Drivers of jaguar (Panthera onca) and puma (Puma concolor) predation on endangered primates within a transformed landscape in southern Mexico

Human pressures have increasingly placed keystone species, such as large cats, under threat. Together with forest loss, prey depletion is one of the main threats to the survival of jaguars (Panthera onca) and pumas (Puma concolor) throughout the Neotropics. Generally, primates are not considered main prey for jaguar and puma, and their inclusion in the diet could be indicative of ongoing prey species decline. Here, we investigate the effect of habitat type and disturbance on primate predation by large cats. Surveys took place during the dry seasons (March to June) of 2010 and 2011, covering a total of 608.5 km across 24 localities in the Uxpanapa Valley, Mexico. We found 65 felid scat samples with the aid of a wildlife scat detection dog, and then examined them to identify predator species and classify the prey remains they contained. Primates represented the most frequent prey (35%) for both jaguar and puma in our study site and constituted approximately half of the biomass consumed by these felines in the area. Primate remains were more likely to be found in scats surrounded by the lowest percentage of conserved forest or in areas surrounded by more villages, showing the potential effects of human activities on these species' populations. The high proportion of primates found in scats within our study site could be an early indication that populations of ungulates and other “typical” prey are beginning to collapse, and urgent conservation interventions are needed for both large cats and primates before they become locally extinct. Abstract in Spanish is available with online material.     

Differential impact of landscape transformation on pumas (Puma concolor) and jaguars (Panthera onca) in the Upper Paraná Atlantic Forest

Aim Jaguars and pumas, being similar in size and behaviour, are the largest felids of the Neotropics. However, pumas appear to be more resistant to human impacts. Our objective was to compare the response of both species with human impacts at a regional scale in a highly modified region where both species had continuous distribution in the past. Location The Upper Parana Atlantic Forest (UPAF). Methods Pumas and jaguars presence‐only data were used in an Ecological Niche Factor Analysis (ENFA). From the total number of records, we resampled 95 records of each species 10 times to characterize and compare their habitat requirements, built habitat‐suitability maps and examined interspecific differences in niche parameters related to present landscape characteristics. Results Both species showed high dependence on native forest and habitat protection, and low tolerance to anthropogenic environments. However, jaguars showed higher differences between their optimal habitat and the available landscape (mean ± SD; marginality M = 2.290 ± 0.072) and lower tolerance to deviations from their optimal habitat (tolerance T = 0.596 ± 0.013) than pumas (M = 1.358 ± 0.067, P < 0.001; T = 0.742 ± 0.022, P < 0.001). Although their niches highly overlapped (Pianka’s O = 0.746 ± 0.069), pumas’ higher tolerance resulted in a larger area covered by suitable patches of habitat with higher connectivity. All jaguar‐suitable areas were also suitable for pumas; however, 44 ± 8% of puma‐suitable areas were unsuitable or marginal for jaguars. Main conclusions Pumas showed more tolerance than jaguars to human impacts at a regional scale in the UPAF, a pattern also observed at local and continental scales. Although the proximate factors responsible for the differential response of pumas to human‐altered environments seem to be similar at all spatial scales (e.g. broader trophic niche than jaguars), the resultant spatial configuration of suitable habitat at a regional scale might be another important factor determining puma persistence and higher jaguar demands on conservation efforts.     

Noninvasive individual and species identification of jaguars (Panthera onca), pumas (Puma concolor) and ocelots (Leopardus pardalis) in Belize,Central America using cross‐species microsatellites and faecal DNA

There is a great need to develop efficient, noninvasive genetic sampling methods to study wild populations of multiple, co‐occurring, threatened felids. This is especially important for molecular scatology studies occurring in challenging tropical environments where DNA degrades quickly and the quality of faecal samples varies greatly. We optimized 14 polymorphic microsatellite loci for jaguars (Panthera onca), pumas (Puma concolor) and ocelots (Leopardus pardalis) and assessed their utility for cross‐species amplification. Additionally, we tested their reliability for species and individual identification using DNA from faeces of wild felids detected by a scat detector dog across Belize in Central America. All microsatellite loci were successfully amplified in the three target species, were polymorphic with average expected heterozygosities of H_E = 0.60 ± 0.18 (SD) for jaguars, H_E = 0.65 ± 0.21 (SD) for pumas and H_E = 0.70 ± 0.13 (SD) for ocelots and had an overall PCR amplification success of 61%. We used this nuclear DNA primer set to successfully identify species and individuals from 49% of 1053 field‐collected scat samples. This set of optimized microsatellite multiplexes represents a powerful tool for future efforts to conduct noninvasive studies on multiple, wild Neotropical felids.     

