Ecography 30: 193 208, 2007 doi: 10.1111/j.2007.0906-7590.04818.x Copyright # Ecography 2007, ISSN 0906-7590 Subject Editor: John Spence. Accepted 5 February 2007
From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of dung beetle (Scarabaeinae) assemblages along three altitudinal gradients in the Neotropical region Federico Escobar, Gonzalo Halffter and Lucrecia Arellano F. Escobar (
[email protected]), G. Halffter and L. Arellano, Dept de Biodiversidad y Comportamiento Animal, Inst. De Ecologı´a A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico. (Present address of F. E.: Dept of Zoology and Entomology, Univ. of Pretoria, 0002 Pretoria, South Africa.)
The objective of this study is to evaluate the effect of environmental (associated with the expansion of cattle ranching) and biogeographical factors on the diversity of dung beetle (Scarabaeinae) assemblages along three altitudinal gradients in the Neotropical region. One gradient is located in the Mexican Transition Zone, on the Cofre de Perote mountain, the other two are in the northern Andes (the Chiles Volcano and the Rı´o Cusiana Basin). For the three gradients, the number of species decreased as altitude increased. On the Cofre de Perote, regardless of altitude, the number of species and of individuals was similar in both forest and pasture, while species composition was different between habitats. On this mountain, species turnover in pastures was characterized by the addition of new species as altitude increased. In the northern Andes, species diversity was always greater in the forest than in the pasture, and species turnover between habitats was notably influenced by species loss with increasing altitude. As such the pasture fauna of the northern Andes was an impoverished derivative of the fauna present in the forests at the same altitude characterized by species of Neotropical affinity with a limited capacity for colonizing open, sunnier habitats. The opposite occurs in the areas used by cattle on the Cofre de Perote. This habitat has its own fauna, which is mainly comprised of Holarctic and Afrotropical species adapted to the prevailing environmental conditions of areas lacking arboreal vegetation. These results suggest that the impact on beetle communities caused by human activities can differ depending on the geographic position of each mountain and, particularly, the biogeographical history of the species assemblage that lives there.
A decrease in species richness and changes in the composition of the flora and fauna with increasing altitude have frequently been described in the literature (Huston 1994). However, it is not possible to describe a general relationship between changes in diversity and increasing altitude (Rahbek 1995), because the ecological factors (current environmental conditions, e.g. land use) and biogeographical factors differ in their relative effect depending on the mountain system being studied (Brown 2001). This is emphasized by the fact that we still do not understand how these factors vary and interact as altitude changes. For this reason comparative studies using the same taxonomic group
along altitudinal gradients on different mountains (such as this one), and those that use several taxonomic groups along the same altitudinal gradient of the same mountain are very useful for explaining this co-variation (Lomolino 2001). Studying the altitudinal variation in dung beetle assemblages on different mountains around the world, Lobo and Halffter (2000) proposed two different biological and interrelated processes to explain the conformation of the biota on mountains, the patterns of species richness and variations in composition: horizontal colonization by elements originating from lineages inhabiting higher altitudes, and vertical
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colonization by lineages from surrounding lower lands at the same latitude. The relative effect of both processes depends on the orientation and location of the mountains, and on their degree of isolation and biogeographical history, as these characteristics greatly influence the refuge and ‘‘corridor’’ capacity of mountain areas (Lobo and Halffter 2000). Two hypotheses for explaining the changes in diversity with altitude emerge from the relative influence of these processes: 1) the mountain fauna is composed of a lesser number of phylogenetically related species relative to the fauna of lower altitudes (colonization vertical model), and 2) the mountain fauna is composed of elements with different evolutionary histories and origins compared to the lowlands fauna (horizontal colonization model). According to the first hypothesis, we would expect to find mountains that, owing to their geographic isolation, limited extension or recent geological formation, have yet to accumulate their own species assemblages. Therefore we would expect species substitution to be slow and species richness to notably decrease with increasing altitude. This would be the consequence of the environmental restrictions imposed by high altitudes on the fauna from warmer altitudes, especially in tropical regions (Janzen 1967). This appears to be the case for the northern Andes (Escobar et al. 2005) and southeastern Asia (Hanski 1983). In contrast, in the horizontal colonization model (second hypothesis), geographical and historical factors become especially relevant. This situation has been described for the mountains located in the central Iberian Peninsula (Martin-Piera et al. 1992), those of southern France (Errouissi et al. 2004) and of the Mexican Transition Zone (MTZ, Halffter 1987). Mountains that owing to their geographic location and orientation have served as refuge and speciation areas for lineages from more northern regions during the climatic changes of the Plio-Pleistocene. They consequently host a fauna adapted to cold environment and annual fluctuations in climate (Halffter 1987, Martin-Piera et al. 1992). When horizontal colonization is the main process governing the establishment of mountain fauna, one would expect to find greater phylogenetic diversity, fast species substitution and a less pronounced decrease in species richness with increasing altitude (Lobo and Halffter 2000). Our ability to understand contemporary biogeographical patterns also relies on our understanding of human impact, and specifically on how human impact affects natural ecosystems, modifying the spatial distribution of species, community and population structure throughout large geographic areas (Lomolino and Perault 2004). One such activity is cattle ranching in the mountains of the Neotropical region, which has resulted in a continuous increase in the area covered by pasture and is responsible for the homogenization of the
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mountain landscape (Kappelle and Brown 2001). During this process, sunnier open areas are created and the environmental conditions there become much more severe. Additionally, the quantity of dung, mainly from cattle, is greater, which has been shown to modify the structure of the dung beetle assemblages at the local and landscape levels in the different tropical and subtropical regions of the world (Halffter 1991, Nichols et al. in press). From these studies, the general conclusion is that vegetation cover determines species abundance and richness of this group of beetles. The association of the species with a given type of habitat appears to be related to its micro-climatic requirements (i.e. temperature, relative humidity, light intensity) and to its close dependence on mammalian dung for feeding and reproduction (Halffter and Matthews 1966). It has also been observed, however, that the preferences of species for certain habitats, both natural and anthropogenic, varies with altitude in different ways depending on the geographic position of the mountain and, therefore, the biogeographical affinity of the fauna that live there (Halffter et al. 1995, Davis et al. 1999, Romero-Alcaraz and Avila 2000, Errouissi et al. 2004). From the above, it might be expected that the effects of expanding cattle ranching on dung beetle assemblage diversity would be different in each mountain region. To evaluate this prediction we studied the diversity patterns of dung beetles along three altitudinal gradients that are ecologically similar but have different biogeographical histories. One is in the MTZ and two are in Colombia, located on opposite slopes of the northern Andes. In both mountain systems the main change in the landscape is a notable conversion of the original forest into cattle pasture and, to a lesser degree, agricultural crop fields. Given that the pastures are a relatively new type of vegetation, and the mountains vary with respect to the influence of the vertical vs horizontal colonization processes, we expect: a) the fauna of the pastures in the northern Andes to be a rarefied subset of the species found in the surrounding forested areas, comprised of species belonging to genera of Neotropical affinity with a limited capacity for colonizing open areas (Amat et al. 1997, Escobar 2004), and b) the fauna of the MTZ pastures to be a mixture of species of wide ecological tolearance, capable of leaving the forested sites, and species from nonNeotropical lineages adapted to the prevailing conditions of the areas without any arboreal cover (Halffter et al. 1995, Arellano and Halffter 2003). In this study we address the following questions: 1) how does dung beetle diversity changes with respect to altitude along three altitudinal gradients? 2) How do changes in the dung beetle assemblages occur in forests and pastures at each altitude, along the altitudinal gradient, and according to the geographical position of the mountain? 3) How do environmental and biogeographical factors
influence any differences detected (points 1 and 2) between the MTZ gradient and the two northern Andean gradients?
