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CAPÍTULO II

LIFE HISTORY PATTERNS IN TROPICAL SOUTH AMERICAN LIZARDS

Daniel O. Mesquita y Guarino R. Colli

ABSTRACT

We use comparative methods to investigate the relative contributions of environmental conditions and histori-cal effects upon life history aspects of tropical South American lizards. We assembled a dataset based on our sampling in 25 localities in tropical South America and additional data from 31 localities based on the litera-ture. To investigate the roles of phylogenetic history and environmental parameters in life history variables, we used Canonical Phylogenetic Ordination – CPO. Most populations from Cerrado, Amazonian Savannas, and Restinga are single-brooded, while most populations from Amazon Forest are multiple-brooded, corroborat-ing the hypothesis that species from seasonal regions

tend to reproduce ciclically, whereas species from less seasonal regions reproduce continuously. We found no significant differences in clutch size among regions. The CPO detected a significant historical effect in life his-tory aspects mainly in the node separating Iguania and Scleroglossa and for Cnemidophorus lizards, similar to other results reported elsewhere. Probably, the advanced age of the separation between Iguania and Scleroglossa (late Triassic), when probably most of the environmen-tal influence occurred, are responsible for the historical significant effect encountered. Much of the life history variation exhibits today simply reflect phylogenetic conservatism, thus having an historical basis.

Life history studies are essential for understanding the diversity and complexity of the vital cycles of living organisms (Roff, 1992; Stearns, 1992). Lizards are excellent subjects for ecological studies, because they are often abundant and easy to observe and capture. As a consequence, lizard studies have contributed enormously to the development of several areas of research, including foraging and life-history theory, population and community ecology, and the growing field of comparative biology (Huey et al., 1983; Vitt and Pianka, 1994). The number of studies on life-history variation has increased steadily since the classic comparative studies of Tinkle (Tinkle, 1969; Tinkle et al., 1970), and has developed enormously in the last decades (see Ballinger, 1983; Dunham et al., 1988; Shine and Schwarzkopf, 1992; Shine and Charnov, 1992; Stearns, 1984; Vitt, 1992). However, the majority of these studies was conducted either on species from temperate areas or on tropical anoles. The relevance and application of such theoretical developments to a great number of poorly known tropical species remains to be determined. For

instance, the gathering and analysis of massive amounts of data indicates that both phylogenetic inertia and adaptive responses to environmental conditions seem to influence lizard life-history patterns (Dunham and Miles, 1985; Dunham et al., 1988; Vitt, 1992). Therefore, several lineages restricted to tropical regions and under-represented in life-history studies, such as Gymnophthalmidae, Hoplocercidae, and Leiosauridae, might possess unique attributes that can substantially affect both the generality and the predictions of life-history models. Conversely, tropical regions contain unique ecogeographic features and conditions that can influence lizard ecologies in ways that disagree with current life-history theory. Nowadays, we know that there is a great variation on life-history patterns of South American tropical lizards (e.g., Colli et al., 1997; Colli et al., 2003; Mesquita and Colli, 2003b; Van Sluys, 1993; Van Sluys, 2000; Vitt, 1992; Wiederhecker et al., 2002).

Life-history variation among populations or species can have genetic and non genetic causes (Ballinger, 1983; Dunham et al., 1988). Several environmental

INTRODUCTION

LIFE HISTORY PATTERNS IN TROPICAL SOUTH AMERICAN LIZARDS50

factors can influence the life history of organisms, such as temperature, precipitation and photoperiod (Censky, 1995; Wiederhecker et al., 2002), the availability of favorable sites for egg development (Andrews, 1988), environmental predictability (Colli, 1991; Mesquita and Colli, 2003b; Vitt and Colli, 1994) and food availability (Vrcibradic and Rocha, 1998b). In addition, foraging mode can affect life history traits. Vitt and Congdon (1978) proposed that foraging mode, body shape, and relative clutch mass have coevolved in lizards. Actively foraging lizards rely on speed to avoid predation, have typically streamlined bodies, and clutches that comprise a relatively low proportion of total body mass. Conversely, sit-and-wait lizards rely on crypsis against predators, have a stocky body shape, and high relative clutch mass (Vitt and Congdon, 1978). This dichotomy was corroborated by several studies (e.g., Anderson and Karasov, 1981; Huey and Pianka, 1981; Vitt and Price, 1982; Dunham and Miles, 1985). Further, habitat specialization can also constrain life history parameters. For instance, many species of anoles have fixed clutch size of a single egg, which is compensated by multiple clutches spread throughout

the reproductive season, presumably related to the microhabitat used by these species (arboreal), which can limit the production of larger clutches because of the weight excess (Dunham et al., 1988; Roff, 1992; Stearns, 1992). Likewise, the utilization of rock crevices as shelter to avoid predators has strong influences in the morphology of Tropidurus semitaeniatus, resulting in a reduced clutch size (Vitt, 1981).

