Niche Partitioning at Local and Regional Scale in the North African Salamandridae DANIEL ESCORIZA,1,2
` AND JIHENE
BEN HASSINE3,4
1 Institute of Aquatic Ecology, University of Girona, Girona, Spain Department of Biology, Faculty of Science, University Tunis El Manar, Tunisia 4 ˆ Tetouan, Morocco Laboratory "Ecology, Biodiversity and Environment," Department of Biology, Faculty of Sciences of Tetouan, University Abdelmalek Essaadi, 3
Journal of Herpetology, Vol. 49, No. 2, 276–283, 2015 Copyright 2015 Society for the Study of Amphibians and Reptiles
Niche Partitioning at Local and Regional Scale in the North African Salamandridae DANIEL ESCORIZA,1,2
` AND JIHENE
BEN HASSINE3,4
1 Institute of Aquatic Ecology, University of Girona, Girona, Spain Department of Biology, Faculty of Science, University Tunis El Manar, Tunisia 4 ˆ Tetouan, Morocco Laboratory "Ecology, Biodiversity and Environment," Department of Biology, Faculty of Sciences of Tetouan, University Abdelmalek Essaadi, 3
ABSTRACT.—The composition of Urodela assemblages is regulated by macro- and microclimatic conditions and by the interactions established between ecologically analogous species. Species of the North African Urodela are distributed unevenly; some species have large ranges whereas others occur in fragmented populations or in restricted ranges. We examined the niches occupied by these species to determine the factors that regulate their range patterns. The niches were examined at two spatial levels; regionally, using climatic and vegetation cover data, and locally by studying the selection of aquatic habitats. Our results indicate that Salamandra algira (North African fire salamander) and North African Pleurodeles species are segregated along a thermal and vegetation cover axis, although with considerable overlap. The fragmentation observed in the distribution of the North African Urodela is caused by prevailing arid conditions in the region. The three Pleurodeles species appear under similar climate conditions and mostly use temporary ponds to breed. There is some overlap comparing species from both genera in the selection of breeding habitats, but the North African Pleurodeles species occur in ponds with higher water temperatures than do S. algira. Preserving temporary ponds, streams, and springs is essential for conserving these species, particularly under the semiarid conditions that favor the fragmentation of their populations. ` RE´SUME´.—La composition des assemblages des urodeles est re´gule´e par les conditions macro- et microclimatiques et par les interactions ` ` ` ` e´tablies entre des especes e´cologiquement proches. Les especes d’urodeles d’Afrique du Nord sont ine´galement re´parties: certaines especes ont de grandes aires de re´partition, tandis que d’autres pre´sentent des populations fragmente´es ou a` re´partition restreinte. Dans cet article, nous ` avons examine´ les niches occupe´es par ces especes afin de de´terminer les facteurs qui re´gulent leurs patterns de distribution. Les niches ont e´te´ examine´es a` deux niveaux spatiaux: au niveau re´gional, en utilisant des donne´es climatiques et des donne´es portant sur le couvert ve´ge´tal, et ` localement, par l’e´tude de la se´lection des habitats aquatiques. Nos re´sultats indiquent que Salamandra algira et les especes Nord africaines de Pleurodeles sont se´pare´s par des axes relatifs a` la tempe´rature et a` la structure de la ve´ge´tation avec un chevauchement conside´rable. La ` fragmentation observe´e dans la distribution des urodeles de l’Afrique du Nord est due aux conditions arides re´gnant dans la re´gion. Les trois ` especes de Pleurodeles apparaissent dans des conditions climatiques similaires et utilisent principalement des mares temporaires pour se ` reproduire. En comparant les especes des deux genres, on observe un certain chevauchement dans la se´lection des habitats de reproduction, toutefois les Pleurodeles d’Afrique du Nord se reproduisent dans des e´tangs dont la tempe´rature de l’eau est plus e´leve´e que ceux de S. algira. ` Pre´server les mares temporaires, les ruisseaux, et des sources est essentiel pour la conservation de ces especes, en particulier dans les conditions semi-arides qui favorisent l’isolement de leurs populations.