coffee plantations and at high altitudes, seasonal agriculture (wheat, oats and potato) and intensive dairy cattle ranching (Challenger 1998).
Materials and methods
Northern Andes, the Chiles Volcano and the Rı´o Cusiana
MTZ, Sierra Madre Oriental-Sistema Volca´nico Transversal Halffter (1987) defined the MTZ as a complex and varied region extending from northern Mexico to southern Nicaragua in which Nearctic and Neotropical biota overlap. To the north, there are Nearctic elements that gradually decrease towards the south. The northern lineages have dispersed through the mountains, which in the MTZ have a generally N-S orientation, facilitating horizontal colonization. In contrast, the coastal plains and tropical lowlands are the penetration route for Neotropical elements. This double occupation of the territory that occurs latitudinally in the MTZ has an altitudinal equivalent in the mountains: higher altitudes are occupied by lineages of northern affinity, lower altitudes by lineages of neotropical affinity and intermediate altitudes are characterized by an overlap of these two lineages and strong in situ speciation, particularly of those lineages with a long evolutionary history in the zone. The altitudinal gradient is located on the eastern slope of the Cofre de Perote volcano in the state of Veracruz (19819?19839?N, 96824?97812?W; Fig. 1) and on the eastern end of the Sistema Volca´nico Transversal where it meets the Sierra Madre Oriental. The Sierra Madre Oriental is comprised of a series of NNW-SSE folds, with an average width of 80 to 600 km each. It starts in the north on the Texas platform and is interrupted by the Sistema Volca´nico Transversal. The latter is a complex mountain chain that runs W-E and is 950 km long, and 50150 km wide. It is considered one of the youngest mountain systems in the country (Pliocene-Quaternary, 2 3 million years BP; Ferrusquı´a-Villafranca 1993). This altitudinal gradient covers different types of vegetation: tropical deciduous forest in the lowlands (B1000 m a.s.l.; temperature: 228248C; annual precipitation: 1500 2000 mm), cloud forest, oak forest and pine-oak forest at intermediate altitudes (1000 2000 m a.s.l.; 128 188C; 2000 3000 mm), pine forest and oyamel fir forests at 2000 3000/3500 m a.s.l. (58 128C; 1000 1800 mm). Above this altitude, there are high natural pastures (2858C; B1200 mm). Land use varies with altitude. In the lowlands extensive cattle ranching is the main land use, but there are also irrigation agriculture, sugar cane and fruit crops (orange, mango and tamarind). At intermediate altitudes there are corn crops, dairy farming and especially
The northern Andes belong to a mountain system that extends from northern Peru (the Huancabamba Depression) to Venezuela. In Colombia, the Andes represent an enormous mass of mountains that occupies ca 30% of the country, and diverges into three branches or ranges: the Western, the Central and the Eastern, each extending in a general south-north direction. The Western Range is considered one of the oldest ranges of the Colombian Andes (Oligocene, 38 million years BP). This range is ca 650 km long and is the narrowest of the three at B50 km wide and altitudes no higher than 4800 m a.s.l. The Eastern Range, with a length of 1200 km, is 200 km at its widest and reaches altitudes 5500 m a.s.l. It is considered the main mountain chain of the northern Andes. It originated in the Miocene (18 million years BP) and its final formation occurred in the PliocenePleistocene (2.5 million years BP; van der Hammen and Hooghiemstra 2001). The slopes of the altitudinal gradients studied in the Colombian Andes have different aspects. The Chiles Volcano (0810? 1817?N, 78815?77811?W; Narin˜o Department) is on the western slope of the Eastern Range, facing the Pacific Plain. The other gradient is in the Rı´o Cusiana Basin (5826?5823?N, 72841? 728 42?W, Boyaca´ Department), on the eastern slope of the Eastern Range, facing the Amazonia-Orinoquia region. The following vegetation types are found in the northern Andes: tropical lowland forest (up to 1000/ 1250 m a.s.l.; 228 268C; 4000 8000 mm), tropical sub-Andean forest (1000/12502000/2300 m a.s.l.; 168228C; 2000 4000 mm); high Andean forest (2000/23003200/3600 m a.s.l.; 68128C; 1000 1500 mm) and pa´ramos (above 3200/3900 m a.s.l.; 3868C; 500 1000 mm). The limits of the vegetation zones vary depending on the topography and local climate, as indicated by the values given in parentheses (van der Hammen 1995). On the Chiles Volcano, in addition to extensive cattle ranching, the lowlands are mostly used for cultivating African palm, bananas and corn. At intermediate altitudes there are coffee plantations, sugar cane and cattle ranching; and the highest altitudes (above 2500 m a.s.l.) are used for dairy farming and potato crops. In the Rı´o Cusiana basin, human activites have reduced the forested areas to remnants of varying sizes along the entire altitudinal gradient. The lower part of the mountain is dominated by pastures and small parcels with corn crops, intermediate altitudes are used for banana and sugar cane
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Forest
Pasture
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20
20
16
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450 m 1360 m 2000 m
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20
(b)
16
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12 8
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50 m
520 m
1000 m
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400
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800
50
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(c)
16
16
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450 m
900 m
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2000 m
8
4
2250 m 0
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Cumulative number of individuals Fig. 1. Smoothed species accumulation curves using the number of individuals collected as a substitute for the sampling effort applied at each forest and pasture site along each altitudinal gradient: (a) Cofre de Perote; (b) Chiles Volcano (except the pasture at 1000 m a.s.l.) and, (c) Rı´o Cusiana (except the pasture at 2000 m a.s.l.). For those sites where abundance values were 52 individuals it was not possible to estimate species richness, such as at 2600 and 3300 m a.s.l. for the Chiles Volcano.