Although environmental conditions, like precipitation, temperature, and environmental predictability no doubt influence life history traits (e.g., Vitt and Colli, 1994; Censky, 1995; Wiederhecker et al., 2002; Mesquita and Colli, 2003b), it is becoming increasingly clear that life history traits could also have their origins deep in evolutionary history (e.g., Dunham and Miles, 1985; Dunham et al., 1988; Vitt, 1992). The aim of this work is to compare life history attributes of tropical South American lizards, identifying the relative contributions of environmental conditions and evolutionary history, using comparative methods combining life-history data with current phylogenetic hypotheses.

REPRODUCCIÓN EN REPTILES: MORFOLOGÍA, ECOLOGÍA Y EVOLUCIÓN 51

Study localities. 1- Cuyabeno, Colombia, 2- Santander, Colombia, 3- Boa Vista, RR,

4- Porto Walter, AC, 5- Guajará-Mirim, RO, 6- Santa Cruz da Serra, RO, 7- Ariquemes,

RO, 8- Santa Barbara, RO, 9- Humaitá, AM, 10- Amapá, AP, 11- Monte Alegre, PA, 12-

Alter do Chão, PA, 13- Curuá-Una, PA, 14- Altamira, PA, 15- Carajás, PA, 16- São Luís,

MA, 17- Serra do Cachimbo, PA, 18- Chapada dos Guimarães, MT, 19- Jaru, PA, 20- Ilha

do Bananal, TO, 21- Alto Araguaia, MT, 22- Barra do Garças, MT, 23- Pirenópolis,

GO, 24- Minaçu, GO, 25- Jalapão, TO, 26- São Domingos, GO, 27- Dianópolis, TO,

28- Alto Paraíso, GO, 29- Alvorada do Norte, GO, 30- Paranã, TO, 31- Correntina, BA,

32- Coribe, BA, 33- Brasília, DF, 34- Cristalina, GO, 35- Paracatu, MG, 36- Mirorós,

MATERIAL AND METHODS

Study sites

Used data collected by the authors during ca. two decades, from 25 localities distributed in tropical South America (Fig. 1). In addition, we searched the literature for the same kind of data, adding 31 more localities (Fig. 1). All lizards collected by authors were deposited in Coleção Herpetológica da Universidade de Brasília (CHUNB).

Reproduction

We sexed lizards by dissection and direct examination of gonads. Females were considered reproductive if vitellogenic follicles or oviductal eggs were present. We regarded the simultaneous presence of enlarged vitellogenic follicles and either oviductal eggs or corpora lutea as evidence for the sequential production of more than one clutch of eggs during the year. We considered clutch size as the number of vitellogenic follicles or oviductal eggs in mature females. For each lizard, we recorded the snout-vent length (SVL) with Mitutoyo® electronic calipers to the nearest 0.01 mm.

The data

We recorded for each population the following variables: mean SVL, mean clutch size (number of offspring per

Figure 1


clutch for all reproductive females in the population), clutch frequency (single or multiple-brooded) and preferred habitat type. We collected life history data of tropical South American lizards from 151 populations. Data from 68 populations (45%) were collected by the

authors and data the remaining 83 populations (55%) were obtained from the literature. All data collected are described in Appendix 1. From this data, we extracted common patterns and mean clutch size and SVL for species that were represented by more than one population (Table 1). We obtained climatic data, like mean annual temperature, total annual precipitation, and annual variation in precipitation for each study locality (available in Instituto Nacional de Meteorologia, 1998). To estimate annual variation in precipitation we used the coefficient of variation of total monthly precipitation.

Individual groups used in canonical phylogenetic ordination for life history data. Phylogeny based in Estes et al. (1988), Reeder et al. (2002), Frost et al. (2001) and

Giugliano (2003).

Figure 2

BA, 37- Irecê, BA, 38- Petrolina, PE, 39- Exu, PE, 40- Prado, BA, 41- Buzios, RJ,

42- Barra de Maricá, RJ, 43- Ilha Grande, RJ, 44- Ubatuba, SP, 45- Caraguatatuba, SP,

46- São Sebastião, SP, 47- Bertioga, SP, 48- Alcatrazes, SP, 49- Enseada, SP, 50- Queimada

Grande, SP, 51- Peruíbe, SP, 52- Valinhos, SP, 53- Campinas, SP, 54- Itirapina, SP,

55- Serra do Cipó, MG, 56- Vitória, ES, 57- Vilhena, RO and 58- Itatiaia, RJ. Closed

symbols: data collected by authors; open symbols: data from literature.


Statistical analyses

To assess the role of evolutionary history and environmental parameters (mean annual temperature, total annual precipitation, annual variation in precipitation, preferred habitat type and biome) in life history traits, we used Canonical Phylogenetic Ordination-CPO (Giannini, 2003). CPO is a modification of Canonical Correspondence Analysis-CCA (Ter Braak, 1986), a constrained ordination method that promotes the ordination of a set of variables in such a way that its association with a second set of variables is maximized. The significance of the association is tested via randomizations of one or both of the data sets. In our CPO, one of the matrices (Y) contained life history data (clutch size and clutch condition) measured over

the lizard populations, whereas the second matrix (X) consisted of a tree matrix that contained all monophyletic groups (Fig. 2). Each coded separately as a binary variable, and environmental parameters (mean annual temperature, total annual precipitation, annual variation in precipitation, preferred habitat type and biome). The analysis thus consisted of finding the subset of X that best explained the variation in Y, using CCA coupled with Monte Carlo permutations. Because SVL does influence life-history parameters, like clutch size (e.g., Colli, 1991; Vitt and Zani, 1996a; Vitt and Zani, 1996b; Colli et al., 2003; Mesquita and Colli, 2003a), we used mean SVL as a covariate. We performed CPO in CANOCO 4.5 for Windows, using the following parameters: symmetric scaling, biplot scaling, manual selection of environmental variables (monophyletic groups and environmental

