2001 Number 3
18 July 2001
THE ECOLOGICAL CONSEQUENCES OF HABITAT AND MICROHABITAT USE IN LIZARDS: A REVIEW
Geoffrey R. Smith1,
Royce E. Ballinger2
of Biology, Denison University, Granville, OH 43023, USA
School of Biological Sciences, University of Nebraska, Lincoln, NE 68588-0118,
Abstract. We review the ecological consequences of habitat and microhabitat use in lizards. Different habitats have different biotic and abiotic properties and thus are likely to have different consequences for the lizards that occur in them. Individual performance and life histories are influenced by habitat use, particularly when habitats differ in thermal characteristics that may influence physiological processes or constrain activity. We know relatively little about how the effects of habitat use on individual performance translate into population dynamics. We do know that the ability of lizards to use particular habitats can influence the persistence of populations in the face of habitat changes. Community-level processes (e.g., competition) and community structure (e.g., diversity) can be influenced by habitat use in lizards, often by habitat use facilitating co-existence of two or more potentially competing species. We know relatively little about how other community processes, such as predation and parasitism, are influenced by habitat use.
Why do animals occur where
they do? Beyond the basic requirement that an individual must be able to survive,
different locations or habitats may provide different conditions for an individual's
existence. Thus, another question arises: What are the consequences of the choice
of habitat or microhabitat on the biology and ecology of the organism being
considered? From an ecological point of view, habitat selection can influence
physiological processes (Huey, 1991), population dynamics (Holt, 1987; Pulliam
and Danielson, 1991), and community level processes (Morris, 1988; Rosenzweig,
Lizards are an excellent group
of organisms with which to examine the ecological consequences of habitat and
microhabitat use. First, there is a relatively long history of studying habitat
and microhabitat use in lizards, at least qualitatively (reviewed by Heatwole,
1977). Second, lizard ecology and physiology is well studied, at least for some
species (see papers in Milstead, 1967; Gans and Pough, 1982a,b; Huey et al., 1983;
Gans and Huey, 1988; Vitt and Pianka, 1994). Finally, recent studies have begun
to examine the relationship between lizards and their environments in greater
detail (see below) and provide a means to assess the role of habitat and microhabitat
use in a lizards ecology. There is also a practical reason for looking at the
ecological consequences of habitat and microhabitat use in lizards, and that is
the on-going alterations of the environment by humans. We need to understand the
role of habitat and microhabitat use in lizard ecology to be able to assess the
potential impacts of such environmental changes and to suggest possible conservation
Before we begin our review
of habitat use in lizards, it is necessary for us to define what we mean by
"habitat". Habitat can mean a number of things and its meaning can depend heavily
on the scale one is considering (see Morris, 1987a,b, 1992 for discussions of
the interaction of scale and habitat use). For the majority of this review,
habitat is used in a broader sense to include the general type of area in which
an individual occurs (e.g., woodland or desert). However, in some instances,
we use habitat and microhabitat synonymously to mean the actual substrate or
perch on which an individual occurs. We feel our use of habitat in both these
contexts is appropriate for our review because we believe that the general consequences
of habitat (or microhabitat) use at any scale will be the same for a given species
(i.e., certain requirements must be met for an individual or population to be
CONSEQUENCES OF HABITAT AND MICROHABITAT USE
The consequences of living in a particular habitat can be manifested at several levels, ranging from effects on the individual to effects on an entire community. Below we discuss the implications of using different habitats for (1) individuals, (2) populations, and (3) communities.
