Printer Friendly

Aplicaciones e implicaciones de la filogeografia para la conservacion de los canidos.

APPLICATIONS AND IMPLICATIONS OF PHYLOGEOGRAPHY FOR CANID CONSERVATION

INTRODUCTION

Phylogeography is the analysis of the principles and processes that govern the geographic distribution of genealogical lineages (Avise et al., 1987; Avise, 2000). In this sense, this approach involves the study of the interaction between demographic aspects, the genetics of populations, and the dynamics of physical processes (geological or climatic) to address relevant questions in the areas of evolutionary biology, ecology, and conservation.

Phylogeography is currently being used as a tool for the inference of historical demographic processes such as gene flow, effective population size, colonisation sequences, and populational bottlenecks, and also for determining species boundaries and identifying possible conservation units (Avise et al., 1987; Avise, 2000, 2008; Vazquez-Dominguez, 2002; Freeland, 2005). In the latter aspect, studies of geographic distribution of genealogical lineages have been widely used to describe historical events such as habitat fragmentation or expansions in the distribution areas of species and populations, migration events, vicariance and extinction of genetic lineages, as well as other processes affecting population structure or causing speciation in a spatial or temporal context (Hardy et al., 2002). The comparative analysis of the phylogeographic patterns of different species allows the formulation of hypotheses about possible shared events such as vicariance or dispersion which then can be associated to geological, ecological and ethological processes (Arbogast and Kenagy, 2001; Zink, 2002; Lanteri and Confalonieri, 2003).

From its origins, phylogeography has been closely associated with analyses based on information of the mitochondrial genome (Avise, 1998). However in recent years, the utilisation of microsatellites (and other nuclear DNA loci) has drastically increased. These studies facilitate the interpretation of recent events due to the high rate of mutation of microsatellites. More generally, the use of different markers allows the understanding of phylogeographic patterns and processes at different evolutionary scales (Beheregaray, 2008). Thus, population genetics and phylogeographic studies may be considered as part of a continuum and not independent fields (Joseph and Omland, 2009).

Members of the Family Canidae are usually characterised by high mobility and vagility, ethological characteristics that result in low levels of geographical genetic differentiation (Dalen et al., 2005; Iyengar et al., 2005; Tchaicka et al., 2006). However, habitat fragmentation and loss have intensified genetic drift in small populations, accelerating differentiation and loss of genetic variability. The erosion of genetic diversity has occurred in many species, increasing extinction risk because of the maintenance of isolated subpopulations with reduced effective population numbers. High vagility may also be influential in promoting hybridisation and affecting genetic composition (Lehman et al., 1991; Jenks and Wayne, 1992; Wayne, 1992; Mercure et al., 1993; Wilson et al., 2000; Wayne and Brown, 2001), having an impact on interspecific gene flow and affecting the gene pools of species (Jenks and Wayne, 1992; Wilson et al., 2000; Wayne and Brown, 2001).

Phylogeographic concepts are increasingly being applied to the biological conservation of species (Beheregaray, 2008). We herewith present a review of the different contributions of this approach to the understanding of the processes and patterns of the spatial distribution of genetic variability, and its applications and implications for canid conservation.

EVOLUTIONARY SIGNIFICANT UNITS

The patterns of variation of genetic and phenotypic characteristics and their interactions with environmental variation provide substrate that ultimately leads to geographical population differentiation (Avise, 2000; Coyne and Orr, 2004). In heterogeneous landscapes, restrictions to gene flow between populations may result not only from geographic barriers or isolation by distance (Ribera and Vogler, 2004; Knowles and Richards, 2005), but also because of non-vicariant events, among them, diversifying natural selection, when environmental conditions and selective regimes differ between different locations (Nosil et al., 2008). Most conservation biologists consider that sets of populations that show restricted gene flow with other equivalent units represent the highest level of the species geographical structure and require differentiated genetic management. (Fraser and Bernatchez, 2001). Such populations are called 'evolutionary significant units' (ESU) (Ryder, 1986). The concept of ESUs was developed to provide an objective approach for the protection of units below the species level, because subspecies delineations may be absent and often do not adequately reflect the geographical genetic structure existing within species (Avise, 1989).

Several large-scale phylogeographic studies have been developed in canids, allowing the identification of different patterns and levels of geographic genetic structuring. One of these studies analysed the genetic patterns in most of the distribution of the arctic fox (Alopex lagopus) using mtDNA D-loop sequences. Geographical differentiation was generally moderate in this species, reflecting ongoing frequent gene flow and/or recent isolation or divergence. However, high Fst values between Iceland and other populations demonstrated that the former were relatively more isolated from the rest (Dalen et al., 2005). Microsatellite population analyses of another Arctic emblematic canid, the grey wolf (Canis lupus), revealed high gene flow between continental and island populations (Carmichael et al., 2008). New methodological advances based on estimations from Bayesian analyses allow the estimation of rates and directionality of migration, growth, effective population sizes and extinction events (Sacks et al., 2005; Palstra and Ruzzante, 2008; Ilves et al., 2010, among others). For example, it is important to estimate such parameters to know if the Arctic species A. lagopus and C. lupus exhibit metapopulation dynamics where extinctions occur in islands that are then recolonised from the continent (Elhmagen and Angerbjorn, 2001), possibly facilitated by the ice that forms connecting bridges during winters (Johnston, 2002). The understanding of the population dynamics of a species is central to conservation programs because metapopulations do not occupy all adequate habitats as a consequence of the equilibrium between colonisation and extinction; thus, the conservation of seemingly unoccupied habitat may still be a priority (Hanski, 1998). Studies of mtDNA sequences comprising a large part of the geographic distribution of C. lupus demonstrated that North America, Europe and most of Asia populations represent a single mega-ESU, showing reciprocal monophyly with allopatric distributions. The exception to this lack of structuration are the Himalayan and Indian populations that form two haplogroups that can be considered independent ESUs each and isolated from the rest of the populations of North America, Europe and the rest of Asia (Pilot et al., 2010) (Fig. 1). In general, different studies of C. lupus have shown that the low structuring of their populations is not explained by evident geographic barriers and historical events (Carmichael et al., 2001; Geffen et al., 2004; Musiani et al., 2007). Nevertheless, in a study in nortwestern Canada using microsatellites, Carmichael et al. (2001) found that genetic structuring may be influenced by prey specialization, suggesting that prey (caribou) migration could serve as a corridor for gene flow. In North America, Geffen et al. (2004), analysing populations using microsatellites and RFLP observed that genetic structuring could be correlated with the climatic characteristics of different regions. These data are consistent with the phenotypic variation shown by the species: colour and size vary from North to South (Gipson et al., 2002); these phenotypic charac teristics could result in restrictions to gene flow, allowing genetic drift and/or natural selection to maintain genetic and phenotypic differentiated populations (Geffen et al., 2004). These findings led to the development of the 'wolf ecotype' concept, thus extending the ESU concept to consider not only the genetic composition of populations but also functional characteristics and local adaptations (Crandall et al., 2000). When C. lupus is analysed with mitochondrial markers at a reduced geographic scale, no significant structuring is observed, but when multilocus markers shuch as microsatellites are employed, small-scale geographical structuring related to prey availability and environmental characteristics is observed. Genetic structuring must be interpreted jointly with ecological and morphological data when defining ESUs. Furthermore, clinal variations of body size and coloration are common in homeothermic animals generating patterns known as Bergmann's and Gloger's rules, respectively, where larger and less pigmented individuals are found at higher latitudes (Bergmann, 1847; Gloger, 1883). Because this is a common pattern for mammals, it is possible that clinal variation of body mass or colour are not necessarily related with restrictions to gene flow between populations. Morphological analyses of the cranium, and the mandible, may allow the detection of functional characteristics and local adaptations subjected to natural selection, which in turn are important for the delimitation of ESUs (Cardini et al., 2003).