Lizard Species

Gekkonidae

Coleodactylus meridionalis

Gonatodes humeralis

Gymnodactylus geckoides

Phyllopezus pollicaris

Thecadactylus rapicauda

Gymnophthalmidae

Colobosaura modesta

Micrablepharus maximiliani

SVL

24.78 (2)

36.40 (1)

40.71 (8)

76.10 (2)

109.10 (2)

45.35 (3)

39.04 (5)

Clutch size

1.00 (2)

1.00 (2)

1.72 (8)

2.00 (2)

1.00 (2)

2.00 (3)

2.20 (5)

Clutch condition

Fixed

Fixed

Not fixed

Fixed

Fixed

Fixed

Not fixed

Table 1


Polychrotidae

Anolis meridionalis

Polychrus acutirostris

Scincidae

Mabuya caissara

Mabuya frenata

Mabuya guaporicola

Mabuya heathi

Mabuya macrorhyncha

Mabuya nigropunctata

Teiidae

Ameiva ameiva

Cnemidophorus cryptus

Cnemidophorus lemniscatus

Cnemidophorus mumbuca

Cnemidophorus cf ocellifer

Kentropyx striata

Polychrotidae

Anolis meridionalis


Tropiduridae

Tropidurus hispidus

Tropidurus itambere

Tropidurus cf oreadicus

54.92 (2)

109.34 (3)

71.58 (1)

65.96 (4)

65.27 (3)

63.30 (2)

66.80 (1)

84.15 (5)

114.77 (14)

59.19 (3)

58.51 (4)

50.07 (2)

59.07 (19)

93.45 (2)

54.92 (2)

109.34 (3)

81.19 (3)

66.65 (4)

71.72 (11)

1.54 (2)

15.77 (3)

4.85 (4)

4.05 (4)

4.08 (3)

4.00 (2)

2.78 (7)

4.26 (5)

1.46 (14)

1.49 (3)

1.67 (4)

1.00 (2)

2.11 (19)

5.30 (2)

1.54 (2)

15.77 (3)

5.82 (3)

3.51 (4)

4.32 (11)

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Not fixed

Summary of life history data of Tropical South American lizard species. Note: Clutch sizes (in parenthesis) are relative to populations.

Continuation...


Biome

All biomes

Amazon Forest

Amazonian Savannas

Caatinga

Cerrado

Restinga

Single-brooded

52.38% (55)

10.53% (2)

61.54% (8)

53.33% (8)

64.58% (31)

62.50% (5)

Multiple-brooded

47.62% (50)

89.47% (17)

38.46% (5)

46.67% (7)

35.42% (17)

37.50% (3)

Comparison

x2 = 0.238; df = 1; P = 0.626

x2 = 11.842; df = 1; P = 0.001

x2 = 0.692; df = 1; P = 0.405

x2 = 0.067; df = 1; P = 0.796

x2 = 4.083; df = 1; P = 0.043

x2 = 0.500; df = 1; P = 0.480

Percentages of populations of South American Tropical lizards per biome according with clutch frequency. Sample sizes are in parenthesis.

Table 2

parameters), 9,999 permutations, and unrestricted permutations. We carried out other statistical analyses using SYSTAT 11.0 for Windows, with a significance level of 5% to reject null hypotheses. Throughout the text, means appear ± 1 SD.

RESULTS

In 31% of studied populations clutch size was fixed (Table 1). Apparently, similar numbers of populations of tropical South American lizards are single brooded or multiple-brooded (Table 2). Considering populations per biome, most populations from Cerrado, Amazonian Savannas, and Restinga were single-brooded, while most populations from Amazon Forest were multiple-brooded (Table 2; Appendix 1). We found no significant difference in clutch size among biomes, independently of SVL (ANCOVA F4,1,60 = 1.450, P = 0.538; Adjusted Means Amazon

Forest = 2.74 ± 2.03, Caatinga = 2.99 ± 1.77, Cerrado = 3.35 ± 1.33, Restinga = 3.41 ± 1.10, and Amazonian Savannas = 3.71 ± 1.87).

The CPO revealed a significant phylogenetic effect on life history aspects at the node separating Iguania and Scleroglossa, which accounted for 22% of total life history variation (Table 3). In addition, historical significant effects were detected in the clade containing the Cnemidophorus species from Amazonian Savannas (E’), the clade with Cnemidophorus from central and eastern Brazil (I’), in Autarchoglossa (M’), Tropidurinae and Liolaeminae (E), in the node separating Teioidea and Anguidae (L’), in Tropidurinae (F), and in Tropidurinae without Uracentron (G), accounting respectively 18, 14, 14, 12, 12, 12, and 10% of the life history variation (Table 3). No significant phylogenetic effects were detected in any other clade or in any environmental parameter (Table 3), indicating that life history parameters are shaped primarily by historical factors.