Being ectotherms means that lizards are affected by the thermal and biophysical environments that they experience. Ectotherm physiology and ecology are intimately linked (Huey and Stevenson, 1979) and so anything influencing physiology can affect performance or life histories (e.g., Congdon, 1989; Dunham et al., 1989; Porter, 1989). Different habitats often provide different biophysical environments (e.g., Bartlett and Gates, 1967; Pearson, 1977; Bakken, 1989; Bashey and Dunham, 1997). Indeed, lizards often choose habitats and microhabitats that facilitate thermoregulation or that allow them to maintain the appropriate body temperature
Different habitats can influence thermoregulatory behavior. For example, Anolis cristatellus in Puerto Rico actively thermoregulate when in open habitats, but passively thermoregulate in closed habitats (Huey, 1974; see also Gillis, 1991 for an example from Sceloporus undulatus). Some habitats (e.g., those with low transmittance of solar radiation) virtually eliminate the possibility for active thermoregulation by lizards, as in the case of the Australian forest dragon (Hypsilurus spinipes) (Rummery et al., 1994), the crevice-dwelling lizard, Xenosaurus newmanorum (Lemos-Espinal et al., 1998), and the lacertid lizards Podarcis melisellensis and P. muralis in the autumn (but not other times of the year) (Grbac and Bauwens, 2001). Kentropyx calcarata and Mabuya nigropunctata in lowland Amazonian tropical forest occur near opening or treefall clearings because they require sunlight to be able to maintain high body temperatures (Vitt et al., 1997).
Lizards inhabiting certain habitats providing a given biophysical environment can be expected to experience different internal environments than lizards in another habitat which could result in differences in physiological performances (see Huey, 1991), possibly resulting in differentiation of thermal preferences, physiology, and performance between individuals in different populations and habitat types (Garland and Adolph, 1991; Miles, 1994). Ultimately the habitat in which a lizard occurs can influence its energy budget (Bartlett and Gates, 1967; Congdon et al., 1982) since digestive efficiency and capacity are often influenced by body temperature (Harlow et al., 1976; Harwood, 1979; Troyer, 1987; Zimmerman and Tracy, 1989; van Marken Lichtenbelt, 1993), suggesting that lizards in different habitats may experience different digestive efficiencies. The metabolic rate of lizards in habitats with different thermal regimes can be different (e.g., Beaupre et al., 1993; Beyer and Spotila, 1994). Often metabolic rates increase with temperature (e.g., Christian et al., 1998; Mouton et al., 2000). Feeding rate and energy expenditure can also differ between habitats (Karasov and Anderson, 1984), as can other aspects of foraging behavior (e.g., capture rate; Bullock et al., 1993). In addition, temperature can affect other aspects of feeding behavior, such as foraging activity and handling time (Moermond, 1979a,b; Avery et al., 1982; Karasov and Anderson, 1984; DeQuieroz et al., 1987; Grant and Dunham, 1988; Avery and Mynott, 1990), as well as capture success (Díaz, 1994).
Lizard sprint speed and behavior are often significantly affected by body temperature (Rand, 1964b; Hertz et al., 1982, 1983; Mautz et al., 1992; Torr and Shine, 1993). Lowered sprint speeds conceivably influence susceptibility to predation (see Christian and Tracy, 1981). Habitat use, by its effects on body temperature, can generate habitat specific sprint speeds for lizards (e.g., Waldschmidt and Tracy, 1983), resulting in habitat specific predator escape ability; as well as habitat specific escape behavior. For example, during periods of the year when vegetation is sparse (e.g., early spring),
Psammodromus algirus flee from the approach of a possible predator earlier than when vegetation is more dense (e.g., summer) (Martín and López, 1995a). Within a season, escape behavior by
P. algirus is also dependent on the amount of vegetation present: in more open microhabitats flight distances are greater than in more vegetated microhabitats (Martín and López, 1995a,b; see also Martín and Lopez, 2000). Snell et al. (1988) got similar results in a study on
Tropidurus albemarlensis in the Galápagos Islands. In three species of
Anolis from Cuba, the habitat used affected escape strategies: anoles on trees with big trunks ran around to the other side of the trunk whereas anoles on trees with small trunks jumped to another tree or perch (Regalado, 1998). However, escape tactics are not always affected by habitat structure (e.g.,
Sceloporus virgatus; Smith, 1996a). In addition, lizard morphology can interact with habitat use to affect sprint speed and clinging ability (Losos and Sinervo, 1989; Losos et al., 1993b). For example, Irschick and Losos (1999) found that eight species of
Anolis tend to use habitats whose structure (e.g., distribution of perch diameters) allows maximal performance (e.g., sprint speed).
