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Project Title: Population assessment of Belizean jaguars (Panthera onca) through non-invasive demographic, genetic, stress-hormone, and diet analyses

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Research Progress Report Forest Department, Belize. May 06, 2013 Project Title: Population assessment of Belizean jaguars (Panthera onca) through non-invasive demographic, genetic, stress-hormone, and
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Research Progress Report Forest Department, Belize. May 06, 2013 Project Title: Population assessment of Belizean jaguars (Panthera onca) through non-invasive demographic, genetic, stress-hormone, and diet analyses J. Bernardo Mesa Department of Fish and Wildlife Conservation, Virginia Tech; Blacksburg VA; USA Marcella J. Kelly Department of Fish and Wildlife Conservation, Virginia Tech; Blacksburg VA; USA ; Executive Summary The jaguar (Panthera onca) is difficult to study due to its secretive nature, the thick habitat in which it resides, its wide-ranging behavior, the low densities in which it naturally occurs. These factors, in addition to the perceived risk of aggression to humans, are all limitations for conducting jaguar research. Habitat fragmentation and direct killing of jaguars are major threats to their continued existence. Reduction in jaguar numbers has been reported in fragmented and disturbed areas along its entire range. Causes of decline include retaliation in circumstances human-jaguar conflict. This type of conflict appears to be on the rise, especially in areas surrounding the protected areas in Belize. Increased stress levels or even distress caused by anthropogenic disturbances in communities surrounding protected areas could potentially reduce reproductive rates and/or increasing disease mortality. In this study, we examine stress hormones in jaguars occurring inside protected areas and in areas outside of protected areas with known human-jaguar conflict in northern Belize. We conducted jaguar scat surveys in Rio Bravo Conservation and Management Area (both La Milpa and Hill Bank sites), and areas surrounding Indian Church and Shipyard communities, where known human-jaguar conflict occurs. We conducted genetic analysis of scat samples to determine species and individual, hormone analysis to assess stress hormones, and diet analysis of scat samples after verified genetic identification. Our results are preliminary and on-going. We collected 336 scat samples from wild felids from which we were able to extract DNA from 33%. DNA amplification success within protected areas was 63%, while scat found in non-protected areas was 24%. We detected 5 felid species: jaguar, puma, ocelot, jaguarundi and domestic cat. Most jaguar, puma, and ocelot samples were found in protected areas while most jaguarundi and all domestic cat samples were found in non-protected areas. Fecal matter and prey remains are currently being separated. Diet analysis is currently underway and hormone analyses will be completed in June Introduction The jaguar (Panthera onca) is the only representative of the Panthera genus in the Americas, the third largest felid the world, and the largest spotted cat. Habitat fragmentation and habitat loss within the jaguar s range have led to their threatened status and these threats are increasing. The jaguar is considered an umbrella species because it has an extensive home range and it occurs in diverse habitat types (Roberge and Angelstam 2004). Therefore, it is important to conserve jaguars to maintain ecological integrity and protect co-existing species ranging within these highly diverse ecosystems (Davis et al. 2011; Sanderson et al. 2002a). In addition, jaguars have been considered in landscape species conservation approaches (Coppolillo et al. 2004). Extensive spatial distribution, socioeconomic significance (depredation on livestock, human persecution), and species vulnerability are important criteria that jaguars possess, which aid in to designing conservation strategies targeting multiple species across a mosaic landscape (Sanderson et al. 2002b, Coppolillo et al. 2004). Belize has seen a progressive increase in human activities such as hunting, housing developments, forest eradication and conversion to agriculture (Barbier 2001; Davis and Holmgren 2000; Dycka and Baydack 2004; Whitman et al. 1997). Thus, it is likely that humanjaguar conflict is increasing. Local communities are not generally concerned about the risk of jaguar attacks on humans, but rather livestock depredation is the strongest factor provoking human-jaguar conflict (Michaslki et al. 2006). This has led to jaguar killing resulting in a reduction in numbers and, in some areas such as El Chaco, Argentina, local extinction (Altricher et al. 2006; Amorim Conforti and Cascelli de Azevedo 2003). Reduction in jaguar abundance has been reported in fragmented and disturbed areas along its entire range (Altricher et al. 2006; Novack et al. 2005; Wallace et al. 2003; Weber and Rabinowitz 1996); however, the cause is not well understood and does not