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Top-Down and Bottom-Up Control on Cougar and Its Prey in a Central Mexican Natural Reserve

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Top-Down and Bottom-Up Control on Cougar and Its Prey in a Central Mexican Natural Reserve Eur J Wildl Res (2017)63:73 DOI 10.1007/s10344-017-1129-y ORIGINAL ARTICLE Top-down and bottom-up control on cougar and its prey in a central Mexican natural reserve Leroy Soria-Díaz1 & Mike S. Fowler2,3 & Octavio Monroy-Vilchis4 Received: 26 December 2016 /Revised: 26 July 2017 /Accepted: 1 August 2017 # Springer-Verlag GmbH Germany 2017 Abstract Top-down and bottom-up controls are hypothe- focal prey, and we used the normalized difference vegetation sized to regulate population structures in many ecosystems. index (NDVI) as a proxy of primary productivity. We con- However, few studies have had the opportunity to analyze structed multiple regression models and selected the best lin- both processes in the natural environment, especially on large ear models based on ranking the AICc values. Our analysis carnivores like the cougar (Puma concolor). Previously, stud- suggests that P. concolor pca is best explained by bottom-up ies show that cougar diet in the Sierra Nanchititla Natural control and intraspecific feedback. White-tailed deer and ar- Reserve (SNNR), central Mexico, is mainly armadillo, coati, madillo pca were both significantly affected by cougar abun- and white-tailed deer. We assess whether top-down and/or dance, indicating top-down control for these prey species, but bottom-up control regulate this endangered food web: (a) we NDVI was not retained in any of the models selected for prey predicted that seasonal per capita changes in abundance (pca) pca. Our results indicate that both bottom-up and top-down of cougar will be positively affected by the abundance of their control are involved in regulating this endangered food web in main prey; (b) primary productivity in SNNR will affect the the SNNR, Mexico. pca of prey species, driving bottom-up control; and (c) arma- dillo, coati, and white-tailed deer pca will be affected by the Keywords Competition . Food web . Mexico . NDVI . abundance of cougar, generating top-down control. Using 15 Predator-prey . Species interactions camera traps for 6 years in the SNNR, we calculated a relative abundance index (RAI) and pca for cougar and each of the Introduction Electronic supplementary material The online version of this article (doi:10.1007/s10344-017-1129-y) contains supplementary material, Large carnivores are critical functional components of their which is available to authorized users. ecosystems, exerting both direct and indirect effects across a wide range of taxa and habitat features (Ripple et al. 2014). * Octavio Monroy-Vilchis Top-down and bottom-up ecosystem control generate trophic [email protected] cascades and regulate population structure, constituting a clas- sic theme in ecology (Lindeman 1942;Power1992; Hunter 1 Instituto de Ecología Aplicada, Universidad Autónoma de et al. 1997; Denno et al. 2002; Vucetich and Peterson 2004; Tamaulipas, Av. División del Golfo No. 356, Col. Libertad C.P. Keeler et al. 2006). Top-down describes the control of primary 87019, Ciudad Victoria, Tamaulipas, Mexico 2 resources and intermediate consumers by consumers at higher Department of Biosciences, Swansea University, Singleton Park, trophic levels, while bottom-up control describes how the Swansea SA2 8PP, UK 3 amount and quality of resources control the dynamics of con- Population Ecology Group, IMEDEA (CSIC-UIB), Institut sumers on higher trophic levels (Dawes-Gromadzki 2002; Mediterrani d’Estudis Avançats C/Miquel Marquès, 21, Esporles, 07190 Mallorca, Spain Sinclair and Krebs 2002; Keeler et al. 2006). The importance of understanding what factors drive population growth through 4 Centro de Investigación en Ciencias Biológicas Aplicadas, Universidad Autónoma del Estado de México, Instituto Literario top-down and bottom-up controls is necessary for effective 100, Centro, CP 50000 Toluca, Mexico ecosystem management to preserve biodiversity (Sinclair and 73 Page 2 of 10 Eur J Wildl Res 63:73 (2017) Krebs 2002; Elmhagen and Rushton 2007). Understanding top- increasing relative abundance of their main prey species (in- down and bottom-up controls can provide useful information to terspecific interactions) and negatively by individuals of the control top predators, e.g., by translocating to other areas, or to same species (intraspecific interactions/self-regulation); (2) conserve threatened prey species by reintroducing native spe- since focal prey species are herbivorous/insectivorous, de- cies (Gasaway et al. 1992;Sinclairetal.1998). pending on vegetation directly or indirectly (Valenzuela Some studies have reported that only top-down or bottom- 1998; Aguilera-Reyes et al. 2013), we predicted that seasonal up control regulates population