The structure of a mediterranean lizard community⁽¹⁾

Doñana, Acta Vertebrata, 2 (2): 145-160, 1975 !he strueture of a Mediterraaean U.ard eommunity Cl) J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO 145 The structure of lizard communities has recently been the object oí numerou$ studies in which characteristic properties of animal communities, such as sharing of resources, niche breadth and overlap, ' as well as strategies utilized by the different species to reduce competition, have be en analyzed. Most of these studies (Rand, 1964; Schoener, 1968; Schoener and Go rman , 1968; Hillman, 1969; Pianka, 196~a; Schoener, 1970; Huey et al., 1974:) havo been made on groups of sympatric oongeneric speci'es, whereas Pianka (1967; 1969b; 1971; 1973) and more recently Sage (1974) analyzed entire communitías of lizards. Here We analyze the structure of a lizard community representative of tha European Mediterranean zone, an area as yet unstudied except for a pr&- cursory investigation carried out by Val verde (967). We also compare this community to those described by Hurtubia and Di Castri (1973) and Saga (1973) for the Mediterranean zones of the New World. Material and Methods 610 specimens belonging 'to eight specíes of lizards were collected at irregular intervals thl'oughollt a period oi 35 months (Octobe1' 1971 to August 1974). These samples were captured principally by shootlng 01' by hand and preservcd in 70 per cent Alcohol, except iol' most Lace-rta. lepid4 whicb were donated by the Ownel'S of prívate esta tes where they are usually killed, being considered as harmtul to hunting; these samples were preserved in 10 per cent forma Un. Tlle buck of all material used he1'e has been donated to the Biological Station of Doñana, Sevilla, Spain. (1): This papel' was originally delivered in a Symposillm on the «Ecosystem structure and stability" in November 1974 at Sevilla, Spain. 146 J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO Time between capture and analysis varied greatly, from immediately afterwards till several months latero Samples collected provided the following morphological data (measured on the preserved animaD : SVL (snout vent length) : Measured from the end of the snout to the distal edge of the anal plateo ear . HL ( Head lenght ): From the end of the snout to the anterior border of the HW (Head widthl: Maximurn width of the head . W (Weight): Only in fresh specimens. Al! rneasurements are in millimeters, weights in grams . Only sto m ac h contents were considered in the study of food. Prey items were coun te d fOl" each stom a ch and clasified into 21 food c ateg o ri es listed in table II. The l eng th of intact prey was me asured to the ne ar est .1 of a millime te l·. Fi e ld ob ser va tíon s were m ade at irregular in ter vals, at least once a month (exc ept Septe mh er), a nd durl ng a minimum p erl od of five days ea ch m ont h, at di ff ere nt time s of day an d nigh t. W hen poss ibl e, the follo win g d ata were no ted in fie ld obs er vati o ns : species , apro x ímate size a nd age , time , locallty and cx act location as we ll as activity wh en first sighted. Sludy Ares Field observationsand material employed in this study come from an extensive area situated at the most western part of the Sierra Morena mountain range in the Province of Huelva (S. W. Spatn, aproximately 38° N by 7° W). This zone comprises lines of mountainous country of roeunded profile, at low altitude (average eleva tion of 500 meters above sea leveD, 'which alternates with wide valleys and peniplanes (for a