- Email: [email protected]
Patterns of ecomorphological variation in the bats of western Madagascar: Comparisons among and between communities along a latitudinal gradient
ARTICLE IN PRESS
www.elsevier.de/mambio
Original investigation
Patterns of ecomorphological variation in the bats of western Madagascar: Comparisons among and between communities along a latitudinal gradient By Julie Ranivo and S.M. Goodman De´partement de Biologie Animale, Universite´ d’Antananarivo and WWF, Antananarivo, Madagascar, Field Museum of Natural History, Chicago, USA and WWF, Antananarivo, Madagascar Receipt of Ms. 24.11.2005 Acceptance of Ms. 17.8.2006
Abstract The ecomorphology of 10 insectivorous bat species at three study zones in western Madagascar was examined using 567 specimens and based on 6 external, 11 cranial, 12 dental, and 11 wing measurements. The three study sites are located along a cline representing 11.61 of latitude. The southern most site has notable differences in vegetational and climatic regimes than the two more northern sites. Principal component analyses were conducted for each of the four datasets to examine the morphological space occupied by each species at the three sites. Most taxa showed clear intra-site separation and little inter-site variation. The exceptions included extensive morphological overlap in two taxa of Triaenops (cranial, dental, and wing), that have allopatric distributions, and between the sympatric Miniopterus manavi and Myotis goudoti (external, cranial, and dental). In the latter case, there was distinct separation in wing shape between these two taxa, which would allow them to exploit local habitats and prey in different manners. The only species that showed considerable inter-site variation was Hipposideros commersoni, which is sexually dimorphic, with individuals from the south being smaller than those in the north. r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Key words: Chiroptera, ecomorphology, community, latitudinal gradient, Madagascar
Introduction Studies in the field of ecomorphology examine the interface between the morphology and behavioral ecology of organisms, specifically attempting to explain how differences in physical attributes allow the coexistence of similarly shaped animals in light of potential inter-specific competition. This research approach, which has been used for nearly 50 years, starting with the work of Brown and Wilson (1956), and in more
recent years has been applied to a variety of groups (e.g. Leisler and Winkler 1985; Saunders and Barclay 1992; Bradley 1994; Garland and Losos 1994; Reilly 1994), provides insight into the relationships and mechanisms between the physical form of the individual components of a community of organisms, aspects of their behavior, and how they physically exploit their environment.
1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2006.08.004 Mamm. biol. 72 (2007) 1 1–13
ARTICLE IN PRESS 2
J. Ranivo, S.M. Goodman
Morphology dictates an individual’s performance limits and restricts its behavioral repertoires; for example, regardless of habitat, a bat cannot fly faster or eat larger prey than its anatomy will allow (Swartz et al. 2003). Thus, ecomorphological studies provide a proxy to examine resource partitioning at the community level, which otherwise would be difficult to measure. An excellent example is the shape of bats’ wings, which provide the locomotory means for various foraging styles and the exploitation of different types of aerial arthropods (Norberg 1981). A number of studies have examined through ecomorphological inference resource partition in bat communities (e.g. Findley and Black 1982; Saunders and Barclay 1992; Findley 1993; Kalko 1998; Aguirre et al. 2002; Van Cakenberghe et al. 2002). In the current study, we investigate four different morphological datasets obtained from bat specimens collected in the western portion of Madagascar, to examine, at a site level, the partition of inter-specific ecomorphological space. The different datasets include: external morphology – coupled with general size and associated with foraging design and locomotory capacity (Norberg 1994; Van Cakenberghe et al. 2002); cranial structure – presumed to be correlated with both feeding types and sonar capacity (Freeman 1979, 1984; Van Cakenberghe et al. 2002); dental morphology and size – linked to food types and processing (Swartz et al. 2003); and wing structure – related to the type of flight, the manner, and habitat type bats forage in (Norberg 1994). The different study sites represent latitudinal shifts from dry deciduous forests in the north to spiny bush in the south, and between the sites, there are some shifts in bat species composition and presumably in food resources with respect to arthropod density and taxonomic representation. Given this variation, we are able to examine, at several different scales, potential shifts in the ecomorphology of the insectivorous bat communities.
Material and methods Species and study sites Ten species of bats where used in this study, that represent the majority of those known from each of the study sites (Goodman et al. 2005). At least in
western Madagascar, these species generally use caves for their day roosts. The species include (n=sample size of each taxon): Emballonura nov. sp. (n=11) (Emballonuridae); Hipposideros commersoni (n=34), Triaenops auritus (n=40), T. furculus (n=53), and T. rufus (n=64) (Hipposideridae); Myotis goudoti (n=99), Miniopterus gleni (n=32), and Miniopterus manavi (n=194) (Vespertilionidae); and Mormopterus jugularis (n=8) and Otomops madagascariensis (n=32) (Molossidae). All of these animals forage on arthropods and are endemic to the Malagasy region based on recent taxonomic assessments (Simmons 2005; Goodman et al. 2006; Ranivo and Goodman 2006). Five different sites were censused for this study, spanning much of the latitudinal breadth of western Madagascar. In two cases, nearby sites were combined to maximize sample sizes; the sites used in the analyses are from north to south Ankarana, Namoroka/Bemaraha, and Sarodrano/Tsimanampetsotsa (Fig. 1). Hipposideros commersoni, T. rufus, Myotis goudoti, Miniopterus gleni, M. manavi, and O. madagascariensis occur at all three study sites, while Emballonura nov. sp. and Mormopterus jugularis are restricted in our dataset to specimens from Ankarana. Two of the Triaenops spp. show non-overlapping distributions, with T. auritus occurring at Ankarana and T. furculus at Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa. Ankarana is a zone of limestone karst containing an extensive cave system and with dry deciduous forest habitat within canyons (Cardiff and Befourouack 2003). The nearest weather station is at Ambilobe that has an annual mean temperature of 26.7 1C, on average 1890 mm of annual rain, and a dry season of approximately 6 months (Nicoll and Langrand 1989). The next study area to the south is the combined sites of Namoroka/Bemaraha, which are also limestone karst zones with a notable number of caves and forested areas within canyons (Rasoloarison and Paquier 2003). The weather station falling between these two sites is at Besalampy, which has an annual mean temperature around 26 1C, on average 1420 mm of annual rain, and a dry season of approximately 7 months (Donque 1975; Chaperon et al. 1993). The southern most study area, composed of the Sarodrano/Tsimanampetsotsa sites, holds zones of subarid thorn scrub or spiny bush (Goodman et al. 2002). Most of the bat netting conducted at these latter two sites was associated with bat day roosts in caves. The nearest weather station is at Toliara, which has an annual mean temperature of 24.2 1C, on average of 390 mm of annual rain, and a dry season of approximately 8 months (Donque 1975; Chaperon et al. 1993).
ARTICLE IN PRESS Ecomorphological variation in bats
3
Fig. 1. Map of Madagascar showing the different study sites, which represent a significant proportion of the complete latitudinal breadth of the island. Locality names of other sites mentioned in the text are also noted.
Specimens Skulls of collected animals were removed before the cadavers were conserved in 12.5% formalin, and consequently cleaned with the use of dermestid beetles. The formalin preserved specimens were consequently washed in running water for about 24 h and then transferred to 75% ethanol. The voucher specimens are held in the collections of the Field Museum of Natural History (Chicago) and the De´partement de Biologie Animale, Universite´ d’Antananarivo (Antananarivo).
Measurements External measurements were made, largely by SMG, using a millimeter ruler accurate to the
nearest 0.5 mm from collected specimens before their preparation. These included: total length (TL), tail length (TAIL), hind foot length (HF) (not including claw), ear length (EAR), and forearm length (FA). Further, we measured body mass (WT) in grams using a spring balance accurate to the nearest 0.1 g. Cranial and dental measurements were obtained by JR using a dial calipers precise to the nearest 0.1 mm and included: cranial — greatest skull length (GKSL), condyle-basal length (CBL), greatest zygomatic breadth (ZYGO), braincase height (BCH), minimum interorbital width (IOW), greatest mastoid breadth (MAST), rostrum length (ROST), palate length (PAL), mandible length (MAND), coronoid-condyle length (CORCON),
ARTICLE IN PRESS 4
J. Ranivo, S.M. Goodman
and condyle-angular process length (CONAN); and dental — length between I1 and M3 (I1 M3), length of upper molar toothrow (MOL), distance across upper canines (C1 C1), distance across upper posterior molars (M3 M3), width of last upper premolar (M3W), length of upper canine (C1L), length between i1 and m3 (i1 m3), length of lower molar toothrow (moli), distance across molar-condyle (molcon), width of last lower premolar (m3w), length of lower canine (c1l), and mandible width at level of m2 (mw2). Wing measurements were made, by JR, using a millimeter ruler accurate to the nearest 0.5 mm from collected specimens before their preparation: length of 1st digit-metacarpal (L1DM), length of 2nd digitmetacarpal (L2DM), length of 3rd digit-metacarpal (L3DM), length of 3rd digit –1st phalanx (L3D1P), length of 3rd digit –2nd phalanx (L3D2P), length of 4th digit-metacarpal (L4DM), length of 4th digit –1st phalanx (L4D1P), length of 4th digit –2nd phalanx (L4D2P), length of 5th digit-metacarpal (L5DM), length of 5th digit –1st phalanx (L5D1P), and length of 5th digit –2nd phalanx (L5D2P). For further precision and definitions for these variables, see Ranivo and Goodman (2006). The age classification of these animals was based on the eruption of teeth, the ossification of the basiosphenoid suture, and the development of the sagittal crest. Only adults, based on these three characters, were used in this study.
Statistical tests We used the program STATISTICA version 5.1 to conduct the various statistical comparisons. For the principal component (PC) analyses, the four different variable types (external, cranial, dental, and wing) were treated separately. These analyses were based on non-log-transformed data and correlation matrices. A series of ANOVA tests were conducted on the first and second PC scores for all species at the three sites. When these tests showed statistical significance (alpha=0.05), Scheffe´ tests were used to examine the internal interactions between sites. The detailed matrices of the Scheffe´ tests are not presented here, but rather only probability values when they were statistically significant. Finally, measurements were made of the inter-species mean distances as calculated by the PC analyses.
