Species composition and morphological structure of thebat fauna of Yucatan, Mexico

HÉCTOR T. ARIT A

Journal o/ Animal

Ecology 1997,66, 83-97

Departamento de Ecología de los Recursos Naturales, Instituto de Ecología, Universidad Nacional Autónoma deMéxico, Apartado Postal 3-27 (Xangari), 58089 Morelia, Mich., Mexico

Summary

1. The relationship between regional and local assemblages of species can be analysedby comparing the composition of species and their morphological structure.2. 1 made such a comparison using data of the bat fauna of Yucatan, Mexico and ofa regional pool of species. Null models were constructed to test for differences incomposition in terms of taxonomic affiliation and of feeding and roosting habits.Additionally, dispersal ability and species-to-genus ratios were compared. Mor-phological structure was analysed using nearest-neighbour distances and minimumspanning trees were constructed on a morphological plane determined by the first twoprincipal components of external and skull measurements.3. No significant differences were detected in the comparisons of species composition,except in the case of dispersal ability. The Yuca tan bat fauna was a random subsampleof the pool in terms of taxonomy, diet and roosting habits. However, species with ahigher dispersal ability were better represented in the Yucatan fauna than expectedby chanceo4. No clear pattern could be detected in the comparisons of morphological structure.Nearest-neighbour analyses and minimum spanning trees showed only unclear andinconclusive results.5. The bat fauna ofYucatan is apparently formed by those species from the pool thatpossess a higher dispersal ability. The forces that determine the composition andstructure of this fauna are probably regional in nature, and the search for structuringfactors at the locallevel might be a futile endeavour.

Key-words: bats, community structure, local and regional processes, Mexico, nullmodels.

J ournal 01 Animal Ecology (1997), 66, 83-97

lntroduction

As stated by Elton (1927), whether communities have'limited membership' or are mere assemblages of spec-ies that happen to co-occur is one of the primaryquestions in community ecology (Roughgarden 1989).For several years, researchers have tried to answerthis question regarding communities of neotropicalbats (Findley 1993). The study of assemblages of neo-tropical bats has in some sense mirrored the devel-opment of ideas in community ecology.

Early studies of bat communities were based onthe premise of local ecological interactions, mainlycompetition, as structuring forces and on Hut-chinson's (1959) empirical rule of a regular spacing ofspecies along a size gradient (Tamsitt 1967; MacNab1971; Fleming, Hooper & Wilson 1972). Despite thefailure of most studies to find regular pattems, many

(¡;;) 1997 British

Ecological Society

researchers continued to think of neo tropical bat com-munities as structured assemblages organized by com-petition(Bonaccorso 1979; Humphrey, Bonaccorso &Zinn 1983).

Simberloff and collaborators (e.g. Connor & Sim-berloff 1979; Strong, Szyska & Simberloff 1979; Sim-berloff & Boecklen 1981) proposed the use of nullmodels to challenge most ideas of the MacArthurianperception of communities, and called attention toalternative factors (including random effects) that canaffect ecological assemblages. Soon after, similar stud-ies based on morphological analyses found no eVi-dence for competition in neo tropical bat communities(Willig & Moulton 1989).

Current research in community ecology focuses onthe relative contribution of local and regional forcesin shaping assemblages of species (Ricklefs 1987; Cor-nell & Lawton 1992; Ricklefs & Schluter 1993). Inter-

83

est has been centred on the effect of regional andhistorical factors in determining species richness at thelocallevel. The effect of regional processes on othercomponents of ecological diversity, such as relativeabundance of species and structure and function ofcommunities, has received less attention, althoughresults suggest that this line of research can be veryilluminating in searching for the answer to Elton'slimited membership question. This approach has beenused to suggest that the morphological structure ofneotropical and palaeotropical communities of insec-tivorous bats is determined primarily by evolutionaryhistory, rather than by present day processes (Heller& Volleth 1995).

This paper presents the results of a comparison ofa local community with a regional pool ofneotropicalbats. The comparisons included null-model analysesof patterns of species composition and of mor-phological structure in these assemblages. The resultsare discussed under the light of the current contro-versy on the relative role of local and regional pro-cesses in structuring ecological communities.

84Batfauna ofYucatan, Mexico

Materials and methods

DEFINITION OF THE FAUNA AND THE SOURCE

POOL

The study fauna is defined here as the set ofbat speciesthat are found in the state ofYucatan, which occupiesthe north-western portion of the peninsula of the samellame in Mexico. The political borders of the stateroughly coincide with the limits between evergreenand tropical deciduous forests (Rzedowski 1978). Alesser mountain range, the Sierrita de Ticul ( < 200 minaltitude), marks the southern limit ofthe state and isthe only mountain range in the otherwise flat northernpart of the peninsula. Because of these features, thestate of Yucatan is treated here as a separate entityfrom the rest of the peninsula.

The bat fauna ofYucatan can be considered a localassemblage as most species reported from the statecan be found in any single locality. For example, 29of the 31 Yucatan bat species have been observed inthe vicinity of Tekax, in the Sierrita de Ticul (Jones,Smith & Genoways 1973; Arroyo-Cabrales & Alvarez1990; Arita & Vargas 1995), and one of the missingspecies, Saccopteryx bilineata (Temminck 1838), isvery likely to occur there. As among-locality variationin species composition is negligible in this case, theYucatan fauna is treated here as a single local assem-

blage.The Yuca tan bat fauna consists of 31 species in

seven families (Table 1). The list is based on the speciesreported by Ramírez-Pulido et al. (1986) and a recentrecord of Centuria senex (Bowles, Heideman & Erick-son 1990). Species reported from Yucatan on the basisof erroneously identified specimens, such as Rhyn-chonycteris nasa (Wied-Neuwied 1820), Micronycteris

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Ecology, 66, 83-97

schmidtorum Sanborn 1935, Myotis nigricans (Schinz1921) and Tadarida brasi/iensis (E. GeotIroy 1824),were excluded (see Jones et al. 1973; La Val 1973; Hall1981). Also excluded were Macrotus waterhousii Gray1843 and Plecotus mexicanus (G. M. Allen 1916)because their presence in Yucatan is doubtful(Gaurner 1917; Anderson & Nelson 1965; Jones et al.

