonatalus Nyc.- Nyctiellus Pte.- Pteronotus Mor.- Mormoops

Distribution — Greater Antilles — continent § Lesser Antilles --- equivocal

Figure 4.1. Phylogenies and optimization of geographic distribution for endemic Caribbean bats. Nodes are labeled with Bayesian posterior probability expressed as a percentage, when different from 1.00. Relationships depicted were also consistent with maximum parsimony and maximum likelihood analyses. The descendents of the most recent common ancestor of Erophylla and Monophyllus are herein named Palynophil (Chiroptera: Phyllostomidae), in reference to their love of pollen. A, Phylogeny of Natalidae and close relatives (superfamily Vespertilionoidea). B, Phylogeny of Mormoopidae and relevant Phyllostomidae.

Mormoopidae

98

Pte. portoricensis Pte. pusillus Pte. rubiginosus East Guianas Pte. parnellii Pte. rubiginosus Pte. davyi § Pte. fulvus Pte. gymnonotus Pte. quadridens Pte. macleayii Pte. psilotis Mor. megalophylla Mor. blainvillei

Stenodermatina

Phyllostomidae

Pygoderma Ametrida Sphaeronycteris 98 Centurio Ardops § Ariteus Stenoderma Phyllops Dermanura Erophylla Phyllonycteris Brachyphylla Glossophaga Monophyllus Anoura

Natalidae

Vespertilionoidea

92

Nat. stramineus Nat. tumidirostris § Nat. major Nat. jamaicensis Nat. mexicanus Chi. micropus Chi. tumidifrons Nyc. lepidus Myotis Molossus



Earth History and the Evolution of Caribbean Bats

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Table 4.3.  Ninety-five percent confidence intervals around time estimates for selected nodes in figure 4.2. Node a b c d e f a b c d e f g h i j k l m n o p

Divergence time estimate (Ma) if sdrate = meanrate Natalidae and outgroups (A) 50.9 (31.1–89.0) 15.7 (7.4–32.5) 6.3 (2.5–14.6) 5.3 (2.1–12.4) 3.6 (1.3–8.6) 0.7 (0.1–2.1) Mormoopidae and Phyllostomidae (B) 19.9 (14.6–30.6) 17.0 (12.3–26.2) 14.5 (10.2–22.9) 10.6 (7.2–16.7) 4.9 (3.2–7.8) 15.3 (10.7–24.0) 13.6 (9.5–21.4) 4.7 (3.0–7.7) 2.7 (1.5–4.7) 14.9 (10.5–23.1) 7.8 (4.7–12.8) 1.5 (0.8–2.6) 2.0 (1.2–3.3) 1.5 (0.8–2.7) 2.8 (1.8–4.7) 8.9 (5.9–14.4)

Divergence time estimate (Ma) if sdrate = meanrate/2 54.9 (33.2–88.6) 17.0 (7.6–33.3) 7.0 (2.6–15.7) 5.9 (2.2–13.2) 3.9 (1.4–9.0) 0.8 (0.1–2.3) 18.9 (14.4–26.9) 16.2 (12.1–23.3) 13.8 (10.1–20.1) 10.0 (7.1–14.9) 4.7 (3.2–7.0) 14.7 (10.6–21.5) 13.1 (9.5–19.2) 4.5 (3.0–7.0) 2.6 (1.4–4.3) 14.2 (10.4–20.7) 7.4 (4.6–11.6) 1.4 (0.8–2.4) 1.9 (1.2–3.0) 1.5 (0.8–2.5) 2.7 (1.8–4.3) 8.6 (5.9–12.8)

was estimated as the median of tip–to–root branch lengths over the mean of the prior distribution of the root. The median of the three partitions corresponded to the rate of evolution of mitochondrial ribosomal DNA (12S, tRNAval, and 16S). The standard deviation of the rate of molecular evolution was set to half the rate itself. To compare the effects of prior selection, parallel analyses using a standard deviation equal to the molecular evolution rate were conducted, assuming minimal prior knowledge. The differences between estimates of the mean divergence time were generally on the order of 50,000–500,000 years for the mormoopid and phyllostomid data set, and (exceptionally) up to 5 million years for the oldest divergence in the vespertilionoid data set (table 4.3). The following fossil constraints applied to the data set of natalids and outgroups: (1) minimum 37 Ma for Molossidae to Vespertilionidae, assum­ ing an end of the middle Eocene date for molossid and vespertilionid fossils (McKenna and Bell 1997); (2) minimum 30 Ma for Natalidae to Molossidae/ Vespertilionidae (Morgan and Czaplewski 2003); and (3) minimum of 0.01 Ma for Chilonatalus micropus to Chilonatalus tumidifrons (Morgan 1993). The following fossil constraints applied to the data set of Mormoopidae and Phyllostomidae:

Nat. stramineus § f Nat. tumidirostris d Nat. major e c Nat. jamaicensis Nat. mexicanus Chi. micropus Chi. tumidifrons Nyc. lepidus

A

b A

Myotis Molossus +100 0 Sea level (m) -100 Myr ago

40

Eocene

30

20

10

Plio Pleistocene

Miocene

Oligocene

Pygoderma Ametrida Sphaeronycteris Centurio e m Ardops § Ariteus D l Stenoderma Phyllops Dermanura Erophylla k Phyllonycteris j Brachyphylla B Glossophaga c A Monophyllus Anoura n Pte. pusillus Pte. portoricensis i Pte. rubiginosus East Guianas Pte. parnellii H Pte. rubiginosus Pte. davyi § o Pte. gymnonotus Pte. fulvus G Pte. quadridens p Pte. macleayii Pte. psilotis Mor. megalophylla F Mor. blainvillei

B

+100 0 Sea level (m) Myr ago

40

Eocene

30

Oligocene

20

10

Miocene

Legend Genus abbreviation Nat.- Natalus Chi.- Chilonatalus Nyc.- Nyctiellus Pte.- Pteronotus Mor.- Mormoops

Distribution — Greater Antilles — continent § Lesser Antilles --- equivocal

-100 Plio Pleistocene



Earth History and the Evolution of Caribbean Bats

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(1) minimum of 36 Ma for Mormoopidae to Phyllostomidae (Czaplewski and Morgan 2003); (2) minimum of 12 Ma for Anoura to Dermanura (Czaplewski et al. 2003); and (3) minimum of 0.01 Ma for Phyllops to Stenoderma (Morgan 2001). To compare the effects of phylogenetic uncertainty surrounding the nectar–feeding fossil Palynephyllum antimaster (Czaplewski and Morgan 2003), parallel analyses without constraint number 2 were conducted. Differences between estimates of the mean divergence time were on the order of 10,000– 100,000 years. Figure 4.2 shows the timing of divergences in (A) Natalidae and outgroups and (B) Mormoopidae, Phyllostomidae, and outgroup.

The History of Caribbean Endemic Bats How Did Bats Reach the Antilles? To facilitate discussion, the descendents of the most recent common ancestor of Erophylla and Monophyllus are hereafter called Palynophil after the Greek palyn, “pollen,” and phil, “love.” The monophyly of each of the groups ana­ lyzed here—Mormoops, the subgenus Phyllodia (Pteronotus parnellii sensu lato), the insular species of the subgenus Chilonycteris (Pteronotus macleayii and P. quadridens), Palynophil, Stenodermatina, and Natalidae—was supported with Bayesian posterior probability (BPP) of 1.00 and maximum likelihood bootstrap (MLB) of 100% (except Palynophil, MLB = 73%). These phylogenies fit the branching pattern expected if a single ancestor had used a land bridge to reach the islands. The divergence dates corresponding to primary dispersal from the continent to the West Indies, however, reject the Oligocene land–bridge hypothe­ sis (nodes in uppercase in fig. 4.2). Five out of six divergences—all but the Natalidae—have 95% confidence intervals (CI) that exclude the period when the land bridge would have existed (table 4.3). The divergence time between natalids and relatives is compatible with the land bridge, but Eocene–age fossils of the two closest extant relatives of natalids (Molossidae and Vespertilionidae) in Europe and North America, and one Oligocene natalid fossil from Florida, imply a northern origin for this West Indian lineage (McKenna and Bell 1997; Morgan and Czaplewski 2003). The South America–West Indies land bridge could not have played a role in the dispersal of natalids to the islands. Fossil evidence, though fragmentary, is also consistent with a post–Oligocene origin

Figure 4.2.  Phylogeny and molecular timescale, with eustatic sea–level curve of Haq et al. 1993. Branch lengths are calibrated to match divergence times estimated using the Thorne and Kishino method, and each calibrated with three fossil constraints (McKenna and Bell 1997). Geological events indicated by shading include the period when Gaarlandia was exposed around the Eocene/ Oligocene transition (Iturralde–Vinent and MacPhee 1999), and transitions that were marked by relatively low sea levels from the early to middle Miocene (~16 Ma), middle to late Miocene (~11 Ma), and Miocene to Pliocene (~5 Ma). A, Phylogeny of Natalidae and close relatives (superfamily Vespertilionoidea). B, Phylogeny of Mormoopidae and relevant Phyllostomidae.

106

L. M. Dávalos

for the remaining five bat groups. The oldest West Indian bat fossils in all lineages are from the Pleistocene and Holocene epoch (50 species (Simmons and Voss 1998), and Pygoderma is known from the Atlantic forest and Cerrado of Paraguay and Brazil, again in sympatry with >50 species (Marinho–Filho 1996a, 1996b; Willig et al. 2000). Only two vertebrate groups—bats and anoles—have phylogenies that strongly support West Indian origin for extant continental species. Phyloge­ netic analyses have revealed that dispersal from the Caribbean likely gave rise to an evolutionary radiation of anoles in Central America and South America (Nicholson et al. 2005), and at least one instance of dispersal out of Cuba co­ incides with the Miocene/Pliocene transition (Glor et al. 2005). Until now no single overarching hypothesis has been advanced to explain how these Carib­ bean endemics reached the continent, or how their ancestors reached the West Indies in the first place. The results presented here show that sea–level changes in the Miocene constitute a viable mechanism for facilitating dispersal between landmasses in the Caribbean.

The Deep Roots of Caribbean Bat History The Caribbean bat community has been structured, at least in part, by geologi­ cal changes that allowed short bursts of biotic exchange with other islands and with the mainland. During the early Miocene, Cuba, Hispaniola, and Puerto Rico were emergent, and western Cuba was separated by the Havana–Matanzas channel from the block formed by eastern Cuba, northern Hispaniola, and Puerto Rico (Graham 2003; Iturralde–Vinent and MacPhee 1999). The rise in sea level following the early/middle Miocene transition (Haq et al. 1993; Miller et al. 1996), probably in combination with the definitive separation of Cuba from northern Hispaniola and Puerto Rico, isolated populations of Chilonatalus, and Brachyphylla from the ancestor of Erophylla–Phyllonycteris (fig. 4.2). Abrupt changes in the benthic fauna signal uplift along the Isthmus of Panama, and perhaps a temporary closure of the isthmus, during the middle/late Miocene transition (Duque–Caro 1990; Roth et al. 2000). This might explain how the South American ancestors of the Stenodermatina reached Central America, and through it, the Greater Antilles (fig. 4.2). At the closing of the Miocene, Jamaica had reemerged, the Havana–Matanzas channel had disappeared, and northern and southern Hispaniola were united, matching the modern Greater Antillean contours (Iturralde–Vinent and MacPhee 1999). By the early Pliocene

110

L. M. Dávalos

the Stenodermatina reached Jamaica (Ariteus), the Lesser Antilles (Ardops), and the Neotropical mainland, mirroring the expansion of natalids to Jamaica (Natalus jamaicensis), the Lesser Antilles (N. stramineus), and Central America (N. mexicanus) and in synchrony with another eustatic decline. As the Miocene ended, Phyllodia was the last of the mormoopids to colonize the Greater Antil­ les (fig. 4.2). By the Pliocene frugivores (Stenodermatina), pollen/nectar feeders (Paly­ nophil), and three lineages of mormoopid insectivores were already part of the Caribbean bat community. Griffiths and Klingener (1988) suggested that eustatic minima caused by glacial cycles in the Pleistocene could help explain West Indian bat biogeography. Only one of the island–to–continent disper­ sal nodes (i in fig. 4.2B) might be compatible with this mechanism, and even the most recent primary dispersal node (H in fig. 4.2B) is too old to fit the Pleistocene hypothesis (table 4.3). Several island–island diversification events, however, are potentially compatible with a Pleistocene isolation model, sug­ gesting a more localized role for this mechanism than previously believed (i in fig. 4.2A; and m, l, i, and n in fig. 4.2B). Because this study has narrowly fo­ cused on endemic genera and subgenera, the role of Plio–Pleistocene sea–level changes in the dispersal and diversification of nonendemic groups remains to be evaluated.

Conclusions Dispersal events in West Indian vertebrates were constrained to narrow win­ dows of time, even among flying organisms that presumably need no raft to breach ocean barriers. In fact, the flying abilities of bats do not mean they can disperse across oceanic barriers easily: most West Indian bats hardly tolerate hunger, and are highly susceptible to desiccation (Silva Taboada 1979). Periods of exceptionally low sea level have facilitated dispersal by decreasing the sepa­ ration between landmasses, leading to congruent temporal divergences that should be common to many other organisms. This mechanism is an alterna­ tive hypothesis to land bridges or pure dispersal, and can readily be tested at other locations and for other groups (see, for example, Mercer and Roth 2003). The striking congruence across multiple bat groups found here underscores the influence of geological history in all biogeographic scenarios, including dispersal.

Acknowledgments For specimen loans, collecting permits, field assistance, lab support, research support, and editorial advice, I thank R. J. Baker (Texas Tech University), F. K. Barker, A. S. P. Corthals, J. L. Cracraft, N. Czaplewski, M. Delarosa, R. DeSalle,



Earth History and the Evolution of Caribbean Bats

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A. Donaldson (NEPA, Jamaica), K. Doyle, E. Dumont, R. Eriksson, T. Fleming, N. Gyan (Wildlife Section, Trinidad), R. Harbord (British Museum–Natural History), S. A. Jansa, S. Koenig, S. McLaren (Carnegie Museum), J. Mercedes, J. C. Morales, G. S. Morgan, T. Nicole (Department of Agriculture, Bahamas), H. Ochman, J. L. Patton (Museum of Vertebrate Zoology, University of Califor­ nia, Berkeley), A. L. Porzecanski, P. Racey, C. Raxworthy, A. Rodríguez (In­ ter–American University, Puerto Rico), A. L. Russell, R. O. Sánchez (Dirección General de Vida Silvestre y Biodiversidad, Dominican Republic), P. Schickler, M. Schwartz, N. B. Simmons (American Museum of Natural History), C. Stihler, E. Sutherland, V. Tavares, A. Tejedor, J. Wible (Carnegie Museum), and A. Wright. This publication has been funded in part with federal funds from the National Science Foundation (DEB–0206336), the National Aeronautic and Space Agency (NAG5–8543), and the National Institutes of Health (GM56120). This research has also received financial support from the Ambrose Monell Cryogenic Collection, the Monell Molecular Laboratory, and the Cullman Re­ search Facility in the Department of Ornithology; and the Center for Biodiver­ sity and Conservation at the American Museum of Natural History; the Center for Environmental Research and Conservation and the Department of Ecology, Evolution, and Environmental Biology at Columbia University; the University of Arizona; the Explorers’ Club (New York); and E. Dumont’s NSF grant.

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Chapter 5

Phylogeography and Genetic Structure of Three Evolutionary Lineages of West Indian Phyllostomid Bats Theodore H. Fleming, Kevin L. Murray, and Bryan Carstens

Introduction Like the Philippines and Wallacea, the West Indian archipelago has been a major center of evolution for many groups of vertebrates, including bats. This archipelago has had a complex geological history (reviewed in Buskirk 1985; Dávalos 2004b; Graham 2003; Iturralde-Vinent and MacPhee 1999; and Jones 1994, among others) and consists of two major geological units: (1) the Greater Antilles, whose islands lie on the Caribbean plate and attained their present positions and configurations beginning about 25 Ma, and (2) the Lesser Antilles, which consists of a double arc of volcanic islands along the eastern margin of the Caribbean plate that date from mid-Eocene/Oligocene (40–45 Ma; the northeast outer arc) or the Oligocene to early Miocene (20–25 Ma; the northwest inner arc; Graham 2003). Estimates of the ages of the present-day Greater Antilles, whose bats are the subject of this chapter, are shown in figure 5.1. Those data and the following synopsis are based primarily on Graham (2003). Although Jamaica was first emergent by late to middle Eocene (49–42 Ma), it was submerged until 10 Ma and is the youngest of the major Greater Antillean islands. The ages of other Greater Antillean islands date from 15–25 Ma. Cuba is a geologically complex landform that attained its present configuration by late Miocene (19–12 Ma). Western and northern Hispaniola plus proto–Puerto Rico separated from Cuba in early to mid-Miocene (25–20 Ma); southern Hispaniola joined northern Hispaniola in about mid-Miocene (ca. 15 Ma). Puerto Rico separated from northern Hispaniola in the Oligocene/early Miocene (25–23 Ma). The Bahamas Platform occupies the southeastern margin of the North American plate and has been in place since Jurassic-Cretaceous times. For most of the Cenozoic, the Bahamas were barrier reefs or low islands. Extent of the subaerial portions of this platform has varied widely, especially during Pleistocene sea-level fluctuations. At low sea levels, the Great Bahama Bank was one of the largest islands in the Greater Antilles, although its topo116



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>> 100 Ma

12-19 Ma

13 Ma

10 Ma

15 Ma

22 Ma

Figure 5.1.  Map of the West Indies. Dates (in millions of years ago, Ma) indicate approximate time a particular island or group of islands has been in its present position and configuration based on Jones 1994 and Graham 2003. (Map reprinted with permission from Morgan 2001.)

