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Naves Cons Biol 03

Naves Cons Biol 03

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 Contributed Papers
 Conservation Biology, Pages 1276–1289 Volume 17, No. 5, October 2003
 Endangered Species Constrained by Naturaland Human Factors: the Case of Brown Bearsin Northern Spain
 *Department of Applied Biology, Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas,CSIC, Avda. María Luisa s/n, Pabellón del Peru, E-41013 Seville, Spain
 Department of Ecological Modelling, UFZ-Centre for Environmental Research, Permoserstrasse 15, D-04318Leipzig, Germany 
 We developed a conceptual framework for classifying habitat quality that requires the construc- tion of separate habitat models for each key demographic feature; the framework can be applied when the factors that determine different demographic processes differ substantially. For example, survival of large car- nivores is mainly determined by human-induced mortality, whereas nutritional condition determines repro- ductive rate. Hence, a two-dimensional habitat model built for reproduction and survival yields five hypothet- ical habitat categories:
 , with no reproduction and/or very high mortality;
 , with low reproductionand high mortality;
 , with low reproduction and low mortality;
attractive sink 
 , with high reproductionand high mortality; and 
 , with high reproduction and low mortality. We applied this framework to twoendangered brown bear ( 
Ursus arctos
 ) populations in the Cantabrian Mountains, Spain. Our aim was to gen- erate working hypotheses about the quality and spatial arrangement of bear habitat to analyze the present conditions of the different population nuclei and to facilitate identification of core areas of high conservationvalue, conflictive areas, or areas with unoccupied potential habitat. We used a geographic information systemand two spatial long-term data sets on presence and reproduction and performed logistic regressions for building a two-dimensional model. The analysis reveals that both populations exist under different subopti- mal conditions: the eastern population mainly occupies areas of suboptimal natural habitat and relativelylow human impact, whereas the western population is located mainly in areas with high human impact but otherwise good natural quality. To test hypotheses about demographic features of the obtained habitat cate-  gories, we classified data on historic extinction in northern Spain (fourteenth to nineteenth centuries) withthe two-dimensional model. Extinction probabilities within each habitat category confirmed the hypotheses:most extinctions occurred in matrix habitat, and the fewest occurred in source habitat.
Especies Amenazadas Limitadas por Factores Naturales y Humanos: el Caso del Oso Pardo en el Norte de España
 Desarrollamos un marco conceptual para clasificar la calidad del hábitat que requiere la con-  strucción de modelos de hábitat separados para cada característica demográfica clave. El marco se puedeaplicar cuando difieren sustancialmente los factores que determinan diferentes procesos demográficos. Por ejemplo, la supervivencia de grandes carnívoros esta determinada principalmente por mortalidad inducida por humanos, mientras que la condición nutricional determina la tasa reproductiva. Consecuentemente, unmodelo bidimensional del hábitat construido para reproducción y supervivencia produce cinco categoríashipotéticas de hábitat:
(sin reproducción y/o mortalidad muy alta),
(reproducción baja,mortalidad alta),
(reproducción baja, mortalidad baja),
sumidero atractivo
(reproducción alta, mor- talidad alta) y fuente (reproducción alta, mortalidad baja). Aplicamos este marco a dos poblaciones en peli-  gro de oso pardo ( 
Ursus arctos
 ) en la Cordillera Cantábrice, España. Nuestra meta fue generar hipótesis detrabajo sobre la calidad y la distribución espacial del hábitat de los osos para analizar las condiciones actu- 
  Address correspondence to E. Revilla, email revilla@ebd.csic.es Paper submitted April 4, 2002; revised manuscript accepted January 21, 2003.