detailed description of this zone, see Lautensach, 1967). The climate is of the type «Mesomedite-- rmnéen accentué» as described by Emberger et al. (1963) with 75 to 100 ' biologi'cally dry days. Annual precipation varies from about 800 to 1,300 mm. of rain which falls mainly from November to March . Temperatures below zero, are infrequent, and the total number of hours per year bel ow zero does not re a ch the three per cent indicated by Aschmann (1973) as a limit for Medite I' ranean climates. Frost ls scarce and snow exceptional on this land, as any snow fall usually melts immediately. WHh regard to vegetation, th is originally co nsisted in a dense evergreen sclerophylous forest of Quercus ilex and/or Q. suber with sorne isolated stems of Q. lusitanica in damper areas . This fQ.rest possessed a dense under . brush made up chiefly of Ulex spp. and several species of Cistus as well as Arbutus unedo. In the brooks and gorges galleries of Alnus glutinosa and Fraxinus sp. occur with thick bushes of Rubus and Nerium oleander. This vegetation has been radically transformed by the hand of man in wide ZQ_ Dañan :>., Acta Vertebrata, 2 (2), 1975 The $tructure 01 a Mediterranean lizard community 147 nes, and due to degeneration of the for.est, two main types of habitat have appeared: Chaparral.-This consists basically of Cístus ladanijerus, Erica australts and E. umbellata, togetber witb Genista sp., A. unedo and E. arborea appea-r ing in damp areas. This underbrush forms a very dense continuous blan· ket oí up to tour meters bigh in some places, and generally occupie·s high areas of mountain ranges. Evergreen oak wood.-A thin forest of Q. ilex and/or Q. suber in which tbe soíl has been completely cleared of underbrush. This habitat occupies the valleys and plains. Extensive park~ oí Castanea sativa oí similar struc· ture a-ppear in the cooler and damper areas. T o these must be added a very peculiar formation consisting oí out· crops of granitic rocks determining fue so·called «Plutonic buttonsll (see Lautensach, 1967). These a-re extremely rocky are as with some stems of ooks , and underbrush of Pistada sp ., Mirtus sp . and Cistus . ResuU. A maximum of eight lizard species can co·exist in the regian studied. These are (2): Tm Tarentola m. mauritaniea Be Blanus e. cinereus Lh Lacerta hispanica vaucheri Ll Lacerta l. lepida Pa Psammodromus a. algirus Ph Psammodromus h. hispanicus Cb Chalcides bedriagai pistaciae Ce Chalcides chalcides striatus Gekkonidae Amphisbenidae Lacertida.e )) )) )) )) )) )) Scincidae » » In the rest of this paper, the symbols preceding each lizard name listed aboye will be used. Table 1 shows the main biometric characteristics of the different species, and figure 1 presents the distribution of snout'vent lengths (SVL). Throo pairs of congeneric speci'es occur in sympatry; these differ from one ano ther wiothin each pair, in aH measurements taken into consideration. (2): Following Meterns and Wermuth, 1960, except for Chalcides bedriagai (see Valverde, 1966). Doñana, A. cta Vertebrata, 2 (2), 1975 148 J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO All these differences are statistica11y significant (P< .05; t-test) except between the two species of the genus Chalcides where none of the differences were staUstica11y significant. Table 1 Morphological statistcs used in tbis study SVL W HW HL m cr n m cr n m cr n m cr n Tm 54·04 14.1 21 6.6 4.4 15 9.66 2.4 18 15.0 3.6 18 Be 160.05 30.3 37 4.6 1·7 15 4.82 1.9 28 7.8 Vi 28 Lh 46.U3 4.7 131 2.0 1.0 45 5.87 1.0 56 10.3 1.8 .'l9 Ll 138.46 53.7 167 71.7 8.4 35 