graphic relief was much less than that of other large Antillean islands. Finally, the Cayman Islands, along with Swan Island, Jamaica, and southern Cuba, were elevated above sea level 10–15 Ma (Jones 1994). In summary, most of the contemporary Greater Antilles have been available for colonization by bats and other organisms for at least 15–20 million years. The extant chiropteran fauna of this archipelago includes 56 species in 7 families, of which 28 species (50%) are endemic to the region (Rodríguez-Durán and Kunz 2001). For comparison, the other group of volant West Indian vertebrates—birds—contains 425 species in 49 families, of which 150 species (35%) are endemic (Hedges 2001). While no chiropteran family is endemic to the West Indies, funnel-eared bats (Natalidae) are thought to have originated there and then colonized the mainland of Central and South America (Dávalos 2005). In birds, two families are endemic to the West Indies—todies (Todidae) with one genus and five species and the monotypic palm chat (Dulidae). Most families of West Indian bats and birds, therefore, did not originate in the Caribbean. This

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is also true of the West Indian flora, which includes no endemic families but over 200 endemic genera (J. Francisco-Ortega, pers. comm.).With 26 species, including 15 endemics (58%), family Phyllostomidae (New World leaf-nosed bats) is the most species-rich and ecologically diverse group of Caribbean bats. Except for a few insect-eaters, this family is represented primarily by nectarand fruit-eating species (Genoways et al. 2005; Rodríguez-Durán and Kunz 2001). A blood-feeding phyllostomid, Desmodus rotundus, is known from fossils on Cuba (Morgan 2001). The evolutionary history of the West Indian bat fauna has been widely discussed by bat biologists (e.g., Baker and Genoways 1978; Dávalos 2004a, 2004b; Genoways et al. 1998; Genoways et al. 2001; Koopman 1989; Morgan 2001). Central issues in this discussion have involved such questions as (1) Where did these bats come from? The obvious choices for bats as well as for Caribbean birds and other organisms have been North America, Mexico and Central America, or South America. (2) How did they get to these islands? The choices here are via vicariance or dispersal (Dávalos 2004b and chapter 4, this volume; Hedges 2001; Iturralde-Vinent and MacPhee 1999). (3) What were the routes of island colonization and did colonization involve a steppingstone-like process? (4) How long have different taxa lived together on these islands? Are contemporary Caribbean bat assemblages relatively young or old (Genoways et al. 2005)? More recent discussion points stem from the use of DNA-based phylogenetic and phylogeographic approaches to address such questions as (5) Are island populations monophyletic or do they contain mixtures of lineages with different colonization histories (Carstens et al. 2004; Emerson 2002; Klein and Brown 1994)? (6) What are the current patterns and rates of migration (and gene flow) among islands and between the mainland and islands? Have most species colonized the islands only once or have they done so multiple times (e.g., Klein and Brown 1994)? Finally, since island bats (and birds) are much more prone to extinction than their mainland relatives, perhaps as a result of reduced genetic variation and inbreeding (Frankham 1997, 1998), (7) how much genetic variation do their populations contain and to what extent is this variation a function of island area (i.e., population size), length of time in the islands, and distance from mainland sources of colonization? Answers to some of these questions are already in hand. Concerning the mode of arrival of bats in the West Indies, for example, the consensus is that dispersal has been the exclusive method (Genoways et al. 2005; Hedges 2001). According to Hedges (2001), at least 18 species of bats dispersed from Mexico/ Central America, at least 14 species dispersed from northern South America, and 2 species came from North America. Based on the apparent ages of different West Indian bat lineages, Griffiths and Klingener (1988) proposed that colonization of the Greater Antilles involved a two-stage process involving two geological events: (1) “old” colonists (i.e., species belonging to endemic



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subfamilies or lacking congeneric mainland relatives) used a Tertiary chain of islands leading from Central America or Mexico to colonize Cuba/Hispaniola before reaching Jamaica and Puerto Rico, and (2) “younger” colonists (i.e., species having conspecific or congeneric mainland relatives) arrived when sea levels were lower in the Pleistocene, with bats from Mexico or Central America colonizing Jamaica before reaching Cuba and Hispaniola. More recently, Dávalos (chapter 4, this volume) used molecular phylogenies and divergence analyses to determine processes involved in faunal buildup of bats in the West Indies. She tested two hypotheses: (1) West Indian bats arrived overland from South America via Gaarlandia at the Eocene/Oligocene transition (IturraldeVinet and MacPhee 1999). (2) They arrived by over-water dispersal from the Neotropical mainland during periods of low sea level. Results allowed her to reject hypothesis 1 and accept hypothesis 2. In this chapter we will use DNA-based techniques to examine the phylogeography, genetic structure, and demographic history of three lineages of phyllostomid bats in the Greater Antilles. Since these lineages differ strongly in their evolutionary ages and length of residency in the West Indies, they should provide us with considerable insight into the patterns and processes of island colonization by phyllostomid bats. Using control-region mitochondrial DNA (specifically, D-loop mtDNA; Avise 2000), we will address the following questions: (1) What is the phylogeographic structure of these taxa? (2) Are island populations monophyletic? (3) How much genetic diversity resides in their populations, and how is this diversity distributed among islands? (4) What are the demographic histories of these lineages? The three phyllostomid lineages we are studying include Macrotus waterhou­ sii, Erophylla sezekorni and E. bombifrons, and Artibeus jamaicensis. Since these lineages differ in their evolutionary histories and general ecology, it is reasonable to expect that their genetic structure and demographic histories in the Greater Antilles are very different. One of their major differences is evolutionary age, as reflected by their positions in the phyllostomid phylogenetic tree. According to the molecular phylogeny of Baker et al. (2003), Macrotus is the basal genus in the family, whose age has been estimated to be 28–34 million years ( Jones et al. 2005; Teeling et al. 2005). Additional genetic data (e.g., chromosome banding patterns; Baker 1979) also support the hypothesis that Macrotus is basal in the family. Two species of Macrotus are currently recognized (Simmons 2005)—M. californicus, which occurs in arid parts of the southwestern United States and the Mexican states of Sonora, Chihuahua, and Tamaulipas, and M. waterhousii, which occurs in tropical dry forest in western Mexico from southern Sonora south to Guatemala and in the Greater Antilles as far north as Abaco in the Bahamas (Koopman 1993). The two currently recognized species of Erophylla (sezekorni and bombifrons) are members of the endemic West Indian subfamily Phyllonycterinae, which also includes Phyllonycteris with two species. E. sezekorni is a western clade

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that occurs in the Bahamas, Cuba, Jamaica, and the Caymans; E. bombifrons is an eastern clade that occurs on Hispaniola and Puerto Rico (Simmons 2005). The Phyllonycterinae and another endemic West Indian subfamily, Brachyphyllinae (containing one genus, Brachyphylla, with two currently recognized species; Simmons 2005), fall midway in the phyllostomid molecular phylogeny of Baker et al. 2003, and both groups are thought to be about 18 million years old (Dávalos, chapter 4, this volume ). According to Dávalos, Erophylla and Phyllonycteris last shared a common ancestor about 8 Ma. Artibeus jamaicensis belongs to the highly derived subfamily Stenodermatinae and is clearly the most recent of these three lineages to have colonized the Caribbean (Genoways et al. 2005; Morgan 2001; Phillips et al. 1989; Phillips et al. 1991). This species is one of the most common phyllostomids throughout the lowland Neotropics from Mexico to northern Argentina and the West Indies. It is absent from the central and northern Bahamas. Ecological differences between these species are summarized in table 5.1. At 55–60 g, adults of A. jamaicensis are substantially larger than those of the other two species, which weigh 15–20 g. Reflecting its basal position in phyllostomid phylogeny, M. waterhousii is an insectivore that feeds on large moths and orthopterans. It has relatively generalized roosting requirements and usually lives in small colonies near the entrances of caves and in abandoned mines and buildings (Genoways et al. 2005). Compared to the other two lineages, it appears to be more extinction-prone and is extinct on 5 of 15 islands (33%), including Puerto Rico, from which its fossils are known (Morgan 2001). Erophylla and A. jamaicensis are both plant-feeding bats and are more common than M. waterhousii on most Antillean islands. Erophylla appears to feed mostly on fruit produced by early successional shrubs and small trees; it also visits flowers for nectar and pollen and eats insects, primarily beetles (Soto-Centeno and Kurta 2006). Except in the northern Bahamas, it roosts exclusively in caves but is not restricted to “hot caves” in the Greater Antilles (see Rodríguez-Durán, chapter 9, this volume; Gannon et al. 2005); it is known to roost in abandoned buildings on Grand Bahama and Abaco (Clark and Lee 1999; THF and KLM, pers. obs.; K. Semon, pers. comm.). Compared with M. waterhousii, Erophylla bats are extinction-resistant and are not known to have become extinct on any Antillean island (Morgan 2001). A. jamaicensis is the most common of the three lineages where it occurs in the Greater Antilles (Gannon et al. 2005; Genoways et al. 2005). It is a frugivore that feeds mostly on fruit produced by canopy trees, especially those in the family Moraceae (figs and their relatives). Its relatively broad roosting habits include caves, hollow trees, and the foliage of canopy trees. Compared with the other two lineages, A. jamaicensis has a poor fossil record in the Antilles, which Morgan (2001) interpreted as indicating that it is a recent colonist in the Caribbean. Finally, although all three lineages probably have polygynous mating systems that could reduce effective population



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Table 5.1.  Summary of the body sizes and ecological characteristics of three phyllostomid bats Characteristic

Macrotus waterhousii (15–20 g)

Erophylla sezekorni/ bombifrons (15–20 g)

Artibeus jamaicensis (55–60 g)

General distribution and abundance in Greater Antilles

Widespread and common throughout, but extinct on Puerto Rico

Widespread and usually common throughout

Widespread, but missing from most of the Bahamas; very common

Roost use

Caves, mines, abandoned buildings

Exclusively caves except in northern Bahamas; not a “hot cave” specialist

Mostly caves but also tree hallows and foliage

Colony sizes

Usually small (≤50) but up to ca. 500

1,000s to 100,000s on Puerto Rico; usually in 100s elsewhere

Usually few 100s in caves; fewer in trees

Diet

Strictly insects, esp. Lepidoptera, Orthoptera, and Odonata

A generalist that eats mostly fruit but also nectar/pollen and insects (esp. beetles); fruit tend to be from early successional shrubs/small trees

Mostly frugivorous but also nectar/ pollen and leaves; fruit tend to be from canopy trees

Reproduction and mating system

Monestrus; polygynous but specific form currently unknown

Monestrus; polygynous, probably promiscuous

Bimodal polyestrous; harem-polygynous

% islands known only as fossil [= known extinctions] (N islands)

33% (15)

0% (12)

0% (11)

% islands with no fossil record [= recent colonist?] (N islands)

0% (15)

16.7% (12)

45% (11)

Sources: Gannon et al. 2005; Genoways et al. 2005; Morgan 2001; Silva Taboada 1979; KLM and THF, unpublished data.

sizes (Ne) and increase rates of inbreeding (Frankham 1998; Storz 1999), they differ in their annual reproductive output. Females of A. jamaicensis are polyestrus and typically have two babies a year whereas females of the other two bats are monestrus and produce only a single baby annually (SilvaTaboada 1979). Based on their evolutionary and ecological differences, we made the following a priori predictions about the phylogeography and genetic structure of these bats: 1.  Assuming that these bats or their ancestors colonized the West Indies from Mexico or Central America, genetic diversity should decrease from west

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to east across the Greater Antilles in all three lineages. It should decrease from south to north in the Bahamas in Erophylla and M. waterhousii. 2.  If genetic diversity decreases with age of island residency (Frankham 1997), then diversity should be lowest in species of Erophylla and highest in A. jamaicensis. Alternatively, because it is the oldest of the three lineages, M. waterhousii might have the lowest genetic diversity. 3.  If genetic diversity is correlated with population size and trophic position, it should be lowest in M. waterhousii (an insectivore) and highest in A. jamaicensis (a frugivore). 4.  If mobility is correlated with trophic position (Fleming 1992; Levey and Stiles 1992), rates of interisland migration (gene flow) should be higher in the two plant-visiting bats than in the insectivore. Owing to its low mobility, island populations of M. waterhousii are more likely to be monophyletic than those of Erophylla and A. jamaicensis.

Methods We tested these predictions using control-region mitochondrial DNA (D-loop mtDNA; Avise 2000). We collected tissue samples from the three species from islands throughout the Greater Antilles except Cuba (appendix 5.1). In addition, we analyzed tissue samples from one Mexican population of A. jamaicensis and M. waterhousii (table 5.2). Bats were captured with extendable hand nets inside of caves or with mist nets set at cave entrances. We recorded age, sex, reproductive status, body mass (g), and forearm length (mm) for all captured individuals. A small piece of tissue (2–20 mg) was clipped from one wing membrane and stored in 95% ethanol until analyzed in the lab. This protocol was approved by the University of Miami IACUC (permit 03–119).

DNA Sequencing and Phylogenetic Analyses Methods that we used to extract and sequence mtDNA are described in appendix 5.2. Number of haplotypes and their frequencies are shown in appendix 5.3. The evolutionary relationships among haplotypes and islands were explored using maximum likelihood (ML) analysis in PAUP 4.0b10 (Swofford 2002). Likelihood parameters from ModelTest were entered into PAUP to approximate the appropriate model of nucleotide evolution (appendix 5.4). We conducted heuristic ML searches with tree bisection and reconnection (TBR) branch swapping and tested the reliability of particular nodes by performing 100 bootstrap replicates. We used parametric bootstrapping to test the null hypothesis that island populations were monophyletic following Carstens et al. (2004). Individuals in intraspecific studies are often too closely related to be amenable to traditional phylogenetic analyses. As an alternative, we constructed a



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Table 5.2.  Summary of genetic diversity data based on 334 bp of control region mtDNA Site

N

Nh

S

Haplotype diversity (h)

Nucleotide diversity (π)

Macrotus waterhousii   Mainland   Hispaniola   Jamaica   Abaco   Exuma   Grd. Cayman

9 12 19 20 22 10

2 2 5 1 2 1

2 1 15 0 7 0

0.50 ± 0.128 0.17 ± 0.134 0.53 ± 0.127 0.00 0.45 ± 0.078 0.00

0.0031 ± 0.0026 0.0005 ± 0.0008 0.0053 ± 0.0036 0.00 0.0096 ± 0.0058 0.00

Erophylla sezekorni/bombifrons   Hispaniola 29   Jamaica 10   Puerto Rico 23   Abaco 16   Grd. Bahama 28   Exuma 23   Grd. Cayman 3   San Salvador 15   Cayman Brac 8

14 7 5 4 6 4 2 2 2

21 13 10 5 7 4 1 1 5

0.91 ± 0.032 0.87 ± 0.107 0.72 ± 0.058 0.66 ± 0.108 0.79 ± 0.036 0.58 ± 0.072 0.67 ± 0.314 0.13 ± 0.112 0.25 ± 0.180

0.0164 ± 0.0091 0.0144 ± 0.0087 0.0123 ± 0.0071 0.0056 ± 0.0038 0.0057 ± 0.0037 0.0035 ± 0.0026 0.0020 ± 0.0025 0.0004 ± 0.0007 0.0038 ± 0.0030

Artibeus jamaicensis   Mainland   Hispaniola   Jamaica   Puerto Rico   Grd. Cayman   Cayman Brac

11 3 3 5 2 3

23 2 2 4 4 5

0.93 ± 0.050 0.22 ± 0.124 0.23 ± 0.130 0.44 ± 0.133 0.11 ± 0.092 0.71 ± 0.127

0.0249 ± 0.0136 0.0007 ± 0.0009 0.0007 ± 0.0010 0.0017 ± 0.0016 0.0013 ± 0.0013 0.0052 ± 0.0039

16 18 17 20 19 7

Note: Sites are listed in order of largest to smallest area within species. Data are means ±1 SE. N = number of samples; Nh = number of haplotypes ; S = number of variable sites.

minimum spanning tree (MST) for the haplotypes using Arlequin 3.01 (Excoffier et al. 2005).

Population Genetic Analyses We used Arlequin 3.01 (Excoffier et al. 2005) to conduct standard population genetic analyses for the three species. To assess genetic diversity, we calculated the number of polymorphic sites (S), haplotype diversity (h), and nucleotide diversity (π). Diversity indices were calculated for the entire population and for each island. To examine the extent of genetic subdivision within the data sets, we computed global ΦST values for each species. In Arlequin, global ΦST values represent the correlation of random haplotypes within a population (island) relative to random haplotypes drawn from the entire data set. We also calculated pairwise ΦST values to estimate average genetic distance among island populations and mainland populations when warranted. Islands are discrete geographic entities often separated by substantial boundaries to dispersal and gene flow. We tested the amount of genetic structure

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imposed by islands using an analysis of molecular variance (AMOVA; Excoffier et al. 1992). In one set of analyses we treated each island as a separate population, but in a separate analysis we partitioned the data further. In A. ja­ maicensis and M. waterhousii, we partitioned the data into a mainland group and a Greater Antillean island group. In Erophylla, data were partitioned into two groups corresponding to the two species, E. bombifrons (Hispaniola and Puerto Rico) and E. sezekorni (Cuba, Jamaica, Cayman Islands, Bahamas). We performed Mantel tests to determine if geographic distances among populations were correlated with genetic distances (Rousset 1997). We used the How Far Is It? Web site (http://www.indo.com/distance/) to determine geographic distances among island sampling localities. All geographic distances were natural-log transformed. Genetic distances were computed in Arlequin as FST values. Finally, we estimated the per-site θ under a coalescent model implemented in Migrate-n (Beerli and Felsenstein 2001) to determine the relative effective population size of these species. Theta (for mtDNA, θ = 2Nefµ where Nef is effective population size and µ is per-site mutation rate) is an important parameter because the rate at which ancestral polymorphisms sort is proportional to θ. Populations with large effective sizes will take, on average, longer to lose ancestral genetic diversity than small populations. From the standpoint of comparative phylogeography, estimates of θ provide a means to compare genetic diversity across organisms.

