Activity patterns of jaguar, puma and their potential prey in san luis potosi, mexico
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ACTIVITY PATTERNS OF JAGUAR, PUMA AND THEIR POTENTIAL PREY IN SAN LUIS POTOSI, MEXICO A nuAr D. HERNÁNDEZ-SAINTMARTÍN, 1 O ctAviO C. ROSAS-ROSAS, 1,3 J Orge PALACIO-NÚÑEZ, 1 L uis A. TARANGO-ARÁMBULA, 1 Fernando CLEMENTE-SÁNCHEZ 1 & A LmirA L. HOOGESTEIJN 2 1 Colegio de Postgraduados Campus San Luis Potosí, Iturbide #73, C.P.78622, Salinas de Hidalgo, San Luis Potosí, México. mx>, 2 Departamento de Ecología Humana, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Antigua carretera a Progreso Km 6, C.P. 97310, Mérida, Yucatán, México. 3 corresponsalauthor: Hernández-SaintMartín, A. D., Rosas-Rosas, O. C., Palacio-Núñez, J. Tarango-Arámbula, L. A., Clemente-Sánchez, F., & Hoogesteijn, A. L. 2013. Activity patterns of jaguar, puma and their potential prey in San Luis Potosí, Mexico. Acta Zoológica Mexicana (n.s.), 29(3): 520-533. ABSTRACT. Jaguars (Panthera onca) and pumas (Puma concolor) are sympatric species in Mexico and have ecological similarities. The understanding of interespecific interactions between these species are important for effective conservation strategies. We studied activity patterns of jaguars, pumas and their potential prey species through camera-trapping photographs obtained by during four seasonsin the Abra-Tanchipa Biosphere Reserve , San Luis Potosí, Mexico. We described activity patterns of 12 terrestrial vertebrate species, the degree of overlap of jaguar and puma activity; and the prey – predator relationship. Both felids showed cathemeral activity and overlapping between their activities. Jaguar activity showed a significant correlation with eight prey species activity. Puma activity was no related with any prey species activity. Activity peaks of both felids suggest that temporal segregation is a strat- egy which minimizes interspecific encounters allowing the coexistence of several individuals in this small reserve.
presas potenciales en San Luis Potosí, México. Acta Zoológica Mexicana (n.s.), 29(3): 520-533. RESUMEN. El jaguar (Panthera onca) y el puma (Puma concolor) en México son especies simpátri- cas y presentan similitud ecológica. El entendimiento de las interacciones interespecíficas entre estas ISSN 0065-1737
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especies es importante para la elaboración de estrategias efectivas de conservación. Se estudiaron los patrones de actividad del jaguar, el puma y sus presas potenciales, a través del análisis de las fotografías obtenidas en cuatro temporadas de foto-trampeo en la Reserva de la Biosfera Sierra del Abra-Tanchipa (RBSAT), San Luis Potosí, México. Se describieron los patrones de actividad de 12 especies de fauna, el grado de sobreposición en la actividad del jaguar y el puma; y su relación con la actividad de sus presas. Ambos felinos presentaron actividad catemeral con traslape en sus patrones de actividad. La actividad del jaguar está relacionada significativamente con la actividad de ocho especies de presas; la actividad del puma no se relacionó con la actividad de ninguna presa. Los picos de actividad de ambos felinos sugieren que la separación temporal es una estrategia para minimizar los de encuentros interespecíficos que permite la coexistencia de varios individuos en reservas pequeñas. Palabras clave: jaguar, puma, presas, patrones de actividad, foto-trampeo. INTRODUCTION Large carnivores are fundamental elements in all terrestrial ecosystems (Terborgh et al. 2001) and one of the most worldwide endangered groups of mammals (Ceballos et al. 2005; Weber & Rabinowitz 1996). Large felid populations have been reduced by habitat loss; prey depletion and hunting of individuals for traditional medicine and/or predator control (Inskip & Zimmerman 2009). One