crops, and extensive cattle ranching, and finally the highest altitudes are mostly used for dairy farming and potato, barley and wheat crops. In both the MTZ and the northern Andes mountain systems, the transformation of the forest into pastures for cattle began with the arrival of the Spaniards 500 yr ago, and has dramatically modified native ecosystem throughout tropical America (Murgueitio 2003). It is currently estimated that ca 33% (602 million ha) of this
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region is covered by permanent cattle pastures (Anon. 2002). In the mountainous regions of the Americas, the most conspicuous changes to the landscape occurred at the beginning of the 20th century, particularly form the 1950s onwards and the transformation process continues at an alarming pace to this day (Challenger 1998, Kapelle and Brown 2001). In these mountains the cattle management systems vary widely and largely depend on the climatic and topographic conditions. They also vary
in size and range from 1 to 500 ha (Murgueitio 2003). In the lowlands there are 1 8 cows ha1. At intermediate altitudes there is greater variation (1 15 ha1) and at very high sites where natural pastures are used, cattle density is 5 8 cows ha 1 (Anon. 2002). Sampling Sampling was carried out in two contrasting habitat types occurring along each of the three altitude gradients: forested areas and induced pastures used for cattle. Beetles were caught with buried pitfall traps (top flush with the soil) with two types of bait (excrement and carrion). The bait was wrapped in muslin and suspended from a wire right above the trap. The volume of the traps was ca 1000 ml (13 mm deep and 11 mm in diameter) and a mixture of water and detergent was placed inside to prevent caught beetles from leaving. On the Cofre de Perote, 16 sites were sampled at eight altitudes between 50 and 3000 m a.s.l., from May to October 1994. At 450 m a.s.l., the sites were sampled in April and May of 1993. At each site, a line of traps was set with alternating bait of fresh excrement (human and cattle mixed) and decomposing squid. Eight to 17 traps were set per forest site (mean9SD: 12.893.0) and 15 traps were set in the pastures (12.591.9). Traps were placed 2530 m apart and left in the field for one day and one night (24 h) before being collected. On the Chiles Volcano, 13 sites were sampled at seven altitudes between 50 and 3300 m a.s.l. during April and September 1993. At each site we placed a line of 12 traps with 2530 m between traps. Similarly, in the Rı´o Cusiana basin, 13 sites were sampled at seven altitudes between 450 and 2500 m a.s.l. during May and June 1997. At each site we placed a line of 10 traps, with the traps 2530 m apart. In both cases, traps were alternately baited with fresh human excrement and decomposing meat. Baited traps were left in place for two days and two nights (ca 48 h) at each site before being collected. For the gradients in the northern Andes it was not possible to collect from the pastures at 1000 m a.s.l. (on the Chiles Volcano) or at 2000 m a.s.l. (Rı´o Cusiana) owing to the lack of sites appropriate for sampling. Data analysis Given that sampling effort was different in each mountain region, we used accumulation curves with the number of individuals collected, rarefaction based on individuals, as a measure of sampling effort. For each site, the number of species observed was obtained995% confidence interval (Colwell et al. 2004). As an estimate of species richness, we used the Michaelis-Menten equation (MM), one of the curvi-
linear asymptotic functions most commonly used in the evaluation of diversity inventories and adequate for a small number of samples (Colwell and Coddington 1994). The smoothed accumulation curves were obtained by repeated random reordering (500 times) of the samples using v. 7.5.0 of EstimateS program (Colwell 2005). Analyses were carried out for three levels of comparison: a) total diversity (Gamma diversity, g) defined in this case as the cumulative number of species by habitat type along each altitudinal gradient, b) local diversity between habitats (Alpha diversity, a) along each gradient, using the total number of species recorded at each site (St) and the mean number of species per trap (Sm) and, c) species turnover (Beta diversity, b). To compare the process of g diversity accumulation in each habitat type along each gradient, we calculated the slope of the linear regression of altitude (independent variable) against the observed cumulative number of species (dependent variable). We used a Student’s t to test whether the slopes (forest vs pasture) were significantly different between habitats (Zar 1996). In order to determine the relationship between local species richness (quantified as St and Sm) and habitat along each gradient, we used an analysis of covariance (ANCOVA) with altitude as the covariable. For all cases, the model fit to the data Y mHabitat AltitudeHabitat Altitudeo. For St, we obtained the complete model assuming a Poisson distribution of errors (link function Log; Crawley 2002). For Sm, error distribution was assumed to be normal. In both cases, the model was verified by examining the standardized residuals vs the fit values, in addition to the graphical distribution of errors. Species turnover along each gradient was analyzed in two ways: a) between adjacent altitudes for each habitat type along each altitudinal gradient and, b) between habitat types (forest vs pasture) at each altitudinal level. Wilson and Shmida’s (1984) index (bt) was used: (bt) (ac)/(2abc), where a is the number of species found at two sites and b and c are the number of species lost and gained in each comparison. Values of bt vary between 0 and 1, with 1 indicating the greatest degree of dissimilarity between sites. This index produces results similar to those of other indices of b diversity and is one of the most recommended since it provides a direct expression of species turnover when the samples are arranged along an environmental gradient and because it is independent of a diversity (Wilson and Shmida 1984). Since the indices of b diversity do not reveal whether turnover values are a product of the loss or gain of species, and in order to understand the relative influence of each process, we calculated the number of species lost and gained for each comparison.