J

C

K

J’

L

M

A

Preferred habitat type

X

C’

O

S

Mean annual temperature

T

0.004

0.003

0.003

0.002

0.002

0.002

0.001

0.001

0.001

0.001

0.001

0.001

0.001

0.001

8.00

6.00

6.00

4.00

4.00

4.00

2.00

2.00

2.00

2.00

2.00

2.00

2.00

2.00

3.056

2.395

2.390

1.864

1.809

1.452

1.120

1.118

1.040

0.972

0.945

0.942

0.881

0.836

0.0856

0.1163

0.1301

0.1803

0.1862

0.2275

0.3590

0.2954

0.4023

0.3232

0.3541

0.3389

0.3574

0.3675

Group(s)

D/R

E’

I’

M’

E

L’

F

G

H

Z

I

B

K’

Variation

0.011

0.009

0.007

0.007

0.006

0.006

0.006

0.005

0.005

0.004

0.004

0.004

0.004

Variation %

22.00

18.00

14.00

14.00

12.00

12.00

12.00

10.00

10.00

8.00

8.00

8.00

8.00

F

9.142

6.811

5.804

5.545

4.774

4.659

4.385

4.150

3.803

3.396

3.311

3.209

3.098

P

0.0023

0.0056

0.0165

0.0204

0.0287

0.0341

0.0394

0.0444

0.0520

0.0667

0.0724

0.0616

0.0770

Table 3


Continuation....

Historical effects on the life history parameters South American Tropical lizards. Results of Monte Carlo permutation tests of individual groups (defined in Figs. 2) and environmental

variables, for the Y matrix of life history data, with mean SVL as a covariate. Percentage of the variation explained (relative to total unconstrained variation), and F and P values for

each variable are given (9999 permutations were used) for each main matrix.

V

W

Biome

D’

P

N

B’

G’

H’

Annual variation in precipitation

Y

Q

U

A’

F’

Total annual precipitation

0.001

0.001

0.001

0.001

0.001

0.001

0.001

0.000

0.000

0.000

0.000

0.000

0.000

0.000

0.000

0.000

2.00

2.00

2.00

2.00

2.00

2.00

2.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.818

0.771

0.749

0.670

0.638

0.546

0.446

0.295

0.242

0.205

0.167

0.139

0.089

0.058

0.054

0.016

0.4179

0.4571

0.3849

0.4205

0.4295

0.4726

0.5227

0.5899

0.6279

0.6489

0.6782

0.7128

0.7756

0.8695

0.8277

0.9001

DISCUSSION

Reproductive parameters are often related to environmental factors that limit reproduction (Tinkle et al., 1970; Dunham et al., 1988). In temperate regions, the main limiting factor is the rigorous winter, being the reproductive timing and the clutch size affected (McCoy and Hoddenbach, 1966; Pianka, 1970). In tropical regions, the reproduction is also affected by climatic variables. Some species

reproduce continuously with usually several clutches per reproductive season, where the precipitation is better distributed throughout the year (e.g., Amazon Forest) or is unpredictable (e.g., Caatinga), and reproduce cyclically with only one or a few clutches per reproductive season, in regions with seasonal climate (e.g., Cerrado and Amazonian Savannas) (see Vitt, 1982a; Vitt and Blackburn, 1983; Vitt, 1983; Vitt and Goldberg, 1983; Colli, 1991; Vitt and Colli, 1994; Wiederhecker et al., 2002; Colli et


al., 2003; Mesquita and Colli, 2003b). Apparently, in temperate regions reproduction is affected by a cold-warm seasonality; whereas in tropical regions by a wet-dry seasonality.

The seasonality in reproduction influences directly the clutch sizes. The production of bigger clutches, distributed in only one or a few hatches, in populations that live in regions with seasonal climate appear to be an adaptation to concentrate the reproductive effort in a short period, differently of what occur in unpredictable environments and in places where the precipitation is well distributed throughout the year, where generally the species reproduce continuously with smaller clutches distributed in several hatches (Colli, 1991; Vitt and Colli, 1994; Colli et al., 2003; Mesquita and Colli, 2003b). This was reported for several species. For example, Ameiva ameiva reproduce continuously with smaller clutches in the Caatinga and Amazon Forest, and seasonally with bigger clutches in Cerrado (Vitt, 1982a; Colli, 1991; Vitt and Colli, 1994), and Cnemidophorus ocellifer and Gymnodactylus geckoides reproduce seasonally with bigger clutches in Cerrado and continuously with smaller clutches in the Caatinga (Vitt and Goldberg, 1983; Vitt, 1983; Colli et al., 2003; Mesquita and Colli, 2003b). Our results partially support this tendency. We showed that most lizard populations from Cerrado, Restinga and Amazonian Savannas (seasonal biomes) are single-brooded and most populations from Amazon Forest

are multiple-brooded, but our results for Caatinga contradict this hypothesis. However, data from a very well studied Caatinga site in Northeast Brazil, Pernambuco State, clearly reveal this tendency. From 13 species from this area, nine shows prolonged reproductive period and are multiple-brooded (Vitt, 1992). Regarding the clutch size, even which our results showed the tendency of clutch sizes of lizards from Cerrado, Restinga and Amazonian Savannas being bigger than from Amazon Forest and Caatinga, the comparisons were not significant. However, studies comparing reproduction aspects from the same species among biomes, like Ameiva ameiva, Cnemidophorus ocellifer and Gymnodactylus geckoides from Caatinga and Cerrado, confirm this trend (Colli, 1991; Vitt and Colli, 1994; Colli et al., 2003; Mesquita and Colli, 2003b).

