Tendencias en la investigacion sobre especies terrestres del orden Carnivora.
The members of the order Carnivora display great diversity in their demography, body size, feeding habits, behavior, home range, and habitats (Gittleman et al., 2001). Frequently, members of this order are essential in determining the structure of the terrestrial communities, primarily as a result of their ecological role in trophic webs and their effects on the different groups present in the environments they inhabit (Terborgh et al., 1999; Gittleman and Gompper, 2005).
Many conservation strategies may be based on carnivorous mammals (Loyola et al., 2008). Nevertheless, for these strategies to be effective, they require reliable information on the population dynamics, distribution, and ecological requirements of the species of interest, as well as the impact they have on their ecosystems (Ray et al., 2005).
However, the degree of information for each species is often not homogeneous (Ginsber, 2001), and the compilation and analysis of the issues addressed in the scientific literature are available only for some groups. In previous works, some studies have analyzed the information about particular groups in specific regions, such as those conducted for the family Canidae and Felidae in South America (Medel and Jaksic, 1988; Lucherini et al., 2004; Clavijo and Ramirez, 2009). For some species, such as puma Puma concolor (Lopez-Gonzalez and Gonzalez, 1998), polecat Mustela putorius (Blandford, 2008), genet Genetta genetta (Virgos et al., 1999), and European badger Meles meles (Rope and Mickevicius, 1995), reviews of particular issues, such as diet, are available.
These studies show the advance of knowledge in one or more disciplines, as well as areas where more research is needed for each group. But there is no previous work to provide a perspective on this situation for the order Carnivora as a whole. This work aims to provide information on trends in research on the order Carnivora in terms of topics and species that have been addressed in the scientific literature in the last three decades, and to make recommendations to guide future research.
MATERIALS AND METHODS
We reviewed the contents of fifteen internationally circulating scientific journals and recorded the number of articles published between 1980 and 2010 that made reference to one or more species of the order Carnivora. This was considered as the adequate period of time to provide an overview on recent research with this group.
The journals consulted were Studies on Neotropical Fauna and Environmental, The Southwestern Naturalist, Journal of Animal Ecology, Journal of Zoology, Journal of Mammalogy, Mammalia, Mammal Review, Mastozoologia Neotropical, Small Carnivore Conservation, Canid News, Cat News, African Journal of Ecology, Journal of East African Natural History, South African Journal of Wildlife Research, and Raffles Bulletin of Zoology. These journals were selected because of their relevance, availability, and because they published a wide range of topics, including diversity in general (two journals), zoology (six), mammals (four), and carnivores specifically (three). To avoid bias in the percentage of subjects covered, we did not include journals that address a specific topic such as conservation, distribution or diseases, to name a few. Although these journals are edited mainly in Europe (9), the Americas (3), and Africa (3), they include studies addressing species from around the world.
For each article, we recorded the species, general topic, and country in which the study was performed. The articles were classified into 16 topics (Table 1), according to the content expressed in the title and abstract. In the classification of the topics we followed Guevara Chumacero et al. (2005), with some modifications.
The studies were analyzed on both a global level and by continent, as well as by the most studied topics, species, and families, with respect to the total number of published articles. As species richness varies across continents, the number of articles published on each continent was expressed as a proportion (PAC = the number of articles published in each continent/the number of species present in that continent). Likewise, when comparing the number of studies for each family, the number of contributions referring to a given family was expressed as a proportion of the number of species each family contains (PAF = the number of articles published per family/the number of species per family). In addition, the publication Mammalian Species, which includes monographs of species from around the world, was reviewed to get an idea of rogress in knowledge of species of this order. We considered that the species included in this publication are relatively well understood in terms of natural history, distribution and ecology. In this study we followed the taxonomy proposed by Wilson and Mittermeier (2009).
