Vitt. Reproductive Tactics of Ameiva Ameiva in A Seasonally Fluctuating Tropical Habitat
Vitt. Reproductive Tactics of Ameiva Ameiva in A Seasonally Fluctuating Tropical Habitat
Vitt. Reproductive Tactics of Ameiva Ameiva in A Seasonally Fluctuating Tropical Habitat
tropical habitat
LAURIE
J. VITT'
Savannah River Ecology Laboratory, Drawer E, Aiken, SC, U.S.A. 29801
Received April 26, 1982
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VITT,L. J. 1982. Reproductive tactics of Ameiva ameiva (Lacertilia: Teiidae) in a seasonally fluctuating tropical habitat. Can. J.
ZOO^. 60: 31 13-3120.
The reproductive ecology of Ameiva ameiva was studied for 12 months in a caatinga habitat of northeast Brazil. Even though
rainfall was seasonal, the female reproductive cycle was not associated with this seasonality. Females reproduced year-round,
with peak reproductive periods during August-October and January-February. Clutch size ranged from one to nine and was
correlated to female size but egg size was constant. Males showed evidence of reproductive activity throughout the year. Fat body
mass of males and females varied greatly among individuals. There was no association between fat storage and wet-dry
seasonality. In females, fat body mass tended to decrease during peak reproductive periods. Most striking was the observation
that 97.8% of all adult Ameiva possessed enlarged fat bodies, suggesting that resource periods low enough to affect reproduction
did not exist during 1977- 1978. The reproductive tactics of Ameiva were similar to those of other tropical macroteiids, regardless
of their distribution, but very different than reproductive tactics of sympatric iguanid lizards. Compared with iguanid lizards,
resources may be less limiting for macroteiids because their widely foraging behavior for prey acquisition may allow them to find
rich patches of resources which would be unavailable to habitat specific sit-and-wait foragers, like most iguanid lizards.
VITT,L. J. 1982. Reproductive tactics of Ameiva ameiva (Lacertilia: Teiidae) in a seasonally fluctuating tropical habitat. Can. J.
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reproduction of tropical lizards (see Sherbrooke (1975) region is susceptible to extreme droughts or flooding (Eicit
and Duellman (1978) for review), very little is known 1968). During 1977- 1978, monthly rainfall (recorded approx-
concerning reproductive tactics of tropical lizards in imately 50 km from Exu at Ouricuri, Sudene, Divisiio de
certain environments. The Caatinga is a semiarid region Hydrologia) was similar to long-term averages (Vitt and
Goldberg 1983). In typical years, there is a dry season
of northeast Brazil which harbors a saurofauna including extending from May until November, considering months
seven gekkonids, four iguanids, five teiids, one scincid, receiving less than 50 mm rainfall to be dry. During 1977-
one anguid, and one amphisbaenid (Vanzolini et al. 1978, the dry season began in June and persisted until nearly
1980).
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this locality the same as at other localities? and (v) Is killed with Nembutal within 1 h after collection, a variety of
seasonality in the reproductive pattern of Ameiva similar measurements were taken, and lizards were fixed in 10%
to that of sympatric lizards? formalin. Measurements on fresh animals included snout-vent
length (SVL) and total body mass. Following fixation, lizards
Methods were autopsied. For males, length of each testis was recorded
Study area and climate and observations on condition of testes and epididymides were
This study was carried out near Exu, Pernambuco, a small recorded. For females, the number of corpora lutea, vitello-
town near the geographical center of "zonas das caatingas," a genic follicles, and (or) oviductal eggs was recorded. Diameter
vast semiarid region of northeastern Brazil (Reis 1976). The of vitellogenic follicles and width and length of oviductal eggs
region is of particular interest with respect to studies on lizard were recorded. Testes with attached epididymides, fat bodies,
reproductive tactics in that it is the largest dry region entirely and oviductal eggs were removed and transferred to fresh
contained within the tropics, it is surrounded by mesic Formalin. Formalin-fixed testes, fat bodies, and individual
habitats, and it contains a saurofauna exhibiting taxonomic and eggs were rolled dry on paper towels, and weighed to 0.001 g.