Several Anoline lizards are characterized by a clutch size of a single egg as a consequence of an extremely low relation between clutch and body weight, which is partly compensated by multiple broods (Andrews and Rand, 1974). A characteristic of the genus Anolis is the possession of expanded subdigital lamellae or adhesive toe pads. These are adaptively associated with arboreal habitats in most species (Andrews and Rand, 1974; Roff, 1992). The number of subdigital lamellas is positively correlated with the degree of arboreality in Anolis species; the loading capacity of a female anole may limit the amount of additional weight she can


carry and still climb effectively (Collette, 1961). In contrast, arboreal lizard species without toe pads (e.g., Polychrus, Iguana and Chamaleo) have a large clutch size (see Vitt and Lacher, 1981; Campos, 2004). Thus, the low clutch number in some anoles is explained by their climbing habitats (Andrews and Rand, 1974; Roff, 1992). Also, the use of crevices to avoid predators could also play an important role in the evolution of body and egg morphology and clutch size in the lizard Tropidurus semitaeniatus (Vitt, 1981). Unlike most Tropidurus species, which lay hatches of 3-8 eggs (This work, Vitt, 1991c; Van Sluys, 1993; Vitt, 1993; Van Sluys et al., 2002; Wiederhecker et al., 2002), T. semitaeniatus lay only two elongated eggs as an adaptation for its habit (Vitt, 1993). In addition, an unrelated genus with crevice-dwelling habits, the African Cordylidae Platysaurus showed similar modifications to those in T. semitaeniatus (Roff, 1992). However, our results do not corroborate this hypothesis. The CPO analysis indicated none significant effect of preferred habitat type on life history traits, accounting only 2% of the total variation. We have no doubt about the constraining of life history traits by mechanical factors imposed by habitat type; nevertheless, this constrains appear to be uncommon, in whole South America, only T. semitaeniatus appear to have this trait. Also, the anoles species used in the analysis (Anolis meridionalis and A. nitens), are not arboreal and probably do not suffer this constrains.

The CPO detected a significant historical effect in life history aspects mainly in the node separating Iguania – Scleroglossa and for the Cnemidophorus lizards. Similar results, based on dietary shifts, were reported elsewhere. In a study with diet data of 184 lizard species of four families from four continents reveal significant historic effects on dietary shifts, being the most striking divergence in the node separating Iguania – Scleroglossa (Vitt et al., 2003; Vitt and Pianka, 2005). The authors suggested the hypothesis that ancient events in squamate cladogenesis, rather than present–day interactions, caused dietary shifts in these major clades, which promoted that some lizards gained access to new resources, influencing much of the biodiversity observed today (Vitt et al., 2003; Vitt and Pianka, 2005). Even that the environmental variables influenced and still influence in life history traits of lizards, the separation between Iguania and Scleroglossa, when probably most of this influence occurred, was long ago in the evolutionary history of these clades (late Triassic). In addition, much of the life history variation exhibit today simply reflect phylogenetic conservatism, thus having an historical basis (see Harvey and Pagel, 1991; Brooks and McLennan, 1993). Regarding the historical effects encountered in Cnemidophorus lizards, the genus occurs from Argentina to north of Central America (Zug et al., 2001; Reeder et al., 2002). In spite of their wide distribution, they exhibit similar


ecological traits along them (see Pianka, 1970; Vitt et al., 1997b; Mesquita and Colli, 2003b). Studies with South American Cnemidophorus, show that their ecological traits are very conservative, varying a little, even among drastically different biomes, which is an indication that these parameters have an historical basis (Vitt et al., 1997b; Mesquita and Colli, 2003b), corroborating with the results encountered in the present work.

Although there are some analyses to examine the historical influences on ecological aspects, the use of phylogenetically based analyses is in its infancy, and the nature of forces acting on species remains unclear. Previous studies have suggested that ecological aspects have both historical and non historical basis (Ballinger, 1983; Dunham et al., 1988; Vitt and Colli, 1994; Mesquita and Colli, 2003b). In addition, observations on ecological characteristics of species and the use of great amount of data, especially involving a significant portion of clades (global ecology) are essential to elucidate the origins of life history variations.