structures (Hunter et al. 1997; normalized difference vegetation index (NDVI), as an approx- Huryn 1998;Menge2000; Walker and Jones 2001; Vucetich imation of primary productivity in SNNR, will affect the pca and Peterson 2004), but the patterns and processes of bottom- of prey species, resulting in bottom-up control of intermediate up control are less well documented (Brose 2003;Scherber consumers. This index has been found to provide a strong et al. 2010). Large mammalian herbivores and their predators vegetation signal and is a good indicator of plant biomass are important for studying top-down and bottom-up relation- (Oindo and Skidmore 2002); and (3) the pca of the three prey ships. Some studies of insect parasitoids and other inverte- species, D. novemcinctus, N. narica,andO. virginianus, will brates (e.g., Dyer and Letourneau 2003;GrattonandDenno be affected by the relative abundance of cougar, indicating 2003;Gruner2004) have tried to extrapolate their results to top-down control. Our overall objective was to determine give insight into predator-prey dynamics for large mammal whether top-down, bottom-up, or both controls regulate this population regulation, which has been questioned (Bowyer endangered pine-oak woodland food web in the SNNR, et al. 2005). Some experimental studies have simultaneously México, assessed through the strength and direction of intra- manipulated productivity and predation to assess their top- specific and interspecific feedbacks among the populations. down and bottom-up controls on prey assemblages in the lab (Horppila et al. 1998;JiangandMorin2005), but few studies have analyzed both effects in the natural environment, where Materials and methods it is difficult to manipulate biotic and abiotic factors (but see Mduma et al. 1999; Sinclair et al. 2003; Grange and Duncan Study site 2006). Top-down predation by Canis lupus, Puma concolor, and Ursus arctos has been shown to affect ungulate density, The study was carried out in the SNNR, located in central foraging patterns, and plant species in North America Mexico in the Balsas River basin, at altitudes ranging from (Peterson 1999; Ripple and Beschta 2008) where top-down 410 to 2080 m a.s.l. (Fig. 1). The SNNR has an area of and bottom-up forces have also been shown to act simulta- 663.93 km2, with marked seasonality characterized by a wet neously between cougar and mule deer (Adocoileus season from June to October and dry season from November hemionus) populations (Pierce et al. 2012). In the latter case, to May, with an average annual temperature of 14 °C. The the availability of forage, which was linked to environmental main vegetation types are pine-oak forest, which account for effects, generated bottom-up control of the herbivore dynam- 47.9% of the total area, deciduous low land forest (37.1%), ics, with a slight, but time-lagged impact on the cougar pop- grassland (8.4%), and agriculture (6.6%). This study was con- ulation. The top-down effects of cougar limited, but did not ducted only in the pine-oak forest, because it is an area prevent, increases in the mule deer population. protected by the State Government of México (Comisión In the Sierra Nanchititla Natural Reserve (SNNR), central EstataldeParquesNaturalesydelaFauna(CEPANAF): Mexico, 10 years of trophic niche studies have determined http://cepanaf.edomex.gob.mx/parques_turisticos) with no that the cougar (P.concolor) is an generalist predator, consum- human disturbance. Logging and hunting of feline species ing 21 different mammal species, of which the armadillo and their prey have not been permitted since 1977. SNNR (Dasypus novemcinctus) is the most highly predated (54% has 53 mammal species, which comprise 10% of Mexico’s occurrence in cougar scats), followed by coati (Nasua narica, mammalian diversity (Monroy-Vilchis et al. 2011a), including 16% occurrence) and white-tailed deer (Odocoileus 5 out of 6 feline species recorded for Mexico (Puma concolor, virginianus, 8% occurrence), with other species contributing Puma yagoaroundi, Panthera onca, Leopardus pardalis,and less than 5% (Monroy-Vilchis et al. 2009a; Gómez-Ortiz et al. Leopardus wiedii). Of these, cougars are of interest as one of 2011). Here, we assess the relative influence of top-down and the most abundant felines, taking advantage of existing bottom-up controls on these mammals in the endangered pine- knowledge about its trophic ecology in SNNR (Monroy- oak woodland food web, based on three a priori biological Vilchis et al. 2009a; Gómez-Ortiz et al. 2011). hypotheses: (1) Given that the cougar is a strict carnivore, dependent on prey availability, is dominant over resources in Sampling design the environment, and shows territorial behavior (Sunquist and Sunquist 2002), we predicted that the per capita changes in Fifteen camera traps (Camtrakker® 35 mm and ScoutGuard cougar abundance (pca) would be positively
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