ecological diversity. There was no apparent change in size or shape of testes or fat
Most Ameiva sampled were taken from Low Caatinga bodies due to Formalin fixation and thus their masses are
(Caatinga Baixa) habitats. Low Caatinga communities contain considered reasonable estimates of fresh mass. Oviductal
xerophytic trees ranging from 3 to 5 m, occasional emergents eggs, however, appeared to swell in fixative (see also Martin
up to 8m, and large cacti including Cereus jamacura, 1978)and thus my wet mass estimates may be high. Eggs were
Cephalocereus gounellei, and Zehntherella squamulosa then soaked for 48 h in water and freeze-dried. Dry mass of
(Mares et al. 1981). A variety of Euphorbiacea and Legumi- eggs should not be subject to variation due to Formalin fixation
nosae are also common. The thorn forest habitat is interrupted or variation attributable to hydration state of the eggs following
by occasional granitic extrusions (Lajeiros) which provide ovulation.
refugia for many reptiles, amphibians, and mammals (see for To gain the maximum amount of information from the data
example, Lacher 1981; Mares et al. 1981; Vanzolini et al. set, females were divided into five categories: (1)containing
1980; Vitt 1980, 1981). Only one lizard, Platynotus semitae- oviductal eggs, (2) containing enlarged vitellogenic follicles
niatus, is restricted primarily to Caatinga (see Vanzolini and oviductal eggs or corpora lutea, (3) containing corpora
1976), the remaining lizard fauna resulting from colonization lutea only, (4) containing enlarged vitellogenic follicles only,
by species from the Amazon Basin, Atlantic Forest, and the and (5)nonreproductive, i.e., containing no evidence of recent
remaining open formations (Cerrado and Chaco) which extend reproductive activity. Females in any of the first three
from northeastern Brazil to Paraguay and Argentina (Vanzo- categories were considered "reproductive" because their re-
lini 1974, 1976). Ameiva ameiva is most often associated with productive state indicates that they would deposit eggs in a
open areas between the lajeiros and is uncommon where short time (categories 1 and 2) or they had recently deposited
vegetation is dense. eggs (category 3 ) .
The Caatinga climate is considered semiarid with annual For estimation of clutch size, I used only counts of enlarged
rainfall varying from less than 400 to just over 1000 mm. vitellogenic follicles (>3.0 mm) or oviductal eggs. Number of
Rainfall is highly unpredictable in timing and intensity and the corpora lutea was also recorded but used only in comparing
VITT 31 15
Results
Body size and apparent sexual dimorphism in size
Ameiva ameiva in northeastern Brazil range from 40
to 176 mm SVL (Fig. 1). Males reach sexual maturity at
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males were 141.4 + 1.6 (N = 172) mm and 90.7 + FIG. 2. Seasonal distribution of reproductive categories in
3.0 g. Means of SVL and body mass for reproductively Ameiva ameiva from northeast Brazil. Monthly sample size is
mature females were 128.8 2 1.1 (N = 144) mm and indicated across the top of the figure.
61.0 + 1.5 g. Both mean SVL and mean body mass nonvitellogenic follicles. The wide variation in size of
differed significantly between sexes (SVL: Mann- vitellogenic follicles within any given month suggests
Whitney U = 177250, p < 0.0001; body mass: that at least some females were close to ovulation during
Mann-Whitney U = 17 3 11.5, p < 0.0001). Analysis each of these months. The time period during which few
of covariance with log SVL as the covariate revealed females had vitellogenic follicles large enough to
significant differences in slopes (F1,354= 10.22, p = suggest that ovulation was near (>10 mm), corres-
0.0015) and intercepts (F1,355= 8.66, p = 0.035) of the ponded to the time period when many females contained
log body mass - log SVL relationships between sexes oviductal eggs (August-October) and was followed by
with males attaining significantly heavier mass at a a period during which no females sampled contained
given SVL than females. The latter analysis included all oviductal eggs (November-January) . Relative clutch
Ameiva sampled. mass (clutch massltotal mass) for 25 females averaged
Female reproduction 0.159 2 0.007.