Characterization of microsatellite loci in the Jamaican fruit‐eating bat Artibeus jamaicensis and cross‐species amplification

Artibeus jamaicensis is one of the most common bat species in the neotropics, with a well‐defined polygynous social structure in caves. In order to study behaviour and to examine patterns of paternity and relatedness between different harem groups, we developed 14 microsatellite loci from two different enriched genomic libraries. We screened 125 individuals from two different bat colonies and found that polymorphism ranged from five to 13 alleles. Heterozygosity ranged from 63 to 95%. The primers amplified across 14 bat species, indicating their potential utility for population‐level studies in several closely related bat species.     

Jaguar (Panthera onca) feeding ecology: distribution of predator and prey through time and space

Jaguars Panthera onca inhabiting tropical or subtropical evergreen moist forest have often been classified as opportunistic predators because they consume prey relative to its availability. However, these studies failed to address simultaneously the distribution of predator and prey through time and space, which may lead to an incomplete or erroneous understanding of jaguar foraging strategies. In this study, we reconstructed jaguar diet from scat, and used camera traps to investigate jaguar prey availability and the distribution of jaguar and its prey through space and time. We focused our examination of predator–prey temporal and spatial relations on forest infrastructure comprising man-made paths, small mammal trails, tapir Tapirus bairdi trail and trail-less, forested areas as they represent distinct habitats for prey selection. Overall, we observed high overlap between the prey used and available, suggestive of opportunistic foraging. However, jaguars exhibited selective tendencies in discriminating between larger prey. Jaguars used collared peccary Tayassu tajacu greater than its availability, while preying upon the equally abundant and similarly distributed white-lipped peccary Tayassu pecari and tapir less than predicted based upon availability. Armadillo Dasypus novemcinctus and paca Agouti paca , 56.6% of total consumption, were consumed relative to availability but exhibited low spatial overlap with jaguar. Armadillo and paca used trail-less, forested areas and small mammal trails not used by jaguar and were photographed more frequently at greater distances from man-made paths, major thoroughfares for jaguars. This study suggests that although forest jaguars use prey relative to its abundance, jaguars may rely on foraging strategies other than chance encounters for exploiting prey.     

A Comparative Analysis of Genetic Diversity and Structure in Jaguars (Panthera onca), Pumas (Puma concolor), and Ocelots (Leopardus pardalis) in Fragmented Landscapes of a Critical Mesoamerican Linkage Zone

With increasing anthropogenic impact and landscape change, terrestrial carnivore populations are becoming more fragmented. Thus, it is crucial to genetically monitor wild carnivores and quantify changes in genetic diversity and gene flow in response to these threats. This study combined the use of scat detector dogs and molecular scatology to conduct the first genetic study on wild populations of multiple Neotropical felids coexisting across a fragmented landscape in Belize, Central America. We analyzed data from 14 polymorphic microsatellite loci in 1053 scat samples collected from wild jaguars (Panthera onca), pumas (Puma concolor), and ocelots (Leopardus pardalis). We assessed levels of genetic diversity, defined potential genetic clusters, and examined gene flow for the three target species on a countrywide scale using a combination of individual- and population-based analyses. Wild felids in Belize showed moderate levels of genetic variation, with jaguars having the lowest diversity estimates (H_E = 0.57 ± 0.02; A_R = 3.36 ± 0.09), followed by pumas (H_E = 0.57 ± 0.08; A_R = 4.20 ± 0.16), and ocelots (H_E = 0.63 ± 0.03; A_R = 4.16 ± 0.08). We observed low to moderate levels of genetic differentiation for all three target species, with jaguars showing the lowest degree of genetic subdivision across the country, followed by ocelots and pumas. Although levels of genetic diversity and gene flow were still fairly high, we detected evidence of fine-scale genetic subdivision, indicating that levels of genetic connectivity for wild felids in Belize are likely to decrease if habitat loss and fragmentation continue at the current rate. Our study demonstrates the value of understanding fine-scale patterns of gene flow in multiple co-occurring felid species of conservation concern, which is vital for wildlife movement corridor planning and prioritizing future conservation and management efforts within human-impacted landscapes.     

