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Spatial patterns of rodent communities in the Ramon erosion cirque, Negev Highlands, Israel
Journal of Arid Environments (1996) 32: 319–327
Spatial patterns of rodent communities in the Ramon erosion cirque, Negev Highlands, Israel
B. Krasnov*, G. Shenbrot*, I. Khokhlova† & E. Ivanitskaya‡ *Ramon Science Center, Ben-Gurion University of the Negev, Mizpe Ramon 80600, Israel †Desert Animal Adaptations and Husbandry, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel †Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel (Received 13 July 1994, accepted 13 October 1994) Habitat distribution of 12 rodent species in the Negev Highlands, Israel was studied. Five main habitat types were distinguished, based on similarity in rodent species composition of sample plots: (i) sand dunes, (ii) flat gravel plains (hammadas), (iii) limestone cliffs, (iv) wadis among loess hills and (v) wadis among gravel plains. Species richness was highest in (v) and lowest in (iii). Species diversity was highest in (iii) and lowest in (v) and intermediate and similar in all other habitat types. Rodent biomass was the lowest in (ii) and highest in (iv). Indirect rodent ordination showed that species were spatially segregated along the first three ordination axes. These axes may be interpreted as (a) a gradient of soil hardness from rock to sand, (b) a gradient of relief from cliffs to flat plains and (c) a gradient of vegetation density. We classified rodents into five groups by their habitat preferences: petrophyles (Acomys spp. and Sekeetamys calurus), psammophyles (Gerbillus gerbillus), inhabitants of densely vegetated wadis (Psammomys obesus and Eliomys melanurus), inhabitants of open gravel plains (Jaculus jaculus, Gerbillus henleyi and G. nanus), and habitat generalists (Meriones crassus and Gerbillus dasyurus). ©1996 Academic Press Limited Keywords: rodents; habitats; desert; community structure
Introduction In modern ecology the term ‘habitat’ is used in a variety of ways. Most often this term is used to describe an area of a particular relief, vegetation and soil structure. It is commonly thought that the structure of an animal community is determined by the habitat structure of an area. Another concept is to consider habitat as related to a particular species or group of species. In the framework of this concept, habitat is a patch with a set of environmental 0140–1963/96/030319 + 09 $18.00/0
© 1996 Academic Press Limited
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conditions and resources promoting the occupancy, survival and reproduction by individuals of a given species (Morrison et al., 1992). Hence, habitat structure of an area is not predefined, but is a complex of co-evolved responses of organisms to abiotic and biotic factors (Rosenzweig, 1993). In our opinion, this concept is more objective because it reflects the integrated results of interactions of organisms and their environments. Examples of such an approach to habitat classification using clusteranalysis based on rodent species composition were presented for Mojave Desert (Matson, 1976) and the Central Chihuahua (Mexico) (Rogovin et al., 1985). The object of our study was to investigate the spatial structure of desert rodent communities in the Ramon erosion cirque. We distinguished, a priori, several habitat types (rocks, sand dunes, hammadas and dry riverbeds) by their physiognomic appearance. We then attempted to identify habitat structure of the studied area based on the relative abundance of rodent species. Results of the study would be a posteriori scheme of habitat types from a ‘rodent’s point of view’.
Material and methods Study area The Ramon erosion cirque (30°35'N, 35°45'E, about 200 km2 total area) forms the southern boundary of the Negev Highlands. The northern and southern rims of the cirque are 800 m and 510 m a.s.l., respectively, and the lowest point of the cirque bottom is 420 m.a.s.l. Summer is hot and winter is relatively cold (mean monthly maximum and minimum air temperatures are 33·9°C and 19·7°C in August and 14·9°C and 6·4°C in January, respectively). There is a very sharp decrease in annual rainfall from 85 mm on the cirque’s north rim to 56 mm at its bottom (data from Nature Reserves Authority of Israel). This precipitation gradient is also expressed from the west to the east of the Ramon cirque. The landscape of the Ramon cirque ranges from sand dunes to limestone and sandstone rocks in the rims.
Data collection Rodents were trapped in 1992–1993 on 31 one hectare plots that were chosen to represent main substrate and vegetation gradients. Seven of these plots were sampled regularly once every 2 to 3 months to estimate seasonal patterns of community organization. The other 24 plots were sampled twice a year. Each plot was sampled over 3 to 5 days using 50 Sherman live-traps placed in a grid at 5 3 5 stations with two traps per station and an interval of 20 m between stations. Each trapped animal was sexed, weighed, marked by toe-clipping and released. Jerboas were caught with a net at night using a searchlight. Fat sand rats were counted in the morning using binoculars. In total, 844 individuals of 12 species were captured. Data on Mus musculus were excluded from the analysis because of extremely low numbers. In accordance with our observations, M. musculus is characterized in this area by very unstable numbers. Just before the beginning of regular sampling, during preliminary trapping, this species was locally common (up to six individuals per ha). However, at the main sampling period it had almost completely disappeared.