[FIGURA 1 OMITIR]

In the African continent, the analyses of the mitochondrial control region (D-loop), as well as eleven microsatellite loci of the African wild dog (Lycaon pictus), demonstrated genetic differentiation between all studied populations which, however, maintain genetic flow between them. Also, from mitochondrial data, two highly structured clades were found, one including genotypes exclusive of the southern populations and the second one conformed by an exclusive eastern haplotype, the rest of haplotypes being shared by the southern and eastern populations. These genetic patterns where exclusive haplotypes are found in southern and eastern populations, could be the result of the Pleistocene/Holocene climatic transitions. Besides, the haplotypes shared by the southern and eastern populations could be the consequence of secondary migrations between these populations (Girman et al., 2001; Marsden et al., 2012). These information, added to that of previous work by Girman et al. (1993) who demonstrated that southern and eastern populations are genetically and morphologically distinct, support the classification of these two groups (eastern and southern) as different ESUs. Consequently, translocations of individuals from the south and the east are not advised, since possible adaptive differences may exist (Crandall et al., 2000). Since the eastern populations (Masai Mara and Serengeti) are in serious extinction risk, the locality of Selous would be a suitable alternative as a source for the introduction of individuals because it has genotypes typical of the eastern clade. Furthermore, captive populations showed typical southern genotypes, thus representing potential individuals for introduction in southern wild populations (Girman et al., 2001) (Fig. 2).

Lycaon pictus had a very large historical distribution inhabiting all African ecosystems south of Sahara, with the exception of tropical forests. However, its populations have dwindled dramatically after the arrival of Europeans and the subsequent growth of human populations (Creel and Creel, 1998); currently, the species is limited to isolated patches. In the study of Girman et al. (2001), which compared the genetic diversity of L. pictus with other phylogenetically close canids, no loss of genetic diversity could be detected using either mtDNA or microsatellite markers. However, this kind of approach is limited by the availability of populations for comparison and in fact, it is frequently difficult to verify the assumptions (Garza and Williamson, 2001). Recent analytical developments based on Markov chain Monte Carlo methods allow a robust characterization of historical variations of population size (Girod et al., 2011), which is central to L. pictus conservation because loss of genetic diversity may limit its evolutionary potential (Frankham et al., 1999) and reduce the ability of a population to produce a response to recently introduced pathogens and parasites (O'Brien and Evermann, 1989). The latter is probably the cause of the recent extinction of populations in the Kenya-Tanzania frontier (Sillero-Subiri et al., 2004).

The Crab-eating Fox (Cerdocyon thous) is one of the most common canid species in South America. This species has a disjunct distribution inhabiting northern Amazonia in Colombia and most of Venezuela (except for the southern region of the State of Amazonas), and to the south of Amazonia in northeastern, central and southern Brazil, Paraguay, central and northern Argentina, western Bolivia, and Uruguay (Sillero-Zubiri et al., 2004), showing a clear preference for open habitats (Bisbal, 1989; Trovati et al., 2007). Phylogeographic analyses of this species using nuclear and mitochondrial sequences in different Brazilian populations revealed two phylogenetic clades, one corresponding to the North, and the other to the Southern region of Brazil (Tchaicka et al., 2006). This structure may be related to habitat fragmentation during the Late Pleistocene; it is estimated that during the Last Glacial Maximum two isolated regions of high probability of occurrence existed for this species-one in northeastern Brazil in the Caatinga region, and the other in northern Argentina (Cha coan region) (Martinez et al., 2013). Despite the generalist ecology of C. thous, changes in the environment may have limited its dispersion possibly as a result of drastic vegetation changes. These observations suggest that the apparent cotinuity of present day biomes is deceiving, obscuring historical fragmentation (Martinez et al., 2013). The subdivision identified in C. thous does not correspond with the previously proposed subspecies by Cabrera (1931), who recognized three subspecies in Brazil, C. t. entrerrianus in the south, C. t. azarae in the center and north-east and C. t. thous in the north. Phylogeographic studies comprising the whole geographic distribution of C. thous are necessary to determine the taxonomic status of the subspecies and, with that information, define and delimit the ESUs, because at present genetic data from populations of northern Amazonia of C. t. thous and C. t. aquilus in Venezuela that show morphological differentiation between them and the rest of subspecies, are practically non-existent (Bisbal, 1988; Machado and Hingst-Zahaer, 2009).