We recorded a total of 2117 studies and of these, the 14.8% were published in the 1980s, the 29.9% in the 1990s, and the 55.3% in the 2000s. Of the 2117 studies found, 758 (35.8%) were performed in the Americas, 476 (22.48%) in Europe, 390 (18.42%) in Africa, and 417 (19.7%) in Asia. The remaining (3.6%) were works spanning more than one continent (72 studies), or were conducted in Oceania (five studies). The most studied topics were distribution, diet, ecology, and natural history, both globally and in each continent (Table 1). In contrast, the topics less addressed were taxonomy, evolution, genetics and zoosanitary issues. Considering the number of contributions as a proportion with respect to the number of carnivore species present on each continent, Europe displayed the highest value (PAC = 20.7), followed by the Americas (PAC = 9.5). Asia and Africa displayed low and similar values (PAC = 4.0 and PAC = 4.6, respectively).
The families with fewer studies were Eupleridae, Mephitidae and Herpestidae, and the families most studied were Mustelidae, Canidae and Felidae, both globally and by continents (Table 2). The articles published on the global level made reference to 196 of the 245 known terrestrial species of Carnivora in the world (Wilson and Mittermeier, 2009). Of these 196 species, the most studied were the European badger M. meles and the coyote Canis latrans, followed by the red fox Vulpes vulpes, and the river otter Lutra lutra, the lion Panthera leo, the wolf Canis lupus, the leopard Panthera pardus, and the puma (Table 3).
From a total of 73 species registered in this review for the Americas, the most studied species were the coyote (84 articles), the puma (55), the black bear Ursus americanus (51), the jaguar Panthera onca (41) and the wolf (38). In Europe, we recorded 35 species, included 11 non-native species, as for example the giant panda Ailuropoda melanoleuca native of Asia, and the fosa Cryptoprocta ferox native of Africa. The most studied species were the European badger (118 articles), the river otter (67), and the red fox (48). In Asia, the leopard and the tiger Panthera tigris (27 articles, each), the giant panda (13 articles), the European mink Mustela lutreola (11), and the Owston's palm civet Chrotogale owstoni (10) were the most studied out of a total of 83 registered species. In Africa, the most studied species were the lion (61 articles), the spotted hyena Crocuta crocuta (42), the cheetah Acinonyx jubatus (35), the African wild dog Lycaon pictus (34), and the leopard (28) out of a total of 60 registered species.
Of the 848 monographs published in Mammalian Species, 105 belong to the order Carnivora. Thus, 42.9% of the carnivores have a monograph: 28% of the monographs corresponds to mustelids (29 species), 26% to canids (28 species), 12% to felines (13 species), and 10% to herpestids (11 species). The remaining 24% is distributed among the other families. For the families Canidae and Hyaenidae, between 80 y 75% of their species already have a monograph in this journal; for the families Ursidae, Mustelidae, and Mephitidae, between 50 and 60%; for the families Procyonidae, Felidae and Herpestidae, between 40 and 30%, and for the families Eupleridae and Viverridae, about 10%. No species of the families Nandiniidae and Prionodontidae (one and two species, respectively), have monographs to the date of this review.
Although the thematic analysis presented here does not represent the entirety of the studies performed on species of the order Carnivora on the global level, and although we did not take into account information published in regional journals, we think it does give a realistic and updated view of the research trends for this order.
Field work for the articles included in this study was concentrated in Europe and the Americas, leaving the remaining continents with a low proportion of studies. The greatest proportion of studies was carried out in Europe (PAC = 20.7), despite the fact that this continent has fewer terrestrial species (24 species). In contrast, the proportion of studies carried out in Asia was low (PAC = 4.0) in spite of the fact that the species richness of this continent is quite high (104 species).
The production of published articles on a global scale has principally focused on few families. Of the 13 terrestrial families that make up the order Carnivora, just three summed 70.3% of the total number of publications: Felidae, Mustelidae and Canidae. Of the remaining ten families, six (Eupleridae, Herpestidae, Mephitidae, Nandiniidae, Viverridae, and Prionodontidae) were scarcely studied. This low number of studies may be due to the species richness of each family. However, the ursids, despite having the same species richness as euplerids (eight species), have a considerably larger proportion of studies. In contrast, although the viverrids constitute almost the same number of species as canids (34 vs. 35 species, respectively), they have a considerably smaller proportion of studies (3.1 vs. 13.1).