1973; Koopman 1974).In studies dealing with archipelagos, source pools

have been constructed from the faunas of the main-land adjacent to the islands (Grant 1966; SimberlotI1970; Graves & Gotelli 1983) or using the combinedfauna of the archipelago itself (Connor & SimberlotI1979; Gotelli & Abele 1982). For a study of con-tinental faunas of neotropical bats, Willig & Moulton(1989) created nested source pools based on the wholefauna of South America. As discussed by Graves &Gotelli (1983), none ofthese approaches is completelyobjective. Habitat and topographic ditIerencesbetween islands and the source afea are frequentlyignored, and the geological and climatological historyof the region is rarely considered. Further com'"plications are ditIerences in habitat preference anddispersal ability of the potential colonizing species.

The source pool is defined here as the set of batspecies found in the lowlands (altitude < 1000 m) ofthe Gulf and Caribbean versants of south-easternMexico, Belize and Guatemala, afeas that constitutethe base of the Yucatan Peninsula. Alternative sour-ces, including the state of Florida (bat fauna fromHall 1981); north-eastern Mexico, including the statesofTamaulipas, San Luis Potosí and Nuevo León (Wil-son et al. 1985); the northern extreme ofSouth Amer-ica (Eisenberg 1989); and the Greater Antilles, includ-ing Cuba, Jamaica, Puerto Rico and Hispaniola(Koopman 1990), were discarded in preliminaryanalyses because they showed much less similarity toYucatan than the chosen source. The bat fauna ofYucatan is a subset of the source pool, and the samesubspecies occur in both regions. A review of theliterature revealed the presence of 85 bat species in the

source pool.The natural vegetation of the state of Yucatan is

tropical deciduous and thorn forests, whereas the sou-thern part of the peninsula additionally harboursother more humid habitats (Rzedowski 1978). To cor-rect the original source pool for habitat preferencesamong species, 16 of the original 85 species weredeleted because they are not known to occur in dryafeas elsewhere in the neotropics, based on Koopman(1978), Ceballos & Miranda (1986), Eisenberg (1989),Willig (1983) and Wilson (1983). The remaining 69species, representing eight families, formed the sourcepool controlling for habitat use, and will be referredto as 'the pool' hereafter.

TESTS FOR COMPOSITION OF THE FAUNA

One type of null-model test in ecological communitiesis the search for unusual patterns of species compo-

Table 1. List ofbat species recorded from Yucatan

Emballonuridae Centurio senex Gray 1842Peropteryx macrotis (Wagner 1843) Sturnira lilium (E. Geoffroy 1810)Saccopteryx bilineata(Temminck 1838) Desmodontinae

Noctilionidae Desmodus rotundus (E. Geoffroy 1810)Noctilio leporinus (Linnaeus 1758) Diphylla ecaudata Spix 1823

Mormoopidae NatalidaeMormoops megalophylla (Peters 1864) Natalus stramineus Gray 1838Pteronotus davyi Gray 1838 VespertilionidaePteronotus parnellii (Gray 1843) Eptesicusfurinalis (d'Orbigny 1847)

Phyllostomidae Lasiurus blossevillii (Lesson & Gamot 1826)Phyllostominae Lasiurus ega (Gervais 1856)

Chrotopterus auritus (Peters 1856) Lasiurus intermedius H. Allen 1862Micronycteris megalotis (Gray 1842) Myotis keaysi J. A. Allen 1914Mimon bennettii (Gray 1838) Rhogeessa aeneus Goodwin 1958

Glossophaginae MolossidaeGlossophaga soricina (Palias 1766) Eumops bonariensis (peters 1874)

Carolliinae Eumops glaucinus (Wagner 1843)Carol/ia perspicillata (Linnaeus 1758) M olossus ater E. Geoffroy 1805

Stenodermatinae Molossus sinaloae J. A. Allen 1906Artibeusjamaicensis Leach 1821 Nyctinomops laticaudatus (E. Geoffroy 1905)Artibeus lituratus (Olfers 1818) Promops centralis Thomas 1915Artibeus phaeotis (Miller 1902)

85H. T. Arita

sition. Species in the study afea are classified intocategories defined by some criterion (taxonomic, eco-logical, behavioural) and the frequency distributionof species among the categories in the derived fauna(s)is then compared against the null distributionobtained by randomly sampling from the pool. If sig-nificant differences are found, the possible forces thatwould have produced such deviations can then beconsidered (Harvey et al. 1983).

The structure ofthe bat fauna ofYucatan was com-pared with that of the pool using four classificationcriteria: taxonomy, diet, roosting preferences and dis-tributional range. Additionally, the species-to-genusratio in the source pool and the Yucatan fauna werecompared to examine further the structure of the batfauna.