of the principal strategies for large felids conservation is the establishment of natural protected areas. Current land management aspects, tolerance and public policy have limited the creation of protected areas large enough to maintain viable population of these species (Parris et al. 2003). Under these circumstances, small sized protected areas become more important in large felids conservation (Núñez 2010). However, small protected areas are more susceptible to isolation and degradation processes; strategies for large felids conservation and management should be based in extensive ecological knowledge of the species. This knowledge has toinclude data related to abundance, population dynamics, intra and/or interspecific relationships (Beck et al. 2005). The jaguar (Panthera onca) and the puma (Puma concolor) are the only species of large felids inhabiting the Americas (Currier 1983, Seymour 1989). Both are con- sidered key and umbrella species (Miller & Rabinowitz 2002); under this paradigm, strategies for its long term conservation should benefit the entire ecosystem (Roberge & Angelstam 2004). In Mexico, the jaguar is listed as endangered and legally pro- tected since 1987 (Diario Oficial de la Federación 2010), however, habitat loss and hunting of individuals in response to livestock predation are the likely causes for a significant reduction of its original distribution, and population numbers (Chávez et al. 2005). In contrast, the puma is subject to regulated harvest, but scarce information about their real population status and illegal predator control could represent a threat for their populations (Laundré & Hernández 2010). Throughout their distribution both jaguars and pumas are sympatric (Haines 2006); in northern habitats both species are very similar in body size (Iriarte et al. 1990, Núñez et al. 2002), and they can consume the same prey species (Harmsen et Hernández-Saint Martin et al.: Activity of large felids in San Luis Potosí 522
al. 2011, Núñez et al. 2000, Taber & Novaro 1997). Despite this ecological similari- ty, it has been suggested that competition between jaguars and pumas is low because they evolved coexisting strategies (Haines 2006), including trophic segregation (e. g. Aranda & Sánchez-Cordero 1996), mutual avoidance by spatial separation (Taber & Novaro 1997, Scognamillo et al. 2003, Núñez et al. 2002, Emmons 1987) and different daily activity patterns (Romero-Muñoz 2010). Studies about interactions of these felids conducted in other countries, have reported activity of jaguars as pri- marily nocturnal (Di Bitteti et al. 2010, Emmons 1987, Gómez et al. 2005, Maffei et al. 2004, Núñez et al. 2002, Rabinowitz & Nothingham 1986). In contrast, pumas tend to be more active in crepuscular hours with an important activity along daytime (Di Bitteti et al. 2010, Estrada 2008, Núñez et al. 2002). The difference in activity patterns has been suggested as a strategy to avoid and / or minimize confrontations, and to maximize the probability of encounter with their preferred prey (Rabinowitz & Nottingham 1986, Harmsen et al. 2011). In this study we analyze temporal activity of jaguars, pumas and their potential prey using data obtained by camera-trapping in the Abra-Tanchipa Biosphere Re- serve (RBSAT) San Luis Potosi, Mexico. Previous studies conducted in the region, showed that jaguars and pumas can consume the same prey species and travel along the same trails (Rueda et al. in press, Hernández-Saint Martin in revision). We expect to find ecological segregation by differential activity patterns in these species. The objectives of this study were 1) to describe and compare activity patterns of jaguars and pumas, 2) to describe activity patterns of potential prey, and 3) to relate activity of both large felids with activity patterns of their potential prey species.