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The abundance distribution of species in each habitat was compared using range-abundance curves. These curves can also be used to describe the changes in community structure (Magurran 1988). In order to determine how different observed changes are from random differences in the structure of the beetle community when forest is replaced by pasture at each altitude, we used the test developed by Solow (1993, available in the program developed by Henderson and Seaby 2002). This randomization test can be used together with any other species abundance-based measure of community structure. We used Simpson’s index (D) (in its reciprocal form 1/D) to evaluate the change in diversity between sites: D ani (ni 1)=[N(N1)]; where ni is the number of individuals of species i and N ani : Simpson’s index represents the probability that two individuals randomly selected from a sample belong to different species, and in its reciprocal expression is a measure of dominance (Magurran 1988). In Solow’s test (1993), the observed change (d) in 1/D is compared with the values obtained from 10000 random partitions of the total sample of individuals in a set of samples similar in size to the observed. The statistical significance of the observed value of d can be evaluated by its position relative to those of the ordered values of d obtained randomly. In this test, the value of probability for a two-tailed test is given by the proportion of partitions where the simulated value ½d½ is greater than the observed value ½d½.
Results On the Cofre de Perote, we captured a total of 3245 individuals belonging to 40 species. The number of species and individuals caught in the forest was similar to that of the pasture (Table 1). For this mountain the rate of accumulation of g diversity was not different between habitats (bforest 8.1 species/1000 m, bpasture 7.5 species/1000 m; t1.62, DF 12, p 0.13). In contrast, the dung beetle diversity in the northern Andes was remarkably different between habitats. On the Chiles Volcano 1746 individuals belonging to 37 species were caught: 89% of the species (87% of individuals) were from the forest and 57% of the species (13% of individuals) were from the pasture (Table 1). Although there was no significant difference in the rate of accumulation of g diversity with increasing altitude, the value was higher in the forest than in the pasture (bforest 5.4 species/1000 m, bpasture 3.4 species/1000 m; t 1.79, DF 9, p 0.10). At Rı´o Cusiana, 1518 individuals belonging to 49 species were caught. Of these 88% (90% of individuals) were caught in the forest and 45% (10% of individuals) were caught in the pasture (Table 1)
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while g diversity accumulated at a greater rate in the forest than in the pasture (bforest 17.2 species/1000 m, bpasture 9.3 species/1000 m; t 7.36, DF 9, p B 0.0001). In spite of the limited variation in the total number of tribes, genera and species between mountains, on the Cofre de Perote, 58% of species and 53% of the individuals caught were Neotropical. On this mountain the species belonging to genera with an Afrotropical affinity (Digitonthophagus ) were captured more often in pastures, while those of Holarctic affinity (Copris and Onthophagus ) were captured equally in the forest and in the pasture (Table 1). In contrast, in the northern Andes ca 92% of species and85% of the individuals belonged to genera of Neotropical affinity and these were caught more frequently in forested areas (Table 2). In these mountains, no genus was clearly dominant in the pastures and only two species (Anisocanthon villosus and Canthon sp. 1) were exclusive to areas used for cattle located at low altitudes (Appendix 1). The complete list of species by habitat along each altitudinal gradient is given in Appendix 1. Species richness reliability Visual comparison of the species accumulation curves for the forest and the pasture at each altitude indicate that at the Cofre de Perote most of the sites reached an asymptote (Fig. 1). Estimated species richness values (MM) indicate that a large proportion of the species (80%) present at each site were captured (Table 2). In contrast, for the two northern Andes gradients, regardless of altitude the species accumulation curves for the pastures rarely reached the asymptotic phase (Fig. 1), due in part to the low number of individuals captured and to the high dominance of a few species. In this environment, the percentage of species captured was 70% in only a few cases and the estimated species richness values were highly variable, ranging from 37 to 88% (Table 2). On the other hand, at the forest sites the species accumulation curves were clearly asymptotic (Fig. 1b, c), and the proportion of species captured at each site was 76 95% (Table 2). The analysis of the entire gradient by habitat type indicates that at the Cofre de Perote 90% of the species present in each type of habitat were captured. For the northern Andes, and similar to the results found at the sites level, the proportion of species captured was lower in the pasture than in the forest (Table 2). The analysis for each mountain shows that between 88% (Rı´o Cusiana) and 95% (Cofre de Perote) of all the species present on each gradient were captured (Table 2).
Table 1. Composition at the levels of tribe and genus: number of species and individuals (in parentheses) captured in the forest and pasture along each altitudinal gradient. Biogeographical affinity of each genus: AFRAfrotropical, HOLHolarctic, NEONeotropical. *Endemic to the Neotropical region. The observed species richness (Sobs9995% CI) was calculated using the Analytical formula proposed by Colwell et al. (2004); a indicates the proportion of species observed relative to Michaelis-Menten (MM) that was used as an estimate of expected richness. Tribe
Genus
Cofre de Perote Forest
Canthonini
Coprini Dichotomiini
Eurysternini Phanaeini
Onthophagini Sysiphini Total number of tribes Total number of genera Total number of species (Sobs995%CI) Michaelis-Menten (MM) Estimate(%)a Total number of individuals
Anisocanthon NEO* Canthon NEO Cryptocanthon NEO* Deltochilum NEO* Scybalocanthon NEO* Copris HOL Ateuchus NEO* Canthidium NEO* Dichotomius NEO* Ontherus NEO* Scatimus NEO* Uroxys NEO* Eurysternus NEO* Coprophanaeus NEO* Phanaeus NEO Oxysternon NEO* Sulcophanaeus NEO* Digitonthophagus AFR Onthophagus HOL Sisyphus AFR/HOL
Pasture
Chiles Volcano Both
Forest
Pasture
Rı´o Cusiana Both
7 (723)
6 (321)
7 (1044)
2 (3)
2 (120)
3 (123)
3 (287)
2 (36)
3 (323)
1 (8)
3 (89)
3 (97)
4 (285) 1 (164) 1 (4)
2 (5) 1 (23) 1 (2)
4 (290) 1 (187) 1 (6)
1 (7) 3 (77) 1 (27)
1 2 1 1
1 3 1 1 1 1 2 3
3 (29) 2 (6)
2 (4) 3 (202) 3 (259)
(31) (13) (54) (9)
1 (45) 2 (30) 2 (16)
11 (608) 1 (21) 6 11 3393.0 36.2 91.1 1849
1 (2) 1 (33) 2 (4) 1 (53) 10 (751) 6 12 3194.4 34.3 90.4 1396
(38) (90) (81) (9) (45) (2) (63) (20)
1 (53) 12 (1359) 1 (21) 7 14 4092.7 42.2 94.8 3245
2 (4) 3 (173) 3 (253) 6 4 1 1 2 2
(400) (29) (5) (20) (21) (86)
1 (4)
7 4 1 1 2 2
3 (72)
2 (12)
3 (84)
6 14 3592.8
6 11 2195.4
6 14 3792.7
38.2 91.6 1519
2 (5) 4 (19) 1 (2)
27.6 76.0 227
(405) (48) (7) (20) (21) (90)
40.5 91.3 1746
Forest 3 (197) 1 (46) 5 (100)
Pasture 1 (5) 1 (4) 1 (1)
1 4 1 5
(5) (201) (46) (101)
1 10 6 2
(1) (129) (210) (279)
5 5 1 3
(63) (179) (3) (30)
1 10 6 2
(1) (129) (193) (231)
3 (17) 2 (48)
5 4 1 2
(56) (153) (2) (26)
3 4 1 2
(7) (26) (1) (4)
1 (30) 2 (199) 5 13 4393.8 48.7 88.3 1363
Both
1 (30) 4 (42) 5 10 2293.9 27.9 78.8 155
4 (241) 5 14 4993.8 55.4 88.4 1519
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Table 2. Observed and estimated species richness (forest/pasture) in each of the sites along each altitudinal gradient. *Denotes those sites where the estimates were lower than 80%. For the Chiles Volcano at 2600 m a.s.l., it was not possible to calculate the estimated value of species richness because abundance was52 individuals. Mountain/elevation (m a.s.l.)