The presence of a species in an ecological niche is regulated by several factors such as the physiological tolerance of the species (Kearney and Porter, 2004) and the interactions established with other species (Price and Kirkpatrick, 2009). These factors act at different spatial scales; the physiology of an amphibian species determines the regional niche it occupies, whereas habitat specialization and species interactions regulate its local presence (Wiens et al., 2006; Werner et al., 2007). Therefore, it is important to analyze these two niche scales when examining the distribution patterns of the species that form an assemblage. The North African members of the family Salamandridae are represented by four species belonging to the genera Pleurodeles and Salamandra (Stuart et al., 2008). Pleurodeles waltl (Iberian ribbed newt) Michahelles, 1830, the only species that also appears outside the studied region (Mateo et al., 2003), extending through Morocco’s Atlantic region, whereas Pleurodeles (poireti) nebulosus (Algerian ribbed newt; Guichenot, 1850) occurs in the eastern Maghreb region between northwestern Algeria and Tunisia (Veith et al., 2004). Pleurodeles poireti (Edough ribbed newt; Gervais, 1835) is a microendemic species, occupying a relatively homogeneous area in the Edough Massif in northeastern Algeria (Samraoui et al., 2012). Salamandra algira (North African fire salamander) Bedriaga, 1883 is restricted mainly to mountainous regions, occurring in several isolated populations ranging between Morocco and northeastern Algeria (Escoriza et al., 2006; Escoriza and Ben Hassine, 2014a). We used ecological data 2
Corresponding author. E-mail:
[email protected]
DOI: 10.1670/13-151
to examine spatial partitioning among the Salamandridae species that occur in North Africa. Spatial partitioning was analyzed at two spatial scales; at the regional scale, using climate and vegetation cover data, and at the local scale comparing habitat associations. Climate is a key factor determining the distributions of amphibian species because of the narrow limits imposed by their physiology (Araujo ´ et al., 2006; Hua and Wiens, 2010). In amphibians, species richness is structured along thermal and aridity axes (Qian et al., 2007; Escoriza and Ruhı´, 2014). In North Africa, there is a rapid transition from humid to arid climates that produces sharp changes in the composition of amphibian assemblages and hinders the dispersal of mesic species, favoring allopatric speciation (Schleich et al., 1996; Ben Hassine and Nouria, 2012; Recuero et al., 2012). We expected that in North Africa, parapatric species may be segregated following climatic gradients, while allopatric populations could survive in separate climate refugia under similar environmental conditions. The presence of Urodela can also be determined by the structure of the vegetation cover, with this group being more dependent on this factor than are other groups of amphibians (De Maynadier and Hunter, 1995). Climate and vegetative cover are correlated variables (Pearson et al., 2004), but both can describe different gradients of species composition (Thuiller et al., 2004). For these reasons, we analyzed the effects of both sets of variables (climate and vegetation cover) to explain the distribution of North African salamandrids.
NICHE PARTITIONING OF NORTH AFRICAN SALAMANDRIDAE
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FIG. 1. Localities included in climate models and in habitat sampling. Yellow triangles: Salamandra algira; brown circles: P. waltl; red circles: P. poireti; blue circles: P. nebulosus.
Habitat use has been studied by comparing the characteristics of the aquatic habitats in which different species occur. In other regions, where several species of Urodela coexist, they display segregation mechanisms in the use of aquatic habitats to reduce predation and competition (Joly and Giacoma, 1992; Fasola, 1993). Therefore, we expected similar patterns to occur when two Urodela species occurred sympatrically in northern Africa. Both Pleurodeles and Salamandra species breed in water bodies and have a prolonged larval stage (Garcı´a-Paris et al., 2004), but only the adults of the genus Pleurodeles occur regularly in aquatic habitats (Dı´az-Paniagua, 1983; Ben Hassine et al., 2013). In summary, we used ecological data from the four species of salamandrids that occur in North Africa to examine the following hypotheses on the distribution of these species: 1) Unrelated but sympatric species segregate at either or both spatial levels of a niche; and 2) these species are ecologically conservative, and related species retain the same niche at several spatial scales (i.e., there is phylogenetic signal in niche occupancy). MATERIALS
AND
METHODS
Climatic and Land Cover Data.—We compiled 142 georeferenced records for the four Urodela species (P. nebulosus, P. poireti, P. waltl, and S. algira) across Morocco, Algeria, and Tunisia (Fig. 1 and Table 1) using a Garmin Dakota 100 navigator (accuracy 6 30 m). These records were based on the observation of adults or larvae in terrestrial or aquatic habitats, obtained over several surveys (Escoriza and Comas, 2007; Ben Hassine and Nouira, 2012; Escoriza, 2013; Ben Hassine and Escoriza, 2014; Escoriza and TABLE 1. Descriptive statistics of the climate niche (mean and range) for four North Africa Urodela species, obtained at 30 arc-seconds resolution.
n
Pleurodeles waltl
42
Pleurodeles nebulosus 28 Pleurodeles poireti
10
Salamandra algira
62
Mean annual temperature (8C)
Aridity index
17.8 17.1–19.6 17.5 14.3–18.1 18.2 17.8–18.4 15.2 9.7–17.8
0.42 0.27–0.64 0.53 0.23–0.95 0.63 0.54–0.70 0.7 0.28–1.32
Biomass carbon density (m3C/ha)
14.3 5.0–84.0 40.5 5.0–84.0 67.9 5.0–84.0 65.8 3.0–84.0
Ben Hassine 2014a; Escoriza and Boix, 2014). We included two types of climatic variables, water-energy balance and thermal gradient. We characterized water-energy balance using an aridity index (mean annual precipitation/mean annual potential evapotranspiration; Trabucco and Zomer, 2009) with values ranging from 0.65 (humid). Thermal variation was acquired from variable annual mean temperature (mean monthly temperature/12, measured in 8C; Hijmans et al., 2005). We also included a proxy for vegetation cover, that of biomass carbon density (amount of carbon stored in living vegetation; Ruesch and Gibbs, 2008). Biomass carbon density is measured in m3C/ha, ranging from