Statistical data processing Plots were classified based on similarity of rodent species composition using cluster-
PATTERNS OF RODENT COMMUNITIES
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analysis (cosine similarity measure, UPGMA algorithm). An indirect ordination procedure was performed by correspondence analysis to reveal placement of species’ positions along main environmental gradients. Correspondence analysis is an ordination technique in which the species’ scores on ordination axes are obtained from the sample scores (Gauch, 1982). We used Hill’s N2 index (reciprocal Simpson’s) as a measure for species diversity, N2 = 1∑pi2, where pi is the proportion of individuals belonging to species i in a collection (Hill, 1973). Results Rodent species and habitat types In total we recorded 21 individuals of Jaculus jaculus (L., 1758), four Eliomys melanurus (Wagner, 1840), 142 Gerbillus henleyi (de Winton, 1903), four G. nanus (Blanford, 1875), 395 G. dasyurus (Wagner, 1842), 20 G. gerbillus (Olivier, 1801), 22 Sekeetamys calurus (Thomas, 1892), 130 Meriones crassus (Sundevall, 1842), 50 Psammomys obesus (Cretzschmar, 1828), two Mus musculus (L., 1758), 34 Acomys cahirinus (Desmarest, 1819), and 20 A. russatus (Wagner, 1840). Results of cluster-analysis of rodent species composition and relative abundances indicate that from our sample plots several groups were distinguishable (Fig. 1). The number of distinguished groups depends on the selected critical level of similarity
Rescaled similarity (% %) Habitat type
(c) v (b) (a)
iv
iii
ii
i
100
Plot number 19 25 7 15 8 11 10 22 9 26 29 28 5 17 24 18 12 23 30 20 21 31 13 14 6 16 2 27 1 4 3
80
60
40
20
0
Figure 1. Dendrogram showing results of cluster-analysis of sample plots based on their similarity in rodent species composition.
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among them. We chose the 60% level of similarity as a critical because at this level the grouping of sample plots revealed the habitat types in the clearest way. Four of the five obtained groups may be related directly to distinct habitat types as follows: (i) sand dunes of the easternmost edge of the cirque with cover of Calligonum comosum or Echiochilon fruticosum (perennial vegetation cover 7·4%); (ii) flat gravel plains (hammadas) of the eastern part of the cirque with sparse vegetation of Hammada salicornica, Anabasis articulata and Gymnocarpos decandrum (cover 5·7%); (iii) limestone cliffs of the southern rim of the cirque with sparse cover (4·0%) of Zygophyllum dumosum, Helianthemum kahiricum and Reaumuria hirtella; and (iv) densely vegetated (cover 18·5%) wadis among loess hills on the northern rim of the cirque with Anabasis articulata, Atriplex halimus and Artemisia herba-alba. The fifth group is a complex conglomerate, which may be interpreted as dry riverbeds (or wadis), which varied in vegetation density. It includes: (v(a)) wide dry wadis of the eastern and central parts of the cirque with dense cover (30·9%) of Retama raetam, Moricandia nitens, Tamarix nilotica and Artemisia monosperma; (v(b)) narrow shallow wadis and loess hills of the western parts of the cirque with cover of Salsola schweinfurthii, Anabasis articulata and Atriplex leucocardia (perennial vegetation cover 6·0%); and (v(c)) narrow shallow wadis of the eastern and central cirque parts with 21·1% cover of Retama raetam, Moricandia nitens and Gymnocarpos decandrum. Parameters of rodent communities occurring in different habitat types are presented in Table 1. Similar numbers of species (5–6) occurred in most habitat types. Minimal species richness (4) was recorded for cliffs (iii) and maximal (7) for wide eastern wadis Table 1. Average rodent density (individuals per ha), species richness, diversity (reciprocal Simpson’s measure) and biomass (g per ha) in main habitat types of the Ramon cirque. Habitat types are: (i) sand dunes; (ii) flat gravel plains (hammadas); (iii) limestone cliffs; (iv) densely vegetated wadis among loess hills; (v(a)) wide wadis among gravel plains; (v(b)) scarcely vegetated wadis among loess hills; (v(c)) narrow wadis among gravel plains. Average adult body mass (g) for each species is represented in parentheses after the species name
Habitat types Species
i
ii
iii
iv
v(a)
v(b)
v(c)
0·33 0·00 0·17 0·00 0·33 3·33 0·00 1·50 0·00 0·00 0·00 0·00
0·77 0·00 0·38 0·01 1·62 0·00 0·00 0·40 0·00 0·00 0·01 0·00
0·00 0·00 1·32 0·00 0·00 0·00 1·07 0·00 0·00 0·00 0·88 0·21