 Conservation Biology  Volume 17, No. 5, October 2003
 Naves et al.Two-Dimensional Habitat Mode
 Habitat modeling has become an important field in con-servation biology because it improves our understandingof the factors that determine the distribution of habitatsand the human factors leading to habitat change. The ba-sic idea of most habitat models is to predict the probabil-ity of occupancy from a set of landscape-scale explana-tory variables (Manly et al. 1993). The obtained functioncan then be mapped over the whole area of interest.One usual assumption of this approach is that a singlefunction best describes habitat quality. However, such aone-dimensional approach may be insufficient in somecases because, to be useful, habitat quality should be de-rived from the biological requirements of the speciesand explicitly linked with demographic features, such asreproduction and mortality (e.g., Hall et al. 1997; Tho-mas & Kunin 1999). If we define habitat as an area with enough resources and conditions to permit occu-pancy—including survival and reproduction—by a givenorganism (Hall et al. 1997), it might be more appropri-ate to construct for each of the basic demographic pro-cesses a separate model and to classify a given area within the multidimensional phase diagram spanned by these models (Fig. 1a). Such a multidimensional ap-proach that focuses on biological processes and require-ments (Caughley & Gunn 1996; Hall et al. 1997; Beutelet al. 1999) would be especially useful when the factorsthat determine the different demographic processes dif-fer substantially.For long-lived species with low reproductive rates,such as most large carnivores, it is well known thatdeaths are mainly caused by humans (reviewed in Woo-droffe & Ginsberg 1998), whereas nutritional conditiondetermines reproductive rate (e.g., Bunnell & Tait 1981;Rogers 1987; Stringham 1990). Additionally, a poorly perceived risk of human-caused mortality in otherwisegood habitats, where resources are abundant and repro-ductive potential could be high, may create “deceptive”sources (Fig. 1) that act functionally as attractive sinks(Delibes et al. 2001
 , 2001
  ). Attractive sinks are com-monly associated with human activities in the literatureon endangered species or reported as “ecological traps”for breeding birds (Knight et al. 1988; Merrill et al.1999; Novaro et al. 2000; Revilla et al. 2001). On theother hand, suboptimal refuge areas with scarce nutri-tional resources but a lower risk of human-induced mor-tality may allow for population persistence. These phe-nomena could be common when relicts of endangeredspecies persist in the periphery of their historical geo-graphical range (Channell & Lomolino 2000). In thiscase the species survives not because the habitat is goodfor them but because it is poor for its enemies.In practice, however, it might be difficult to apply thisframework because information on the spatial heteroge-neity of demographic features is rarely available. In con-trast, data on presence and absence, which contain in-formation on both mortality and reproduction, are easier to obtain. For large carnivores, an indirect approach canuse the potential separation of habitat factors influenc-ing mortality (anthropogenic factors, hereafter humanfactors) and reproduction (nutritional factors, hereafter natural factors). Instead of relating a set of independent variables that describe habitat characteristics to the twodependent variables, mortality and reproduction (Fig.1b), we relate two separate sets of potentially explana-tory variables (one comprising the human factors andanother comprising the natural ones) to the same de-pendent variable of presence and absence (Fig. 1b). Thetwo critical assumptions of this indirect approach arethat (1) human factors mainly determine mortality, whereas natural factors mainly determine reproductionand (2) presence is a surrogate for reproduction and sur- vival. We used the case of brown bears ( 
 Ursus arctos
  ) innorthern Spain as an example of the application of theframework. The plight of brown bears in Spain, wherethey have been protected since 1973 and are listed asendangered (Clevenger & Purroy 1991; Naves & Palo-mero 1993; Swenson et al. 2000), is typical of many 
 ales de los diferentes núcleos de población, para facilitar la identificación de áreas núcleo de alto valor deconservación, áreas conflictivas o áreas con hábitat potencial desocupado. Utilizamos un sistema de infor- mación geográfica y dos conjuntos de datos históricos de presencia y reproducción y aplicamos regresioneslogísticas para construir un modelo bidimensional. El análisis revela que ambas poblaciones existen bajodiferentes condiciones sub-óptimas: la población oriental ocupa principalmente áreas de hábitat natural sub- óptimo y relativamente bajo impacto humano, mientras que la población occidental se localiza principal- mente en áreas con alto impacto humano, pero por lo demás con buena calidad natural. Para evaluar lashipótesis sobre las características demográficas de cada tipo de hábitat, clasificamos datos de extincioneshistóricas en el norte de España (siglos XIV a XIX) con el modelo bidimensional. Las probabilidades de extin- ción en cada categoría de hábitat confirmaron las hipótesis: la mayoría de las extinciones ocurrieron en hábitat matriz y la minoría ocurrió en hábitat fuente.