Forest/pasture No. individuals
Cofre de Perote 50 450 900 1340 1860 2000 2340 3000 Chiles Volcano 50 520 1000 1350 1800 2600 3300 Rı´o Cusiana 450 900 1250 1500 1750 2000 2500
MM
Estimate(%)
306/226 721/125 389/250 102/236 57/47 44/186 216/240 14/68
1093.3/1192.5 1593.5/1094.5 1092.4/1494.0 1090.9/692.3 591.2/593.0 491.3/892.4 391.2/390.0 290.0/392.2
11.6/13.4 16.9/11.7 11.1/18.2 11.3/6.6 5.7/5.9 4.2/8.3 3.5/3.6 2.8/3.2
86.2/89.1 88.7/85.4 90.1/76.2* 88.5/90.9 87.7/84.7 95.2/96.4 85.7/83.3 71.4*/93.7
216/181 85/21 357/ 684/14 175/6 2/1 0/4
1791.5/992.4 1295.1/693.1 1291.8/ 1390.0/592.3 891.3/492.9
19.5/10.2 14.5/8.8 12.3/ 13.7/8.5 8.8/10.7
87.2/88.2 82.7/68.1* 97.5/ 94.9/58.8* 90.9/37.3*
13/17 338/33 280/57 187/20 309/20 53/ 65/16
Variation in Alpha diversity The number of species decreased with increasing altitude on the three gradients (Fig. 2). However, the pattern of change in species richness at the local level (St and Sm) at each habitat type was different for each mountain system. On the Cofre de Perote values of St were similar for the forest and the pasture regardless of altitude (mean9SD: forest 7.6590.81, pasture 7.7590.80, p0.92; Table 3), and there were even some altitudes for which St was greater in the pasture (Fig. 2a). On this mountain, altitude explained 74% of the variation and habitat type explained 1%. In contrast, on the Chiles Volcano St values were always higher for the forest than for the pasture. (forest 9.090.61, pasture4.390.66, p0.001; Fig. 2b). On this mountain, altitude explained 62% of the variation and habitat type accounted for 17% (Table 3). Similarly, at Rı´o Cusiana, St was also consistently greater in forest than in pasture (forest 10.5891.4, pasture 5.891.53, p0.002; Fig. 2c). The model explained 48% of the total variation, much of which was associated with habitat type (40%), while altitude accounted for the remaining 8% (Table 3). The lack of fit of the model, particularly for the forest, is a result of the increase in St at intermediate altitudes. The analyses
200
Sobs.995% IC
0/190.0 1092.5/390.9 1691.3/692.4 1294.8/1195.1 1392.7/391.2 1492.7/391.2 591.2/ 591.3/490.9
/1.5 11.2/7.16 18.3/13.7 14.5/15.6 14.9/3.4 18.4/3.4 5.5/ 5.9/5.7
/66.6* 89.3/41.9* 87.4/43.8* 82.7/70.5* 87.2/88.2 76.1*/88.2 90.9/ 84.7/70.1*
did not detect significant differences in the three altitudinal gradients regarding the rate at which species are lost as altitude increases for either type of habitat (Table 3). The analysis using mean species richness (Sm) produced a pattern similar to that described for St (Table 3). Variation in Beta diversity Species turnover patterns between adjacent levels were different on each mountain according to habitat type (Fig. 3). On the Cofre de Perote for the forest the values of bt reached a maximum between 900 and 1340 m a.s.l. and then slowly decreased with increasing altitude (bt: 0.90.6). In this habitat the values of bt were influenced by the loss of species (Fig. 3a). In contrast, for pastures species turnover increased rapidly up to 1860 m a.s.l. (bt: 0.45 0.82) and stayed constant above 2000 m a.s.l. For the pasture of the Cofre de Perote, values of bt were the result of gaining species at certain altitudes (Fig. 3b). The comparison between forest and pasture habitats for each altitude shows that although species turnover between habitats tends to decrease with increasing altitude (bt: 0.52 0.2), the values of bt reflect the gain of species, particularly above 1800 m a.s.l. (Fig. 3c).
12
Table 3. Summary of the ANCOVA results. For St (total number of species per site) a Generalized linear model (GLM) was used with a Poisson error distribution (link functionLog). Deviance values (ca x2) are given as a measure of the model’s fit. Sm denotes the mean number of species per trap. In both cases, the fit model was YmHabitatAltitudeHabitatAltitudeo. * pB0.05*; pB0.01**; pB0.001***; ns not significant.
10
Factor
DF
St Deviance (x2 approx.)
Sm F
Cofre de Perote Habitat Altitude HabitatAltitude Error
1 1 1 12
0.03ns 26.73*** 0.29ns 8.76
1.69ns 17.39*** 1.0ns
Chiles Volcano Habitat Altitude HabitatAltitude Error
1 1 1 9
10.10*** 38.32*** 0.09ns 12.85
8.69** 9.65** 1.63ns
Rı´o Cusiana Habitat Altitude HabitatAltitude Error
1 1 1 9
12.53*** 2.16ns 0.75ns 15.75
16.40** 2.75ns 2.67ns
20
(a)
Forest: a = 13.3; b = -3.9 Pasture: a = 12.7; b = -3.3
18 16 14
8 6 4 2 0 0 20
500
1000
1500
2000
(b)
2500
3000
3500
Forest: a = 17.0; b = - 5.3 Pasture: a = 8.2; b = - 3.4
18
Number of species
16 14 12 10 8 6 4 2 0 0
20
500
1000
1500
2000
(c)
2500
3000
3500
Forest: a = 16.1; b = -3.7 Pasture: a = 5.9; b = -0.4
18 16 14 12 10 8 6 4 2 0 0
500
1000
1500
2000
2500
3000
Altitude (m a.s.l.)