appear to be due strictly to poaching. One possibility is that increased stress levels or even distress caused by anthropogenic disturbances in communities surrounding protected areas is reducing reproductive rates and/or increasing disease morbidity and mortality. Declining small populations are known to fall into an extinction vortex due to compromised genetics and environmental and demographic uncertainty (Caughley 1994), but little work has been done to incorporate factors such as high stress environments into the equation. The stress response could be classified as either acute or chronic depending on the length of exposure, intensity of the stressor (i.e., threat), and the ability of the individual to find a physiological balance (i.e., acclimatization/acclimation). Acute stress allows an organism to modulate its metabolism, redirecting resources from innate processes like digestion, growth, immune function, and reproduction, to counter an immediate threat (Nelson 2005). When a stress response is sustained over extended periods of time, the organism is thought to be experiencing chronic stress. Glucocorticoids (GCs) are steroid hormones that are produced in response to physiological and pathological demands, and environmental disturbances. These steroid hormones circulate in the blood stream looking for target organs to perform their physiological function, such as control of circadian rhythms, metabolism of carbohydrates, proteins and lipids, enhancing cardiocyte activity, and immune-modulation, among others (Martin and Crump 2003). 2 Depending on the species of interest those corticoids are excreted mainly in feces in the form of fecal glucocorticoid metabolites (FGM) (Möstl and Palme 2002). Chronically elevated GC concentrations induced by a persistent stressor (e.g. deforestation or intense persecution) can have negative effects on the organism, including behavioral, reproductive, metabolic, immune, and neurological function, ultimately having the potential to decrease survival and reproduction. For example, Wasser et al. (1997) showed the use of such a proxy in their study on the effects of logging on the northern spotted owl (Strix occidentalis caurina). Male owls in logged areas had higher concentrations of FGM than those in undisturbed areas. Creel et al. (2002) observed higher FGM concentrations in feces of elk and wolves in relation to the intensity of winter snowmobile activity in Yellowstone National Park. These studies demonstrate that noninvasive FGM can be measured as an indicator of the physiological response of wild animals to anthropogenic activities. However, no study to date has examined FGM concentrations in wild jaguars, or for that matter any wild felid species to assess the impact of high versus low stress environments on adrenal activity. Little is known about the ecology of the largest felid in America. A secretive nature, thick habitat, wide ranging behavior, low densities, and the risk of aggression to humans are limitations for conducting research on jaguars. Recently Kelly and Wultsch (see Wultsch 2009) have assessed genetic structure of the jaguar population in Belize employing scat detector dogs and fecal DNA analysis as a non-invasive technique to survey extant populations. In this study we use scat detector dogs to find scat samples both inside protected areas that are thought to be low stress environments, and outside protected areas in cattle ranching areas thought to be high stress areas for jaguars. We are analyzing scat samples for species and individual identification, diet, and FGM to examine if jaguars outside of protected areas appear to be exhibiting chronic stress loads. Objective 1. Identify areas with high versus low anthropogenic activities and human-wildlife conflict using previously published data, geographical information system data, and expert opinion. We conducted scat surveys in the Rio Bravo Conservation and Management Area (RBCMA); which the largest protected area in Belize ( hectares), accounting for 4% of the total protected land in the country. We surveyed in both La Milpa (unlogged) and in HillBank (sustainably logged). Lowland broad-leaved moist forest is the predominant ecotype at RBCMA. In this area, jaguars are found at densities of 5-6 individuals per 100 km 2. Adjacent to RBCMA is highly modified land, dominated by farmland and cattle ranching surrounding the Mennonite towns of Blue Creek and Shipyard. We conducted scat surveys in this human-dominated landscape where several human settlements such as Blue Creek, Indian Church, San Felipe, San Carlos, among others, describe the occurrence of frequent human-jaguar conflict. It is estimated that humans kill 5 jaguars per year in this region (V. Briggs - Pers. comm.). The jaguar scat survey was conducted during the dry season of Surveys ran from March 2011 until the end of July Objective 2. Collect fecal samples for analysis of fecal glucocorticoid metabolites from freeranging jaguars in the interior protected Belizean forests and in areas of high jaguar-human conflict outside the core of these protected forests over a 