Results and discussion External measurements The results of the PC analysis for the external measurements (Fig. 2A), which include all
species from the three study sites, show that five of the six measurements are strongly correlated with the first axis, explaining 69.5% of the variance, and only the TAIL shows important loading for the second axis, adding an additional 21.6% to the total explained variance (Tab. 1). There is a clear separation of the different species based on their size (Fig. 2A). The two largest species, H. commersoni and O. madagascariensis, are notably separated from the other taxa. Five groupings can be distinguished based on the second axis. The ANOVA conducted on the first axis is significant across species at a level of Po0.0001. Scheffe´ tests indicate that the two largest species are significantly different than the others used in this analysis (Pp0,01). Hipposideros commersoni shows a shift in occupied morphological space between the sites of Ankarana and Namoroka/Bemaraha (Pp0,001), while O. madagascariensis does not show inter-locality differences. Amongst the additional five groups, two show species overlap in morphological space: T. rufus–Mormopterus jugularis and Myotis goudoti Miniopterus manavi. The first axis of the PC analysis for Myotis from Namoroka/Bemaraha is significantly different from that of Miniopterus manavi from Ankarana (P=0.01) and Namoroka/Bemaraha (Pp0.001); these two species do not show any inter-locality difference. Miniopterus manavi shows no inter-locality difference, but occupies a different morphological space from the other species based on its separation along the second axis. Emballonura nov. sp. is also notably distinct from the other species based on external characters. T. furculus and T. auritus overlie one another in their interlocality positions based on the first axis. Cranial measurements The results of the PC analysis for the cranial variables for all species from the three sites (Fig. 2B) shows virtually all of the variables are strongly correlated with the first axis, which explains 82.0% of the variation, with the exception of PAL and IOW, which show heavy loadings on the second axis, accounting for another 12.9% of the variation (Tab. 2).
ARTICLE IN PRESS Ecomorphological variation in bats
3.5 2.5
1.5
1.5
0.5 –0.5
0.5 –0.5
–1.5
–1.5
–2.5
–2.5
(A)
CP 2
CP 2
2.5
1.5 2.5 CP 1
3.5
4.5
–3.5 –1.5 – 0.5 0.5
5.5
(B)
3.5
3.5
2.5
2.5
1.5
1.5
0.5
0.5
CP 2
CP 2
3.5
–3.5 –1.5 –0.5 0.5
–0.5
–1.5
–2.5
–2.5
(C) Emballonura nov. sp. Hipposideros Ank Hipposideros N/B Hipposideros S/T
1.5 2.5 CP 1
3.5
4.5
–3.5 –1.5 – 0.5 0.5
5.5
M.gleni Ank M.gleni N/B M.gleni S/T M.manavi Ank
1.5 2.5 CP 1
3.5
4.5
5.5
1.5 2.5 CP 1
3.5
4.5
5.5
–0.5
–1.5
–3.5 –1.5 –0.5 0.5
5
(D) M.manavi N/B M.manavi S/T Mormopterus Myotis Ank
Myotis N/B Myotis S/T Otomops Ank Otomops N/B
Otomops S/T T.auritus T.furculus N/B T.furculus S/T
T.rufus Ank T.rufus N/B T.rufus S/T
Fig. 2. Scatter diagram of axis 1 and axis 2 in PC analyses of different morphological variables for 10 different bat species: (A) external measurements (see Tab. 1 for associated loadings); (B) cranial measurements (see Tab. 2 for associated loadings); (C) dental measurements (see Tab. 3 for associated loadings); and (D) wing measurements (see Tab. 4 for associated loadings). Key to locality names: Ank=Ankarana, N/B=Namoroka/ Bemaraha, S/T=Sarodrano/Tsimanampetsotsa.
The positions of the different species in scatter projections of PC axis 1 and axis 2 show direct parallels between the external (Fig. 2A) and cranial (Fig. 2B) variables. The ANOVA based on the first axis is significant across species (Po0.0001). The internal Scheffe´ tests comparisons indicate that H. commersoni is notably separated from all of the other species (Pp0.001) and there is a difference in the occupation of morphological space between the individuals of this species from Namoroka/Bemaraha and those from Sarodrano/ Tsimanampetsotsa (Pp0.001). Based on the
first two axes, Miniopterus manavi of Ankarana occupy a similar morphological space as Myotis goudoti at the same locality. No interlocality difference was found for Otomops, Miniopterus gleni, M. manavi, Myotis, and the three Triaenops spp. Dental measurements The results of the PC analysis for the dental variables (Fig. 2C), for all species from the three sites, indicate that nine of the 12 variables are strongly correlated with the first
ARTICLE IN PRESS 6
J. Ranivo, S.M. Goodman
Table 1. Correlations between external measurement variables and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variance Eigenvalues TL TAIL HF EAR FA WT
Axis 1
Axis 2
69.5 4.17 0.74 0.05 0.95 0.87 0.98 0.93
91.1 1.29 0.64 0.99 0.07 0.01 0.01 0.15
Table 2. Correlations between cranial measurement variables and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variation Eigenvalues GSKL CBL ZYGO BCH IOW MAST ROST PAL MAND CORCON CONAN
Axis 1
Axis 2
82.0 9.01 0.98 0.95 0.94 0.81 0.08 0.96 0.93 0.41 0.97 0.99 0.89
94.8 1.42 0.16 0.28 0.25 0.33 0.98 0.24 0.33 0.87 0.23 0.03 0.38
axis, accounting for 90.5% of the explained variation, and I1 M3, MOL, and M3W show heavy loadings on the second axis, adding an additional 4.6% of the explained variation (Tab. 3). Compared to the external (Fig. 2A) and cranial (Fig. 2B) variables, dental variables (Fig. 2C) reveal a notable reduction of the inter-species distances. In the case of the dental variables, two groups can be readily distinguished based on the first two axes of the PC analysis: H. commersoni and O. madagascariensis. The remaining taxa (Mormopterus jugularis, Triaenops spp., Miniopterus spp., Myotis goudoti, and Emballonura
Table 3. Correlations between dental measurements and the PC analysis.
% cumulative variation Eigenvalues I1 M 3 MOL C1 C1 M3 M3 M3W C1L i1-m3 moli molcon m3 w c1l mw2
Axis 1
Axis 2
90.5 10.86 0.51 0.66 0.81 0.72 0.33 0.89 0.70 0.73 0.74 0.84 0.88 0.79
95.1 0.55 0.84 0.73 0.53 0.68 0.91 0.40 0.70 0.66 0.64 0.47 0.43 0.49
nov. sp.) form several clouds of points that are not well differentiated. The ANOVA of the first axis across species is statistically significant (Po0.0001). The Scheffe´ tests indicate that Hipposideros from Ankarana and Sarodrano/Tsimanampetsotsa (P=0.01), as well as Namoroka/Bemaraha and Sarodrano/Tsimanampetsotsa (Pp0.001) are different from one another. The three Triaenops spp. show no difference at any given locality, with the exception of T. auritus and T. rufus at Namoroka/Bemaraha (Pp0.001). Otomops, Miniopterus gleni, M. manavi, and Myotis show no inter-locality difference. Based on the first axis of the PC analysis, Emballonura and M. manavi demonstrate considerable overlap in morphological space. On the basis of this same axis, Emballonura is significantly different from Myotis (Pp0.02) and the three Triaenops spp. (Pp0.001). Further, M. manavi is significantly different from Myotis at all localities (Pp0.001) with the exception of Ankarana and Sarodrano/ Tsimanampetsotsa and the three Triaenops spp. (Pp0.001) at all localities. Wing measurements The results of the PC analysis for the different wing measurements (Fig. 2D), for all species from the three sites, indicate that nine of these 11 variables are strongly
ARTICLE IN PRESS Ecomorphological variation in bats
correlated with the first axis of the analysis, explaining 71.7% of the variation, and the remaining two variables, L3D2P and L4D2P, show heavy loadings for the second axis, accounting for an additional 19.6% of the variation (Tab. 4). This analysis shows an arrangement in morphological space somewhat different from the previous three analyses. Five different groups can be readily distinguished (four are mono-specific and the fifth is a composite of several genera and species): H. commersoni, O. madagascariensis, Miniopterus manavi, M. gleni, and then a conglomerate of Myotis goudoti, Mormopterus jugularis, Emballonura nov. sp., and the three Triaenops spp. The ANOVA analyses conducted on the first axis are significant across species (Po0.0001). The internal Scheffe´ tests indicate that Hipposideros from Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa occupy different positions in ecomorphological space (P=0.01). Miniopterus manavi, M. gleni, Myotis, T. rufus, T. furculus, and Otomops show no inter-locality difference based on the first axis of the PC analysis. Myotis goudoti shows broad overlap with Mormopterus jugularis. All three Triaenops spp. coincide in morphological space, with the exception of T. rufus from Namoroka/ Bemaraha and Ankarana are different from T. furculus at Sarodrano/Tsimanampetsotsa
Table 4. Correlations between wing measurements and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variation Eigenvalues L1DM L2DM L3DM L3D1P L3D2P L4DM L4D1P L4D2P L5DM L5D1P L5D2P
Axis 1
Axis 2
71.7 7.89 0.93 0.96 0.92 0.98 0.23 0.93 0.99 0.07 0.77 0.94 0.86
91.3 2.15 0.21 0.19 0.25 0.02 0.96 0.29 0.02 0.99 0.39 0.20 0.16
7
based on the first axis (Pp0.01), and T. rufus from Sarodrano/Tsimanampetsotsa are different from T. furculus at Namoroka/Bemaraha based on the first axis (P=0.005). Amongst the four types of morphological variables used in this study, there are notable differences, based on the PC analyses, in separating or grouping morphological dissimilar or similar species. Based on external morphology (Fig. 2A), the first axis is clearly correlated with size, while tail length is the only variable strongly correlated with the second axis. Two different groupings show overlapping species. The first of these, T. furculus–T. auritus, geographically replace one another between our study sites. The second grouping, Miniopterus manavi–Myotis goudoti, shows broad overlap in the external and cranial measurements, some separation in the dental measurements, and clear distinction in the wing measurements. Hence, while there are similarities in certain aspects of the morphology of these two species, based on wing shape, they are presumed to have different foraging methods or techniques, as has been found for bats elsewhere in the world (Findley and Black 1982; Saunders and Barclay 1992). Freeman (1998) noted that insectivorous bats can be divided in two separate groups, those that consume hard body prey and soft body prey. The former is distinguished from the latter by having more robust mandibles and crania, and longer canines. Bases on the results presented here, specifically aspects of cranial and dental morphology, we can advance that M. manavi probably consumes softer bodied prey than Myotis. More research is needed to see if there are also differences in the types of arthropods these two bat species are feeding on. If indeed they forage on largely the same prey, then it would be presumed they do so in different ecological situations. Another example, with two morphologically similar species from different families, is that of T. rufus and Mormopterus jugularis, which show considerable overlap in the first two axes of the PC analysis of external characters, but in the other character sets are distinctly separated in the second axis. Further, there is a notable separation in these two species
ARTICLE IN PRESS 8
J. Ranivo, S.M. Goodman
based on their forearm length and body mass (Fig. 3). Cranial differences between the study species at the different sites (Fig. 2B) are notably different amongst all of the taxa, with the exception of Triaenops spp. and the Miniopterus manavi–Myotis goudoti group. However, based on dental structure, T. rufus shows clear separation from T. furculus and T. auritus. Within the different data sets, the greatest inter-specific spread is found within H. commersoni (Tabs. 5, 6; Fig. 3). This taxon is the only one amongst the study species that shows notable levels of sexual dimorphism. At an intra-generic level, the two most morphologically similar species are T. auritus and T. furculus and then these two species in comparison to the broadly distributed T. rufus are only subtly different (Tabs. 5, 6). The other possible inter-generic comparison is with Miniopterus, for which notable differences occur between Miniopterus gleni and M. manavi, the former is sympatric across its range with the latter (Tabs. 5, 6). The results of these analyses show few interlocality differences within each of the species examined and there would appear to be no marked latitudinal variation in the measurements of four different types of morphological variables of these different bats. In most cases, when found, it is likely that occasional and seemingly random significant inter-lo-
110.0 forearm length / mm
100.0 90.0 80.0 70.0 60.0 50.0 40.0 30.0 -0.02 0.00 0.02 0.04 0.06 0.08 0.10 0.12 body mass / kg
Fig. 3. Relationship between body mass and forearm length in the ten study species (Y=890.35 X+36.22; R2=0.801 Pp0.0001). See caption to Figure 2 for explanation of symbols.