[FIGURE 2 OMITTED]

Eleven subspecies are traditionally recognized in the Asiatic wild dog (Cuon alpinus) (Cohen, 1978). Studies of mtDNA and microsatellite data revealed that only two phylogeographic groups exist; the accepted taxonomic status is inconsistent because a sufficient genetic structuring between the subspecies of the different regions is not observed. Besides, it was observed that the subspecies C. a. sumatrensis (restricted to Sumatra island) and C. a. javanicus (restricted to Java) could have originated from individuals introduced from India, although further studies are needed to confirm these findings (Iyengar et al., 2005).

The above mentioned studies corroborate that, in general, the number of geographical genetic units is smaller than the number of named subspecies of canids. The latter are primarly based on colour and size variations, Thus, phenotypic differentiation may respond to genetic or plastic variation associated with environmental gradients, whereas differentiation of presumably neutral genetic markers will tend to reflect historical fragmentation (or lack thereof) as well as historical and current levels of gene flow.

INBREEDING

Mating between relatives (inbreeding) may lead to reduction of reproductive potential and survival, as a consequence of the increase in frequency of homozygotes for deleterious or lethal alleles, which increases extinction risk. The harmful effects of inbreeding were for the first time documented in detail by Charles Darwin, who performed experiments in different plant species that exhibited auto-pollination and cross-pollination (Darwin, 1876). Different anomalies, such as lethal phenotypes in the first years of life, or genetic diseases have been reported in inbred individuals. When no major abnormalities are observed, endogamic depression is detectable as it results in low fertility and growth rates (Charlesworth and Willis, 2009).

In Scandinavia, C. lupus became extinct in 1960 but, around 1980, at least two wolves founded a new population in South-Central Scandinavia (Vila, 2003). The first reproductive event occurred in 1983, and in 1991 a new wolf contributed genetically to the preexistent population. By 2005, this population consisted of about 135-153 individuals (Wabakken et al., 2005). Using microsatellite analyses, Lieberg et al. (2004) produced a pedigree of the population and observed a high level of inbreeding depression manifested in a reduction in the number of offspring and an increased level of vertebral fracture due to malformation (Raikkonen et al., 2006).

A clear case of inbreeding can be observed in the Ethiopian wolf (Canis simensis) that is distributed in the country's highlands at about 3000 m in seven small, isolated populations. The susbspecies C. s. simensis is found to the north of the Great Rift Valley, and C. s. citernii occurs to the south (Gottelli et al., 2004). This species presents an imminent extinction risk. Studies using mtDNA and microsatellite sequences have shown that C. simensis has very low genetic variability. The isolation of the populations due to habitat seems to be the crucial factor influencing genetic diversity. These low genetic diversity values are consistent with an effective population number of a few hundred individuals. Anthropogenic perturbations have led to a reduction of population size, increasing the probability of allele fixation and of global loss of haplotypes and heterozygosity (Gottelli et al., 1994; Gottelli et al., 2004; Randall et al., 2010).

Canids in general show low levels of inbreeding because of their great dispersal potential, but in endemic species on islands the situation is very different due to the limitations to their dispersal. In North America, the island fox (Urocyon littoralis) is critically endangered and is only found in six islands of southern California (Wayne et al., 1991). Molecular studies indicated that the San Nicolas island population was invariant for all genetic markers, including multiple loci obtained by fingerprinting and 19 microsatellite loci (Gilbert et al., 1990; Goldstein et al,. 1999). No other wild population approaches this lack of genetic variation. In the same way, the lesser island, San Miguel, revealed low levels of genetic variation relative to the larger islands of Santa Catalina, Santa Rosa and Santa Cruz. Mitochondrial data suggested that the island of Santa Catalina may have been colonised several times from neighbouring islands (Roemer et al., 2002). These results indicate that each island should be considered as a different conservation unit.

In the coast of Chile, on the Pacific littoral of South America, lies Chiloe Island, where Darwin first observed a small endemic fox, Lycalopex fulvipes. Darwin's Fox is the sole canid species on Chiloe island and has the smallest geographic distribution of all canids (Cabrera, 1958). Genetic analyses of this species using mtDNA confirmed that only three haplotypes exist and genetic variability is very low. It is estimated that less than 500 individuals exist, and none in captivity (Vila, unpublished data).

Increased fragmentation of species habitat has occurred during the last 200 years, leading to the isolation of populations. Some canid species have shown enough physiological and ethological plasticity to survive in open habitats along with agriculture and cattle, thus maintaining gene flow between populations. Two different scenarios may be expected: 1) Canid species of large size are probably less susceptible to fragmentation but usually have low densities (Carbone and Gittleman, 2002). If fragmentation leads to an interruption of gene flow between populations, the resulting subpopulations will have reduced size and the effects of inbreeding will be evident in a few generations. 2) In contrast, species of smaller size that depend on closed habitats are more susceptible to fragmentation, thus inbreeding is favoured, but because of higher population densities the effects of inbreeding will be evident only after longer periods of time (Hartl and Clark, 2007).

HYBRIDISATION

Along the history of life on Earth, hybridisation has played a very important role in the evolution of biodiversity. On the one hand, hybridisation processes may produce novel gene combinations that could promote speciation and adaptive radiation generating new phenotypes on which natural selection can operate (Mavares and Linares, 2008). Conversely, hybridisation also can contribute to the extinction of species producing introgression of exotic alleles, causing possible exogamic depression and reducing species fitness (Templeton, 1986; Lynch, 1991; Edmands and Timmerman, 2003). Hybridisation between genetically distinct populations which are adapted to their local environments may modify the interaction between genes and environment producing less fit offspring, and lead to the disruption of coadapted gene complexes and exogamic depression. Since nowadays natural processes are strongly affected by anthropic action, hybridisation has become one of the main causes of extinction risk (Wolf et al., 2001).

Hybridisation, with and without genetic introgression has been frequently reported in Canidae (Lehman et al., 1991; Mercure , 1993; Roy et al., 1996; Sillero-Zubiri et al., 1996; Wayne et al., 1997; Wayne and Brown, 2001; Hailer and Leonardo, 2008; Kays et al., 2010; Wheeldon et al., 2010) leading in some cases to put the survival of species or populations at risk (Nowak, 1979; Wayne and Jenks, 1991; Gottelli et al., 1994; Roy et al., 1994).

