ArticlePDF Available

Function of Body Coloration in Green Anoles (Anolis carolinensis) at the Beginning of the Breeding Season: Advertisement Signaling and Thermoregulation

Authors:

Abstract and Figures

We examined two hypotheses regarding the function of body coloration in green anoles Anolis carolinensis. First, their bright green coloration serves as a social signal advertising territorial possession or dominance. From this hypothesis, two predictions derive: 1) most anoles with bright green coloration are adult males; and 2) adult males with bright green coloration tend to perch at higher positions to send the signal to broad areas. Another hypothesis, which is not exclusive to the former one, is that the dark coloration functions to raise their body temperature. From this hypothesis, three predictions derive: the anoles with dark (brown) coloration are 1) observed more frequently in the morning than in the daytime, 2) more likely to engage in basking behavior than in other behaviors, and 3) observed more frequently when air temperature is low. We tested these predictions in the field at the beginning of their breeding season. The results supported the advertisement signal hypothesis, but not the thermoregulation hypothesis. However, since our negative results against the latter may actually be attributable to relatively low air temperature throughout our observation period, additional observations are desired to verify rejection of the thermoregulation hypothesis as resulting from the present study.
Content may be subject to copyright.
doi 10.5358/hsj.30.155Current Herpetology 30(2): 155–158, December 2011
© 2011 by The Herpetological Society of Japan
Function of Body Coloration in Green Anoles (Anolis
carolinensis) at the Beginning of the Breeding Season:
Advertisement Signaling and Thermoregulation
SHINJI YA B U TA 1* AND AKIKO SUZUKI-WATANABE2
1Department of Animal Science, Teikyo University of Science & Technology, Uenohara,
Yamanashi 409–0193, JAPAN
2Department of Biological Science, Nara Womens University, Kitauoyahigashi-machi,
Nara 630–8506, JAPAN
Abstract: We examined two hypotheses regarding the function of body colora-
tion in green anoles Anolis carolinensis. First, their bright green coloration
serves as a social signal advertising territorial possession or dominance. From
this hypothesis, two predictions derive: 1) most anoles with bright green colora-
tion are adult males; and 2) adult males with bright green coloration tend to
perch at higher positions to send the signal to broad areas. Another hypothesis,
which is not exclusive to the former one, is that the dark coloration functions to
raise their body temperature. From this hypothesis, three predictions derive:
the anoles with dark (brown) coloration are 1) observed more frequently in the
morning than in the daytime, 2) more likely to engage in basking behavior than
in other behaviors, and 3) observed more frequently when air temperature is
low. We tested these predictions in the field at the beginning of their breeding
season. The results supported the advertisement signal hypothesis, but not the
thermoregulation hypothesis. However, since our negative results against the
latter may actually be attributable to relatively low air temperature throughout
our observation period, additional observations are desired to verify rejection
of the thermoregulation hypothesis as resulting from the present study.
Key words: Advertisement signals; Anolis carolinensis; Behavior; Color change;
Thermoregulation
INTRODUCTION
The green anole, Anolis carolinensis, is
known to change its body coloration from
bright green to dark brown, but why does such
a change occur? There are several putative
functions in the lizards changing body colora-
tion, such as predation avoidance by making
itself more cryptic, advertisement by demon-
strating its presence to conspecific individuals,
and advantage in thermoregulation. However,
recent relevant studies yielded no evidence that
in A. carolinensis body color changes so as to
match the substrate coloration for crypsis
(Jenssen et al., 1995). Thus, we have tested
two other hypotheses related to functions of
the phenomenon, advertisement signal and
thermoregulation, on the basis of predictions
deriving from them as below.
* Corresponding author. Tel: +81–554–63–4411;
Fax: +81–0554–63–4431;
E-mail address: shinji@ntu.ac.jp
156 Current Herpetol. 30(2) 2011
HYPOTHESES TESTED
Advertisement signal hypothesis
Many animals use visual and auditory signals
to advertise territorial possession. Conspicuous-
ness is significant for such signals. For example,
experimental changes in conspicuousness of
color signals in birds lead to change in territory
size: males with increased conspicuousness
obtain larger territories than those with reduced
conspicuousness and controls (Marchetti, 1993).
Dominant males of the anole defend territories
during the breeding season (Greenberge and
Noble, 1944). For these individuals, the brilliant
green coloration may advertise dominance,
being advantageous in defending and maintain-
ing the territory (advertisement signal hypoth-
esis). If this is the case, two predictions would
be possible. First, most anoles with bright
green coloration should be adult males. Sec-
ondly, bright green males should perch portions
of trees and other objects in their territories
where they can broadcast the signal effectively:
in a higher position that is visible from a broader
area. Actually, in laboratory experiments in
which two males were encountered to determine
the dominant-subdominant relationship, a
dominant male wore brighter green body col-
oration and attained a higher place (Korzan et
al., 2002; Plavicki et al., 2004).
Thermoregulation hypothesis
Reflectance strongly affects the warming
rate of animals exposed to insolation. For this
reason, body coloration might affect heating
rates in lizards during basking (Cooper and
Greenberg, 1992). Green anoles may there-
fore change their body coloration to regulate
body temperature. If this is the case, they
should choose darker (brownish) coloration
when they seek to raise their body tempera-
ture. Three predictions derive from this infer-
ence. First, more anoles would be brownish in
the morning (i.e. before being active) than in
the daytime. Secondly, the lower the air
temperature, the more anoles would be brown-
ish. Finally, anoles would be brownish at higher
frequency in basking than in other behaviors.
MATERIALS AND METHODS
Green anoles have been introduced to
Chichi-jima island (27°N, 142°E) around 1965
(Hasegawa et al., 1988). The breeding season
of anoles on this island ranges from March–
September (Suzuki, 1996). Observations were
carried out between 14 and 19 March 2000
when the breeding season had just started (see
above). We set a route to walk and observe
anoles in the morning (0750–0830 h) and
daytime (early in the afternoon, 1310–1430 h)
everyday. We recorded the body coloration,
approximate body size, behavior, and approxi-
mate height from the ground and substrate col-
oration of perching position for each individual
encountered. The height was estimated to
nearest 10 cm. Substrate coloration was identi-
fied to one of the following six categories: dark
brown, brown, gray, beige, green, and dark
green. Air temperatures were measured at 1 m
height in shade before each observation.
Body coloration was visually assigned to one
of the four classes of brightness: bright green,
green, brown, and dark brown. Body size was
also visually categorized into three classes: large
(snout-vent length [SVL] >180 mm), medium
(120–180 mm), and small (<120 mm). The
large anoles were adult males because they
always had well-developed jaws and dewlaps.
Behaviors in which anoles engaged were
classified into four categories: basking (stayin-
ing motionless in the sun), resting (staying
motionless in the shade), patrolling (moving
around), and displaying.
RESULTS
We made a total of 169 individual observa-
tions. Obviously the anoles’ body coloration
did not match the substrate coloration: in only
17 of these 169 observations their body color-
ation matched the substrate coloration.
Large, medium, and small anoles took bright
green coloration in 29 of 80, one of 54, and six
of 35 observations, respectively. The ratio of
the number of anoles that adopted bright
green coloration was significantly larger in
YABUTA & SUZUKI-WATANABE—BODY COLORATION IN GREEN ANOLE 157
large anoles than in medium (chi-squared test,
χ2=21.95, df=1, P<0.001) and small (chi-
squared test, χ2=9.40, df=1, P<0.005) anoles.
In approximately half cases (85/169), anoles
took dark coloration (brown and dark brown).
The ratio of the number of individuals that
adopted brown coloration was higher in the
morning than in the daytime, but that for dark
brown showed the opposite pattern (Table 1).
Collectively, anoles showed no tendency to
take dark coloration more frequently in the
morning (i.e. before activity) than in the
daytime. In addition, no significant associa-
tion was recognized between the coloration and
behavior (Table 2: chi square test, χ2=4.66,
df=3, P>0.05). Also, there was no tendency
of taking darker coloration when air tempera-
ture was low (Fig. 1).
In anoles of the large body class, the
frequency of individuals adopting each colora-
tion did not differ between the morning and
daytime observations (chi-squared test, χ2=
0.59, df=3, P>0.05). In addition, this fre-
quency did not change between individuals
engaging in basking and the other behaviors
(chi-squared test, χ2=4.66, df=3, P>0.05). In
contrast, anoles of the large body class showed
a significant tendency of taking green colora-
tion at higher perching positions (Fig. 2,
ANOVA, df=1, 78, F=6.73, P=0.011).
DISCUSSION
The results supported the two predictions
from advertisement signal hypothesis. Large
anoles adopted bright green coloration more
frequently than medium-sized and small anoles
TABLE 1. The number of anoles that adopted
each body coloration in the morning and daytime.
Time
Body coloration
Bright green Green Brown Dark brown
Morning 22 26 35 13
Daytime 14 22 14 23
TABLE 2. The number of anoles that adopted
each coloration when engaging in basking or the
other behaviors (resting, patrolling, and displaying).
No significant association was detected between the
coloration and the behavior.
Behavior
Body color
Bright green Green Brown Dark brown
Basking 16 29 26 22
Not Basking 20 19 23 14
FIG. 1. Air temperature and the numerical ratio
of anoles adopting each body coloration. Numeral
above each column equals the sample size for each
air temperature condition.
FIG. 2. The perching height of adult male
anoles observed. These anoles were divided into
four groups based on their body coloration: bright
green (BG), green (G), brown (B), and dark brown
(DB). Upper and lower margins of, and thick hori-
zontal line in each box indicate upper and lower
quartiles, and median, respectively. The upper and
lower lines outside the boxes indicate UQ+1.5·IQD
and LQ-1.5·IQD, respectively, where UQ, LQ, and
IQD represent upper quartile, lower quartile, and
inter-quartile distance, respectively.
158 Current Herpetol. 30(2) 2011
did. Moreover, in the large bodied class (or
among adult males [see above]), the higher the
perching position is, the more frequently an
individual showed bright green coloration.
During the breeding season, adult males need
to advertise their territorial possession or
dominance. A signal by more brilliant body
coloration from a higher perching position
would be more visible from a broader area
than that broadcasted by darker coloration
from a lower position, dissuading other males
from intruding the territory. On the other
hand, it is known that territorial male A.
carolinensis show reduced aggression towards
established territorial neighbors (“dear enemy”
phenomenon) (Qualls and Jaeger, 1991). The
males distinguish familiar and unfamiliar
opponents mainly by vision (Forster et al.,
2005). Advertising in a visually conspicuous
way (wearing brilliant greenish coloration at
higher perch) might help territorial males to
establish and maintain the social relationships
with the neighbors, reducing aggressive inter-
actions with them.
The results did not support the three predic-
tions from thermoregulation hypothesis. How-
ever, this does not necessarily completely negate
the function of body coloration for thermoreg-
ulation. In the present study, approximately
half of the anoles observed were brownish, a
result contrasting to that in the study of Jens-
sen et al. (1995), in which most anoles were
green. In the present study, air temperature,
ranging from 18.3–23.3C, was lower than that
in the study of Jenssen et al. (1995: almost
thoroughly higher than 25C). Therefore,
difference in the pattern of variation in body
coloration between these studies may actually
reflect the difference in range of air tempera-
ture between them, that is, more brownish
when cooler and greenish when hotter.
In conclusion, we suspect that A. carolinensis
takes darker coloration as its base color at the
beginning of the breeding season when it is gen-
erally cooler, and that adult males change their
body coloration to more greenish when they
need to advertise their territorial possession.
This idea needs further verification on the
basis of appropriately designed experiments
and observations.
LITERATURE CITED
COOPER, W. AND GREENBERG, N. 1992. Color and
behavior. p. 298–422. In: C. Gans and D. Crews
(eds.), Biology of Reptilia, Volume 18, Physiology
E: Hormones, Brain, and Behavior. University
of Chicago Press, Chicago.
FORSTER, G. L., WATT, M. J., KORZAN, W. J.,
RENNER, K. J., AND SUMMER, C. H. 2005. Oppo-
nent recognition in male green anoles, Anolis
carolinensis. Animal Behaviour 69: 733–740.
GREENBERG, B. AND NOBLE, G. K. 1944. Social
behavior of the American chameleon (Anolis
carolinensis Vo ig t ) . Physiological Zoology 17:
392–439.
HASEGAWA, M., KUSANO, T., AND MIYASHITA, K.
1988. Range expansion of Anolis c. carolinensis
on Chichi-jima, the Boin Islnds, Japan. Japanese
Journal of Herpetology 12: 115–118.
JENSSEN, T. A., GREENBERG, N., AND HOVDE, K.
A. 1995. Behavioral profile of free-ranging male
lizards, Anolis carolinensis, across breeding and
post-breeding seasons. Herpetological Mono-
graphs 9: 41–62.
KORZAN, W. J., SUMMERS, T. R., AND SUMMERS, C.
H. 2002. Manipulation of visual sympathetic
sign stimulus modifies social status and plasma
catecholamines. General and Comparative Endo-
crinology 128: 153–161.
MARCHETTI, K. 1993. Dark habitats and bright
birds illustrate the role of the environment in
species divergence. Nature 362: 149–152.
PLAVICKI, J., YANG, E., AND WILCZYNSKI, W. 2004.
Dominance status predicts response to nonsocial
forced movement stress in the green anole lizard
(Anolis carolinensis). Physiology and Behavior
80: 547–555.
QUALLS, C. P. AND JAEGER, R. G. 1991. Dear enemy
recognition in Anolis carolinensis. Journal of
Herpetology 25: 361–363.
SUZUKI, A. 1996. Green anole. p. 72. In: S. Sengoku,
T. Hikida, M. Matsui, and K. Nakano (eds.), The
Encyclopaedia of Animals in Japan Volume 5:
Amphibians, Reptiles, Chondrichthyes. Heibon-
sha, Tokyo. (in Japanese)
Accepted: 29 November 2011
... We found that males of A. carlliebi follow this trend, since they used higher perches (which correspond to inflorescences of Agave stricta) than females, but only during the warm season, which could be explained by many reasons. First, by perching higher during the reproductive season, males can easily defend their territories (Andrews, 1971;Ramírez-Bautista and Benabib, 2001;Yabuta and Suzuki-Watanabe, 2011) resulting in a greater opportunity to win aggressive encounters against conspecific males (Andrews, 1971;Kamath and Losos, 2017). Second, advertisement and courtship displays are more conspicuous and, therefore, can be easily seen by conspecific males and females, respectively (Eifler and Eifler, 2010;Johnson and Wade, 2010;Edwards and Lailvaux, 2012;Kamath and Losos, 2017). ...
Article
Thermal ecology and microhabitat use by lizards are affected directly and indirectly by intrinsic (e.g., sex and body size) and extrinsic (e.g., environmental seasonality, vegetation cover, and wind speed) factors. Herein we evaluate the effect of seasonality and sex on field thermal ecology and microhabitat utilization of a population of Anolis carlliebi inhabiting a xeric scrubland in Central Mexico. Lizards were found primarily in full and filtered sun conditions, strongly associated, respectively, with inflorescences and leaves of Agave stricta. Males were slightly larger than females. Mean field body temperature did not differ between sexes within seasons, but males used higher perches than females in the warm season. We observed a seasonal shift in body temperature and perch use in males, which exhibited higher body temperatures and occupied wider and higher perches in the warm season. Female body temperature and perch use did not differ between seasons. This study reports the first case of a population of Anolis specializing in a species of Agave as microhabitat. These results add to our understanding of thermoregulation and microhabitat use of mainland species of Anolis since they face different environmental pressures than Caribbean species. La ecología térmica y el uso del microhá bitat de las lagartijas se ven afectados directa e indirectamente por factores intrínsecos (p. ej. sexo y tamaño corporal) y extrínsecos (p. ej. estacionalidad ambiental, cobertura vegetal, y velocidad del viento). En este trabajo evaluamos el efecto del sexo y la estacionalidad sobre la ecología térmica en campo y la utilización del microhá bitat de una población de Anolis carlliebi que habita en un matorral xerófilo del centro de México. Las lagartijas se encontraron principalmente en condiciones de sol directo y sol filtrado, fuertemente asociadas, respectivamente, con inflorescencias y hojas de Agave stricta. Los machos fueron un poco má s grandes que las hembras. La temperatura corporal promedio de campo no difirió entre sexos dentro de unaépoca, pero los machos usaron perchas má s altas que las hembras en laépoca cá lida. Encontramos un cambio estacional en la temperatura corporal y el uso de la percha en los machos, quienes exhibieron temperaturas corporales mayores y ocuparon perchas má s anchas y altas en laépoca cá lida. La temperatura corporal y uso de la percha de las hembras no cambiaron entreépocas. Este estudio reporta el primer caso de una población de Anolis especializada en una especie de Agave como microhá bitat. Estos resultados se suman a nuestra comprensión de la termorregulación y el uso del microhá bitat de las especies continentales de Anolis, ya que se enfrentan a presiones ambientales diferentes a las especies del Caribe.
... Lizards within the genus Anolis Daudin, 1802 have historically attracted attention for their ability to change from a bright green to dark brown within only a few minutes (e.g., Parker and Starratt 1904;Kleinholz 1936). Rapid color change in Anolis continues to be a topic of interest because of its broad relevance to physiological ecology and the evolution of animal signals (Plavicki et al. 2004;Yabuta and Suzuki-Watanabe 2011;Wilczynski et al. 2015). The green-to-brown transition is induced by the stimulation of melanophores, cells that contain melanin pigments (Hadley and Goldman 1969;Vaughan 1987). ...
Article
Full-text available
Many species use color change to optimize body coloration to changing environmental conditions, and drivers of rapid color change in natural populations are numerous and poorly understood. We examined factors influencing body coloration in the Water Anole (Anolis aquaticus Taylor, 1956), a lizard possessing color-changing stripes along the length of its body. We quantified the color of three body regions (the eye stripe, lateral stripe, and dorsum) before and after exposure to a mild stressor (handling and restraint). Based on current understanding of the genus Anolis Daudin, 1802, we hypothesized that exposure to a stressor would generate genus-typical skin darkening (i.e., increased melanism). Contrary to expectations, stress consistently brightened body coloration: eye and lateral stripes transitioned from brown to pale blue and green and the dorsum became lighter brown. Sex, size, and body temperature did not correlate with any aspect of body coloration, and a laboratory experiment confirmed that ligh...
Article
The behavior of 10 free-ranging male green anoles A. carolinensis was videotaped in a riparian habitat. Comparisons of breeding versus non-breeding seasons showed dramatic shifts in the percentage of time spent in the various behavioral modes. Over all contexts, the respective breeding versus post-breeding season rates for distance moved and displaying were 26 m/h versus 8 m/h and 100 displays/h versus 6 displays/h. Breeding males were polygynous and defended exclusive, closely monitored home ranges that overlapped an average of 2.8 resident females. Males used all available microhabitats and were considered perch generalists. Males exhibited a wide range of foraging behaviour, reflecting a generalist's mode of prey capture. Males were bright green 75% (breeding season) and 87% (post-breeding season) of the time. Based on the results, the influence of captivity on lizard behaviour is discussed. -from Authors
Article
Male green anoles convey territorial ownership to rivals through use of stereotyped aggressive displays, with intrasexual interactions often escalating to physical combat. In the laboratory, losers of such interactions significantly reduce their aggressive behaviour when interacting with the same opponent 7 days later. In the current study, we examined whether this behavioural modification is a function of opponent recognition. Pairs of size-matched male A. carolinensis were allowed to interact for 2 h. Following this, subjects were separated for varying intervals, and then participated in a second interaction with either the same or an unfamiliar opponent. Losers of the first interaction significantly reduced their total aggressive behaviour when re-paired with the same opponent after a 3-day interval but not after a 10-day interval between the first and second interaction. However, losers of the first interaction failed to show reduced aggression during their second interaction when paired 3 or 10 days later with an unfamiliar opponent. Therefore, A. carolinensis appear to learn information specific to their opponent during an initial agonistic interaction, with the salience of this information declining when the interval between interactions increases. Males also showed low levels of chemosensory taste behaviour during agonistic interactions, suggesting that opponent recognition does not rely on chemoreception. Similarities between our results and findings from other vertebrate species suggest that the motivation to behave aggressively during social interactions can be influenced by opponent recognition rather than by previous experience of social defeat alone.
