ECOMORPHOLOGICAL RELATIONSHIPS IN SIX LIZARD SPECIES OF
RESTINGA DA BARRA DE MARICÁ, RIO DE JANEIRO, BRAZIL

RELACIONES ECOMORFOLÓGICAS EN SEIS ESPECIES DE LAGARTOS DE LA
RESTINGA DE LA BARRA DE MARICÁ, RÍO DE JANEIRO, BRASIL

Pedro Teixeira-Filho^*,**; Oscar Rocha-Barbosa^*; Viviane Paes^*; Sueli Carvalho Ribas^*; & Josimar R. de Almeida^***

SUMMARY: We studied some ecomorphological relationships in six lizard species (Ameiva ameiva, Cnemidophorus littoralis, Tropidurus torquatus, Liolaemus lutzae, Mabuya agilis and M. macrorhyncha) from Restinga de Barra de Maricá, RJ. These species have marked differences in microhabitat utilization and in foraging behavior, which vary from active to «sit-and-wait». In this study, we compared the morphology of the fingers and claws of these lizards species with the different behaviors. The species that showed higher degree of arboreality (T. torquatus and M. macrorhyncha) had the 4^th finger of the forelimb as the largest, while the other species had the 3^rd. This seems to give some advantage for vertical sustains of the arboreal species. All species had the 4^th finger as the largest of the hind limb. The two scincids (M. agilis and M. macrorhyncha) had more curved and shorter claws, which appears to aid in the climbing on the leaves of the bromeliad Neoregelia cruenta. In addition, the claws of the essentially ground-dwelling species were larger than in the other species, suggesting that larger claws give some advantage for support on sand (providing a better impulse and speed), in the excavation of burrows, in the defense against predators, in the dispute for foraging ranges and in mate selection. In this study, the foraging strategy does not seem to be related to the absolute size of the fingers of the lizards, but with relative differences in the fingers of the forelimbs.

KEY WORDS: 1. Ecomorphology; 2. Lizard; 3. Claw; 4. Microhabitat utilization.

INTRODUCTION

Williams (1972) proposed that ecology, behavior and ecology of species coevolve, in what we known the ecomorphological hypothesis. In lizards, while some studies have proven the relationship between ecology and morphology (e.g., Moermond, 1979; Williams, 1983; Pounds; 1988; Vitt, 1991 and Colli et al., 1992), others have proven the absence of that relationship. (Jaksic et al., 1980). However, when analyze the different foraging strategies of lizards and compare them with morphological aspects, this relationship is generally present (Vitt & Congdon, 1978; Huey & Pianka, 1981 and Colli et al., 1997).

The traditional division of foraging strategies defines two groups of foragers, the active and the sedentary or «sit-and-wait « foragers (Vitt & Congdon and Huey & Pianka). More recently, lizards in an intermediary category, adopting both strategies, were defined as cruising foragers (Pough et al., 1999). There are morphological, physiological and reproductive differences between these groups, as well as different prey. The active foragers have, generally, body and tail more elongated, larger and more muscular legs, greater aerobic capacity, higher body temperatures, disruptive coloration, lower clutch mass and greater sedentary prey consumption then the sit-and-wait foragers (Vitt & Congdon; Huey & Pianka; Magnusson et al., 1985; Huey & Bennett, 1986; Rocha, 1994; Colli et al. and Pough et al.).

The relationships among the habitat use and the morphology of lizards are known from many years ago. Lundelius (1957), studying two species of the genus Sceloporus established that the ground-dwelling species tend to have longer hind limbs than the arboreal ones. The same relationship was described in lizards of the genus Anolis (Collette, 1961). In the other hand, arboreal species have more elongated fingers in the forelimb than the ground-dwelling species (Colli et al., 1992 and Vrcibradic & Rocha, 1996). This fact seems to be related to an increase in frictional grip for the arboreal species (Cartmill, 1974).

Climbing ability is related with a physical problem: the point of gravity. If this point is higher, the stability will be more difficult. As the point of gravity decreases, more stable will be the animal. So, lizards that have vertical use of the habitat (arboreal species or those which climb on rocks) tend to have short and heavy distal limb segments, while runner species have long and light ones, to reduce the internal inertia (Losos et al., 1993 and Van Damme et al., 1997).

In this study, we try to verify the existence of morphological differences in the members of the lizards Ameiva ameiva, Cnemidophorus littoralis (Teiidae), Liolaemus lutzae, Tropidurus torquatus (Tropiduridae), Mabuya agilis e M. macrorhyncha (Scincidae) of Restinga da Barra de Maricá, RJ. These species already had some ecological aspects studied in this area (e.g. Fialho, 1990; Ribas et al., 1995; 1998a, b; Rocha, 1988, 1991, 1993; Teixeira-Filho, 1995; Teixeira-Filho et al., 1995, 1996; Vrcibradic & Rocha and Zaluar, 1993), but there is little information about ecomorphology of these lizards. We try to relate the morphological differences to the foraging patterns and to the microhabitat use by the species, in other words, to define ecomorphological patterns among the species.