Wolves and domestic dogs are very closely related, the latter having been domesticated from the former probably in several independent episodes of domestication (Vila et al., 1997; Wayne and Ostrander, 1999). Both taxa differ in only 1.8% of their genome sequences and have identical karyotypes which greatly facilitate hybridisation (Mech and Beitani, 2003) and the production of fertile progeny in captivity and in nature, where they overlap. In the last few years, with the increase of human settlements, hybridisation between wolves and feral dogs has increased, resulting in introgression of dog genes into the wolf gene pool. Several phylogeographic studies have detected hybrids of Canis lupus and domestic dog in nature. This situation has already been recorded in North America and several European countries (Dolf et al., 2000; Garcia-Moreno et al., 1996; Randi et al., 2000; Randi and Lucchini, 2002).

In C. simensis, microsatellite analyses identified hybrid individuals in a population of the Sanetti plateau at the mountains of the Bale National Park. In this region, typical domestic dog alleles were found in C. simensis, and typical C. simensis alleles, in some domestic dogs. Hybridisation between these two species seems to have no restrictions since offspring are produced through both species, indicating lack of hybrid inviability and/or sterility (Gottelli et al., 1994). In these conditions, domestic dogs not only hybridise with C. simensis but also compete with them for food resources, and may function as reservoirs of canine diseases (Sillero-Zubiri et al., 1996). Because population size of C. simensis is critical (300-500 individuals), hybridisation events may be sufficient to swamp the species genetic identity.

Alopex lagopus is classified as threatened and in risk of extinction in Sweden and Norway, respectively (Linnell et al., 1999; Gardenfors, 2000). One of the threats to this species is hybridisation with domesticated A. lagopus (Angerbjorn et al., 2004). Noren et al. (2005) analysed, by means of mtDNA and microsatellites, wild and captive A. lagopus individuals and observed strong genetic differentiation, possibly due to different geographic origins and selective breeding. Among the individuals from wild populations, some were related to the captive foxes, which suggests that occasional escapes from the farms do occur. Alopex lagopus is well adapted to its particular habitat (Angerbjorn et al., 2004) showing examples of local adaptations related to the time of reproduction, care of the young, and skin insulation and camouflage (Prestrud, 1991). Besides, the thickness of the fat layer of Scandinavian Arctic foxes seems to be adapted to fluctuations in food availability caused by the lemming cycles (Tannerfeldt and Angerbjorn, 1998). In view of this complex adaptive pattern, Noren et al. (2005) raised the hypothesis that hybridisation may lead to the loss of local adaptations, with the consequent risks for wild populations.

Wayne and Jenks (1991) analysing mitochondrial DNA, proposed that the red wolf (C. rufus) is a hybrid between the gray wolf (C. lupus) and the coyote (C. latrans), rather than a valid species or subspecies. This finding was used to criticise efforts made to reintroduce C. rufus in the wild (Gittleman and Pimm, 1991). However, evidence contradicting this hypothesis based on genetic, paleontologic and morphological data was almost immediately produced (Dowling et al., 1992a, b; Nowak, 1992). Nowadays, the taxonomic status of C. rufus is not clear, although recent evidences support C. rufus as a valid species (SilleroZubiri et al., 2004).

During the XXth century, putative hybrids between C. rufus and C. latrans have been reported. These cases are probably recent phenomena that resulted from anthropogenic modification of habitats or population decline caused by direct persecution (Nowak, 2002). In the United States, the state of Texas has historically been characterised by the presence of three morphologically distinct canid species that coexist sympatrically since the Holocene: the Mexican wolf (Canis lupus baileyi), the red wolf (C. rufus), and the coyote (C. latrans). Hailer and Leonard (2008) analysed these species using sequences of mtDNA control region and microsatellites located in the Y chromosome, in order to identify maternal and paternal lineages, respectively. In this study, the authors observed that one individual of C. latrans carried a mitochondrial haplotype of C. l. baileyi, and another one had Y chromosome alleles of the same species C. l. baileyi, evidencing that both males, and females of C. latrans may be involved in hybridisation events. Also, one individual of C. l. baileyi showed a mitochondrial C. latrans haplotype. A mitochondrial haplotype closely related with those of C. latrans was found in C. rufus. Another individual of this species had a Y chromosome haplotype possibly related to C. latrans. However, the lack of reciprocal specific monophyly between C. latrans and C. rufus as well as the lack of information of Y chromosome sequences of other canid species difficults the determination of the origin of the haplotypes. Hybridisation between C. latrans and C. rufus might have a strong impact on C. rufus populations (Adam et al., 2003; Fredrickson and Hedrick, 2006), while hybridisation between C. l. baileyi and C. rufus may have the same consequences on C. rufus, although presently both species are totally allopatric (Hailer and Leonard, 2008).

Molecular information has increased the ability to detect hybrids in recent years, but no easy answer exists in relation to whether hybrids should or should not be protected. There are big economic interests that would benefit from any suggestion that a species is not taxonomically valid to argue that conservation efforts are not guaranteed and its habitat may be exploited (Nowak, 1995).

Naturally occurring hybridisation, whether leading to speciation or extinction, does not constitute a threat in itself for the involved species since it is part of their evolutionary history (Arnold, 1992), but it may turn into a problem if it is favoured by changes in habitat or in the composition of the species through anthropogenic activities. In the latter cases, immediate management action is required to avoid compromising the evolutionary histories and genetic integrity of the affected species (Allendorf et al., 2001).

FINAL CONSIDERATIONS

Phylogeographic studies have contributed to systematics in the recognition of species and subspecies boundaries, and more generally to identify genetic units in the wild. In recent years, the possibility of using a larger number of molecular genetic markers has increased. This will facilitate the understanding of the dynamics and the status of populations of different canid species. An increase of studies simultaneously using different mitochondrial and nuclear (autosomal and sex-linked) markers is decisive because the use of just mitochondrial markers may be telling only a part of the story, since mitochondrial inheritance is strictly maternal. More generally, multilocus analyses are far more informative than single-locus assays. Comprehensive sampling at the adequate level (ideally comprising the entire distribution of the focal species), involving different habitats and coupled to morphological studies for detecting adaptive characteristics represent the more adequate condition for the identification of actual evolutionary significant units. In turn, this information is critical to guide management and conservation policies. It is also necessary to study genetic variation of populations kept in natural preserves and ex-situ conservation centres. It will thus be possible to identify the potential of individuals for possible reintroductions, because knowledge of the genetic relationship with the wild populations is essential to avoid incorporating organisms with unwanted characteristics.

