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The courtship behaviour of the

Apalachicola dusky salamander,
Desmognathus apalachicolae Means & Karlin
(Amphibia Caudata Plethodontidae)
a
Paul A. Verrell
a
Department of Zoology , Washington State University , Pullman,
Washington, 99164, USA
Published online: 19 May 2010.

To cite this article: Paul A. Verrell (1994) The courtship behaviour of the Apalachicola dusky salamander,
Desmognathus apalachicolae Means & Karlin (Amphibia Caudata Plethodontidae), Ethology Ecology &
Evolution, 6:4, 497-506, DOI: 10.1080/08927014.1994.9522974

To link to this article: http://dx.doi.org/10.1080/08927014.1994.9522974

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 Ethology Ecology & Evolution 6: 497-506, 1994

The courtship behaviour

of the Apalachicola dusky salamander,
Desmognathus apalachicolae Means & Karlin
(Amphibia Caudata Plethodontidae)

PAUL A. VERRELL
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Department of Zoology, Washington State University, Pullman, Washington 99164,

USA

Received 18 September 1993, accepted 23 May 1994

This paper provides the first description of the courtship behaviour of the
plethodontid salamander Desmognathus apalachicolae. After a brief phase of
orientation of the male to the female, most courtship interactions consist of the
male stimulating his partner (in effect, “persuading” her to mate). Tactile stimuli
are produced by the behaviour patterns “head-rubbing” and “stroking”. Chemical
stimuli are provided by secretions from the male’s mental (= chin) gland, which
are transferred to the female by the behaviour patterns “snapping” and “pulling”.
Courtship ends with indirect sperm transfer by means of a spermatophore
deposited on the substrate. This phase is marked by a behaviour pattern known
as “tail-straddle walk”, exhibited only by plethodontid salamanders. A complete
understanding of the evolution of courtship behaviour in desmognathine sala-
manders awaits availability of detailed ethograms for all taxa currently recog-
nized. However, it appears that patterns of sexual incompatibility observed
among populations of D. apalachicolae and D. ochrophaeus may be explained, at
least in part, on the basis of similarities and differences in certain courtship
behaviour patterns.

KEY WORDS: Amphibia, salamanders, Plethodontidae, Desmognathus apalachico-

lae, courtship.

Introduction . . . . . . . . . . . . . . . . . 498
Materials and methods . . . . . . . . . . . . . . 499
Results . . . . . . . . . . . . . . . . . . 499
Ethogram of courtship behaviour . . . . . . . . . . 499
Temporal organization of courtship . . . . . . . . . . 501
Discussion . . . . . . . . . . . . . . . . . 502
Acknowledgments . . . . . . . . . . . . . . . . 504
References . . . . . . . . . . . . . . . . . 505
 498 P.A. Verrell