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LS

Scleroglossa

Anguidae

Diploglossus lessonae

Gekkonidae



Gonatodes humeralis

Gonatodes humeralis

Gonatodes hasemani









Lygodactylus klugei

Hemidactylus mabouia





Gymnophthalmidae

Bachia bresslaui

Colobosaura modesta

Colobosaura modesta

B

CA

CE

CE

AF

AF

AF

CE

CE

CE

CE

CA

CE

CE

CA

CA

CA

CA

CE

AF

AF

CE

CE

CE

POP

39

30

46

5

16

5

30

46

25

38

23

24

39

39

39

39

46

13

1

35

35

46

SVL

141.4 (28)

23.16 (7)

26.40 (25)

36.40 (7)

40.10 (11)

41.98 (85)

39.67 (75)

39.55 (370)

47.17 (107)

37.49 (5)

38.29 (61)

39.74 (287)

41.8 (191)

28.85 (355)

57.90 (29)

75.25 (70)

76.95 (19)

105.90 (29)

112.30 (24)

90.67 (12)

47.43 (14)

51.33 (6)

CS

3.33 (9)

1.00 (1)

1.00 (4)

1.00 (7)

1.00 (14)

1.00 (11)

1.67 (6)

1.75 (4)

1.65 (32)

2.00 (1)

1.00 (2)

2.00 (1)

1.71 (28)

2.00 (47)

2.00 (94)

2.00 (2)

2.00 (12)

2.00 (3)

1.00 (7)

1.00 (7)

2.00 (1)

2.00 (5)

2.00 (1)

CF

1

-

1

+ 1

+ 1

+ 1

1

1

1

-

-

-

1

+ 1

+ 1

1

+ 1

-

+ 1

+ 1

-

1

-

PHT

SF

LL

LL

TR

TR

LG

TN

UL

UR

TN

UR

UR

UR

UR

TR

B

RO

RO

B

TR

LL

LL

LL

REF

(Vitt, 1985)

This work

This work

(Vitt et al., 2000)

(Miranda and Andrade, 2003)

(Vitt et al., 2000)

This work

This work

(Colli et al., 2003)

This work

This work

This work

This work

(Vitt, 1986; Vitt, 1995)

(Vitt, 1986; Vitt, 1995)

(Vitt, 1986; Vitt, 1995)

(Vitt, 1986; Vitt, 1995)

This work

(Vitt and Zani, 1997)

(Vitt and Zani, 1997)

This work

This work

This work

Appendix 1


Colobosaura modesta

Micrablepharus atticolus






Neusticurus ecpleopus

Neusticurus juruazensis

Vanzosaura rubricauda

Scincidae

Mabuya agilis

Mabuya caissara

Mabuya caissara

Mabuya caissara

Mabuya caissara

Mabuya frenata

Mabuya frenata

Mabuya frenata

Mabuya frenata

Mabuya dorsivittata

Mabuya guaporicola

Mabuya guaporicola

Mabuya guaporicola

Mabuya heathi

Mabuya cf heathi

Mabuya macrorhyncha

Mabuya macrorhyncha

Mabuya macrorhyncha

CE

CE

CE

CE

CE

CE

CE

AF

AF

CA

RE

RE

RE

RE

RE

CE

CE

CE

CE

MF

CE

CE

CE

CA

CE

RE

RE

RE

25

20

29

17

46

25

21

4

4

39

42

26

45

44

47

33

24

52

21

35

30

39

25

42

41

49

37.30 (20)

38.05 (45)

36.11 (27)

42.67 (3)

40.64 (14)

38.77 (48)

37.00 (6)

60.75 (14)

33.27 (26)

34.83 (121)

66.80 (41)

-

-

71.58 (16)

-

60.06 (264)

66.42 (206)

71.95 (233)

65.40 (12)

54.60 (16)

76.00 (1)

60.80 (10)

59.00 (5)

67.05 (272)

59.54 (20)

66.80 (98)

2.00 (3)

1.90 (13)

2.00 (4)

2.00 (1)

3.00 (4)

2.00 (1)

2.00 (6)

2.00 (8)

2.00 (11)

2.00 (45)

3.50 (18)

4.00 (9)

5.60 (14)

5.00 (17)

4.80 (12)

3.50 (15)

3.80 (31)

4.90 (113)

4.00 (12)

3.20 (5)

4.00 (1)

4.00 (3)

4.25 (4)

5.00 (131)

3.00 (10)

2.66 (38)

3.30 (35)

2.40 (11)

+ 1

+ 1

1

-

+ 1

-

1

+ 1

+ 1

1

1

1

1

1

1

1

+ 1

1

1

-

-

-

-

1

1

+ 1

-

-

LL

OG

TN

OG

LL

OG

OG

M

LL

OG

LL

BS

BS

BS

BS

-

-

RO

TR

RO

SS

SS

SS

BS

BS

BR

BR

BR

This work

(Vieira et al., 2000)

This work

This work

This work

This work

(Vitt, 1991c)

(Vitt and Ávila-Pires, 1998)

(Vitt and Ávila-Pires, 1998)

(Vitt, 1982b; Vitt, 1995)

(Rocha and Vrcibradic, 1999;

Rocha and Vrcibradic, 1996)

(Vanzolini and Rebouças-Spieker, 1976)




(Pinto, 1999b)

(Pinto, 1999b)

(Vrcibradic and Rocha, 1998a)

(Vitt, 1991c)

(Vrcibradic et al., 2004)

This work

This work

(Mesquita et al., 2000)

(Vitt and Blackburn, 1983)

This work

(Rocha and Vrcibradic, 1999)



Continuation...