Life histories in lizards are often influenced by the proximate environment (see Ballinger, 1983; Dunham et al., 1989). Habitat use can affect lizard life histories by determining the proximate environment (biotic or abiotic) experienced by the lizard. For example, the habitats and microhabitats used by lizards may differ in the amount of food available for consumption (e.g., Alberts, 1993; Hews, 1993; Durtsche, 1995; Vitt and de Carvalho, 1995; Vitt et al., 1996; Smith, 1998). In combination with the potential thermal differences between habitats outlined above, use of different habitats and microhabitats could easily affect the growth, reproduction, and survivorship of lizards (i.e., their life histories).
Several studies have demonstrated an effect of habitat use on the life history traits of lizards (see
Table 2). Often the effects of habitat are due to differences in food availability or activity periods that can be affected by the habitat an individual is in. Along an elevational gradient populations of
Sceloporus merriami experience different biophysical environments which determine activity regimes (Grant and Dunham, 1988; Grant, 1990).
Podarcis torquatus, which occur in forest habitats in Chile, have longer activity periods than
P. volcanensis, which occur in more open habitats (Labra and Rosenmann, 1992). The activity regime of a population can interact with the amount of food available to create life history differences between populations (Grant and Dunham, 1990; Niewiarowski and
The habitat that a parent lizard uses, particularly a pregnant female (if viviparous) or an ovipositing female (if oviparous), can have consequences for the performance of their offspring (see Overall, 1994 for a detailed discussion). Many of these consequences arise from the thermal or hydric environments experienced by the pregnant female or the incubating eggs. In many species, cooler incubation sites lead to slower embryonic developmental rates than warmer incubation sites (e.g., Qualls and Andrews, 1999; Shine, 1999). Incubation conditions can also affect hatchling performance such as growth rate, sprint speed, and endurance (e.g., Qualls and Andrews, 1999; Shine, 1999).
Sceloporus undulatus eggs incubated at different temperatures differed in tail length (shorter at cooler temperatures), SVL (shorter at cooler temperatures), growth rate of hatchlings in the laboratory (faster at cooler temperatures), 42 d and overwinter survival (higher at cooler temperatures) (Andrews et al., 2000). Hatchlings from
Cyclura nubila eggs incubated at warmer temperatures were no different in size at hatching than eggs incubated at lower temperatures, but did grow faster during their first year (Alberts et al., 1997). In four species of
Sceloporus (S. aeneus, S. scalaris, S. undulatus,
S. virgatus), eggs incubated at a range of temperatures did not differ in mortality (except for a high elevation population of
S. virgatus which showed higher mortality at low temperatures) but did show a delay in hatching at low incubation temperatures (Andrews et al., 1997). In addition to the effects on aspects of offspring performance (e.g., growth and survivorship), the physical characteristics of the habitat in which a female lizard lays her eggs can determine the sex of her offspring in some species (e.g.,
Agama agama, Charnier, 1966; Chlamydosaurus kingii, Harlow and Shine, 1999;
Ctenophorus decresii and C. ornatus, Harlow, 2000; Eublepharis
macularis, Viets et al., 1993).
Pregnant females often use their habitats in such a way as to maintain a body temperature that is different from those maintained by males or non-pregnant females (e.g., Garrick, 1974; Beuchat, 1986; Smith and Ballinger, 1994a,b; Mathies and Andrews, 1997; Rock et al., 2000). Such thermoregulation may influence embryonic development and neonate performance (e.g., Beuchat and Ellner, 1987; Beuchat, 1988; Shine and Harlow, 1993; Mathies and Andrews, 1997). Swain and Jones (2000) experimentally evaluated the effects of manipulating the opportunity for pregnant female
Niveoscincus metallicus to thermoregulate (i.e., bask) on aspects of their reproduction and offspring performance. They found that females that could not bask as often gave birth less often, had a longer gestation period, and had smaller neonates that grew slower after birth as females that could bask without restrictions.