Demographic Analyses We used three general methods to test our data for signatures of recent demographic expansion. First, we calculated the expansion coefficient (S/d), where S = number of polymorphic sites and d = mean number of pairwise differences among haplotypes (Peck and Congdon 2004). High values of the expansion coefficient are consistent with recent population growth, whereas low values are indicative of stable population size (Russell et al. 2005; Von Haeseler et al. 1996). Values for S and d were calculated in Arlequin. Second, we used various neutrality tests, which in combination can indicate the presence or absence of recent population expansion. We calculated Tajima’s D for each species (Tajima 1989). A significant negative Tajima’s D is consistent with recent population expansion (Aris-Brosou and Excoffier 1996; Peck and Congdon 2004). We also calculated Fu’s FS and Fu and Li’s D* and F*. A combination of a significant FS value and nonsignificant D* and F* values indicates demographic expansion (Fu 1997). Finally, we computed mismatch distributions, plotting the observed frequencies of particular pairwise differences among haplotypes. The expec­ tation of the exponential growth model is a unimodal distribution, whereas a population in mutation-drift equilibrium is expected to have a multimodal mis­ match distribution (Rogers 1995; Rogers and Harpending 1992). We used a ragged­ ness statistic to test goodness of fit of the observed data to a model of exponential population growth. Significance of the raggedness (rg) statistic was tested with



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125

1,000 coalescent simulations (Harpending et al. 1993). Neutrality tests and mismatch distribution analyses were conducted in DnaSP 4.0 (Rozas et al. 2003).

Results For Artibeus jamaicensis we sequenced a total of 97 individuals from six geographic areas (five islands). There were 19 haplotypes (overall h = 0.52). The most common haplotype B1 (67 of 97 individuals) was shared among all five sampled Greater Antillean islands, and three haplotypes (B2, B3, and B5) were shared among at least two islands (fig. 5.2A). There were no shared haplotypes between island and mainland samples. We sequenced 155 individuals of Ero­ phylla sezekorni/bombifrons from nine Greater Antillean islands and found 34 haplotypes (overall h = 0.89). Haplotypes were shared extensively between islands within the E. bombifrons and E. sezekorni, but not between them (fig. 5.2C). We sequenced 92 individuals of Macrotus waterhousii from six geographic areas (five islands) and found 13 haplotypes (overall h = 0.88). In contrast to the other species, there were no shared haplotypes among islands in M. waterhousii (fig. 5.2E).

Phylogenetic and Phylogeographic Analyses Traditional phylogenetic analyses (e.g., maximum likelihood) were hindered by several factors. As with most intraspecific analyses, there were often too few polymorphic sites to provide any resolution among haplotypes. Both A. jamai­ censis and Erophylla phylogenies suffered from this problem. In M. waterhousii, sequences were actually too divergent. Samples from Sonora, Mexico, and Hispaniola presented significant alignment problems due to their dissimilarity to other geographic areas. Most importantly, the absence of Cuba from the data set tempered all of our phylogenetic (and population genetic) interpretations. We will discuss phylogenetic relationships within our taxa using a larger database elsewhere (KLM and THF, unpublished data). ML and MST analyses based on sequence evolution models summarized in appendix 5.4 indicated that phylogeographic structure differs strongly in the three species. In A. jamaicensis, both the ML tree and the MST showed a clear split between mainland and Greater Antillean haplotypes (fig. 5.2A, B). There was strong bootstrap support (99%) for the mainland clade, and the MST showed seven mutational steps among island and mainland haplotypes. Interestingly, in both trees, two mainland haplotypes (A10 and A11) were nested within the Greater Antillean group, a strong indication that recolonization of the mainland by island populations has occurred in this species. In Erophylla, there was good support for the two clades corresponding to specific designations: bombifrons (Puerto Rico and Hispaniola) and sezekorni (Cuba, Jamaica, Caymans, Bahamas; fig. 5.2C, D). However, as seen in the MST, two intermediate haplotypes (B10 and S16) blurred the boundary between the two clades (fig.



Phylogeography and Genetic Structure of West Indian Phyllostomid Bats

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5.2D). Finally, data for M. waterhousii revealed four main groups: group 1 from Sonora, Mexico; group 2 from Grand Cayman, Exuma, and Abaco (and presumably Cuba); group 3 from Jamaica; and group 4 from Hispaniola (fig. 5.2E, F). As mentioned above, groups 1 and 4 were extremely divergent, and there are clear distinctions between all groups (fig. 5.2F). These data strongly support the hypothesis that M. waterhousii is a polytypic taxon in the West Indies. A formal taxonomic analysis of Macrotus is needed to delimit species boundaries. For both A. jamaicensis and E. sezekorni/bombifrons, we rejected the null hypothesis of island monophyly, which indicates either that these bats likely fly across ocean gaps regularly or that ancestral polymorphisms have not yet fully sorted (δTLA. jamaicensis = 28, p < 0.01; δTLE. sezekorni/bombifrons = 28, p < 0.01). Given the long residence time of Erophylla in the Caribbean, the former explanation is more likely than the latter for those species. For M. waterhousii, we were unable to reject the null hypothesis of island monophyly (δTLM. waterhousii = 1, p = 0.43). Because of the absence of shared haplotypes among islands and the high level of divergence revealed in the ML tree and MST (fig. 5.2.E, F), this result was not unexpected. M. waterhousii appears to be a much less vagile bat than the other two species.

Population Genetic Analyses Molecular diversity varied substantially within and between species (table 5.2). The mainland population of A. jamaicensis had the highest haplotype and nucleotide diversity of any population in this study. In contrast, molecular diversity was generally low in island populations of A. jamaicensis and was not correlated with island area (fig. 5.3A), latitude, or longitude (data not shown). In Erophylla, there was a clear trend of high molecular diversity on large islands and low genetic diversity on small islands. The regression equation for nucleotide diversity (fig. 5.3B) is Y = −0.008 + 0.005 log Area (r 2 = 0.83, p A. jamaicensis, a result that likely reflects the length of island residency of these bats rather than their trophic position or current population sizes. Although it is presently one of the most common phyllostomid bats in the Greater Antilles (Gannon et al. 2005; Genoways et al. 2005), A. jamaicensis has apparently not been present in the islands long enough to generate a large Nef and large amounts of neutral variation compared with the two older residents. Overall, our results clearly indicate that the two frugivores are substantially more mobile than the insectivore. A higher extinction rate in M. waterhousii (table 5.1) also supports the hypothesis that this species has had low (absolute) population sizes and very low/no rates of migration between islands. Alternatively, perhaps M. waterhousii has become extinct on some Antillean islands as a result of Pleistocene and/or post-Pleistocene climatic and habitat changes. According to Pregill and Olsen (1981), xeric habitats were more extensive in the West Indies during periods of Pleistocene glacial advance when air temperatures and humidity were lower. Interglacial and post-Pleistocene increases in temperature and humidity favored expansion of more mesic habitats and contraction of xeric habitats and was likely responsible for the extinction of

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a number of xeric-adapted vertebrates in the Greater Antilles. On the Mexican mainland, M. waterhousii currently lives in relatively xeric tropical habitats, and so the loss or reduction of similar habitats in the Greater Antilles probably caused its populations to decrease in size, thereby increasing its likelihood of extinction. If Macrotus bats were affected negatively by expansion of mesic habitats, frugivorous bats such as A. jamaicensis might have benefited from such changes. Phillips et al. (1991) postulated that this species colonized the Greater Antilles in the Pleistocene during a period of mesic habitat expansion. Finally, the molecular genetic data indicate that the demographic histories of the three bat lineages differ significantly. Evidence for population expansion was seen in the two frugivores but not in the insectivore (fig. 5.5). A significant expansion signal was seen in island, but not in mainland, populations of A. jamaicensis. This pattern is what one would expect if Artibeus has recently colonized the Greater Antilles. Timing of the expansion appears to be late Pleistocene (ca. 45,000 BP; table 5.4), although Phillips et al. (1991) suggested that A. jamaicensis has been in the West Indies for about 225,000 years. A significant expansion signal was also found in the western clade of Erophylla but not in the eastern clade. That is, populations on the large stable islands of Hispaniola and Puerto Rico have not expanded recently, unlike those inhabiting the low-lying islands of the western Greater Antilles (e.g., the Caymans and Bahamas), whose areas increased in the late Pleistocene as sea levels fell. Since genetic diversity in Erophylla appears to be strongly correlated with island area (unlike the other two species), we predict that rising sea levels will cause genetic diversity in the western clade to decrease with time as low-lying islands decrease in area. We found no evidence of population expansion in either mainland or island populations of M. waterhousii. This is the pattern we would expect to see in a food-limited, sedentary species with low fecundity and low rates of betweenpopulation and between-island dispersal. We summarize our results with respect to the four genetic predictions in table 5.5.

Comparisons with Other Island Bats How do the phylogeographic and genetic patterns we have documented in three lineages of West Indian phyllostomid bats compare with those found in other island bats? Specifically, how do the predictions we tested with our bats hold up for other West Indian bats and for bats in other archipelagos? Except for A. jamaicensis (Phillips et al. 1991; Pumo et al. 1988; Pumo et al. 1996), genetic data are very limited for other West Indian bats. In A. jamaicensis, Phillips et al. (1991) reported that haplotype diversity was reduced in the Greater Antilles compared to Mexico and that one island haplotype was found in Mexico—results that are concordant with ours. Carstens et al. (2004) studied the phylogeography of A. jamaicensis and two endemic phyllostomids, Ardops nicholsi and Brachyphylla cavernarum, on several islands in the northern Lesser Antilles using cytochrome b sequence data. Haplotype diversity was much higher in



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137

Table 5.5. Comparison of four genetic predictions with results from three island archipelagos Prediction

West Indies (4 species)

Philippines (6 species)

Wallacea (7 species)

1. Genetic diversity (GD) decreases with distance from a mainland source.

Not supported in any species; one species shows a decrease in GD with latitude.

Not tested.

Supported in 4 species; not supported in 3 species.

2. GD decreases with age of island residency (nonendemics > endemics).

Not supported; the endemic species of Erophylla have more GD on islands than the 2 nonendemic species.

Supported; GD > in 3 nonendemic species compared to 3 endemic species.

Supported in one comparison: GD in Cynopterus nusatenggara < that of C. brachyotis.

3. GD positively correlated with island area (population size) and negatively correlated with trophic position (herbivores > insectivores).

Not supported; only Erophylla had a positive correlation with island area; GD correlates better with age of island residency than with trophic position.

Not supported; only 1/6 species had a positive correlation with island area; small islands seem to retain substantial GD.

Not supported.

4. Degree of genetic subdivision inversely correlated with vagility.

Supported; subdivision much greater in the insectivore than in the 3 frugivores.

Supported; 3 “weedy” species showed less subdivision than 2 of the 3 endemic species.

Supported in the comparison between Myotis muricola and Scotophilus kuhlii; mobility of other species not described.

A. jamaicensis than in the two island endemics as predicted above, and island monophyly occurred only in A. nicholsi. Incomplete lineage sorting owing to recent colonization from the Greater Antilles likely accounts for the absence of monophyly in B. cavernarum, whereas interisland migration likely accounts for its absence in A. jamaicensis. Heaney et al. (2005; Heaney and Roberts, chapter 2, this volume) and Roberts (2006a, 2006b) present allozyme and DNA data for six species of Philippine pteropodid bats from seven islands. Three species (Cynopterus brachyotis, Macro­ glossus minimus, and Rousettus amplexicaudatus) are “weedy” (i.e., early successional) species that are widely distributed throughout Southeast Asia, and three species (Haplonycteris fischeri, Ptenochirus jagori, and Ptenochirus minor) are Philippine endemics. All of these species are fruit eaters, but the three endemics are much more restricted to primary forest habitats than the non­ endemics. As summarized in table 5.5, their data support two of the three genetic predictions they could test. Populations of the nonendemic species generally contained more genetic diversity and were less subdivided than those of the endemic species (prediction 2). In contrast, genetic diversity was correlated with island area in only one of five species (R. amplexicaudatus), and it was not

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especially low in any species on small islands (contra prediction 3). Analysis of genetic structure indicated that subdivision was generally low in all species within islands as defined by their Pleistocene boundaries but that only the more mobile, nonendemic species evidenced gene flow between Pleistocene islands (prediction 4). They concluded that two factors, (1) mobility as reflected by habitat breadth and geographic distribution and (2) geological history, particularly Pleistocene sea-level fluctuations, have strongly influenced the genetic structure of these species. Lincoln Schmitt and colleagues (Hisheh et al. 1998; Hisheh et al. 2004; Kitchener et al. 1993; Kitchener et al. 1997; Maharadatunkamsi et al. 2000, 2003; Schmitt et al. 1995; Schmitt et al., chapter 3, this volume) have studied the genetic structure of seven species of bats in three families (Pteropodidae, Rhinolophidae, and Vespertilionidae) in Wallacea. Like the Greater Antilles, the Lesser Sundas form a west-east chain of islands. Reflecting this topology, four of the species evidenced a significant west-east decline in heterozygosity at allozyme loci (prediction 1). No longitudinal trend was seen in two pteropodids (Aethalops alecto, Dobsonia peronii) and one vespertilionid (Scotophilus kuhlii). Regarding levels of genetic diversity (prediction 2), these species generally did not exhibit reduced diversity compared with other mammals, but the endemic Cynopterus nusatenggara had lower diversity than its nonendemic congener, C. brachyotis (but not the nonendemic C. sphinx). In general, levels of genetic diversity were not correlated with island area or trophic position (contra prediction 3); mean heterozygosity was highest in the frugivorous pteropodid A. alecto and lowest in the insectivorous vespertilionid S. kuhlii. Finally, levels of interisland genetic subdivision were relatively high in six species (FST values ranged from 0.17 to 0.40) but were notably low (0.03) in S. kuhlii, the only species that roosts in human structures. Genetic subdivision was correlated with vagility in the two species of vespertilionids (S. kuhlii and Myotis muricola) (prediction 4). Although the nectar-feeding pteropodid Eonycteris spelaea is a wide-ranging forager (e.g., Start and Marshall 1976), it apparently does not migrate regularly between islands and hence displays substantial genetic subdivision (Fst = 0.12) in Wallacea. Data from three other island systems can also be used to test these four predictions. Prediction 1 is supported in two species of pteropodid bats (Ei­ dolon helvum and Rousettus aegyptiacus) on a series of four islands in the Gulf of Guinea, West Africa. In both species, populations living on the two most isolated islands differ genetically and morphologically from the other islands and the mainland (Juste et al. 1996; Juste et al. 2000). Prediction 2 is generally not supported in island bats, which tend to have similar allozyme diversity compared with their mainland relatives and with other mammals (Juste et al. 2000). Like the Philippine endemic pteropodids, however, the Azorean vespertilionid Nyctalus azoreum has lower nucleotide (but not haplotype) diversity than its European congeners (Salguiero et al. 2004). Prediction 3 was not supported by the pteropodid studies in the Gulf of Guinea (Juste et al. 1996;



Phylogeography and Genetic Structure of West Indian Phyllostomid Bats

139

Juste et al. 2000) and in northern Melanesia (Pulvers and Colgan 2007). Finally, prediction 4 was supported in the Gulf of Guinea and Canary Island studies. Extent of genetic subdivision was higher and estimated interisland migration rates were lower in nonmigratory R. aegyptiacus than in migratory E. helvum. Similarly, Plecotus teneriffae, whose European relatives are highly philopatric and sedentary, exhibits greater genetic subdivision than two species of Pipistrel­ lus and Hypsugo savii in the Canary Islands (Pestano et al. 2003a; Pestano et al. 2003b).

Conclusions Reflecting their different ages of residency in the West Indies, the three lineages of phyllostomids that we are studying differ strongly in their phylogeography and genetic structure. The canopy frugivore Artibeus jamaicensis is a vagile species that colonized the northern West Indies in the late Pleistocene and has undergone population expansion since then. Its current molecular diversity, however, is low, and it has not yet attained migration-drift equilibrium in the Greater Antilles. It still likely exchanges individuals with the Mexican mainland. Belying its old endemic status, the frugivore-omnivore Erophylla sezekorni was nearly panmictic in the Greater Antilles until recently (i.e., 1 Ma). Separation into two monophyletic clades is now nearly complete, and its genetic diversity is strongly correlated with island area. Population expansion occurred in the late Pleistocene in the western clade (E. sezekorni) but not in the eastern clade (E. bombifrons). Despite a long residency in the West Indies, its levels of genetic diversity are still high, and genetic subdivision within the two clades is low. In contrast, the insectivore Macrotus waterhousii exhibits substantial genetic subdivision, and its populations contain low levels of genetic diversity. Unlike the other two taxa, populations on different islands are monophyletic, and genetic distances between islands and its mainland relatives are substantial, indicating that, like Erophylla, M. waterhousii has resided in the Greater Antilles for a substantial period of time (i.e., much longer than just the Pleistocene). Genetic isolation and low population sizes, perhaps as a result of habitat contraction, have resulted in elevated extinction risk in M. waterhousii. In summary, vagility and length of residency in the West Indies have had a strong effect on the genetic diversity and structure of these species and lineages. Vagility and length of island residence are also important factors in the genetic structure of other island bats. High vagility significantly reduces extent of subdivision in pteropodid, phyllostomid, and vespertilionid bats on islands, and long island residency tends to reduce genetic diversity within populations. Recent colonization, however, can also have this effect, as exemplified by A. jamaicensis. Contrary to the predictions of Frankham (1997), however, populations of island bats do not generally contain less genetic variation than mainland relatives, even on small islands in some cases (Heaney et al. 2005). Perhaps this reflects the large population sizes of many bats on islands. For example,

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Lloyd (2003) used mtDNA sequence data to estimate that past populations of the endemic bat Mystacina tuberculata on New Zealand were as large as 7.8 million females, although current population sizes are orders of magnitude smaller than this. Likewise, current population sizes of mormoopid and certain phyllostomid bats in the Greater Antilles number in the hundreds of thousands (Gannon et al. 2005). Whatever the cause, island bat populations are not necessarily genetically depauperate. As discussed by Heaney and Roberts (chapter 2, this volume) for bats and more generally by Frankham et al. (2002), this trend has important conservation implications. Low genetic diversity generally puts species at risk of extinction (e.g., M. waterhousii in this study) and reduces a species’ ability to adapt to changing environmental conditions. Many island bats are currently at risk of extinction (Jones et al., chapter 16, this volume), but their major threat is direct human disturbance and not lack of genetic flexibility.