cality differences are spurious and probably related to type II errors. The major exception is with H. commersoni, in which animals from the south are smaller than those in the north; although a portion of these differences might be associated with small samples sizes at the Sarodrano/Tsimanampetsotsa site. This supports the conclusion of another analysis where this species was found to show decreasing size with increasing latitude (Ranivo and Goodman unpublished data). Along the latitudinal gradient of our study sites in western Madagascar, a few species drop out at the more southern sites. Amongst the ten species used in this analysis, nine occur at Ankarana and seven at Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa – Emballonura nov. sp. and Mormopterus jugularis are not represented in the specimens from the two southern sites. In the four different datasets Emballonura is generally well separated from the other species in morphological space, while Mormopterus shows considerable overlap with T. rufus in external measurements, some overlap with Miniopterus gleni in dental characteristics, and with Myotis goudoti in wing shape. Based on our PC analyses, there is not a notable shift in the morphological space occupied by similar species in the presence or absence of Emballonura nov. sp. and Mormopterus jugularis. The explanation for this lack of increase in variation in a morphologically similar species in the absence of these taxa might be related to several different factors: (1) for any given species there is regular dispersal and subsequent genetic exchange between populations occurring at our three study sites, hence reducing the means for microgeographic differentiation, (2) food is not a limiting factor and competition for available resources has not been an important recent factor in the evolution of morphological characters, (3) most of these species are generalists in the prey they hunt, (4) they may forage in different areas, and (5) they may occur at the southern sites but were undetected during our surveys. Knowledge on the dispersal, natural history, and distribution of Malagasy bats is still at a relatively rudimentary stage, but these five points can be addressed at certain levels.
ARTICLE IN PRESS Ecomorphological variation in bats
9
Table 5. Distance measurements for each of 10 bat species between the mid-position of point scatters for axes 1 and 2 of PC analyses. Values for external measurements characters are presented in the lower left portion of the matrix and cranial measurements in the upper right portion. Abbreviations for species names include: Emballonura nov. sp.=Em, Hipposideros commersoni=Hip, Miniopterus gleni=Mglen, M. manavi=Mman, Mormopterus jugularis=Mjug, Myotis goudoti=Mgoud, Otomops madagascariensis=Otom, Triaenops furculus=Tfurc, T. rufus=Truf, and T. auritus=Taur. Em Em Hip Mglen Mman Mjug Mgoud Otom Tfurc Truf Taur
4.17 3.48 2.04 1.52 2.17 3.26 0.74 1.43 0.83
Hip
Mglen
Mman
Mjug
Mgoud
Otom
Tfurc
Truf
Taur
3.83
1.96 3.48
0.87 3.83 1.17
1.48 3.04 0.70 0.91
1.04 3.48 0.91 0.35 0.57
3.39 2.65 1.74 2.78 1.96 2.43
1.00 2.96 2.26 1.52 1.57 1.48 3.22
0.87 3.00 2.04 1.35 1.35 1.26 3.04 0.22
1.04 2.87 2.22 1.57 1.52 1.48 3.13 0.09 0.22
3.52 3.83 3.35 3.65 1.61 3.48 3.17 3.35
1.57 2.00 1.39 1.96 2.96 2.13 2.96
0.78 0.22 2.39 1.65 1.00 1.70
0.78 2.04 0.96 0.22 0.96
2.17 1.74 1.00 1.74
2.52 1.96 2.43
0.83 0.13
0.83
Table 6. Distance measurements for each of 10 bat species between the mid-position of point scatters for axes 1 and 2 of PC analyses. Values for dental measurements characters are presented in the lower left portion of the matrix and wing measurements in the upper right portion. See table 5 for definitions of abbreviations. Em Em Hip Mglen Mman Mjug Mgoud Otom Tfurc Truf Taur
4.13 2.30 0.74 1.78 1.35 3.13 0.87 1.00 0.83
Hip
Mglen
Mman
Mjug
Mgoud
Otom
Tfurc
Truf
Taur
3.96
2.09 3.17
1.35 4.09 1.17
0.35 3.65 1.78 1.22
0.43 3.65 1.65 1.09 0.17
2.13 1.83 2.04 2.52 1.87 1.87
0.35 3.83 2.30 1.70 0.52 0.70 2.00
0.57 3.65 2.30 1.78 0.61 0.74 1.83 0.22
0.39 3.74 2.26 1.65 0.48 0.65 1.91 0.09 0.13
3.39 3.96 3.43 3.78 2.52 3.30 3.13 3.35
1.65 0.61 1.04 1.17 2.22 1.96 2.26
1.13 0.65 2.57 1.13 1.04 1.13
Amongst the three Triaenops spp., T. rufus shows no geographical correlation to genetic structuring amongst and within populations, while in T. furculus haplotypic variation shows a strong geographical component (Russell et al. 2006). Genetic data from Triaenops auritus comes from a very limited geographical range (extreme northern Madagascar) and it is not surprising that there is little genetic variation in this species (Russell et al. 2006). Thus, at least within the genus Triaenops, the question of dispersal patterns does not appear to be related to shifts in morphological characters associated with the
0.65 1.43 1.61 1.39 1.65
2.04 1.52 1.35 1.57
2.74 2.43 2.78
0.30 0.09
0.35
sympatric occurrence between congeners. Triaenops rufus is common at the three study sites and coexists with either T. auritus in the far north and T. furculus further south. We are unaware of any published data on the seasonal occurrence of arthropods on Madagascar that are important prey for insectivorous bats (e.g., Diptera). Thus, it is impossible to address the second point mentioned above in any meaningful way. However, given the differences in the forest and vegetation types of the three study regions (Gautier and Goodman 2003), as well as climatic regimes (Cornet 1974; see Material and methods),
ARTICLE IN PRESS 10
J. Ranivo, S.M. Goodman
between the two northern and the southern study sites, it can be assumed that there are important differences in the density and taxonomic representation of arthropods between these sites. By extrapolation, the prey species consumed by a given bat species at the Sarodrano/Tsimanampetsotsa site should show notable differences from those at the two more northern sites. An analysis of the arthropods in the stomachs of bats collected at sites in western Madagascar, including those represented in the current study, gives the impression that there is no clear dietary specialization in many of the species examined in the current study and that many are generalists (Razakarivony et al. 2005). One of the problems with interpreting the results of this study is that most of the arthropod remains could not be identified at a fine taxonomic level, which might mask differences in the diets of these different bat species. This lack of prey specificity is in notable contrast to members of certain bat communities in tropical America, particularly forest-dwelling species, that show a high degree of specialization in their diets (Kalko 1998); however, these differences may in part be to the lack of precise data on the diet and associated specializations of Malagasy species (sensu Patterson et al. 2003). Further, the vast majority of the Malagasy species used in this current study are not obligatory forestdwelling species (Goodman et al. 2005), which might help to explain this difference. Emballonura nov. sp. is probably one of the few largely forest-dependent bat species in the western portion of the island (Goodman et al. 2005), and is presumed to feed in the lower portion of the forest substrates. This would imply that its foraging behavior is different from above canopy feeders or those in open areas, such as Mormopterus jugularis. Hence, even though certain taxa might show considerable convergence in morphological characteristics, differences in some natural history parameters infer a direct separation in some of their ecological aspects. Based on our field surveys, Emballonura nov. sp. was not found at the southern two study zones. However, this species has been reported as far south as Toliara and is known from the Bemaraha region (Peterson et al.
1995; Goodman et al. 2006). Further, M. jugularis is known to occur as a synanthropic species across the western and southwestern portion of the island, even to the south of the Tsimanampetsotsa region (Goodman unpublished data), hence it is presumably in contact with bat communities occurring in more natural settings. We found little evidence of morphological overlap, based on an overlay of four different datasets, in species of bats occurring along the western portion of the island. In the few cases when sympatric species overlap for certain types of variables, they show separation for other types of morphological attributes. In other cases, allopatric species show broad overlap in certain aspects of their morphology. Even though there is considerable clinal variation between the study sites in certain biotic and abiotic parameters, we have found little evidence that the different bat species are responding accordingly in aspects of their morphology. The single exception is H. commersoni, which shows geographic variation in size. In the western portion of the island the different study species are not restricted to forest habitats, are largely habitat generalists, and based on current evidence are not known to show clear dietary specialization.