tosi, Mexico (22° 04’ 38’’-22° 23’ 56’’ N and 98° 53’ 07’’-99° 00’ 44’’ O). It is located about 30 km north of Ciudad Valles, the second largest city of the state (Fig. 1). RBSAT is the only federal protected area in the subtropical ecosystems of San Luis Potosi and covers approximately 220 km 2 of well-preserved tropical dry fo- rest surrounded by fragmented areas (Arriaga et al. 2000, Rzedowski 2005). The predominant arboreal species are chaka (Bursera simaruba), ojite (Brosium alicas- trum), limoncillo (Esenbeckia berlianderi), rajador (Lysiloma divaricata), volantín (Wimmeria concolor), ebano (Ebano ebanopsis), tenaza (Pithecellobium pallens), uña de gato (Zanthoxylum fagara), chicharrillo (Harpalyce arborescens), aguacatillo (Persea palustris), palma real (Sabal mexicana), and soyate (Beaucarnea recurvata) (Rzedowski 2005). The area has 161 vertebrate species including five of the six wild felids of Mexico: the jaguar, puma, ocelot (Leopardus pardalis), margay (L. wiedii) and jaguarundi (Puma yagouaroundi) (Martínez-Calderas et al. 2011, Villordo-Gal- ván et al. 2010). The topography is rugged with numerous rock outcrops. The eleva- Acta Zool. Mex. (n.s.) 29(3) (2013) 523
Figure 1. Camera trapping surveys in Sierra del Abra-Tanchipa Biosphere Reserve (RBSAT). Black dots represent camera stations. Hernández-Saint Martin et al.: Activity of large felids in San Luis Potosí 524
tion range from 400 to 700 meters, and an average annual rainfall of 1100 mm with a marked seasonality: torrential rains may be present during July through October (wet season) and the dry season extends from November to May. The average annual temperature is 25.5°C but temperatures can range between 35°C and 50°C (Arriaga et al. 2000). The protected area has no perennial waterways, the only water source during the dry season are artificial livestock ponds located outside the reserve. There are few wildlife trails. The only road suitable for vehicles inside the protected area consist in an old mine dirt road to the North. Three firebreaks surround the borders of protected area; the longest runs 20 km along the West border, and two 3 km long are located in the North and South limits. All these trails are rarely used by people; consequently human disturbance in the core area is practically absent. RBSAT is one of the smallest Biosphere Reserves of Mexico (Vargas & Escobar 2000), surrounded by an ongoing change of land use, principally sugar cane (Saccharum spp.) planta- tions to the West and sorghum (Sorghum spp.) plantations and cattle ranching to the East (Chapa-Vargas & Monzalvo-Santos 2012). Nine human settlements surround the RBSAT with a total of 3860 habitants. Data sampling. Data of activity patterns of jaguars and pumas and their prey were obtained through analysis of photographs collected by three camera-trapping surveys (Bridges & Noss 2011) from October 2010 to March 2012. We deployed camera stations inside the core and surrounding areas of RBSAT. Each camera station con- sisted of one (single stations) or two (double stations) camera traps fixed to trees at 40 cm overground; these were placed in sites with previous evidence of large felids or prey activity (game trails, fresh tracks, scrapes, scats). We programed all cameras to operate continually for 24 hrs with 3-5 minutes delay between photographs; date and hour were printed in each photographic event. We placed camera stations at a distance of two to three km. No attractants were used at camera stations. We checked camera stations every 20 days to verify proper functioning, check-ups included bat- tery changes, photograph unloading and memory/film capacity. Trapping efforts were different between the three surveys (Table 1). Different ca- mera models were used. In the first survey we deployed 51 camera stations, 45 single and six double composed of the following brands and models: a) thirty three Capture Cuddeback ® Digital; b) eight StealthCam ® Digital; c) five Xtreme-5 Wildview ® Di-
gital; d) three Moultrie ® DGS-200 Digital and e) eight DeerCam ® DC200 35 mm. During the second survey we used 23 camera stations, 11 singles and 12 double, composed of the following brands and models: a) thirteen Xtreme-5 Wildview ® Di-
gital, b) nine StealthCam ® Digital; c) five Moultrie ® DGS-200-Digital; and d) eight DeerCam ®
single and 19 double composed of the following brands and models: a) nine Stealth- Cam
® Digital and b) thirty seven Xtreme-5 Wildview ® .