One of the main anthropic phenomena is the alteration and fragmentation of natural habitats which has an enormous impact on inbreeding and hybridisation processes. Thus, assessing the effects of habitat modification is of extreme relevance in conservation decision-making. In this sense, the genetic knowledge across the distributional range of species is essential, although many canids have been ignored in this respect. The majority of phylogeographic studies have been devoted to large-sized canids, while little has been done and is known about smaller-sized species (Schwartz et al., 2005). The latter may turn out to be more susceptible to habitat fragmentation. This is particularly evident for example, in species of the genus Vulpes in North America, Asia and Africa or species of Lycalopex in South America. In view of this, it is necessary to increase our knowledge of how different species are affected by restrictions to movements between different habitat fragments, and to what extent the different production matrices (e.g., cattle raising, agricultural lands, plantations, oil fields) interact and affect gene flow in many of these canid species.

Food chains are generally complex, and include both direct and indirect interactions between different trophic levels. Frequently this complexity confounds our best efforts to anticipate how wild populations will respond to human activities (Polis and Strong, 1996). Since canids either behave as top predators or have generalist habits, their loss represents a high impact in community structure. In view of this, the precise knowledge of their genetic diversity and subdivision, and demographic characteristics is of great relevance to guide their management before these carnivores disappear with negative social, economic and ecological implications.

ACKNOWLEDGEMENTS

We thank Dr. Rocio Has san for critical reading of the manuscript. We are very grateful to Associate Editor Enrique Lessa and two anonymous reviewers for comments and suggestions that improved the manuscript substantially. The authors wish to thank the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq-Proc. 556793/2009-9) and CAPES (REUNI) for their support. CJB dedicates this paper to Valeria Ximena Rodriguez, for friendship and stimulating discussions.

REFERENCES

ADAMS JR, JA LEONARD, and LP WAITS. 2003. Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes. Molecular Ecology 12:541-546.

ALLENDORF FW, RF LEARY, P SPRUELL, and JK WENBURG. 2001. The problems with hybrids: Setting conservation guidelines. Trends in Ecology and Evolution 16:613-622.

ANGERBJORN A. 2005. Population history and genetic structure of a circumpolar species: The arctic fox. Biological Journal of the Linnean Society 84:79-89.

ANGERBJORN A, P HERSTEINSSON, and M TANNERFELDT. 2004. Europe and North and Central Asia (Palaearctic): Arctic fox, Alopex lagopus. Pp. 117-123, in: Canids: Foxes, Wolves, Jackals and Dogs (C Sillero-Zubiri, M Hoffman, and DW Macdonald, eds.). Status Survey and Conservation Action Plan. The Wildlife Conservation Research Unit, Oxford, UK.

ARBOGAST BS and GJ KENAGY. 2001. Comparative phylogeography as an integrative approach to historical biogeography. Journal of Biogeography 28:819-825.

AVISE JC. 2000. Phylogeography. Harvard University Press, Cambridge, USA.

AVISE JC, J ARNOLD, RM BALL, E BERMINGHAM, T LAMB, LE NEIGEL, CA REEB, and NC SAUNDERS. 1987. Intraspecific phylogeography: The mitocondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18:489-522.

AVISE JC. 1989. A role for molecular genetics in the recognition and conservation of endangered species. Trends Ecology and Evolution 4:279-281.

AVISE JC and D WALKER. 1998. Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings Royal Society B: Biological Sciences 265:457-463.

AVISE JC. 2008. Phylogeography: retrospect and prospect. Journal of Biogeography 36:3-15.

BEHEREGARAY LB. 2008. Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology 17:3754-3774.

BERGMANN C. 1847. Ueber die verha ltnisse der warmeo konomie der thiere zu ihrer grosse. Gottinger Studien 3:595-708.

BISBAL FJ 1988. A taxonomic study of the crab-eating fox, Cerdocyon thous, in Venezuela. Mammalia 52:181-186.

BISBAL FJ 1989. Distribution and habitat association of the carnivores in Venezuela. Pp. 339-362, in: Advances in neotropical mammalogy (KH Redford and JF Eisenberg, eds.). The Sandhill Crane Press, Gainesville, FL.

CABRERA A. 1931. On some South American canine genera. Journal of Mammalogy 12:54-67.

CABRERA A. 1958. Catalogo de los mamiferos de America del Sur. Revista del Museo Argentino de Ciencias Naturales 'Bernardino Rivadavia, Ciencias Zoologicas 4:1-307.

CARBONE C and JL GITTLEMAN. 2002. A Common rule for the scaling of carnivore density. Science 295:2273-2276.

CARDINI A. 2003. The geometry of the marmot (Rodentia: Sciuridae) mandible: phylogeny and patterns of morphological evolution. Systematic Biology 52:186-205.

CARMICHAEL LE, JA NAGY, NC LARTER, and C STROBECK. 2001. Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Molecular Ecology 10:2787-2798.

CARMICHAEL LE, J KRIZAN, JA NAGY, M DUMOND, D JOHONSON, A VEITCH, and C STROBECK. 2008. Northwest passages: Conservation genetics of Arctic Island wolves. Conservation Genetics 9:879-892.

CHARLESWORTH D and JH WILLIS. 2009. The genetics of inbreeding depression. Nature Reviews Genetics 10:783-796.

COHEN JA. 1978. Cuon alpinus. Mammalian Species 100:1-3.

COYNE JA and HA ORR. 2004. Speciation. Sinauer Associates, Sunderland, MA, USA.

CRANDALL KA, ORP BININDA-EMONDS, GM MACE, and RK WAYNE. 2000. Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution 15:290-295.

CREEL S and NM CREEL. 1998. Six ecological factors that may limit African wild dogs, Lycaon pictus. Animal Conservation 1:1-9.

DALEN L, E FUGLEI, P HERSTEINSSON, CMO KAPEL, JD ROTH, G SAMELIUS, M TANNERFELDT, and AD DITCHFIELD. 2005. Population history and genetic structure of a circumpolar species: The arctic fox. Biological Journal of the Linnean Society 84:79-89.

