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Accepted: 6 September 2005
Associate Editor: Troy A. Baird
Herpetologica, 62(1), 2006, 18–27
Ó 2006 by The Herpetologists’ League, Inc.
VISUAL SIGNALING IN PHRYNOBATRACHUS KREFFTII
BOULENGER, 1909 (ANURA: RANIDAE)
WALTER HIRSCHMANN1
1
AND
WALTER HÖDL1,2
Department of Evolutionary Biology, University of Vienna, Althanstraße 14, A-1090 Wien, Vienna, Austria
ABSTRACT: During intraspecific interactions involving males, females and subadults, acoustic as well as
visual signals were observed in the diurnal frog Phrynobatrachus krefftii. Strikingly, interactions between adult
males are highly dominated by inflations of the bright yellow subgular vocal sac without sound production. We
studied the signaling behavior in males of P. krefftii at the Amani Nature Reserve, Usambara mountains,
Tanzania, from November 2001 to March 2002. Under nonmanipulated conditions, we registered 641 malemale interactions involving 31 individuals during 323 hours of observation. Most (496 or 77 % ) inflations of the
vocal sac were purely visual; the remainder (145 or 23%) of the signals were bimodal, and accompanied by
sound production. To test whether exclusive visual signaling can be evoked under experimental conditions,
we introduced tethered males into the visual field of 28 residents, registering the elicited responses over
10 minutes after the introduction. Unimodal (i.e., exclusive visual) signals (825 out of 1106 responses)
dominated over vocal-sac inflations accompanied with sound production. In seven selected focal males, the
rate of exclusive visual signaling (0.57 signals/min), however, was more frequent than under nonmanipulated
conditions (0.13 signals/min). Phrynobatrachus krefftii is the first species of anuran amphibians reported to
perform nonaudible vocal-sac inflations during intraspecific male-male signaling behavior.
Key words: Acoustic communication; Agonistic behavior; Amphibia; Anura; Phrynobatrachus krefftii;
Visual signaling; Vocal sac
THE MOST prominent mode of communication in anuran amphibians is, by far, the use
of sound production. Compared to acoustic
cues, visual signals play a subordinate role in
amphibian communication. Some anuran species, however, perform remarkable visual displays in variable social contexts (Amézquita
and Hödl, 2004; Davison, 1984; Haddad and
Giaretta, 1999; Harding, 1982; Hödl et al.,
2
CORRESPONDENCE: e-mail, walter.hoedl@univie.ac.at
1997; Lindquist and Hetherington, 1996,
1998; Richards and James, 1992). All presently
described species performing visual displays
emit acoustic signals as well (Hödl and
Amézquita, 2001), which makes it difficult to
separate the functional role of both communication modalities (but see Narins et al., 2003).
Diurnal species of anurans commonly produce
visual displays (Durant and Doyle, 1975;
Wells, 1980) with limb signals being the most
distinctive behavior described (e.g., Davison,
1984; Harding, 1982; Heyer et al., 1990; Hödl
March 2006]
HERPETOLOGICA
19
FIG. 1.—Phrynobatrachus krefftii. Female (above left) and male without (above right), partly (below right) and fully
expanded vocal sac (below left). Note the bright yellow subgular region of the male. Photographs taken by W. Hödl at
Zigi River (Amani Nature Reserve), Tanzania.
et al., 1997; Pombal et al., 1994 ). In addition to
its acoustic function, the vocal sac also may act
as a conspicuous visual signal. Despite of the
variety of diverse vocal-sac types, their visual
relevance has not yet been explored thoroughly
(Hödl, 1996).
Visual signaling so far has been recorded only
in tropical frogs, with many species occurring
along streams and creeks (Hödl and Amézquita, 2001; Lindquist and Hetherington,
1998). We searched for other visually communicating species along East African mountain
streams, and found that the diurnally active
Phrynobatrachus krefftii appeared to be a good
candidate. Males of this ranid species are dull
brown in color, but possess a strikingly brightyellow vocal sac. Thus, the aim of this study was
to investigate the possible role in communication of the conspicuously colored gular region
during intraspecific encounters.