Two-Dimensional Habitat ModelNaves et al.
 Conservation Biology  Volume 17, No. 5, October 2003
  wildlife populations that have suffered long-lasting per-secution and progressive loss and fragmentation of their habitat. The surviving populations are relicts from a dis-tribution that once covered the entire Iberian Peninsula(Nores 1988; Nores & Naves 1993). Extinction appearsimminent in the Pyrenees (Swenson et al. 2000), andthe two remaining subpopulations in the CantabrianMountains are remnants of a distribution that during theeighteenth through nineteenth centuries still extendedover the entire mountain range. Wiegand et al. (1998)performed a nonspatial demographic population viabil-ity analysis (PVA) to diagnose the state and dynamics(for 1982–1995) of the western population and foundthat it is not viable if mortality rates remain at the levelof the last years of analysis. They identified adult femalesurvival as key to population recovery and argued thatmortality can be assessed in terms of human access tobears. This view is supported by several intensive studiesof carnivores (Woodroffe & Ginsberg 1998) and data ongrizzly bears showing that since the 1970s humans havedirectly caused 70–90% of known deaths in YellowstoneNational Park (Mattson et al. 1996; Mattson 1998; Pease& Mattson 1999) and 77–85% in the Rocky and Colum-bia mountains (McLellan et al. 1999). Thus, it is appar-ent that, to manage the species adequately, an analysisis needed of the spatial arrangement of risk areas—areasof high risk of human-bear contact and otherwise goodhabitat quality—within the habitat network. We aimed to generate working hypotheses about thequality the spatial arrangement of brown bear habitat innorthern Spain to analyze the present conditions andconflicts of the different population nuclei and to iden-tify core areas of high conservation value and areas with unoccupied potential habitat. We used geographic infor-mation system (GIS) data to obtain several logistic mod-els that describe habitat quality in the traditional manner  with a one-dimensional model (e.g., Tyre et al. 2001)and, following our framework, another that describeshabitat quality with a two-dimensional model (Fig. 1a).To test hypotheses about the demographic features of the habitat categories, we classified areas where extinc-tion occurred during the fourteenth through nineteenth centuries within the two-dimensional habitat model. Wehypothesize that extinction should be most frequent inareas classified at present as matrix and the least fre-quent in habitat with low human impact and good natu-ral quality.
 Study Area and Spatial Grain
 Our study area was the northwestern Iberian peninsula,including the entire range of the Cantabrian Mountainsnorth of Spain (Fig. 2). The two brown bear subpopula-
 Figure 1. (a) Conceptual framework for classifying habitat within a two-dimensional space spanned bytwo separate models for reproduction and survival.Classical source-sink theory assumes, on evolutionarytime scales, an approximately constant mortality rate,and variation of reproduction according to habitat quality results in sources (growth rate
1) and  sinks ( 
1; see ellipse). On an ecological time scale,however, disturbances by humans may cause largevariations in habitat quality for survival and the ap-  pearance of new habitat types. Refuge areas with lowhabitat quality for reproduction but good for survival can guarantee population persistence ( 
1), whilehigh human-caused mortality in otherwise good habi- tat (where reproduction could be high) can create “de- ceptive” sources which act functionally as attractive sinks (i.e.,
1). (b) Application of the framework tolarge carnivores (mortality and reproduction, dashed arrows; presence and absence, solid arrows). Where factors determining mortality and reproduction arelargely separated (i.e., the relations indicated by the gray arrows are less important), presence of the spe- cies in a certain area can be used as surrogate for mortality and reproduction because it indicates bothlow mortality and sufficient reproduction. In suchcases, one can construct the habitat model for repro- duction by relating data on presence of the species tothe subset of natural habitat variables and the habitat model for survival by relating data on presence to the subset of human habitat variables (pathway of solid arrows).

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