Fig. 2. Variation in total species richness (St) in each type of habitat as elevation increases: (a) Cofre de Perote, (b) Chiles Volcano, (c) Rı´o Cusiana. The black dots represent forest sites and the open rectangles represent the pastures. Lines indicate the fitted curve (forest continuous line; pasture dotted line).
Species turnover between adjacent altitudes on the Chiles Volcano, both in the forest and the pasture, show a similar pattern, decreasing at intermediate
altitudes and then reaching maximum values at the upper end of the gradient, although for the pasture the increase was more gradual (bt forest: 0.28 1.0; bt pasture: 0.55 1.0). In both habitats the values of bt were affected by the constant loss of species with increasing altitude (Fig. 3d, e). Likewise, when species turnover was compared between the forest and the pasture at each altitude, above 1800 m a.s.l. the similarity between habitats was lower and the values of bt reflect the loss of species (Fig. 3f). As for t he Chiles Volcano, at Rı´o Cusiana, species turnover between adjacent altitudinal levels in both forest and pasture decreases from low to intermediate altitudes around 1250 m a.s.l., and then rapidly increases towards the top of the gradient the (bt forest:. 0.24 0.9; bt pasture: 0.52 1.0). On Rı´o Cusiana, in contrast to what we observed on the other altitudinal gradients, the values of bt for both the forest and the pasture reflect the gain of species at the beginning of the gradient between 450 and 1250 m a.s.l. Above this the values of bt reflect the loss of species (Fig. 3g, h). The comparison between the forest and the pasture at each altitude indicate a strong species turnover between habitats, especially above 1500 m a.s.l., as well as values of bt that are strongly influenced by the loss of species along the entire altitudinal gradient (Fig. 3i). Variation in abundance and dominance On comparing the distribution of species abundance between habitats, above 1340 m a.s.l. on the Cofre
201
Cofre de Perote
Chiles Volcano 1 0 .8
12
Río Cusiana
(d)
16
1 0.8
12
0 .6 8
8
0
Number of species
50
0 -45
0 45
12
8 0.4
4
0
0
0
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520 000 350 600 800 300 500-1 0-1 0-1 0-2 0-3 52 135 100 260 180
1
16
0 .8
12
(e)
0.8
50
16
-45
0 45
0-9
8 0.4
0. 8
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30
450
900 1340 1860 2000 2340 3000
0.4
0
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20
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000 600 0-3 0-2 260 180
(f)
16
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0.2 0
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00 900
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50 12
00 -15
50 00 -17 -25 00 50 15 17
(i)
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1 0.8
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0.6
0.6
8
8
0
8
0
0.4 4
0.8 0.6
4
0. 6 8
1
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5 50-
1
(h)
16
4
00 000 -2340 -3000 340 86 0 0-1 40-1 60-2 40 00 90 20 13 23 18
(c)
0
0.6
0 .2 0
0.2
00 50 00 00 50 00 0-9 -12 -15 -25 -17 -20 45 50 00 50 00 900 12 20 15 17
1
0. 4
0
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8 4
0.6
0. 2
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0 860 340 000 -2340 -3000 -90 0-1 40-1 60-2 00 40 90 13 18 20 23
(b)
16
1
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0 .4 4
(g)
16
0.4
0.4
0.2
4
0
0
βt
(a)
16
0.2 0 50
0 52
0 100
0 135
0 180
0 260
0 330
4
0.2 0
0 450
900
50 12
00 15
17
50
00 20
00 25
Altitude (m a.s.l.)
Fig. 3. Changes in bt diversity (Wilson and Shmida index; black dots) between adjacent altitudes in the forest (a, d, g) and pasture (b, e, h) along each altitudinal gradient. The bottom figures (c, f, i) show species turnover between habitats (forest vs pasture) at each altitudinal level. The filled bars indicate the number of species lost and the open bars indicated the number of species gained in each comparison.
de Perote, abundance was greater in pastures (Table 2). High on this mountain, the areas used for cattle were dominated by very few species (Fig. 4), while between 50 and 900 m a.s.l. the distribution of abundances was more even and the number of individuals captured was greater in the forest than in the pasture. On this mountain, Simpson’s index was greater for pastures for some altitudes and the change in diversity between habitats was significantly different from a random distribution (Table 4). In contrast, for the northern Andes independent of altitude, abundance was always greater in the forest (Table 2). For both the Chiles Volcano and Rı´o Cusiana, the range-abundance curves for the forest show a more even distribution than the open areas used for cattle do; areas where the dominance of only a few species increased (Fig. 4). On these mountains, Simpson’s index was generally greater at forest or was similar between habitats and, the changes in diversity were not significantly different from a random distribution (Table 4).
202
Discussion On the three altitudinal gradients studied, we observed a decrease in species richness as altitude increased; this phenomenon has been reported for different taxonomic groups on different mountains (Rahbek 1995 and references therein). However, the lack of comparative studies between taxonomic groups, and between natural and anthropogenic environments hinders efforts to properly contrast patterns of diversity with altitude (Lomolino 2001). In the case of dung beetles, this study indicates that in the northern Andes the rate of species loss with increasing altitude was much more pronounced in the forest than in the pasture. While on the Cofre de Perote (MTZ) the decrease was very similar for both habitat types. In these pastures, the decrease in species richness was lower owing to the presence of a set of species of northern affinity (Paleoamerican Montane and Nearctic Patterns) or of those that evolved on the Mexican High Plain (Altiplano Distribution Pattern). The latter is
Cofre de Perote 1000
50 m
900 m
450 m
2340 m
1340 m 2000 m
100
3000 m
1860 m 10
1
Chiles Volcano
1000
Abundance (Log 10)
1350 m 50 m 100
1000 m*
1800 m
520 m 10
1
Río Cusiana
1000
900 m
1500 m
1250 m 100
1750 m 2500 m 2000 m*
450 m
10
1
Abundance Range
Fig. 4. Dominance-diversity curves comparing the distribution of abundance for forest (black dots) and pasture (open squares) at each elevation along each gradient. Altitudes marked with an asterisk * indicate sites where it was not possible to collect in pastures (1000 m a.s.l. on the Chiles Volcano and 2000 m a.s.l. on the Rı´o Cusiana).
