Ecology

of

a Snake

Community

in Northeastern

Brazil

Laurie J. Vitt, and Larry D. Vangilder1 BiologyDepartment, University of California,Los Angeles, CA 90024USA and Savannah River Ecology Laboratory,P.O. Drawer E, Aiken, SC 29801USA

Abstract. Nineteen speciesof snakesrepresenting four familieswere simultaneouslystudied in a caatinga habitat of northeastern Brazil. Of these, 10are terrestrial, 3 are terrestrial-aquatic, 1 is arboreal-terrestrial, 4 are arboreal, and 1 is terrestrial-fossorial.Four speciesare nocturnal, 5 speciesare nocturnal and diurnal, and 10are strictly diurnal. Diets include mammals,birds, bird eggs, lizards,snakes, frogs, toads, and reptile eggs,with some snake speciesbeing foodspecialists andothers being foodgeneralists.Surprisingly, none of the species of snakes at the study site feed on invertebrates. A diversity of reproductive tactics is evident among the species in this snake community.There are oviparous andviviparous species, and clutch/brood size may be large or small depending upon the species. Both clutch/brood size and neonate (or egg) size were correlated with body size of female snakes. A principalcomponents analysis (PCA) morphological data revealedthat twoaxes,one representing of variation in body size and one representing variation tail lengthand head size, explained 95% in ofthe variation in the data. Portions of the morphological results corresponded well with ecological data. However, in some instancesthe morphologicalresults were discordantwith ecologicalresults. Certain patterns, for example appear to have a phylogenetic basis. It is concluded that morphological analyses of snake communities cannot be adequately interpreted in the absence of ecologicaldata.

Introduction Recent descriptions of ecological relationships of South American reptiles and amphibians have demonstrated the diversity of morphological, ecological, behavioral, and reproductive adaptations within and among populations of these poorly known faunas (for example seeD?xoN andSoiNi, 1975,1976; CRUMP, 1971; DUELLMAN,1978). For logistic reasons (a given tropical reptile and amphibian community may contain well over 100 species) it is often difficult to obtain more than cursory information on ecology of components of such communities. Identifying the fauna and working out taxonomic relationships necessary for interpretation of biogeographical patterns has been and continues to be a major task in itself(D UELLMAN 1979). Moreover, the modification of many tropical habitats by man and the associated loss of natural habitat is occurring at such a rapid rate that biologists may not find natural faunas to study in the near future (ANTONYMous, 1980). In this paper a portion of the results of a year-long study on ecology of lizards and snakes in a caatinga habitat of northeastern Brazil is presented, focusing on the snake com1 Present Address of L.D. Vangilder: Patuxant Wildlife Research center, USFWS, Laurel, MD 20708USA

274 munity. Lizards will only be mentioned as they affect snakes, either as prey or predators. Because of differences in abundance and catchability of snake species, the data vary from nearly complete to ancedotal. Nevertheless, a general picture of the structure of this snake community results. Previous papers by V ANZOLINI1974,1976) and VANZOLI( Ni et al. (1980) have described the fauna, but not all of the snakes occurring in caatinga habitats occurred at the study area. We first present data summaries on habitats, activity patterns, and foods of the nineteen species of snakes occurring at the study site. We then provide morphological data on the species including a multivariate analysis of the morphological data. Additionally, information on life history characteristics measured is presented. The primary focus is on the integration of ecological and morphological data in examining the structure of the snake community. Similar approaches have been used for rodents (BROWN, 1975), birds (DIAMOND, 1975; RICKLEFSand TRAVIS, 1980) and lizards (RICKLEFSet al., 1981).