Acta Zool. Mex. (n.s.) 29(3) (2013) 525
Data analysis. Of all obtained photographs we select those that consisted of indepen- dent events. We define these independent events as: a) consecutive photographs of different individuals of the same species; b) each individual of one species in a group photograph; c) photographs of individuals of the same species with a separation of at least 30 minutes; d) consecutive photographs of individuals of different species; and e) photographs of individuals that can be individually identified (O’Brien et al. 2003). Following the suggestion of Maffei et al (2004) we analyzed activity patterns of all species with an average ≥11 independent events across surveys. Because trap- ping effort was significantly different between surveys (χ 2 =274.41, d.f.=2, p> 0.05), we obtained the mean value of independent event´s percentage by hour of the diffe- rent surveys. We assumed that these values correctly represent the activity patterns of species during the study period. We calculated percentage of diurnal (from 06:01 to 18:00) and nocturnal (from 18:01 to 6:00) independent events of each species. Using this information, we clas- sified species as diurnal (<15% of observations at night), nocturnal (>85% of obser- vations at night), mostly diurnal (15–35% of observations at night), mostly nocturnal (65–85% of observations by night), and cathemeral (organisms active intermittently both day and night) (Romero-Muñoz et al. 2010). We plotted bar charts with percen- tages of independent events by hour (Romero-Muñoz et al. 2010). Activity patterns data present a circular distribution (Zar 2010), consequently we compared activity patterns of jaguars and pumas in two ways; first we used the Pianka index O jk
et al. 2008, Krebs 1999). We also compared the activity patterns of both felids using the non-parametric Wheeler and Watson test (W); this test indicates if there is a sig- nificant statistic difference between two circular distributions, and it has been used to analyzed data from 24 hrs activity patterns (Romero-Muñoz et al. 2010). The statistic W can be compared with a χ 2 distribution with two degrees of freedom (Zar 2010). We calculated Pearson correlations between the 24-hour activity patterns of ja- guar and pumas and the activity patterns of each prey species to assess the level of association in activity. Prior to this analysis we transformed percentages with the
October 16 th – December 17 th
2010 3264 516
276 April 16
th – July 16 th 2011
2161 697
287 November 15 th 2011- March 11 th 3238
937 487
Mean± SD 2887.7±629.4 716.7±211.2 350±118.8 Hernández-Saint Martin et al.: Activity of large felids in San Luis Potosí 526
Arcsine-root transformation (Zar 2010). Descriptive analyses were conducted with Microsoft Excel (Microsoft Corporation 2006) and circular statistics analysis we- re made with Oriana 4.0 (www.kovcomp.com) and Stat Graphics Centurion XV (StatPoint Inc. 1982-2007); all at a significance level of p= 0.05. RESULTS We deployed 101 camera stations inside the core and surrounding areas of RB- SAT in three surveys (Fig. 1). We obtained 2628 photographs of 25 species, 1194 photographs were identified as independent events (Table 2). Of the 25 species only 12 (including the jaguar and the puma) had an average of independent events≥11. The 10 prey species have been reported as components in the diet for jaguars or pumas by other authors in other regions of Mexico, Central and South America (Aranda & Sán- chez-Cordero 1996; Foster et al. 2009, Garla et al. 2001; Novack et al. 2005; Núñez et al. 2000, Rosas-Rosas et al. 2003, Taber & Novaro 1997, Weckel et al. 2006). Do- mestic species (cattle, horses and dogs) were photographed only in the surrounding areas outside the polygon of RBSAT. Jaguars were cathemeral; but activity was significantly higher in night hours (χ 2 =
milarly, pumas were also cathemeral; however percentages of diurnal and nocturnal activity were similar (χ 2 =0.26, d.f.=1, p>0.05). Puma activity peaks where opposite to those of the jaguar; with activity peaks between 02:00 and 10:00 hr (Fig. 2). Jaguars and pumas showed a relative high overlap in their activity patterns (Pianka’s index O jk
both felids (χ 2 =0.75, df= 2, p˃0.05). Seven prey species can be considered diurnal and showed significantly more ac- tivity at day hours; these included great curassow (Crax rubra) (χ 2 =77.79, d.f.=1, p<0.05); Plainchachalaca (Ortalis vetula) (χ 2 =79.85, d.f.=1, p<0.05); collared pec- cary (Pecari tajacu) (χ 2 =44.44, d.f.=1, p<0.05); white-nosed coati (Nasua narica) (χ 2 =91.32, d.f.=1, p<0.05); white-tailed deer (Odocoileus virginianus) (χ 2 =34.29,
d.f.=1, p<0.05), cattle (Bos sp.) and horses (Equus sp.) (χ 2 =77.79, d.f.=1, p<0.05). Ocelots (χ 2 =35.43, d.f.=1, p<0.05); grey foxes (Urocyon cinereoargenteus) (χ 2 =47.44,
d.f.=1, p<0.05) and rabbits (Sylvilagus sp.) (χ 2 =26.54, d.f.=1, p<0.05) were mostly nocturnal (Fig. 3). The activity of jaguars was positively related with the activity of gray foxes, oce- lots and rabbits (all p<0.05). In contrast, puma activity had no significant correlation to any prey species (Table 3). DISCUSSION Cathemeral activity of jaguar found in this research is rarely reported in other studies and only had been described for Amazonian rain forest habitats of Peru (Gómez et al.