Acknowledgements This project was conducted under the terms of an Accord de Collaboration between the De´partement de Biologie Animale of the University of Antananarivo with WWFMadagascar and The Field Museum of Natural History. We are grateful to Prof. Olga Ramilijaona and Dr. Daniel Rakotondravony for their aid in numerous ways. Permits to conduct this research were kindly provided by the Direction des Eaux et Foreˆts and the Association Nationale pour la Gestion des Aires Prote´ge´es. The field research was financed by grants from the John D. and Catherine T. MacArthur Foundation, National Geographic Society (6637-99 and 7402-03), and the Volkswagen Foundation. For assistance in the field, we acknowledge the help of Scott Cardiff, Achille Raselimanana, Fanja Ratrimomanarivo,
ARTICLE IN PRESS Ecomorphological variation in bats
Vola Razakarivony, and Harald Schu¨tz. For comments on an earlier version of this ms. we are grateful to Prof. Dr. Dieter Kruska and an anonymous reviewer. Prof. Dr. Jo¨rg
11
Ganzhorn kindly translated the abstract into German and Lucienne Wilme´ prepared Figure 1.
Zusammenfassung Muster o¨komorphologischer Charakteristika von Flederma¨usen in West-Madagaskar: Vergleich innerhalb und zwischen Gemeinschaften auf verschiedenen Breitengraden O¨komorphologische Studien untersuchen Zusammenha¨nge zwischen Morphologie und Verhalten von Arten. Ziel dieser Arbeiten ist herauszufinden, ob und in welchen morphologischen Merkmalen sich a¨hnlich gestaltete Arten unterscheiden und wie sie dadurch mo¨gliche zwischenartliche Konkurrenz vermeiden ko¨nnten. Wir untersuchten die O¨komorphologie von 10 Fledermausarten aus drei Gebieten im Westen Madagaskars. O¨komorphologische Charakteristika basierten auf Messungen von 6 a¨uXerlichen, 11 Scha¨del-, 12 Zahn- und 11 Flu¨gelmerkmalen. Insgesamt wurden 567 Individuen vermessen. Die drei Untersuchungsgebiete umfassten einen Vegetations- und Umweltgradienten von 11,6 Breitengraden, der von Dornbuschformationen im Su¨den bis zu regengru¨nen Trockenwa¨ldern im Norden reicht. Das su¨dlichste Gebiet unterschied sich dabei wesentlich von den beiden Gebieten weiter im Norden. Die vier Datensa¨tze wurden mit Hilfe von Hauptkomponentenanalysen zusammengefaXt. Die Hauptkomponenten wurden dann dazu benutzt, um den o¨komorphologischen Raum zu beschreiben, den die Arten in den drei Gebieten einnehmen. Die meisten Arten zeigten klare Trennung innerhalb eines Gebietes und variierten wenig zwischen den Gebieten. Ausnahmen waren zwei Arten von Trianops, die sich stark in Scha¨del-, Zahn- und Flu¨gelmerkmalen u¨berlappten. Diese beiden Arten haben allopatrische Verbreitungsgebiete. Starke U¨berlappung in a¨uXeren, Scha¨del- und Zahnmerkmalen trat auch bei den sympatrischen Arten Miniopterus manavi und Myotis goudoti auf. Diese Arten unterscheiden sich aber wesentlich in ihrer Flu¨gelmorphologie. Dies sollte ihnen erlauben, unterschiedliche Mikrohabitate und Beute in ihrem Lebensraum zu nutzen. Hipposideros commersoni war die einzige Art, die deutliche Unterschiede zwischen Gebieten zeigte. Diese Art ist sexualdimorph. Individuen aus dem Su¨den waren kleiner als Individuen aus dem Norden. r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved.
References Aguirre, L. F.; Herrel, A.; Van Damme, R.; Matthysen, E. (2002): Ecomorphological analysis of trophic niche partitioning in a tropical savanna bat community. Proc. R. Soc. London B 269, 1271–1278. Bradley, T. J. (1994): The role of physiological capacity, morphology, and phylogeny in determining habitat use in mosquitoes. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp., 303–318. Brown Jr., W. L.; Wilson, E. O. (1956): Character displacement. Syst. Zool. 5, 49–64. Cardiff, S. G.; Befourouack, J. (2003): The Re´serve Spe´ciale d’Ankarana. In: The Natural History of Madagascar. Ed. by S. M. Goodman and
J. P. Benstead. Chicago: The University of Chicago Press. Pp. 1501–1507. Chaperon, P.; Danloux, J.; Ferry, L. (1993): Fleuves et Rivie`res de Madagascar. Paris: Editions ORSTOM. Cornet, A. (1974): Essai de cartographie bioclimatique a` Madagascar, Carte a` 1/200.000 et notice no. 55. Paris: ORSTOM. Donque, G. (1975): Contribution Ge´ographique a` l’e´tude du Climat de Madagascar. Antananarivo: Nouvelle Imprimerie des Arts Graphiques. Findley, J. S. (1993): Bats: A Community Perspective. Cambridge: Cambridge University Press. Findley, J. S.; Black, H. (1982): Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64, 625–630.
ARTICLE IN PRESS 12
J. Ranivo, S.M. Goodman
Freeman, P. W. (1979): Specialized insectivory: Beetle-eating and moth-eating molossid bats. J. Mammallogy 60, 467–479. Freeman, P. W. (1984): Functional cranial analysis of large animalivorous bats (Microchiroptera). Biol. J. Linn. Soc. 21, 387–408. Freeman, P. W. (1998): Form, function, and evolution in skulls and teeth of bats. In: Bat Biology and Conservation. Ed. by T. H. Kunz and P. A. Racey. Washington, DC: Smithsonian Institution Press. Pp. 140–156. Garland, Jr. T.; Losos, J. B. (1994): Ecological morphology of locomotor performance in squamate reptiles. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp. 240–302. Gautier, L.; Goodman, S. M. (2003): Introduction to the flora of Madagascar. In: The Natural History of Madagascar. Ed. by S. M. Goodman and J. P. Benstead. Chicago: The University of Chicago Press. Pp. 229–250. Goodman, S. M.; Cardiff, S. G.; Ranivo, J.; Russell, A. L.; Yoder, A. D. (2006): A new species of Emballonura (Chiroptera: Emballonuridae) from the dry regions of Madagascar. Am. Mus. Nov. (in press). Goodman, S. M.; Raherilalao, M. J.; Rakotomalala, D.; Rakotondravony, D.; Raselimanana, A. P.; Razakarivony, H. V.; Soarimalala, V. (2002): Inventaire des verte´bre´s du Parc National de Tsimanampetsotsa (Toliara). Akon’ny Ala 28, 1–36. Goodman, S. M.; Andriafidison, D.; Andrianaivoarivelo, R.; Cardiff, S. G.; Ifticene, E.; Jenkins, R. B.; Kofoky, A.; Mbohoahy, T.; Rakotondravony, D.; Ranivo, J.; Ratrimomanarivo, F.; Razafimanahaka, J.; Racey, P. A. (2005): The distribution and conservation of bats in the dry regions of Madagascar. Anim. Conserv. 8, 153–165. Kalko, E. K. V. (1998): Organisation and diversity of tropical bat communities through space and time. Zoology 101, 281–297. Leisler, B.; Winkler, H. (1985): Ecomorphology. Curr. Ornith. 2, 155–186. Nicoll, M. E.; Langrand, O. (1989): Madagascar: Revue de la conservation et des aires prote´ge´es. Gland: WWF. Norberg, U. M. (1981): Allometry of bat wings and legs and comparison with bird wings. Phil. Trans. Roy. Soc. London B 292, 359–398. Norberg, U. M. (1994): Wing design, flight performance and habitat use in bats. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly.
Chicago: The University of Chicago Press. Pp. 205–239. Patterson, B. D.; Willig, M. R.; Stevens, R. D. (2003): Tropic strategies, niche portioning, and patterns of ecological organization. In: Bat Ecology. Ed. by T. H. Kunz and M. B. Fenton. Chicago: The University of Chicago Press. Pp. 536–579. Peterson, R. L.; Eger, J. L.; Mitchell, L. (1995): Chiropte`res Faune de Madagascar. Vol. 84. Paris: Muse´um National d’Histoire Naturelle Pp. 1–204. Ranivo, J.; Goodman, S. M. (2006): Re´vision taxinomique des Triaenops malgaches (Mammalia: Chiroptera: Hipposideridae). Zoosystema (in press). Rasoloarison, V.; Paquier, F. (2003): Tsingy de Bemaraha. In: The Natural History of Madagascar. Ed. by S. M. Goodman and J. P. Benstead. Chicago: The University of Chicago Press. Pp. 1507–1512. Razakarivony, H. V.; Rajemison, B.; Goodman, S. M. (2005): The diet of Malagasy Microchiroptera based on stomach contents. Mamm. biol. 5, 312–316. Reilly, S. M. (1994): The ecological morphology of metamorphosis: Heterochrony and the evolution of feeding mechanisms in salamanders. In: Ecological Morphology: Integrative organismal biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp. 319–338. Russell, A. L.; Ranivo, J.; Palkovacs, E. P.; Goodman, S. M.; Yoder, A. D. (2006): Working at the interface of phylogenetics and population genetics to discriminate among competing biogeographic hypotheses of dispersal. Mol. Ecol. (in press). Saunders, M. B.; Barclay, R. M. R. (1992): Ecomophology of insectivorous bats: a test of predictions using two morphologically similar species. Ecology 73, 1335–1345. Simmons, N. B. (2005): Order Chiroptera. In: Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd ed. Ed. by D. E. Wilson and D. M. Reeder. Baltimore: Johns Hopkins University Press. Pp. 312–529. Swartz, S. M.; Freeman, P. W.; Stockwell, E. F. (2003): Ecomorphology of bats: Comparative and experimental approaches relating structural design to ecology. In: Bat Ecology. Ed. by T. H. Kunz and M. B. Fenton. Chicago: The University of Chicago Press. Pp. 257–300. Van Cakenberghe, V.; Herrel, A.; Aguirre, L. F. (2002): Evolutionary relationships between cranial shape and diet in bats (Mammalia: Chiropetra). In: Topics in functional and
ARTICLE IN PRESS Ecomorphological variation in bats
ecological vertebrate morphology. Ed. by P. Aerts, K. d’Aouˆt, A. Herrel and R. Van Damme. Maastricht: Shaker Publishing. Pp. 205–236. Authors’ addresses: Julie Ranivo, De´partement de Biologie Animale, Universite´ d’Antananarivo, B.P. 906, Antananarivo
13
(101), Madagascar and WWF, Ecology Training Program, BP 738, Antananarivo (101), Madagascar Steven M. Goodman, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA and WWF, BP 738, Antananarivo (1 0 1), Madagascar (e-mail: [email protected])
www.elsevier.de/mambio
Original investigation
Patterns of ecomorphological variation in the bats of western Madagascar: Comparisons among and between communities along a latitudinal gradient By Julie Ranivo and S.M. Goodman De´partement de Biologie Animale, Universite´ d’Antananarivo and WWF, Antananarivo, Madagascar, Field Museum of Natural History, Chicago, USA and WWF, Antananarivo, Madagascar Receipt of Ms. 24.11.2005 Acceptance of Ms. 17.8.2006
Abstract The ecomorphology of 10 insectivorous bat species at three study zones in western Madagascar was examined using 567 specimens and based on 6 external, 11 cranial, 12 dental, and 11 wing measurements. The three study sites are located along a cline representing 11.61 of latitude. The southern most site has notable differences in vegetational and climatic regimes than the two more northern sites. Principal component analyses were conducted for each of the four datasets to examine the morphological space occupied by each species at the three sites. Most taxa showed clear intra-site separation and little inter-site variation. The exceptions included extensive morphological overlap in two taxa of Triaenops (cranial, dental, and wing), that have allopatric distributions, and between the sympatric Miniopterus manavi and Myotis goudoti (external, cranial, and dental). In the latter case, there was distinct separation in wing shape between these two taxa, which would allow them to exploit local habitats and prey in different manners. The only species that showed considerable inter-site variation was Hipposideros commersoni, which is sexually dimorphic, with individuals from the south being smaller than those in the north. r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Key words: Chiroptera, ecomorphology, community, latitudinal gradient, Madagascar
Introduction Studies in the field of ecomorphology examine the interface between the morphology and behavioral ecology of organisms, specifically attempting to explain how differences in physical attributes allow the coexistence of similarly shaped animals in light of potential inter-specific competition. This research approach, which has been used for nearly 50 years, starting with the work of Brown and Wilson (1956), and in more
recent years has been applied to a variety of groups (e.g. Leisler and Winkler 1985; Saunders and Barclay 1992; Bradley 1994; Garland and Losos 1994; Reilly 1994), provides insight into the relationships and mechanisms between the physical form of the individual components of a community of organisms, aspects of their behavior, and how they physically exploit their environment.