15.9 9.8 73 32.8 4.3 74 Pa 58.88 14.6 141 7.7 2.4 65 10.6 1.9 39 15.9 2.2 39 Ph 40.05 5.S 57 1.1 1.1 42 5.54 4.0 34 9.8 1.4 35 Cb 66.14 10.6 21 4.4 1.2 11 6.71 1.8 21 8·0 .9 21 Ce 95.08 31.0 22 4.9 3·8 21 5.90 1.2 22 8.5 1.7 19 SVL = Snout-vent length; HW = Head width; HL = Head length; W = Weight. Food A total of 511 stomachs were analyzed. Table 2 summarizes the main features of the diet of the eight lizard species integrated in the community. Most lizard species are ecclectic predators, feeding on a wide ~ange of invertebrate prey (see e.g. Pianka, 1973, and included references). In frequency of appearance of prey üems in stomachs analyzed and frequency oí each prey item in the total, the most abW1dant groups in the diet were beetIes, spiders and .insect 18irvae,amonga wide variety of g·roups of invertebrates. Seeds 8ind vertebrate prey are also included in the diet of several species. Table 3 shows the prey size distribution and the mean prey size for each lizard species. Lizard size i:; generally correlated with that of the prey ingested. In this case, mean prey size was col1related both with snout-vent length and he8id dimensions of the lizard of 8111 species. Of these comparísons, only mean prey size vs. mean head width was statistically significant (r: .720; P< .05; n: 8). Doiíana, Aeta Vertebrata, 2 (2), 1975 The structure 01 a MediteTTanean lizara communlt'll 1.9 • Be Ll Ce - Cb ~ Pa Tm Lh 40 Ph o 20 100 , v.o . 180 220 mm. 60 Fig. 1. Frequency distributions of snout-vent lengths (millimeters) lor the eight lizard species comp'lsing the community . Doñana, Acta Vertebrata, 2 (2), 1975 150 J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO Trophic diversity was calculated by Pielou's method (1966), using the BriUouin formula: H=(1/N) (logIa Ni! -I loglO Ni!) This method was formerly applied to the analysis of diet of predators by Hurtubia (1973). Plotting accumulated trophic di ' versity (Hk) vs. total number of stomachs (k), diversity curves are obtained (Figure 2). These curo ves are higher for larger species, in pairs of congeners. Duo to sample heterogeneity, including stomachs from very different periods, localities and habitats, it is difficult to determine the stabilization point (t) of the curves, and so the diversity for a11 the stomachs (Hz) of each Table 2 Percentage compm:ition, by numbers, of the diet of Uzard species composing the community The number oC stomachs and prey items on which these percelltages are based, as well as the average trophic diversity (Hz), are al so shown. Oligoehaeta Isopoda Gasteropoda Miliapoda Arane ae fhalangidae Seorpionidae Orthoptel'a Dermaptera 'BJatlaria Hemyptera Formicidae Other hymenoptera Lepidoptcra Diptera Coleoplera Lepidoptera Iarvae Other Iarvae Seeds Vertebrate items lTnidentified Preys items Stomaehs Trophic diversity (Hz) Tm 2.85 2. 85 20.0 1.42 10.0 7.14 1.42 8.57 1.42 10.0 17.13 8.57 4.28 2.85 70 18 .975 Be 4.9 .98 2.94 12.74 .98 Lh 3.24 .36 1.79 24.46 1.08 2·16 .72 1.08 2.16 Ll .47 1.12 .42 1.26 0.5 ·08 1.77 .28 .56 16.66 9.35 1.85 3.95 2,4 .03 7. 19 . 98 9.80 20.87 68.42 l7.64 9.71 5.0 28.40 6.47 9.36 2.94 103 23 .760 1.5 .36 .25 5.09 .90 268 2919 9S 158 1.059 1.087 Doñana, Acta Vertebrata, 2 (2), 1975 Pa Ph Cb l.19 9.4 22.5 .39 2.5 1. 38 2.3 5.0 7,14 24.8 20.0 .39 8.53 .19 .19 1.98 12.60 10.11 2. 