INTRODUCTION

As clearly stated by TINBERGEN (1963), the goals of ethology are to understand

the causation, development, function and evolution of behaviour patterns in ani-
mals. Central to this mission is the acquisition of complete inventories of all rele-
vant behaviour patterns. Indeed, detailed, quantitative ethograms were often the
primary goal of pioneering ethological studies.
Investigations of the evolution of behaviour patterns among closely-related spe-
cies have a long history. The oldest approach is exemplified by LORENZ’s (1941) classic
study of display evolution in ducks and geese, in which behaviour patterns were used
directly as taxonomic characters on a presence/absence basis (see also LORENZ 1950).
Later workers largely abandoned this approach, due in most part to the widespread
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assumption that behaviour patterns are too evolutionarily flexible to be useful phyloge-
netically (e.g., ATZ 1970). However, recent research suggests that behaviour patterns
may be no more subject to convergence or reversal than other phenotypic characters
used to construct phylogenetic hypotheses (DE QUEIROZ & WIMBERGER 1993).
Conceptual and technological advances in systematic and evolutionary biology
over the last 20 or so years have made available an alternative approach to under-
standing behavioural evolution. Ethologists now have access to detailed phylogenet-
ic hypotheses of ancestor-descendant relationships for many groups of animals,
often based on molecular data. The availability of such independent phylogenies
permits ethologists to optimize, or “map”, behavioural characters onto phylogenetic
trees and so obtain a more detailed understanding of ancestor-descendant changes
in behavioural evolution (e.g., BROOKS & MCLENNAN 1991, WENZEL 1992, GREENE
1994). Neontological studies may reveal details of the evolution of behaviour pat-
terns in the absence of any palaeontological record (see BOUCOT 1990).
Our understanding of the evolution of courtship behaviour in newts and sala-
manders (Amphibia Caudata) has largely rested on the “classic” approach in which
behavioural characters are themselves used to formulate phylogenetic hypotheses
(e.g., ARNOLD 1972, 1977; HALLIDAY 1977; HALLIDAY & ARANO 1991). However, our
ability to optimize behavioural characters onto independent phylogenies is fast
approaching as the systematics of the Caudata is explored from a molecular per-
spective (reviewed by LARSON & DIMMICK 1993).
Molecular approaches are proving especially fruitful in studies of salamanders
of the family Plethodontidae, an exclusively New World group except for a single
genus found in southern Europe (LARSON & CHIPPINDALE 1993). Two subfamilies are
recognized (WAKE 1966), one of which, the Desmognathinae, contains three genera
found in the Appalachian Mountains, Ouachita Uplift and Gulf and Atlantic Coastal
Plains of North America (CONANT & COLLINS 1991). Two of these genera, Leurogna-
thus (which is highly aquatic: MARTOF 1963) and Phaeognathus (which is highly ter-
restrial: BRANDON 1966), are monospecific and little is known about their natural
histories. The third genus, Desmognathus, consists of at least 12 species, varying
greatly in body size and tendency toward terrestriality (BRUCE 1991). Independent
research is currently underway to produce a molecular phylogeny for this subfami-
ly (T. TITUS, Washington University, MO: see TITUS 1992). One long-term goal of my
own research is to obtain detailed ethograms of courtship behaviour for all of these
desmognathine taxa, with a view to reconstructing the evolution of courtship by
optimization onto the independent phylogeny. This paper provides the first descrip-
tion of the courtship behaviour for one of these taxa, the Apalachicola dusky sala-
mander Desmognathus apalachicolae.
 Courtship behaviour of Desmognathus apalachicolae 499

MATERIALS AND METHODS

Subjects

Desmognathus apalachicolae is a medium-sized salamander found in the Chattahoochee

and Choctawatchee river drainages of Alabama-Georgia, and in the Apalachicola and Och-
lockonee river drainages of Georgia-Florida. It occurs in moist ravines and seepages, where it
spends the day hidden in debris and leaf litter. Salamanders emerge at night to forage and,
presumably, engage in courtship and mating.
The Apalachicola dusky salamander was formally diagnosed as a distinct species on the
basis of both morphological and electrophoretic data (MEANS 1974, MEANS & KARLIN 1989). It
most closely resembles populations of the mountain dusky salamander, D. ochrophaeus, from
the southern Blue Ridge Mountains. This similarity led MEANS & KARLIN (1989) to propose
that populations of D. apalachicolae originated from an ochrophaeus-like ancestor that
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migrated southward along moist river drainages during the Pleistocene.

Collection and maintenance

Salamanders used in the present study were collected from moist ravines in the vicinity
of Big Sweetwater Creek in Liberty County in the panhandle of Florida. Only sexually mature
individuals in reproductive condition were taken. Animals were transported in cooled con-
tainers to the laboratory where they were maintained at a temperature of approximately 15
°C on a natural (Chicago) photoperiod. Salamanders were housed individually in plastic shoe
boxes measuring 9 × 17 × 31 cm, with a damp paper towel as substrate and a crumpled damp
paper towel as a refuge. Each box contained two culture vials of Drosophila, which were
replaced frequently to ensure continuous access to food. Diet was supplemented with vita-
min-mineral dusted waxworms (lepidopteran larvae) when available.

Observation procedure

Complete courtship encounters resulting in spermatophore deposition were observed

April through May 1992 for nine male-female pairs produced from combinations of five
males and four females. No salamander was paired with the same partner more than once,
ensuring that each encounter consisted of a unique combination of individuals. Salamanders
were kept in solitary confinement for at least 3 nights between successive encounters. Encoun-
ters were staged in a Plexiglass observation arena measuring 17 × 17 × 5 cm, floored with a
damp paper towel (no refuge was made available). I introduced a single male and single
female at approximately 16:00 hr and left them together until 08:00 hr the following morning.
All interactions between partners were recorded under dim red illumination on a time-lapse
videotape recorder (Panasonic AG-6010), using a low-light video camera (Panasonic WV-
BD400).

RESULTS

Ethogram of courtship behaviour

Female actions

1. Move away: the female moves or turns away from the male as he approaches.
2. Move toward: the female moves or turns toward the male when he is in her
vicinity.
 500 P.A. Verrell

Male actions

1. Follow: the male moves after the female, either as she moves away from
him or when she is separated from him.
2. Approach: the male moves toward the female when she is stationary and in
his vicinity. The male moves more slowly in approach than in follow.
3. Butterfly: the male moves his forelimbs backward, raises them from the
substrate and then brings them forward and downward in a circular motion. But-
terfly usually involves the simultaneous movement of both forelimbs, although
asynchronous forelimb movements also are frequently observed.
4. Stroke: the male raises his forelimb which is closest to the female in what
appears to be a butterfly-like movement. However, he extends it and repeatedly
strokes it against the female in a series of rapid movements and in a more-or-less
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horizontal plane.
5. Nudge: the snout of the male contacts the dorsal or lateral part of the body
or tail of the female.
6. Head-rub: the male rubs the female’s head with his own head. Head-rub-
bing may occur with the male positioned beside or in front of the female. Two
types of head-rubbing are apparent: (i) cheek rubbing, in which the male rubs his
cheek against the female’s cheek in a more-or-less horizontal plane, and (ii) chin
rubbing, in which the male rubs the top of his head against the female’s throat
and chin.
7. Pull: the male presses his chin against the dorsum of the female (or, less
frequently, her tail) by bending his head downward. He then pulls his head back-
ward in one or more short strokes, keeping his chin in contact with the female.
8. Snap: the male presses his chin against the female’s dorsum by bending his
head sharply downward. He then draws his head backward in a sudden and rapid
movement of his whole body. This may be sufficiently forceful to flip the male sev-
eral centimetres away from the female.
9. Tail undulation: the male laterally undulates the whole length of his tail.

Combined male and female actions

Tail-straddle walk: the male slides his body under the head of the stationary
female until her chin is positioned on the proximal part of his tail and her fore-
limbs straddle the more distal part. The male then moves forward in a straight line,
undulating his tail laterally, and the female follows, remaining astride the male’s
tail. The male then ceases his forward movement, the intensity of his tail undula-
tions increases and he deposits a spermatophore on the substrate below his cloaca.
Immediately after deposition the male resumes his forward movement and the
female follows, still astride his tail. As he moves forward approximately one body
length in distance, the male swings his tail out from underneath the female and
holds it to one side. With the female resting her head on his tail-base, the male
then halts, and vigorously and repeatedly raises and lowers his pelvis and the prox-
imal part of his tail, largely by extending and flexing his hindlimbs. These move-
ments repeatedly raise and lower the head and forebody of the female, who also
generates rapid, lateral movements of her own pelvic area at this time. It is at this
point that the uppermost, sperm-filled cap of the spermatophore may lodge in the
female’s cloaca. The female then moves away from the male, who may turn back
and briefly follow her before losing interest.
 Courtship behaviour of Desmognathus apalachicolae 501