DARWIN CR 1876. The effects of cross and self fertilization in the vegetable kingdom. John Murray, London, UK.

DOLF G, J SCHLAPFER, C GAILLARD, E RANDI, V LUCCHINI, U BREITENMOSER, and N STAHLBERGER-SAITBEKOVA. 2000 Differentiation of the Italian wolf and the domestic dog based on microsatellite analysis. Genetics, Selection, Evolution 32:533-541.

DOWLING TE, BD DEMARAIS, WL MINCKLEY, ME DOUGLAS, and PC MARSH. 1992a. Use of genetic characters in conservation biology. Conservation Biology 6:7-8.

DOWLING TE, WL MINCKLEY, ME DOUGLAS, PC MARSH, and BD DEMARAIS. 1992b. Response to Wayne, Nowak, and Phillips and Henry: Use of molecular characters in conservation biology. Conservation Biology 6:600-603.

EDMANDS S and CC TIMMERMANN. 2003. Modelling factors affecting the severity of outbreeding depression. Conservation Biology 17:883-892.

ELMHAGEN B and A ANGERBJORN. 2001. The applicability of metapopulation theory to large mammals. Oikos 94:89-100.

FERGUS C. 1991. The Florida panther verges on extinction. Science 251:1178-1189.

FRANKHAM R, K LEES, ME MONTGOMERY, PR ENGLAND, EH LOWE, and DA BRISCOE. 1999. Do population size bottlenecks reduce evolutionary potential? Animal Conservation 4:255-260.

FRASER DJ and L BERNATCHEZ. 2001. Adaptive evolutionary conservation: Towards a unified concept for defining conservation units. Molecular Ecology 10:2741-2752.

FREDRICKSON RJ and PW HEDRICK. 2006. Dynamics of hybridization and introgression in red wolves and coyotes. Conservation Biology 20:1272-1283.

FREELAND JR. 2005. Molecular ecology. John Wiley and Sons, London, UK.

GARCIA-MORENO J, MD MATOCQ, MS ROY, E GEFFEN, and RK WAYNE. 1996. Relationships and genetic purity of the endangered Mexican wolf based on analysis of microsatellite loci. Conservation Biology 10:376-389.

GARDENFORS U. 2000. The 2000 Red List of Swedish Species. Art Datanken, SLU, Uppsala, Sweden.

GARZA JC and EG WILLIAMSON. 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10:305-318.

GEFFEN E, MJ ANDERSON, and RK WAYNE. 2004. Climate and habitat barriers to dispersal in the highly mobile grey wolf. Molecular Ecology 13:2481-2490.

GILBERT DA, N LEHMAN, SJ O'BRIEN, and RK WAYNE. 1990. Genetic fingerprinting reflects population differentiation in the California channel island fox. Nature 344:764-767.

GIPSON PS, EE BANGS, TN BAILEY, DK BOYD, HD CLUFF, DW SMITH, and MD JIMINEZ. 2002. Color patterns among wolves in western North America. Wildlife Society Bulletin 30:821-830.

GIRMAN DJ, PW KAT, MGL MILLS, JR GINSBERG, M BORNER, V WILSON, JH FANSHAWE, C FITZGIBBON, LM LAU, and RK WAYNE. 1993. A genetic and morphological analysis of the African wild dog (Lycaon pictus). Journal of Heredity 84:450-459.

GIRMAN DJ, C VILA, E GEFFEN, S CREEL, GL MILLS, JW MCNUTT, J GINSBER, PW KAT, KH MAMIYA, and RK WAYNE. 2001. Patterns of population subdivision, gene flow and genetic variability in the African wild dog (Lycaon pictus). Molecular Ecology 10:1703-1723.

GIROD C, R VITALIS, R LEBLOIS, and H FREVILLE. 2011. Inferring population decline and expansion from microsatellite data: A simulation-based evaluation of the Msvar method. Genetics 188:165-179.

GITTLEMAN JL and SL PIMM. 1991. Crying wolf in North America. Nature 351:524-525.

GLOGER CL. 1833. Das Abandern der Vogel durch Einfluss des Klimas. August Schulz, Breslau, Germany.

GOLDSTEIN DB, GW ROEMER, DA SMITH, DE REICH, A BERGMAN, and RK WAYNE. 1999. The use of microsatellite variation to infer patterns of migration, population structure, and demographic history, an

evaluation of methods in a natural model system. Genetics 151:797-801.

GOTTELLI D, C SILLERO-ZUBIRI, GD APPLEBAUM, MS ROY, DJ GIRMAN, J GARCIA-MORENO, EA OSTRANDER, and RK WAYNE. 1994. Molecular genetics of the most endangered canid, the Ethiopian wolf, Canis simensis. Molecular Ecology 3:301-312.

GOTTELLI D. 2004. The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Molecular Ecology 13:2275-2286.

HAILER F and JA LEONARD. 2008. Hybridization among three native North American Canis species in a region of natural sympatry. PLoS ONE 3:1-9.

HANSKY I. 1998. Metapopulation dynamics. Nature 396:41-49.

HARDY ME, JM GRADY, and EJ ROUTMAN. 2002 Intraspecific phylogeography of the slender madtom: The complex evolutionary history of the Central Highlands of United States. Molecular Ecology 11:2393-2403.

HARTL DL and AG CLARK. 2007. Principles of population genetics, 4th edition. Sinauer Associates, Inc., Sunderland, MA, U.S.A.

ILVES KL, W HUANG, JP WARES, and MJ HICKERSON. 2010. Colonization and/or mitochondrial selective sweeps across the North Atlantic intertidal assemblage revealed by multi-taxa approximate Bayesian computation. Molecular Ecology 19:4505-4519.

IYENGAR A, VN BABU, S HEDGES, AB VENKATARAMAN, N MACLEAN, and PA MORIN. 2005. Phylogeography, genetic structure, and diversity in the dhole (Cuon alpinus). Molecular Ecology 14:2281-2297.

JENKS SM and RK WAYNE. 1992. Problems and policy for species threatened by hybridization, the red wolf as a case study. Pp. 237-251, in: Wildlife 2001: Populations (DR McCullough and RH Barrett, eds.). Elsevier Science Publishers, London, UK.