Acta Zool. Mex. (n.s.) 29(3) (2013) 527
2005) and Bolivia (Emmons 1987). In contrast, cathemeral pattern with highly diur- nal activity founded in pumas is reported in several studies (Chávez et al. 2005, Di Bitteti et al. 2010, Estrada 2008, Harmsen et al. 2009, Núñez et al. 2002). Cathemeral activity increments probability of encounter with a more diverse prey base (Scogna- Table 2.Independent events obtained by camera trapping in the Sierra del Abra-Tanchipa Biosphere Reserve, Mexico. Survey Species
1 2 3 Mammals Brocket deer Mazama temama 9 1
Cattle Bos sp. — 85 86 Collared pecari Pecari tajacu 4 3
White-tailed deer Odocoileus virginianus 103
29 77 Coyote Canis latrans — 1 1 Domestic Dog Canis familiaris — 9 7 Gray fox Urocyon cinereoargenteus 5 15
Jaguar Panthera onca 19 22 34 Jaguarundi Puma yagouaroundi 2 Margay Leopardus wiedii 4 — 4 Ocelot Leopardus pardalis 9 18 28 Raccon Procyon lotor 7 Puma Puma concolor 25 31 22 White-nosed coati Nasua narica 58 62 12 Nine-banded armadillo Dasypus novemcinctus 1 —
Opossums Didelphis sp. 3 5 2 Horses Equus sp. — 22
Spotted paca Cuniculus paca 5 2 11 Squirles Sciurus sp. 8 2
Rabbits Silvilagus sp. 3 24 124 Birds
Crested Guan Penelope purpurescens 7 — — Great curassow Crax rubra 70 78
Plain Chachalaca Ortalis vetula 6 15 38 Thicket Tinamou Crypturellus cinnamomeus 4 6
Wild turkey Meleagris gallopavo — 2 7 Hernández-Saint Martin et al.: Activity of large felids in San Luis Potosí 528
millo et al. 2003), this could be specifically beneficial for a generalist predator like puma which consume a broader prey variety including diurnal and nocturnal prey (Oliveira 2002). In RBSAT, jaguars and pumas showed important activity at day hours (34.09% and 53.59%, respectively); these findings are similar to results obtained in the Ve- nezuelan llanos (Scognamillo et al. 2003) and some biomes of Brazil (Foster et al. 2013). Diurnal activity of large felids has been reported as an indicator of absence of human disturbance in the habitat (Paviolo et al. 2009). The rugged topography and lack of trails inside RBSAT generate minimal human presence inside protected area; this allows jaguars and pumas to be active during diurnal hours without risk of en- counters with humans.Unsurprisingly, both felids showed less activity around noon, period whit the highest temperatures (Hernández-Saint Martín, Pers. Obs.) sugges- ting that jaguars and pumas tend to avoid movement during the hottest hours, this has also been reported in other sites of neotropics (Estrada 2008). Temporal segregation among carnivore’s species has been suggested as a strategy to reduce interference competition and the risk of intraguild predation (Fedriani et al. 2000), however this pattern is rarely reported for large predators species like jaguar and puma (Romero-Muñoz et al. 2010). In this study, activity of both large felids was no significantly different. However, jaguar showed peaks of activity that began around sunset decreasing about two hours after sunrise; this is in opposition to the highest activity of the puma that began around dawn, decreasingat 10:00 and staying relatively stable during the remaining hours of the day. This suggests that despite the overlap of activity patterns (Pianka Index O jk =0.73), the activity of jaguars is at its Figure 2. Activity patterns of jaguar and puma and their potential prey in Sierra del Abra–Tanchipa Biosphere Reserve. Acta Zool. Mex. (n.s.) 29(3) (2013) 529
