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Notes on the Feeding Behavior and Caudal Luring by Juvenile Alsophis portoricensis
(Serpentes: Colubridae)
Author(s): Manuel Leal and Richard Thomas
Reviewed work(s):
Source: Journal of Herpetology, Vol. 28, No. 1 (Mar., 1994), pp. 126-128
Published by: Society for the Study of Amphibians and Reptiles
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126
NOTES
P. V. 1969. Prevues paleontologiques d'une
vegetation tardi-Pleistocene (dat6e par le 14C) dans
les regions aujohord'hui d6sertiques d'Amerique
du Nord. Rev. G6ogr. Rhys. G6ol. Dynam. 11:335340.
B. A. 1980. Species number, stability, and
WILCOX,
equilibrium status of reptile faunas on the California islands. In D. M. Power (ed.), The California
Islands: Proceedings of a Multidisciplinary Symposium, pp. 551-564. Santa Barbara Museum of
Natural History, Santa Barbara, California.
WELLES,
Accepted: 28 October 1993.
Journalof Herpetology,Vol. 28, No. 1, pp. 126-128, 1994
Copyright 1994 Society for the Study of Amphibians and Reptiles
Notes on the Feeding Behavior and
Caudal Luring by Juvenile
Alsophis portoricensis
(Serpentes: Colubridae)
MANUEL LEAL AND RICHARDTHOMAS, Department of
Biology, P.O. Box 23360, University of Puerto Rico, Rio
Piedras,Puerto Rico 00931-3360, USA.
Caudal luring, the waving or wriggling of a conspicuously colored tail by an otherwise cryptically
colored snake in the presence of prey (Heatwole and
Davison, 1976), has been reported for species of viperid, elapid, and boid snakes (Neill, 1960; Heatwole
and Davison, 1976; Murphy et al., 1978) and recently
for the colubrid snakes Tropidodryasstriaticeps(Sazima
and Puorto, 1993) and Alsophis dorsalis(Greene, pers.
comm.). This behavior has been documented most
frequently for juvenile crotaline vipers (Neill, 1960).
Caudal luring may function by luring a potential prey
to striking distance (Neill, 1960; Greene and Campbell, 1972; Heatwole and Davison, 1976) and/or distracting the prey's attention, thereby facilitating close
approach of the predator's head to within striking
distance (Greene and Campbell, 1972; Murray et al.,
1991; Sazima and Puorto, 1993).
With the exception of Acanthophisantarcticuslaevis
(Carpenter et al., 1978), caudal luring has been documented exclusively in snakes that bear a conspicuously colored tail. Conspicuously colored tails and
luring behavior are exhibited mostly by juveniles,
and in most cases both are lost before adulthood
(Heatwole and Davison, 1976). A lack of ontogenetic
diet change was associated with retention of caudal
luring by adult Bothropsbilineatus(Greene and Campbell, 1972), Cerastes vipera (Heatwole and Davison,
1976), Acanthophisa. antarcticusand Acanthophisa. laevis (Carpenter et al., 1978), and Sistrurusmiliariusbarbouri(Jackson and Martin, 1980).
Alsophis portoricensisis the larger of two colubrids
that inhabit the Puerto Rican Bank. It is largely a
ground-dwelling, diurnal snake that uses mainly visual cues to locate prey. Here we report the use of
caudal luring by juveniles of this species. This is the
third known case of caudal luring for a colubrid and
the second report for Alsophis.
We observed 12 feeding episodes by four juvenile
Alsophis portoricensiswithin two months after they
hatched in the laboratory (body mass [BM] 1.5-2.1 g).
Each individual was presented with three different
prey species: two species of lizards, Anolis cristatellus
(Polychridae) and Sphaerodactylusmacrolepis(Gekkonidae), and the frog Leptodactylusalbilabris(Leptodactylidae). Snakes were weighed (BM + 0.1 g) immediately after each trial, and prey were measured (snoutvent length [SVL] to nearest mm) and weighed (BM
+ 0.1 g) prior to the feeding trials. Feeding trials were
conducted in the snake cage (40 cm long x 30 cm
high x 20 cm wide) with a soil substrate. Prey was
introduced by hand into the snake cage. Both the
snakes and the lizards were maintained at a temperature of 25-27 C. Using a stop watch and an audio
tape recorder, we recorded all behaviors exhibited by
the snakes and the prey during each feeding episode.
Caudal luring was exhibited on three of the 12
feeding trials by two of the four individuals. Of the
two individuals that lured, one did so when presented
with Anolis cristatellusand Sphaerodactylusmacrolepis,
and the other when presented with S. macrolepis.None
of the snakes lured when presented with Leptodactylus
albilabris.The first episode of caudal luring was recorded on 31 August 1992. Alsophis(BM 2.1 g) began
to exhibit caudal luring 300 sec after the A. cristatellus
(SVL 20 mm, BM 0.3 g) was introduced into the cage.
The snake continued twitching its tail in a waving
fashion while maintaining the rest of its body immobile for the next 150 sec. During this period, the
prey oriented toward the twitching tail of the snake
and fixated on it; at 460 sec the lizard moved toward
the snake, and the snake attacked it.
On 4 September 1992, one Sphaerodactylusmacrolepis
was offered to each snake. An Alsophis (BM 2.1 g)
began to flick its tongue 40 sec after the prey (SVL
25 mm, BM 0.4 g) was introduced into the cage. The
snake remained immobile for the next 300 sec while
the lizard was moving around the cage; 600 sec later
the snake began to twitch its tail while remaining
immobile, and the prey responded by orienting toward the snake's twitching tail, and began to move
toward it. The lizard kept moving toward the twitching tail and was grabbed by the snake at 790 sec. The
snake finished swallowing it at 990 sec. The other
Alsophis (BM 1.7 g) began to flick its tongue 90 sec
after the S. macrolepis(SVL 28 mm, BM 0.6 g) was
introduced into the cage, while the prey remained
immobile. At 900 sec after introduction, the snake
began to twitch its tail, which lasted for the next 95
sec. However, the lizard did not react to the twitching
tail. At 1200 sec, the snake attacked and grabbed the
lizard, and finished swallowing it at 1940 sec. The
other two Alsophis individuals (BM 1.5 g and 1.8 g)
did not exhibit caudal luring to any of the prey. Caudal luring was never exhibited before the prey was
introduced into the cage or after the snake finished
eating it.
Although two of the four juvenile Alsophis portoricensisnever exhibited caudal luring, they subdued
their prey in the same manner as those that did lure.
In all feeding episodes, when presented with Leptodactylusor Sphaerodactylus,the snake seized and swal-
NOTES
lowed them directly without envenomating them, but
when presented with Anolis, the snake subdued the
prey with venom before swallowing it. The variation
in the use of venom to subdue prey seems to be in
response to the lack of strong retaliation presented
by Leptodactylusand Sphaerodactyluscompared with
the strong retaliation employed by Anolis when handled by Alsophis (Leal and Rodriguez-Robles, unpubl.). Retaliatory power, along with visual and
chemical stimuli, may be used as clues by A. portoricensis to assess prey and to "decide" if it will envenomate or not (Rodriguez-Robles and Leal, 1993). Variation in the use of venom to subdue prey also has
been reported for adult A. portoricensis(RodriguezRobles and Leal, 1993).
Alsophis portoricensisexhibited caudal luring from a
loosely coiled or looped posture in which the tail was
in the same direction as the snake's head. The snakes
never exhibited the vertical positioning of the tail
that has been reported in Bothropsbilineatus (Greene
and Campbell, 1972), Viperarusselli(Henderson, 1970),
and Tropidodryasstriaticeps(Sazima and Puorto, 1993).
Instead, with the body immobile and the tail horizontal, A. portoricensistwitched its tail spasmodically.
The tail undulated vertically with the tip sometimes
curving into a U-shape, and there were occasional
rotations through nearly 360? about the longitudinal
axis. This movement is similar to that described for
Sistrurus miliariusbarbouri(Jackson and Martin, 1980)
and Bothropsjararacussu(Sazima, 1991).
Although caudal luring has been associated with a
combination of a conspicuously colored tail and its
movements (Neill, 1960; Heatwole and Davison, 1976),
the observation that Alsophis portoricensis is able to
attract prey by the movement of an inconspicuously
colored tail indicates that the movement of the tail
itself is sufficient as a lure. The use of an inconspicuously colored tail as a lure also has been suggested
for Acanthophisantarcticuslaevis (Carpenter et al., 1978).
In that case, luring was inferred (Pough, 1988), because the prey was not in the cage of the snake and
there was no observation of prey being attracted by
the snake's tail.
Many snakes twitch or vibrate their tails in response to a threat (Greene, 1973), but we never observed juvenile Alsophis portoricensismoving their tail
when approached or handled by a person. Instead,
the snakes spread their neck and occasionally emitted
a short hiss, a behavior which is commonly exhibited
by adults. Nonetheless, adult A. portoricensismay rarely exhibit erratic movement of the tail when handled
(J. A. Rodriguez-Robles, pers. comm.).
Although caudal luring is an ambush hunting technique compatible with a sit-and-wait foraging strategy, it is possible that juvenile Alsophis portoricensis
also forage actively. There seem to be no literature
reports of foraging by A. portoricensis,although based
on its size, shape, and diurnal activity, the species is
assumed to be an active forager (Henderson and Sajdak, 1986; Henderson and Crother, 1989). Sazima and
Puorto (1993) also suggested a combination of sit-andwait and active foraging for the colubrid Tropidodryas
striaticeps.
Heatwole and Davison (1976) proposed that ontogenetic changes in diet may account for the lack of
caudal luring in adult crotaline snakes. We suggest
127
that different predation pressures on juvenile and adult
Alsophis portoricensismay account for the presence of
caudal luring in juveniles. The small size of hatchlings probably exposes them to greater predation
pressure than adults, and the sit-and-wait foraging
strategy may reduce predation risk (Huey and Pianka,
1981). Caudal luring is a way by which these small,
diurnal, surface-feeding juveniles may lessen predation. After hundreds of hours observing A. portoricensis feeding in captivity by ourselves and J. Rodriguez-Robles (pers. comm.), we have not observed
caudal luring by adults. We conclude that caudal luring is a juvenile behavior in A. portoricensis.
That two juvenile Alsophis portoricensisdid not use
caudal luring, although they did feed, indicates that
variation exists in hunting behavior. Variability in
luring tendencies also has been observed in juvenile
Agkistrodon contortrix (Fitch, 1960), Bothrops jararaca
(Sazima, 1991), and Tropidodryasstriaticeps(Sazima and
Puorto, 1993). Individual variation in use of caudal
luring may be a response to differences in hunger
level at the time that the prey was presented (Greene
and Campbell, 1972; Murray et al., 1991; Chiszar et
al., 1990).
Acknowledgments.-We thank J. A. Rodriguez-Robles, and I. Sazima for helpfully criticizing the manuscript. The Department of Natural Resources of Puerto Rico provided permits for the collection of all
specimens. This research was partially supported by
a grant from the Fondo Institucional para la Investigaci6n, University of Puerto Rico, to R. Thomas.
LITERATURE
CITED
C. C., J. B. MURPHY,
ANDG. C. CARPENTER.
CARPENTER,
1978. Tail luring in the death adder, Acanthophis
antarcticus (Reptilia, Serpentes, Elapidae). J. Herpetol. 12:574-577.
CHISZAR,
D., D. BOYER,R. LEE,J. B. MURPHY,AND C.
W. RADCLIFFE.
1990. Caudal luring in the southern death adder, Acanthophis antarcticus. J. Herpetol. 24:253-260.
FITCH,H. S. 1960. Autecology of the copperhead.
Univ. Kansas Publ. Mus. Nat. Hist. 13:85-288.
H. W. 1973. Defensive tail display by snakes
GREENE,
and amphisbaenians. J. Herpetol. 7:143-161.
1972. Notes on the use
, ANDJ. A. CAMPBELL.
of caudal lures by arboreal green pit vipers. Herpetologica 28:32-34.
HEATWOLE,
H., AND E. DAVISON. 1976. A review of
caudal luring in snakes with notes on its occurrence in the Saharan sand viper, Cerastes vipera.
Herpetologica 32:332-336.
R. W. 1970. Caudal luring in a juvenile
HENDERSON,
Russell's viper. Herpetologica 26:276-277.
, ANDB. I. CROTHER.1989. Biogeographic patterns of predation in West Indian colubrid snakes.
In C. A. Woods (ed.), Biogeography of the West
Indies: Past, Present, and Future, pp. 479-517.
Sandhill Crane Press, Gainesville, Florida.
, ANDR. A. SAJDAK.1986. West Indian racers:
a disappearing act or a second chance? Lore 36:
13-18.
HUEY,R. B., AND E. R. PIANKA. 1981. Ecological consequences of foraging mode. Ecology 62:991-999.
JACKSON,
J. F., ANDD. L. MARTIN.1980. Caudal luring
128
NOTES
in the dusky pygmy rattlesnake Sistrurusmiliarius velopmental pattern in Atelopus differs from those of
barbouri.Copeia 1980:926-927.
firmisternal and arciferal taxa (Noble, 1926; Griffiths,
1984. MiscellaMURPHY,
J. B., ANDL. A. MITCHELL.
1963); (2) whether the posterior plate-like structure
neous notes on the reproductive biology of rep- in Atelopuscorresponds to epicoracoidal horns or the
tiles. 6. Thirteen varieties of the genus Bothrops sternum (Griffiths, 1963; McDiarmid, 1971; Tyson,
1987); and (3) whether the sternum (if present) is
(Serpentes: Crotalidae). Acta Zool. Path. Antverfused to, or discrete from, the rest of the girdle
piensia 78:199-214.
AND J. C. GILLINGHAM. 1978.
C. C. CARPENTER,
,
(McDiarmid, 1971; Tyson, 1987).
These controversies are still unresolved. The power
Caudal luring in the green tree python, Chondrophythonviridis(Reptilia, Serpentes, Boidae). J. Her- of developmental studies for analyzing these controversies has not been yet fully recognized. For expetol. 12:117-119.
B. A., S. D. BRADSHAW,
ANDD. H. EDWARD. ample, even though many arguments revolve around
MURRAY,
1991. Feeding behavior and the occurrence of
developmental issues, no developmental study of the
caudal luring in Burton's Pygopodid Lialisburtonis pectoral girdle of Atelopus has been made. Developmental studies can also provide detailed information
(Sauria: Pygopodidae). Copeia 1991:509-516.
about morphological structure by, for example, showNEILL,W. T. 1960. The caudal lure of various juvenile snakes. Q. J. Florida Acad. Sci. 23:173-200.
ing that a structure is the result of the fusion of two
or more elements.
F. H. 1988. Mimicry and related phenomena.
POUGH,
I investigated the development of the pectoral girIn C. Gans and R. B. Huey (eds.), Biology of the
dle in Atelopus to examine these and other related
Reptilia, Vol. 16, Ecology B, Defense and Life Hiscontroversies, and to shed light on some related and
tory, pp. 153-234. Alan R. Liss, Inc., New. York.
RODRIGUEZ-ROBLES,
J. A., ANDM. LEAL. 1993. Effects persistent misconceptions on this specific topic. My
of prey type on the feeding behavior of Alsophis study was based mainly on one species (Atelopusfarci),
portoricensis(Serpentes:Colubridae). J. Herpetol. 27: but four other species of Atelopuswere also examined
to help resolve these crucial issues.
163-168.
I studied preserved tadpoles and juveniles of AteSAZIMA,I. 1991. Caudal luring in two neotropical
pitvipers, Bothropsjararacaand B. jararacussu.Colopus farci (lot ICN [Instituto de Ciencias Naturales,
Universidad Nacional de Colombia] 15853), Atelopus
peia 1991:245-248.
, ANDG. PUORTO.1993. Feeding technique of
nicefori,Atelopusebenoidesmarinkeli(lot IND-AN 4477),
Atelopus ignescens (lots KU 131940, 180275, 180276),
juvenile Tropidodryasstriaticeps: probable caudal
and Atelopussubornatus(lots ICN 15828, 15820). Table
luring in a colubrid snake. Copeia 1993:222-226.
1 gives stages of development (Gosner, 1960) and the
number of individuals examined per stage.
Accepted: 28 October 1993.
Histological cross sections (10 x) were prepared using the paraffin method of Weesner (1960). Surgipath
infiltration and embedding paraffin were used. Specimens were placed in alcoholic Bouins at least 24 h
before infiltration. Froglets were placed in EDTA for
Journalof Herpetology,Vol. 28, No. 1, pp. 128-131, 1994
24 h to decalcify and then transferred to Bouins. SecCopyright 1994 Society for the Study of Amphibians and Reptiles
tions were stained with Masson's trichrome (Weesner, 1960).
Only the stages of development relevant to imporAnalysis of Some Long-standing
tant systematically-related conflicts are described. ReControversies Concerning the
sults can be divided into three primary observations.
Pectoral Girdle of Atelopus
First, from stage 42 to froglet, a slight overlap (due
to growth of both halves) can be seen at the coracoid
(Bufonidae) Using Ontogenetic Studies
level (Fig. 1B). In many individuals, the epicoracoids
Schoolof BiologicalSciences,University are also
MOISES
KAPLAN,
overlapping; however they do not expand
of Nebraska,Lincoln,Nebraska68588-0118, USA.
forming blades but rather remain rounded (Fig. 1A).
No overlap was observed in the two individuals of
In the history of anuran systematics, the genus AteA. nicefori (stages 42 and 44). In the adult stage of
lopus has been the protagonist in many controversies
Atelopus,the two halves are fused all along the girdle.
Second, from stage 36, the posteromedial tips of the
concerning pectoral girdle characters. Some long-lastcoracoids extend posteriorly, forming two short proing controversies include: (1) whether the girdle deTABLE1. Stages and individuals per stage studied in each of five species of Atelopus. Abbreviations:
Af = Atelopusfarci;Ae = A. ebenoides;Ai = A. ignescens;An = A. nicefori;As = A. subornatus;fl = froglet; ad = adult.
Species
Af
Ae
Ai
An
As
27
1
~~~~~~~~Spe-
s~~Stage
28
33
34
35
36
38
40
41
42
1
3
3
1
2
1
3
3
1
6
5
1
5
1
43
44
fl
ad
1
1
1
1
2
1
2