97 38.07 8.92 3.76 1.1 .5 15.3 1.1 2.3 23.9 5.9 8.8 7.5 35.0 7.5 Ce 10.3 2·06 18.55 6.18 8.25 3.10 1.03 4.12 24.73 10.jO 7.21 3.10 .19 1.78 504 3.5 169 48 40 79 132 1.225 .852 15 22 .707 .960 The structure 01 a Mediterranean lizard community 151 species, is used as indicator of trophic diversity; values obtained appear in table II. A statistically significant cOI1relation exists between trophic diversity and head width of the lizard species (rs: .643; P<.05; n: 8. Spearman rank correlation coef.icient. Siegel, 1956). Finally, with respect to hunting strategy, Pianka 0966; see also 1973) Table 3 Trophic resource matrix. Rows represents prey size items at 5 mm. intervalo Total number of prey measured (N), and mean prey size (MPS) are also shown. Tm Be Lh Ll Pa Ph Cb Ce OS 9 15 64 10 39 60 11 16 610 23 47 51 660 63 54 15 28 1115 7 2 25 389 34 9 2 15 1620 3 4 7 255 33 2 4 2125 1 4 55 7 3 2630 ~ 5 1 66 11 3135 5 23 3640 1 10 4 4145 1 1 3 4650 4 5155 1 56 · 60 1 6165 3 6670 2 7175 1 7680 1 8185 8690 91· 95 1 96-100 2 N 46 76 158 1486 197 125 30 68 MPS 10.06 11.35 8.72 13.72 12.9 6.0 7.16 9.72 -defines two basic ones: «sit-and-wait» and «active foraging». In our case only one species (Tm) is a «sit-and-wait)), while the remainder seem to be <mctive foraging» hunters. .. ¡ Doñana, Aeta Vertebrata, 2 (2), 1975 152 J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO Activity The presence oí a well-defined wir.ter lateney has been attributed as a fundamental charaeteristie to the fauna of reptiles of the Temperate zone (Saint-Girons, 1956). Saint-Girons (1953) attributes two diapauses to the Me' diterranean zones, the one in winter and a summer latency, due to the ex· Hk 11 .9 7 , r , .5 ..- . I -' / .. .... '" ........ ', ..... Ce Cb Ll Pa Ph .3 .1 o 5 10 15 5 10 15 5 15 20 K Fig. 2. Accumulate trophic diversity (Hk) curves vs . total numbr of stomachs (k). Comparison between congeneric pairs oi species. eesive dryness. Data offered by ourselves in this respeet, although ineornpIete for sorne species, do however, perrnit us to draw attention to two types oí behaviour. Tablc 4 Spatial resource matrix. Symbols heading the table Indicates microhabUat typea drawn in detail in the texto A B e 2 3 1 2 3 Tm o 22 o o o o o Be o 20 o o 17 o Lh () 40 o o 6 o o Ll 27 24 o o 3 o o Pa o o o 141 3 o o Ph 32 o o o o o (j Cb o o o 1 o 21 o Co o o o o o o 22 Doñana, Acta Vertebrata, 2 (2), 1975 The structure 01 a Mediterranean lizard communitll 153 At least two species (Ll and Pa) show a marked diapause, with an inactive period of some four months (November to February), although the smaHer members of these species are active throughout the Whole year. In other species (Tm and Lh), both adults and young are active aH year. As far as dai1y activity is concemed, only one species (Tm) is nocturnal, while the remainder are essentially diurnal. However, this pattern oí activity is subject to appreciable changes throughout the year, with the nocturIl8l species becoming diurnal during winter months , whereas some diurna! species (Ll and Pa) have often been observed at night during hotter months (Mellado and Hiraldo, unpublished). Mierohabitat prelerenee AH place locations obseJ'ved for lizards when first sighted were classified into seven weH-differentiated categories to define the spatial reS<Jurce sha.- ring of the community. We consider only observations referring to feeding behaviour of thermoregulatory activities. These categories include: A Zones of scarce or no plant cover. B Zones of dense plant cover . Within each of the above-inentioned types the foHowing divisions are made: 1 On the ground. 2 On rocks, trees and buildings. 