One of the things that becomes clear as one considers the studies above is that we have a fairly good understanding of how variations in the thermal environment affect individual lizard performance. It is also clear that we do not have a full understanding of how other aspects of a habitat or microhabitat (e.g., predation risk, food availability, water relations) affect individual performance, nor do we understand how these different aspects of a habitat or microhabitat interact to determine individual performance, let alone the consequences for lizard populations (see Populations). There is a definite need for additional studies to assess the relative importance of various habitat characteristics for individual performance in lizards.
While it is clear from the studies above that the physical and biotic characteristics of a habitat have ecological consequences for the performance of individual lizards, the impacts on lizard populations are often assumed to follow from the impacts on individual lizards. Unfortunately, there are few studies that have attempted to directly assess the link between the correspondence between habitat quality from the individual lizard's perspective and the performance of lizard populations in the same habitat. One exception is a study by Díaz (1997). He studied two populations of
Psammodromus algirus, one at high elevation and one at low elevation. From a performance perspective (e.g., sprint speed, ability to thermoregulate), the low elevation site would be considered a higher quality habitat than the high elevation site. Interestingly, the abundance of lizards was significantly higher at the high elevation site, suggesting that simply measuring various aspects of individual performance in a habitat may not be sufficient to understand the consequences of habitat use on population performance and abundance. We need more studies like this to determine whether the consequences for individuals also necessarily have consequences for populations, or whether we can overestimate the importance of a single aspect of habitat use, such as thermal quality, while not considering other consequences such as predation risk, prey availability, as suggested by Díaz (1997).
There are several studies that assess the impact of habitat and microhabitat changes on lizard populations; however, the specific mechanisms causing the population changes are often poorly understood. The habitat used and preferred by lizards has definite consequences for the success of populations of lizards in the face of habitat changes. For example, lizards that use open habitats tend to be positively affected at a population level by livestock grazing whereas lizards that need vegetative cover tend to be negatively affected at a population level by livestock grazing
(Table 3). Similarly, some lizard species (e.g.,
Urosaurus ornatus) are able to exploit residential areas along an urbanization gradient, whereas other lizards are only able to exploit the natural habitats (e.g.,
Cnemidophorus spp.) along the urbanization gradient (Germaine and
In some cases, habitat use may increase the possibility of a decline in a lizard population. For example, the common chameleon
(Chamaeleo chamaeleon) in Spain often uses habitats that are closely associated with human activity, thus making them more susceptible to possible declines due to over collection, road related mortality, and agricultural practices (Hódar et al., 2000). Clearcutting has a strong negative effect in arboreal lizards and decreased total lizard biomass in a north Florida flatwood (Enge and Marion, 1986). In Argentina, a change in habitat structure due to road building changes a lizard assemblage due to loss of particular habitats (e.g.,
Spartina ciliata patches) used by some species but not others (Vega et al., 2000). Those that use that habitat decreased while those that did not use the habitat did not show changes in abundance (Vega et al., 2000). Rock collectors removing rocks from the environment of the velvet gecko,
Oedura lesueurii, reduces the amount of habitat available for it to use (Schlesinger and Shine, 1994), thus possibly leading to a decline in velvet gecko abundance (Shine et al., 1998). The rocks appear to be important for thermoregulation by these geckos (Downes and Shine, 1998; Webb and Shine, 2000), which may affect gecko growth and survivorship (Webb and Shine, 2000).