1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2006.08.004 Mamm. biol. 72 (2007) 1 1–13
ARTICLE IN PRESS 2
J. Ranivo, S.M. Goodman
Morphology dictates an individual’s performance limits and restricts its behavioral repertoires; for example, regardless of habitat, a bat cannot fly faster or eat larger prey than its anatomy will allow (Swartz et al. 2003). Thus, ecomorphological studies provide a proxy to examine resource partitioning at the community level, which otherwise would be difficult to measure. An excellent example is the shape of bats’ wings, which provide the locomotory means for various foraging styles and the exploitation of different types of aerial arthropods (Norberg 1981). A number of studies have examined through ecomorphological inference resource partition in bat communities (e.g. Findley and Black 1982; Saunders and Barclay 1992; Findley 1993; Kalko 1998; Aguirre et al. 2002; Van Cakenberghe et al. 2002). In the current study, we investigate four different morphological datasets obtained from bat specimens collected in the western portion of Madagascar, to examine, at a site level, the partition of inter-specific ecomorphological space. The different datasets include: external morphology – coupled with general size and associated with foraging design and locomotory capacity (Norberg 1994; Van Cakenberghe et al. 2002); cranial structure – presumed to be correlated with both feeding types and sonar capacity (Freeman 1979, 1984; Van Cakenberghe et al. 2002); dental morphology and size – linked to food types and processing (Swartz et al. 2003); and wing structure – related to the type of flight, the manner, and habitat type bats forage in (Norberg 1994). The different study sites represent latitudinal shifts from dry deciduous forests in the north to spiny bush in the south, and between the sites, there are some shifts in bat species composition and presumably in food resources with respect to arthropod density and taxonomic representation. Given this variation, we are able to examine, at several different scales, potential shifts in the ecomorphology of the insectivorous bat communities.
Material and methods Species and study sites Ten species of bats where used in this study, that represent the majority of those known from each of the study sites (Goodman et al. 2005). At least in
western Madagascar, these species generally use caves for their day roosts. The species include (n=sample size of each taxon): Emballonura nov. sp. (n=11) (Emballonuridae); Hipposideros commersoni (n=34), Triaenops auritus (n=40), T. furculus (n=53), and T. rufus (n=64) (Hipposideridae); Myotis goudoti (n=99), Miniopterus gleni (n=32), and Miniopterus manavi (n=194) (Vespertilionidae); and Mormopterus jugularis (n=8) and Otomops madagascariensis (n=32) (Molossidae). All of these animals forage on arthropods and are endemic to the Malagasy region based on recent taxonomic assessments (Simmons 2005; Goodman et al. 2006; Ranivo and Goodman 2006). Five different sites were censused for this study, spanning much of the latitudinal breadth of western Madagascar. In two cases, nearby sites were combined to maximize sample sizes; the sites used in the analyses are from north to south Ankarana, Namoroka/Bemaraha, and Sarodrano/Tsimanampetsotsa (Fig. 1). Hipposideros commersoni, T. rufus, Myotis goudoti, Miniopterus gleni, M. manavi, and O. madagascariensis occur at all three study sites, while Emballonura nov. sp. and Mormopterus jugularis are restricted in our dataset to specimens from Ankarana. Two of the Triaenops spp. show non-overlapping distributions, with T. auritus occurring at Ankarana and T. furculus at Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa. Ankarana is a zone of limestone karst containing an extensive cave system and with dry deciduous forest habitat within canyons (Cardiff and Befourouack 2003). The nearest weather station is at Ambilobe that has an annual mean temperature of 26.7 1C, on average 1890 mm of annual rain, and a dry season of approximately 6 months (Nicoll and Langrand 1989). The next study area to the south is the combined sites of Namoroka/Bemaraha, which are also limestone karst zones with a notable number of caves and forested areas within canyons (Rasoloarison and Paquier 2003). The weather station falling between these two sites is at Besalampy, which has an annual mean temperature around 26 1C, on average 1420 mm of annual rain, and a dry season of approximately 7 months (Donque 1975; Chaperon et al. 1993). The southern most study area, composed of the Sarodrano/Tsimanampetsotsa sites, holds zones of subarid thorn scrub or spiny bush (Goodman et al. 2002). Most of the bat netting conducted at these latter two sites was associated with bat day roosts in caves. The nearest weather station is at Toliara, which has an annual mean temperature of 24.2 1C, on average of 390 mm of annual rain, and a dry season of approximately 8 months (Donque 1975; Chaperon et al. 1993).
ARTICLE IN PRESS Ecomorphological variation in bats
3
Fig. 1. Map of Madagascar showing the different study sites, which represent a significant proportion of the complete latitudinal breadth of the island. Locality names of other sites mentioned in the text are also noted.
Specimens Skulls of collected animals were removed before the cadavers were conserved in 12.5% formalin, and consequently cleaned with the use of dermestid beetles. The formalin preserved specimens were consequently washed in running water for about 24 h and then transferred to 75% ethanol. The voucher specimens are held in the collections of the Field Museum of Natural History (Chicago) and the De´partement de Biologie Animale, Universite´ d’Antananarivo (Antananarivo).
Measurements External measurements were made, largely by SMG, using a millimeter ruler accurate to the
nearest 0.5 mm from collected specimens before their preparation. These included: total length (TL), tail length (TAIL), hind foot length (HF) (not including claw), ear length (EAR), and forearm length (FA). Further, we measured body mass (WT) in grams using a spring balance accurate to the nearest 0.1 g. Cranial and dental measurements were obtained by JR using a dial calipers precise to the nearest 0.1 mm and included: cranial — greatest skull length (GKSL), condyle-basal length (CBL), greatest zygomatic breadth (ZYGO), braincase height (BCH), minimum interorbital width (IOW), greatest mastoid breadth (MAST), rostrum length (ROST), palate length (PAL), mandible length (MAND), coronoid-condyle length (CORCON),
ARTICLE IN PRESS 4
J. Ranivo, S.M. Goodman
and condyle-angular process length (CONAN); and dental — length between I1 and M3 (I1 M3), length of upper molar toothrow (MOL), distance across upper canines (C1 C1), distance across upper posterior molars (M3 M3), width of last upper premolar (M3W), length of upper canine (C1L), length between i1 and m3 (i1 m3), length of lower molar toothrow (moli), distance across molar-condyle (molcon), width of last lower premolar (m3w), length of lower canine (c1l), and mandible width at level of m2 (mw2). Wing measurements were made, by JR, using a millimeter ruler accurate to the nearest 0.5 mm from collected specimens before their preparation: length of 1st digit-metacarpal (L1DM), length of 2nd digitmetacarpal (L2DM), length of 3rd digit-metacarpal (L3DM), length of 3rd digit –1st phalanx (L3D1P), length of 3rd digit –2nd phalanx (L3D2P), length of 4th digit-metacarpal (L4DM), length of 4th digit –1st phalanx (L4D1P), length of 4th digit –2nd phalanx (L4D2P), length of 5th digit-metacarpal (L5DM), length of 5th digit –1st phalanx (L5D1P), and length of 5th digit –2nd phalanx (L5D2P). For further precision and definitions for these variables, see Ranivo and Goodman (2006). The age classification of these animals was based on the eruption of teeth, the ossification of the basiosphenoid suture, and the development of the sagittal crest. Only adults, based on these three characters, were used in this study.
Statistical tests We used the program STATISTICA version 5.1 to conduct the various statistical comparisons. For the principal component (PC) analyses, the four different variable types (external, cranial, dental, and wing) were treated separately. These analyses were based on non-log-transformed data and correlation matrices. A series of ANOVA tests were conducted on the first and second PC scores for all species at the three sites. When these tests showed statistical significance (alpha=0.05), Scheffe´ tests were used to examine the internal interactions between sites. The detailed matrices of the Scheffe´ tests are not presented here, but rather only probability values when they were statistically significant. Finally, measurements were made of the inter-species mean distances as calculated by the PC analyses.