Methods Study area and climate. - Field work was carried out within 20 km of Exu, Pernambuco (725'S latitude x 4010'W longitude), in the semi-arid northeast of Brazil (Reis, 1976). This site is near the geographic center of the "zona da caatinga" (L IMA,1960; V AscoNCELos, 1941). This locality is of particular interest in terms of studying reptilian ecology because it is the largest dry region entirely contained within the tropics, being surrounded by mesic habitats. To the east, caatinga meets Atlantic forest, the remainder coming into contact with cerrados. Often, the contact areas are complex and at least in the case of caatinga - cerrado contacts, may consist of "a mosaic of interdigitations and mutual enclaves" (V ANZOLINI, 1974, p. 61). Enclaves of forest occur within caatinga and these contain isolated communities consisting of subsets of the fauna and flora of tropical forest. These "refugia" have recently become of great interest in a biogeographic context (VANZOLINI,1980, 1981; VANZOLINIand WILLIAMS, 1981; WILLIAMSand VANzoLINI, 1980). There is no endemic snake fauna of caatinga, rather, the snake community consists of subsets of cerrado and Atlantic forest communities. The morphological and ecological diversity as well as the relatively high abundance of many species renders the caatinga snake community particularly amenable to ecological study. A majority of the habitat surrounding the city ofExu consists of Caatinga Baixa (low caatinga) habitats, characterized by xerophytic trees from 3-5 m in height, emergents up to 8 m and a variety of large cacti (Cereus jamacura, Cephalocereus gounellei, and Zehntherella squamulosa) (MARES et al., 1981). Euphorbs and legumes are also common. Granitic extrusions (Lajeiros) interupt the CaatingaBaixa providing refuges for a large number of vertebrates and invertebrates (LACHER, 1981; MARES et al., 1981; VANzoLINI et al., 1980; VITT, 1980, 1981). Climatologically, caatinga is considered semi-arid, receiving 400 to 1000 mm annual rainfall. The actual amount of rainfall and its timing are highly unpredictable and consequently extreme drought or flooding may occur (EIDT, 1968). Thermally, the climate

275 dry season. A more thorough escription of climatic conditions presented elsewhere (VtTT and GOLDBERG, 1983). during 1977-1978 is

Field and laboratory methods. - Snakes were collected by hand, pellet rifle, pitfall traps, drift fences and by placing flat objects on the ground and checking under them each day. In additon, a large number of local youths were paid to collect non-poisonous snakes. Although the latter yielded no information on habitats snakes might use, the snakes did provide data on morphology, size, food, and reproduction. When snakes were observed in the field, notes were taken on habitat and microhabitat, methods employed in foraging or predator escape, and any other biotic attributes deemed important. In certain instances, interactions among species of snakes or between snakes and other vertebrates were observed in the field or the laboratory. Most snakes were killed with nembutal immediately upon return from the field or shortly after being bought. Only a few snakes were kept alive for more than 6 hr following capture. Most of the snakes collected have been deposited in MZUSP, Sao Paulo, Michigan, USA. For each freshly kilBrazil, but a few are housed atUMMZ, AnnArbor, led and relaxed snake, the following morphological measurements were taken: snoutvent length (SVL) to 1 mm, tail length to 1 mm, total mass to 0.1 g, head length (tip of snout to posterior edge of mandible), head width (at posterior edge of mandible), gape (taken by placing a flat edge of dial calipers across the tip of both lower jaw bones, then opening the mouth with the calipers until strong resistance was felt), body width, and body height (at approximately mid-body). The measurements were all to 0.1mm. Following fixation in 10 % formalin, snakes were dissected and data on reproductive condition and stomach contents were recorded. In many instaances, it was possible to identify stomach contents to species. In females, length and width of yolked vitellogenic follicles or oviductal eggs were measured. Data on eight morphological variables (SVL, tail length, body mass, head length, head width, gape, body width, and body height) were transformed to their logarithms (base 10) and principal components (PCA) extracted from the correlation matrix of the log- transformed variables using the SAS procedure FACTOR (H ELmG and COUNCIL, 1979). Principal component axes with eigenvalues greater than unity were retained. The approximate score of each species on each axis was then calculated using the SAS procedure SCORE (HELWIG and COUNCIL, 1979). Results Habitatsand diets. - Two boids, fifteen colubrids, one elapid and one viperid occur in the (Table 1). Of these, 10 are terrestrial, 3 are terrestrial-aquavicinity ofExu,Pernambuco tic, 1 is both arboreal and terrestrial, 4 are arboreal and 1 is terrestrial-fossorial. Four species are strictly nocturnal, 5 species may be active by day or night, and 10 are strictly diurnal. A large majority of snakes collected during this study were in or near Lajeiros, particularly during the dry season when vegetative coverwas reduced. These structurally diverse habitats provide abundant refuges for small vertebrates (Fig. 1). Among these sympatric snakes are species which feed on mammals, birds, bird eggs, lizards, snakes, frogs, toads, and reptile eggs. A breakdown of diet results by species appears in Table 2. Only the genera Clelia, Epicrates, and Philodryas feed on prey in several