The exclusive African frog genus Phrynobatrachus currently contains 66 species, all of
which occur in sub-saharan Africa (Poynton,
1999). The endemic P. krefftii is diurnal and
inhabits localities of seepage water, rivulets
and streams in submontane and montane
rainforest within the East and West Usambara
Mountains in Tanzania (Barbour and Loveridge, 1928). Within the Amani Nature Reserve
(ANR) of the East Usambara mountains, P.
krefftii occurs at elevations above 800 m in
a submontane evergreen forest.
A remarkable color dimorphism is found
between males and females: Males reach up to
50 mm in snout–vent length (SVL) and possess
a brightly yellow subgular region. Females
reach 40 mm in SVL (Barbour and Loveridge,
1928), and their throat region is light brown
colored (Fig. 1). Inflatable vocal sacs are
present only in sexually mature males. Two
more species of the genus Phrynobatrachus,
P. alleni and P. accraensis (5 P. latifrons), also
possess yellow throat coloration in breeding
males (Rödel, 2000, 2003; Rödel and Agyei,
2003).
20
HERPETOLOGICA
Due to the regular occurrence of egg
clutches and tadpoles throughout a nine
month observation period (July 2001–March
2002), P. krefftii is considered a ‘‘prolonged
breeder’’ (sensu Wells, 1977). Males occupy
breeding territories containing rocks and fallen
branches in shallow water. Territories are sites
for mate attraction and oviposition, as well as
areas for feeding and shelter. Male residents
readily scrutinize conspecific intruders in their
visual field by leaving their calling sites and
approaching the offenders. At night, adult as
well as juvenile frogs are found at resting sites
on leaves within the vegetation along the banks
of the stream at approximately one meter
above the ground. Out of 158 recaptures, 59
(30%) toe-clipped individuals were found less
than 20 cm from the initially marked site on
leaves each night over a period of seven days.
Calling activities of male frogs were observed
throughout the day (W. Hirschmann and
M. Franzén, unpublished data).
MATERIALS AND METHODS
The study was conducted near the village of
Amani (5869 S and 388389 E, 900 m), TangaDistrict, Tanzania within a submontane forest
of the East Usambara Mountains belonging to
the Zanzibar-Inhambane transitional rainforest type (White, 1983). Mean annual rainfall
(1902–1970) is 1910 mm (Rodgers and Homewood, 1982) with peak precipitation in March,
April and May. Two study areas were selected
within the boundaries of the Amani Nature
Reserve. A 400-m transect along the margin of
the Zigi river (58099 S and 388639 E) and a 112m stretch along the border of a rivulet (58109 S
and 388639 E) were marked by colored tapes.
The stream was bordered by gallery forest and
secondary growth, with the soil surface continuously being soaked by seepage water. The
rivulet was partly covered with dense vegetation. Because of unusual dryness during the
study period the water level in both stream and
rivulet was exceptionally low.
The behavior of P. krefftii was studied from
19 November 2001 to 09 March 2002, totaling 77 days and 323 h of observation. For
orientation within the study sites and to
observe the patterns of activity and site fidelity
of P. krefftii, a preliminary study was carried
out in July 2001, with observations taken
[Vol. 62, No. 1
during both day and night hours. The frogs
were located on their nocturnal resting sites in
the dense vegetation using a head lamp
between 2000 h–0300 h every night between
09 June 2001 and 15 July 2001. All individuals
larger than 20 mm SVL were toe clipped
(according to Hero, 1989). The nonmanipulated observations started at 0900 h and ended
at 1700 h, and corresponded to the typical
period of diurnal activity of P. kreffii. In total,
14 sites (seven each along a stream and
a rivulet) with good visibility and access were
selected, each containing at least four adult
males. The order of observations within the
pool of individuals was chosen randomly.
Nonmanipulated observations were obtained
from a distance of approximately 2 m from the
focal individual. Each individual observation
lasted 30 min. For vocal recording, a microphone was placed 0.75 m in front of the focal
male. Recordings were made with a Sony Professional Walkman WMDC6 using a directional
microphone (AKG C568 EB). To measure the
background noise and to test the possible
acoustic energy produced during nonaudible
vocal sac inflation, a sound-pressure level meter (Volticraft No. 33-2050; ‘‘A’’ weighted, fast
response) was positioned 0.75 m in front of
the signaling individual. Sonagrams were produced with a MAC computer using Canary
(1.2.4) software.