peak when the activity of the puma´s decrease. Encounters between two species of large carnivores usually end with interspecific aggression and the maiming or killing of one of the aggressors. The severity of the attack seems to increase with the high densities of carnivores (Palomares & Caro 1999). Individual identification using differential coat patterns and conspicuous features of the photographed jaguars and pumas (Kelly et al. 2008, Silver et al. 2005) showed that at least 13 different jaguars and six pumas were present in RBSAT during this study (Hernández-Saint Martín in revision). This abundance of large felids without evidence of interspecific aggression (e. g. scars or wounds produced by fighting) in
Hernández-Saint Martin et al.: Activity of large felids in San Luis Potosí 530
photographed animals, suggest temporal segregation is a mechanisms which allows coexistence of several individuals of both species in the small area of RBSAT. Other studies across Latin-American countries have suggested that activity pat- terns of jaguars and pumas are determined by activity of their prey species (Foster et al. 2013, Emmons 1987, Núñez et al. 2000, Scognamillo et al. 2003, Harmsen et al. 2011). In RBSAT, jaguar’s diet is mainly collared peccary, withe-tailed deer and whi- te-nosed coati; and puma prey consists mainly on withe-tailed deer, rabbits and great curassow (Hernández-Saint Martín in revision); activity of jaguars was significantly related with activity of their principal prey species, but all these relationships were negative (Table 3). This suggests that jaguar hunts prey when they are not active and probably more vulnerable, like during the night hours. In contrast, activity of pumas was no significantly related with activity of any prey species. The RBSAT is one of the last protected refuges for wildlife, especially for large felids northeast of the Sierra Madre Oriental in San Luis Potosi. Despite its small size, it protects a large diversity of medium and great sized mammals.The results of this study suggest that temporal segregation allows coexistence of several individual of jaguars and pumas in small protected areas (Núñez 2010). This situation depends on the existence of large and diverse prey base that allows a flexible carnivore community in the area (Harmsen et al. 2009). However, the accelerated change in land use and tenure around the reserve could alter these patterns and may derivate in intra-guild aggressions and interference competence that could threat the long term survival of large felid in this area.
Potosí) and L. Chapa (Instituto Potosino de Investigación Científica y Tecnológica A.C.) for funding Table 3.Correlations between activity patterns of jaguar, pumas and prey species. Potential prey species Jaguar Puma
Cattle −0.34
0.24 Collared peccary −0.39* 0.15
Great curassow −0.48*
0.24 Grey fox
0.44* 0.11
Horse −0.35
−0.26 Ocelot
0.43* 0.20
Plain chachalaca −0.66*
−0.03 Rabbits
0.41* 0.07
White-nosed coati −0.46*
−0.03 White-tailed deer −0.61* 0.07
* Significant correlations p< 0.05 Acta Zool. Mex. (n.s.) 29(3) (2013) 531
support to this study. A. Durán (CONANP-RBSAT) provided logistic support in fieldwork. L. Bender (Alaska Department of Fish and Game, U.S.), L. Chapa (Instituto Potosino de Investigación Científica y Tecnológica A.C.) and H. López (Universidad Autónoma de Nuevo León) provided camera traps. H. Guzman, M. Aguilar and L. Martínez assisted during the field work; their contribution was instrumental to the study.
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