Results and discussion External measurements The results of the PC analysis for the external measurements (Fig. 2A), which include all
species from the three study sites, show that five of the six measurements are strongly correlated with the first axis, explaining 69.5% of the variance, and only the TAIL shows important loading for the second axis, adding an additional 21.6% to the total explained variance (Tab. 1). There is a clear separation of the different species based on their size (Fig. 2A). The two largest species, H. commersoni and O. madagascariensis, are notably separated from the other taxa. Five groupings can be distinguished based on the second axis. The ANOVA conducted on the first axis is significant across species at a level of Po0.0001. Scheffe´ tests indicate that the two largest species are significantly different than the others used in this analysis (Pp0,01). Hipposideros commersoni shows a shift in occupied morphological space between the sites of Ankarana and Namoroka/Bemaraha (Pp0,001), while O. madagascariensis does not show inter-locality differences. Amongst the additional five groups, two show species overlap in morphological space: T. rufus–Mormopterus jugularis and Myotis goudoti Miniopterus manavi. The first axis of the PC analysis for Myotis from Namoroka/Bemaraha is significantly different from that of Miniopterus manavi from Ankarana (P=0.01) and Namoroka/Bemaraha (Pp0.001); these two species do not show any inter-locality difference. Miniopterus manavi shows no inter-locality difference, but occupies a different morphological space from the other species based on its separation along the second axis. Emballonura nov. sp. is also notably distinct from the other species based on external characters. T. furculus and T. auritus overlie one another in their interlocality positions based on the first axis. Cranial measurements The results of the PC analysis for the cranial variables for all species from the three sites (Fig. 2B) shows virtually all of the variables are strongly correlated with the first axis, which explains 82.0% of the variation, with the exception of PAL and IOW, which show heavy loadings on the second axis, accounting for another 12.9% of the variation (Tab. 2).
ARTICLE IN PRESS Ecomorphological variation in bats
3.5 2.5
1.5
1.5
0.5 –0.5
0.5 –0.5
–1.5
–1.5
–2.5
–2.5
(A)
CP 2
CP 2
2.5
1.5 2.5 CP 1
3.5
4.5
–3.5 –1.5 – 0.5 0.5
5.5
(B)
3.5
3.5
2.5
2.5
1.5
1.5
0.5
0.5
CP 2
CP 2
3.5
–3.5 –1.5 –0.5 0.5
–0.5
–1.5
–2.5
–2.5
(C) Emballonura nov. sp. Hipposideros Ank Hipposideros N/B Hipposideros S/T
1.5 2.5 CP 1
3.5
4.5
–3.5 –1.5 – 0.5 0.5
5.5
M.gleni Ank M.gleni N/B M.gleni S/T M.manavi Ank
1.5 2.5 CP 1
3.5
4.5
5.5
1.5 2.5 CP 1
3.5
4.5
5.5
–0.5
–1.5
–3.5 –1.5 –0.5 0.5
5
(D) M.manavi N/B M.manavi S/T Mormopterus Myotis Ank
Myotis N/B Myotis S/T Otomops Ank Otomops N/B
Otomops S/T T.auritus T.furculus N/B T.furculus S/T
T.rufus Ank T.rufus N/B T.rufus S/T
Fig. 2. Scatter diagram of axis 1 and axis 2 in PC analyses of different morphological variables for 10 different bat species: (A) external measurements (see Tab. 1 for associated loadings); (B) cranial measurements (see Tab. 2 for associated loadings); (C) dental measurements (see Tab. 3 for associated loadings); and (D) wing measurements (see Tab. 4 for associated loadings). Key to locality names: Ank=Ankarana, N/B=Namoroka/ Bemaraha, S/T=Sarodrano/Tsimanampetsotsa.
The positions of the different species in scatter projections of PC axis 1 and axis 2 show direct parallels between the external (Fig. 2A) and cranial (Fig. 2B) variables. The ANOVA based on the first axis is significant across species (Po0.0001). The internal Scheffe´ tests comparisons indicate that H. commersoni is notably separated from all of the other species (Pp0.001) and there is a difference in the occupation of morphological space between the individuals of this species from Namoroka/Bemaraha and those from Sarodrano/ Tsimanampetsotsa (Pp0.001). Based on the
first two axes, Miniopterus manavi of Ankarana occupy a similar morphological space as Myotis goudoti at the same locality. No interlocality difference was found for Otomops, Miniopterus gleni, M. manavi, Myotis, and the three Triaenops spp. Dental measurements The results of the PC analysis for the dental variables (Fig. 2C), for all species from the three sites, indicate that nine of the 12 variables are strongly correlated with the first
ARTICLE IN PRESS 6
J. Ranivo, S.M. Goodman
Table 1. Correlations between external measurement variables and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variance Eigenvalues TL TAIL HF EAR FA WT
Axis 1
Axis 2
69.5 4.17 0.74 0.05 0.95 0.87 0.98 0.93
91.1 1.29 0.64 0.99 0.07 0.01 0.01 0.15
Table 2. Correlations between cranial measurement variables and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variation Eigenvalues GSKL CBL ZYGO BCH IOW MAST ROST PAL MAND CORCON CONAN
Axis 1
Axis 2
82.0 9.01 0.98 0.95 0.94 0.81 0.08 0.96 0.93 0.41 0.97 0.99 0.89
94.8 1.42 0.16 0.28 0.25 0.33 0.98 0.24 0.33 0.87 0.23 0.03 0.38
axis, accounting for 90.5% of the explained variation, and I1 M3, MOL, and M3W show heavy loadings on the second axis, adding an additional 4.6% of the explained variation (Tab. 3). Compared to the external (Fig. 2A) and cranial (Fig. 2B) variables, dental variables (Fig. 2C) reveal a notable reduction of the inter-species distances. In the case of the dental variables, two groups can be readily distinguished based on the first two axes of the PC analysis: H. commersoni and O. madagascariensis. The remaining taxa (Mormopterus jugularis, Triaenops spp., Miniopterus spp., Myotis goudoti, and Emballonura
Table 3. Correlations between dental measurements and the PC analysis.
% cumulative variation Eigenvalues I1 M 3 MOL C1 C1 M3 M3 M3W C1L i1-m3 moli molcon m3 w c1l mw2
Axis 1
Axis 2
90.5 10.86 0.51 0.66 0.81 0.72 0.33 0.89 0.70 0.73 0.74 0.84 0.88 0.79
95.1 0.55 0.84 0.73 0.53 0.68 0.91 0.40 0.70 0.66 0.64 0.47 0.43 0.49
nov. sp.) form several clouds of points that are not well differentiated. The ANOVA of the first axis across species is statistically significant (Po0.0001). The Scheffe´ tests indicate that Hipposideros from Ankarana and Sarodrano/Tsimanampetsotsa (P=0.01), as well as Namoroka/Bemaraha and Sarodrano/Tsimanampetsotsa (Pp0.001) are different from one another. The three Triaenops spp. show no difference at any given locality, with the exception of T. auritus and T. rufus at Namoroka/Bemaraha (Pp0.001). Otomops, Miniopterus gleni, M. manavi, and Myotis show no inter-locality difference. Based on the first axis of the PC analysis, Emballonura and M. manavi demonstrate considerable overlap in morphological space. On the basis of this same axis, Emballonura is significantly different from Myotis (Pp0.02) and the three Triaenops spp. (Pp0.001). Further, M. manavi is significantly different from Myotis at all localities (Pp0.001) with the exception of Ankarana and Sarodrano/ Tsimanampetsotsa and the three Triaenops spp. (Pp0.001) at all localities. Wing measurements The results of the PC analysis for the different wing measurements (Fig. 2D), for all species from the three sites, indicate that nine of these 11 variables are strongly
ARTICLE IN PRESS Ecomorphological variation in bats
correlated with the first axis of the analysis, explaining 71.7% of the variation, and the remaining two variables, L3D2P and L4D2P, show heavy loadings for the second axis, accounting for an additional 19.6% of the variation (Tab. 4). This analysis shows an arrangement in morphological space somewhat different from the previous three analyses. Five different groups can be readily distinguished (four are mono-specific and the fifth is a composite of several genera and species): H. commersoni, O. madagascariensis, Miniopterus manavi, M. gleni, and then a conglomerate of Myotis goudoti, Mormopterus jugularis, Emballonura nov. sp., and the three Triaenops spp. The ANOVA analyses conducted on the first axis are significant across species (Po0.0001). The internal Scheffe´ tests indicate that Hipposideros from Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa occupy different positions in ecomorphological space (P=0.01). Miniopterus manavi, M. gleni, Myotis, T. rufus, T. furculus, and Otomops show no inter-locality difference based on the first axis of the PC analysis. Myotis goudoti shows broad overlap with Mormopterus jugularis. All three Triaenops spp. coincide in morphological space, with the exception of T. rufus from Namoroka/ Bemaraha and Ankarana are different from T. furculus at Sarodrano/Tsimanampetsotsa
Table 4. Correlations between wing measurements and the PC analysis. The majority of variables show a strong correlation with the first axis of the analysis.
% cumulative variation Eigenvalues L1DM L2DM L3DM L3D1P L3D2P L4DM L4D1P L4D2P L5DM L5D1P L5D2P
Axis 1
Axis 2
71.7 7.89 0.93 0.96 0.92 0.98 0.23 0.93 0.99 0.07 0.77 0.94 0.86
91.3 2.15 0.21 0.19 0.25 0.02 0.96 0.29 0.02 0.99 0.39 0.20 0.16
7
based on the first axis (Pp0.01), and T. rufus from Sarodrano/Tsimanampetsotsa are different from T. furculus at Namoroka/Bemaraha based on the first axis (P=0.005). Amongst the four types of morphological variables used in this study, there are notable differences, based on the PC analyses, in separating or grouping morphological dissimilar or similar species. Based on external morphology (Fig. 2A), the first axis is clearly correlated with size, while tail length is the only variable strongly correlated with the second axis. Two different groupings show overlapping species. The first of these, T. furculus–T. auritus, geographically replace one another between our study sites. The second grouping, Miniopterus manavi–Myotis goudoti, shows broad overlap in the external and cranial measurements, some separation in the dental measurements, and clear distinction in the wing measurements. Hence, while there are similarities in certain aspects of the morphology of these two species, based on wing shape, they are presumed to have different foraging methods or techniques, as has been found for bats elsewhere in the world (Findley and Black 1982; Saunders and Barclay 1992). Freeman (1998) noted that insectivorous bats can be divided in two separate groups, those that consume hard body prey and soft body prey. The former is distinguished from the latter by having more robust mandibles and crania, and longer canines. Bases on the results presented here, specifically aspects of cranial and dental morphology, we can advance that M. manavi probably consumes softer bodied prey than Myotis. More research is needed to see if there are also differences in the types of arthropods these two bat species are feeding on. If indeed they forage on largely the same prey, then it would be presumed they do so in different ecological situations. Another example, with two morphologically similar species from different families, is that of T. rufus and Mormopterus jugularis, which show considerable overlap in the first two axes of the PC analysis of external characters, but in the other character sets are distinctly separated in the second axis. Further, there is a notable separation in these two species
ARTICLE IN PRESS 8
J. Ranivo, S.M. Goodman
based on their forearm length and body mass (Fig. 3). Cranial differences between the study species at the different sites (Fig. 2B) are notably different amongst all of the taxa, with the exception of Triaenops spp. and the Miniopterus manavi–Myotis goudoti group. However, based on dental structure, T. rufus shows clear separation from T. furculus and T. auritus. Within the different data sets, the greatest inter-specific spread is found within H. commersoni (Tabs. 5, 6; Fig. 3). This taxon is the only one amongst the study species that shows notable levels of sexual dimorphism. At an intra-generic level, the two most morphologically similar species are T. auritus and T. furculus and then these two species in comparison to the broadly distributed T. rufus are only subtly different (Tabs. 5, 6). The other possible inter-generic comparison is with Miniopterus, for which notable differences occur between Miniopterus gleni and M. manavi, the former is sympatric across its range with the latter (Tabs. 5, 6). The results of these analyses show few interlocality differences within each of the species examined and there would appear to be no marked latitudinal variation in the measurements of four different types of morphological variables of these different bats. In most cases, when found, it is likely that occasional and seemingly random significant inter-lo-
110.0 forearm length / mm
100.0 90.0 80.0 70.0 60.0 50.0 40.0 30.0 -0.02 0.00 0.02 0.04 0.06 0.08 0.10 0.12 body mass / kg
Fig. 3. Relationship between body mass and forearm length in the ten study species (Y=890.35 X+36.22; R2=0.801 Pp0.0001). See caption to Figure 2 for explanation of symbols.