JOHNSTON DM. 2002. The Northwest Passage revisited. Ocean Development and International Law 33:145-164.

JOSEPH L and KE OMLAND. 2009. Phylogeography: Its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds. Emu 109:1-23.

KAYS RK, A CURTIS, and JJ KIRCHMAN. 2010. Rapid adaptive evolution of northeastern coyotes via hybridization with wolves. Biology Letters 6:89-93.

KNOWLES LL and CL RICHARDS. 2005. Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation. Molecular Ecology 14:4023-4032.

LANTERI A and V CONFALONIERI. 2003. Filogeografia, objetivos, metodos y ejemplos. Pp. 185-194, in: Una perspectiva Latinoamericana de la Biogeografia (JJ Morrone and J Llorente, eds.). CONABIO, Mexico.

LEHMAN N, A EISENHAWER, K HANSEN, DL MECH, RO PETERSON, PJP GOGAN, and RK WAYNE. 1991. Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104-119.

LIEBERG O, H ANDREN, H-C PEDERSEN, H SAND, D SEJBERG, P WABAKKEN, M AKESSON, and S BENSCH. 2005. Severe inbreeding depression in a wild wolf (Canis lupus) population. Biology Letters 1:17-20.

LINNELL JDC, O STRAND, A LOISON, EJ SOLBERG, and P JORDH0Y. 1999. A future for arctic foxes in Norway? A status report and action plan. NINA Oppdragsmelding 576:1-16.

LYNCH M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622-629.

MACHADO F and E HINGST-ZAHER. 2009. Investigating South American biogeographic history using patterns of skull shape variation on Cerdocyon thous (Mammalia: Canidae). Biological Journal of the Linnean Society 98:77-84.

MARSDEN CD, R WOODROFFE, MG MILLS, JW McNUTT, S CREEL, R GROOM, M EMMANUEL, S CLEAVELAND, P KAT, GS RASMUSSEN, J GINSBERG, R LINES, JM ANDRE, C BEQQ, RK WAYNE, and BK MABLE. 2012. Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pic tus). Molecular Ecology 21(6):1379-1393.

MARTINEZ PA, D MARTI, W MOLINA, and CJ BIDAU. 2013. Bergmanns rule across the Equator: A case study in Cerdocyon thous (Canidae). Journal of Animal Ecology, Early online view, DOI: 10.1111/13652656.12076

MAVAREZ J and M LINARES. 2008. Homoploid hybrid speciation in animals. Molecular Ecology 17:4181-4185.

MECH LD and L BOITANI. 2003. Wolves. Behavior, ecology and conservation. The University of Chicago Press, Chicago.

MERCURE A, K RALLS, KP KOEPFLI, and RK WAYNE. 1993. Genetic subdivisions among small canids, mitochondrial DNA differentiation of swift, kit, and Arctic foxes. Evolution 47:1313-1328.

MUSIANI M, JA LEONARD, HD CLUFF, CC GATES, S MARIANI, PC PAQUET, C VILA, and RK WAYNE. 2007. Differentiation of tundra/taiga and boreal coniferous forest wolves: Genetics, coat colour and association with migratory caribou. Molecular Ecology 16:4149-4170.

NOREN K, L DALEN, K KVAOY, and A ANGERBJORN. 2005. Detection of farm fox and hybrid genotypes among wild artic foxes in Scandinavia. Conservation Genetics 6:885-894.

NOSIL P, SP EGAN, and DJ FUNK., 2008. Heterogeneous genomic differentiation between walking-stick ecotypes, isolation by adaptation and multiple roles for divergent selection. Evolution 62:316-336.

NOWAK RM. 1979. North American Quaternary Canis. Monographs of the Museum of Natural History, University of Kansas 6:1-154.

NOWAK RM. 1992. The red wolf is not a hybrid. Conservation Biology 6:593-595.

NOWAK RM 1995. Hybridization: the double-edged threat. IUCN/SSC Canid Specialist Group Canid News 3:2-6.

NOWAK RM. 2002. The original status of wolves in eastern North America. Southeastern Naturalist 1:95-130.

O'BRIEN S and J EVERMANN. 1989. Interactive influence of infectious disease and genetic diversity in natural populations. Trends in Ecology and Evolution 3:254259.

PALSTRA FP and DE RUZZANTE. 2008. Genetic estimates of contemporary effective population size: What can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology 17:3428-3447.

PILOT M, W BRANICKI, W JCDRZEJEWSKI, J GOSZCZYNSKI, B JCDRZEJEWSKA, I DYKYY, M SHKVYRYA, and E TSINGARSKA. 2010. Phylogeographic history of grey wolves in Europe. BMC Evolutionary Biology 10:104.

POLIS GA and DR STRONG. 1996. Food web complexity and community dynamics. American Naturalist 147:813-846.

PRESTRUD P 1991. Adaptations by the arctic fox (Alopex lagopus) to the polar winter. Arctic 44:132-138.

RAIKKONEN J, A BIGNERT, P MORTENSEN, and B FERNHOLM. 2006. Congenital defects in a highly inbred wild wolf population (Canis lupus). Mammalian Biology 71:65-73.

RANDALL DA, JP POLLINGER, K ARGAW, DW MACDONALD, and RK WAYNE. 2010. Fine-scale genetic structure in Ethiopian wolves imposed by sociality, migration, and population bottlenecks. Conservation Genetics 11:89-101.

RANDI E and V LUCCHINI. 2002. Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conservation Genetics 3:31-45.

RANDI E, V LUCCHINI, MF CHRISTENSEN, N MUCCI, SM FUNK, G DOLF, and V LOESCHCKE. 2000. Mitochondrial DNA variability in Italian and East European wolves. Detecting the consequences of small population size and hybridization. Conservation Biology 14:464-473.

REICH DE, RK WAYNE, and DB GOLDSTEIN. 1999. Genetic evidence for a recent origin by hybridization of red wolves. Molecular Ecology 8:139-144.

RIBERA I and AP VOGLER. 2004. Speciation in Iberian diving beetles in Pleistocene refugia (Coleoptera, Dytiscidae). Molecular Ecology 13:179-193.

ROEMER GW, CJ DONLAN, and F COURCHAMP. 2002. Golden eagles, feral pigs and insular carnivores: How exotic species turn native predators into prey. Proceedings of the National Academy of Sciences of the United States of America 99:791-796.