To do the comparisons based on taxonomy, dietand roosting habits, sampling without replacementfrom the pool was simulated using the hypergeometricfrequency distribution (Hastings & Peacock 1975;Graves & Gotelli 1983). Species in the pool were div-ided into fami1ies and, for the diverse family Phy1-lostomidae, into subfamilies (Table 1). For feedinghabits, the broad categories used in other studies ofneotropical bats (Table 2; Fleming et al. 1972; Wilson1973; LaVal & Fitch 1977; Bonaccorso 1979; Willig1983; Willig & Moulton 1989) were maintainedbecause the foraging habits of many species are notknown in detail, so a filler classification was not feas-ible. Frugivores included for example Artibeus spp.and Carollia perspicillata, which feed mainly on fruitsalthough they algo consume some insects and, lesscommonly, nectar and pollen. The category offoliagegleaners included species such as Micronycteris mega-lotis and Chrotopterus auritus, which capture insectsor vertebrates from a substrate. In contrast, aerial

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Ecology, 66, 83-97

insectivores, such as Myotis keaysi and Natalus stra-mineus, capture flying insects on the wing, frequentlymanoeuvring near dense vegetation. Fast-flying insec-tivores members ofthe family Molossidae algo captureflying insects, but they do so by pursuing their prey athigh speed in open spaces. The diet of nectarivores isbased on nectar and pollen, although the sole member

Table 2. Expected and observed values for the number ofspecies in taxa and feeding categories of bats of Yucatan.Probabilities are two-tailed exact probabilities of deviations> observed, calculated using the hypergeometric distri-bution. Expected number of species was based on the pro-portions in the source pool

Species inYucatan Expected P

TaxaEmballonuridaeNoctilionidaeMorrnoopidaePhyllostominaeGlossophaginaeCarollinaeStenoderrnatinaeOesmodontinaeNatalidaeVespertilionidaeMolossidae

Feeding categoriesFrugivoresGleanersAerial insectivoresFast-fiying insectivoresNectarivoresVampiresPiscivores

2.250.451.806.291.800.904,941.350,455.844.94

1.000.450.320,070.620.201.000.580.451.000,53

5.846.29

10.334.941-801.350.45

1-000-070-45O-530-62O-580-45

ofthis group in Yucatan (Glossphaga soricina) is actu-ally an omnivorous species. The two species of vam-pire bats that occur in Yucatan (Desmodus rotundusand Diphylla ecaudata) feed exclusively on vertebrateblood. Finally, Noctilio leporinus, the only piscivorousspecies in Yucatan, feeds almost exclusively on smallfish, which it captures from the surface ofwater usingits elongated claws.

The classification of Mexican bats in terms of caveuse proposed by Arita (1993b) was used to test forroosting preferences. Species in the pool were allottedeither to the category of cave bats (species that usecaves as the mairi 9r alternative diurnal roosting sites)or non-cave bats (species that do not use caves or thatuse caves occasionally). Using a BASIC program based

on the formulae provided by Graves & Gotelli (1983),exact probabilities were computed for the deviationof the Yucatan fauna from distributions created byrandom sampling from the pool.

To quantify the afea of distributional range for eachspecies in the pool, its presence or absence in eightdiscrete zoogeographical afeas of the neotropics wasrecorded: (i) the Pacific versant in western Mexico(Ceballos & Miranda 1986); (ii) the Gulf of Mexicoversant in north-eastern Mexico (Hall 1981; Ramirez-Pulido et al. 1986); (iii) the West Indies (Koopman1990); (iv) thenorthern Neotropics (Eisenberg 1989);(v) the Amazon basin; (vi) eastern Brazil; (vii) thePacific versant of South America; (viii) the Patagonia(these last four afeas as defined by Koopman 1983).For each afea in which a species was present, onepoint was added, so a given species could have anyvalue from O (endemic to the Yucatan península andits pool) to 8 units (present in all afeas). The use ofthis scale provides a better resolution than the binaryclassification (widespread vs. restricted species) thathas been used in other studies. For species in the pool,the frequency distribution of the number of occupiedgeographical afeas was approximately normal, allow-ing the null hypothesis that the Yucatan fauna doesnot differ in terms of dispersal ability of its constituentspecies, to be tested by using the statistical distributionof the mean of samples from finite populations(Freund & Walpole 1987).

Several studies have shown that communities withlower species richness tend to have fewer species pergenus (SjG) than richer assemblages (Jiirvinen 1982;Harvey et al. 1983). It can be shown statistically, how-ever, that communities with few species have lowerSjG ratios simply because of their smaller sample sizecompared with that of more complete communities.In fact, real assemblages tend to have higher SjGratios than expected on the basis of adequate samplingmodels (Simberloff 1970; Gotelli & Abele 1982; Jiir-vinen 1982). A BASIC program was developed to cal-culate the expected value and the variance for the SjGratio ofthe Yucatan fauna, using rarefaction formulaebased on the hypergeometric distribution (Heck, vanBelle & Simberloff 1975; Simberloff 1978).

86Bat fauna ofYucatan, Mexico

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Ecology, 66,83-97

MORPHOLOGICAL COMPARISONS

In what is known as the ecomorphological approach,morphological traits of organisms are used to inferecological features ofthe species (Karr & James 1975;Wainwright & Reilly 1994). This approach has beenused extensively for studying the structure ofbat com-munites, as the correlation between ecology and mor-phology is well established for chiropteran species(Findley & Wilson 1982; Findley 1993; Norberg 1994).The bat fauna of Yucatan was analysed using theecomorphological approach by comparing the dis-tribution of the species of Yucatan in morphospacewith that of the source pool to provide a test for thenull hypothesis that the derived fauna is a randomsubsample of the pool.