276 Table 1. Summary of habitats, activity patterns and foods of snakes in northeastern Brazil.

* Formerly considered Dromicus (DIXON, 1980) **Formerly considered Lygophis(DIXON, 1980) ***Both of these may be new species (R. THOMAS, comm.) but for descriptivepurposes we assign pers. them to T.pallidus and T. strigilis because they appear closest to these.

Fig. 1. Photograph of a typical Lajeiro habitat in the interior of northeast Brazil showing the structural diversity of the habitat available to small vertebrates.

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281 classes. The remainder possess diets restricted to one class. Note also that several snakes (Clelia, Oxyrhopus, Philodryas nattereri, and Pseudoboa) contained lizard tails, evidence of the success of tail autotomy by lizards for escaping predation attempts. At least seven species (Leptophis, T. pallidus, all four Liophis, and Waglerophis) are anuran specialists. Because the diets ofL. lineatus, L. mossoroensis, L. poecilogyrus, W. merremii (VtTT,1983a),P. nattereri, andP. olfersii(VITT, 1980), have been quantitatively compared elsewhere, the analysis is not included here. Female reproduction. - Species producing eggs or offspring nearly year round as well as species with rather restricted breeding seasons are represented among caatinga snakes (Table 3). It is evident that few snakes showed reproductive activity during mid-wet season (March through April) whereas most species were reproductive during all or a portion of the dry season (June through November). Clutch or litter size and egg and/or offspring size varied considerably among species (Table 4), but appears associated with size of adults (Figs. 2 and 3). In this analysis we chose the minimum size of reproductive females as our estimate of female size as it esti-

Table 3. Seasonaloccurrenceoffemale snakescontainingoviductaleggs(0), or enlargedyolkingfollicles (F) and the seasonaloccurrenceof hatchlings collectedin northeasternBrazil.Becausesamplesizesof (H) mature femaleswere small for many of the species(but see VITT, 1980, 1983a), seasonaldistributions the of presence of folliclesor oviductaleggsonly minimallyrepresent the length of the reproduction season.

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of Fig. 2. Relationshipsbetweensize (SVL)of hatchlingsnakesand size (SVL) the smallestreproductive female of the same speciesfor seven caatingasnakes.The correlationcoefficient (r)is 0.91and is signifiare: 3) L. n= cant (p < 0.01, 7). Species included 1)E. cenchria, 2) L, poecilagvrus, viridis,4)L.mossoroensis, 5) L. lineatus, 5 O. trigeminusand 7) P. olfersii.

Fig. 3. Relationshipbetween mean clutch size and size(SVL)at sexual maturity for 16speciesoftropical snakes.The correlationcoefficient(r) is 0.76and is significant(p < 0.01,n= 16).Speciesare: 1)L. viridis,2) M. T strigilis,3)L. lineatus,4)L. mossoroensis, L. poecilogvrus, 6) ibiboboca, 0. trigeminus, P.olfersii, 8) 5) 7) 9) P. nattereri,10)L. ahaetulla, 11) 0. aeneus, 12) W.merremi,13)E. cenchria,14)C. occipitolutea,15)C. durissus, and 16)B. constrictor. mates size at sexual maturity. Also, among females within certain species, clutch size was correlated with body size but these results are presented elsewhere (VITT, 1980, 1983 a). Table 5 summarizes data on snout-vent length, tail Morphological relationships. head length and width, gape, and body width and height. We ignore length, body mass,