0·13 0·75 6·88 0·00 0·00 0·00 0·00 1·00 7·25 0·00 0·13 0·00
0·01 0·00 2·42 0·03 1·47 0·00 0·00 0·98 0·00 0·14 0·01 0·00
0·83 0·00 2·33 0·00 0·00 0·00 0·00 0·33 0·17 0·00 0·17 0·00
0·08 0·00 5·54 0·00 0·29 0·00 0·00 0·94 0·00 0·00 0·02 0·00
5
6
4
6
7
5
5
Diversity
2·36
2·89
3·27
2·57
2·85
2·33
1·49
Biomass
20·55
103·9
126·2 1449·9 155·2
173·5
213·6
Jaculus jaculus (67·0) Eliomys melanurus (49·6) Gerbillus dasyurus (21·1) G. nanus (22·3) G. henleyi (9·8) G. gerbillus (20·1) Sekeetamys calurus (52·8) Meriones crassus (81·1) Psammomys obesus (166) Mus musculus (14·0) Acomys cahirinus (42·8) A. russatus (51·4) Species richness
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v(a). Rodent fauna of sandy habitats (i) was characterized by dominance of G. gerbillus with M. crassus being subdominant. The eastern gravel plains (ii) were inhabited mainly by G. henleyi and J. jaculus. In rocky habitats (iii) three species (G. dasyurus, S. calurus and A. cahirinus) had almost equal densities and A. russatus was less abundant. Wadis of the northern rim among the loess hills (iv) were characterized by high densities of G. dasyurus and P. obesus and low densities of M. crassus and E. melanurus. Other species were recorded only occasionally. The internal cirque wadis (v) had G. dasyurus as a dominant species. Subdominant species varied greatly: G. henleyi was subdominant in the wide eastern riverbeds v(a), J. jaculus in narrow western wadis v(b) and M. crassus in narrow eastern wadis v(c). Species diversity was the highest in rocky habitats (iii) and the lowest in narrow eastern wadis v(c) and intermediate and similar in all other habitat types (Table 1). Rodent biomass was the lowest in hammadas (ii) and the highest on the northern rim of the cirque (iv). Spatial relationships of rodent species Habitat distribution of individual rodent species is presented in Fig. 2. J. jaculus, M. crassus and G. henleyi occurred in flat sites with clay, gravel or sand surfaces. The first two species were recorded across the whole study area, whereas G. henleyi was confined to the eastern parts of the cirque. J. jaculus and G. henleyi preferred open places, while M. crassus occurred in more vegetated patches (wadis and sand dunes). G. gerbillus, G. nanus and M. musculus (not presented in Fig. 2) were recorded only in the easternmost plots, the first species in sand dunes and the other two in large sandy
Jj Em Gd Gg Gn Gh Sc Mc Po Ac Ar
v(b)
iv
iii
v(a)
v(c)
ii
i
Figure 2. Scheme of rodent species distribution through habitats in the Ramon cirque. Habitat types (i–v(c)), see text. Horizontal line breadth corresponds to relative density of the species. (Jj = J. jaculus; Em = E. melanurus; Gd = G. dasyurus; Gg = G. gerbillus; Gn = G. nanus; Gh = G. henleyi; Sc = S. calurus; Mc = M. crassus; Po = P. obesus; Ac = A. cahirinus; Ar = A. russatus).
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wadis. Two Acomys species and S. calurus inhabited rocky areas; A. russatus and S. calurus were restricted to these areas whereas A. cahirinus was also recorded in wadis near rocky outcrops. P. obesus and E. melanurus were found mainly in densely vegetated wadis among the loess hills in western most parts of the cirque and on its northern rim. G. dasyurus occurred in all habitats. Results of indirect species ordination showed that species were spatially segregated mainly along the first three ordination axes. These axes together explained 70·3% of observed variability (the first axis explained 27·3%, the second axis 23·3% and the third one 19·7%). Each subsequent axis explained less then 10% of variability. The possible interpretation of the axes in the indirect ordination is circumstantial and will be presented below. Distribution of rodent species in the space of ordination axes is presented in Fig. 3. Distribution was uneven. G. gerbillus was separated from other species along the first axis. S. calurus, A. cahirinus and A. russatus were distanced from a relatively compact group of other rodents along the second axis (Fig. 3(a)). G. henleyi, G. nanus and J. jaculus formed a distinct cluster along the third axis (Fig. 3(b)).
4
3
Axis 2
(a)
Sc Ar Ac
2 Gg
1 Gd
0
Mc Jj Gn Gh
Em Po
–1 –2 –1.5 –1 –0.5 0
0.5
1 1.5 Axis 1
2
2.5
3
3.5
4
2 Gh 1.5
(b)
Jj Gn
Axis 3
1 0.5 Ar 0
–0.5 –1
Ac Sc
Mg Gd
Em Po
–1.5 –2 –1.5 –1 –0.5 0
Gg 0.5
1 1.5 Axis 1
2
2.5
3
3.5
4
Figure 3. Positions of rodent species in ordination space. ((a) = axes 1 and 2; (b) = axes 1 and 3). Abbreviations of species names as in Fig. 2.