Museum skins and skulls deposited in the collectionof the National University of Mexico (UNAM) wereexamined, including specimens for all bat species inthe pool. Five external and five skull measurementswere recorded for each specimen. Length of the fore-arm is a measure of overall size. Wing tip length,including the lengths of the metacarpal and the phal-anges of the third digit, and length of the fifth digitcorrelate with wing span and wing width, respectively.Length of the tibia measures the size of the uro-patagium in those species that have one. Length ofthe ear is an indicator of auditory and echolocationcapabilities in bats (Fenton 1972; Arita 1990). Thegreatest length of the skull, depth of the brain case,and mastoid breadth quantify the size of the skull inthe three dimensions, whereas length of maxillarytooth row and width at the level of the last molarsmeasure the size of the trophic apparatus. All vari-ables except length of ear were measured directly frommuseum specimens; length of the ear was recordedfrom the collectors' tags. Adult specimens both fromthe pool afea and from Yucatan were measured. Formost species reported from Yucatan, the sampleincluded at least five males and five females from eachafea. For a few very rafe species, such as Phyllostomusstenops, only one or few specimens were availablefrom the afea of study.

Preliminary analyses showed little sexual or geo-graphic variation in size as detected by univariate andmultivariate analyses of variance (ANOVA andMANOV A). Differences between sexes or between thestudy fauna and the pool were significant in only asmall proportion of cases with sufficient sample sizes(five of 52 for sex differences, four of 18 for geographicvariation). Given these results, averages were used foreach species, regardless of sex or locality.

Univariate analyses

Several parameters were used to measure the regu-larity of the distribution of species along a mor-phological gradient to compare the Yucatan assem-blage with the pool (Simberloff & Boecklen 1981;

87H.T. Arita

Pleasants 1990, 1994; Arita 1993a). For an assemblageof n species arranged along a logarithmic size gradient,let X; be the 10g value of the size of the ith species, soXI corresponds to the smallest and Xn to the largestspecies. Define di to be equal to Xi+ 1 - X;, the distancebetween adjacent species. The parameter Var (Poole& Rathcke 1979) is the variance of the values of d:

Var = (n-2)-1

Min is the minimum value of d, that is the magnitudeof the shortest segment of the morphologicalline.

If distances are arranged in increasing order of mag-nitude and they are renamed so g¡ becomes the shor-test and gn-l the longest distance, the G parametersof SimberlotI & Boecklen (1981) can be defined asfollows: Gr.s = gr/gs (the ratio of the rth smallest tothe sth smallest segments of the morphologicalline).SimberlotI & Boecklen (1981) proposed the use ofthree of these ratios (G¡.n, G2.n and G¡.n-l) to testHutchinson's (1959) hypothesis of size-ratio con-stancy. Pleasants (1990) has argued deficiencies in theG parameters, but Arita (1993a) has shown otherwise,and the efficiency of these parameters in detectingcharacter displacement has been demonstrated inrecent papers (Dayan et al. 1989, 1990).

A preliminary analysis was performed to search forunusual morphological dispersion in the pool. If thepool itself is organized in any manner, detecting anadditional structure in a sample can be a misleadingexercise (Colwell & Winkler 1984). Tests were madein four ofthe feeding categories (frugivores, gleaners,aerial insectivores and fast-flying insectivores) for oneexternal (forearm length) and one skull (length of thetooth row) variable. Species were arranged by theirsize and the morphological distances were calculated,using a logarithmic scale, for contiguous species. Bymeans of a BASIC program, parameters of dispersion(Var and Min) were computed and the values werecompared against hypothetical faunas generated bysampling from a random uniform distribution. Foreach feeding category, 1000 simulations were ron.

A similar test was performed for two of the mostspeciose genera in the pool: Artibeus, with four species,and Myotis, with six species. The tests using these twogenera were performed to have a better resolution inthe question of a possible pattern of unusual mor-

phological dispersion. Traditionally, such tests aredesigned to study closely related species, normallybelongingto the same genus (Hutchinson 1959; Dayanet al. 1989, 1990).

Unusual dispersion was tested in four ofthe feedingcategories ofYucatan bats (frugivores, gleaners, aerialinsectivores and fast-flying insectivores). Sample sizeswere insufficient for the piscivorous (n = 1), vampire(n = 2) and nectarivorous (n = 1) groups. For each

category, morphological gradients were created foreach of the 10 log-transformed variables definedabove. Then, using a BASIC program, the parameters

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for dispersion (Var, Min and the G parameters) werecomputed and the values were compared against afrequency distribution of hypothetical communitiesgenerated by randomly sampling the pool. Por thegleaner and the fast-flying insectivore groups, the pro-gram generated all possible assemblages of the samenumber of species as in the Yuca tan fauna (364 poss-ible combinations of three-species assemblages froma pool of 14 gleaner species; 462 possible combinationsof six-species communities from a pool of 11 molos-sids). Por frugivores and aerial insectivores, IODO ran-dom assemblages were created. (Por frugivores, therewere 1716 possible combinations of six species from apool of 13; for aerial insectivores, with a pool of 23species, > 1.35 x 106 assemblages of 12 species werepossible.) The null hypothesis is that species in thereal communities are not particularly segregated alongthe morphologicalline. One-tailed probabilities wereestimated by comparing the observed values of thefive parameters against the distribution obtained fromthe hypothetical assemblages generated from the pool.