Mabuya macrorhyncha

Mabuya macrorhyncha

Mabuya macrorhyncha

Mabuya macrorhyncha






Mabuya sp.

Teiidae

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva

Ameiva ameiva




Cnemidophorus gramivagus


RE

RE

RE

RE

AS

AS

CE

CE

AF

CE

CE

CA

AS

CE

CE

CE

AS

CE

AS

CE

AF

AF

AS

AS

AS

AS

AS

AS

AS

50

51

56

48

11

25

33

24

46

17

39

11

35

46

33

12

24

3

21

14

19

3

15

11

10

14

9

12

82.30 (10)

80.17 (6)

80.40 (338)

88.71 (307)

89.15 (143)

55.79 (35)

85.11 (115)

135.10 (316)

84.86 (80)

126.71 (61)

128.00 (6)

133.69 (358)

78.07 (43)

113.42 (31)

118.26 (116)

122.80 (11)

125.30 (21)

114.00 (137)

126.50 (33)

115.00 (34)

58.89 (85)

53.77 (81)

64.90 (21)

55.84 (93)

51.13 (54)

2.20 (51)

3.20 (12)

3.40 (5)

2.33 (3)

3.00 (2)

4.00 (4)

5.30 (9)

4.30 (97)

4.70 (94)

3.54 (13)

2.60 (5)

5.65 (106)

3.33 (3)

5.93 (14)

5.50 (2)

6.40 (83)

8.00 (1)

3.67 (3)

4.20 (5)

4.30 (10)

4.40 (12)

3.20 (110)

3.90 (28)

4.80 (5)

1.09 (23)

1.48 (21)

1.90 (15)

1.68 (3)

1.13 (8)

-

-

-

-

-

-

1

1

-

1

1

+ 1

-

+ 1

-

+ 1

-

-

1

+ 1

+ 1

+ 1

+ 1

1

1

+ 1

-

1

1

BR

BR

BR

BR

BS

BS

LG

LL

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG





This work

This work

(Pinto, 1999b)

(Pinto, 1999b)

(Vitt and Blackburn, 1991)

This work

This work

(Vitt, 1982a)

This work

This work

This work

(Colli, 1989; Colli, 1991)

This work

This work

This work

(Vitt and Colli, 1994)




This work

This work

(Mesquita, 2001; Mesquita and Colli, 2003b)

(Vitt et al., 1997b)


This work

Continuation...





Cnemidophorus nativo






















Cnemidophorus parecis

Dracaena guianensis

Kentropyx calcarata

AS

AS

DF

RE

CE

CE

CE

CE

CE

CE

CE

CE

CE

CE

CA

CA

CE

CE

CA

CA

CA

CE

CE

CA

CA

CE

AF

AF

3

2

40

27

25

21

29

35

30

24

28

22

33

32

31

34

18

37

36

38

23

39

57

10

62.44 (125)

57.45 (74)

63.03 (250)

56.10 (48)

50.63 (27)

49.51 (193)

57.40 (12)

50.46 (77)

57.46 (22)

52.33 (162)

53.69 (142)

54.62 (29)

53.29 (59)

58.33 (28)

59.75 (20)

56.50 (14)

56.22 (37)

59.49 (36)

69.64 (45)

59.91 (22)

65.14 (63)

60.33 (81)

59.35 (322)

72.52 (464)

65.85 (99)

65.78 (99)

303.38 (6)

80.28 (122)

1.88 (8)

1.50 (16)

2.17 (46)

2.20 (37)

1.00 (3)

1.00 (43)

2.30 (12)

1.50 (2)

3.00 (2)

1.80 (5)

2.25 (16)

2.00 (2)

1.75 (4)

2.60 (5)

2.00 (5)

2.25 (4)

3.25 (4)

1.83 (6)

1.50 (2)

1.60 (5)

1.75 (4)

2.20 (15)

2.07 (41)

2.67 (41)

1.83 (23)

1.58 (12)

6.00 (1)

6.00 (11)

1

1

+ 1

+ 1

-

1

1

-

-

1

1

-

-

1

1

-

-

1

-

1

-

1

1

+ 1

1

1

+ 1

-

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

OG

TE

BS

This work


(Mojica et al., 2003)

(Menezes et al., 2004)

This work

This work

(Vitt, 1991c)

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

This work

(Mesquita and Colli, 2003a; Mesquita

and Colli, 2003b)

(Vitt, 1983)



This work

(Vitt, 1991b)

(Anjos et al., 2002)

Continuation...