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Discussion Habitat preferences of rodents We distinguished groups of species with different environmental preferences. The first group consists of petrophylous forms — two Acomys species and S. calurus. These species inhabit exclusively rocky areas throughout their geographical ranges (A. cahirinus also occasionally occurs in other types of habitats) (Osborn & Helmy, 1980; Harrison & Bates, 1991). The psammophylous rodents are represented only by G. gerbillus. Depauperation of psammophylous fauna of the Ramon cirque is determined by the isolation and young age of sand areas. Sand dunes in the Ramon cirque have an aeolian origin and are not connected with other sand masses of the Negev desert (Placht, pers. comm.). In the Ramon cirque G. gerbillus occupies all types of sand substrates, from densely vegetated sandy plains to drifted dunes. When this species coexists with other psammophylous rodents (G. pyramidum and G. andersoni) it is restricted to sparsely vegetated crests of dunes (Abramsky et al., 1985a). The third group consists of P. obesus and E. melanurus, species occupying densely vegetated dry riverbeds and slopes. These rodents occur in areas with loess soils on the west of the cirque and on its northern rim; they are not found on other soil types. The fourth group contains three species, namely J. jaculus, G. henleyi and G. nanus, that inhabit scarcely vegetated patches with a low density of annuals. G. nanus is included in this group but its extremely low abundance suggests that its position may change with additional data collection. Previous studies report that these three species are considered psammophylous (Abramsky, 1984; Abramsky et al., 1985b). However, in our case they are recorded on a variety of soils. The last group consists of two species, M. crassus and G. dasyurus, and is characterized by a broad distribution and presence in almost all types of habitats (excluding M. crassus in rocky sites). Thus, these species may be considered generalists, as has been reported earlier (e.g. Osborn & Helmy, 1980; Harrison & Bates, 1991).
General patterns of rodent spatial segregation Ordination diagrams reflect a general pattern of spatial relationships among species. Differences in species’ positions in ordination space may indicate their different responses to environmental gradients (Jongman et al., 1987). With the absence of quantitative environmental data, we can only interpret ordination axes on the basis of the relative positions of the species in ordination space together with observations on their habitat distribution (Table 1, Fig. 2). The first ordination axis may be interpreted as a gradient of soil hardness from rock to sand marked from the negative extreme by Acomys spp. and S. calurus and from the positive extreme by G. gerbillus. The second axis is a gradient of relief from cliffs to flat plains determined by P. obesus, E.melanurus, J.jaculus, M.crassus and Gerbillus spp. (negative values) and by Acomys spp. and S. calurus (positive values). The third axis presents a gradient of vegetation density determined by annuals from northern wadis (P. obesus) to hammadas (G. henleyi).
Habitat structure and species structure Habitat classification based on rodent distribution differs in some details from initial a priori classification. Classification of habitats within an area may be performed in two
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ways: by physiognomic appearance or by responses of organisms of interest to main environmental gradients. The first classification is relatively subjective and the second is relatively objective. These classifications coincide when the differences of landscape units are expressed clearly (rocks, sands, hammadas). In other cases the second classification may be more detailed and show distinct elements within presumably uniform categories (wadis). Thus, habitat structure of an area is determined both by landscape structure and species responses. The resulting classification reveals habitats that are comparable in principal parameters of the rodent community — species richness, species diversity and biomass. The only exclusion is a relatively high rodent biomass in dry riverbeds of the northern rim of the cirque which is probably due to a higher level of primary productivity resulting from higher amounts of precipitation and the presence of the largest species (P. obesus) in high density there. Observed species richness and diversity are similar with those for other deserts of the Northern hemisphere (Kyzylkum, Gobi, Thar, Chihuahua) (Rogovin et al., 1991, 1994; Shenbrot, 1992). Rodent biomass within the Ramon cirque is on the same level as found in the extra-arid Southern Gobi. Biomass on the northern rim of the cirque is similar with that of temperate deserts (Kyzylkum, Northern Gobi, Chihuahua) (Shenbrot et al., 1994). We thank Prof. A.A. Degen (Ben-Gurion University of the Negev) and Dr M. Rowen (Ramon Science Center) for their helpful comments on the manuscript. This is publication No. 30 of the Ramon Science Center and No. 65 of the Desert Animal Adaptations and Husbandry.
References Abramsky, Z. (1984). Community ecology of small mammals in Israel. Acta Zoologica Fennica, 172: 41–44. Abramsky, Z., Rosenzweig, M.L. & Brand, S. (1985a). Habitat selection of Israel desert rodents: comparison of a traditional and a new method of analysis. Oikos, 45: 79–88. Abramsky, Z., Brand, S. & Rosenzweig, M. (1985b). Geographical ecology of gerbilline rodents in sand dune habitats of Israel. Journal of Biogeography, 12: 363–372. Gauch, H., Jr. (1982). Multivariate Analysis in Community Ecology. Cambridge: Cambridge University Press. 298 pp. Harrison, D.L. & Bates, P. (1991). The Mammals of Arabia (2nd Edn). Sevenoaks: Harrison Zoological Museum Publications. 354 pp. Hill, M. (1973). Diversity and evenness: an unifying notation and its consequences. Ecology, 54: 427–432. Jongman, R.H.G., ter Braak, C.J.F. & van Tongeren, O.F.R. (Eds) (1987). Data Analysis in Community and Landscape Ecology. Wageningen: Pudoc. 301 pp. Matson, J. (1976). The distribution of rodents in Owens Lake region, Inyo County, California. Contributions in Science. Natural History Museum of Los Angeles County, No 276: 1–27. Morrison, M.L., Marcot, B.G. & Mannan, R.W. (1992). Wildlife–habitat Relationships. Concepts and Applications. Madison: The University of Wisconsin Press. 364 pp. Osborn, D.J. & Helmy, I. (1980). The contemporary land mammals of Egypt (including Sinai). Fieldiana: Zoology, No 5: 579 pp. Rosenzweig, M. (1993). Species diversity and habitat diversity: which is the chicken and which is the egg? Sixth International Theriological Congress. Abstracts. p. 267. Sydney: University of New South Wales. 336 pp. Rogovin, K.A., Surov, A.V. & Serrano, V. (1985). Niche convergence in the desert rodents of two geographically isolated communities. Acta Zoologica Mexicana Nueva Seria, 10: 1–36. Rogovin, K.A., Shenbrot, G.I. & Surov, A.V. (1991). Analysis of spatial organization of a desert rodent community in Bolson de Mapimi, Mexico. Journal of Mammalogy, 72: 347–359. Rogovin, K.A., Shenbrot, G.I., Surov, A.V. & Idris, M. (1994). Spatial organization of a rodent community in the Western Rajasthan desert (India). Mammalia, 58: 18–33. Shenbrot, G.I. (1992). Spatial structure and niche patterns of a rodent community in the south Bukhara desert (Middle Asia). Ecography, 15: 347–357.