MATERIAL AND METHOD

The chosen species are two active foragers (A. ameiva and C. littoralis), two sit-and-wait foragers (L. lutzae and T. torquatus) and two cruising foragers (M. agilis and M. macrorhyncha). We used only adult animals (18 A. ameiva; 27 C. littoralis; 18 L. lutzae; 24 T. torquatus; 14 M. agilis and 13 M. macrorhyncha), males and females, collected in Restinga da Barra de Maricá. The specimens belong to the collections of Zoology and Ecology sectors of Departamento de Biologia Animal e Vegetal of Universidade do Estado do Rio de Janeiro. This restinga (sand plain) is located approximately 38 Km east of the city of Rio de Janeiro, Brazil (22 ^o 57' S, 43^o 50' W). It is a coastal area comprising a sand ridge covered by vegetation that varies from herbaceous (in the beach area) to shrubby (in the primary and secondary dunes) (Henriques et al., 1984; Silva & Somner, 1984).

We measured the snout-vent length (SVL), the length of the bigger finger of the forelimb (LBFF) and the length of the largest finger of the hindlimb (LBFH), using a vernier caliper with precision of 0.05 mm. To very small animals, LBFF and LBFH were measured under stereoscopic microscope. In addition, the structure of the claws of each species was also analyzed. We compared their relative lengths and curvatures to the size of the fingers. The size of the claw in relation to the finger size was calculated to establish the mean size of the claw for each species and to compare these measures to the microhabitat use and to the foraging mode of each lizard.

In the species which shows a very little difference in the size of the fingers, we used an one-way analysis of variance (one-way Anova - Zar, 1999) to verify if those differences were significant.

RESULTS AND DISCUSSION

The data showed that in A. ameiva, C. littoralis, L. lutzae and M. agilis the largest finger of the forelimb is the 3^rd, while for T. torquatus and M. macrorhyncha the largest finger is the 4^th. This possibly represents some relationship with the larger degree of arboreality of these two species when compared with the others. Possibly, the larger length of the 4^th finger aids in the vertical support of the animal, increasing its frictional grip (as described to anoline lizards by Collette, 1961) when it encounters a branch (in the case of T. torquatus) or when it climbs the leaves of a bromeliad (in the case of M. macrorhyncha). In addition, Vitt et al. (1997), comparing two populations of T. hispidus, found an increased hind limb length for those which use more vertically the habitat.

A study with two other species of the gender Tropidurus, Colli et al. (1992) established that arboreal species have relatively longer fingers than ground-dwellers. Our results are in agreement with those obtained by Vrcibradic & Rocha, who, analyzing ecomorphological differences between M. agilis and M. macrorhyncha, found a larger relative size of the fingers in the latter.

This species in Barra de Maricá uses preferentially the bromeliad Neoregelia cruenta as microhabitat, while M. agilis uses more the leaf-litter around this bromeliad (Vrcibradic & Rocha).

Although the scincids had different larger fingers in the forelimb, in M. macrorhyncha the difference between the 3^rd and the 4^th finger was not significant (Anova, F = 0.119; p > 0.05). In M. agilis, this difference was significant (Anova, F = 4.081; p = 0.05). This result may be associated with the differences in the microhabitat utilization by these two species. In M. macrorhyncha, the elongation of the 4^th finger may give to the lizard a better sustain in the leaves of N. cruenta, as a result of an evolutionary adaptation for the vertical use of the habitat. However, further studies about the evolution of this group will be necessary to clear up this fact.

With relationship to the hind limbs, in all the studied species the 4^th finger was the largest. However, the two scincid presented a proportionally smaller LBFH as well as LBFF. This may represent an advantage for the escape from predators, as part of the secondary defensive mechanisms (Greene, 1988). For the scincids of Barra of Maricá, this consists of hiding at a lair in the base of a clump of the bromeliad N. cruenta, while the other species race across the sand, to the interior of vegetation thickets (A. ameiva, C. littoralis and T. torquatus), or into tidal debris that serves as refuge or for a lair in the sand (L. lutzae) (Teixeira-Filho, personal observation; Rocha, 1993). Our results are in agreement with other studies (Lundelius; Collette; Williams, 1983; Pounds and Vitt et al., 1997) which has shown that lizards that use open microhabitats tend to have longer hind limbs when compared with others that use less open microhabitats. Longer hind limbs may provide an advantage for running in open habitats. This is not the case for M. agilis and M. macrorhyncha. In addition, these species seems to follow the pattern proposed by Losos et al. (1993) and Van Damme et al. in which lizards that have some degree of vertical use of the habitat tend to have short and heavy distal limb segments, when compared with other essentially terrestrial species. When compared with M. agilis, M. macrorhyncha shows another morphological adaptation for the use of N. cruenta, which is a more flattened body (Vrcibradic & Rocha). This is also a form to put down the point of gravity of the animal (Van Damme et al.).