cality differences are spurious and probably related to type II errors. The major exception is with H. commersoni, in which animals from the south are smaller than those in the north; although a portion of these differences might be associated with small samples sizes at the Sarodrano/Tsimanampetsotsa site. This supports the conclusion of another analysis where this species was found to show decreasing size with increasing latitude (Ranivo and Goodman unpublished data). Along the latitudinal gradient of our study sites in western Madagascar, a few species drop out at the more southern sites. Amongst the ten species used in this analysis, nine occur at Ankarana and seven at Namoroka/ Bemaraha and Sarodrano/Tsimanampetsotsa – Emballonura nov. sp. and Mormopterus jugularis are not represented in the specimens from the two southern sites. In the four different datasets Emballonura is generally well separated from the other species in morphological space, while Mormopterus shows considerable overlap with T. rufus in external measurements, some overlap with Miniopterus gleni in dental characteristics, and with Myotis goudoti in wing shape. Based on our PC analyses, there is not a notable shift in the morphological space occupied by similar species in the presence or absence of Emballonura nov. sp. and Mormopterus jugularis. The explanation for this lack of increase in variation in a morphologically similar species in the absence of these taxa might be related to several different factors: (1) for any given species there is regular dispersal and subsequent genetic exchange between populations occurring at our three study sites, hence reducing the means for microgeographic differentiation, (2) food is not a limiting factor and competition for available resources has not been an important recent factor in the evolution of morphological characters, (3) most of these species are generalists in the prey they hunt, (4) they may forage in different areas, and (5) they may occur at the southern sites but were undetected during our surveys. Knowledge on the dispersal, natural history, and distribution of Malagasy bats is still at a relatively rudimentary stage, but these five points can be addressed at certain levels.
ARTICLE IN PRESS Ecomorphological variation in bats
9
Table 5. Distance measurements for each of 10 bat species between the mid-position of point scatters for axes 1 and 2 of PC analyses. Values for external measurements characters are presented in the lower left portion of the matrix and cranial measurements in the upper right portion. Abbreviations for species names include: Emballonura nov. sp.=Em, Hipposideros commersoni=Hip, Miniopterus gleni=Mglen, M. manavi=Mman, Mormopterus jugularis=Mjug, Myotis goudoti=Mgoud, Otomops madagascariensis=Otom, Triaenops furculus=Tfurc, T. rufus=Truf, and T. auritus=Taur. Em Em Hip Mglen Mman Mjug Mgoud Otom Tfurc Truf Taur
4.17 3.48 2.04 1.52 2.17 3.26 0.74 1.43 0.83
Hip
Mglen
Mman
Mjug
Mgoud
Otom
Tfurc
Truf
Taur
3.83
1.96 3.48
0.87 3.83 1.17
1.48 3.04 0.70 0.91
1.04 3.48 0.91 0.35 0.57
3.39 2.65 1.74 2.78 1.96 2.43
1.00 2.96 2.26 1.52 1.57 1.48 3.22
0.87 3.00 2.04 1.35 1.35 1.26 3.04 0.22
1.04 2.87 2.22 1.57 1.52 1.48 3.13 0.09 0.22
3.52 3.83 3.35 3.65 1.61 3.48 3.17 3.35
1.57 2.00 1.39 1.96 2.96 2.13 2.96
0.78 0.22 2.39 1.65 1.00 1.70
0.78 2.04 0.96 0.22 0.96
2.17 1.74 1.00 1.74
2.52 1.96 2.43
0.83 0.13
0.83
Table 6. Distance measurements for each of 10 bat species between the mid-position of point scatters for axes 1 and 2 of PC analyses. Values for dental measurements characters are presented in the lower left portion of the matrix and wing measurements in the upper right portion. See table 5 for definitions of abbreviations. Em Em Hip Mglen Mman Mjug Mgoud Otom Tfurc Truf Taur
4.13 2.30 0.74 1.78 1.35 3.13 0.87 1.00 0.83
Hip
Mglen
Mman
Mjug
Mgoud
Otom
Tfurc
Truf
Taur
3.96
2.09 3.17
1.35 4.09 1.17
0.35 3.65 1.78 1.22
0.43 3.65 1.65 1.09 0.17
2.13 1.83 2.04 2.52 1.87 1.87
0.35 3.83 2.30 1.70 0.52 0.70 2.00
0.57 3.65 2.30 1.78 0.61 0.74 1.83 0.22
0.39 3.74 2.26 1.65 0.48 0.65 1.91 0.09 0.13
3.39 3.96 3.43 3.78 2.52 3.30 3.13 3.35
1.65 0.61 1.04 1.17 2.22 1.96 2.26
1.13 0.65 2.57 1.13 1.04 1.13
Amongst the three Triaenops spp., T. rufus shows no geographical correlation to genetic structuring amongst and within populations, while in T. furculus haplotypic variation shows a strong geographical component (Russell et al. 2006). Genetic data from Triaenops auritus comes from a very limited geographical range (extreme northern Madagascar) and it is not surprising that there is little genetic variation in this species (Russell et al. 2006). Thus, at least within the genus Triaenops, the question of dispersal patterns does not appear to be related to shifts in morphological characters associated with the
0.65 1.43 1.61 1.39 1.65
2.04 1.52 1.35 1.57
2.74 2.43 2.78
0.30 0.09
0.35
sympatric occurrence between congeners. Triaenops rufus is common at the three study sites and coexists with either T. auritus in the far north and T. furculus further south. We are unaware of any published data on the seasonal occurrence of arthropods on Madagascar that are important prey for insectivorous bats (e.g., Diptera). Thus, it is impossible to address the second point mentioned above in any meaningful way. However, given the differences in the forest and vegetation types of the three study regions (Gautier and Goodman 2003), as well as climatic regimes (Cornet 1974; see Material and methods),
ARTICLE IN PRESS 10
J. Ranivo, S.M. Goodman
between the two northern and the southern study sites, it can be assumed that there are important differences in the density and taxonomic representation of arthropods between these sites. By extrapolation, the prey species consumed by a given bat species at the Sarodrano/Tsimanampetsotsa site should show notable differences from those at the two more northern sites. An analysis of the arthropods in the stomachs of bats collected at sites in western Madagascar, including those represented in the current study, gives the impression that there is no clear dietary specialization in many of the species examined in the current study and that many are generalists (Razakarivony et al. 2005). One of the problems with interpreting the results of this study is that most of the arthropod remains could not be identified at a fine taxonomic level, which might mask differences in the diets of these different bat species. This lack of prey specificity is in notable contrast to members of certain bat communities in tropical America, particularly forest-dwelling species, that show a high degree of specialization in their diets (Kalko 1998); however, these differences may in part be to the lack of precise data on the diet and associated specializations of Malagasy species (sensu Patterson et al. 2003). Further, the vast majority of the Malagasy species used in this current study are not obligatory forestdwelling species (Goodman et al. 2005), which might help to explain this difference. Emballonura nov. sp. is probably one of the few largely forest-dependent bat species in the western portion of the island (Goodman et al. 2005), and is presumed to feed in the lower portion of the forest substrates. This would imply that its foraging behavior is different from above canopy feeders or those in open areas, such as Mormopterus jugularis. Hence, even though certain taxa might show considerable convergence in morphological characteristics, differences in some natural history parameters infer a direct separation in some of their ecological aspects. Based on our field surveys, Emballonura nov. sp. was not found at the southern two study zones. However, this species has been reported as far south as Toliara and is known from the Bemaraha region (Peterson et al.
1995; Goodman et al. 2006). Further, M. jugularis is known to occur as a synanthropic species across the western and southwestern portion of the island, even to the south of the Tsimanampetsotsa region (Goodman unpublished data), hence it is presumably in contact with bat communities occurring in more natural settings. We found little evidence of morphological overlap, based on an overlay of four different datasets, in species of bats occurring along the western portion of the island. In the few cases when sympatric species overlap for certain types of variables, they show separation for other types of morphological attributes. In other cases, allopatric species show broad overlap in certain aspects of their morphology. Even though there is considerable clinal variation between the study sites in certain biotic and abiotic parameters, we have found little evidence that the different bat species are responding accordingly in aspects of their morphology. The single exception is H. commersoni, which shows geographic variation in size. In the western portion of the island the different study species are not restricted to forest habitats, are largely habitat generalists, and based on current evidence are not known to show clear dietary specialization.