comprised of species with a heliophile habit that are of South American origin and were isolated in the MTZ a very long time ago (having migrated during the Oligocene-Miocene period, Halffter 1987). Consistent with the rate of species loss with increasing altitude, the opposite process species accumulation or g diversity in each type of habitat along each altitudinal gradient exhibited a similar pattern. For the Cofre de Perote, both habitats accumulated a similar number of species; while in the northern Andes species accumulation was
always lower for pasture than for the forest. As such, a first conclusion that can be drawn from these results is that the degree to which species richness decreases and the degree to which species are added in each type of habitat as altitude increases, indicate that the impact of cattle pasturing is different for each gradient, and results from the biogeographical differences between the mountain systems studied. At the local level, the pastures of the northern Andes always were less diverse than sites at equivalent altitudes
203
Table 4. Simpson’s index values (1/D) obtained for each type of habitat along each altitudinal gradient; d is the difference between forest and pasture in the Simpson’s index (see Data analysis). * Denotes elevations on the Chiles Volcano where it was not possible to calculate 1/D because abundance was52 individuals. Elevation (m a.s.l.)
Forest
Pasture
d
Number of times ½d½ simulated½d½ observed
p
Cofre de Perote 50 450 900 1340 1860 2000 2340 3000
2.13 6.07 2.94 6.00 3.03 2.71 1.28 1.57
5.41 3.90 6.29 1.44 1.60 4.27 1.94 1.06
3.28 2.17 3.35 4.56 1.43 1.56 0.66 0.51
0 2 0 0 42 10 0 215
B0.0001 0.0002 B0.0001 B0.0001 B0.0042 0.001 B0.0001 0.02
7.67 4.70 4.58 5.68 5.90
2.19 3.33 4.79 5.00
5.48 1.37 0.89 0.90
0 3091 5788 7897
B0.0001 0.31 0.57 0.78
4.18 2.43 5.30 2.39 2.32 2.78 2.44
3.5 4.16 4.47 1.38 3.00 2.85
0.68 1.73 0.83 1.01 0.68 0.41
199 7992 3894 1566 2378 5860
0.02 0.79 0.39 0.15 0.23 0.58
Chiles Volcano 50 520 1000 1350 1800 2600* 3300* Rı´o Cusiana 450 900 1250 1500 1750 2000 2500
on the Cofre de Perote (MTZ). On the Cofre de Perote differences were accentuated at lower altitudes and less conspicuous on the upper parts of the altitudinal gradient. The latter was particularly notable at altitudes over 1800 m a.s.l. owing to the influence of the previously mentioned Holarctic and High Plain elements. This agrees with findings for different mountain regions in Europe where dung beetle richness and abundance, especially in open habitats, are not negatively correlated with altitude (Mene´ndez and Gutie´rrez 1996, Romero-Alcaraz and A´vila 2000). In temperate climates, such as the upper part of the Cofre de Perote, Scarabaeinae are restricted to or dominate open environments. This is a general phenomenon characteristic of the northern hemisphere, both latitudinally and altitudinally (Martin-Piera et al. 1992), and one that does not occur or is very limited in the northern Andes. There, the regional set of species than is adapted to forest conditions has more species that the set that is adapted to open habitats. The study by Amat et al. (1997) shows that the forests of the Sabana de Bogota´, Eastern Range (2800 2900 m a.s.l.) has up to 11 species while the pastures only have three, and these belong to genera that are widely diversified in the lowland forests. Based on these results it is also possible to conclude that if the reduction of forest in the upper slopes of the northern Andes continues as a conse-
204
quence of creating cattle pastures, the beetle fauna will become isolated in small forest remnants, as has been documented for birds and amphibians in fragmented areas above 1500 m a.s.l. in the mountains of Colombia and Ecuador (Kattan and A´lvarez-Lo´pez 1996, Marsh and Pearman 1997). Therefore, the integrity of these communities depends to a large extent on the connectivity of the forests along the altitudinal gradient, and on alternative land uses, both of which can buffer the impacts of cattle ranching on biodiversity (Pineda et al. 2005). The comparison of fauna composition at the tribe and genus level for each mountain and between habitats reveals notable differences: 32.5% of the species and 43% of the individuals on the Cofre de Perote belong to Onthophagini, while in the northern Andes this tribe represents no more than 8% of the species and 15% of the individuals. The present day distribution of Onthophagus (Onthophagini) is the result of an ancient process of invasion of the Americas from Asia, followed by intense diversification in North America, including Mexico. With 2000 species described, this genus is considered one of the most modern of the dung beetles and is supposed to have diversified during the Oligocene (ca 23 33 million years BP), a diversification that coincided with the expansion of pastures and the spread of mammals (Davis et al. 2002). Currently, the
representatives of this genus are ubiquitous members of beetle communities in areas where the forest has been cut at different altitudes in both Mexico and Central America (Halffter et al. 1995, Horgan 2002). In South America, however, this genus is restricted to distinct habitat types below 2000 m a.s.l. with few species at higher altitude in the mountains (Zunino and Halffter 1997). The other member of tribe Onthophagini found on the Cofre de Perote, Digitonthophagus gazella , is a notable example of the modern expansion process on the American continent and could serve as a model for understanding how Paleo-American tropical lineages expanded on this continent. This Afrotropical species was introduced in Texas in 1972 and in little more than 30 yr has made its way down to southern Nicaragua (Montes de Oca and Halffter 1998). According to Halffter et al. (1995), D. gazella is found in open habitats and is markedly associated with cattle dung. Its dispersal has been favored by deforestation and by the change in the use of large tracts of land to cattle pasture. Consequently, the invasion of introduced species is indicative of possible habitat deterioration (Kennedy et al. 2002). The results of this study and others (Halffter et al. 1995, Arrellano and Halffter 2003) indicate that the pastures of the Cofre de Perote have served as altitudinal dispersal routes for heliophile and thermophile species such as D. gazelle , and Euonicitellus intermedius (another species introduced in North America) from tropical lowland landscapes. So, the expansion of areas used for pasturing cattle in the mountains appears to have facilitated the expansion of those species adapted to open environments previously present in the region. This may be contributing to the homogenization of the fauna along altitudinal gradients, as reported for amphibians, reptiles and birds in Costa Rica’s mountains where this process is favored by an increase in temperature at higher altitudes as a consequence of global climate change (Pounds et al. 1999). Although we do not have a definitive image of horizontal colonization by beetles in the northern Andes mountain ranges, studies of plants and birds allows us to illustrate its relevance; as one moves up these mountains, the proportion of genera originating outside the tropics increases (Vuilleumier 1986, Gentry 2001). However, for the dung beetles and butterflies, colonization is mainly vertical (Decimon 1986, Escobar et al. 2006). The fauna of the intermediate and high altitudes on these mountains is a derivative of the found in the neighboring lowlands. This also occurs in the mountains of southeast Asia (Hanski and Niemela¨ 1990), Ecuador (Celis et al. 2004) and in some of the mountains of Costa Rica (Halffter and Reyes-Castillo unpubl.). Therefore for historical-biogeographical reasons, in the northern Andes species turnover between