Predicting potential distribution of the jaguar (Panthera onca) in Mexico: identification of priority areas for conservation

Aim The jaguar, Panthera onca, is a species of global conservation concern. In Mexico, the northernmost part of its distribution range, its conservation status, is particularly critical, while its potential and actual distribution is poorly known. We propose an ensemble model (EM) of the potential distribution for the jaguar in Mexico and identify the priority areas for conservation. Location Mexico. Methods We generated our EM based on three presence‐only methods (Ecological Niche Factor Analysis, Mahalanobis distance, Maxent) and considering environmental, biological and anthropogenic factors. We used this model to evaluate the efficacy of the existing Mexican protected areas (PAs), to evaluate the adequacy of the jaguar conservation units (JCUs) and to propose new areas that should be considered for conservation and management of the species in Mexico. Results Our results outline that 16% of Mexico (c. 312,000 km²) can be considered as suitable for the presence of the jaguar. Furthermore, 13% of the suitable areas are included in existing PAs and 14% are included in JCUs ( Sanderson et al., 2002 ). Main conclusions Clearly much more should be carried out to establish a proactive conservation strategy. Based on our results, we propose here new jaguar conservation and management areas that are important for a nationwide conservation blueprint.     

The role of ecologic diversification in sibling speciation of Empidonax flycatchers (Tyrannidae): multigene evidence from mtDNA

Avian genera characterized by sibling species with distinctive habitat preferences present an evolutionary enigma in view of the more commonplace occurrence of syntopic congeners that differ strikingly in colour and pattern. No existing theory has explained the evolutionary background that led to these differences. Here we propose that great phenotypic similarity among some groups of sibling species limits their coexistence and that clues to their radiation can be seen in patterns of geographical occurrence. To illustrate our thesis we focused on the New World flycatcher genus Empidonax, a group of 15 species notorious for their great phenotypic similarity. Using 3069 base pairs of mitochondrial DNA from four genes, we produced a complete molecular phylogeny that identified four clades, three of which represent close relatives. The fourth clade includes only E. virescens, which apparently has no close living relatives. The majority of species, including many distant relatives, are completely (58.1%) or essentially (6.7%) allopatric in breeding distribution and exhibit striking ecological segregation into distinctive climate-vegetation zones. Even where ranges overlap, occupancy of the same habitat by different species is rare. Phylogenetic and distributional patterns in Empidonax suggest a peripatric model of stepwise colonization and then range expansion of small groups of pioneers during glacial periods into initially enlarging, distinctive habitats destined to be widespread during interglacials. Vicariance is not indicated in the absence of barriers of appropriate age and geographical position. Rapoport's rule that northern species have larger ranges than southern species is strongly supported.     

The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca)

Habitat fragmentation may disrupt original patterns of gene flow and lead to drift-induced differentiation among local population units. Top predators such as the jaguar may be particularly susceptible to this effect, given their low population densities, leading to small effective sizes in local fragments. On the other hand, the jaguar's high dispersal capabilities and relatively long generation time might counteract this process, slowing the effect of drift on local populations over the time frame of decades or centuries. In this study, we have addressed this issue by investigating the genetic structure of jaguars in a recently fragmented Atlantic Forest region, aiming to test whether loss of diversity and differentiation among local populations are detectable, and whether they can be attributed to the recent effect of drift. We used 13 microsatellite loci to characterize the genetic diversity present in four remnant populations, and observed marked differentiation among them, with evidence of recent allelic loss in local areas. Although some migrant and admixed individuals were identified, our results indicate that recent large-scale habitat removal and fragmentation among these areas has been sufficiently strong to promote differentiation induced by drift and loss of alleles at each site. Low estimated effective sizes supported the inference that genetic drift could have caused this effect within a short time frame. These results indicate that jaguars' ability to effectively disperse across the human-dominated landscapes that separate the fragments is currently very limited, and that each fragment contains a small, isolated population that is already suffering from the effects of genetic drift.     

Retrospective study of morbidity and mortality of captive jaguars (Panthera onca) in North America: 1982–2002

One hundred seventy‐two medical records of captive jaguars (Panthera onca) were examined from 30 American Zoo and Aquarium Association (AZA) institutions housing jaguars between 1982–2002. The study determined common causes of morbidity and mortality, and the influence of age, gender, and melengestrol‐acetate (MGA) exposure on these rates. The most common causes of morbidity in captive jaguars were found to be dental, gastrointestinal, integumentary, and musculoskeletal diseases. Prevalence of types of disease varied with age, with older animals experiencing a higher prevalence of multiple types of disease. Females developed reproductive disease more frequently than males, and the data suggest that MGA exposure increased the risk of developing female reproductive disease. The most common causes of mortality were reproductive diseases in females and musculoskeletal diseases in males. There was a high rate of neonate and pediatric mortality, primarily due to stillbirths or unexplained neonatal death, trauma, and pneumonia. Other diseases or clinical signs that seemed remarkable were a high prevalence of episodes of epistaxis among young, as well as old, jaguars. Based on these findings, management suggestions for the captive jaguar population are presented. Zoo Biol 0:1–12, 2006. © 2006 Wiley‐Liss, Inc.     