To test the importance of visual encounters
and to confirm that the visual signal is directed
towards an introduced male frog during
territorial interactions, we performed experiments with tethered frogs. Individual P. krefftii
males (SVL x 6 SD 5 36.4 6 3.6 mm, n 5
15) were caught and used at the onset of the
rainy season between 28 February 2002 and 15
March 2002 starting each day at 0900 h and
ending at 1700 h. Experimental manipulations
were restricted to the manual introduction of
a tethered male P. krefftii hanging on a fishing
rod, which was tied to a waist band. Because
preliminary observations showed that soundless vocal-sac expulsions occur mainly during
close-range encounters, the tethered males
were positioned within the visual field of
a resident male at a 30 cm distance (cf.
Amézquita and Hödl, 2004). We observed
the behavior for 10 min immediately following
the insertion of the tethered male. Focal
individual and all-occurrence samplings (con-
March 2006]
HERPETOLOGICA
21
FIG. 2.—Territorial male of Phrynobatrachus krefftii, in upright position and without (left) or with vocal-sac display
(right). Drawn by H. C. Grillitsch after a photographs taken by W. Hödl at Zigi River (Amani Nature Reserve), Tanzania.
(Graphics courtesy of H. C. Grillitsch).
tinuous recording) were used for behavioral
records (Martin and Bateson, 1986). Descriptions of the behavior were made of toe-clipped
individuals (according to Hero, 1989) observed
and videotaped in the field. With the exception
of two adult specimens (female and male)
deposited at the Institute of Zoology at the
University of Dar Es Salaam USDM 1697
(male), USDM 1698 (female), all tested
individuals were released after the experiments. Chi-square tests for significance were
two tailed with a 5 0.05.
RESULTS
Males of P. krefftii were acoustically and
visually active during the daytime and
throughout the study period. After rainfall
and during the rainy periods in December
2001 and February 2002, signaling activity
increased. Males displayed four conspicuous
inter-individual behaviors: orientation shift to
face an intruder, assuming an upright posture
displaying their throat, vocalization, and expulsion of the vocal sac without audible sound
production. Soundless expulsions of the vocal
sac were observed in 49 out of 51 studied
individuals under nonmanipulated conditions.
Visual communication of P. krefftii consists
of unimodal (visual) and bimodal (acoustic and
visual) signals as described below.
Visual Signaling Performed by Males
Purely visual signals were associated with
the exposure of the highly contrasting gular
region. In contrast to the cryptic dorsal and
pectoral coloration, the singular subgular
vocal sac is brightly yellow-colored, and
thus highly conspicuous. When the male is
observed at ground level from the front, as
is the case during encounters with conspecifics, the visibility of the male in alerted
position is greatly enhanced (Figs. 1, 2). We
quantified the visual displays of 49 signaling
males and observed that 77% of vocal-sac
expulsions were performed without (audible) sound production under nonmanipulated conditions (Table 1). During
nonaudible vocal-sac expulsions no excess
energy beyond the background noise was
detectable within the frequency range of
the A-weighted sound-pressure level (SPL)
meter positioned 0.75 m in front of the
signaling males. In contrast, SPL of the two
recorded call-types clearly exceeded the
SPL of the environment (SPL x 6 SD 5
51.5 6 2.7 dB, n 5 15) at 0.75 distance
(Fig. 3).
TABLE 1.—Relative frequency (%) of call-type 1, call-type 2,
and exclusive visual signals given by focal males in relation
to closest conspecific individual under (a) nonmanipulated
conditions, and (b) during manipulated encounters under
experimental conditions.
Type of encounter
(a) Male-male
(a) Male-female
(a) Male-subadult
(a) Male-no other
individuals visible
(b) Male-male
No. of
males
No. of
signals
Calltype 1
Calltype 2
Visual
signal
31
19
24
641
188
190
0,15
0,18
0,23
0,08
0,78
0,20
0,77
0,04
0,57
51
28
1856
1106
0,52
0,17
0,29
0,08
0,19
0,75
22
HERPETOLOGICA
[Vol. 62, No. 1
FIG. 3.—Sonagram (above) and oscillogram, (below) of call-type 1 (A) and call-type 2 (B) of Phrynobatrachus krefftii.
Air temperature 20 C, water temperature 19 C.
Agonistic Behavior by Males
During the day, males signaled in shallow
water on rocks and from fallen branches within
their territory. Individual males (n 5 51) used
almost the same calling sites within their
territory in successive days throughout the
study period and returned to the marked
nocturnal resting site over a period of seven
nights (W. Hirschmann and M. Franzén,
unpublished data). No evidence of female
territorial behavior was observed. However,
females (n 5 30) returned to the same
nocturnal shelter over seven successive nights
(W. Hirschmann and M. Franzén, unpublished data). Males were observed attracting
females and actively hunting prey in the
vicinity of their calling sites. Males of P. krefftii
appear to have an acute visual sense of
movements. We observed males moving
quickly and highly directionally towards potential prey, such as small insects, three meters
away. When a territorial male perceived an
intruder, it turned to the intruder, assumed an
upright position, and started or increased vocal
sac inflations (Fig. 2) towards the conspecific
male. A maximum of nine visual signals was
performed consecutively without sound production. If the intruder had not retreated
after these signals, he was leaped upon and
chased away.
Over the course of 70 observed male-male
encounters, we registered 641 behavioral acts
performed by 31 individuals: 469 of these acts
(77%) were exclusively visual displays, 93 (15%)
were of call-type 1, and 52 (8%) were of
call-type 2. The mean duration of the soundless vocal-sac expulsions was 2.52 s (SD 5 1.49
s; range 1.44–6.64 s; n 5 11). Other behavioral
acts observed during agonistic interactions
included turning, approaching or jumping
away. During 21 observed male-female encounters, involving 19 males, acoustic displays
March 2006]
HERPETOLOGICA
23
FIG. 4.—Exclusive visual signaling (black bar) versus bimodal signaling (visual and acoustic) (gray bar) in
Phrynobatrachus krefftii under nonmanipulated and manipulated conditions. White bars: visual-signaling rate.
dominated significantly (x2 5 157.4, df 5 1,
P , 0.05). Call-type 2 (78%, n 5 147) dominated over call-type 1 (18%, n 5 33). With
only 8 out of 188 responses, visual signals did
not play a significant role in male-female encounters (Table 1). In 37 male-subadult encounters with 24 individual males involved, we
registered a total of 190 signals. Call-type 1
(23%, n 5 43) dominated over call-type 2
(20%, n 5 38). With 109 responses (57%),
visual signals were frequently used in malesubadult encounters (Table 1). Additionally,
we observed 51 males signaling without a
visible conspecific individual within the vicinity. Out of 1856 signals given without another
individual of P. krefftii obviously present, 353
(19%) purely visual signals (i.e., soundless
vocal-sac expulsions) were observed. We recorded 985 acoustic signals of call-type 1
(52%) and 88 displays of call-type 2 (29%) in
this context.
During our experimental introduction of
tethered males (n 5 15), all focal males (n 5
28) tested performed signals with vocal-sac
expulsions. Out of these 1106 signals, 825
(75%) were purely visual. Bimodal signals
were given at a rate of 25%, including 17%
of call-type 1 and 8% of call-type 2. Within
these staged male-male interactions, purely
visual signaling significantly dominated over
the bimodal signals (x2 5 267.6, df 5 1, P ,
0.05).
In male-male encounters, unimodal (i.e.,
purely visual) signaling under nonmanipulated conditions (77%) as well as in experimental manipulations (75%), significantly
exceeded bimodal signaling (Table 1, Fig. 4).
Calls (type 1 and 2 summarized) made up 23%
of the signals under nonmanipulated conditions and 25% in experimental manipulations,
respectively. In seven selected focal males, the
rate of exclusive visual signaling (0.57 signals/
min), however, was four times more frequent during the experimental manipulations than under nonmanipulated conditions
(0.13 signals/min).
Acoustic and Visual (Bimodal) Signaling
Due to the process of vocal-sac expulsion
during calling, each acoustic signal has a visual
component. Male P. krefftii produces two calltypes: Call-type 1 (1127 out of 1909 calls; Fig.
3) was most frequently recorded. It consists of
a single note, with a duration of 177–374 ms
24
HERPETOLOGICA
(
x 6 SD 5 268.0 6 66.3 ms; n 5 9). The
dominate frequency is 1.97–2.60 kHz (
x 6
SD 5 2.20 6 0.20 kHz; n 5 9). When other
individuals were absent or at least not visible to
us, 52% of the acoustic signals given consisted
of call-type 1. The mean SPL of call-type 1,
recorded at 0.75 m distance of vocalizing
individuals, measured 61.5 dB (SD 5 3.3 dB;
n 5 9) and thus exceeded the ambient SPL
by 10 dB.
Call-type 2 (Fig. 4) consisted of 4 to 6 notes.
The mean duration of call-type 2 was 950 ms
(SD 5 100.6 ms; range 842.2–1180.4 ms; n 5
7). The first note of call-type 2 lasted from
243–335 ms (
x 6 SD 5 278.7 6 31.8 ms; n 5
7) and possessed a dominant frequency at
2.075–2.52 kHz (
x 6 SD 5 2.31 6 0.14 kHz;
n 5 7) and thus resembles call-type 1. The
duration of the following notes is much
shorter: 34–47 ms (
x 6 SD 5 39.3 6 4.4 ms;
n 5 28), with a dominant-frequency range
between 1.92–2.575 kHz (
x 6 SD 5 2.20 6
0.24 kHz; n 5 28).
Each note was separated by an interval of
108.7–146 ms (
x 6 SD 5 123.8 6 9.6; n 5
27). The SPL of call-type 2 (
x 6 SD 5 62.9 6
1.8 dB; n 5 7) exceeded the ambient SPL by
11.4 dB.
DISCUSSION
Our results demonstrate evidence of unimodal visual signaling in P. krefftii and this
complements other studies that have demonstrated visual signaling behavior in several frog
genera (reviewed in Hödl and Amézquita,
2001). Consecutive expulsions of the vocal sac
without sound production significantly dominated male-male encounters. These results
indicate that visual signals have a distinctive
function in P. krefftii male-male agonistic
interactions.
During male-male agonistic interactions,
exclusive visual signals are more frequently
used than bimodal signals, both in the number
of interactions in which they occur and in
the number of behavioral acts within a single
interaction. The extensive use of purely visual
signals suggests that they are functional
components of the communication system;
this raises the question about their role in
communication and the evolutionary scenario
under which they evolved.
[Vol. 62, No. 1
From various studies of anuran acoustic
communication (Bogert, 1960; Duellman and
Trueb, 1986; Kluge, 1981; Rand, 1988), it
becomes apparent that social interactions have
favored the evolution of cross-species categories of signals. In addition to advertisement
calls, used both to attract females and to keep
competitors at a distance, at least two other
types of calls are known: aggressive/territorial
calls, and—in some species—courtship calls.
Aggressive calls are produced by frogs prior
to or during agonistic interactions. Unlike the
advertisement call, aggressive vocalization
often exhibits structural gradation that may
reflect the level of aggression (Wells, 1988).
We believe, however, that exclusive visual
signaling in P. krefftii does not support nonagonistic purposes, for we rarely observed
visual displays performed by individuals that
were not approached by a second adult male.
Visual signaling usually requires the presence
of another male. The possibility still remains
that purely visual vocal-sac displays function as
courtship signals that allow, for example, sex
recognition between males and females (Rand,
1988; Wells, 1977; Zimmerman and Zimmerman, 1988). For that purpose, further experiments including females of P. krefftii are
needed.
Advertisement calls often fulfill the dual
function of mate-attraction and territorial
defense. The advertisement call thus communicates not only the male’s reproductive state,
but also the readiness to defend the calling
site or mating territory. When the minimally
acceptable threshold distance is exceeded, the
resident enters into physical conflict with the
intruder.