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Multivariate tests

The multivariate analysis of structure in ecologicalcommunities is a direct extension of the univariatecase. The procedure involves the study of the relativeposition of the different species in an n-dimensionalmorphospace that is assumed to mirror the mul-tidimensional ruche space (Karr & James 1975; Fin-dley 1976; Ricklefs & Travis 1980; Ricklefs, Cochran& Pianka 1981; Findley & Black 1983; Moulton &Pimm 1986; Willig & Moulton 1989; Ricklefs & Miles1994). Using skull and external measurements, mul-tivariate analyses for each of the feeding groups wereperformed. Principal-components analysis of the log-transformed data was used to reduce the dimen-sionality ofthe morphospace. Because they accountedfor most (> 90%) of the variance of the original vari-ables, only the first two components were retained inall cases. Principal components were extracted fromthe correlation matrix and Euclidean distances werecomputed for each of the n(n-l )/2 pairs of species inthe plane of the first two principal components.

Mean neighbour distances and variances were usedto quantify the spacing of the elements of the assem-blages. In previous studies, only the nearest-neighbourdistances were normally used. However, a completeseries of means and variances for the different ordersof nearest-neighbours, as defined by Manly (1991),were calculated for the bats ofYucatan. For an assem-blage of n species, q¡ (i = 1 to n -1) is defined asthe mean distance from points to their ith nearestneighbour. The first-order mean distance (qt) is equalto the nearest-neighbour distance used in previousstudies to quantify species packing in the community(Findley 1976; Ricklefs & Travis 1980; Travis & Rick-lefs 1983).

As defined here, qt tests for patterns of competitive

exclusion. An unusually high value for this parameterwould indicate a lowered frequency of pairs of verysimilar species in the derived fauna, suggesting theeffect of exclusion of competing species. Parametersfor higher orders test for patterns of segregationamong more distant species. High values for theseparameters would show displacement among specieswith less similarity, indicating the effect of a morediffuse competition. Similarly, the variance ofthe dis-tances for the different neighbour orders can be usedto quantify the eveness of the distances between spec-ies, therefore testing the idea of a displacement amongspecies in the morphospace.

For each feeding category, the n-l q parametersand their variances were computed and their valuecompared against the frequency distribution compiledfrom 1000 randomly generated communities from thepool. Under the competition hypothesis, q-valuesshould be significantly higher and variances shouldbe significantly lower than expected by chanceo One-tailed probabilities were used for testing the nullhypothesis of no segregation.

In an additional battery of tests, a series of par-ameters that are analogous to those used in the univ-ariate analyses were computed. First, a minimumspanning tree in the plane of the first two principalcomponents was constructed for each feeding cate-gory. The minimum spanning tree is the series of n-lsegments connecting all species in the community thathas the minimum extension. The length of this treehas been used to quantify the dispersion of species inthe morphospace (Moulton & Pimm 1986; Willig &Moulton 1989). Using the lengths of the segments inthe trees as the lengths of the morphologicallines inthe univariate cases, the same variables (Var, Min andthe G parameters) were calculated. Although similar,these parameters are not exactly equivalent in theunivariate and the multivariate cases. In the univariateanalyses the segments are arrayed along a line,whereas in the multivariate case they are arranged inmultidimensional space (in the present study, on a

plane).An additional parameter, Mean, which is the mean

distance between pairs of species along the minimumspanning tree, was used. In contrast with the univ-ariate case, in which its value is determined by theposition of only two species (Arita 1993a), Mean is avalid parameter in the multivariate case. Mean mea-sures the dispersion of the species because it is directlyproportional to the totallength ofthe minimum span-ning tree.

88Bat fauna ofYucatan, Mexico

Results

TESTS FOR COMPOSITION OF THE FAUNA

There was almost no deviation of the proportion ofspecies in the different taxonomic groups from theexpected values. In fact, most taxa were represented

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by the number of species that would be expected in arandom draw from the source pool (Table 2). In thepresent study, the traditional classification of Phyl-lostomidae in six subfamilies was used (Smith 1972;Hill & Smith 1984). Baker, Hood & Honeycutt (1989)have proposed a new arrangement that summarizesrecent information on the phylogeny of this diversefamily. The results were not affected if the new classi-fication was used, because the majar groups !emainintact in the new arrangement, changing only theirhierarchy from subfami1ies to tribes. The only taxo-nomic group that would yield different results is thePhyllostominae, which Baker el al. (1989) and vanden Bussche & Baker (1992) have split into four sub-families. The subfamily Vampyrinae in the new classi-fication would be represented in Yucatan by one spec-ies out of three from the pool, whereas the tribe Phyl-lostomini would be represented by one of the eightspecies in the pool. In both cases the deviation fromthe expected number of species is not significant(P > 0.05).

Similarly, there was little deviation from expectedvalues in the observed number of species grouped byfeeding categories (Table 2). All groups were rep-resented in the Yuca tan fauna proportionally to theirfrequency in the pool.

Of the 69 species in the pool, 31 (45%) roost incaves. In Yucatan, 17 out of 31 use caves regularly(55%; Arita & Vargas 1995). The expected number ofYucatan cave species based on a random draw fromthe pool is 14.78. The hypergeometric probahility ofdrawing 17 or more cave species from the pool in asample of 31 is P = 0.197. Thus, the apparent over-

representation of cave species in the Yuca tan fauna isnot statistically significant, and no difference can beclaimed.

The mean number of zoogeographical units inwhich a species from the pool occurred was 4,26, witha variance of3.65. The observed mean for the Yuca tanfauna was 5,35 units with a sample variance of 2.92(Fig. 1). The probability of observing a mean > 5.35for a sample of n = 31 is very low (z = 4,26,

P < 0.001). The null hypothesis was c1early rejected;species with larger afeas of distribution were over-represented in the bat fauna ofYucatan.