3 Under stones, tree trunks, etc. In adition to these categories, another one must be added . It is: e In small thick pastures in valleys and pJains. One of the species (Cc) is restricted to C; morphologically it is a snakelike lizard which Uterally «swimsll in the pastures it inhabits . The rest ol the species are limited to a special kind of substratum: three species (Ll, Pa and Ph) live on the ground surface, one of them (Pa) in places were there íS a thick underbrush, whereas the other two (Ll and Ph) are found on open ground (Ll needs traes and rocks for protection). Be is a typical subterranean species, morphologicallya worm-like lizard. Cb lives under stones in thls region. Finally, Lh and Tm live on rocks and tlree trunks. Doñana, Acta Vertebrata, 2 (2), 1975 160 J. MELLADO, F. AMORES, F. F. PARREÑO AND F. HIRALDO I.&VINS, R. (1968): Evolution in changing enviTonments. Princeton Univ. Press: 120 pp. MERTENS, R, and WERMUTII, H. (1960): Die Amphibien uoo Reptilien EUTOpa& Verlag Waldemar Kramer, Frankfurt a. M. PIANKA, E. R (1966): Convexity, desert lizaros and spatial heterogeneity. Ecolog¡¡ 47: 1.055-1.059. - - (1967): On lizard species diversity: North American flatland deserts. Eco· logy 48: 333-351. - - (1969a): Habitat specificity, speciation and species density in Australian desert lizards. Ecology 50: 498-502. ~ -(1969b): Sympatr y of desert lizards (Ctenotus) in Western Australia. Ecology 50: 1.012-1.020. - - (1971): Lizard spacies density in the Kalahari deserto Ecology 52: 1.024-1.029. - - (1973): The structure of lizard cornmunities. Ann. Rev. Ecol. Syst. 4: 53-74- - - (1974): Niche overlap and diffuse competition. Proc. Nat. Acad. Sci. USA 71: 2.141-2.145. PIELOU, E. C. (1966): The measurement 01 diversity in different types of biological collections. J. Theoret. Biol. 13: 131-144RAND, A. S. (1964): Elcological distribution in anoline lizards of Puerto Rico. Ecology 45: 745-752. SAGE, R D. (1973): Ecological convergence 01 the lizard faunas of the chaparral communities in Chile and California, p. 339-348. In: Mediterran!lan type ecosystem. F. Di Castri and H. A. Mooney eds., Springer-Verlag, BerlinHeildelberg-New York. - - (1974): The estructure of lizard 1aunar: comparative biologies of lizards in two Argentina deserts. Ph. D. thesis, Univ. of Texas at Austin. Diss. Abstr. 35,1. SAINT-GIRONS, H. (1953): Note sur les periodes de latence des reptiles au Maroc. Bull. Soco Zool. France 78: 377-381. - - (1954): Cycle d'activité et thermoregulation chez les reptiles <lezards et serpents). Vie et MiHeu 7: 133-226. SCHOENER, T. W. (1968): The Anolis lizard of Bimini: resource partitioning in a complex fauna. Ecology 49: 704-726. - - aud GORMAN, G. C. (1968): Sorne nicha differences among three species of Lesser Antilleau anoles. Ecology 49: 819-830. SCHOENER, T. W., and GoRMAN, G. C. (1970): Nonsynchronous spatial overlag ot lizards in patchy habitats. Ecology 51: 408-4118. - - and SCHOENER, A. (1971a): Structural habitats of West Indian Anolis lizards I. Lowland Jamaica. Breviora 368: 1-53. - - - - (1971b): Structural habitats of West Indian Anolis lizards n. Puerto Rican uplands. Ibid. 375: 1-39. - - (1974): Resource partitioning in ecological communities. Science 185: 2739. SIEGEL, S. (1956): Nonparametric statistics fOT the behavioral sciences. McGraw Hill Book Company, Inc., New York-Toronto-London. VALVERDE, J. A. (1966): Sobre las sub especies de Chalcides bedriagai (Basca). Bol. R. Soco Española Hist. Nat. (BioU, 64: 169-170. - - (1967): Estructura de una comunidad de vertebrados terrestres. C. S. r. C. Madrid. J. MELLADO, F. AMoRES, F. PARRKÑO and F. HIRALDO Centro Biológico del Sur Reina Mercedes, 17. Sevilla-12 ESPAÑA (SPAIN). :Doiíana, Acta Vertebrata, 2 (2), 1975