Zani (2000) demonstrated that the increase in claw curvature is related to the clinging performance on smooth substrates, such as leaves. The structure of the claws of the scincids seems also to favor their grasp on the leaves of N. cruenta, because they come shorter and more curved than the claws of the other species, as much in the forelimbs as in the hind limbs (Table I). This possibly allows the claws to work as hooks, also aiding in the climbing on leaves. Such a relationship seems also to occur in T. torquatus, which presented relative lengths of the claws closer to those of the scincids than those of the other tropidurid (L. lutzae) (Table I). This suggests a possible relationship between the size of the claws and the vertical use of the habitat, with the essentially ground-dwelling species possessing proportionally larger claws. For these, the largest relative length of the 4^th finger of the hind limb, associated with the longest claws, can represent a larger support on the sand, providing a better impulse and higher speed. As well, larger claws can aid in the excavation of burrows, to act in the defense against predators, in the dispute for foraging ranges and in mate selection.

Our results do not show a clear relationship between foraging mode used by the lizards and their finger morphology. However, the active foragers (A. ameiva and C. littoralis) have proportionally longer fingers and claws than the other species. If this is due to the foraging mode or to a feature of the Teiidae family, only further studies can prove.

* UERJ/Lab. Zoologia de Vertebrados (Tetrapoda);
** Colégio Pedro II
*** UERJ/ Ecologia (CNPq/FAPERJ)
CNPq, process n. 521378/97-4/FAPERJ/UERJ-PROCIÊNCIA.

RESUMEN: Estudiamos algunas relaciones ecomorfológicas en seis especies de lagartos (Ameiva ameiva, Cnemidophorus littoralis, Tropidurus torquatus, Liolaemus lutzae, Mabuya agilis y M. macrorhyncha) de la Restinga de la Barra de Maricá, RJ. Estas especies poseen marcadas diferencias en la utilización del microhabitat y en el comportamiento en la búsqueda de alimento, que varía de activo a «sienta-y-espera». Comparamos la morfología de los dedos y de las garras de especies de lagartos con estos comportamientos diferentes. Las especies que mostraron el grado más alto de arborealidad (T. torquatus e M. macrorhyncha) tenían el 4º dedo del miembro anterior como el más grande, y las otras especies tenían el 3º. Esto parece otorgarle una ventaja para la sustentación vertical de las especies arboreas. Todas las especies tenían el 4º dedo como el más grande del miembro posterior. Los dos scincídeos (M. agilis e M. macrorhyncha) tenían garras más cortas y curvas, que parecen ajudarle para la escalada de las hojas de la bromelia Neoregelia cruenta. Adicionalmente, las garras de las especies esencialmente terrícolas son mayores que las de otras especies, sugeriendo que garras mayores confieren un mejor apoyo en la arena (dándole mejor impulso y velocidad), en la excavación de escondrijos, en la defensa contra los predadores, en la disputa por sitios de alimentación y en la selección sexual. En el estudio, la estrategia de alimentarse no parece estar relacionada con el tamaño absoluto de los dedos de los lagartos, pero sí con las diferenciass relativas en los dedos de los miembros anteriores.

PALABRAS CLAVE: 1. Ecomorfología; 2. Lagarto; 3. Garra; 4. Utilización del microhabitats.

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ACKNOWLEDGEMENTS

We thank Priscilia M. Gasparelo for her help in the measurements. This research was partially supported by Brazilian agencies CNPq and FAPERJ and the Universidade do Estado do Rio de Janeiro, Brazil special program PROCIÊNCIA.

Dirección para correspondencia:
Prof. Dr. Oscar Rocha-Barbosa
Universidade do Estado do Rio de Janeiro
Instituto de Biologia Roberto Alcântara Gomes
Departamento de Biologia Animal e Vegetal
Laboratório de Zoologia de Vertebrados, PHLC, Sl. 513b.
Rua São Francisco Xavier, 524
20550-013 - Maracanã - Rio de Janeiro, RJ,
BRASIL

E-mail: obarbosa@uerj.br

Recibido : 01-02-2001
Aceptado : 05-03-2001