Analysis of the species-to-genus ratio provided noevidence of any deviation from random samp1ing fromthe source pool. The expected number of genera in a31-species sample from a pool of 69 species in 44genera is 24.52. The observed value for the Yucatanfauna was 24 genera (probability of a deviation >observed is P > 0.05).

MORPHOLOGICAL COMP ARISONS

Preliminary analyses

Almost no evidence of any unsual morphological pat-

tern was found in the preliminary analysis ofthe pool.

89H. T. Arita

1 2 3 4 5 6 7 8

Zoogeographical areas

Fig.l. Frequency distribution of the afea of distributional range for bat species in the pool and the Yucatan fauna. Zoogeo-graphical afeas are defined in the texto The mean for the Yucatan fauna differed from the expected value (P < 0.001).

In all cases (frugivores n = 13; gleaners n = 14; aerialinsectivores n = 23; fast-flying insectivores n = 11)

results were not significant (P > 0.05) for both fore-arm length and length oftooth row. In the analysis ofthe genus Myotis (n = 6), a similar result wasobtained; no significant pattern was found for forearmlength or for length of the tooth row. For Artibeus,only the analysis for forearm length using the Minparameter was significant (P = 0'03).

Univariate analyses

The results revealed little evidence for segregation ofbat species along univariate morphological gradients.In the guild of frugivores, for example, there wasno significant deviation from expected for any of theparameters in any of the variables (in all casesP > 0.05; Table 3. Similarly, for the group of gleaners,none of the external variables indicated a~y tendencyto morphological segregation (all cases P > 0.05).Only two parameters suggested segregation for maxil-lary tooth row and for mastoid breadth (P < 0.05).

In the category of aerial insectivores,only one ofthe 10 variables (mastoid breadth) showed an indi-cation of a regular arrangement of species. For thisvariable, parameters Min and G¡,(n-¡) deviated sig-nificantly (P < 0'05) from their expected values, butthe other parameters did noto Among fast-flying insec-tivores, one variable (width at the level of the lastmolars) showed an isolated significant deviation(P < 0,05 for GZ,n), and the parameters for another(greatest length of skull) were significantly (P < 0'05)different from that expected.

Multivariate tests

As with the univariate analyses, multivariate testsshowed little evidence of any structure in the fauna ofbats of Yucatan. Mean Euclidean distances in theplane of the first two principal components revealedno significant pattern in the guilds of gleaners, aerialinsectivores and fast-flying insectivores-iFig.2). AIIvalues were within the 95% confidence interval deter-

(Q) 1997 British

Ecological Society,Journal o/ Animal

Ecology, 66, 83-97

20

(/)Q)

'uQ)c.(/)

'O

~.cE:J

Z

15

10

5

mined by random sampling from the pool. In theaerial insectivore group, the mean Euclidean distancesfor the first three orders were very close to the upper5% limit, suggesting a tendency of similar species notto coexist in the Yucatan fauna, but the pattern wasstatistically not significant. In the guild of frugivores,q-values tended to be higher than expected, with threeof them (qb q3 and q4) being significantly so (one-tailed P < 0'05; Fig. 2). In the case of the variance ofthe distances, all values for all guilds for all neighbourorders were within the expected values with a 95%confidence.

The analysis of the minimum spanning trees yieldedsimilar results, and demonstrated no tendency foroverdispersion or segregation. None of the values forany of the parameters was significantly different fromexpected in any of the cases (Fig. 3 and Table 4).

Discussion

SPECIES COMPOSITION

The results of comparisons based on species com-position indicate that the study fauna is a randomsubsample of the pool in terms of taxonomic com-position, feeding strategies and roosting preferences.Dispersal ability, measured by the size of dis-tributional range, is the only characteristic thatdifferentiates the fauna of Yucatan from its source.

This result dismisses the significance of some pat-terns of the Yuca tan fauna that would seem to bestriking. For example, Phyllostomines are representedby 14 species in the pool and by only three in theYuca tan fauna. Even in this case, however, the devi-ation from expected was not statistically significant(P > 0.05). In a similar case, only one ofthe six speciesof the genus Myotis that exist in the pool was presentin Yucatan (M. keaysi), and the peninsular fauna har-boured only one nectar-feeding bat (G. soricina).Other tropical afeas of Mexico normally contain sev-eral species of Myotis and many nectarivorous species(for example, the tiny state of Colilla in western Mex-ico contains six Myotis species and five Glos-

Table 3. One-tailed probabilities for parameters ofmorphological displacement for the bat fauna ofYucatan. For G parametersand for Min, probabilitiesareforvalues > than observed. For Meanand Var, probabilitiesare for values < observed. FA,length of forearm; TIP, length of the metacarpal and phalanges of the third digit; D5, length of fifth digit; EAR, length of ear;TIB, length of tibia; GLS, greatest length of skull; MTR, length of maxillary toothrow; DBC, depth of brain case; MB,mastoid breadth; MM, width at the level of the last molars

FA TIP D5 EAR TIB

Frugivores (1,000 simulations)Mean 0.323 0.204 0.421 0.190 0.536Var 0.707 0,784 0.698 0-701 0-701Min 0-417 0-808 0-533 0-279 1.000G1. 0.423 0-874 0.669 0-442 0.924G2,n 0-499 0-974 0-885 0-425 0-636GI,<n-l) 0-532 0,980 0-700 0.665 0-923