adjacent altitudes mainly results from the loss of species. This is a product of the process of vertical colonization and can be explained by the restrictions imposed by altitude in environmental terms (decreasing temperature) and the reduction in food availability; conditions that require physiological adjustments if the higher altitudes of the mountains are to be colonized (Chown et al. 2002). There is an important difference in the species turnover between the two Andean transects. On the Chiles Volcano (located on the western slope of the Eastern Range), species turnover was dominated by the loss of species, while on the Rı´o Cusiana transect (located on the eastern slope of the Eastern Range), there was a gain of species below 1250 m a.s.l. the contact zone between the lowland fauna and the mountain forests. According to Lomolino (2001), the degree of overlap or juxtaposition between adjacent communities along altitudinal gradients contributes to explaining the type of relationship between species richness and altitude (monotonic model vs hump-shape model) and particularly, the degree of faunistic turnover between adjacent altitudinal bands. Precisely this was observed for five altitudes gradients between 08 and 78 North latitude on the Eastern cordillera of the Andes, Colombia (Escobar et al. 2005). Therefore, the differences in the species turnover patterns for opposite slopes in the northern Andes could result from the fact that their lowland dung beetle faunas differ in diversity and composition. This has been documented for the less diverse lowlands of the Pacific Plains on the western slope of the Andes (Peck and Forsyth 1982, Medina and Kattan 1996) and for the locations of the Amazonia-Orinoquia that are richest in species on the eastern slope of the Andes (Howden and Nealis 1975, Pulido et al. 2003). There appears to be an altitudinal gradient with respect to abundance, and it depends on habitat type. In general, abundance was much greater in forests than in pastures, while dominance increased in the pastures. However, the differences in abundance between the pastures of the different mountains above altitudes of 1750 m a.s.l. are marked. On the Cofre de Perote (MTZ) pastures were home to 39% of all the individuals collected, while in the northern Andes the proportion of individuals found in pastures was never higher than 10%. High total abundance values (biomass) have been recorded in the higher zones where species richness decreases in the mountains of Europe (Lumaret and Stiernet 1991) and in Asia (Hanski and Krikken 1991). In all of these studies, the dominance of a few species was found to increase in what seemed to be a compensating mechanism for adjusting populations to the available resources (Hanski and Cambefort 1991).
205
Although cattle dung can be abundant resource in the pastures of many tropical mountains, in this environment it dries out quickly and this modifies its microenvironmental and nutritional characteristics (Halffter 1991). Once changed, this dung can only be used by some species; species that are physiologically and behaviorally adapted to using the dung of medium sized and large herbivores in open areas. This is the case for many species of Holarctic (Onthophagus chevrolati , O. incensus) and Afrotropical (D. gazella and E. intermetus ) affinity in the MTZ or those of Neotropical affinity that exhibit wide ecological tolerance and are present in both mountain systems, such as Dichotomius colonicus , Ontherus mexicanus and Scatimus ovatus in the MTZ (Halffter et al. 1995, Arellano and Halffter 2003) and Dichotomius satanas , D achamas , Ontherus kirchii , O. brevicollis , Eurysternus marmoreus and E.caribaeus in the northern Andes (Amat et al. 1997, Escobar 2004). The limited presence of the Scarabaeinae in the pastures of the northern Andes highlights the following paradox: in spite of the abundance of food cow dung this environment is not available and effectively does nor exist for the majority of species that inhabit the native forest. This supports the concept that in Tropical America plant shade and its influence on microclimatic conditions on the ground are more important than a greater abundance of food (Halffter 1991).
Conclusion Although it was not possible to control factors such as the size of the mountains, the topography, the climatic variation, the configuration of the landscape and food supply, the results are revealing. The change in beetle community attributes that we observed in the face of an ecological change resulting from the transformation of forest to cattle pastures were clearly different along each altitudinal gradient. This suggests that processes of disturbance caused by human activity along altitudinal gradients can impact communities in different ways, depending on the geographic position of each mountain and particularly the biogeographical history of the group of species that inhabits it. This study contributes to the understanding that the response of communities to human activities (such as replacing forest with pastures, habitat loss and fragmentation) cannot be extracted from their regional context. Nor can they be understood without considering the biogeographical patterns and the evolutionary restrictions (e.g. habitat specialization) of species that belong to these communities (Ewer and Didham 2006).
Acknowledgements We are grateful to the subject editor of Ecography for valuable remarks and critiques. We thank
206
Bianca Delfosse for translating the article into English and Ute Kryger for offering valuable suggestions to the last version. Research in Colombia was supported by the Financiera Ele´ctrica Nacional (FEN) and by the Inst. Colombiano para el Desarrollo de la Ciencia y la Tecnologı´a (COLCIENCIAS, project 2245-13-306-97). In Mexico, this research was financed by the Consejo Nacional de Ciencia y Tecnologia de Me´xico (CONACYT, project 37514-V), by the Comisio´n Nacional para el Uso y Conocimiento de la Biodiversidad (CONABIO, projects 093-01 and EE005) and by Ministerio del Medio Ambiente y Recursos Naturales y el Consejo Nacinal de Ciencia y Tecnologia de Me´xico (SEMARNAT-CONACyT, project 2004-56-A1). Finally, the first author appreciates support from Univ. of Pretoria (Postdoctoral Fellowship Programme) to allow writing the last version of this article.
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