3-month period. Mesa received scat detector dog training at Packleader LLC headquarters in Gig Harbor, WA. During a two-week period (in February, 2011) he obtained basic training in the handling of a scat dog for working in the field. Thereafter, Barbara Davenport (Packleader trainer), provided two weeks of extra training in Belize to account for landscape and climatic differences that could affect the performance of the scat detector dog (Figure 1). Scat collection surveys started in mid-march in the protected areas and surrounding conflict zones. After the first month of survey, Boomer, the first scat dog was unable to acclimate to the hot, dry season in our target area in Belize (Figure 2). Therefore, we had to recruit another scat dog named CJ from Packleader. Figure 3 shows CJ performing while searching for scat samples. CJ had a rapid acclimation process, and performed flawlessly under the climatic conditions and terrain. Figure 4 shows Bernardo Mesa-Cruz collecting scat and their subsamples for DNA and hormones analysis. During the entire field season we surveyed approximately 420 km in different habitat types. We collected 336 scats samples from wild felids; with approximately 40% of those samples correspond to large felids. Figure 5 shows the distribution of sample location across the study area. Fecal samples were freeze-dried in December From December to January 2013, fecal DNA extractions were performed in a basic genetics lab at Virginia Tech. A total of 359 extractions, including controls, were completed. Genetic analyses were completed by March of PCR reactions and microsatellite analysis were performed at the Laboratory for Ecological and Conservation Genetics at the University of Idaho. Currently, fecal matter and prey remains are being separated to be able to extract the hormones from feces and run the endocrine analysis (stress hormones). Hormone analyses will be completed by June 2013 at the Smithsonian Conservation Biology Institute in Front Royal, Virginia. DNA amplification success on scat samples was fairly poor. Only 33% of the total number of samples were positive to our gene markers. This percentage is low compared to a previous study done by Claudia Wultsch, former graduate student from Virginia Tech, who obtained about 60% successful DNA amplification for her research focused mainly in protected areas. Interestingly, when the DNA amplification success is calculated by status of land protection, results are congruent to those of Wultsch. DNA amplification success of scat collected by this project within protected areas was 63%, while scat found in non-protected areas was 24%. Preliminary analyses indicate that samples found in non-protected areas had highly degraded DNA, while scat found in protected areas was usually sheltered from the sun by trees. The scat in non-protected areas was directly exposed to the sun. Direct exposure to the sun (e.g., UV rays) affects greatly the viability of DNA in feces. For instance, samples found in protected areas are three times more likely to amplify for DNA than samples found in nonprotected areas (χ²=40.690; P 0.0001). Therefore, we also conducted analysis of mitochondial DNA (mtdna), which is usually present in scat at higher quantities than nuclear DNA (used for microsatellite analysis). This technique allows the identification of species but, it is impossible to 4 identify individuals. We used DNA sequences of a short fragments (308 bp) previously tested by Farrell, Roman and Sunquist in 2000 (Molecular Ecology 9, ). We detected 5 felid species: jaguar, puma (Puma concolor), ocelot (Leopardus pardalis), jaguarondi (Puma yagouaroundi) and domestic cat (Felis silvestris catus). Table 1 summarizes the number of individuals detected by species, sex, and molecular technique used. Figure 5 shows a map of the distribution of the samples by species. Most jaguar, puma, and ocelot samples were found in protected areas. In contrast, most jaguarundi and all domestic cat samples were found outside of protected areas. Objective 3. Analyze the diet in jaguar scats collected for objectives 2 and 3. We collected samples of hair, claws, and teeth from over 30 potential jaguar prey species. Samples were collected at the Belize Zoo, farms around the study sites, and opportunistic sampling from road killed animals (Figure 6). Reference samples are currently under analysis. Prey remains are currently being separated from fecal matter. The diet analysis began in April Currently, there are two VT wildlife science undergraduate students working in this process. Outreach Mesa participated in the 5 th Natural Resource Management Symposium, jointly hosted by UB s Environmental Research Institute (ERI) and MSBC Belize Chapter on March 25, 2011 (Figure 7). Mesa gave a short presentation about this project and future work. In addition, we presented a poster with previous data showing validation, degradation of the FGM, and the applicability to perform this type of research on wild, free-roaming jaguars. Finally, we attended The Wildlife Society national meeting, in October 2012, were we presented the work