Acknowledgments We thank many people for their help during this study. For hospitality, field assistance, and/or information about bat roosts, we thank F. Molina (Mexico); N. Albury, M. Bethel, N. Bottomley, L. Cheong, C. Kettel, C. McCain, B. Milligan, J. Mylroie, and J. Rolle (Bahamas); S. Koenig and Albert (Jamaica); L. Blumenthal, F. Burton, M. C. and M. S. Fleming, and W. Platt (Caymans); A. RodríguezDurán, C. McCain, and B. Rivera (Puerto Rico); and A. Tejedor, J. Orihuela, and N. Garcia (Dominican Republic). For loan of tissue samples, we thank L. Dávalos, J. Ortega, and A. Tejedor. For lab assistance, we thank R. Lamazares, Y. Escobedo, P. Esquivel, M. Ostentoski, and especially, D. Williams. We thank government officials in the Bahamas, Cayman Islands, Dominican Republic, Jamaica, Mexico, and Puerto Rico for issuing research permits. L. Dávalos and P. Racey provided useful suggestions for improving this chapter. This study was supported by funds from the Department of Biology (M. S. Gaines) and College of Arts and Sciences (J. Wyche, A. Kaifer), University of Miami, the Cayman National Trust, and the U.S. National Science Foundation (DEB-0505866).

27.03900˚N, 109.0170˚W 17.75326˚N, 77.15795˚W 17.96016˚N, 71.18336˚W 19.34530˚N, 81.13302˚W 26.32653˚N, 77.00171˚W 23.57405˚N, 75.90583˚W

Macrotus waterhousii   Aduana Mina   Portland Bay Cave 9   Los Patos Cave   Salinas Cave   Little Harbour Cave 3   Nursery Cave

Sonora, Mexico Jamaica Dominican Rep. Grand Cayman Abaco Exuma

17.87502˚N, 76.48270˚W 17.96016˚N, 71.18336˚W 19.07773˚N, 69.46648˚W 18.41667˚N, 66.71667˚W 18.41433˚N, 66.72920˚W 19.27694˚N, 81.28279˚W 19.73636˚N, 79.73571˚W 26.52582˚N, 78.77835˚W 26.32522˚N, 77.00197˚W 26.14469˚N, 77.18855˚W 23.55582˚N, 75.88206˚W 24.11758˚N, 74.46432˚W

Erophylla sezekorni and E. bombifrons   Ratbat Hole Jamaica   Los Patos Cave Dominican Republic   Cueva de Linea Bahia de Semana, Dominican Rep.   Culebrones Cave Mata de Platano RS, Puerto Rico   Cueva Larvas Puerto Rico   Mist net Grant Cayman   Great Cave Cayman Brac   Bahamas Cement Co. Grand Bahama   Little Harbour Cave 1 Abaco   Long Bay Cave North Abaco   Cabbage Hill Cave Exuma   Lighthouse Cave San Salvador

Coordinates 20.15000˚N, 89.21667˚W 18.35131˚N, 77.64753˚W 18.48158˚N 77.53884˚W 17.96016˚N, 71.18336˚W 19.05833˚N, 69.45359˚W 18.48800˚N, 66.86681˚W 18.41433˚N, 66.72920˚W 19.27694˚N, 81.28279˚W 19.33717˚N, 81.17647˚W 19.75383˚N, 79.74130˚W

Location

Yucatán, Mexico Windsor RS, Jamaica Jamaica Domincan Rep. Cano Hondo NP, Dominican Rep. Puerto Rico Puerto Rico Grant Cayman Grand Cayman Cayman Brac

Artibeus jamaicensis   Murciélago Cave   Windsor Cave   Dead Goat Cave   Los Patos Cave   Mist net   Cueva Amador   Cueva Larvas   Mist net   Old Man Bay Cave   Pete’s Cave

Capture site

Table A5.1.  Sampling localities

9 19 12 10 20 22

3 8 28 7 9 23 15

10 10 19 20

16 8 9 10 8 11 9 9 10 7

N

THF, F. Molina THF, KLM, L. Dávalos KLM, A. Tejedor THF, KLM THF, KLM THF, KLM

THF, KLM, L. Dávalos KLM, A. Tejedor KLM, A. Tejedor C. McCain, A. Rodríguez-Durán THF, A. Rodríguez-Durán THF, KLM THF, KLM THF, KLM THF, KLM THF, KLM THF, KLM THF

THF, KLM THF, KLM

J. Ortega THF, KLM THF, KLM KLM, A. Tejedor KLM, A. Tejedor THF, A. Rodríguez-Durán THF, A. Rodríguez-Durán

Collected by

A p p e n di x 5 . 1

A p p e n di x 5 . 2 .

mtDNA Sequencing and Analyses

Genomic DNA was extracted from 5-mg pieces of tissue using a standard ethanol precipitation procedure or DNeasy DNA isolation kits (Qiagen) and stored in 50 µ1 of Tris-HCl, pH 8.5. We amplified fragments of approximately 350 bp of D-loop mtDNA using polymerase chain reaction (PCR). Because the traditional primers used to amplify bat control-region fragments (P and F; Wilkinson and Chapman 1991) were not reliable for our species, we used primer F1:5′-CCCCACCCT-CAACACCCAAA-3′, redesigned from the Artibeus jamaicencis mitochondrial genome (Pumo et al. 1988) coupled with the traditional primer F:5′-GTTGCTGGTTTCACGGA-GGTAG-3′. Total PCR volume was 10 µ1, with 1.0 µ1 Promega 10× buffer (1.5 mM MgCl2 added), 1 unit Taq DNA polymerase (Promega), 0.1 mM dNTPs, and 14 pmol of each primer. PCR conditions were initial denaturation at 94°C for 2 min, followed by 30 cycles of 94°C for 10 s, 55°C for 10 s, and 72°C for 20 s, with a final elongation step at 72°C for 5 min. Before cycle sequencing, DNA fragments were incubated with ExoSAP-IT (USB) to dephosphorylate double-stranded DNA and degrade excess primer. Fragments were sequenced with Big Dye Terminator Cycle Sequencing Kit, version 1.1 (Applied Biosystems). Reaction volumes of 10 µ1 contained 2.5 µ1 of Big Dye reaction mix, 10–50 ng of template DNA, and 3.2 pmol of forward or reverse primer. The sequencing reaction involved an initial denaturation of 92°C for 1 min, followed by 25 cycles of 92°C for 10 s, 50°C for 5 s, and 60°C for 4 min. Products were run through sephadex columns (Princeton Solutions) to remove unincorporated nucleotides. Samples were then dried for 30 min with a vacuum centrifuge and resuspended in 15 µ1 of Hi-Di Formamide (Applied Biosystems) for sequencing. All samples were sequenced in both directions using an ABI 310 automated sequencer. For each species, raw sequence data was edited in Sequencher 4.5 (Gene Codes). We used consensus sequences to determine unique haplotypes, which were then aligned in Clustal X (Thompson et al. 1994). Indels were treated as a fifth character in all analyses. ModelTest 3.7 (Posada and Crandall 1998) was used to determine the appropriate model of nucleotide evolution (appendix 5.4). We used the Akaike information criterion (AIC) test statistic in ModelTest to evaluate goodness of fit of the nucleotide evolution model to our data. The AIC has been shown to outperform the hierarchical likelihood ratio test statistic (Posada and Buckley 2004). 142

A p p e n di x 5 . 3

Table A5.3.  Summary of haplotypes (mtDNA control region) for three lineages of West Indian phyllostomid bats Haplotype name

Haplotype frequencya

Areas of occurrenceb

Artibeus jamaicensis, 97 samples: Yuc (16), Jam (17), His (18), PR (20), GCy (19), CyB (7) A1 4 (0.041) Yuc (4) A2 1 (0.010) Yuc (1) A3 1 (0.010) Yuc (1) A4 1 (0.010) Yuc (1) A5 1 (0.010) Yuc (1) A6 1 (0.010) Yuc (1) A7 1 (0.010) Yuc (1) A8 1 (0.010) Yuc (1) A9 1 (0.010) Yuc (1) A10 3 (0.031) Yuc (3) A11 1 (0.010) Yuc (1) B1 67 (0.691) Jam, His, PR, GCy, CyB B2 3 (0.031) Jam, PR B3 3 (0.031) Jam, His, PR B4 3 (0.031) CyB B5 2 (0.021) GCy, CyB B6 1 (0.010) PR B7 1 (0.010) DR B8 1 (0.010) PR Erophylla sezekorni and E. bombifrons, 155 samples: Jam (10), His (29), PR (23), GCy (3), CyB (8) GBa (28), Aba (16) S1 39 (0.252) GCy (2), GBa (8), Aba (2), Exu (13), SS (14) S2 25 (0.161) GBa (8), Aba (9), Exu (8) S3 10 (0.065) GBa (7), Aba (3) S4 8 (0.052) GCy (1), CyB (7) S5 5 (0.032) GBa (3), Aba (2) S6 5 (0.032) Jam (4), CyB (1) S7 1 (0.006) SS (1) S8 1 (0.006) Exu (1) S9 1 (0.006) Exu (1) S10 1 (0.006) GBa (1) S11 1 (0.006) GBa (1) S12 1 (0.006) Jam (1) S13 1 (0.006) Jam (1) S14 1 (0.006) Jam (1) S15 1 (0.006) Jam (1) S16 1 (0.006) Jam (1) S17 1 (0.006) Jam (1) B1 11 (0.071) His (1), PR (11) B2 7 (0.045) His (1), PR (6) B3 6 (0.039) His (6) B4 6 (0.039) His (6) B5 5 (0.032) PR (5) B6 4 (0.026) His (4) B7 2 (0.013) His (2) (continued on next page)

T. H. Fleming, K. L. Murray, and B. Carstens

144 Table A5.3.  (continued) Haplotype name

Haplotype frequencya

B8 B9 B10 B11 B12 B13 B14 B15 B16 B17

2 (0.013) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006) 1 (0.006)

Areas of occurrenceb His (2) His (1) His (1) His (1) His (1) His (1) His (1) His (1) PR (1) PR (1)

Macrotus waterhousii, 92 samples: Son (9), Jam (19), His (12), GCy (10), Aba (20), Exu (22) S1 6 (0.065) Son (6) S2 3 (0.033) Son (3) E1 15 (0.163) Exu (15) E2 7 (0.076) Exu (7) A1 20 (0.217) Aba (20) C1 10 (0.109) GCy (10) J1 13 (0.141) Jam (13) J2 3 (0.033) Jam (3) J3 1 (0.011) Jam (1) J4 1 (0.011) Jam (1) J5 1 (0.011) Jam (1) H1 11 (0.120) His (11) H2 1 (0.011) His (1) Note: Aba = Abaco; CyB = Cayman Brac; DR = Dominican Republic; Exu = Exuma; GBa= Grand Bahama; GCy = Grand Cayman; His = Hispaniola; Jam = Jamaica; PR = Puerto Rico; Son = Sonora, Mexico; SS = San Salvador; Yuc = Yucatán, Mexico. a

Numbers in parentheses are proportions.

b

Numbers in parentheses indicate number of individuals per geographic area with that haplotype.

A p p e n di x 5 . 4

Table A5.4.  ModelTest summary Artibeus jamaicensis

Erophylla sezekorni/bombifrons

Macrotus waterhousii

Substitution model Total bps Number of indels Mean indel length

HKY + I 335 1 1

K81uf + I 334 2 1

TrN + Γ 340 10 2.1

Base frequencies   A   C   G   T % invariable sites (I) Γ shape parameter (α)

0.3452 0.1793 0.1174 0.3582 0.8502 0

0.3351 0.1698 0.1405 0.3546 0.8370 0

0.3839 0.2002 0.1038 0.3121 0 0.2262

145

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Part 2

Ecology of Island Bats

Chapter 6

Physiological Adaptation of Bats and Birds to Island Life Brian K. McNab

Introduction Recorded familiarity with the distinctive biota endemic to oceanic islands has a long history, starting at least with the early naval expeditions and commercial trade of European expansionist empires, followed by an extensive period of collecting by field naturalists like Alfred Russel Wallace, Joseph Hooker, and Ernst Mayr, and by the analyses of Philip Darlington, Robert MacArthur, and E. O. Wilson. Recent work by Jared Diamond, Peter and Rosemary Grant, R. N. Holdaway, Helen James, Bradley Livezey, M. V. Lomolino, Ernst Mayr, Storrs Olson, David Steadman, and T. H. Worthy, among others, examined the ecological, morphological, and paleontological characteristics of island avifaunas. In spite of the breadth and intensity of this interest, other possible approaches to island biology remained unexplored. For example, nothing was known until recently of whether, or the extent to which, the physiology of island endemics might differ from that of the endemics’ continental relatives. The absence of such information reflects the paucity of biologists that combine field and laboratory work and the absence of a rationale suggesting that an island existence in and of itself should be expected to have an impact on the physiology of endemics. Several hints that the functional biology of island endemics might differ from that of their continental relatives, in retrospect, included the widely known observations that island endemics were often larger or smaller than their continental relatives, birds on isolated islands were often approachable, birds repeatedly evolved a flightless condition on oceanic islands, and large reptiles were an important component of island faunas. However, these observations were usually placed in the context of reduced species diversity, the absence of mammalian predation, and the loss of dispersibility (Whittaker 1998). Before 1990 few measurements on the energetics of island endemics were available. Among the first, two Hawaiian honeycreepers belonging to the genus 153

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Loxops (= Hemignathus) were shown to have low basal rates, which were associated with social position and food abundance (MacMillen 1974, 1981), not with an island existence. Weathers and van Riper (1982) and Weathers et al. (1983) found that, of two other honeycreepers, one (Loxioides baileui) had a high basal rate and the other (Telespiza catans) had a low basal rate that was ascribed to life in an arid environment. The Cuban rodent Capromys pilorides was shown to have a very low basal rate for its mass, which was referred to semiarboreal habits and a folivorous diet (McNab 1978, 1986), again without a reference to its island endemism. Only later (Arends and McNab 2001) was the point made that Capro­ mys and two other island capromyids, the Bahaman Geocapromys ingrahami and Jamaican G. brownii, have low basal rates possibly in association with an island existence. A distinctive pattern in the energetics of vertebrates endemic to small oceanic islands has been recently emerging (Köhler and Moyà-Solà 2004; McNab 1994a, 1994b, 2001, 2002): many have lower levels of energy expenditure than their large-island and continental relatives. This reduction is accomplished in a variety of ways, including a reduction in (1) mass, (2) activity level, and (3) standard energetics, as well as by (4) a propensity of some birds to evolve a flightless condition. Further evidence of the importance of low levels of energy expenditure in island endemics is the widespread occurrence on tropical islands of large reptiles, including the carnivorous varanid lizards on Komodo and adjacent islands (Auffenberg 1981) and formerly on New Caledonia (Flannery 1991); terrestrial crocodiles formerly on New Caledonia (Balouet and Buffetaut 1987), Fiji (Worthy et al. 1999; Worthy 2001), and Vanuatu (Mead et al. 2002); herbivorous lizards on Fiji and the Galápagos; and tortoises on the Galápagos, Aldabra, and (formerly) on many other oceanic islands (Arnold 1979; Whittaker 1998). Ectothermic vertebrates have field energy expenditures that are only about 5 to 10% of the expenditures found in endotherms of the same mass (Nagy et al. 1999). The recognition of the common element of a reduced energy expenditure in these observations required the recent acquisition of data on points 3 and 4. As a reviewer of this chapter pointed out, several island endemics that descended from continental nocturnal stocks have attained diurnal habits, including some flying foxes (e.g., Pteropus samoensis, P. neohibernicus) and the short-eared owl (Asio flammeus) in Hawaii and the Galápagos, although this owl is often active in the late afternoon in continental settings. Whether this switch has any significance for energetics, or whether it reflects opportunism in the context of low species diversity, is unclear. In this chapter island endemism will be demonstrated first in distributional patterns and then by their impact on the energetics of island endemics. Most data on the energetics of island endemics have come from measurements on the two groups of endotherms that most frequently colonize oce-



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anic islands, birds and bats. Island endemics native on and around New Zealand and New Guinea have received the most attention, although limited data are also available on bats from the Caribbean. Although bats are the subjects of this book, some relevant examples among birds will provide a broader perspective to the nature of the adaptation to island life, a decision required by the limited amount of data available on the energetics of island bats.