The seasonal distribution of reproductive categories Clutch and egg characteristics
in Ameiva females appears in Fig. 2. The greatest Clutch size ranged from one to nine in Ameiva with
proportions of reproductive females occurred during larger females producing larger clutches (Fig. 4). Mean
June, July, and August, even though there were repro- clutch size based on oviductal egg counts was 5.7 2
ductive females during every month. The greatest 0.29 (N = 26) and mean clutch size based on counts of
proportions of nonreproductive females were observed vitellogenic follicles was 5.6 + 0.19 (N = 80). The
from September to February. models for the relationships of number of oviductal eggs
During March-July and again from December to to SVL (OVI = -9.46 + 0.114 SVL) and number of
February, size of vitellogenic follicles varied consider- vitellogenic follicles to SVL (FOLL = -7.47 + 0.099
ably among females (Fig. 3). Follicles 1 3.0 mm con- SVL) were both significant (OVI-SVL; F, ,24 = 19.7, p
tained yolk material rendering them easily distin- = 0.0002: FOLL-SVL; F1,9= 51.2, p < 0.001) and
guishable from the translucent and small (<3.0mm) SVL explained 45.1 and 39.3% of the variance (r2),
31 16 CAN. J. ZOOL. VOL. 60, 1982
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p 20
1 3 5 7 9
Clutch Size
I I 1 I 1 I I
110 120 130 140 150 160
Snout-Vent L e n g t h (mm)
MONTH
FIG. 4. The relationship between clutch size and snout-
FIG. 3. Seasonal distribution of vitellogenic follicle diam- vent length in Ameiva ameiva based on counts of oviductal
eters in Ameiva ameiva. The line at the top of the figure eggs and vitellogenic follicles. The size of dot indicates
indicates the percent of the total monthly sample containing number of data points at a given x, y coordinate. The inset
oviductal eggs or both oviductal eggs and vitellogenic follicles shows frequency of clutch sizes based on counts of oviductal
(see Fig. 2 for monthly sample sizes). eggs (shaded) and vitellogenic follicles (open).
respectively, in the clutch size estimates. Intercepts and
slopes were significantly different from zero in both
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tend to be larger than females in Ameiva, suggesting the Africa. Barbault (1976) found that Mabuya buttneri
possibility of competition among males. On several reproduced in the late wet season, M . maculilabris
occasions I observed premating , mating, or aggressive reproduced in the dry season, and Panaspis nimbaensis
behavior in Ameiva. Pertinent to sexual selection, reproduced in the wet season. Thus tropical iguanids and
chasing and fighting among male teiids is not uncom- skinks exhibit a diversity of reproductive tactics within
mon (Stamps 1977). Intrasexual aggression has been and among localities in respect to seasonality, whereas
reported, for example, in Ameiva quadrilineata (Hirth macroteiids do not. The capability of macroteiids to
1963) and a number of other teiids (Stamps 1977). reproduce continuously may be an adaptation allowing
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Reproductive success in males may be associated with them to take advantage of high resource habitats that
size and this perhaps explains the apparent size dimor- may be unpredictable in time and space. The high
phism in Ameiva ameiva. An alternate hypothesis is that mobility of these widely foraging lizards may make it
reproduction is riskier for females than males and that possible for them to find high resource patches that
apparent sexual dimorphism in size is simply a reflec- would be unavailable to sit-and-wait predators such as
tion of higher mortality rates on larger sized females. most iguanid lizards. The latter tend to be habitat
Presumably, egg or offspring size is optimized in specialists (Vitt and Price 1982) and thus many patches
animals (Smith and Fretwell 1974; Brockleman 1975) are unavailable to them. The specific habitat patches
and the lack of association of egg size in Ameiva with used by sit-and-wait foragers may have seasonal re-
any measure of parental size or season adds support to source variation which affects timing of reproduction.