ROY MS. 1994. Patterns of differentiation and hybridization in North American wolf-like canids revealed by analysis of microsatellite loci. Molecular Biology and Evolution 11:553-570.

ROY MS. 1996. Molecular genetics of red wolves. Conservation Biology 10:1413-1424.

RYDER OA. 1986. Species conservation and systematics, The dilemma of subspecies. Trends in Ecology and Evolution 1:9-10.

ROZHNOV VV. 1993. Extinction of the European mink, ecological catastrophe or a natural process? Lutreola 1:10-16.

SACKS BN. 2005. Coyote movements and social structure along a cryptic population genetic subdivision. Molecular Ecology 14:1241-1249.

SCHWARTZ MK. 2005. Gene flow among San Joaquin kit fox populations in a severely changed ecosystem. Conservation Genetics 6:25-37.

SILLERO-ZUBIRI C, AA KING, and DW MACDONALD. 1996. Rabies and mortality in Ethiopian wolves (Canis simensis). Journal of Wildlife Diseases 32:80-86.

SILLERO-ZUBIRI C, M HOFFMANN, and DW MACDONALD. 2004. Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid Specialist Group. Gland, Switzerland and Cambridge, UK.

TANNERFELDT M and A ANGERBJORN. 1998. Fluctuating resources and the evolution of litter size in the arctic fox. Oikos 83:545-559.

TCHAICKA L, E EIZIRIK, TG OLIVEIRA, JR CANDIDO, and TR FREITAS. 2006. Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Molecular Ecology 16:819-838.

TEMPLETON AR. 1986. Coadaption and outbreeding depression. Pp. 105-116, in; Conservation biology, The science of scarcity and diversity (ME Soule, ed.). Sinauer Associates, Sunderland, MA, USA.

TROVATI RG, BA DE BRITO, and JMB DUARTE. 2007. Area de uso e utilizacao de habitat de cachorro-domato (Cerdocyon thous Linnaeus, 1766) no cerrado da regiao central do Tocantins, Brasil. Mastozoologia Neotropical 14:61-68.

VAZQUEZ-DOMINGUEZ E. 2002. Phylogeography, historical patterns and conservation of natural areas. Pp. 369-378, in: Protected areas and the regional planning imperative in North America (G Nelson, JC Day, LM Sportza, J Loucky, and C Vasquez, eds.). University of Calgary Press, Edmonton, Canada. VILA C. 2003. Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society: Series B, Biological Sciences 270:91-97.

VILA C, P SAVOLAINEN, JE MALDONADO, IR AMORIM, JE RICE, RL HONEYCUTT, KL CRANDALL, J LUNDEBERG, and RK WAYNE. 1997. Multiple and ancient origins of the domestic dog. Science 276:1687-1689.

WAYNE RK. 1991. A morphologic and genetic study of the island fox, Urocyon littoralis. Evolution 45:1849-1868.

WAYNE RK. 1992. On the use of molecular genetic characters to investigate species status. Conservation Biology 6:590-592.

WAYNE RK. 1997. Molecular systematics of the Canidae. Systematic Biology 46:622-653.

WAYNE RK and DM BROWN. 2001. Hybridisation and conservation of carnivores. Pp. 145-162, in: Carnivore conservation (JL Gittleman, S Funk, DW Macdonald, and RK Wayne, eds.). Cambridge University Press, Cambridge, UK.

WAYNE RK and SM JENKS. 1991. Mitochondrial DNA analysis supports extensive hybridization of the endangered red wolf (Canis rufus). Nature 351:565-568.

WAYNE RK and EA OSTRANDER. 1999. Origin, genetic diversity, and genome structure of the domestic dog. BioEssays 21:247-257.

WABAKKEN P, A ARONSON, TH STR0MSETH, H SAND, L SVENSSON, and I KOJOLA. 2005. The wolf in Scandinavia: Status report of the 2004-2005 winter. Hogskolan i Hedmark, Oppdragsrapport nr. 6-2005. (in Norwegian with English summary).

WHEELDON TJ, BR PATTERSON, and BN WHITE. 2010. Sympatric wolf and coyote populations of the western Great Lakes region are reproductively isolated. Molecular Ecology 19:4428-4440.

WILSON PJ. 2000. DNA profiles of the eastern Canadian wolf and the red wolf provide evidence for a common evolutionary history independent of the gray wolf. Canadian Journal of Zoology 78:2156-2166.

WOLF DE, N TAKEBAYASHI, and LH RIESEBERG. 2001. Predicting the risk of extinction through hybridization. Conservation Biology 15:1039-1053.

ZINK RM. 2002. Methods in comparative phylogeography, and their application to studying evolution in the North American aridlands. Integrative and Comparative Biology 42:953-959.

Pablo A. Martinez (1), Juan P. Zurano (2), Wagner F. Molina (1), and Claudio J. Bidau (3)

(1) Departamento de Biologia Celular, Centro de Biociencias, Universidade Federal do Rio Grande do Norte, Natal, RN, Brasil.

(2) Centro de Rehabilitacion y Cria de Animales Silvestres, Parque Ecologico 'El Puma' Candelaria, Misiones, Argentina.

(3) Universidad Nacional de Rio Negro, Sede Alto Valle, Tacuari 668, 8336 Villa Regina, Rio Negro, Argentina; present address: Parana y Los Claveles, 3304, Garupa, Misiones, Argentina [Correspondence: <bidau47@yahoo.com>].
COPYRIGHT 2013 Sociedad Argentina para el Estudio de los Mamiferos
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2013 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:texto en ingles
Author:Martinez, Pablo A.; Zurano, Juan P.; Molina, Wagner F.; Bidau, Claudio J.
Publication:Mastozoologia Neotropical
Date:Jun 1, 2013
Words:7820
Previous Article:Dimorfismo sexual en la pelvis de Lama guanicoe (Artiodactyla, Camelidae): un caso de aplicacion en el sitio Paso Otero 1, Buenos Aires, Argentina.
Next Article:Diferenciacion geografica en caracteres de la morfologia craneana en el roedor subterraneo Ctenomys australis (Rodentia: Ctenomyidae).
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters