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Diet of the desert lizard Liolaemus pseudoanomalus (Iguania: Liolaemini) in northern La Rioja Province, Argentina

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  • Instituto Patagónico para el Estudio de los Ecosistemas Continentales (IPEEC-CONICET)
Article

Diet of the desert lizard Liolaemus pseudoanomalus (Iguania: Liolaemini) in northern La Rioja Province, Argentina

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The diet of a species can help us to understand its natural history, ecological requirements, and strategies involved in searching for food. Liolaemus pseudoanomalus is a rare desert lizard where previous studies showed no seasonal, ontogenetic or sexual differences observed in microhabitat use; however the sexual dimorphism is evident in the number of precloacal pores and in the snout-vent length. In this work, we investigate if there are differences in the diet composition between sexes and age groups. Herein we describe the diet of L. pseudoanomalus, of the Central West Monte desert of Argentina, based on the analysis of 63 stomach contents. We found that ants are the most important food item and some characteristics of foraging behavior suggest similarities with other ant-eating lizards.
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Short Communication
Diet of the desert lizard Liolaemus pseudoanomalus (Iguania: Liolaemini)
in northern La Rioja Province, Argentina
M.L. Kozykariski
a
,
*
, L.C. Belver
b
, L.J. Avila
a
a
CENPAT, CONICET, Boulevard Almirante Guillermo Brown 2915 (U9120ACD), Puerto Madryn, Chubut, Argentina
b
Universidad Nacional de la Patagonia Sede Esquel, Sarmiento 840 (9200), Esquel, Argentina
article info
Article history:
Received 4 October 2010
Received in revised form
31 May 2011
Accepted 2 June 2011
Available online 13 July 2011
Keywords:
Liolaemini
Foraging ecology
Western Argentina
Squamata
abstract
The diet of a species can help us to understand its natural history, ecological requirements, and strategies
involved in searching for food. Liolaemus pseudoanomalus is a rare desert lizard where previous studies
showed no seasonal, ontogenetic or sexual differences observed in microhabitat use; however the sexual
dimorphism is evident in the number of precloacal pores and in the snout-vent length. In this work, we
investigate if there are differences in the diet composition between sexes and age groups. Herein we
describe the diet of L.pseudoanomalus, of the Central West Monte desert of Argentina, based on the
analysis of 63 stomach contents. We found that ants are the most important food item and some
characteristics of foraging behavior suggest similarities with other ant-eating lizards.
Ó2011 Elsevier Ltd. All rights reserved.
1. Introduction
In arid and semiarid environments of western Argentina, lizards
of the genus Liolaemus are a signicant component of the verte-
brate community in both species richness and population density
(Cei, 1993). Liolaemus pseudoanomalus (Burmeister, 1861) is a small
(mean adult snout-vent length [SVL] ¼45.8 11.1 mm), diurnal,
terrestrial, and oviparous desert lizard restricted to open sandy at
areas of intermontane valleys, across southern Catamarca to San
Juan Provinces (Avila et al., 2003, but see Abdala, 2007). This lizard
has an ambiguous conservation status, dened as a species for
which insufcient knowledgeexists (Avila et al., 2000). At that
time, only Sage (1972) reported a few ecological observations of L.
pseudoanomalus, without any quantitative or detailed analysis. But
in recent years, several studies were carried out, and added
important information about its natural history, habitat, behavior,
karyology, and geographic distribution (Avila et al., 2003), as well as
on its reproduction, thermoregulation, sexual dimorphism, time
budgets, and spatial use (Villavicencio et al., 2002, 2003a,b, 2006,
2007a,b). Villavicencio et al. (2006) reported no sexual differ-
ences in microhabitat use, but in another study, sexual differences
were reported in snout-vent length (Villavicencio et al., 2003b).
Thus, our expected results were to nd differences between sexes,
and ontogenetic categories according to requirements and
behavior. Food is one of the principal components in the ecological
niche of a species, and data about diet provide basic information in
studies of population and community ecology (Pianka, 1982). The
goal of this study was to describe the diet of L.pseudoanomalus, and
document sexual and ontogenetic variation in the diet.
Lizards were collected as part of an ecological study on lizard
communities carried out in the Monte phytogeographic formation
(Cabrera, 1976), along Provincial Road No. 7, 6 km east of Anillaco
(28
49
0
S, 66
57
0
W), Castro Barros Department, La Rioja Province,
Argentina. The study area was in an open sand-rocky environment
with clumps of bushes. Mean annual temperature is 19.7
C, and
there is a marked rainy season (DecembereFebruary). Vegetation is
typical of the northern area of Monte, an open shrubland of jarilla
(Larrea spp.) with several species of xerophytic plants associated
with species of cacti. Lizards were sampled between October 1998
and May 1999, with a total of 63 lizards ranging from 25 to 63 mm
snout-vent length (SVL) collected by hand, forks or rubber bands. In
most cases, lizards were collected under similar weather conditions
(sunny days) within an interval of two or 3 h in the late afternoon
after they had the opportunity to ingest food. Lizards were killed in
the laboratory by freezing or by cardiac injection of an anesthetic
drug (Pentotal
Ò
Sodico Abbott) (Simmons, 2002). Carcasses were
xed in 10e20% formalin within 3 h of the capture and stored in
70% ethanol. Snout-vent length (SVL) and jaw length (JL) were
taken to the nearest mm on all individuals, and lizards were divided
in two groups on the basis of their age category: adults
*Corresponding author. Tel.: þ54 2965 451024; fax: þ54 2965 451543.
E-mail address: kozykariski@cenpat.edu.ar (M.L. Kozykariski).
Contents lists available at ScienceDirect
Journal of Arid Environments
journal homepage: www.elsevier.com/locate/jaridenv
0140-1963/$ esee front matter Ó2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jaridenv.2011.06.004
Journal of Arid Environments 75 (2011) 1237e1239
Author's personal copy
(SVL >45.00 mm) and juveniles (SVL <45 mm). Stomachs were
removed and stored separately in vials with 70% ethanol. Stomach
contents were analyzed under a Leica Zoom 2000 stereomicro-
scope. Non-food items (small gravel, sand) were separated and
recorded. Only items found in the stomachs were considered
because these were the least digested and easiest to identify. Prey
items were identied to the lowest useful taxonomic level, usually
order or family, based on entire items or estimates of residues.
Length and width of each prey item was measured and its volume
estimated as Dunham (1983): Volume ¼4/3
P
(0.5 length) (0.5
width)
2
. The equitability index was calculated as Pielou (1969):
J¼H/H
max.
For each sex and age, the trophic diversity was calcu-
lated with Shannons Index (H ¼Sp
i
log
2
p
i
). In order to
appreciate the variation of H with respect to the number of
analyzed stomachs and to infer if sample size is adequate, the
accumulated diversity of 1, 2, 3,.nstomachs was calculated from
the sample dates (Maury, 1981).
Diet was summarized in three ways: 1) the proportion of the
total number of prey items in the stomach; 2) the proportion of the
total volume of prey items in the stomach; and 3) the proportion of
lizards eating a prey taxon. The relationship between the JL and the
length and width of the prey consumed by lizards was estimated
using the Spearman rank correlation. Sexual and ontogenetic
differences in the distribution of the items in the diet (in terms of
volume and number of items) were tested using analysis of
covariance (ANCOVA, with SVL as covariable). The relationship
between SVL, sex and percentage of volume of ants, beetles and
other prey items consumed by lizards were tested using Pearson
correlation.
Out of 63 lizards collected, 28 were adults (16 males, 12
females), and 35 were juveniles (17 males, 18 females). The equi-
tability index (J) was 0.14. The estimated trophic diversity for
juveniles was higher than adults, but the equitability index was
similar between ages. When we calculated the trophic (H) and
equitability (J) indices considering sex, both indices were higher in
males than females, indicating that males eat all prey items in
a more proportional way than females (Table 1). A sample of 23
stomachs was considered sufcient to stabilize the diversity curve
and show the diet composition of L.pseudoanomalus (Fig. 1). No
empty stomach was found in the sample. Non-food items represent
less than 1% of the stomach content (in volume). Adult males are
not signicantly larger than adult females in SVL (ANOVA, F¼1.61 ;
p¼0.2153; SVL
_
¼57.18 4.09, SVL
\
¼55.19 4.13 mm) but
differences were observed in JL between adults males and females
(ANOVA, F¼12.11; p¼0.002; JL
_
¼13.41 0.90,
JL
\
¼11.90 1.38 mm). Differences in average values of SVL
between juvenile males and females were observed (ANOVA,
F¼6.44; p¼0.02; SVL
_
¼34.36 5.25, SVL
\
¼38.53 4.46 mm),
but this differences were not observed in average values of
JL (ANOVA, F¼1.97; p¼0.17; SVL
_
¼8.68 1.26,
SVL
\
¼9.23 1.01 mm). A summary of the diet of L.pseudoano-
malus is presented in Table 2. Formicidae was the dominant prey
item by volume, number, and frequency of occurrence. Coleoptera
(50%), Aranaeae (31%) and Homoptera (22%) were important when
considered as frequency by occurrence (Table 1). There was no
signicant correlation between jaw length (JL) and length (R¼0.10,
p¼0.22) or width (R¼0.13, p¼0.10) of consumed prey. Diet of
juveniles and adults and between sexes, did not differ signicantly
by number and volume (ANCOVA, effect Prey Number: sex, F¼3.60,
p¼0.06; age, F¼0.96, p¼0.33; Sex *age, F¼2.92, p¼0.09; effect
Prey Volume (mm
3
): sex, F¼2.38, p¼0.13; age, F¼0.19, p¼0.67,
Sex *Age, F¼1.39, p¼0.24). No signicant relationship was found
between SVL and percentage of ingested ants (R
\
¼0.14, p
\
¼0.48;
R
_
¼0.04, p
_
¼0.84), beetles (R
\
¼0.19, p
\
¼0.32; R
_
¼0.07,
p
_
¼0.70) or others(R
\
¼0.07, p
\
¼0.71; R
_
¼0.10, p
_
¼0.58)
was found.
Our data indicate that L.pseudoanomalus eat mainly ants, which
constitute 90% of food items and up to 74% of the total volume in the
diet. They also feed on a variety of other arthropods such as spiders,
grasshoppers, leafhoppers, beetles and beetle larvae, this is also
indicated in the low equitability index. A high abundance of ants in
the habitat could be an explanation of our results, but we do not
evaluate food availability. In Phrynosoma, another lizard genera
from the northern hemisphere, any single individual could feed on
several ant nests within the same day, and this was the most widely
selected prey item, no ontogenetic and sexual differences were
observed in the diet (Munger, 1984); suggesting that ants
consumption may imply high energetic convenience for the lizards.
This pattern of high Formicidae consumption in L.pseudoanomalus
could have a similar energetic advantage in this environment,
however in this study we observed that females eat fewer prey
items than males and there are items that are more represented
than others. These results could indicate that males and females use
this resource in different ways, as was observed in Liolaemus
quilmes (Halloy et al., 2006). Other Liolaemus species also eat For-
micidae at high frequencies in the Argentinean lowland deserts, e.g.
90% in Liolaemus inacayali in an ecotonal area between Patagonian
Steppe and Austral Monte (Acosta et al., 1996); 100% in Liolaemus
Table 1
The diversity index (H) and equitability index (J) for age (adults and juveniles) and
sex (males and females) for Liolaemus pseudoanomalus.
Index Age Sex
Juveniles Adults Males Females
H 0.42 0.33 0.55 0.13
J 0.16 0.14 0.24 0.06
Fig. 1. Accumulated trophic diversity of Liolaemus pseudoanomalus, a good estimation
of the trophic diversity by individuals was obtained from 23 stomachs.
Table 2
Diet of Liolaemus pseudoanomalus, with prey items presented as frequency of
occurrence, percentage by number and percentage by volume (mm
3
), for eight
major taxa of food items.
Frequency Number Volume
N%N% Vol %
Araneae 20 31.75 26 0.90 996.42 6.25
Acari 5 7.94 13 0.45 9.83 0.06
Coleoptera 32 50.79 102 3.54 1816.03 11.40
Formicidae 63 100.00 2671 92.77 11,863.3 74.47
Hemiptera 1 1.58 1 0.03 58.830 0.37
Homoptera 14 22.22 52 1.81 267.46 1.68
Hymenoptera 5 7.93 7 0.24 232.81 1.46
Orthoptera 3 4.76 7 0.24 684.95 4.30
M.L. Kozykariski et al. / Journal of Arid Environments 75 (2011) 1237e12391238
Author's personal copy
darwinii, in northern Austral Monte desert of Mendoza (Avila and
Acosta, 1993); 79% in Liolaemus koslowskyi in a Monte desert
environment less than 50 km from our study site (Aun and Martori,
1998), and 93% in L.quilmes (Halloy et al., 2006). However another
species from the Monte Desert (Liolaemus scapularis) rarely
consumes Formicids (Garcia et al., 1989). None of these studies was
carried out with a study of food availability or behavior. Ants are
common and abundant arthropods of the Monte biodiversity, and
usually they are active in early morning and late afternoon to avoid
the hottest midday hours in coincidence with the liolaemids
regular activity in this desert. Ant consumption could be related
only to a coincidence with L.pseudoanomalus daily activity and not
to prey selection behavior. Nevertheless, our study supports Sages
(1972) hypothesis that L.pseudoanomalus appears to be an
ecological equivalent of the ant specialists Moloch horridus in the
Australia deserts and, similarly, to Phrynosoma platyrhinos in North
American deserts. However, a moredetailed study of the ecology of
this species must be carried out to test this hypothesis.
Acknowledgments
We are grateful to J.W. Sites Jr. (Brigham Young University,
Provo, Utah, USA), M. Morando (CENPAT-CONICET, Puerto Madryn,
Argentina), J. Marshall, (Weber State University, Ogden, Utah, USA)
and Arley Camargo (Brigham Young University, Provo, Utah, USA)
for their helpful suggestions and manuscript revision. We also
thank M. Archangelsky for the critical notes on the style of the
English text of an early version.
Animal ethics procedures were carried out in accordance with
the Institutional Animal Care and Use Committee Guidebook.
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M.L. Kozykariski et al. / Journal of Arid Environments 75 (2011) 1237e1239 1239
... quilmes, Halloy et al., 2006;L. pseudoanomalus;Kozykariski et al., 2011;L. crepuscularis, Semhan et al., 2013;L. ...
... En la mayoría de las especies del género estudiadas, las presas principales son las hormigas. En Eulaemus esto se verifica para L. lutzae (Rocha, 1989); L. darwinii (Avila y Acosta, 1993); L. quilmes (de Viana et al., 1994); L. koslowskyi (Aun y Martori, 1998;Semhan, 2015); L. wiegmannii (Aun y Martori, 1999); L. pacha (Halloy et al., 2006), L. chacoensis (Acosta y Hernando, 2009); L. pseudoanomalus (Kozykariski et al., 2011); L. cuyanus (Moreno Azócar y Acosta, 2011); L. irregularis, L. albiceps y L. multicolor (Valdecantos, 2011); L. crepuscularis (Semhan et al., 2013) y L. laurenti (Gallardo et al., 2018). Dentro de Liolaemus sensu stricto, las hormigas son el alimento más importante para L. fuscus y L. lemniscatus (Hurtubia, 1973); L. pictus (Ortiz, 1974); L. montícola (Fuentes e Ipinza, 1979); L. elongatus (Videla, 1983;Quatrini et al., 2001), y L. bibronii (Videla, 1983;Semhan, 2015); L. curis (Nuñez, 1996); L. yanalcu (Valdecantos, 2011); L. punae (Mella et al., 2010) y L. gracilis (Semhan, 2015). ...
... Liolaemus is a genus of lizards found mainly throughout the arid west of South America (Avila et al., 2010) that includes 260 species (Lobo et al., 2010;Abdala and Quinteros, 2014). Various studies describe their diet (e.g., A´un et al., 1999;Halloy et al., 2006;Kozykariski et al., 2011;Valdecantos, 2011) or reproductive biology (e.g., Martori and A´un, 1997;Vega and Bellagamba, 2005;Martori and A´un, 2010), but few consider both traits simultaneously (e.g., Martori, 2005, in the oviparous Liolaemus koslowskyi; Semhan et al., 2013, in the viviparous Liolaemus crepuscularis). ...
... Because of this, consuming small insects may be the best strategy during pregnancy because plant tissues contain less energy and nutrients per gram than do insects (Iverson, 1982;Troyer, 1991). Diet differences between the sexes have been reported for several species of Liolaemus such as in L. scapularis (García et al., 1989), L. wiegmannii (A´un et al., 1999), L. multimaculatus (Vega, 1999), L. quilmes (Halloy et al., 2006), and L. pseudoanomalus (Kozykariski et al., 2011), but in other species sex differences were small or absent (A´un and Martori, 1998;Moreno Az´ocar and Acosta, 2011;Valdecantos, 2011). ...
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... The genus Liolaemus has received great attention in recent years, including anatomical (Abdala et al. 2006;Tulli et al. 2011), biogeographic (Díaz Gómez & Lobo 2006Díaz Gómez 2007, 2011, ecological (Halloy et al. 2006;Kozykariski et al. 2011;Moreno Azocar & Acosta, 2011), ethological (Halloy et al. 2007;Labra et al., 2007;Kacoliris et al. 2008), and taxonomic studies (Abdala 2005a;Quinteros et al. 2008;Nori et al. 2010); thus, Liolaemus has become a much debated genus in the herpetological community. With several of these studies, the genus increased from 180 species in 2000 (Etheridge & Espinoza 2000) to more than 225 in the beginning of 2011 (Abdala et al. , 2009Ávila et al. 2008Quinteros et al. 2008;). ...
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... Se analizó además la relación entre la dieta y el estado reproductivo en esta especie . Como resultado se obtuvo que los formícidos constituyen una parte fundamental en la dieta de L. crepuscularis, como se ha informado para otras especies de Liolaemus (Aún y Martori, 1998;Aún et al., 1999;Kozykariski et al., 2011; Moreno Azocar y Acosta, 2011). Sin embargo, Figura 3. Valores promedio del matiz (color amarillo a naranja) y croma (saturación) para hembras adultas de Liolaemus quilmes, correspondientes a diferentes estados reproductivos (modificado de Salica y Halloy, 2009). ...
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