Temporal organization of courtship

As is typical in all other desmognathine salamanders which have been obser-

ved, the courtship of D. apalachicolae could be divided into three, more-or-less dis-
tinct and consecutive phases: orientation, persuasion and sperm transfer.
Orientation consisted largely of the male attempting to attain a position from
which he could stimulate the female both tactually and chemically. The male
repeatedly followed the female as she moved around the observation arena, or
approached her when she was stationary. The male often performed butterfly when
close to his partner, and frequently nudged her with his snout. The female usually
moved away when followed or approached, especially early in the orientation
phase.
The persuasion phase began when the female eventually ceased to flee from
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the male. The earliest stimuli produced by the male typically were tactile, resulting
from head-rubbing. Episodes of head-rubbing were often lengthy (in excess of 5
min), and consisted of both cheek- and chin-rubbing. Occasionally the male moved
posterior to the female’s head, delivered one or more pulls, and then returned to
head-rubbing. The male invariably butterflied while rubbing, often moving both of
his forelimbs simultaneously. However, instances of butterfly with just one forelimb
were common, and these almost always involved the forelimb closest to the female.
On many occasions this single, moving forelimb was extended and made clear
physical contact with the female, apparently stroking her head and neck.
If the female turned toward the male during rubbing, he often slid his body
forward under her chin with his tail undulating laterally. When the female’s chin
was resting on the dorsal surface of the base of his tail, the male usually curved his
body backward, toward his partner’s neck or dorsum, so that his body was in a C-
shaped position. Then, with his tail still undulating, the male snapped against the
female. Males also snapped when they were positioned alongside and more-or-less
parallel to the female. I observed a total of 29 individual snaps, most of which
(76%) occurred with the male in a C-shaped position. Until the female became fully
responsive (either remaining stationary or moving toward the male), she often
moved away from the male during the persuasion phase. When this occurred, the
male reoriented to the female so that he could continue stimulating her.
The sperm transfer stage of courtship was initiated when the male slipped
underneath the female’s chin, the female straddled the male’s undulating tail with
her forelimbs and the pair moved forward in tail-straddle walk (TSW: described in
detail above). Females exhibited rapid lateral undulations of their pelvic areas in
those encounters in which they remained with males after spermatophore deposi-
tion, perhaps “feeling for” the spermatophore below.
Males deposited single spermatophores during single episodes of tail-straddle
walk in all nine of the encounters observed, and insemination of the female was
successful in all but one encounter. In this latter encounter the female moved away
from the male just after he deposited his spermatophore.
The time elapsed from introduction of the partners to the start of orientation
by the male (defined as first follow or approach) was very variable (median = 169
min, range = 28-543 min). During this time the salamanders moved extensively
around the observation arena, but seemed unaware of one another’s presence. The
duration of the orientation phase of courtship, measured as the time from first fol-
low or approach to first period of head-rubbing, was short and varied little among
encounters (median = 15 min, range = 6-30 min). The persuasion stage of court-
 502 P.A. Verrell

ship, measured as time from first period of head-rubbing to the start of tail-strad-
dle walk (TSW), was of more variable duration than the orientation phase (median
= 51 min, range = 37-117 min), but was of longer duration in all nine encounters
observed. All episodes of TSW were of short duration (median = 5 min, range = 4-
7.5 min).

DISCUSSION

A detailed comparative study of courtship in salamanders of the genus

Desmognathus will not be possible until ethograms are available for all taxa pres-
ently recognized (work in progress).
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Table 1 summarizes information on courtship behaviour patterns for all taxa

of Desmognathus observed to-date, including D. apalachicolae. Here I briefly dis-
cuss some trends suggested by these incomplete data.
An invariant feature in courtship encounters of all Desmognathus observed to-
date is the use of tail-straddle walk to achieve sperm transfer. No obvious qualita-
tive differences are apparent among the species listed in Table 1. I predict that tail-
straddle walk will be found in all desmognathine salamanders, given that this
uniquely plethodontid behaviour pattern has been observed in members of all three
tribes of the subfamily Plethodontinae (SALTHE 1967, ARNOLD 1977).
Interspecific variability is most marked during the orientation and persuasion
stages of courtship. Jerky, to-and-fro movements are shown by males as they
approach females in both subspecies of D. fuscus, in D. santeetlah, and in some
populations of D. monticola (perhaps representative of intraspecific variation in the
latter species). However, I did not observe jerking in D. apalachicolae.

Table 1.
Courtship behaviour patterns in eight species of Desmognathus.

Behaviour patterns*

Species A B C D E F G H Source**

D. wrighti – + – + + – – + 1,2
D. aeneus – – – – + – – + 3
D. ochrophaeus – –+ – + – + + + 1,4,5,6
D. imitator – + – + – + + + 7
D. fuscus fuscus + + – + – + + + 1,4,5
D. fuscus conanti + + – + – – + + 8
D. santeetlah + + – + – – + + 9
D. monticola –+ + + + – –+ + + 1,4,10
D. apalachicolae – + + + – + + + 11

* A: jerk; B: movements of forelimbs; C: stroke; D: head–rub; E: bite–and–seize; F: pull; G: snap; H:

tail–straddle walk. ** 1: ORGAN (1961); 2: HOUCK (1980); 3: PROMISLOW (1987); 4: ARNOLD (1972); 5:
UZENDOSKI & VERRELL (1993); 6: K. HERRING (unpubl.); 7: VERRELL (in press a); 8: VERRELL (in press
b); 9: MAKSYMOVITCH & VERRELL (1992); 10: BROCK & VERRELL (in press); 11: Present study. + indi-
cates presence of behaviour pattern; – indicates absence of pattern, or pattern not reported; – +
indicates variable occurrence/reports.
 Courtship behaviour of Desmognathus apalachicolae 503

Males of all but one species examined to-date exhibit head-rubbing, although
choreographic details vary interspecifically. Head-rubbing usually occurs together
with forelimb movements. Butterfly-like movements of the male’s forelimbs appear to
be common in Desmognathus salamanders, although their occurrence varies intra-
specially in the D. ochrophaeus complex. Butterfly was first described by ORGAN
(1961) and later in more detail by ARNOLD (1972), with both authors reporting only
synchronous movements of the male’s forelimbs. Personal observations of butterfly in
D. ochrophaeus, D. imitator, D. fuscus (both subspecies), D. santeetlah and D. apala-
chicolae have revealed that males may also move their forelimbs asynchronously. Nei-
ther ORGAN (1961) nor ARNOLD (1972) reported contact of the male’s moving limbs
with the female’s body in their descriptions of desmognathine courtship. However, I
found such contacts to be very numerous and apparently “deliberate” in D. apalachi-
colae. For this reason I recognize a new behavioural category named stroking. This
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behaviour pattern appears to be absent in all other species examined except for D.
monticola (in which it is very conspicuous: BROCK & VERRELL in press). Stroking in
this species and in D. apalachicolae appear to be very similar in both form and con-
text, and must surely provide females with tactile stimulation.
The behaviour pattern named “bite-and-seize” has only been observed in the
dwarf species D. wrighti and D. aeneus, in which it is believed to be used to trans-
fer secretions produced by the male’s mental (= chin) gland (SEVER 1976). These
secretions have been shown to increase the rate at which females become fully sex-
ually responsive in D. ochrophaeus, and so may be regarded as courtship phero-
mones (HOUCK & REAGAN 1990). In all other taxa examined males use snapping to
transfer courtship pheromones. ARNOLD (1972) was the first to describe a behaviour
pattern that he called pulling, in which the male draws his chin backward against
the female’s dorsum (a much less abrupt action than snapping). Pulling is thought
to be yet another behaviour pattern used to transfer courtship pheromones, and is
variable in its taxonomic occurrence (Table 1).
Thus, the sexual behaviour of salamanders of the genus Desmognathus clear-
ly fulfills three of the functions of courtship proposed by TINBERGEN (1953): syn-
chronization and orientation between partners (in both time and space), and per-
suasion of the female to mate by the male. The latter is achieved largely through
the use of chemical cues (ARNOLD & HOUCK 1982, HOUCK 1986). Coordination and
persuasion are especially important in salamanders, with their intrinsically risky
mode of indirect sperm transfer (VERRELL 1988, 1989). The question of why spe-
cies differ in the exact behaviour patterns used to achieve these goals must be
deferred until courtship in the subfamily Desmognathinae can be viewed from a
truly phylogenetic perspective. Only then may it be possible to distinguish simi-
larities due to common descent (homology) from those due to independent evolu-
tionary events (convergence).
TINBERGEN (1953) proposed a fourth function of courtship. He suggested that
interspecific differences in courtship behaviour may reduce, if not prevent, deleteri-
ous matings among different species by promoting sexual incompatibilty (a phe-
nomenon often called sexual isolation). Although many contemporary systematists
would not use information on patterns of sexual compatibility to diagnose species
boundaries (e.g., CRACRAFT 1989), differences in sexual behaviour that result in
reproductive closure among taxa are of considerable interest to evolutionary biolo-
gists studying processes underlying population differentiation and speciation (OTTE
& ENDLER 1989; VERRELL in press c). It hardly needs to be said that detailed court-
ship ethograms are crucial if the behavioural basis of sexual incompatibility among
taxa is to be understood (VERRELL & ARNOLD 1989).
 504 P.A. Verrell