this hypothesis. Recently, offspring size of certain It is clear that a great deal remains to be learned about
female lizards has been shown to vary in association reproductive tactics of tropical lizards. Sorting out
with seasonality in resource levels (Derickson 1976; phylogenetic , historical, and ecological factors contri-
Ferguson et al. 1980; Nussbaum 1981). The low value buting to the suite of reproductive characteristics that
for relative clutch mass (RCM) reported here (0.159) is renders individuals of a species successful in a particular
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similar to that reported for other macroteiids and environment remains to be one of the overriding
supports models predicting low RCM in widely foraging challenges to evolutionary ecologists.
species for ecological and energetic reasons (Vitt and
Congdon 1978; Vitt and Price 1982). Acknowledgments
It is difficult to make accurate geographic compari- T. E. Lacher, K. E. Streilein, and M. Willig provided
sons among Ameiva populations. Ameiva ameiva re- occasional assistance during the field portion of this
production has only been studied in Amazonian Ecuador study. The people of Exu, Pernambuco, were particu-
(Duellman 1978; Simmons 1975) and Peru (Dixon and larly cooperative and provided a setting which fostered a
Soini 1975). Simmons ( 1975) considered the reproduc- great amount of research. I thank Chico Ventura for
tive season to extend from late May through early allowing me access to the relatively undisturbed Fa-
December, although his data were incomplete from zenda Batente, where much of the fieldwork was carried
January to March. The observations of Dixon and Soini out. Dr. Paulo E. Vanzolini, Museo de Zoologia da
(1975) indicate that Ameiva ameiva breed continuously Universidade de S i o Paulo, provided the impetus for
in the Iquitos region of Peru. Hirth (1963) suggested this and other studies in addition to keeping up the flow
nearly continuous egg laying by Ameiva quadrilineata of much-needed supplies. Aristides Leio and the people
in Costa Rica. Other tropical macroteiids including at the Brazilian Academy of Sciences were of unmea-
Cnemidophorus ocellifer (Vitt 1983), Cnemidophorus surable help. Comments of two anonymous reviewers
deppii and Cnemidophorus lemniscatus (Fitch 1970) aided greatly in the final revision. Financial support was
apparently breed continuously. provided by the people and Federal government of
Lizards of various taxa which are sympatric with Brazil in support of the project: Estudos Ecologicos no
Ameiva ameiva in northeast Brazil exhibit a diversity of Nordeste Semi-arido do Brasil, undertaken by the
reproductive tactics. The iguanids Tropidurus torquatus Academia Brasileira de Cikncias. The final stages of this
and Platynotus semitaeniatus reproduce primarily dur- research and manuscript preparation were conducted
ing the dry season and early wet season (Vitt and under contract EY-76-C-09-0819 between the United
Goldberg 1983), whereas another iguanid, Polychrus States Department of Energy and the University of
acutirostris, reproduces at the beginning of the wet Georgia.
season over a 3-month period (Vitt and Lacher 1981). ANDREWS, R. M., and A. S. RAND. 1974. Reproductive effort
Thus it appears that Ameiva ameiva reproduction in in anoline lizards. Ecology, 55: 13 17- 1327.
northeast Brazil is more like reproduction in other BALLINGER, R. E., and J . D. CONGDON . 1981. Population
tropical macroteiids regardless of geographic location ecology and life history strategy of a Montane lizard
than it is like sympatric species of different taxa. A quite (Sceloporus scalaris) in southeastern Arizona. J. Nat. Hist.
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