Kentropyx paulensis

Kentropyx striata

Kentropyx striata

Kentropyx vanzoi

Kentropyx pelviceps

Crocodilurus amazonicus

Iguania

Leiosauridae

Enyalius leechii

Enyalius brasiliensis

Polychrotidae

Anolis meridionalis

Anolis meridionalis

Anolis nitens




Tropiduridae

Eurolophosauros nanuzae

Liolaemus lutzae

Plica plica

Plica umbra

Tropidurus etheridgei

Tropidurus hispidus

Tropidurus hispidus

Tropidurus hispidus

Tropidurus semitaeniatus

Tropidurus insulanus

Tropidurus itambere

Tropidurus itambere

CE

AS

AS

CE

AF

AF

AF

AF

CE

CE

CE

CE

CE

CA

CE

RE

AF

AF

CE

AS

AS

CA

CA

CE

CE

CE

54

3

3

57

1

9

43

21

35

46

46

33

39

55

42

21

11

3

39

39

17

24

35

70.22 (5)

100.90 (146)

86.00 (110)

46.91 (47)

105.00 (42)

189.21 (62)

97.30 (14)

81.25 (15)

58.00 (1)

51.83 (53)

61.60 (191)

104.63 (8)

114.05 (118)

51.00 (236)

56.80 (19)

127.35 (32)

86.95 (32)

67.50 (45)

78.64 (44)

74.08 (130)

90.85 (478)

76.70 (370)

74.60 (73)

68.21 (154)

4.20 ()

5.29 (7)

5.30 (21)

3.00 (2)

6.50 (11)

5.67 (3)

12.30 (6)

7.50 (2)

1.00 (1)

2.07 (31)

3.09 (35)

17.50 (2)

13.00 (1)

16.80 (46)

2.06 (51)

2.27 (84)

2.90 (63)

1.90 (10)

4.90 (45)

4.27 (15)

7.20 (5)

6.00 (95)

2.00 (102)

3.68 (22)

3.00 (11)

3.98 (54)

1

+ 1

+ 1

-

+ 1

-

1

1

-

+ 1

+ 1

1

-

1

+ 1

+ 1

+ 1

+ 1

+ 1

+ 1

1

+ 1

+ 1

1

1

+ 1

OG

BR

BS

LL

WA

BR

LL

BS

BS

BS

TE

TE

RO

OG

TR

TR

SS

RO

TR

RO

RO

RO

RO

OG

This work

(Vitt and Carvalho, 1992)

(Vitt and Caldwell, 1993)

(Vitt et al., 1995)

This work

(Vitt et al., 1996)

(Van Sluys et al., 2004)

(Vitt, 1991c)

This work

This work

This work

(Luedemann et al., 1997)

(Vitt and Lacher, 1981; Vitt, 1995)

(Galdino et al., 2003)

(Rocha, 1992; Araújo, 1991)

(Vitt, 1991a)

(Vitt et al., 1997a)

(Vitt, 1991c)

This work

This work

(Vitt and Goldberg, 1983; Vitt, 1995)

(Vitt and Goldberg, 1983; Vitt, 1995)

This work

This work

This work

(Faria, 2001)

Continuation...


Tropidurus itambere

Tropidurus itambere

Tropidurus montanus

Tropidurus spinulosus

Tropidurus torquatus












Uracentron flaviceps

CE

CE

CE

CE

CE

CE

CE

CE

CE

AS

CE

CE

AF

AF

AF

AF

AF

23

17

55

21

33

29

27

30

46

15

25

23

8

7

6

14

1

60.13 (194)

71.60 (176)

73.95 (243)

86.20 (21)

94.72 (299)

57.17 (41)

69.31 (48)

55.18 (51)

79.73 (26)

65.47 (72)

42.62 (165)

71.94 (136)

80.00 (56)

89.65 (53)

85.25 (82)

92.60 (38)

98.69 (20)

3.57 (35)

3.50 (40)

3.48 (52)

4.00 (21)

6.10 (56)

6.00 (1)

4.12 (17)

4.50 (2)

5.00 (3)

5.33 (3)

4.00 (1)

3.65 (26)

3.40 (17)

3.50 (18)

3.80 (45)

4.20 (24)

2.00 (5)

+ 1

+ 1

+ 1

+ 1

+ 1

-

1

-

-

-

-

1

1

+ 1

+ 1

+ 1

+ 1

RO

RO

RO

TR

RO

OG

RO

RO

RO

RO/OG

RO

RO

RO

RO

RO

TR

(Van Sluys, 1993)

(Van Sluys et al., 2002)

(Vitt, 1991c)

(Wiederhecker et al., 2002; Pinto, 1999a)

This work

This work

This work

This work

This work

This work

(Faria, 2001)

(Vitt, 1993)

(Vitt, 1993)

(Vitt, 1993)

(Vitt, 1993)

(Vitt and Zani, 1996a)

Life history data per population of Tropical South American lizards. Note: LS- lizard species, B- biome, POP- population, SVL- mean Snout vent-length, CS- clutch size,

CF- clutch frequency, FM- foraging mode, PHT- preferred habitat type, REF- Reference, AC- active foragers, SW- sit and wait foragers, B- building, BR- branches, BR-

bromeliads, BS- bushes, LG- log, LL- leaf litter, OG- open ground, RO- rock outcrops, SF- semi-fossorial, SS- sandy soils, TE- trees, TN- termite nests, TR- trunks, UL-

under log, M- Mud, UR- under rock, WA- water, AF- Amazon Forest, CA- Caatinga, CE- Cerrado, DF- Dry Forest, RE- Restinga, MF- Montane Fields and AS- Amazonian

Savanna. Population codes are defined in Figure 1. Sample sizes (in parenthesis) refer to individuals in each population.

Continuation...

life history patterns in tropical south american …colli2010.pdf · 50 life history patterns in...

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