In addition, we found a wide variety of species groups that have not been researched within the areas in which they are distributed. For example, the proportions of studies generated on the families Viverridae, Herpestidae, and Eupleridae were low in Africa or in Asia, although these two continents include most of the range of these three families. The families Procyonidae and Mephitidae faced the same situation in the Americas. Heterogeneous representation of families was also seen in the percentage of appearance in Mammalian Species. More than half of the 105 species with a monograph in the journal belong to the families Canidae and Mustelidae, whereas the families Herpestidae, Procyonidae, Viverridae, and Eupleridae are little represented. That is, close to 70% of the species that makes up these families lack of the general descriptions provided by this journal.
The studies published over the last three decades are concentrated on few species, generally large in size, habitat generalists, or charismatic, such as M. meles, L. lutra, C. latrans, P leo, and A. melanoleuca. In contrast, other species groups, generally little charismatic, small sized, or those that may be difficult to observe and study due to their habitats or behavior, have received less attention. This is the case of many small cats, the procyonids Nasuella olivacea, Bassaricyon alleni, and B. gabbii, the canid Nyctereutes procyonoides, the mustelids M. felipei, and M. lutreolina, and the viverrid G. thierryi, to mention a few.
In terms of research topics, this review revealed that the distribution and diet were the most recurrent aspect in studies within the order Carnivora, especially for the families Felidae, Mustelidae and Canidae. However, for some species even basic aspects such as natural history, breeding behavior and habitat association remain unknown (Wilson and Mittermeier, 2009), among which are the herpestids Helogale hirtula and Herpestes semitorquatus, the mustelids M. felipei and M. lutreolina, or the viverrids G. bourloni , G. poensis, and G. thierryi.
Added to this, the lack of knowledge of some aspects has contributed to discrepancies in the systematics of some species of the order Carnivora. In such circumstances are South American cats, which have a long history of changes in their taxonomy, even in recent years (Clavijo and Ramirez, 2009; Wilson and Mitttermeier, 2009). A similar problem also face the procyonids Procyon insularis, Nasua nelsoni (Cuaron et al., 2004), B. beddardi, B. lasius, and B. pauli, or the mustelid Lutra nippon (Wozencraft, 2005; Wilson and Mittermeier, 2009). These differences are also present at the family level in various classifications, such as in the case of Prionodontidae (Wozencraft, 2005; Schipper et al., 2008; Wilson and Mittermeier, 2009). This suggests that studies on genetics, evolution, taxonomy, and morphology are required to help the clarification of the systematics of the order Carnivora (Cuaron et al., 2004; Clavijo and Ramirez, 2009).
Although some authors consider that conservation efforts do not require an understanding of all aspects for the species of interest (Ginsber, 2001), knowledge of ecological requirements is necessary, especially in cases where the risk of extinction is found to be significant, to appropriately channel conservation actions and resources (Ginsberg, 2001; Meiri, 2005; Jenning and Veron, 2009). However, the lack of studies on groups of species may hamper the accurate identification of their conservation status within each region, there may be discrepancies in terms of risk category assessment between the local conservation perspective and the global conservation perspective (Dalerum et al., 2009). As a result of this situation, only a few of the species in this order have been classified in a higher risk category in the international context (Schipper et al., 2008; IUCN, 2010). Therefore it is advisable to collect information on various aspects of threatened species in order to make it possible to reevaluate the conservation status (Schipper et al., 2008).
Some research indicates that the regions of Asia, Africa and South America have high species richness (Mills et al., 2001; Dalerum et al., 2009). However, is in these places where a large number of species are at risk (Servheen et al., 1999; Cardillo et al., 2004; Mills et al., 2005). Despite this diversity and degree of threat, these regions do not excel in the number of published studies. It would be important to increase the number of studies on native species of these regions before the environmental changes drastically affect these populations.
Future research should be directed towards addressing topics other than natural history, such as genetics, habitat selection, activity patterns, or zoosanitary issues. Similarly, it is advisable to expand the scope of future studies to include little studied groups, especially threatened species, small-sized species, and species which are not very abundant or charismatic. Given this situation, the study of aspects such as population trends or demography, as well as community level ecology, is needed in order to understand under what circumstances or through what ecological patterns, communities are developed and maintained, with the aim of maximizing the effectiveness of conservation actions and resources.