Distributions The physiological distinctiveness of island bats might be most marked in populations that show the greatest morphological divergence, under the assumption that this is evidence of long-term isolation. The endemism of bats on islands has occurred at various taxonomic levels, including family, subfamily, genus, species, and subspecies. But the endemics that are most morphologically distinct are not necessarily the most physiologically distinct if the physiological adjustment to island life occurs rapidly. Indeed, the evolution of a flightless condition in island rails appears to be rapid (Olson 1973; Slikas et al. 2002; Worthy 1988), as was character displacement in island honeyeaters (Diamond et al. 1989). Two families of bats are restricted to islands, Myzopodidae on Madagascar and Mystacinidae on New Zealand, two smaller remnants of Gondwana, that is, landmasses with a long history (unlike the ephemeral existence of many coralreef and volcanic islands). Both families are distinctive. Myzopoda aurita, the Old World sucker-footed bat, and a new species of Myzopoda (M. schliemanni) that has just been described (Goodman et al. 2007) have suction disks attached to the wrists and ankles, the anatomy of which suggests evolution independent of the four species of the continental New World sucker-footed bats in the family Thyropteridae. Little else is known about these small insectivorous species, but given these characters, they undoubtedly readily go into torpor. The New Zealand family Mystacinidae is slightly better known. It has, or had, two species, Mystacina tuberculata and M. robusta; the latter species may have recently become extinct. These highly agile forest bats have very distinctive behaviors, including roosting in a great variety of sites, such as hollow trees, caves, crevices, and even burrows (see O’Donnell, chapter 15, this volume). They feed on flying and resting arthropods, fruit, nectar, and pollen (Daniel 1979; Arkins et al. 1999). Their expanded behavior occurs in an environment in which only one other bat is found, Chalinolobus tubercu­ latus, an insectivorous, hibernating member of the Vespertilionidae in a genus shared with Australia, New Caledonia, and New Guinea, that is, western Gondwana. Unfortunately, nothing is known of the physiology of the mystacinids, except for the observation that M. tuberculata enters torpor in winter

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and spontaneously arouses during mild winter periods (Christie and Simpson 2006; Daniel 1979). Two subfamilies of the Phyllostomidae, the Phyllonycterinae and Brachyphyllinae, are restricted to the Greater and Lesser Antilles and the Bahamas. The Phyllonycterinae contains two genera, Erophylla and Phyllonycteris, and the Brachyphyllinae has only Brachyphylla. These bats are fruit and nectar consumers. Another chiropteran subfamily that is nearly endemic to islands is the Nyctimeninae of the Pteropodidae. Only two genera are in this subfamily, one of which, Nyctimene, has 15 species. They are found principally on islands from the Philippines to Sulawesi, the Moluccas, New Guinea (which has 7 species), the Bismarcks, Solomon Islands, and Santa Cruz Islands (Mickleburgh et al. 1992). Two species reside in Queensland, Australia, one shared with New Guinea as a relict on the northern end of York Peninsula. The second genus, Paranyctimene, is represented by two species, both of which are limited to eastern New Guinea. Whether the Nyctimeninae evolved in an island environment or on the Sahul (Tasmania/Australia/New Guinea) continent is unknown. Many bat genera are endemic to islands. They include Ardops, Phyllops, Ariteus, and Stenoderma of the Stenodermatinae of the Phyllostomidae on Caribbean islands, and at least 13 genera in the Pteropodidae, most of them in southeast Asian and Pacific islands east as far as Fiji. One of the most distinctive pteropodids is Dobsonia, which has 14 species found from the Philippines and Sulawesi through New Guinea to the Solomons, one of which marginally occurs on the York Peninsula of Australia (Mickleburgh et al. 1992). The distribution of the pteropodid genus Pteropus is distinctive. It has more species than any other genus in the Pteropodidae, approximately 57 (65 by recent estimates [Simmons 2005]), but it “is primarily an island taxon, with 55 species (96.5%) having some or all of their distribution on islands. In this genus levels of endemism are extremely high, with 35 species (61.4%) confined to single islands or small island groups. Only nine species are found in continental areas (five in Asia and four in coastal Australia), and only two (P. lylei and P. poliocephalus) are restricted to continents” (Mickleburgh et al. 1992, 2). No Pteropus is found on continental Africa, two species being limited to the coastal islands of Pemba and Mafia in the Indian Ocean (fig. 6.1). One species, P. rufus, is found on Madagascar, but there it is “mostly confined to coastal areas, offshore islands, and low-lying plains towards the interior” (Mickleburgh et al. 1992, 127), although some roosts have been found in the central highlands (McKinnon et al. 2003). Why Pteropus usually avoids continental interiors is unclear. Leen and Novick (1969) suggested that the absence of Pteropus from continental Africa might result from competition with other bats or frugivorous primates, or from

SAUDI ARABIA

OMAN

YEMEN

ETHIOPIA

SO

M AL I

A

INDIAN OCEAN

KENYA

Pemba

TANZANIA

Les Amirantes

voeltzkowi

SEYCHELLES Mafia Groupe d’ Aldabra

seychellensis

Mahé

Coetivy

Atoll de Providence

Atoll de Cosmoledo

Atoll de Farquhar

COMOROSGlonoso Islands

Agalega Islands

Moroni Mayotte

E

M

B

ZA

U IQ

livingstonii

MADAGASCAR

Port Louis

O

M

Cargados Carajos Shoais

Tromelin Islands

Saint-Denis

Rodrigues Mauritius

Reunion

rufus

rodricensis

niger, subniger

Figure 6.1. The distribution of various species of Pteropus in the western Indian Ocean. (Data from Mickleburgh et al. 1992.)

Fig. 1

158

B. K. McNab

an inability to tolerate the presence of arboreal carnivores. One possibility might be competition with the superabundant pteropodid Eidolon helvum, although what characteristics this species has that might exclude Pteropus are unknown. Besides, Eidolon coexists with Pteropus on Madagascar. Kingdon (1974) questioned this interpretation, vaguely suggesting that it would be surprising if “Pteropus had not evolved subtle . . . peculiarities that reflected the stability . . . of island life, [which could have] . . . general implications for the biology of island communities in relation to continental ones” (142). (Indeed, he may have been correct—see below.) Bonaccorso (1998, 120) observed that a small proportion of a P. conspicillatus “camp” near Madang, Papua New Guinea, would fly offshore every evening and “dip their head in the ocean one or more times to drink.” Strahan (1995) noted a similar behavior in this species off Australia, which permitted crocodiles to prey on these bats. Bonaccorso raised the possibility that this behavior is required by Pteropus to compliment mineral deficiencies in its fruit diet, but if that accounts for the absence of Pteropus from continental Africa, it must distinguish Pteropus from the other pteropodids that inhabit central Africa (also see Íudica and Bonaccorso 2003). The distributional pattern of Pteropus on islands is highly variable. Some species are limited to small islands, which suggests a highly sedentary existence. Such sedentary species include P. voeltzkowi on Pemba, P. livingstonii on Anjouan and (perhaps) Mohéli in the Comoros, P. rodricensis on Rodrigues, although it was also found on Mauritius (Mickleburgh et al. 1992), and P. niger on Mauritius, all four in the Indian Ocean (fig. 6.1); and P. howensis on Ontong Java Atoll and P. mahaganus on Santa Isabel in the Solomon Islands (fig. 6.2). Other species are found on islands that are hundreds or even thousands of kilometers apart, but they usually avoid large islands or continents, even if nearby. In the South Pacific these species include P. tonganus, P. samoensis, and P. mariannus (fig. 6.2). Some predominantly small-island species are occasionally found on larger islands. These species include P. pumilus, a Philippine species that occurs on the intermediate-sized islands of Leyte and Negros (Mickleburgh et al. 1992), and P. hypomelanus, which at the eastern edge of its distribution has been found twice on New Guinea and once on New Britain (fig. 6.3). This latter species (or species complex, which molecular data may show to be several distinct species) is found as far west as the Philippines, Malay Peninsula, and Burma, principally on coastal islands. A small-island distribution similar to that of some Pteropus is found in some fruit-eating imperial-pigeons, genus Ducula, especially D. pacifica, D. pis­ trinaria, and D. oceanica, which collectively divide the central Pacific into allopatric distributions, whereas other species belonging to this genus, most notably D. zoeae, D. rufigaster, D. chalconata, and D. pinon, are almost completely restricted to the large island of New Guinea (Coates 1985). Still other species, e.g., D. latrans, D. aurorae, and D. galeata, today are restricted to one or two

alecto

GU INE

AUSTRALIA

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K I R I B AT I (GILBERT ISLANDS)

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SANTA CRUZ ISANDS

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Norfolk Island

COOK ISLANDS

tonganus

Pago Pa ago Pago

TONGA

KERMADEC ISLANDS

Apia

Avarua

samoensis

NEW ZEALAND

Suva

SAMOA

nitendiensis, santacrucis

Tarawa

anetianus vetulas Kingston

Noumea

poliocephalus

ornatus

New Caledonia

SOLOMON ISLANDS

NAURU rayneri howensis Bougainville

mahaganus

New Britian

New Ireland

capistratus, gilliardorum

Kosrae

MARSHALL ISLANDS

phaeocephalus

molossinus Palikia

insularis

CAROLINE ISLANDS

neohibernicus tonganus NE

Yap

Saipan Hagatna Guam

NORTHERN MARIANA ISLANDS

Figure 6.2. The distribution of some species of Pteropus in the central Pacific. (Data from Mickleburgh et al. 1992.)

scapulatus

conspicillatus

PALAU

Koror

mariannus

B. K. McNab

160

.%7)2%,!.$

"/5'!).6),,% 0!05!.%7'5).%! .%7"2)4!).

3/,/-/.)3,!.$3

Figure 6.3.  The distribution of Pteropus hypomelanus in Papua New Guinea and the Solomons. (Figure and data modified from Bonaccorso 1998 and Flannery 1995b.)

islands as a result of human-based extinctions on other islands (Steadman &IG 1997, 2006).

Energy Expenditure One of the responses of many endotherms committed to life on oceanic islands is a reduced rate of energy expenditure. Ideally, the most appropriate information would concern the energy expenditure of individuals free-living under field conditions, but such data are rarely available, and not at all for island endemics. However, some measurements are available on the standard, or basal, rate of metabolism of island endemics and their large-island or continental relatives. An examination of the variation in basal rate is justified by the general correlation that exists between field and basal rates in mammals (Koteja 1991; Nagy 1987; Nagy et al. 1999; Ricklefs et al. 1996; Speakman 2000): species with low basal rates generally have low field expenditures, both because of a reduction in mass and independent of the influence of mass. Because basal rate increases with body mass, one way to reduce energy expenditure is through a reduction in mass. (The widespread notion that rate of metabolism decreases with an increase in body mass derives from the dependence of total rate on mass raised to a power less than 1.00 and therefore applies only to mass-specific units. All animals live on a total mass basis: the only species that live on per-gram basis weigh 1 g [McNab 1999].) An intraspecific correlation exists between body size and island size in some widely distributed Pteropus (e.g., P. tonganus, P. neohibernicus [Bonaccorso 1998]), but the extent to which this occurs and the magnitude of this correlation are unexplored.



Physiological Adaptation of Bats and Birds to Island Life

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Interspecifically, the largest Pteropus are limited to continents and the largest islands, intermediate-sized species are found on large and intermediate islands, and the smallest species are found on intermediate and small islands, which suggests that a maximal size limit exists in Pteropus relative to island size (fig. 6.4). The only exceptions occur when a large species spills over to small islands from an adjacent large island or continent, which is the case in P. vampyrus. These small-island populations of large-bodied species are unlikely to be self-sustaining. Rate of energy expenditure can also vary independently of mass. Basal rate of metabolism in phyllostomids, pteropodids, and pigeons, corrected for body mass, correlates with island size. A potential complication (see below) is that a widely distributed species may have populations that have adjusted their expenditures to local conditions, so no one rate may characterize a species. Unfortunately, few endotherms have had their basal rates measured from landmasses of different sizes, observations that are critical to understanding the impact of a commitment to island life. In one example, two banded rails (Gallirallus philippensis) from Australia had slightly higher, but not significantly different, basal rates than two individuals from New Zealand (McNab and Ellis 2006), a comparison plagued by a small sample size. A crocidurine shrew also may have lower rates of metabolism on a Mediterranean island than on the French mainland (see below). With these limitations in mind, a reduction of basal rate in island endemics has been shown among phyllostomids in the Caribbean (fig. 6.5). Among 25

vampyrus size limit 

Forearm length (cm)

20

neohibernicus rayneri

giganteus

X

X

samoensis 15

X

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scapulatus

X

hypomelanus 10

rodricensis

pumilus

personatus

molossinus 0

2

4

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!5

6



Log10 Island area (km2)

Figure 6.4.  Forearm length of various species of Pteropus as a function of the area of the landmasses on which they are found. A size limit is suggested. (Figure modified from McNab 1994b.) NG = New Guinea; AU = Australia. &IG

B. K. McNab

162 3.5 Pteropodidae

Log10 basal rate of metabolism (mL O2/h)

3.0 continental species/good tr ( )

2.5 small-island endemics

2.0 island species/good tr ( )

1.5 X

X

X X

continental species /poor tr ( X )

1.0

0.5 0.5

1.0

1.5

2.0

2.5

3.0

3.5

Log10 body mass (g)

Figure 6.5.  The correlation of log10 basal rate of metabolism in pteropodid bats as a function of log10 Fig. 5 body mass. The data are segregated into three groups: continental species with good temperature regulation, continental species with marginal temperature regulation, and island endemics with good temperature regulation. (Data and analysis derived from McNab and Bonaccorso 2001.)

30 species of phyllostomids, variation in body mass, food habits, altitudinal distribution, and presence on Caribbean islands or on South America accounted for 99.4% of the variation in basal rate (McNab 2003). Two nectar/fruit-eating species native to the intermediate-sized island of Puerto Rico, the glossophagine Monophyllus redmani and the phyllonycterine Erophylla bombifrons (RodríguezDurán 1995), have basal rates that averaged 58% of the mean basal rates of continental species. Although some continental phyllostomids have basal rates as low as the two island endemics, they have food habits (insectivory, sanguinivory, or omnivory) that are correlated with low basal rates, whereas South American nectar/frugivores, the appropriate standard for these Caribbean species, have basal rates that are 1.73 times those endemic to Puerto Rico (fig. 6.5). Unfortunately, no data are available from populations of phyllostomids found on small islands in the Bahamas and Lesser Antilles. Especially interesting would be measurements of Glossophaga soricina from Jamaica and the Bahamas, or of G. longirostris from the Lesser Antilles, to compare with South American populations of the same species. Among 23 populations and species of pteropodids, variation in body mass,



Physiological Adaptation of Bats and Birds to Island Life

163

capacity for temperature regulation, and distribution on large islands/continents or small islands accounted for 98.0% of the variation in basal rate (McNab and Bonaccorso 2001). Small-island endemics, Pteropus pumilus, P. rodricensis, and P. hypomelanus, collectively had basal rates that were 78% of those from large islands or continents (fig. 6.6). Of these three “small-island” species, the one truly limited to a small island, P. rodricensis, which is found only on Rodrigues in the Indian Ocean, has by far the lowest basal rate (73%, corrected for body size), whereas the other two species, P. hypomelanus (88%) and P. pumilus (85%), are occasionally found on larger islands and have basal rates equal to the two continental species with the lowest basal rates, P. poliocephalus (86%) and P. giganteus (83%). The highest mass-independent basal rate in Pteropus was found in vampyrus (141%), a species found on mainland Southeast Asia, Sumatra, the Philippines, and smaller islands east to Timor. Furthermore, of four species of Dobsonia studied, the two with the highest basal rates (D. mo­ luccensis [136%] and D. minor [109%]) are found on the large-island/continent of New Guinea, whereas the other two (D. anderseni [98%] and D. praedatrix [102%]) have lower basal rates and are found on the intermediate islands of New Britain and New Ireland (fig. 6.6), although recent measurements on these

Log10 basal rate of metabolism (mL O2/h)

2.5 Phyllostomidae

2.0

continental species, nectar/fruit-eaters, carnivores( )

continental omnivores( )

high-altitude x

1.5

x x

continental vampires (x )

M. californicus (continental insect-eater)

1.0

0.5 0.5

island nectar/fruit-eaters ( )

1.0

1.5 Log10 body mass (g)

2.5

2.0

Figure 6.6.  The correlation of log10 basal rate of metabolism in phyllostomid bats as a function of log10 body mass. The data are divided into five groups: continental lowland species with various diets, continental omnivores (Phyllostomus), continental vampires, island nectar and fruit eaters, and Macrotis californicus, a continental insect eater. (Data and analysis derived from McNab 2003.) Fig. 6

B. K. McNab

164

two latter species indicated higher basal rates (S. G. Hamilton, pers. comm.). Some small continental pteropodids have basal rates as low as those found in small-island endemics, but they are characterized by a propensity to enter torpor (fig. 6.6). A similar pattern exists among pigeons: variation in body mass, climate, and a continental or island distribution accounted for 94.8% of the variation in basal rate of metabolism in 27 species (McNab 2000). The effect of island size is clearly seen in Ducula. The small-island endemics D. pacifica and D. pistrinaria have basal rates that averaged 66% of those found in large-island or continental species, corrected for mass (fig. 6.7). Of these two species, D. pistrinaria has a higher basal rate than D. pacifica, 74% and 61%, respectively, possibly associated with the occasional occurrence of D. pistrinaria on larger islands, for example, in lowland New Britain, New Ireland, and Bougainville (Coates 1985; fig. 6.7), and the near restriction of D. pacifica to small islands. Furthermore, D. pacifica is smaller (330 g) than D. pistrinaria (394 g), which further contributes to a reduced expenditure in D. pacifica. Imperial-pigeons that are principally found on intermediate-sized and smaller islands, including D. bicolor and D. rubricera, have intermediate basal rates, 87% and 91%, respectively, whereas species that 3.0 large-island/continental species Columbidae Goura

Log10 basal rate of metabolism (mL O2/h)

Aschoff-Pohl nonpasserine curve

2.5

continental species

all-columbid curve

intermediate-island species X

X

small-island species

2.0 X

temperate species tropical species X desert species

X X

1.5 1.5

2.0

2.5

3.0

3.5

Log10 body mass (g) Figure 6.7.  The correlation of log10 basal rate of metabolism in pigeons as a function of log10 body mass. The data are divided into four groups: continental species living in the temperate zone, continental and large-island species living in the tropics, tropical species living on intermediate-sized isFig. 7 lands, and tropical species living on small islands. (Data and analysis derived from McNab 2000.)



Physiological Adaptation of Bats and Birds to Island Life

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"ASALRATEOFMETABOLISMM,/H



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Figure 6.8.  The correlation of the absolute basal rate of metabolism (mL O2/h) as a function of log10 island area in bats and pigeons. A suggested limit to metabolism is indicated by the dotted &IG curve. (Data from McNab 2000, 2003; McNab and Armstrong 2001; McNab and Bonaccorso 2001.) NG = New Guinea; AU = Australia; NB = New Britain.

are restricted to New Guinea, including D. rufigaster, D. pinon, and D. zoeae have higher basal rates, that is, 90%, 97%, and 108%, respectively. Clearly, the basal rate of imperial-pigeons is positively correlated with island size. What is most striking about the relationship between basal rate and island size in bats and pigeons is that species with high basal rates, both because of a large mass and high rates independent of body size, tend to be limited to intermediate and large islands, whereas small-island bats (P. rodricensis, P. pumilus) and pigeons (D. pacifica, D. pistrinaria) have the lowest absolute basal rates (fig. 6.8). Bats and pigeons appear to differ in one distributional aspect of energetics: the relation between energy expenditure and altitude. The few data presently available indicate that basal rate in bats increases with altitude in South America (e.g., high-altitude [2,400 m] Anoura latidens and Sturnira erythromos have higher basal rates [155% and 151% of the values expected for phyllostomids, respectively] than low-altitude [20–700 m] A. caudifer [134%], S. lilium [120%], and S. tildae [127%]; McNab 2003; Soriano et al. 2002). Similarly, in New Guinea intermediate-altitude (650 m and 2,100 m) populations of Syconycteris australis and Macroglossus minimus have higher basal rates (110% and 94% of the values expected of pteropodids, respectively) than low-altitude (0–40 m) populations of the same species (68% and 57%, respectively; Bonaccorso and McNab 1997; McNab and Bonaccorso 2001).

166

B. K. McNab

In contrast, some fruit pigeons that are found on small islands near sea level also occur on large islands in the South Pacific at high altitudes, and these species have lower basal rates than fruit pigeons limited to low altitudes on large islands. This is the case in the Papuan mountain-pigeon (Gymnophaps albertisii), which principally breeds at altitudes >2,000 m in New Guinea (Beehler et al. 1986) and is also found on Bacan, Yapen, and Goodenough islands; it has a basal rate that is 88% of the mean columbid curve. The white-throated pigeon (Columba vitiensis), which is found preferentially on small islands from the Philippines to Samoa, is also found on New Guinea, where it occurs up to 2,750 m (Beehler et al. 1986); this pigeon has a basal rate equal to 90% of the columbid curve, equivalent to the basal rates of Ducula from intermediate islands. Low-altitude pigeons restricted to New Guinea, however, have basal rates between 90% and 112%. The Pacific imperial-pigeon (D. pacifica), which is normally restricted to small islands and has a very low basal rate, is found on the larger Samoan islands, but only at altitudes >1,000 m, where no other Ducula is found. This species does not occur on the larger islands of Fiji, which have the endemic Ducula latrans (Watling 1982). Some birds other than pigeons are also found at sea level on small islands and at high altitudes on New Guinea, including Megalurus timoriensis, Turdus poliocephalus, Phylloscopus trivirgatus, and Erythrura trichroa, and species that belong to the genera Zoothera, Rhipidura, and Petroica (Mayr and Diamond 2001). Furthermore, the minimal altitude at which these incursions occur increases with island size. This distributional pattern cannot be due to a climatic similarity among these environments, so it must be explicable by some other factor (see below). Recent measurements on T. poliocephalus, Gallicolumba beccarii, and two species of Rhipidura at altitudes from 2,000 to 2,850 m in New Guinea indicated that the species most prone to occupy high altitudes have low basal rates (pers. obs.). Whether this pattern is found in any bats is unclear, although various species of Rhinolophus, which occur at low altitudes on smaller islands, are most abundant at altitudes >1,000 m on New Guinea (Bonaccorso 1998, pers. comm.; Flannery 1995a, 1995b).

Food Habits Because rate of energy expenditure and capacity for endothermy are correlated with food habits in mammals (McNab 1992), and specifically in phyllostomids (McNab 2003), a question arises whether a change in rate of metabolism in bats that colonize oceanic islands might reflect a change in food habits during the evolution of endemic taxa. As we have seen, the Mystacinidae in New Zealand, which presumably was derived from insectivorous microchiropteran ancestors and may be related to the noctilionids of the Neotropics (Pierson et al. 1986; Teeling et al. 2003; Van den Bussche and Hoofer 2000), a family of two species, one insectivorous and the other piscivorous/insectivorous, evolved a highly



Physiological Adaptation of Bats and Birds to Island Life

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diversified diet in the absence of other bats with these habits. If energetics in the Phyllostomidae is a guide (McNab 2003), a dietary shift from insects to a mixed diet of insects, fruits, and nectar might be associated with an increase in rate of metabolism and the capacity for endothermy, but no data are available on the energetics of Mystacina. No evidence suggests that other groups of bats endemic to oceanic islands have changed their diet, compared to the diets of their continental relatives, although few studies of the food habits of bats on isolated islands are available.

Why No Flightless Bats? A common response of some birds to life on oceanic islands has been the evolution of a flightless condition (McNab 1994a). This has occurred repeatedly in the Rallidae (rails, gallinules) and Anatidae (ducks, geese), and occasionally in other families, including Phalacrocoracidae (cormorants), Threskiornithidae (ibises), Rhynochetidae (kagus), Raphidae (dodo, solitaire), Columbidae (pigeons), Psittacidae (parrots), Strigidae (owls), Acanthisittidae (New Zealand wrens), and Emberizidae (buntings). A flightless condition has occurred so often that it is unlikely to be the result of chance alone, but has been suggested (McNab 1994a, 1994b, 2002; McNab and Ellis 2006) to be a pattern directed by energy conservation in the absence of eutherian predators: flightless birds have lower basal (and presumably field) energy expenditures than their flighted relatives, in part associated with a reduction in pectoral muscle mass. Given that the evolution of a flightless condition is so widespread in island birds, why has it not occurred in island bats? Although the New Zealand Mystacina tuberculata is occasionally rumored to be flightless, that is not the case, even though it does move on the ground and enter burrows. The evolution of a flightless condition in birds of necessity occurs in species that use food resources that do not require flight. Flightless birds on islands are terrestrial carnivore/omnivores (kiwis, rheas, emus, rails, kagus, ibises), grazing or browsing herbivores (ostriches, takahes, gallinules, moas, kakapos, anatids), aquatic herbivores or carnivores (anatids, gallinules, cormorants), or frugi­ vores (cassowaries, dodos, solitaires, Fiji pigeons) that presumably fed on fallen fruit. So, in spite of bat endemism on landmasses where flightless condition in birds has evolved (e.g., New Zealand, New Caledonia, Fiji), it has not evolved in bats, probably because bats have not evolved the appropriate food habits, the only likely possibilities being terrestrial omnivory or frugivory, food habits usually occupied by birds.

Is Island Size Absolute or Relative? A consideration of the impact of an island environment on the biology of endemics raises a question whether island size is absolute or relative to the size of

168

B. K. McNab

the invader/endemic. That is, do small endemics respond to an island environment with a reduction in rate of metabolism as do many large endemics? As noted, some small island-endemics have low basal rates, including Hawaiian honeycreepers, which weigh between 8 g and 19 g, and Caribbean phyllostomids, which have masses from 9 g to 16 g. Recent measurements on the shrew Crocidura suaveolens have shown that large individuals from the Mediterranean islands of Porquerolles and Corsica have total rates of metabolism similar to those of smaller individuals from mainland France (Magnanou et al. 2005), that is, that island individuals have, corrected for size, lower rates of metabolism. Furthermore, several species of New Zealand wrens (Acanthisittidae) evolved a flightless condition (Millener 1988, 1989; Millener and Worthy 1991), as did a bunting from Tenerife, Canary Islands (Rando et al. 1999). These data suggest that some small species respond to a landmass that is quite large (e.g., Hawaii; South Island, New Zealand) as an island environment, which implies that island size is absolute: that is, an island by definition is different from a continent and that an invading species will respond to this “uniqueness” regardless of its size or that of the island. Difficulties with this conclusion are that a tendency also exists for some species that are small on continents to increase mass on islands (Foster 1964; Kikkawa 1976; Lomolino 1985) and, as seen, fruit pigeons of the genus Ducula have basal rates that vary with island size. And the Puerto Rican tody (Todus mexicanus), in spite of its erroneous species name, is endemic to Puerto Rico, weighs about 6 g, and has a basal rate of metabolism that is 33% higher than expected from mass (Merola-Zwartjes and Ligon 2000). The answer to the question of whether island size is absolute or relative to the size of a resident obviously needs to be investigated by concentrating on the response of small species to an island environment. What is it about islands that may make some, many, or most species physiologically responsive to its island status?

Why Is an Island Environment Different? Three suggestions have been given to explain why island endemics tend to reduce energy expenditure compared to that of their relatives on continents. One is that small islands are characterized by a limited resource base and unstable conditions as a result of their inability to buffer the stochastic effects of cyclonic events, El Niño/La Niña cycles, and volcanic activity (Köhler and Moyà-Solà 2004; McNab 1994b). A reduced individual energy expenditure would facilitate long-term survival in a highly stochastic environment by permitting larger populations to survive on a restricted resource base. A second potential contributor to the low energy expenditures of island endemics, and especially for the presence of flightless birds, is the absence of mammalian predators (Köhler and Moyà-Solà 2004; McNab 1994a). Indeed, it is the absence of eutherian predators that is paramount (McNab and Ellis 2006),



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because the presence of marsupial and avian predators on Australia and New Guinea and avian predators on New Zealand and many other islands did not prevent the evolution of flightless rails. Specifically, avian predators belonging to the genera Falco and Accipiter, which are widespread on oceanic islands, preferentially prey on birds in flight, and are therefore unlikely to be effective predators of flightless birds. From the view of predation, Australia is a continent with many of the characteristics of an island, as shown by the (former) presence of terrestrial crocodiles and large varanid lizards as the top predators (Flannery 1991), conditions that were also seen on islands like New Caledonia, Fiji, and Vanuatu, and by the (former) presence of a flightless gallinule (Gal­ linula mortierii) on Australia in spite of the presence of marsupial predators (Olson 1975). This gallinule disappeared from Australia only after the human introduction of the eutherian dingo (Canis lupus [dingo]; Baird 1991). A third suggestion is that the difference between islands and continents is the greatly reduced species richness on islands (McNab 2007), due principally to the small size and distance of islands from a source of additional species (Mac­ Arthur and Wilson 1967). A high reproductive rate, facilitated by a high rate of metabolism (McNab 1980) and permitted by a large resource base, might be required on continents where competition, predation, parasitism, and disease are intense. On islands these factors are reduced, and therefore a low reproductive output could be tolerated, accomplished by reducing energy expenditure, and even preferred as a result of an area-limited resource base. Indeed, island endemics tend to have long life spans and low rates of reproduction (Cody 1966; McNab and Ellis 2006). A low species richness may also account for the occurrence of some species at sea level on small islands and at high altitudes on large islands since species richness also diminishes with altitude. If the factor most important for setting the level of energy expenditure in island endemics is species richness, including the presence or absence of appropriate predators, then all oceanic islands, regardless of size, would be distinct from continents, evidence of which would be a reduction in energy expenditure in both large and small island-endemics. However, if the problem with an island existence were the shortage of resources and the presence of unstable climatic conditions, a large island would probably be a more “forgiving” environment than a small island, and the reduction in energy expenditure would be most likely to occur in large species. Thus a small species would be less restrained than a large species on the same island, given the correlation of expenditures with body mass.

Where Do We Go from Here? The fundamental problem that we presently have in analyzing the complex physiological responses of vertebrates endemic to islands is that very few data are available. At best, the analysis given above is incomplete. We need many

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more data, especially on small species that live on small and large islands distant from a source area, and on the degree to which populations within species have energy expenditures that vary with the size and isolation of islands. In addition, we need, as a (phylogenetic) control, information on large-island and continental species that are related to small-island endemics. Very few of these requirements have been met, and until they are fulfilled we will not be able to give an adequate analysis of the adjustments required for life on oceanic islands. However, one conclusion appears to be secure: life on oceanic islands is sufficiently different from life on continents to require some (many? most? all?) continental species that invade an island environment to make a significant readjustment of their functional, behavioral, and ecological characteristics for them and their descendents to survive. As a result, island endemics have been shown to include many distinctive species, including terrestrial crocodiles, giant lizards, giant tortoises, and flightless birds. Furthermore, islands to some extent have acted as a refuge for some taxa that have been spared the intense competition and predation found on continents. These taxa include the tuatara, kiwis, mesites, todies, solenodontids, tenrecs, and lemurs, as well as monotremes and marsupial carnivores and grazers (here treating Australia as an island/continent; see McNab 2005), among others, most of which appear to have low standard rates of metabolism. Bats endemic to islands share some of the characteristics found in birds on these islands, including acting as refuge for such distinctive families as Mystacinidae and Myzopodidae, the Phyllonycterinae and Brachyphyllinae subfamilies, and genera like Nyctimene, Dobsonia, Ardops, Phyllops, Ariteus, and Stenoderma.

The Continuing Disaster Befalling Island Faunas Island faunas have experienced some of the greatest destructive impacts of human presence on this planet. Hundreds of flightless birds have evolved on islands in the absence of eutherian predators. Almost all are now extinct, and most disappeared soon after the appearance of the first humans (Steadman 1995; Steadman and Martin 2003), often thousands of years before the appearance of European mercenaries. A factor contributing to the vulnerability of island endemics may have been their propensity to evolve low energy expenditures with the consequent reduction in reproductive output and therefore a reduced capacity to respond to a human-based increase in mortality by increasing fecundity (McNab 2006). Humans have not only been a principal predator, but also have modified the environment through the destruction of native forests and the conversion of islands into minicontinents by the importation of predators, such as the Pacific rat (Rattus exulans), pigs, dogs, mustelids, mongooses, and parasites, such as avian malaria in Hawaii. Although the consequences for faunas native to islands have been most apparent on the avifauna, it also has



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impacted the invertebrate, reptile, and bat faunas of these islands. Some islands that appear either to have few or no bats had larger bat faunas before humans arrived than they presently have (e.g., Koopman and Steadman 1995). Islands occupied by humans probably can never be restored to their original “noncontinental” status without the elimination of all eutherian predators, including humans. The only hope for the long-term survival of distinctive island endemics is on the few offshore islands uninhabited by people (Steadman and Martin 2003) that have been cleared of eutherian predators. This has been the successful strategy of the Department of Conservation in New Zealand and needs to be applied to other island systems. Another long-term threat for terrestrial island faunas (and countries) is the likelihood of sea-level rise as a result of global warming.

Conclusions Bats that are endemic to oceanic islands facilitate long-term survival by reducing their energy expenditures through a reduction in mass and in expenditures independent of a change in mass, in part to reflect a limited resource base. These adjustments have often limited bats to a distribution on small islands where the levels of competition and predation are greatly reduced. This geographic restriction threatens the persistence of island endemics because of the destructive activities of humans and the possibility that a sea-level rise will flood many of the smaller, low-altitude islands and archipelagos.

Acknowledgments This article would not have been written without the invitation and encouragement of Ted Fleming. I thank Frank Bonaccorso for correcting an early version of this manuscript and for all of his aid while cooperatively working in Papua New Guinea. I also greatly appreciate the thoughtful suggestions of this manuscript by three anonymous reviewers and by Ted Fleming. Their views made a constructive contribution to this chapter.

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Chapter 7

The Role of Pteropodid Bats in Reestablishing Tropical Forests on Krakatau Louise A. Shilton and Robert J. Whittaker

Introduction This chapter presents an appraisal of the role of pteropodid bats (Megachiroptera) in the reestablishment of tropical forests on the Krakatau Islands following destruction of the preexisting ecosystems by volcanic eruptions in 1883. The recovery process is sufficiently well known that we can regard Krakatau as a model system, in the present context providing valuable insight into pteropodid bats as agents of seed dispersal at a scale relevant not only to colonization of other islands but also to the exchange of propagules between patches of forest in today’s typically fragmented tropical landscapes. The Krakatau Islands are a group of four small volcanic islands situated in the Sunda Strait between Java and Sumatra, roughly 40 km and 32 km respectively from the two “mainland” landmasses (Whittaker and Jones 1994a). The Sunda Strait area has a tropical rainy climate with few dry months classified as “Afa” under the Koeppens World System (Whittaker et al. 1989). The “wet season” is signified by the west monsoon usually from November to April, which brings heavy rainfall from the Indian Ocean (Dammerman 1948) and prevailing winds from the direction of Sumatra to Java with an average velocity of 20 km/h (Thornton 1996). The “dry season” corresponds with the east monsoon from May to October, when relatively dry air blows from West Java at an average velocity of 22 km/h (Thornton 1996). The region is affected by El Niño Southern Oscillation events, bringing sometimes pronounced interannual variability in prevailing weather conditions. The Krakatau group is highly volcanic as it is close to a point of lateral stress crossing a destructive plate margin (Thornton 1996). In August 1883 the islands were devastated by a sequence of huge volcanic eruptions. At their conclusion on August 28, the largest of the three preexisting islands had been reduced to one-third of its former area, and all three islands were entirely stripped of their forest and covered in great depths of sterile volcanic ejecta (Simkin and Fiske 1983). These islands are now known as Rakata (730 m a.s.1., 17 km2 in 176



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Figure 7.1.  The Krakatau archipelago (Anak Krakatau, Panjang, Rakata, and Sertung) and stepping­­stone ­islands, Sebesi and Sebuku, Sunda Strait, Indonesia.

area), Sertung (180 m, 13 km2), and Panjang (140 m, 3 km2). The fourth island, Anak Krakatau (“child of Krakatau”; 300 m, 3.5 km2), emerged as an enduring presence in the center of the caldera in 1930 and is highly active volcanically (fig. 7.1). Following the 1883 event, natural scientists swiftly recognized the unique potential that the islands, devoid of all life, presented for studying the processes of colonization (e.g., Docters van Leeuwen 1936; Ernst 1908, 1934; Penzig 1902; Treub 1888). Their early survey efforts laid the foundations for what has become the best-known case study of primary succession from bare ground to forest communities in the tropics (Whittaker et al. 1989). Nonetheless, most research on Krakatau prior to the 1920s was undertaken during brief expeditions for which the primary focus was to identify the main plant associations and enumerate the arrival of plant species (e.g., Ernst 1934; Whittaker et al. 1989). More frequent and intensive fieldwork in the period 1919–1932 was accompanied

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by observational and experimental work on plant dispersal mechanisms, notably by Docters van Leeuwen (1936). Despite these efforts, Whittaker and Jones (1994a) and Whittaker et al. (1997) had to rely largely on indirect forms of evidence or inference from the published literature to assign a dispersal mechanism to a plant species. Research reported here was collected during the first systematic and intensive studies attempting to assess animal-mediated seed dispersal on Krakatau through catching pteropodid bats, assessing diet species, and examining their foraging behavior (Shilton 1999; Shilton et al. 1999).