Table 2.
Gross similarities and differences in courtship behaviour between Desmognathus apalachicolae (from
Big Sweetwater Creek, Florida) and two populations of D. ochrophaeus (from Mount Mitchell,
North Carolina and Mount Rogers, Virginia: data are courtesy of K. HERRING).

Behaviour patterns*

Species A B C D E F G

D. apalachicolae – + + + + + +
D. ochrophaeus (NC) – + – + + + +
D. ochrophaeus (VA) – – – + – + +

* A: jerk; B: movements of forelimbs; C: stroke; D: head-rub; E: pull; F: snap; G: tail-straddle walk.

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+ indicates presence of behaviour pattern; – indicates absence.

As reviewed by MAKSYMOVITCH & VERRELL (1993), statistically significant levels

of sexual incompatibility have been detected in the laboratory at three levels in
Desmognathus salamanders: among conspecific populations, among allopatric pop-
ulations of different species and among sympatric populations of different species.
At the second level, VERRELL (1990) reported that D. apalachicolae from Big Sweet-
water Creek in Florida never mates with D. ochrophaeus from Mount Rogers in Vir-
ginia, but will mate in approximately seven out of every 10 encounters with indi-
viduals from a population of D. ochrophaeus at Mount Mitchell in the Blue Ridge
Physiographic Province of western North Carolina.
Data on similarities and differences in courtship behaviour can be used to
develop hypotheses concerning the behavioural basis of sexual incompatibility (VER-
RELL & ARNOLD 1989). Perhaps naively, one might predict the highest levels of incom-
patibility to occur among the most behaviourally-different populations. Table 2 sum-
marizes relevant data for the three salamander populations studied by VERRELL
(1990). All exhibit head-rubbing, snapping and tail-straddle walk, and none exhibit
jerking. Thus these four behaviour patterns appear uninformative with respect to the
basis of sexual incompatibility. Stroking seems unimportant regarding interspecific
mating, for it occurs in neither population of D. ochrophaeus. The data in Table 2 are
consistent with the hypothesis that forelimb movements and/or pulling may be cru-
cial behaviour patterns, with interspecific mating occurring only when they are
exhibited by both of the populations involved. Pulling involves the transfer of male
courtship pheromones to the female, and it is interesting to speculate that species
differences in pheromone quality/quantity may also contribute to sexual incompat-
ibility between Floridian D. apalachicolae and Virginian D. ochrophaeus.

ACKNOWLEDGMENTS

I am especially indebted to Stevan Arnold and Michael Blouin for collecting the sala-
manders used in this study, and to Lisa Diamond for expert animal care. I also thank Kimber-
ley Herring for discussion of intraspecific variation in D. ochrophaeus courtship and for
allowing me to include her data in Table 2. Part of this work was supported by a grant from
the National Science Foundation (BSR 89-06703 to S. Arnold and the author).
 Courtship behaviour of Desmognathus apalachicolae 505

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