on hormonal degradation. References Cited Altrichter M., Boaglio G., and Perovic P The decline of jaguars Panthera onca in the Argentine Chaco. Oryx 40(3): Amorim Conforti V., and Cascelli de Azevedo F Local perceptions of jaguars (Panthera onca) and pumas (Puma concolor) in the Iguac u National Park area, south Brazil. Biological Conservation 111: Barbier E.B Deforestation, land degradation and rural poverty in Latin America: examining the evidence. In R. Seroa da Motta, pp Caughley G Direction in Conservation Biology. The Journal of Animal Ecology 63(2): Davis M.L., Kelly M.J., and Stauffer D. F Carnivore co-existence and habitat use in the Mountain Pine Ridge Forest Reserve, Belize. Animal Conservation IN PRESS. Davis R. and Holmgren P Annotated Bibliography Forest Cover Change, Belize. The Forest Resources Assessment (FRA) FAO. Dycka M. and Baydack R Vigilance behaviour of polar bears (Ursus maritimus) in the context of wildlife-viewing activities at Churchill, Manitoba, Canada. Biological Conservation 116: Coppolillo P. Gomez H., Maisels F., Wallace R Selection criteria for suites of landscape species as a bais for site-based conservation. Biological Conservation 115: Creel F., Fox J., Hardy A., Sands J., Garrott B., and Peterson R Snow Mobile activity and Glucorticoid stress response in Wolves and Elk. Conservation Biology 16(3): Martin PA., and Crump MH The adrenal gland. In: Veterinary endocrinology and reproduction, edited by Pineda MH, and Dooley MP. Iowa State Press. pp Michalski F., Boulhosa R. L. P., Faria A., and Peres C. A Human wildlife conflicts in a fragmented Amazonian forest landscape: determinants of large felid depredation on livestock. Animal Conservation 9: Möstl E. and Palme R Hormones as indicators of stress. Domestic Animal Endocrinology 23: Nelson R. J An introduction to behavioral endocrinology. Third Edition. Sinauer Associates, Inc. Publishers. Sunderland Massachusetts. USA. Novack A., Main M., Sunquist M., and Labisky R Foraging ecology of jaguar (Panthera onca) and puma(puma concolor) in hunted and non-hunted sites within the Maya Biosphere Reserve, Guatemala. J. Zool., Lond. 267: Roberge J-M. and Angelstam P Usefullness of the Umbrella Species Concept as a Conservation Tool. Conservation Biology 18(1): Sanderson E.W., Redford K.H., Chetkiewicz C-L.B., Medellin R.A., Rabinowitz A.R., Robinson J.G. and Taber A.B. 2002a. Planning to Save Species: The Jaguar as a Model. Conservation in Practice 16 (1): Sanderson E.W., Redford K.H., Vedder A., Coppollilo P.B., and Ward S.E. 2002b. A conceptual model for conservation planning based on landscape species requirements. Landscape and Urban Planning 58: Wallace R., Gomez H., Ayala G., and Espinoza F Camera trapping for jaguar (Panthera onca) in the Tuichi valley, Bolivia. Mastozoologia Neotropical/J. Neotrop. Mammal. 10 (1): Wasser S., Bevis K, King G, and Hanson E Noninvasive Physiological Measures of Disturbance in the Northern Spotted Owl. Conservation Biology11 (4): Weber W. and Rabinowitz A A Global Perspective on Large Carnivore Conservation. Conservation Biology 10(4): Whitman A., Brokaw N., and Hagan J Forest damage caused by selection logging of mahogany (Swietenia macrophylla) in northern Belize Forest Ecology and Management 92: Wultsch C Optimizing noninvasive genetic monitoring of jaguars (Panthera onca) and other elusive feline species in the tropics. Wild Felid Monitor 2(1): 21. 6 Figure 1. Barbara Davenport (Packleader dog trainer) and J. Bernardo Mesa in dog survey training in Belize. Figure 2. Boomer having acclimation difficulties due to high temperatures and high humidity. Bernardo cooling Boomer down with a shower (A) and a bath (B.) A B 7 Figure 3. CJ (scat dog) searching for wild felid scat in Belize. CJ and Bernardo looking for scat scent at RBCMA (A); finding a scat sample 2 inches under the leaf litter (B). Figure 4. Procedures on scat data collection. Bernardo taking a reference picture of wild felid scat (A); Bernardo taking a DNA sample from wild felid scat (B). 8 Figure 5. Location and distribution of wild felid scat samples across study sites. Rio Bravo Conservation and Management Area (outlined in black) and Lamanai Archeological area (east of La Milpa and North of Hill Bank). Species: jaguar: orange bubbles (J); puma: red bubbles (P); ocelot: blue bubbles (O); jaguarundi: green bubbles (U), domestic cat: purple bubbles (D). Samples with no DNA amplification are represented by grey hollow diamonds. Map layer was obtained from Google earth. La Milpa Hill Bank 9 Figure 6. Bone and hair sample collection for diet analysis. Bernardo and Julie Golla (field technician) collecting road kill (A); Bernardo collecting hair from peccaries at the Belize Zoo (B). Figure 7. Bernardo at the 5 th Natural Resource Management Symposium in Belize. 10 Table 1. Summary of results from DNA analysis. Species Number of samples Identified Total No. Individuals Sex Molecular Technique Male Female Unknown Microsatellite mtdna Jaguar Yes Yes Puma Yes Yes Ocelot Yes Yes Jaguarundi Yes Yes Domestic cat Yes Yes 11
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