90

Batfauna ofYucatan, Mexico

@ 1997 British

Ecological Society,Journal o/ Animal

Ecology, 66, 83-97

GLS MTR DBC MB MM

Mean 0.186Var 0.568Min 0,055

G1,n 0,172G2,n 0.434Gl,(n-l) 0.105

FA

Gleaners (364 simulations)Mean 0.115Var 0-396Min 0-107

G1,n 0.236G2,n 1.000Gi,(n-l) 1.000

GLS. ",

Mean 0.288Var 0.113Min 0.110G1,n 0.077G2,n 1.000G1,<,!, 1) 1.000

0.2940.1990.0500.0500.2230.074

0.3060.5250.1520.1990.3820.330

EAR

0-2170-6720.6640-8470-4270.815

TIB

0.1620.7240.2370.3080,3490.248

TIP D5

0.1150.4590.0850.2561-0001-000

DBC

0.2250-4530.1590.2861.0001.000

MTR

0-1730-9010-5060-7311-0001-000

MB

0.1730.1480.0710.1071-0001.000

MM

0.4120-036*0.1100,019*1.0001-000

0.2580.1460.0520.0961.0001.000

0.1570.0710.036*0.038*1.0001.000

0-1870-6650-2450-4591-0001-000

TIBFA D5 EAR

Aerial insectivores (1,000 simulations)Mean 0-518 0-787Var 0-388 0-276Min 0-596 0-077G'_n 0-584 0-061G 0-747 0-2252..G.,(n-l) 0,475 0,052

0,5500.8250.0950.1660.4330.166

DBC

0.3940.3831.0000.8480.7030.940

MB

0-2600-4880-5500-4670-6220-629

MMGLS MTR

MeanVarMin

G'.nG2-,G'.(n-'}

0.4830.6900.3740.4330.5440.526

0.4050.6831.0000.9020.5460.939

0,460

0.3970,0870,0740.1970.237

0.4030.4500.030*0.0580.1170.033*

EAR

0.5890-1240.0740-0720-1620.046

TIBFA D5

Fast-fIying insectivores (462 simu1ations)Mean 0.695 0.771Var 0.106 0.219Min 0.448 0.275

G¡.n 0.442 0-063G2,n 0.212 0.167G¡.,(n-.l) 0.537 0.188

0.5500.0580.3940-1260.1880.247

0-3940-5740-8180-8180-8850-818

0.2600.1780,5460-3790.2210,348

91H. T. Arita

sophaginae in a fauna of 47 bats; Ramírez-P. et al.1986). Rarefaction demonstrated that the patterns inthe Yucatan fauna are not as unexpected as they seemto be. In fact, the hypergeometric probability of get-ting one or no Myotis in random 31-species samplesfrom the pool is P = 0.15.

Feeding categories coincide closely withthe taxo-nomic arrangement ofneotropica1 bats. For example,molossids are in their own feeding group, the gleanersare in the subfamily Phyl10stominae, and all fru-givores are classified in the subfami1ies Carol1inae andStenodermatinae. Comparative studies of neotropicalbat faunas face the unavoidable mixing of ecologica1effects and phylogenetic inertia (Fe1senstein 1985;Harvey & Pagel 1991; Brooks & McLennan 1991).Not surprising1y, the analysis using feeding groupsyielded similar results to the one performed with taxo-nomic groups.

The karst landscape ofYucatan, a flat terrain punc-tuated by numerous caves, would lead one to expectcave bats to occur in a higher proportion than in thesource pool, where caves are less abundant. The cavebat fauna of Yucatan is indeed rich and abundant,with individual sites harbouring as many as 12 differ-ent species (Arita & Vargas 1995). However, theapparent overrepresentation of cave species in theYucatan bat fauna (17 of31 species) is not statistically

significant.The afea of distributional range is the only feature

that discriminates species from the pool that occur inYucatan. If one assumes, as Graves & Gotelli (1983)have done, that afea of distributional range is a mea-sure of dispersal capability, the results presented herewould indicate that colonization ability is the keyfactor determining the particular combination of spec-ies that constitute the study fauna. However, thatcould al so be a subtle indication of other forces struc-turing the fauna. Widespread species might havelarger distributional ranges because they are superiorcompetitors, capable of excluding other species inimpoverished afeas. Conversely, species with smalldistributional ranges would be poor competitors,restricted to rich afeas in which competition might beless strong. Similarly, there is a positive correlationbetween afea of distribution and local abundance forneotropical bats (Anta 1993c), suggesting that the batfauna of Yucatan might be formed by proportional

(!:;) 1997 British

Ecological Society,Journal of Animal

Ecology, 66, 83-97

Table 3. (Continued)

GLS MTR DBC MB MM

0.4240.1620.6210.4130.043*0.448

0.5000.7510.5450.7880.4830.695

0-4130-3790-2490-2340-3960-214

0.6190.1020.2750.0910.1650.126

Mean

Var

Min

G1,n

G2,n

G1-<""'J

0.5760.002**0.028*0.002**0.004**0.012*

* P < 0.05, ** P < 0.01.

sampling from the pool, with species that are moreabundant having higher probabilities ofbeing presentin the study fauna.

Graves & Gotelli (1983) and Jarvinen & Haila(1984) have obtained comparable results withavifaunas. Species of neotropical birds with the largestdistributional ranges are more likely to be found inland-bridge islands than restricted species (Graves &Gotelli 1983). Sirnilarly, 33% of the absences of birdspecies in the Finnish island of Ulverso can beaccounted for by initial rarity in the source pool. Inthe short term, that percentage is as high as 75%(Jarvinen & Haila 1984). In these avifaunas and in theYuca tan bat fauna, initial rarity and dispersal abilityseem to be the key features that allow species to occurin the study sites.