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286 sexual differences within species for the multivariate analysis, although these will be examined below. Two axes, explaining 95 % of the variation in the data, were extracted by the PCA. All eight variables were positively correlated with the first axis (Table 6). This axis represents variation along a general body size gradient. Only tail length was highly and positively correlated with the second axis. Body width and head width were negatively but poorly correlated with the second axis. The second axis represents variation along a tail length gradient that is independent of the increase of tail length with body size. Table 6. Correlations of morphologicalvariables of snakes of northeastern Brazil with the first and second principal component axes (see Methods).

Species having extreme positive scores on the first axes were heavy-bodied and had large heads. Species having extreme positive scores on the 2nd axis tended to have long tails and had slightly narrower heads and bodies (Fig. 4).

Fig. 4. Plot of scoresfor each of nineteenspeciesof snakeson the first two principalcomponent axes (see Methods). Factor 1 is an axis representingincreasingbodysize.Factor 2 is an axis representingincreasing tail length and decreasinghead and body width. Speciesare: 1)E. cenchria,2) L. poecilogyras, L. viridis, 3) 4) P. olfersii,5)L. lineatus,6) 0. trigeminus, L. mossoroensis, T.strigilis,9) M. ibiboboca,10)O. aeneus, 7) 8) 11)T.pallidus, 12)L. ahaetuila, 13)P. nigra, 14)P. nattereri,15) S. pullatus, 16)C. occipitolutea, W.merre17) mii, 18)B. constrictor,and 19) C. durissus.

287 Sexual differences in morphology. - In all instances where samples are relatively large, head length, head width, gape and body mass are correlated with SVL. In some instances there are sexual differences either in slopes or adjusted means of the variables based on analysis of covariance with log SVL as the covariate (Table 7), although in many cases no sexual differences are apparent. Table 8 presents means of all morphological variables separated by sex.

Discussion Perhaps the most striking attribute of the caatinga snake fauna described in this study is the complete absence of snakes which feed on invertebrates. All species feed on vertebrates. That this is somewhat of a surprise is based on the presence of many invertebrate eating snakes in other snake communities of xeric areas in the new world. For example, the Sonoran Desert, in addition to having many snakes which eat vertebrates, has many which eat various types of invertebrates (STEBBINS, 1954). These include the genera Tantilla, Chionactis, Chilomeniscus, Gyalopion, Leptotyphlops and Sonora. Both caatinga and the Sonoran Desert have diverse lizard faunas, most of which are insectivorous suggesting that competition with lizards may not be the factor causing this difference. Furthermore, insects do not appear to be in short supply in either habitat. Three factors, or their interaction may partially explain why there are no invertebrate eating snakes in n certain areas one species ofLeptotyphlops and one species of Tantilla occur caatinga (in in caatinga) (VaNZOt,nvt et al., 1980). Unlike the Sonoran Desert, Caatinga contains at least six terrrestrial or arboreal mammals which are wholly or partially insectivorous; Monodelphis domestica, Didelphis albiventris, Tamandua tetradactyla, Euphractus.sexcintus, Dasypus novemcinctus and Marmosa karimii (MARES et a]., 1981). Because the first five of these are abundant and relatively large bodied, they would need considerable amounts of food to meet their energetic demands. They may have a large enough impact on terrestrial or fossorial invertebrates to be important competitors at least during periods (dry season) when insect abundance might be reduced (JANZEN and SCHOENER, 1968). Of the two Sonoran Desert insectivorous mammals, Notiosorex is rare and Onychomys is small bodied. Most invertebrate eating snakes are small in body size and their absence in caatinga may be a consequence offactors favoring large body size and thus not directly related to competitive effects from other insectivorous vertebrates. Small snakes could be prey for a large number of vertebrates and invertebrates. This possibility gains some support based on size of offspring of caatinga snakes. The smallest neonate averages 136 mm (L. poecilogyrus), considerably larger than hatchlings of many Sonoran Desert insectivorous snakes. Finally, most invertebrate eating snakes are semifossorial or fossorial and it is possible that caatinga does not have soils providing aappropriate microhabitats for small invertebrate eating snakes or their prey. Desert habitats of the southwestern United States contain areas with soft sand suitable for fossorial species such as Chionactis and Chilomeliiscus. Furthermore, mesic habitats in the southeastern United States harbor many burrowing snakes which are primarily invertebrate specialists such as Virginia, Carphophis, Tantilla and Diadophis. These occur primarily in leaf litter, rotted wood, or mesic soft soils, habitats that are not available in caatinga. The lack of burro-