Recibido 10 octubre 2012. Aceptado 5 abril 2013. Editor asociado: F Prevosti
Gabriela Perez-Irineo and Antonio Santos-Moreno
Laboratorio de Ecologia Animal, Centro Interdisciplinario de Investigacion para el Desarrollo Integral Regional, Unidad Oaxaca, Instituto Politecnico Nacional, Hornos 1003, 71230 Santa Cruz Xoxocotlan, Oaxaca, Mexico [Correspondence: Gabriela Perez Irineo <firstname.lastname@example.org>].
The authors would like to thank the Mexican Consejo Nacional de Ciencia y Tecnologia and Instituto Politecnico Nacional for its generous funding of the graduate studies of the first author, and G. Ramos-Fernandez for his valuable comments on this work.
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Table 1 Percentage of articles on different research topics for the order Carnivora, from 1980 to 2010. Topic Subtopic The Americas Abundance Density, relative abundance 3.3 Home Range Territory 4.0 Diet Preference, habits 14.7 Natural History Metabolism, reproduction, 12.8 physiology Conduct Activity patterns, behavior 8.5 Conservation Species at risk, programs, risk 6.6 Distribution New records, zoogeography, 13.7 dispersal Ecology Diversity, predation, 14.7 competition Evolution Phylogeny, paleontology 1.8 Genetics Alleles, genetic variation 4.9 Zoosanitary Issues Diseases, zoonosis, parasites 1.5 Methods Efficiency, comparisons, new 2.1 techniques Morphology Morphometry, size, weight 5.6 Taxonomy Classification, systematic 1.3 Habitat Use Selection, preference 2.9 Other Ethnozoology, hunting/poaching, 1.6 literature reviews Topic Africa Asia Europe Total Abundance 2.1 2.8 5.3 3.5 Home Range 2.3 0.7 2.9 2.6 Diet 17.4 7.9 16.0 13.7 Natural History 9.0 5.7 13.0 10.7 Conduct 12.3 4.8 7.1 7.9 Conservation 12.1 18.2 8.4 10.6 Distribution 14.4 32.6 14.9 17.4 Ecology 9.5 11.2 8.0 11.1 Evolution 0.8 0.4 0.6 1.5 Genetics 1.8 0.9 3.2 3.1 Zoosanitary Issues 2.8 1.6 5.0 2.6 Methods 3.8 2.9 5.3 3.4 Morphology 3.4 2.9 6.7 5.7 Taxonomy 0.3 2.4 0.0 1.1 Habitat Use 5.9 1.6 1.9 2.9 Other 2.1 3.2 1.7 2.2 Table 2 Species richness and the number of published works per family of mammalian carnivores between 1980 and 2010 on the global level and by continent. References: a = total species richness, b = number of species with at least one work, c = number of published articles, d = proportion of studies (PAF = the number of articles published per family/number of species of the family). Globally The Americas a b c d a b c d Ailuridae 1 i 10 10 Canidae 35 30 457 13.1 18 17 267 14.8 Euplerida 8 6 13 1.6 Felidae 37 36 530 14.3 15 11 152 10.1 Herpestidae 34 20 58 1.7 1 3 Hyaenida 4 4 52 13 Mephitidae 12 9 27 2.2 10 8 26 2.6 Mustelidae 57 46 501 8.8 21 21 111 5.3 Nandiniidae 1 1 3 3 Prionodontidae 2 2 7 3.5 Procyonidae 12 11 82 6.8 12 11 74 6.2 Ursidae 8 8 134 16.7 4 4 86 21.5 Viverridae 34 22 107 3.1 Order 136 39 TOTAL 245 196 2117 80 73 758 Europe Africa a b c d a b c d Ailuridae 1 1 Canidae 4 7 76 19 14 9 82 5.8 Euplerida 2 3 8 6 10 1.2 Felidae 4 5 49 16.3 10 10 139 13.9 Herpestidae 2 3 6 6 25 13 29 1.7 Hyaenida 4 4 