In other cases, habitat use may facilitate population persistence in the face of human alterations of habitat. For example,
Egernia major uses basking to maintain its body temperature and this is commonly found in more open or edge habitats and thus they may actually benefit from some human activities such as logging (Klingenböck et al., 2000). In French Guiana, one species of lizard,
Kentropyx calcarata, becomes the most abundant and the dominant species on habitat islands created by flooding due to the creation of a hydroelectric dam reservoir, in part because of its generalist habitat use (Cosson et al., 1999). Timber practices in the Amazon, by altering the thermal and solar insolation properties of the habitat alter the make up of the lizard assemblage by increasing the number of heliothermic species in a particular area (Vitt et al., 1998a; Sartorius et al., 1999). Fire and other disturbances, such as clear-cutting timber, by maintaining a variety of successional stages of vegetation often associated with varying amounts of habitat structure and complexity allowing open habitat species and closed habitat species to persist, can be important influences on lizard distributions and abundances in many systems (e.g., mallee woodlands and heathlands of Australia, Friend, 1993; sand-pine scrub of Florida, Mushinsky, 1985; Greenberg et al., 1994).
Differential habitat use by two or more lizard species, whether the result of current ecological interactions or past ecological interactions that have led to evolutionary change (e.g., "ghost of competition past"), may permit coexistence of potential competitors thus affecting community structure and composition. Several authors have suggested that their observations of habitat segregation between lizard species indicate current or past competition. In several cases, experimental evidence is absent, and the conclusions are based upon supposition
(Table 4). Clearly, the strongest evidence for the role of habitat use in allowing coexistence of potential competitors comes from experimental studies. Such studies do exist and the results of these experiments have found evidence for habitat use mediated coexistence or competition enforced habitat segregation in lizards
(Table 5). On the other hand, many authors have used observational evidence and supposition to argue that habitat segregation is not reducing competition, but rather is serving another function (e.g., each species is filling its specific needs independently of the presence or absence of other species)
(Table 4). Experimental evidence also sometimes supports the lack of competition's importance in habitat segregation
Predator-prey interactions can also be influenced by habitat use. Lizards may use habitats based upon the presence of predator refuges, and thus alter their predation risk by using particular habitats. Densities of adult
Sceloporus jarrovii are dependent on the number of rocks present as well as the number of rock cracks which presumably provide predator refuges (Ruby, 1986). Trees with holes in them and surrounded by brush are preferred by
Eumeces laticeps because the holes, in addition to serving a role in nesting, may act as predator refuges (Cooper, 1993; Cooper and Vitt, 1994). In Chile, two species of
Liolaemus (L. platei and L. nigromaculatus) partition rock and ground habitats, with
L. platei on the ground and L. nigromaculatus on rocks (Fuentes and Cancino, 1979). Both morphology and behavior suggest partitioning is based on predation.
Liolaemus platei has both anti-predator behavior and morphology whereas
L. nigromaculatus does not. In this situation, it actually appears that predation and competition interact to influence the observed habitat use in these two lizards: predation limits
L. nigromaculatus to the rocks while competition from L. nigromaculatus excludes
L. platei from the rocks. Anolis stratulus (Reagan, 1992) and Anolis cristatellus (Chandler and Tolson, 1990) use smaller perches presumably because their predators (two larger species of
Anolis, and Epicrates monensis, respectively) are unable to use the smaller perches. Other anoles have been shown to alter their perch heights in response to the introduction of rats (Campbell, 1989 cited in Chandler and Tolson, 1990). The use of lower and narrower perches by juvenile
Anolis lineatopus and A. gundlachi may alter the ability of juveniles to detect predators, and thereby alter predation risk compared to other perches (Irschick et al., 2000).
Ctenosaura hemolopha preferentially select perches on cacti with holes that presumably serve as predator refugia (Blázquez and Rodríguez-Estrella, 1997). Pygmy blue tongue lizards,
Tiliqua adelaidensis, select deep, narrow burrows that increase their ability to protect against predators (Milne and Bull, 2000). Bauwens et al. (1999) suggest that the exclusive use of Euphorbia caput-medusae plants may in part reflect the possible decrease in predation risk these plants provide due to the number of potential shelters found in these plants. Martín and López (1998) argued that a seasonal shift in habitat use by
Psammodromus algirus occurs to allow the lizards to exploit those habitats that provide the most protection from predators: In the spring, lizards avoid shrubs that have lost their leaves and use shrubs that retain their leaves, however, in the summer the lizards prefer to use the shrubs that had lost their leaves in the spring but now have leaves relative to the shrub that keeps its leaves throughout the year. Velvet geckos
(Oedura lesueurii) use experimental rock refuges in such a way as to avoid scent cues of predatory snakes (Downes and Shine, 1998).