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293 wing mammals (except armadillos; MARES et al., 1981) also supports this hypothesis. The most apparent dietary convergence among species centers on anurophagy. Five terrestrial species eat only anurans, and at least two arboreal species (Leptophis ahaetulla and Thamnodynastes pallidus) eat primarily anurans. Several other species eat frogs as well as other vertebrates. This presumably reflects availability of vertebrate prey. During all of the wet season and much of the dry season one is immediately struck by the abundance of anurans in Caatinga. The anuran fauna consists of at least 25 species including arboreal, terrestrial, aquatic, and semi-fossorial forms (VITT, umpubl.). The lack of snake species specializing on mammals may reflect the long-term unpredictability of mammals as a food supply because their populations would be expected to fluctuate drastically. STREILEIN(1982) has shown that small mammals fluctuate seasonally at Exu, Pernambuco. STREILEINpresents data summarized from AGGEU (a Brazilian public health agency) records that show clearly the long-term fluctuations possible in Caatinga mammals. For example, one individual of the rodent Bolomys lasiurus(Muridae) was collected in a three-month period during 1977 consisting of 29,250 trap nights. A capture-recapture study by KARIMI et al. (1976) cited by STREILEINrevealed densities of 187 B. lasiurus per hectare several years earlier. Although the same might be argued for anurans, most of the caatinga anurans are species which can burrow or seek refuge from drought in Lajeiros. Furthermore, because their energetic demands are low relative to mammals, their probability of survival during low resource periods may be relatively high. A diversity of reproductive tactics among sympatric species is evident. There are viviparous and oviparous modes represented, there are species with large and small cluthes, and there are several seasonal patterns apparent. Clutch or brood size, egg size, and neonate size vary considerably among species in the caatinga snake fauna. Clutch or litter size is largest however, in the largest species of snakes. Body size also accounts for much of the variation among species in offspring size. Consistent with data reported on other tropical snake communities (DixoNandSomi, 1975; DUELLMAN, 1978),these data demonstrate an absence of any generalized "tropical" pattern. The terrestrial anuraneating species exhibit extended breeding seasons, nearly year round (mitt, 1983 a) whereas other species, such as Philodryas nattereri and P olfersii breed over a relatively short period of time (V iTT, 1980). This is not surprising considering the breeding season variation among snake species shown by SAINT GIRONS (1982). Tropical (particularly equable tropics) environments are such that extended or continuous breeding is possible, but species may opt for short breeding seasons. The underlying determinants of seasonality in tropical reptiles is not known, even though correlations may often be made between seasonal intensity of reproduction and environmental variables such as light, temperature, moisture, and photoperiod (BARBAULT,1976; FITCH, 1970 ;GORMAN and LICHT, 1974; INGER and GREENBERG, 1966; LICHT and GORMAN, 1970; SEXTONet al., 1971). A great diversity of reproductive tactics is known among lizard species occurring at the locality where this snake study took place (VITT, 1982a, b, 1983b; VITT and GOLDBERG, 1983; VITT and LACHER, 1981). The PCA on morphological variables of caatinga snakes reveals some interesting and in some cases, intuitively expected associations. These associations may have an ecological and/or a taxonomic basis. For example, the branch-mimic types of arboreal snakes (Leptophis ahaetulla, Oxybelis aeneus, and Thamnodynastes pallidus) have high sco-