MORPHOLOGICAL COMPARISONS

Preliminary analyses performed on the pool found noorganized pattern in this fauna. Because the majorpurpose of this study was not to examine the poolfauna, the results of these preliminary analyses wereused only to validate the comparison of the local andregional faunas. If a clear partero of organization isfound for the pool, then the following analyses wouldbe invalid, because the power of the tests to show amore organized partero would be impaired by thestructured nature of the pool itself. For the Yucatanbat fauna, however, it seemed gafe to perform thecomparisons with the pool.

The idea of an almost random construction of theYucatan bat fauna is supported by the lack of evidenceof segregation provided by the morphological tests.Most analyses yielded ambiguous results that allowedno definite conclusion about the morphological struc-ture (if any exists) of the Yucatan bat fauna.

In the guild of frugivores, for example, both univ-ariate analyses and the analysis ofthe minimum span-ning trees showed almost no evidence for unusualpatterns. Only one variable (depth of brain case), forwhich the Min and G¡,n parameters detected somesegregation among the species (P = 0.05), indicatedsome degree of separation. Dayan el al. (1989, 1990)have shown that, for a given group of species, seg-regation can occur in a measurement, whereas othersmar show a great deal of overlap. They found that

92Bat launa 01Yucatan, Mexico

2

O

1 2 3 4 5

Nearest neighbour arder

Fig.2. Mean nearest-neighbour Euclidean distances in four guilds of bats. Points show values for the Yucatan fauna. Lines

are upper and lower 5% limits for expected values obtained from the pool.

segregation in size occurs in carnivores principallyalong the line of the diameter of the upper canines, avariable directly associated with the trophic apparatusof carnivorous animals. In the case of the frugivorousbats of Yucatan, a segregation along the line of thedepth of the brain case has no such direct interpret-ation. Besides, the pattern was not shown for thevariables associated with the trophic structures.

cg 1997 British

Eco1ogical Society,Journal o/ Animal

Ecology, 66,83-97

6

5

4

3

2

1

O

FrugivoresQ)"ClO:n'5~O

.oJ:Q)

"O;c

:nQ)(ijQ)z

t51 2 3

Nearest neighbour arder

4

(b)8

6

4

2

O

GleanersQ)ucm..,:o

~o

.c-'=C)

"o;c

..,Q)(ijQ)Z

21

Nearest neighbour arder

6 Aerial insectivores'"uc:tU'in'6

~o.Q.c:Q)"o;c:

'in'"(ij'"z

4

2 tr,,o

7 81

Nearest neighbaur arder

Fast-flying insectivores8Q)ucro'00'ti

~o

.c

.cC>

"Qjc

'00Q)C5Q)

z

6

4

In the multivariate analyses for frugivores, thevalues of the q parameters suggested, but failed toclearly demonstrate, the exclusion of pairs of verysimilar species. In this particular case the analysisshowed a more subtle segregation of species on themorphological planeo That q¡ was not significantlyhigher than expected means that pairs of very similarspecies do coexist in the Yucatan fauna. Significant

93H.T. Arita

-0.4

-0.8-3 -1 1 3 5

Principal component 1

Fig.3. Projection of bat species of four feeding groups on the plane of the first two principal components for skull variables.Lines are minimum spanning trees connecting Yucatan species. Oren circles are species from the pool not found in Yucatan

~ 1997 British

Ecological Society,Journal o/ Animal

Ecology, 66, 83-97

(a) Frugivores1

oN

'CQ)cOc.

Eo(.)

"iijc."¡¡c"¡:a.

-1

-2

-3

2 3 4 5-3 -2 o 1

Principal component 1

o.~oo

"-~--J

0.5 Gleaners

N

EQ)coQ.Eo(.)

mQ.'(3.S;.t

o

-0.5

2 4 6-4 -2 oPrincipal component 1

(c) Aerial insectivores2

N

C.,c:Oc.Eou

"¡ijc.'".s~

1

.~.o

.1

5-3 -1 1

Principal componen! 1

0.8 Fast-flying insectivores/ .~./. o ~N

EQ)~oO-

Eou

"iOO-.5.s.t

0.4

ooo

that shows the bat fauna of Yucatan as a randomsubsample of the pool in terms of species composition

That almost no unusual pattern can be shown forthe bats of Yuca tan when compared with randomassemblages from the pool does not mean that thestudy fauna lacks order altogether. One could arguethat some partero might be already present in thepool, and that the Yuca tan fauna simply cannot bemore organized than itssource (see similar argumentsin Colwell & Winkler 1984). Ifthis is true, any attemptto showa more conspicuous pattern in the Yucatanfauna would be a futileexercise.

In any case, the results of this study suggest thatlocal processes, and particularly competition, have aminor contribution to1hestructuring of the Yucatanbat fauna. It appears that regional processes havea more determinant effect on the composition andstructure of bat assemblages in Yucatan. Dispersalability seems to be the key characteristic of Yucatanbats; thus, historical events of colonization, and notlocal processes, probably hold the key to the under-standing of this and other neotropical bat com-munities.

95H.T. Arila

Acknowledgements

An early version of this manuscript was part of mydoctoral dissertation at the University of Florida,Gainesville. S. R. Humphrey, P. Feisinger,J. F. Eisen-berg, K. H. Redford and J. Reiskind provided usefulcomments. G. Ceballos, C. Martínez del Río, R. A.Medellín and J. Ortega commented on specific partsofthe project. Funding was provided through a schol-arship from the National University of Mexico(UNAM), a grant from the American Society ofMammalogists, and support from the University ofFlorida's Tropical Conservation and Development

Programo

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