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Shenbrot, G.I., Rogovin, K.A. & Heske, E.J. (1994). Comparison of niche-packing and community organization in desert rodents in Asia and North America. Australian Journal of Zoology, 42: 479–499.
Spatial patterns of rodent communities in the Ramon erosion cirque, Negev Highlands, Israel
B. Krasnov*, G. Shenbrot*, I. Khokhlova† & E. Ivanitskaya‡ *Ramon Science Center, Ben-Gurion University of the Negev, Mizpe Ramon 80600, Israel †Desert Animal Adaptations and Husbandry, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel †Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel (Received 13 July 1994, accepted 13 October 1994) Habitat distribution of 12 rodent species in the Negev Highlands, Israel was studied. Five main habitat types were distinguished, based on similarity in rodent species composition of sample plots: (i) sand dunes, (ii) flat gravel plains (hammadas), (iii) limestone cliffs, (iv) wadis among loess hills and (v) wadis among gravel plains. Species richness was highest in (v) and lowest in (iii). Species diversity was highest in (iii) and lowest in (v) and intermediate and similar in all other habitat types. Rodent biomass was the lowest in (ii) and highest in (iv). Indirect rodent ordination showed that species were spatially segregated along the first three ordination axes. These axes may be interpreted as (a) a gradient of soil hardness from rock to sand, (b) a gradient of relief from cliffs to flat plains and (c) a gradient of vegetation density. We classified rodents into five groups by their habitat preferences: petrophyles (Acomys spp. and Sekeetamys calurus), psammophyles (Gerbillus gerbillus), inhabitants of densely vegetated wadis (Psammomys obesus and Eliomys melanurus), inhabitants of open gravel plains (Jaculus jaculus, Gerbillus henleyi and G. nanus), and habitat generalists (Meriones crassus and Gerbillus dasyurus). ©1996 Academic Press Limited Keywords: rodents; habitats; desert; community structure
Introduction In modern ecology the term ‘habitat’ is used in a variety of ways. Most often this term is used to describe an area of a particular relief, vegetation and soil structure. It is commonly thought that the structure of an animal community is determined by the habitat structure of an area. Another concept is to consider habitat as related to a particular species or group of species. In the framework of this concept, habitat is a patch with a set of environmental 0140–1963/96/030319 + 09 $18.00/0
© 1996 Academic Press Limited
320
B. KRASNOV ET AL.
conditions and resources promoting the occupancy, survival and reproduction by individuals of a given species (Morrison et al., 1992). Hence, habitat structure of an area is not predefined, but is a complex of co-evolved responses of organisms to abiotic and biotic factors (Rosenzweig, 1993). In our opinion, this concept is more objective because it reflects the integrated results of interactions of organisms and their environments. Examples of such an approach to habitat classification using clusteranalysis based on rodent species composition were presented for Mojave Desert (Matson, 1976) and the Central Chihuahua (Mexico) (Rogovin et al., 1985). The object of our study was to investigate the spatial structure of desert rodent communities in the Ramon erosion cirque. We distinguished, a priori, several habitat types (rocks, sand dunes, hammadas and dry riverbeds) by their physiognomic appearance. We then attempted to identify habitat structure of the studied area based on the relative abundance of rodent species. Results of the study would be a posteriori scheme of habitat types from a ‘rodent’s point of view’.
Material and methods Study area The Ramon erosion cirque (30°35'N, 35°45'E, about 200 km2 total area) forms the southern boundary of the Negev Highlands. The northern and southern rims of the cirque are 800 m and 510 m a.s.l., respectively, and the lowest point of the cirque bottom is 420 m.a.s.l. Summer is hot and winter is relatively cold (mean monthly maximum and minimum air temperatures are 33·9°C and 19·7°C in August and 14·9°C and 6·4°C in January, respectively). There is a very sharp decrease in annual rainfall from 85 mm on the cirque’s north rim to 56 mm at its bottom (data from Nature Reserves Authority of Israel). This precipitation gradient is also expressed from the west to the east of the Ramon cirque. The landscape of the Ramon cirque ranges from sand dunes to limestone and sandstone rocks in the rims.