Article
ANIMALS exhibit a diversity of colour patterns that are commonly used in interspecific and intraspecific communication1–3. Factors influencing the evolution of signals used in communication include the properties of the physical environment in which the signal is generated2–10, the perceptual systems of individuals (such as potential mates or predators) receiving the signal2,3,11–16, and the nature of the information signalled. In warblers of the genus Phylloscopus, species differences in colour patterns are correlated with light intensity of the habitat: brighter species live in darker habitats. I report here two observations that colour patterns function to increase conspicuousness, and are used in intraspecific communication. First, individuals make themselves temporarily more conspicuous by flashing the bright colour patterns in display, and are less conspicuous when not displaying. Second, experimentally increasing conspicuousness of males within a given habitat increases territory size, whereas experimentally reducing conspicuousness results in either a smaller territory or its total loss. Traits used in intraspecific communication are often thought to diverge as a result of variation in perceptual systems2,3,13,15–17. This study shows that variation in the physical environment can cause species divergence, and this will occur whether perceptual systems are variable or relatively constant.
Article
We used changes in body color and eyespot formation, two somatic indices of stress controlled mainly by catecholamine activity, to compare the reactions of dominant and subordinate male green anole lizards (Anolis carolinensis) to a nonsocial stressor, forced movement. Individual males were pretested by subjecting them to 10 min of forced movement induced by chasing them around their home cage with a slender wooden stick. Stress responses were assayed via changes in body color (progressive darkening from green to brown indicating increasing stress) and expression of a black postorbital eyespot (which appears with increasing catecholaminergic stress responses). Lizards were paired and allowed to form stable dominant/subordinate relationships for 2 weeks. After that period of stable social status, dominants and subordinates were separated and subjected to the same forced-movement stress. There was no difference between experimental groups in the pretest. After assuming positions in the dominance hierarchy, however, dominant males showed reduced somatic indicators of stress and were quicker to recover from the stress. The data suggest that animals that assumed the dominant position decreased their stress response relative to the pretest, while animals that assumed the subordinate position increased their stress response relative to the pretest. The results indicate that dominant social status may have advantages beyond the realm of social interactions by enhancing an individual's ability to tolerate other, nonsocial stressful events.
Article
Darkening of postorbital skin (eyespots) in Anolis carolinensis occurs during stressful situations via adrenal catecholaminergic activation of beta(2)-adrenergic receptors. The eyespots form more rapidly in dominant males during social interaction. It was hypothesized that eyespot darkening from green to black is a social signal that communicates disposition, resulting from sympathetic activation and determines social hierarchy. To assess the value of the eyespot as a signal influencing social dominance, males were paired according to size and weight, and painted postorbitally; one with green and the other with black paint. Painted pairs interacted with aggressive displays, approaches, and bites. Dominant status was determined by continued displacement of an opponent, superior perching position, and lighter color. Males with eyespots darkened by black paint were dominant in 100% of interactions and more aggressive. Males viewing an opponent with eyespots painted black exhibited higher plasma epinephrine (Epi), norepinephrine (NE), and dopamine (DA) levels than males with eyespots hidden with green paint and isolated controls. Results for behavior were similar, but those for plasma catecholamines contrast with those from recent experiments in which interactions occurred vs. a mirrored reflection. The eyespot is a potent stimulus, acting as a social signal that confers dominant status to its bearer, and activates the sympathetic nervous system in opponents that observe it during aggressive interactions.
The Encyclopaedia of Animals in Japan
  • A Suzuki
SUZUKI, A. 1996. Green anole. p. 72. In: S. Sengoku, T. Hikida, M. Matsui, and K. Nakano (eds.), The Encyclopaedia of Animals in Japan Volume 5: Amphibians, Reptiles, Chondrichthyes. Heibonsha, Tokyo. (in Japanese)
Color and behavior Physiology E: Hormones, Brain, and Behavior Opponent recognition in male green anoles, Anolis carolinensis
  • W And
  • N Greenberg
  • Chicago
  • G L Forster
  • M J Watt
  • W J Korzan
  • K J Renner
  • C H And Summer
COOPER, W. AND GREENBERG, N. 1992. Color and behavior. p. 298-422. In: C. Gans and D. Crews (eds.), Biology of Reptilia, Volume 18, Physiology E: Hormones, Brain, and Behavior. University of Chicago Press, Chicago. FORSTER, G. L., WATT, M. J., KORZAN, W. J., RENNER, K. J., AND SUMMER, C. H. 2005. Opponent recognition in male green anoles, Anolis carolinensis. Animal Behaviour 69: 733-740.