While the logic of the conclusions made in many of these studies appears to be valid, few studies have actually estimated predation risk or differences in predation risk in different habitats. Tail break frequency can often serve as a rough estimate of predation risk, and so by looking for differences in tail break frequency between lizards using different habitats may give us information on whether the habitat used by a lizard affects predation risk. Among
Liolaemus lizards, species that tended to use perches that reduced their visibility to predators had lower tail break frequencies than species using perches that increased their visibility to predators (Jaksic and Fuentes, 1980). Elevational differences in tail break frequency between high and low elevation populations of
Sceloporus jarrovii may arise through differences in the amount of vegetative cover and complexity (e.g., more tail loss in more open habitats) (Brown and Ruby, 1977). Parker (1994) also found that
Sceloporus undulatus in more open habitats had higher tail break frequencies than those in more closed habitats. However, Smith (1996b) found that tail break frequencies did not differ between a wooded habitat and an open habitat in a population of
One might also expect habitat use to affect parasite-host interactions. The evidence for an impact of habitat use on ectoparasite loads is variable. In some cases, such as
Sceloporus occidentalis (Tälleklint-Eisen and Eisen, 1999), mite loads vary between different habitats. However, in other cases (e.g.,
Sceloporus virgatus, Smith, 1996c), mite loads do not vary between different habitats. Endoparasites (e.g., malaria) have also been shown to differ among sites, often because of the thermal or humidity properties of the habitat that may affect both the parasite and their vectors (e.g., Ayala and Spain, 1976; Rand et al., 1983; Schall, 1992; Schall and Marghoob, 1995; Staats and Schall, 1996; Schall et al., 2000); however, detailed studies on the effects of habitat on the distribution and effect of endoparasites are unfortunately lacking. Little else is known about the impact of habitat on parasite loads in lizards.
It is quite apparent from the studies reviewed above that habitat (and microhabitat) use has the potential to be of great importance for individual lizards, populations of lizards, and communities of lizards. At the individual level, the thermal properties of an environment have a major influence on performance, and in many cases, may be the most important factor in determining the consequences of using a particular habitat. Unfortunately we know fairly little about how other characteristics of habitat (e.g., structure, predation risk, food availability, etc.) influence individual performance. We definitely need more studies investigating the consequences of these other habitat characteristics on individual performance. At the population level, the studies reviewed above suggest that how lizards use their environment can influence their persistence in the face of changes in the structure of their habitat, but we actually have little information on the actual mechanisms behind the relationship between habitat use and population dynamics. We need more such studies, and more studies looking for the links between consequences at the individual and population level. In many cases, the mechanistic explanations are assumed, but not investigated. The results may not be what we expect (see discussion of Díaz, 1997 in the Population section). Finally, at the community level, it is clear that habitat use can often either be a consequence of competition (past or present) or be a mechanism of coexistence. Unfortunately, many studies draw conclusions on the role of habitat use mediating community structure without experimental evidence, and just as with populations, conclusions are drawn based on observations that are consistent with certain hypotheses (but actually are consistent with alternative hypotheses as well). Basically, it is time to start moving from studies describing habitat use and its consequences (such studies form the basis of further investigations, and as such should not be abandoned entirely, rather they should be used to focus future research), to studies investigating the specific mechanisms by which habitat use causes the effects on lizards that we see in nature.
We thank M. Angilletta, J. Rettig, and two anonymous reviewers for comments on an earlier version of this manuscript.
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