Data collection Rodents were trapped in 1992–1993 on 31 one hectare plots that were chosen to represent main substrate and vegetation gradients. Seven of these plots were sampled regularly once every 2 to 3 months to estimate seasonal patterns of community organization. The other 24 plots were sampled twice a year. Each plot was sampled over 3 to 5 days using 50 Sherman live-traps placed in a grid at 5 3 5 stations with two traps per station and an interval of 20 m between stations. Each trapped animal was sexed, weighed, marked by toe-clipping and released. Jerboas were caught with a net at night using a searchlight. Fat sand rats were counted in the morning using binoculars. In total, 844 individuals of 12 species were captured. Data on Mus musculus were excluded from the analysis because of extremely low numbers. In accordance with our observations, M. musculus is characterized in this area by very unstable numbers. Just before the beginning of regular sampling, during preliminary trapping, this species was locally common (up to six individuals per ha). However, at the main sampling period it had almost completely disappeared.
Statistical data processing Plots were classified based on similarity of rodent species composition using cluster-
PATTERNS OF RODENT COMMUNITIES
321
analysis (cosine similarity measure, UPGMA algorithm). An indirect ordination procedure was performed by correspondence analysis to reveal placement of species’ positions along main environmental gradients. Correspondence analysis is an ordination technique in which the species’ scores on ordination axes are obtained from the sample scores (Gauch, 1982). We used Hill’s N2 index (reciprocal Simpson’s) as a measure for species diversity, N2 = 1∑pi2, where pi is the proportion of individuals belonging to species i in a collection (Hill, 1973). Results Rodent species and habitat types In total we recorded 21 individuals of Jaculus jaculus (L., 1758), four Eliomys melanurus (Wagner, 1840), 142 Gerbillus henleyi (de Winton, 1903), four G. nanus (Blanford, 1875), 395 G. dasyurus (Wagner, 1842), 20 G. gerbillus (Olivier, 1801), 22 Sekeetamys calurus (Thomas, 1892), 130 Meriones crassus (Sundevall, 1842), 50 Psammomys obesus (Cretzschmar, 1828), two Mus musculus (L., 1758), 34 Acomys cahirinus (Desmarest, 1819), and 20 A. russatus (Wagner, 1840). Results of cluster-analysis of rodent species composition and relative abundances indicate that from our sample plots several groups were distinguishable (Fig. 1). The number of distinguished groups depends on the selected critical level of similarity
Rescaled similarity (% %) Habitat type
(c) v (b) (a)
iv
iii
ii
i
100
Plot number 19 25 7 15 8 11 10 22 9 26 29 28 5 17 24 18 12 23 30 20 21 31 13 14 6 16 2 27 1 4 3
80
60
40
20
0
Figure 1. Dendrogram showing results of cluster-analysis of sample plots based on their similarity in rodent species composition.
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among them. We chose the 60% level of similarity as a critical because at this level the grouping of sample plots revealed the habitat types in the clearest way. Four of the five obtained groups may be related directly to distinct habitat types as follows: (i) sand dunes of the easternmost edge of the cirque with cover of Calligonum comosum or Echiochilon fruticosum (perennial vegetation cover 7·4%); (ii) flat gravel plains (hammadas) of the eastern part of the cirque with sparse vegetation of Hammada salicornica, Anabasis articulata and Gymnocarpos decandrum (cover 5·7%); (iii) limestone cliffs of the southern rim of the cirque with sparse cover (4·0%) of Zygophyllum dumosum, Helianthemum kahiricum and Reaumuria hirtella; and (iv) densely vegetated (cover 18·5%) wadis among loess hills on the northern rim of the cirque with Anabasis articulata, Atriplex halimus and Artemisia herba-alba. The fifth group is a complex conglomerate, which may be interpreted as dry riverbeds (or wadis), which varied in vegetation density. It includes: (v(a)) wide dry wadis of the eastern and central parts of the cirque with dense cover (30·9%) of Retama raetam, Moricandia nitens, Tamarix nilotica and Artemisia monosperma; (v(b)) narrow shallow wadis and loess hills of the western parts of the cirque with cover of Salsola schweinfurthii, Anabasis articulata and Atriplex leucocardia (perennial vegetation cover 6·0%); and (v(c)) narrow shallow wadis of the eastern and central cirque parts with 21·1% cover of Retama raetam, Moricandia nitens and Gymnocarpos decandrum. Parameters of rodent communities occurring in different habitat types are presented in Table 1. Similar numbers of species (5–6) occurred in most habitat types. Minimal species richness (4) was recorded for cliffs (iii) and maximal (7) for wide eastern wadis Table 1. Average rodent density (individuals per ha), species richness, diversity (reciprocal Simpson’s measure) and biomass (g per ha) in main habitat types of the Ramon cirque. Habitat types are: (i) sand dunes; (ii) flat gravel plains (hammadas); (iii) limestone cliffs; (iv) densely vegetated wadis among loess hills; (v(a)) wide wadis among gravel plains; (v(b)) scarcely vegetated wadis among loess hills; (v(c)) narrow wadis among gravel plains. Average adult body mass (g) for each species is represented in parentheses after the species name