Acknowledgements This project was conducted under the terms of an Accord de Collaboration between the De´partement de Biologie Animale of the University of Antananarivo with WWFMadagascar and The Field Museum of Natural History. We are grateful to Prof. Olga Ramilijaona and Dr. Daniel Rakotondravony for their aid in numerous ways. Permits to conduct this research were kindly provided by the Direction des Eaux et Foreˆts and the Association Nationale pour la Gestion des Aires Prote´ge´es. The field research was financed by grants from the John D. and Catherine T. MacArthur Foundation, National Geographic Society (6637-99 and 7402-03), and the Volkswagen Foundation. For assistance in the field, we acknowledge the help of Scott Cardiff, Achille Raselimanana, Fanja Ratrimomanarivo,
ARTICLE IN PRESS Ecomorphological variation in bats
Vola Razakarivony, and Harald Schu¨tz. For comments on an earlier version of this ms. we are grateful to Prof. Dr. Dieter Kruska and an anonymous reviewer. Prof. Dr. Jo¨rg
11
Ganzhorn kindly translated the abstract into German and Lucienne Wilme´ prepared Figure 1.
Zusammenfassung Muster o¨komorphologischer Charakteristika von Flederma¨usen in West-Madagaskar: Vergleich innerhalb und zwischen Gemeinschaften auf verschiedenen Breitengraden O¨komorphologische Studien untersuchen Zusammenha¨nge zwischen Morphologie und Verhalten von Arten. Ziel dieser Arbeiten ist herauszufinden, ob und in welchen morphologischen Merkmalen sich a¨hnlich gestaltete Arten unterscheiden und wie sie dadurch mo¨gliche zwischenartliche Konkurrenz vermeiden ko¨nnten. Wir untersuchten die O¨komorphologie von 10 Fledermausarten aus drei Gebieten im Westen Madagaskars. O¨komorphologische Charakteristika basierten auf Messungen von 6 a¨uXerlichen, 11 Scha¨del-, 12 Zahn- und 11 Flu¨gelmerkmalen. Insgesamt wurden 567 Individuen vermessen. Die drei Untersuchungsgebiete umfassten einen Vegetations- und Umweltgradienten von 11,6 Breitengraden, der von Dornbuschformationen im Su¨den bis zu regengru¨nen Trockenwa¨ldern im Norden reicht. Das su¨dlichste Gebiet unterschied sich dabei wesentlich von den beiden Gebieten weiter im Norden. Die vier Datensa¨tze wurden mit Hilfe von Hauptkomponentenanalysen zusammengefaXt. Die Hauptkomponenten wurden dann dazu benutzt, um den o¨komorphologischen Raum zu beschreiben, den die Arten in den drei Gebieten einnehmen. Die meisten Arten zeigten klare Trennung innerhalb eines Gebietes und variierten wenig zwischen den Gebieten. Ausnahmen waren zwei Arten von Trianops, die sich stark in Scha¨del-, Zahn- und Flu¨gelmerkmalen u¨berlappten. Diese beiden Arten haben allopatrische Verbreitungsgebiete. Starke U¨berlappung in a¨uXeren, Scha¨del- und Zahnmerkmalen trat auch bei den sympatrischen Arten Miniopterus manavi und Myotis goudoti auf. Diese Arten unterscheiden sich aber wesentlich in ihrer Flu¨gelmorphologie. Dies sollte ihnen erlauben, unterschiedliche Mikrohabitate und Beute in ihrem Lebensraum zu nutzen. Hipposideros commersoni war die einzige Art, die deutliche Unterschiede zwischen Gebieten zeigte. Diese Art ist sexualdimorph. Individuen aus dem Su¨den waren kleiner als Individuen aus dem Norden. r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved.
References Aguirre, L. F.; Herrel, A.; Van Damme, R.; Matthysen, E. (2002): Ecomorphological analysis of trophic niche partitioning in a tropical savanna bat community. Proc. R. Soc. London B 269, 1271–1278. Bradley, T. J. (1994): The role of physiological capacity, morphology, and phylogeny in determining habitat use in mosquitoes. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp., 303–318. Brown Jr., W. L.; Wilson, E. O. (1956): Character displacement. Syst. Zool. 5, 49–64. Cardiff, S. G.; Befourouack, J. (2003): The Re´serve Spe´ciale d’Ankarana. In: The Natural History of Madagascar. Ed. by S. M. Goodman and
J. P. Benstead. Chicago: The University of Chicago Press. Pp. 1501–1507. Chaperon, P.; Danloux, J.; Ferry, L. (1993): Fleuves et Rivie`res de Madagascar. Paris: Editions ORSTOM. Cornet, A. (1974): Essai de cartographie bioclimatique a` Madagascar, Carte a` 1/200.000 et notice no. 55. Paris: ORSTOM. Donque, G. (1975): Contribution Ge´ographique a` l’e´tude du Climat de Madagascar. Antananarivo: Nouvelle Imprimerie des Arts Graphiques. Findley, J. S. (1993): Bats: A Community Perspective. Cambridge: Cambridge University Press. Findley, J. S.; Black, H. (1982): Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64, 625–630.
ARTICLE IN PRESS 12
J. Ranivo, S.M. Goodman
Freeman, P. W. (1979): Specialized insectivory: Beetle-eating and moth-eating molossid bats. J. Mammallogy 60, 467–479. Freeman, P. W. (1984): Functional cranial analysis of large animalivorous bats (Microchiroptera). Biol. J. Linn. Soc. 21, 387–408. Freeman, P. W. (1998): Form, function, and evolution in skulls and teeth of bats. In: Bat Biology and Conservation. Ed. by T. H. Kunz and P. A. Racey. Washington, DC: Smithsonian Institution Press. Pp. 140–156. Garland, Jr. T.; Losos, J. B. (1994): Ecological morphology of locomotor performance in squamate reptiles. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp. 240–302. Gautier, L.; Goodman, S. M. (2003): Introduction to the flora of Madagascar. In: The Natural History of Madagascar. Ed. by S. M. Goodman and J. P. Benstead. Chicago: The University of Chicago Press. Pp. 229–250. Goodman, S. M.; Cardiff, S. G.; Ranivo, J.; Russell, A. L.; Yoder, A. D. (2006): A new species of Emballonura (Chiroptera: Emballonuridae) from the dry regions of Madagascar. Am. Mus. Nov. (in press). Goodman, S. M.; Raherilalao, M. J.; Rakotomalala, D.; Rakotondravony, D.; Raselimanana, A. P.; Razakarivony, H. V.; Soarimalala, V. (2002): Inventaire des verte´bre´s du Parc National de Tsimanampetsotsa (Toliara). Akon’ny Ala 28, 1–36. Goodman, S. M.; Andriafidison, D.; Andrianaivoarivelo, R.; Cardiff, S. G.; Ifticene, E.; Jenkins, R. B.; Kofoky, A.; Mbohoahy, T.; Rakotondravony, D.; Ranivo, J.; Ratrimomanarivo, F.; Razafimanahaka, J.; Racey, P. A. (2005): The distribution and conservation of bats in the dry regions of Madagascar. Anim. Conserv. 8, 153–165. Kalko, E. K. V. (1998): Organisation and diversity of tropical bat communities through space and time. Zoology 101, 281–297. Leisler, B.; Winkler, H. (1985): Ecomorphology. Curr. Ornith. 2, 155–186. Nicoll, M. E.; Langrand, O. (1989): Madagascar: Revue de la conservation et des aires prote´ge´es. Gland: WWF. Norberg, U. M. (1981): Allometry of bat wings and legs and comparison with bird wings. Phil. Trans. Roy. Soc. London B 292, 359–398. Norberg, U. M. (1994): Wing design, flight performance and habitat use in bats. In: Ecological Morphology: Integrative Organismal Biology. Ed. by P. C. Wainwright and S. M. Reilly.
Chicago: The University of Chicago Press. Pp. 205–239. Patterson, B. D.; Willig, M. R.; Stevens, R. D. (2003): Tropic strategies, niche portioning, and patterns of ecological organization. In: Bat Ecology. Ed. by T. H. Kunz and M. B. Fenton. Chicago: The University of Chicago Press. Pp. 536–579. Peterson, R. L.; Eger, J. L.; Mitchell, L. (1995): Chiropte`res Faune de Madagascar. Vol. 84. Paris: Muse´um National d’Histoire Naturelle Pp. 1–204. Ranivo, J.; Goodman, S. M. (2006): Re´vision taxinomique des Triaenops malgaches (Mammalia: Chiroptera: Hipposideridae). Zoosystema (in press). Rasoloarison, V.; Paquier, F. (2003): Tsingy de Bemaraha. In: The Natural History of Madagascar. Ed. by S. M. Goodman and J. P. Benstead. Chicago: The University of Chicago Press. Pp. 1507–1512. Razakarivony, H. V.; Rajemison, B.; Goodman, S. M. (2005): The diet of Malagasy Microchiroptera based on stomach contents. Mamm. biol. 5, 312–316. Reilly, S. M. (1994): The ecological morphology of metamorphosis: Heterochrony and the evolution of feeding mechanisms in salamanders. In: Ecological Morphology: Integrative organismal biology. Ed. by P. C. Wainwright and S. M. Reilly. Chicago: The University of Chicago Press. Pp. 319–338. Russell, A. L.; Ranivo, J.; Palkovacs, E. P.; Goodman, S. M.; Yoder, A. D. (2006): Working at the interface of phylogenetics and population genetics to discriminate among competing biogeographic hypotheses of dispersal. Mol. Ecol. (in press). Saunders, M. B.; Barclay, R. M. R. (1992): Ecomophology of insectivorous bats: a test of predictions using two morphologically similar species. Ecology 73, 1335–1345. Simmons, N. B. (2005): Order Chiroptera. In: Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd ed. Ed. by D. E. Wilson and D. M. Reeder. Baltimore: Johns Hopkins University Press. Pp. 312–529. Swartz, S. M.; Freeman, P. W.; Stockwell, E. F. (2003): Ecomorphology of bats: Comparative and experimental approaches relating structural design to ecology. In: Bat Ecology. Ed. by T. H. Kunz and M. B. Fenton. Chicago: The University of Chicago Press. Pp. 257–300. Van Cakenberghe, V.; Herrel, A.; Aguirre, L. F. (2002): Evolutionary relationships between cranial shape and diet in bats (Mammalia: Chiropetra). In: Topics in functional and
ARTICLE IN PRESS Ecomorphological variation in bats
ecological vertebrate morphology. Ed. by P. Aerts, K. d’Aouˆt, A. Herrel and R. Van Damme. Maastricht: Shaker Publishing. Pp. 205–236. Authors’ addresses: Julie Ranivo, De´partement de Biologie Animale, Universite´ d’Antananarivo, B.P. 906, Antananarivo
13
(101), Madagascar and WWF, Ecology Training Program, BP 738, Antananarivo (101), Madagascar Steven M. Goodman, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA and WWF, BP 738, Antananarivo (1 0 1), Madagascar (e-mail: [email protected])