The General Pattern of Colonization of Post-1883 Krakatau The first sign of life on post-1883 Krakatau was a spider, recorded by an expedition in 1884 (Cotteau 1886). Two years later, a botanical team recorded mosses, blue-green algae, flowering plants, and ferns (Treub 1888). Other lifeforms arrived quickly thereafter, and by 1897 Rakata supported young trees interspersed within tall, dense grasslands and an abundance of ferns (Penzig 1902). Since then, cumulative data from botanical surveys indicate a marked and rapid increase in the colonization of vascular plants on Krakatau, with nearly 300 species by 1934, and between 423 and 456 by 1983 (Whittaker et al. 1989; Whittaker et al. 1992; Whittaker and Jones 1994a, 1994b). The cumulative total of vascular plants now stands at approximately 540 species (RJW and T. Partomihardjo, unpublished data). Animal colonization of post-1883 Krakatau has been studied only intermittently since the first zoological survey in 1908 (Jacobsen 1909). Although Dammerman (1922, 1948) made at least four systematic surveys of animals during 1919–1934, the arrival of animals has been less well documented than that of plants (Whittaker and Jones 1994a). The next zoological survey, in 1951, was almost entirely limited to birds (Hoogerwerf 1953). Thereafter, faunal surveys were not resumed until the 1980s (e.g., Rawlinson et al. 1992; Thornton et al. 1988; Thornton et al. 1993; Tidemann et al. 1990; Zann et al. 1990). Consequently, there are substantial gaps in our knowledge of the sequence of arrival of the earliest vertebrate colonists. Today, Krakatau supports a wide variety of vertebrate and invertebrate fauna, including bats, birds, snakes, lizards, rats, pigs, crabs, scorpions, spiders, beetles, butterflies, ants, and termites (e.g., Thornton et al. 1988; Thornton et al. 1993). Cumulatively, 89 species of vertebrates have been recorded on the islands since 1883: 54 birds, 11 microchiropteran bats, 8 pteropodids, 11 reptiles, 2 snakes, 2 species of rat, and a pig (Rawlinson et al. 1992; Schedvin et al. 1994; Shilton 1999; Thornton et al. 1990; Tidemann et al. 1990). Not surprisingly, given the 32–40 km ocean barrier to Krakatau from mainlands, more than 80% of recorded vertebrate species are volant: bats and birds. Three scales of plant dispersal are recognized on Krakatau: first, interisland dispersal of seeds, or spores, to Krakatau from the mainlands or stepping-stone islands (Shilton 1999; Thornton et al. 2002; Whittaker and Jones 1994a); second,



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interisland dispersal within the Krakatau group; and third, local spread or seed scatter intraisland. The first is hereafter referred to as “long-distance” dispersal in the context of the Krakatau group. Following our previous work, the means by which plants are considered most likely to have reached Krakatau is termed the “primary” dispersal mode, and where a species is designated, for instance, as “sea-bat” dispersed, this means that the species is diplochorous, with a primary dispersal mode of flotation and secondary local spread being carried out by bats. Whittaker and Jones (1994a) categorized 124 plant colonists, which had colonized Krakatau by 1992, as being primarily dispersed endozoochorously, internally, via the gut of an animal. Of these, they designated 50 as exclusively bird-dispersed, 31 as primarily bird-dispersed but secondarily bat-spread, and 43 as either bird- or bat-mediated colonists. The latter category was based on a reluctance to discount either possibility without more evidence. Whittaker and Jones (1994a) were able to identify only a small number of species as likely candidates for arrival via bat guts, although this set included early colonists such as Ficus fulva and F. septica. In contrast, Ernst (1908) considered all endochorous arrivals by 1908 to have been introduced by birds, and Docters van Leeuwen (1936) considered only one of the endozoochorous colonists up until 1934, Piper blumei, to have probably been introduced by pteropodid bats rather than birds. Animal introduction of zoochorous plants has been pivotal to the development of Krakatau’s interior forests (Whittaker et al. 1989; Whittaker and Jones 1994a, 1994b). Although the first true zoochores colonized later than the first sea-dispersed (thalassochorous) and wind-dispersed (anemochorous) plants (Whittaker and Jones 1994b), a predominantly zoochorous mode of tree arrival has occurred over the past 70 years, with few solely thalassochorous species colonizing since 1930 (Whittaker et al. 1989; Whittaker and Jones 1994b). Nonetheless, zoochores with seeds too large even for transport by Ducula fruit pigeons, the largest avian frugivores recorded on Krakatau, are unable to reach these islands unless they are diplochores and able to arrive in a viable state after flotation on the sea (Whittaker and Jones 1994b; Whittaker et al. 1997). Hence, arrival rates of zoochores are also constrained by the isolation of the islands. Today, at least 173 primarily zoochorous species have reached Krakatau (RJW and T. Partomihardjo, unpublished data). Many of the primarily endozoochorous species are trees of the interior forests, including numerically important species Timonius compressicaulis, Dys­ oxylum gaudichaudianum, and Ficus species (fig trees; Moraceae). Ficus species were among the first zoochorous trees to establish on post-1883 Krakatau (first records in 1896; Penzig 1902). Despite poor records of early vertebrate arrival, Thornton et al. (1996) showed a positive correlation between the documented arrival of pteropodid bats and frugivorous birds and the accumulation of Ficus species, consistent with a virtual circle of increasing in situ fig fruit production

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making the islands a progressively more suitable habitat for frugivorous birds and bats, thereby bringing more zoochorous species to the islands (Docters van Leeuwen 1936; Thornton 1996). Ficus fulva, F. hispida, F. padana, and F. septica had colonized post-1883 Krakatau by 1897 (Penzig 1902; Thornton et al. 1996), and F. fistulosa, F. hirta, and F. montana by 1908 (Ernst 1908; Whittaker et al. 1989). Fig fruit production was first recorded in 1897 (Penzig 1902), indicating that Ficus arrival preceded 1896. By the mid-1990s, 23 Ficus species had established on Krakatau, including strangler and other canopy-layer fig trees, making Ficus not only the most represented genus of trees but also one of the most important components ecologically (Compton et al. 1994; Thornton et al. 1996; Whittaker et al. 1989; Whittaker and Jones 1994a).

Animal Agents of Seed Dispersal on Krakatau Excluding human introduction and spread of plants on Krakatau, some seed dispersal (and, in some cases, seed predation) is effected by pteropodid bats, birds, rats, skinks, a pig, land crabs, and ants (Iwamoto 1986; Thornton 1996). While rats, land crabs, skinks, and ants provide secondary seed dispersal on a local scale (Shilton 1999; Whittaker and Jones 1994a; Whittaker and Turner 1994) they have no interisland dispersal role. Today, a role in interisland seed transport cannot entirely be eliminated for the pig (Sus scrofa), as these pigs are good swimmers (Wallace 1880, cited in Thornton 1996, 108) and have the potential for endozoochorous seed transport (Green and Jewell 1965). However, all sightings indicate that the pig is confined to Panjang, where it has been recorded since 1982, and suggest a recent, and possibly human-mediated, arrival ­of the species. Hence, in addition to their role in intraisland seed movements at the local scale, pteropodid bats and frugivorous birds are the only nonhuman agents of early zoochorous colonization on Krakatau (Shilton 1999; Whittaker and Jones 1994a). Prior to fieldwork from 1995 to 1997, 16 species of partially or wholly frugivorous birds and 7 species of pteropodid bats had been documented on Krakatau at some point before 1992 (Thornton et al. 1992), but were not necessarily still resident on these islands (Rawlinson et al. 1992; Schedvin et al. 1994; Thornton et al. 1993). Although the documented arrival of bats is almost certainly incomplete, pteropodids are thought to have colonized Krakatau before microchiropteran bats (Tidemann et al. 1990). The earlier establishment of pteropodid populations on Krakatau can be explained by general differences in roosting ecology, because most of the pteropodids in the region roost in vegetation or rocky outcrops (Medway 1983; Payne et al. 1985). In contrast, suitable sites for typically cave-dwelling or tree-hollow-roosting microchiropterans (Kunz and Lumsden 2003) would have been absent early in the recolonization of Krakatau as there were no mature trees and there is a lack of caves or lava tubes on the islands; the site known as “Panjang cave” (e.g., Tidemann et al.



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1990) has a recent origin from dynamite blasting by pumice collectors (LAS, pers. obs.). A dog-faced fruit bat, Cynopterus sphinx, was first recorded on the islands of Rakata and Sertung in 1919 (Dammerman 1922) and has been subsequently recorded on other islands in the Krakatau group (Tidemann et al. 1990). A congener, C. horsfieldii, was recorded on Rakata in 1920 and on Sertung in 1930, but was later considered to be locally extinct (Rawlinson et al. 1992; Schedvin et al. 1994; Thornton et al. 1988). Similarly, a long-tongued blossom bat, Mac­ roglossus sobrinus, was recorded from Rakata in 1979 (Hill 1983), but was not recorded again during zoological expeditions in 1984–1992 (Rawlinson et al. 1992; Schedvin et al. 1994). On Anak Krakatau in 1992, a smaller Macroglossus, M. minimus, was reported from skeletal remains in owl pellets, and a single specimen of Leschenault’s rousette, Rousettus leschenaultii, was caught hovering above bananas at the expedition’s camp (Schedvin et al. 1994). Geoffroy’s rousette, R. amplexicaudatus, was first recorded in a rocky outcrop on the west coast of Panjang in 1933, and this species has been caught on each of the four islands since (Rawlinson et al. 1992). A third Cynopterus, C. titthaecheilus, was first recorded on Rakata in 1984 and was subsequently caught on Sertung and Panjang (Tidemann et al. 1990). The lesser short-nosed fruit bat, C. brachyotis, has occasionally been reported as a fourth Cynopterus on Krakatau (e.g., Schedvin et al. 1994; Tidemann et al. 1990). In 1985 the Malay flying fox, Pteropus vampyrus, was first recorded in a large camp on Sertung, and the species has subsequently been recorded on different islands in the Krakatau group (e.g., Rawlinson et al. 1992; Tidemann et al. 1990; Whittaker and Jones 1994a). Given its high mobility, P. vampyrus undoubtedly visited Krakatau earlier (very likely much earlier) than this (Dammerman 1948). In 1986, in adjacent areas of West Java, Tidemann et al. (1990) caught three species of pteropodids (Eonycteris spelaea, Chironax melanocephalus, and Megaerops kusnotoi) that have not been recorded on Krakatau, indicating that the over-water distance may be limiting their colonization of Krakatau, although other explanations are possible.

The Role of Vertebrate Frugivores and Seed-Dispersal Processes in Reshaping Fragmented Forests The importance of fruit production in tropical forests and the role of vertebrate frugivores in the dynamics of forest regeneration are well established (e.g., Fleming and Estrada 1993; Levey et al. 2001; Terborgh 1986a, 1986b). The potential for plant colonization after internal seed transport by animals is primarily dependent on three factors: first, the time over which a seed may be retained in the gut of an animal before regurgitation or defecation; second, seed viability upon deposition; and third, the quality of the dispersal event in terms of where the seed is deposited (i.e., site or microsite suitability). In fragmented landscapes, seed carriage must be long enough for the island or isolated forest fragment to be reached. This is influenced by gut-passage time, the distance to

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be covered, and the flight speed of the animal, which may in turn be affected by the direction of the prevailing winds. The maximum gut-retention time for the seed will depend on both the animal species and the seed type (Barnea et al. 1990; Shilton et al. 1999). Seed viability can be altered by animal handling and/or ingestion (Aerts et al. 2006; Barnea et al. 1990; Fleming and Heithaus 1981; Shilton et al. 1999). Seed size or morphology influences whether seeds are passed internally or processed in the mouth or bill and then regurgitated (Wheelwright 1985; Boon and Corlett 1989). Typically, times to regurgitation are shorter than times to defecation (Proctor 1968; Eby 1996; Shilton et al. 1999). Consequently, seeddeposition patterns vary with fruit and/or seed size for many frugivorous birds (e.g., Izhaki et al. 1991; Moran et al. 2004; Wheelwright 1985) and pteropodid bats (e.g., Boon and Corlett 1989; Eby 1996; Izhaki et al. 1995). Widespread dispersal usually increases the probability that a seed will land in a suitable establishment site (Higgins et al. 2003; Portnoy and Willson 1993). Thus, seed germination and establishment probabilities vary between different animals (Howe 1989; Portnoy and Willson 1993; Schupp 1988) and between even closely related plant species (Barnea et al. 1990; Shilton 1999). Therefore, attempting to assess the effectiveness of an animal dispersal agent based on studies of related species, or the same species in a different region, is of limited efficacy. As highly volant frugivores, bats and birds create different patterns of seed deposition than nonvolant dispersers (e.g., Medellin and Gaona 1999; Reiter et al. 2006; Thomas et al. 1988). Furthermore, the tendency for bats to defecate across open spaces during flight as well as while roosting in trees is recognized (Boon and Corlett 1989; Fleming and Heithaus 1981; Gorchov et al. 1995; Medellin and Gaona 1999; Nyhagen et al. 2005; Payne et al. 1985; Reiter et al. 2006). In this way, bat-dispersed plants may achieve a more even distribution away from the parent plant than bird-dispersed plants (Medellin and Gaona 1999). Frugivorous birds usually defecate while perched, such that in addition to habitat structure, perch availability influences the deposition patterns of birddispersed seeds (Aerts et al. 2006; Fleming and Heithaus 1981; Gorchov et al. 1993; McClanahan and Wolfe 1993; Thomas et al. 1988).

Animal-Mediated Forest Reestablishment on Krakatau This work is the first to combine data on plant succession processes with quantitative data collected on seed dispersal by vertebrates on Krakatau. While the literature often refers to bird dispersal of plants to, and between, remote oceanic islands (e.g., Carlquist 1967; Proctor 1968), the role of pteropodid bats in such processes has been almost entirely neglected (see Shilton et al. 1999). Based on the available literature, Whittaker and Jones (1994a) argued that bats and birds have partially overlapping, yet complementary, roles as seed dispersers on Krakatau, and they suggested that pteropodid bats were more important for depositing seeds in open habitats. Subsequently, Shilton et al.



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(1999) demonstrated routine retention of food and viable seeds >12 hours, and up to 19 hours, in the gut of Cynopterus sphinx, and reported observations of this behavior in various wild pteropodids. We draw upon this discovery, and data collected on Krakatau from 1995 to 1997, in reevaluating the historical role of pteropodid bats in introducing plants to post-1883 Krakatau, and moving seeds between and within these islands. Here we address the following questions: (1) Which pteropodid bats have a presence on these islands? (2) What plant resources are available to frugivorous vertebrates on Krakatau? (3) What plants are pteropodid bats dispersing on these islands today? (4) Can pteropodid bats transport small-seeded plants between islands in the Krakatau group, and from mainland and stepping-stone islands? (5) Which plants could pteropodids have introduced to Krakatau? Throughout this chapter, the terms fruit and seed are used generically. Fruit refers to berries, drupes, arils, syconia (specifically figs, Ficus species), fleshy stems, and other soft tissue around the ovule. Seed refers to the ovule, including the seed coat and any hard, woody or fibrous structures immediately surrounding the ovule.

Methods Sampling the Pteropodid Bat Community Bat populations were sampled on Krakatau during each of 12 expeditions in July–October 1995, March–September 1996, and July 1997; all fieldwork reported here was conducted by LAS. Bats were captured using 9 m and 12 m double-ply braided nylon mist nets with 32-mm mesh (British Trust for Ornithology, BTO). Mist nets were tied on aluminum poles to intercept bats flying 1–4 m aboveground and were set in areas where there were potential food resources for pteropodids. Peak activity in foraging pteropodid bats usually occurs in the first four hours of the evening (e.g., Funakoshi and Zubaid 1997). Mist nets were opened 30 minutes before dusk (18:00) and were checked thereafter at 30-minute intervals through the evening until at least 21:30, or until bat activity ceased in the early hours of the following morning. Mist nets were set and kept open only in rain-free conditions. Due to logistical constraints, most bat sampling on Krakatau was conducted on Rakata and Panjang, although bats were sampled on the less accessible islands of Sertung and Anak Krakatau when possible (details provided in Shilton 1999). In July 1996 bats were additionally sampled on the nearest potential stepping-stone island, Sebesi, 12 km from the Krakatau group (fig. 7.1). Species; sex; age; reproductive status; length of the forearm, tibia, and ear; and body mass were recorded for each bat caught. Forearm and tibia lengths were measured to the nearest 1 mm using a BTO wing rule. Ear length was measured to the nearest 0.5 mm using calipers, and body mass to the nearest

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1 g using a Pesola 300-g spring balance. Notes were also made on pelage characteristics, and shape and size of the rostrum (LAS, unpublished data). Bat age was recorded as immature, subadult, or adult, and determined by examining the development of testes in males, nipples in females, fusion of the metacarpal epiphyses, overall size, and pelage features. Swelling around the phalangeal joints of wing bones, accompanied by paler and grayer pelage, indicated immature individuals. Reproductive status of adults was assessed on pelage color, since both males and female Cynopterus have a darker orange to rufous-brown collar in breeding condition (Payne et al. 1985), and on enlargement of the testes in males or enlarged nipples in females. Previously suckled nipples indicated parous females, and lactation was recorded if milk was secreted upon gentle squeezing of nipples. Unless pregnancy was clearly visible, the presence of a fetus was detected by gentle palpation of the abdominal area. Young attached to their mothers were recorded as nonvolant and are not counted as a bat capture in analyses. Bat species were identified primarily on the basis of forearm, tibia, and ear measurements, as well as characteristics of the rostrum, skull, and dentition (details provided in Shilton 1999). Cynopterus, Rousettus, and Macroglossus identification followed published species’ descriptions, and measurements (Corbet and Hill 1992; Hill 1983; Payne et al. 1985) and notes taken by LAS from discussions with two Chiroptera taxonomists: the late J. E. Hill (Natural History Museum, NHM) and A. Suyanto (Museum Zoologicum Bogoriense, MZB). In addition, Kitchener and Maharadatunkamsi 1991 and Medway 1983 were referenced for Cynopterus, and Bergmans and Rozendaal 1988 and Goodwin 1979 for Rousettus. C. horsfieldii was distinguished from congeners on the presence of cusps on the last lower premolar and first lower molar (Corbet and Hill 1992; Medway 1983; Payne et al. 1985). Even with genetic advances, the taxonomy of Cynopterus is complex due to the considerable overlap in forearm length, and other morphological measurements, reported in the literature (Bumrungsri and Racey 2005; Campbell et al. 2004; Corbet and Hill 1992; Medway 1983; Payne et al. 1985). Specimens of each pteropodid species were deposited at MZB, West Java, and NHM, London; collection numbers are provided in Shilton 1999. Specimen identifications were confirmed in collaboration with local Chiroptera specialists, Boeadi, I. Maryanto, and A. Suyanto (MZB), and through genetic analyses. Liver samples were collected from 26 individuals thought to represent four Cynopterus species, fixed in liquid nitrogen and sent to S. Hisheh (Western Australian Museum) and L. Schmitt (University of Western Australia) for allozyme analyses following Schmitt et al. 1995.