Habitat types Species
i
ii
iii
iv
v(a)
v(b)
v(c)
0·33 0·00 0·17 0·00 0·33 3·33 0·00 1·50 0·00 0·00 0·00 0·00
0·77 0·00 0·38 0·01 1·62 0·00 0·00 0·40 0·00 0·00 0·01 0·00
0·00 0·00 1·32 0·00 0·00 0·00 1·07 0·00 0·00 0·00 0·88 0·21
0·13 0·75 6·88 0·00 0·00 0·00 0·00 1·00 7·25 0·00 0·13 0·00
0·01 0·00 2·42 0·03 1·47 0·00 0·00 0·98 0·00 0·14 0·01 0·00
0·83 0·00 2·33 0·00 0·00 0·00 0·00 0·33 0·17 0·00 0·17 0·00
0·08 0·00 5·54 0·00 0·29 0·00 0·00 0·94 0·00 0·00 0·02 0·00
5
6
4
6
7
5
5
Diversity
2·36
2·89
3·27
2·57
2·85
2·33
1·49
Biomass
20·55
103·9
126·2 1449·9 155·2
173·5
213·6
Jaculus jaculus (67·0) Eliomys melanurus (49·6) Gerbillus dasyurus (21·1) G. nanus (22·3) G. henleyi (9·8) G. gerbillus (20·1) Sekeetamys calurus (52·8) Meriones crassus (81·1) Psammomys obesus (166) Mus musculus (14·0) Acomys cahirinus (42·8) A. russatus (51·4) Species richness
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v(a). Rodent fauna of sandy habitats (i) was characterized by dominance of G. gerbillus with M. crassus being subdominant. The eastern gravel plains (ii) were inhabited mainly by G. henleyi and J. jaculus. In rocky habitats (iii) three species (G. dasyurus, S. calurus and A. cahirinus) had almost equal densities and A. russatus was less abundant. Wadis of the northern rim among the loess hills (iv) were characterized by high densities of G. dasyurus and P. obesus and low densities of M. crassus and E. melanurus. Other species were recorded only occasionally. The internal cirque wadis (v) had G. dasyurus as a dominant species. Subdominant species varied greatly: G. henleyi was subdominant in the wide eastern riverbeds v(a), J. jaculus in narrow western wadis v(b) and M. crassus in narrow eastern wadis v(c). Species diversity was the highest in rocky habitats (iii) and the lowest in narrow eastern wadis v(c) and intermediate and similar in all other habitat types (Table 1). Rodent biomass was the lowest in hammadas (ii) and the highest on the northern rim of the cirque (iv). Spatial relationships of rodent species Habitat distribution of individual rodent species is presented in Fig. 2. J. jaculus, M. crassus and G. henleyi occurred in flat sites with clay, gravel or sand surfaces. The first two species were recorded across the whole study area, whereas G. henleyi was confined to the eastern parts of the cirque. J. jaculus and G. henleyi preferred open places, while M. crassus occurred in more vegetated patches (wadis and sand dunes). G. gerbillus, G. nanus and M. musculus (not presented in Fig. 2) were recorded only in the easternmost plots, the first species in sand dunes and the other two in large sandy
Jj Em Gd Gg Gn Gh Sc Mc Po Ac Ar
v(b)
iv
iii
v(a)
v(c)
ii
i
Figure 2. Scheme of rodent species distribution through habitats in the Ramon cirque. Habitat types (i–v(c)), see text. Horizontal line breadth corresponds to relative density of the species. (Jj = J. jaculus; Em = E. melanurus; Gd = G. dasyurus; Gg = G. gerbillus; Gn = G. nanus; Gh = G. henleyi; Sc = S. calurus; Mc = M. crassus; Po = P. obesus; Ac = A. cahirinus; Ar = A. russatus).
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wadis. Two Acomys species and S. calurus inhabited rocky areas; A. russatus and S. calurus were restricted to these areas whereas A. cahirinus was also recorded in wadis near rocky outcrops. P. obesus and E. melanurus were found mainly in densely vegetated wadis among the loess hills in western most parts of the cirque and on its northern rim. G. dasyurus occurred in all habitats. Results of indirect species ordination showed that species were spatially segregated mainly along the first three ordination axes. These axes together explained 70·3% of observed variability (the first axis explained 27·3%, the second axis 23·3% and the third one 19·7%). Each subsequent axis explained less then 10% of variability. The possible interpretation of the axes in the indirect ordination is circumstantial and will be presented below. Distribution of rodent species in the space of ordination axes is presented in Fig. 3. Distribution was uneven. G. gerbillus was separated from other species along the first axis. S. calurus, A. cahirinus and A. russatus were distanced from a relatively compact group of other rodents along the second axis (Fig. 3(a)). G. henleyi, G. nanus and J. jaculus formed a distinct cluster along the third axis (Fig. 3(b)).