294 res on factor 2 and mid-range scores on factor 1. These snakes have relatively long and thin bodies, narrow heads, and a long tail. This suite of morphological characters is probably an adaptation for arboreality. However, the same suite of morphological characters may also serve as an adaptation for a fast-moving terrestrial existence as indicated by the similar factor scores of the two whipsnakes Philodryas nattereri and Philodryas olfersii. The remaining species of this community are terrestrial and/or semi-aquatic and have lower scores on factor 2 but encompass the entire range offactor 1, the general body size factor. At the same time, the PCA results are somewhat dissatisfying. Refering to the example above, in thee absence of relatively complete ecological observations, the PCA results could be very misleading. We might, for example, consider the arboreal branch mimic species most similar to the terrestrial whipsnakes, based on morphology alone, even though there are drastic ecological differences between these groups. There also appear in some cases, to be taxonomic biases in morphological relationships which would only be apparent if ecological data were available. The boiids, B. constrictorand E. cenchria are close in morphological space but quite different ecologically, with B. constrictortending more toward arboreality. Furthermore the streamlined morphologies of the arboreal colubrids represent a considerably different morphological solution to arboreal adaptation than found in the heavy-bodied boiid, B. constrictor. As the result of this study, we are convinced that the trophic and life history patterns among snakes occurring sympatrically can only be interpreted if time is a controlled variable, i. e., all species are studied at the same time. The results of species by species studies in different time intervals (seasons or years) or different localities cannot be satisfactorily compared because both diets and reproductive characteristics may be affected by resource availability, which is certainly not predictable through time and from place to place in fluctuating habitats like the caatinga of northeast Brazil. We do not mean to imply, however, that autecological or short-term studies are not of value. Carefully executed short-term or autecological snake studies are needed and encouraged as they can provide the detailed data necessary to understand specific biological phenomena. Community studies as reported on here, can set the stage for more detailed topic-oriented studies. As a cautionary note, because of the long and short-term unpredictability ofclimatological conditions in caatinga, longer term studies are needed to examine stability of this snake assemblage as a community. Finally, the interpretation of morphological analyses of communities of snakes appears dependent upon observational data on ecologies of the various species.

Vanzoliniwho spearheadedecologicalstudies -We Acknowledgments. - gratefullyacknowledgeDr. PauloE. in the "Nordeste"of Braziland providedLJV the opportunity todo the field portion of the study.Both Dr. Rio Vanzoliniand Dr. A ristides de Leao (formerpresident,AcademiaB rasileira C incias, de Janeiro)provided the logisticsupport necessaryfor the completionof thiswork.KarlSteileinand ThomasLacher providedoccasionalhelp in the fieldand identified mammaland bird remains in snake stomachs.W.Ronald oflnternatioHeyer identifiedsamplecollectionsofanurans. The NationalScience Foundation (Division inal Programs,Project No. 80-LA/B-09) the O'Neil Museum Trust, CarnegieMuseum of NaturalHiand to story,providedsupport for a return visit to Brazilallowing LJV collectadditionaldata. A majorityofthe field workwas supported by the peopleand FederalGovernment of Brazilbygrants administrated byAcademia B rasileira de Cincias pertinent to the project"Estudos EcolgicosnoNordeste Semi-aridodoBrasil" conceived by Dr. Paulo E. Vanzolini.

295 Contract DE-AC09-76SROO-819 betweenthe U. S. Department of Energyand the Universityof Georgia provided support for later stages of this research as did the BiologyDepartment, UCLA.Finally,we thank RaymondD. Semlitsch,J. Whitfield Gibbons, Justin D. Congdon and Harry Greene for commenting on various drafts of the manuscript.

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