49 12.2 Mephitidae 1 2 Mustelidae 11 11 292 24.3 7 5 25 3.6 Nandiniidae 1 1 3 3 Prionodontidae Procyonidae 1 Ursidae 2 3 21 10.5 Viverridae 1 3 11 11 16 11 22 1.4 Order 15 30 TOTAL 24 35 476 85 60 390 Asia a b c d Ailuridae 1 1 9 9 Canidae 11 11 37 3.3 Euplerida Felidae 21 20 155 7.4 Herpestidae 9 7 20 2.2 Hyaenida 1 1 2 2 Mephitidae 2 Mustelidae 33 21 60 1.8 Nandiniidae Prionodontidae 2 2 7 3.5 Procyonidae Ursidae 6 5 23 3.8 Viverridae 18 15 70 3.9 Order 34 TOTAL 104 83 417 Table 3 Species of the order Carnivora with the greatest quantity of published works from 1980 to 2010. References: A = refers to whether the species has a review in Mammalian Species, B = number of species by family to have a review within Mammalian Species, C = the value of B expresses as a percentage. Family Species Number of Mammalian Articles Species Presence (A) Ailuridae Ailurus fulgens 10 X Canidae Canis latrans 84 X Vulpes vulpes 72 X Canis lupus 60 X Lycaon pictus 35 Vulpes macrotis 23 X Lycalopex culpaeus 19 X Vulpes lagopus 17 X Canis mesomelas 14 X Chrysocyon brachiurus 14 Eupleridae Crytoprocta ferox 5 Mungotictis decemlineata 3 Felidae Panthera leo 62 X Panthera pardus 57 Puma concolor 55 X Acinonyx jubatus 45 X Panthera onca 41 X Lynx rufus 33 X Panthera tigris 31 X Lynx lynx 25 X Leopardus pardalis 16 X Herpestidae Ichneumia albicaudata 4 Hyaenidae Crocuta crocuta 17 Hyaena brunnea 3 X Mephitidae Mephitis mephitis 11 X Spilogale putorius 7 X Mustelidae Meles meles 123 Lutra lutra 70 Neovison vison 38 X Mustela lutreola 32 X Martes pennanti 13 X Martes americana 12 X Mustela putorius 12 Martes martes 11 Gulo gulo 10 X Nandiniidae Nandinia binotata 3 Prionodontidae Prionodon pardicolor 6 Prionodon linsang 1 Procyonidae Procyon lotor 32 X Nasua narica 9 X Ursidae Ursus americanus 51 X Ursus arctos 24 X Ursus maritimus 22 X Ailuropoda melanoleuca 15 X Viverridae Genetta genetta 14 X Chrotogale owstoni 13 Viverricula indica 6 Family Species Mammalian Species Number of Presence Species Percentage Present (B) (C) Ailuridae Ailurus fulgens 1 100 Canidae Canis latrans 28 80 Vulpes vulpes Canis lupus Lycaon pictus Vulpes macrotis Lycalopex culpaeus Vulpes lagopus Canis mesomelas Chrysocyon brachiurus Eupleridae Crytoprocta ferox 1 12.5 Mungotictis decemlineata Felidae Panthera leo 13 35.1 Panthera pardus Puma concolor Acinonyx jubatus Panthera onca Lynx rufus Panthera tigris Lynx lynx Leopardus pardalis Herpestidae Ichneumia albicaudata 11 32.3 Hyaenidae Crocuta crocuta 3 75 Hyaena brunnea Mephitidae Mephitis mephitis 6 50 Spilogale putorius Mustelidae Meles meles 29 50.8 Lutra lutra Neovison vison Mustela lutreola Martes pennanti Martes americana Mustela putorius Martes martes Gulo gulo Nandiniidae Nandinia binotata 0 0 Prionodontidae Prionodon pardicolor 0 0 Prionodon linsang Procyonidae Procyon lotor 5 41.7 Nasua narica Ursidae Ursus americanus 5 62.5 Ursus arctos Ursus maritimus Ailuropoda melanoleuca Viverridae Genetta genetta 3 8.8 Chrotogale owstoni Viverricula indica
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