Evolutionary history of bulldog bats (genus Noctilio): recent diversification and the role of the Caribbean in Neotropical biogeography

We present phylogenetic relationships and phylogeographic patterns of the two species of bulldog bats, genus Noctilio. Using a comprehensive sampling of 118 individuals throughout the species distribution, we investigated the distribution of molecular variation in one nuclear and two mitochondrial markers. Phylogenetic trees do not recover Noctilio albiventris as a monophyletic group and point to three similar‐age intraspecific genetic lineages, suggesting cryptic diversity in this taxon. These lineages correspond to the subspecies previously proposed, and are strongly associated with major river basins in South America. Analyses also suggest a very recent origin for the fishing bat Noctilio leporinus, which probably originates from N. albiventris, with a population expansion corresponding to its invasion in South America. Based on our analysis, the speciation event was dated in the Pleistocene epoch and seems to be associated with the variation of the sea level in the Caribbean islands. The present work indicates how phylogeographic studies support the identification of independent evolutionary lineages, driving new systematic/taxonomic investigations, while at the same time shed light on the role of the Caribbean in shaping Neotropical bat fauna diversity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Pollination system of the Pilosocereus leucocephalus columnar cactus (tribe Cereeae) in eastern Mexico

It has been suggested that there is a geographic dichotomy in the pollination systems of chiropterophilous columnar cacti: in intra‐tropical areas they are pollinated almost exclusively by bats, whereas in extratropical areas they are pollinated by bats, birds and bees. However, currently the studies are clumped both taxonomically (mainly Pachycereeae species) and geographically (mainly in the Tehuacan Valley and the Sonoran Desert). This clumping limits the possibility of generalising the pattern to other regions or cactus tribes. Only four of the 36 chiropterophilous cacti in Pilosocereus have been studied. Despite the tropical distribution of two Pilosocereus species, bees account for 40–100% of their fruit set. We examined how specialised is the pollination system of P. leucocephalus in eastern Mexico. As we studied tropical populations, we expected a bat‐specialised pollination system. However, previous studies of Pilosocereus suggest that a generalised pollination system is also possible. We found that this cactus is mainly bat‐pollinated (bats account for 33–65% of fruit set); although to a lesser degree, diurnal visitors also caused some fruit set (7–15%). Diurnal visitors were more effective in populations containing honeybee hives. P. leucocephalus is partially self‐compatible (14–18% of fructification) but unable to set fruit without visitors. Despite the variation in pollination system, P. leucocephalus shows more affinity with other columnar cacti from tropical regions than with those from extratropical regions. Although we report here that a new species of tropical Pilosocereus is relatively bat‐specialised, this Cereeae genus is more flexible in its pollination system than the Pachycereeae genera.     

The Role of Fruits and Insects in the Nutrition of Frugivorous Bats: Evaluating the Use of Stable Isotope Models1

We estimated the relative contribution of fruits and insects as sources of dietary protein in two species of Neotropical frugivorous bats (Artibeus jamaicensis and Sturnira lilium) using stable carbon and nitrogen isotope analyses. An insectivorous species (Pteronotus parnellii) was also included for comparison. We found constant patterns in stable carbon and nitrogen isotope composition in blood that separated the two species of frugivorous bats from the insectivorous bat. When we used these isotopic values (combined with those of dietary fruits and insects) to estimate the percent contribution of fruits and insects to the diet of the bats, we obtained different results, depending on assumptions and model adopted. We tested models using both 8“N and 8′³C results simultaneously and separately and further used diet‐tissue fractionation factors of 3%o for nitrogen and 1 and 3.5%o for carbon. We found that a carbon‐based model with a diet‐blood enrichment factor of 3.5%o produced the most parsimonious results. The model estimated that A. jamaicensis and S. lilium obtained most of their protein requirements from fruits, whereas P. parnellii fed mostly on insects. No sexual or seasonal variations in the diet of the two frugivorous species were detected. We found no evidence that the diet of sexually active females differed from that of nonsexually active females in the two species of frugivorous bats. We suggest that future studies better define isotopic fractionation between diet and tissues of bats using captive rearing and controlled diets.     