Females of P. krefftii did not show aggressive behavior. However, females of Colostethus collaris, C. hermine, and C. marchesianus
(Dendrobatidae) exhibit a yellow slowly pulsating throat during aggressive bouts (Durant
and Doyle, 1975; Junca, 1998; Sexton, 1960).
Hödl (1991) discussed visual components of
the vocal sac and demonstrated in a film that
males of Epipedobates pictus at the Panguana
field site in Peru are easily detected at a large
distance due to conspicuous white dots on
their pulsating dark vocal sac. Bright yellow
gular markings which become visible during
vocal-sac expulsions in calling individuals of
members of the diurnal Dendrobates ventri-
March 2006]
HERPETOLOGICA
maculatus group, as well as in nocturnally
active Hyperolius species (f.e. Hyperolius
puncticulatus), also may serve to increase
localization by conspecific individuals (W.
Hödl, unpublished).
According to Wells (1977), prolonged
breeding favors indirect competition for
females. Males engage in signaling competition for the attention of females and may
defend territories around calling sites, courtship areas, or oviposition sites. A recent
playback study showed evidence that female
T
ungara frogs, Physalaemus pustulosus, significantly preferred advertisement calls accompanied by video playback of vocal-sac
inflation over calls presented with male frogs
without vocal-sac expulsion, and therefore
bimodal cues may play a key role in amphibian
mate choice (Rosenthal et al., 2004). Thus, in
that species, the female’s attraction to an
acoustic cue is modulated by the presence of
the inflated vocal sac.
The functional role of purely visual signals in
P. krefftii can be compared to the role of
aggressive calls. Since focal males performed
visual displays during all intrusion experiments, we interpret the soundless expulsion
of the vocal sac as a behavioral act that signals
an aggressive motivational state. Furthermore,
inflation of the vocal sac elicited visual displays
by interacting males. Calls of type 1 also were
produced after the intrusion of a male, but,
interestingly, we did not find any evidence
of a distinctive aggressive call in P. krefftii.
Instead, most males respond to intruders by
combining type-1 calls and soundless vocal-sac
expulsions, suggesting that visual displays may
functionally replace aggressive calls as a spacing mechanism (Amézquita and Hödl, 2004).
The use of tethered males in our experiments was initiated because we rarely observed agonistic displays during our field
study. All observed visual displays were given
at inter-individual distances below 30 cm.
Resident males performed both soundless
vocal-sac inflations and clearly audible calls.
Introduced males rarely performed vocalizations or purely visual signals, possibly because
we tied the frogs to the fishing-line with elastic
rubber bands around their waist. Inter-male
encounters are highly dominated by unimodal
visual displays, and soundless vocal-sac inflations are the prominently given signals at
25
a short distance. The Brazilian Torrent frogs,
Hylodes asper and H. dactylocinus will call
even when no rivals are present, while flagging
signals (with or without accompanying calls)
are given only once the presence of a rival is
detected, indicated by the defendant’s rapid
turn towards the intruder (Hödl et al., 1997).
The evolution of visual communication in
anuran species apparently has been favored by
the availability of ambient light, noisy environments, and highly structured habitats (Hödl
and Amézquita, 2001; Lindquist and Hetherington, 1996). Most frog species exhibiting
visual displays are diurnal. In P. krefftii, the
dorsal coloration does not contrast against
natural backgrounds. Amézquita and Hödl
(2004) discuss the possible importance of
visual signaling for communication in environments where acoustic localization of the
sender is hindered. Calling males were found
on the ground or on low perches between the
boulders of the creek-bed and the vegetation.
Under such conditions, sound propagation
may be reduced (Penna and Solis, 1998;
Richards and Wiley, 1980). Concealing coloration and highly structured environments may
reduce localization of senders to predators.
During this study we observed several vertebrates (e.g., mongoose, heron) as well as large
crabs preying upon P. krefftii. In spite of the
potential benefits as an anti-predator strategy,
calling from relatively hidden perches and dull
coloration reduces the localization of males to
potential conspecific receivers, which could,
in turn, lessen mating opportunities. Within
this scenario, the simultaneous production of
auditory and visual signals may increase the
sender’s localization at short distances, when
a conspecific receiver is detected.
River margins with shallow water, the preferred habitat of P. krefftii, provide constant
humidity, reducing the risk of desiccation
which supports diurnal activity. The combination of all these factors probably favored the
evolution of contrasting colors and dynamic
visual communication in P. krefftii. Due to
several global climatic changes in geological
history (Lovett, 1993), the annual amounts of
precipitation in the study area varies. It is
reasonable to believe that visual signaling
with the brightly colored vocal sac originally
evolved within a much noisier environment.
Highly eroded riverbeds near Amani spectac-
26
HERPETOLOGICA
ularly demonstrate higher amounts of rainfall
over the course of geological history.
The present study shows for the first time
that the anuran vocal sac can be used for
repeated signaling in males without accompanying audible sound production.
Acknowledgments.—We express our sincere thanks to
the Tanzania Commission for Science and Technology
(COSTECH) for allowing us to conduct fieldwork in
Tanzania. The field study was performed under the
auspices of S. Iddy and C. T. Sawe within the Amani
Nature Reserve. We are much indebted to the Tropical
Biology Association (TBA) and its director, R. Trevelyan,
Cambridge, U.K. for introducing us to the Amani Nature
Reserve during TBA field courses. We thank G. Msuya and
R. Killenga, the staff of the Amani Nature Reserve, for
their hospitality and assistance during our stay. The
drawings were done by H. Grillitsch. We thank K. Howell,
J. and S. Vonesh, E. Eder, H. Gasser, I. Lichtscheidl, P.
Narins, M. Svojtka, R. Zirbs and two anonymous reviewers
for their helpful comments and discussions. Financial
support was granted by the Austrian Science Foundation
(FWF, grant number P 15345), the Bureau of International Affairs, University of Vienna and by the Tropical
Biology Association, Cambridge, U.K. Printing costs were
financed through funds from the Austrian Science
Foundation project FWF P 15345 (principal investigator:
W. Hödl).
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Accepted: 11 August 2005
Associate Editor: J. Kelly McCoy
Herpetologica, 62(1), 2006, 27–36
Ó 2006 by The Herpetologists’ League, Inc.
PHENOTYPIC EFFECTS OF THERMAL MEANS AND VARIANCES
ON SMOOTH SOFTSHELL TURTLE (APALONE MUTICA)
EMBRYOS AND HATCHLINGS
MICHAEL A. MULLINS1
1
AND
FREDRIC J. JANZEN1,2
Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA
ABSTRACT: Temperature is a crucial factor in the development of oviparous organisms. Under natural
conditions, the eggs of many species are subjected to changing thermal environments, but most laboratory
studies have incubated eggs at constant temperatures. To evaluate the phenotypic effects of different thermal
means and variances and to separate temperature effects from maternal effects, eggs from 10 clutches of
smooth softshell turtles (Apalone mutica) were equally distributed among six temperature treatments that
reflect thermal conditions observed in natural nests: two eggs each at a mean of 28.5 or 32.5 C, with ranges
of 6 0, 2, and 4 C. In addition to embryonic traits (change in egg mass, hatching success, and incubation
length), we measured and evaluated body size, swimming performance, and righting time of the hatchlings. The
interaction between mean temperature and temperature fluctuation exerted a significant influence on eight of
the ten traits we measured, indicating that fluctuating temperatures do not have equivalent phenotypic effects
at different mean temperatures. Clutch of origin also was responsible for explaining a large fraction of the
variation for nearly all of the traits. Altogether, these results suggests that clutch effects are pervasive and that
thermal effects during embryonic development are complex and deserve further investigation.
Key words: Apalone mutica; Clutch effects; Eggs; Incubation temperature; Offspring; Turtle
PHENOTYPE is the end result of an amalgam
of genetic, maternal, and environmental
effects experienced by an embryo during its
2
CORRESPONDENCE: e-mail, fjanzen@iastate.edu
development (Ackerman, 1991). Due to the
combination of effects involved in the natural
development of a phenotype, describing
a physical trait in terms of a single causative
factor is difficult. In a laboratory setting,