Identifying Fruit Feeders on Krakatau Trees with mature fruit crops were observed for frugivore feeding activity during 90-minute sessions on three consecutive mornings and evenings. Dur-



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ing each field trip, observation sessions were rotated so that each tree was monitored for frugivore activity commencing at 06:00, 08:00, 10:00, 18:00, 20:00, and 22:00. In this way, 9 hours of observation were conducted per fruit crop: 4.5 hours in the morning and 4.5 hours in the evening. Bird vocalizations were systematically recorded during morning observation sessions lasting from 06:00 to 11:00. Sighted birds were identified following MacKinnon and Phillips 1994, and vocalizations were known from White 1984 and discussion with S. van Balen (BirdLife International Indonesia).

Assessing Phenology Patterns on Krakatau To identify the most important plant species for vertebrate frugivores, fruit production was monitored by marking individuals within seven forest plots of 0.2 ha (200 m × 10 m) established on Krakatau in August 1995; five on Rakata (R1 to R5), the largest and most topographically and vegetatively diverse of the Krakatau islands (e.g. Whittaker et al. 1989), and two on Panjang (P1 and P2). Phenology plots were located to include dominant tree species within ecologically representative forest stands (see Whittaker et al. 1989). The phenology plots were situated in forest between 10 and 200 m a.s.1. On Rakata, plot R1 (30 m a.s.1.) was near-coastal, while plots R2 (110 m a.s.1.), R3 (50 m a.s.1.), and R4 (200 m a.s.1.) followed the natural course of gullies, and plot R5 (10 m a.s.1.) spanned a ridge in near-coastal forest. Panjang has fewer gullies and gentler gradients than Rakata (Whittaker et al. 1989); plots P1 (70 m a.s.1.) and P2 (140 m a.s.1.) were both situated on gentle slopes. Within each phenology plot, all individuals with a trunk diameter at breast height (DBH, measured at 1.3 m height) ≥5 cm were marked with numbered aluminum tags. As the size at which reproductive maturity is reached varies among plant species, location, and the conditions of the micro- and macrohabitat (Partomihardjo et al. 1992), individuals with a diameter ≥1 cm and 0.05), and only fig seeds (χ22 = 0.38, p > 0.05), did not differ among bat species. Four small-seeded plants were identified from bat feces collected on Sebesi: Ficus hispida, F. septica, F. variegata, and Pipturus argenteus. Seeds of each of these plants were dispersed by bats on Krakatau (table 7.5). As on Krakatau, F. septica (55% of seed records) was the most common plant species in bat feces on Sebesi, followed by F. hispida (10.7%), F. variegata (3.6%), and P. argenteus in a single fecal sample. Fig seeds of a second unidentified Ficus species were present in a single fecal sample. Two unidentified nonfig species were present in 41% (unidentified sp. 1, as on Krakatau) and 3.6% (unidentified sp. 3) of bat feces, respectively.

Bat Movement Patterns Radio-tracking was more successful for bats tagged on Panjang than on Rakata: this is almost certainly due to Panjang being one-sixth of the area of Rakata,

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Table 7.6.  Pteropodid recaptures on Krakatau, 1995–1997 Bat recapture

Cynopterus species

Bat sex

Banding date

Time (d) between banding and recapture

1 2 3 4 (4) 5 (5) 6 7 8 9 10a 11 12 13 14 15

C. sphinx C. titthaecheilus C. titthaecheilus C. titthaecheilus C. titthaecheilus C. sphinx C. sphinx C. titthaecheilus C. titthaecheilus C. sphinx C. titthaecheilus C. titthaecheilus C. titthaecheilus C. titthaecheilus C. titthaecheilus C. titthaecheilus C. titthaecheilus

F M M M M F F M F F F F F F F F F

23/10/95 28/03/96 10/08/95 22/09/95 22/09/95 28/03/96 28/03/96 5/04/96 23/10/95 24/04/96 28/03/96 22/09/95 22/07/96 23/10/95 23/10/95 22/09/95 25/05/96

161 4 239 196 220 37 57 48 215 58 88 355 51 333 330 364 122

Distance (m) between capture and recapture sites 100 100 180 100 100 100 100 0 0 0 80 6000 50 0 0 0 100

Note: Parentheses indicate second recapture. Details of capture and recapture sites are in Shilton 1999. a

An interisland movement between Rakata and Panjang.

lower in elevation, and lacking the deep gullies and ridges that impeded radiosignal transmission on Rakata. Six day-roosting radio-tagged C. sphinx (50% of tagged Cynopterus) were located between 25 m and 750 m from the site of their capture. Two tagged bats, one C. sphinx and one C. titthaecheilus, were located at feeding roosts 20 m from foraging sites, but daytime roosts were not located for these individuals. Another C. titthaecheilus was sighted foraging 300 m from its site of capture on Rakata. Two C. sphinx caught on Anak Krakatau were recorded roosting 50 m from their capture site; these two bats subsequently left Anak Krakatau and were not located during extensive subsequent daytime searches of the small forested areas of this island. A total of 432 bats were banded on Krakatau: 242 C. sphinx, 151 C. titthaechei­ lus, 9 C. horsfieldii, and 30 Rousettus amplexicaudatus. Fifteen banded Cynopterus bats were recaptured on the islands (table 7.6): three C. sphinx (1.2% of total banded) and 12 C. titthaecheilus (7.9%). No banded C. horsfieldii or R. amplexi­ caudatus were recaptured. The greater proportion of recaptured C. titthaecheilus most likely reflects more success in banding this larger species; it is conceivable that the smaller C. sphinx readily shed the thumb bands. Fourteen recaptured bats were caught within 200 m of their capture site; six of these were recaptured at the same site as first capture (table 7.6). Seven recaptures, all C. titthaecheilus, were made more than six months after original capture, and four recaptures approached one year after banding. Two bats, a female C. sphinx and a male C. titthaecheilus, were each recaptured twice. One



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female C. titthaecheilus banded on Rakata was recaptured almost a year later on Panjang, demonstrating an interisland movement of at least 6 km. Another banded C. titthaecheilus was observed day-roosting in a lava overhang on the west coast of Rakata in September 1996; the red band indicated its original capture 144–182 days earlier by a fruiting F. variegata at net site R6 in Neo­ nauclea/Ficus ­forest, about 400 m southwest of base camp on Rakata. This C. titthaecheilus had ranged at least 5 km since it was banded. Day-roosting radio-tagged bats were located on eight occasions, and averaged 199 m (±SD 248 m) from their capture sites. Individuals and groups of up to four day-roosting Cynopterus bats were inadvertently disturbed on four occasions, causing them to take flight from their tents of Corypha utan fronds. Bat-nibbled fronds of Corypha utan, the most common of the few palms on Krakatau (Whittaker et al. 1989), provided regular evidence of where Cynop­ terus had been resident. On two occasions on Rakata, one and six Cynopterus flew out of a Ficus ampelas tree hollow. The number of C. titthaecheilus day-roosting in rocky overhangs on the west coast of Panjang fluctuated from 6 in August to 20 in September 1995, to 38 in April, down to 11 in June, and up to a peak of 41 in September 1996. The increase in number of individuals reflected the presence of young bats in April and September. A second colony of 80 to 100 C. titthaecheilus, including immature bats and females with nonvolant young, was discovered on the west coast of Rakata in September 1996 in a lava overhang (10 m wide, 6 m high, 3 m deep). Opportunistic observations of medium-sized pteropodids flying over water between islands in the Krakatau group were made from a boat on each of four evenings; generally these commuting bats flew low, within 0.5 m of the water’s surface. At 18:30 hours on October 25, 1995, at least 30 bats were seen flying toward Rakata, as if from the west coast of Panjang; suggesting that these were C. titthaecheilus from the rocky Panjang day roost (reported above). Small numbers (one to five) of seeds from three Ficus species that are not present on the sparsely vegetated island Anak Krakatau were found in bat feces collected on this island. F. fistulosa, F. hispida, and F. variegata were not represented by mature trees on Anak Krakatau during this study (S. G. Compton, pers. comm.; LAS, pers. obs.), so their seeds in the feces of bats captured on this island must have been transported to Anak Krakatau from another island. The small number of “foreign” seeds in each of these bat feces may be due to the daytime retention of food in the gut (Shilton et al. 1999). Bat feces containing small seeds were recorded in all 50 40-m2 quadrats on Rakata, and 49 of the 50 40-m2 quadrats on Panjang (fig. 7.3). These results indicate a high level of seed scatter by pteropodid bats on Krakatau and are assumed to be a reasonable indicator of the level of bat activity. There was no consistent pattern in the distribution of bat feces in space and time; the mean number of bat feces per quadrat in the Rakata and Panjang transects varied widely over seven months (fig. 7.3). Whereas no quadrat on Panjang contained

L. A. Shilton and R. J. Whittaker

200 180

A. Rakata

Mean (+SD) bat faeces

160 140 120 100 80 60 40 20 0 1

5

9

13

17

21

25

29

33

37

41

45

49

Quadrat 35

B. Panjang

Mean (+SD) bat faeces

30 25 20 15 10 5 0 1

5

9

13

17

21

25

Quadrat

29

33

37

41

45

49

Figure 7.3.  Mean (+SD) number of bat feces counted per 40-m2 quadrat in each of seven months, September–October 1995 and March–July 1996, on (A) Rakata and (B) Panjang. Note different y-­axes­ ­scales.

more than 40 bat feces, a single 40-m2 quadrat on Rakata contained more than 400 bat feces in September 1995.

Discussion Krakatau Island Bats: Were Pteropodids Really Late Colonizers Relative to Birds? Records of the recolonization of Krakatau by bats are undoubtedly incomplete (Tidemann et al. 1990). Early naturalists who visited post-1883 Krakatau were



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primarily interested in plants and, to a lesser extent, terrestrial animals and birds. Although Jacobsen (1909) reported no bats on Krakatau during a brief daytime visit in 1908, so far as we can ascertain from the literature, bats were not actively looked for during other early daytime visits. Given the relative ease in surveying diurnal birds, the documentation of bird arrival on Krakatau is certainly more complete than for bats. Our data indicate that five pteropodid species of three genera currently have breeding populations on Krakatau: Cynopterus sphinx, C. titthaecheilus, C. hors­ fieldii, Rousettus amplexicaudatus, and Macroglossus sobrinus. Taxonomic revision using molecular techniques is needed to clarify the species within Cynopterus, in particular the presence or absence of C. brachyotis where C. sphinx is resident (Bumrungsri and Racey 2005). Although R. leschenaultii was not caught on Krakatau during our work, captures on Sebesi (see above) and a single record on Anak Krakatau (Schedvin et al. 1994) indicate that this fast flier (Shilton 1999) also visits Krakatau. We know that Cynopterus bats reached Krakatau before 1919, as Dammerman (1922) regarded C. sphinx as resident on both Rakata and Sertung islands at this time. However, this first confirmation of pteropodid bats on Krakatau came 36 years after the 1883 devastation, 23 years after the first Ficus plants were recorded in 1896 (Penzig 1902), and 11 years after frugivorous birds arrived on Krakatau (e.g., Dammerman 1922; Docters van Leeuwen 1936). As has been shown elsewhere, pteropodids are good colonizers across ocean stretches that present a barrier to less-volant mammals (e.g., Heaney 1986). Many pteropodids undertake seasonal migrations and exhibit nomadic behavior (e.g., Eby 1996; Thomas 1983). In particular, Pteropus species (flying foxes) are highly mobile (e.g., Tidemann and Nelson 2004). We are unaware of large-scale movement data for the smaller pteropodid species, and while the wing morphology of Cynopterus is considered ill-suited to long-distance flight (Hodgkison et al. 2004; Campbell et al. 2004), Krakatau provides evidence for the ability of Cynopterus, Rousettus, and Macroglossus species to cross ocean barriers of at least 12 km, and possibly 40 km (see fig. 7.1). Pteropus vampyrus often visit the archipelago and sometimes form temporary camps on one of the islands (Tidemann et al. 1990; Rawlinson et al. 1992; LAS and RJW, pers. obs.). Given that flying foxes will commute distances of up to 50 km during nightly foraging at speeds of about 40 km/h (11 m/s; L. A. Shilton, D. A. Westcott, and P. J. Latch, unpublished data), and given the mobility and nomadic behavior of P. vampyrus (Dammerman 1948), it is likely that this species visited post-1883 Krakatau long before it, and even before Cynopterus sphinx, was noted as present during research expeditions (see also Tidemann et al. 1990). In contrast to Whittaker and Jones (1994a), who suggested that most of the Krakatau Ficus species are probably spread intestinally by both bats and birds, data presented here strongly suggest a bat mode of introduction for at least the following early tree colonists: F. fistulosa, F. hispida, F. padana, and

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F. septica. The combination of our direct observations of bird and bat fruit feeding on Krakatau, bat fecal analyses, and plant phenological data thus enable us to strongly infer, for the first time, that pteropodid bats at least visited the barren islands of Krakatau prior to 1896. First, while the first four recorded fig species, F. fulva, F. hispida, F. padana, and F. septica, have been considered probable “bat-figs” by earlier authors (e.g., Docters van Leeuwen, 1936; Thornton et al. 1996), our data suggest that on Krakatau today pteropodids are solely responsible for the dispersal of F. fistulosa (a species not recorded in 1897 but already widespread throughout the interior of Rakata by 1905), F. hispida, and F. septica, and are predominantly responsible for the dispersal of F. fulva. No data were obtained for F. padana, a species that we consider to be extinct on the islands today. Thus, there is strong support for the proposition that the first wave of fig colonization was brought about by pteropodid bats within about ten years of the 1883 devastation. Moreover, bats were clearly responsible for spreading fig seeds widely across the interior by 1905.

What Food Resources Are Available to Pteropodid Bats Today? Our phenology data indicate aseasonal, year-round fruiting of the six main bat-figs that have established on Krakatau: Ficus fistulosa, F. fulva (also eaten by birds), F. hispida, F. ribes, F. septica, and F. variegata. With the exception of F. pubinervis and F. subcordata (which is rare on Krakatau; RJW data), each of the 23 Ficus species (Thornton et al. 1996) that has been recorded on Krakatau produces figs aseasonally on Java: F. subcordata “flowers” in December, and F. pubinervis between August and February (Backer and Bakhuizen van den Brink 1963–1968). Asychronous fruiting in Ficus species is common due to their obligate pollination mutualism with single species of fig wasps (e.g., Backer and Bakhuizen van den Brink 1963–1968; Kalko et al. 1996; Lambert and Marshall 1991; Shanahan et al. 2001). Given the risks associated with crossing the Sunda Strait in small boats in the “wet season” months, our monthly phenological records, collected in July– October­ 1995, March–September 1996, and July 1997, are incomplete. However, these data do not indicate a pronounced period of general fruit scarcity in nonfig zoochorous flora (cf. Terborgh 1986b). On Krakatau, an array of nonfig fruits, such as Terminalia catappa, Timonius compressicaulis, and Morinda citrifolia, are also available for pteropodid bats during the dry-season months (table 7.3). On Krakatau, reproductive maturity was reached at 12 hours (Shilton et al. 1999) provides a mechanism for transporting small seeds distances greatly exceeding the 40 km separating Krakatau from mainland, a feat that was not previously considered feasible for pteropodids (e.g., Dammerman 1948; Ernst 1908; Richards 1990). A range of wild pteropodids exhibit the behavior of carrying gut-retained food and seeds to their subsequent night foraging sites and daytime roost sites: Rousettus amplexicaudatus, Cynopterus sphinx, and C. titthaecheilus on Krakatau (Shilton et al. 1999) and flying foxes Pteropus conspicillatus (LAS, pers. obs.) and P. poliocephalus (LAS, pers. obs.) in Australia. Small seeds (e.g., 150 different trees in the breeding season. Interestingly, these bats exhibited strong temporal synchrony in the reuse of the same roosts from year to year; date of reuse was similar each year with 13% of roosts reused within 0–3 days of the date of first use, 37% reused within 9 days, and 62% within 20 days (O’Donnell and Sedgeley 2006).

Social Structure Bats of both species and in all study areas investigated to date form summer colonies dominated by reproductive females and their young. Both species form highly structured subpopulations (Lloyd 2003a, 2003b; O’Donnell 2000b). The social structure of long-tailed bat colonies has been investigated in detail in the Eglinton Valley in the Fiordland region where nonrandom associations of individuals and three subpopulations studied averaged 72–132 bats each. The bats roosted in adjacent, nonoverlapping areas of forest. However, the subpopulations were cryptic because their foraging ranges overlapped almost completely, and bats belonging to each group were spread over many roosts each day. There was virtually no mixing of individuals from different colonies within roost cavities, and young bats returned to their natal groups to breed (O’Donnell 2000b). Colonies exhibited a “fission-fusion” structure. That is, not all members of a colony occupied the same roost on a particular night. Subgroups averaged 34 bats, and subcomponents of each colony would associate

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and mix as they switched roosts each night. Given that long-tailed bats appear to require relatively small cavities that offer significant thermal benefits to their young, constant mixing would ensure that social contacts were maintained and that knowing potential roost mates would maximize the chances of bats forming clusters each day. Such structure has been found in other temperate Microchiroptera (e.g., Myotis bechsteinii, Plecotus auritus; Entwistle et al. 1997; Kerth and König 1999; Park et al. 1998). Lesser short-tailed bats on Codfish Island and in the Eglinton Valley selected cavities that were larger than both random cavities and those used by sympatric long-tailed bats (Sedgeley 2003, 2006). The size of lesser short-tailed bat roosting groups can be considerably larger than those of long-tailed bats, ranging up to nearly 1,500 bats on Codfish Island, and up to 1,200 in the Eglinton Valley. Elsewhere in New Zealand much larger group sizes have been recorded (e.g., >6,000 bats; Lloyd 2005). Consequently, lesser short-tailed bats often select large cavities to accommodate large numbers of bats. Another difference between the two species is that colonies of lesser short-tailed bats contain a significant proportion of adult males (up to 35%), whereas long-tailed colonies include