Patterns of growth of the mandibular corpus in spotted hyenas (Crocuta crocuta) and cougars (Puma concolor)

Differences in jaw morphology among adult carnivorans are well established, but the ontogenetic mechanisms by which these differences arise are largely unexplored. Mandibular ontogeny in Crocuta crocuta and Puma concolor is analysed biomechanically using principles of beam theory. In each species, the development of cross-sectional properties of the mandibular corpus associated with rigidity under loading follows a biphasic pattern of growth. In early postnatal growth, deposition of cortical bone appears to be constrained by the overall weaker tissue with which juvenile skeletons are constructed and by the need to volumelrically accommodate the developing teeth within their bony crypts. Thus, this stage of growth is characterized by a net periosteal deposition of bone and a swelling of the medullary cavity. In late postnatal growth, the constraints on endosteal deposition of bone are relieved as the permanent teeth erupt; thus, cortical thicknesses increase sharply by periosteal expansion as well as medullary contraction. Finally, it is noted that basic differences in jaw construction between Crocuta and Puma appear to develop prenatally as they are largely in place at birth. Hence, postnatal development enhances, but does not soley contribute to, the biomechanical differences in the jaws of these species.     

Determination of the Minimum Population Size of Pumas (Puma concolor) Through Fecal DNA Analysis in Two Protected Cerrado Areas in the Brazilian Southeast

Pumas ( Puma concolor ) are an endangered species due to habitat loss and the ever-growing conflict with expanding human populations. We used genetic analysis of feces, a noninvasive study method, to determine the presence of pumas and their estimated minimum population in two protected areas in the northeast of São Paulo State, Brazil: Jataí Ecological Station and Vassununga State Park. We were able to identify the species that originally deposited the feces by means of amplification of a portion of the mitochondrial cytochrome b gene and comparison of this fragment with reference sequences from pumas and other carnivores present in the region. We used a panel containing four microsatellite loci to individualize each of the samples collected. Among the 20 fecal samples, we identified 10 as clearly belonging to pumas and two as belonging to ocelots ( Leopardus pardalis ), a species sympatric with P. concolor . By plotting the feces sampling points against a satellite image, we determined the presence of at least nine puma individuals in the region, three in the Jataí Ecological Station, four in the Vassununga State Park, and two in their surroundings. The identity probability was 0.0001 and the occurrence of allelic dropout was 10.6 percent. The presence of pumas, the estimate of their minimum population size, as well as their distribution, constitute an important tool for the implementation of management and conservation programs in the areas studied and their surroundings.     

Shape variation in surface and cave populations of the armoured catfishes Ancistrus(Siluriformes: Loricariidae) from the São Domingos karst area, upper Tocantins River, Brazil

Body shape of four distinct populations of Ancistrus cryptophthalmus from different caves in the São Domingos karst area and the local epigean (surface) Ancistrus species were compared using geometric morphometrics. Angélica and Bezerra catfishes were closer to each other and successively to the studied sample of epigean catfishes than to Passa Três and São Vicente I catfishes. Greater similarity between catfishes from the Angélica‐Bezerra cave system to epigean catfishes than to other cave catfishes may represent a plesiomorphic feature. On the other hand, the present analyses allowed the distinction between Passa Três and São Vicente I catfishes, which inhabited the same cave system. Topographic isolation due to the presence of several waterfalls interposed between the stream reaches where these catfishes live may explain such morphological differentiation. Also, the presence of a waterfall downstream of the reach where the Angélica sample was obtained may have contributed to the partial isolation of these catfishes from those living in Bezerra Cave. Differences in population sizes probably influenced the degrees of morphological differentiation observed among the cave populations. The mosaic distribution of character states indicated that the four populations of A. cryptophthalmus have evolved rather independently, but the continuous variation suggests a recent connection between these populations, perhaps with a limited gene flow. Considering other features such as reduction of eyes and pigmentation, and changes in body shape, a separate species status for the epigean and hypogean Ancistrus species from the São Domingos karst area has been maintained.     

Comparison of frugivory by howling monkeys (Alouatta palliata) and bats (Artibeus jamaicensis) in the tropical rain forest of Los Tuxtlas,Mexico

Information on the fruit diets of howling monkeys and fruit-eating bats in the tropical rain forest of Los Tuxtlas, Mexico was collected for a year to compare the plant species used. Howling monkeys used 19 plant species whereas bats used 32 plant species as fruit sources. Eleven species were common in the diet of both mammals. A rank analysis at the plant species level showed that the fruit diets of Alouatta and Artibeus were very different. In contrast to bats, howling monkeys displayed a seasonal pattern in fruit consumption. Diet overlap between the two mammals was highest during the monkeys' fruit-eating season. Measures of fruit production in eight trees (four species) indicated marked variations in fruit biomass produced and in length of fruiting from tree to tree and species to species. Peaks in fruit production were typical both at the species and the individual tree levels, demonstrating the very patchy nature of the fruit available to the monkeys and the bats.