4
3
Axis 2
(a)
Sc Ar Ac
2 Gg
1 Gd
0
Mc Jj Gn Gh
Em Po
–1 –2 –1.5 –1 –0.5 0
0.5
1 1.5 Axis 1
2
2.5
3
3.5
4
2 Gh 1.5
(b)
Jj Gn
Axis 3
1 0.5 Ar 0
–0.5 –1
Ac Sc
Mg Gd
Em Po
–1.5 –2 –1.5 –1 –0.5 0
Gg 0.5
1 1.5 Axis 1
2
2.5
3
3.5
4
Figure 3. Positions of rodent species in ordination space. ((a) = axes 1 and 2; (b) = axes 1 and 3). Abbreviations of species names as in Fig. 2.
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Discussion Habitat preferences of rodents We distinguished groups of species with different environmental preferences. The first group consists of petrophylous forms — two Acomys species and S. calurus. These species inhabit exclusively rocky areas throughout their geographical ranges (A. cahirinus also occasionally occurs in other types of habitats) (Osborn & Helmy, 1980; Harrison & Bates, 1991). The psammophylous rodents are represented only by G. gerbillus. Depauperation of psammophylous fauna of the Ramon cirque is determined by the isolation and young age of sand areas. Sand dunes in the Ramon cirque have an aeolian origin and are not connected with other sand masses of the Negev desert (Placht, pers. comm.). In the Ramon cirque G. gerbillus occupies all types of sand substrates, from densely vegetated sandy plains to drifted dunes. When this species coexists with other psammophylous rodents (G. pyramidum and G. andersoni) it is restricted to sparsely vegetated crests of dunes (Abramsky et al., 1985a). The third group consists of P. obesus and E. melanurus, species occupying densely vegetated dry riverbeds and slopes. These rodents occur in areas with loess soils on the west of the cirque and on its northern rim; they are not found on other soil types. The fourth group contains three species, namely J. jaculus, G. henleyi and G. nanus, that inhabit scarcely vegetated patches with a low density of annuals. G. nanus is included in this group but its extremely low abundance suggests that its position may change with additional data collection. Previous studies report that these three species are considered psammophylous (Abramsky, 1984; Abramsky et al., 1985b). However, in our case they are recorded on a variety of soils. The last group consists of two species, M. crassus and G. dasyurus, and is characterized by a broad distribution and presence in almost all types of habitats (excluding M. crassus in rocky sites). Thus, these species may be considered generalists, as has been reported earlier (e.g. Osborn & Helmy, 1980; Harrison & Bates, 1991).
General patterns of rodent spatial segregation Ordination diagrams reflect a general pattern of spatial relationships among species. Differences in species’ positions in ordination space may indicate their different responses to environmental gradients (Jongman et al., 1987). With the absence of quantitative environmental data, we can only interpret ordination axes on the basis of the relative positions of the species in ordination space together with observations on their habitat distribution (Table 1, Fig. 2). The first ordination axis may be interpreted as a gradient of soil hardness from rock to sand marked from the negative extreme by Acomys spp. and S. calurus and from the positive extreme by G. gerbillus. The second axis is a gradient of relief from cliffs to flat plains determined by P. obesus, E.melanurus, J.jaculus, M.crassus and Gerbillus spp. (negative values) and by Acomys spp. and S. calurus (positive values). The third axis presents a gradient of vegetation density determined by annuals from northern wadis (P. obesus) to hammadas (G. henleyi).
Habitat structure and species structure Habitat classification based on rodent distribution differs in some details from initial a priori classification. Classification of habitats within an area may be performed in two
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ways: by physiognomic appearance or by responses of organisms of interest to main environmental gradients. The first classification is relatively subjective and the second is relatively objective. These classifications coincide when the differences of landscape units are expressed clearly (rocks, sands, hammadas). In other cases the second classification may be more detailed and show distinct elements within presumably uniform categories (wadis). Thus, habitat structure of an area is determined both by landscape structure and species responses. The resulting classification reveals habitats that are comparable in principal parameters of the rodent community — species richness, species diversity and biomass. The only exclusion is a relatively high rodent biomass in dry riverbeds of the northern rim of the cirque which is probably due to a higher level of primary productivity resulting from higher amounts of precipitation and the presence of the largest species (P. obesus) in high density there. Observed species richness and diversity are similar with those for other deserts of the Northern hemisphere (Kyzylkum, Gobi, Thar, Chihuahua) (Rogovin et al., 1991, 1994; Shenbrot, 1992). Rodent biomass within the Ramon cirque is on the same level as found in the extra-arid Southern Gobi. Biomass on the northern rim of the cirque is similar with that of temperate deserts (Kyzylkum, Northern Gobi, Chihuahua) (Shenbrot et al., 1994). We thank Prof. A.A. Degen (Ben-Gurion University of the Negev) and Dr M. Rowen (Ramon Science Center) for their helpful comments on the manuscript. This is publication No. 30 of the Ramon Science Center and No. 65 of the Desert Animal Adaptations and Husbandry.
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