Behavioral Ecology Vol. 9 No. 1: 1-7
Amphisexual parental behavior of a terrestrial
breeding frog Eleutherodactylus johnstonei in
Guyana
Godfrey R. Bourne
Department of Biological Sciences, Florida Atlantic University, Boca Raton, FL 33431-0991, USA
Parental care in Elmtherodactytus johwtonsi, a terrestrially breeding frog, was uniparentaL but care was provided by either sex.
I tested Maynard Smith's evohitionarily stable strategy, continuous breeding model HI, by ^ramining social and ecological
conditions under which die sexes provided parental care in Georgetown, Guyana, South America. During the long wet season
most males chosen by females as mates provided parental care. No males that acquired females through satellite behavior and
displacement competition provided care. Females provided parental care in most cases when males failed to do so, and some
returned to nests for 72 h, even after being repeatedly driven away by attending males. Females initiated maternal care up to
72 h after ovipoarion following temporary removal of males. Male-biased operational sex ratios were signtfirandy different for
wet and dry months, and no females provided care when monthly rainfall was <200 mm. Additionally, operational sex ratio
multiply regressed on paternal and maternal care and rainfall indicated that paternal and maternal care were significantly
correlated with operational sex ratio. Rainfall was not related to operational sex ratio. During the dryer months only males
provided care. Males provided less care during wetter months, when more gravid females were available as mates. Significant
mortality of eggs and embryos occurred in clutches with no parental care, and females and males did not differ in the ability
to protect progeny. Although there was support for Maynard Smith's model of evolution of amphisexual care from biparental
care, it was difficult to ascertain dearly whether amphisexual parental behavior evolved from either biparental behavior or no
care. This uncertainty ensues because the behavior of females and males and development of progeny may have become
coadapted after the initial evolution of care in E. johnstontL Key words: adaptive behavidr, amphisexual parental behavior,
EUiUherodadytus johnstorui, maternal care, paternal care, sexual selection, terrestrial frog. [Bthav Ecol 9:1—7 (1998)]
M
any anisogamous sexually reproductive animals provide
their progeny with postovipositional protection and/or
food (Lack, 1968; McDiarmid, 1978; Shine, 1988). However,
conflict over care of young affects the selective pressures acting on die sexes (Chitton-Brock, 1991; Parker et aL, 1972;
Reynolds, 1996; Trivers, 1972; Westneat and Sargent, 1996).
Maynard Smith (1978) and Houston and Davies (1985) modeled die effects of anisogamous conflict on patterns of parental care and found three outcomes: (1) neither parent provides care, (2) both parents share care because post-courtship
costs and benefits are similar for the sexes, or (3) one parent
compensates for the reduced care of the other. This third
outcome, facultative compensatory parental care, is exhibited
by many taxa (Chitton-Brock, 1991). Although Westneat and
Sargent (1996) found no studies in which the costs of compensatory parental care were determined, other empirical
studies suggest that increased parental care is costly because
it results in reduced future reproduction for individuals providing care (Lessels, 1991; Townsend, 1986). Parental compensation is, as Westneat and Sargent (1996) indicated, a
"best-of-a-badjob" dilemma, so that conflict-induced selection could favor the use of better alternatives. Additionally,
although studies of birds indicate successful alternative strategies to compensation (Slagsvold et aL, 1994; Viega, 1990),
observations of fish and amphibians suggest otherwise (Blumer, 1986; Durand and Vandel, 1968; Myers and Daly, 1983;
Vandel and Bonillon, 1959).
Because our understanding of die evolution of parental
C. R. Bourne is currently at (he Department of Biology, University
of Missouri-Si. Louis, St. Loui*. MO 63121-4499, USA.
Received 17 October 1996; revised 18 April 1997; accepted 10 May
1997.
1045-2249/98/J5.00 O 1998 International Society for Behavioral I cology
care is rudimentary, deciphering its subtleties has become an
important activity of some evolutionary biologists (ChittonBrock, 1991; Crump, 1995). This ensues because of the relationship of anisogamous reproduction to sexual conflict and
sexual selection and because of die differences in female and
male reproductive behaviors and parenting (Chitton-Brock,
1991; Parker et al., 1972; Reynolds, 1996; Westneat and Sargent, 1996; Williams, 1975). Differences between die sexes are
obvious in parental care among reptiles, birds, and mammals.
In these terrestrial taxa there is a pattern of either no male
care or a secondary role of paternal care (Chitton-Brock,
1991; Heiman, 1977; Lack, 1968; McXitrick, 1992; Tinkle and
Gibbons, 1977; Wittenberger and Tilson, 1980). This parental
care pattern also characterizes most non-anuran amphibians
(Crump, 1995; Nussbaum, 1985) and at least three anurans
(Bourne GR, unpublished data; Caldweu, 1997; Thompson,
1996), and contrasts with bony fishes, in which parental care
by males alone is more common than maternal care (Blumer,
1979; Chitton-Brock, 1991; Keenleyside, 1983; Perrone and
Zaret, 1979; Ridley, 1978), and most anurans (Crump, 1995;
Townsend, 1996; Wells, 1977, 1981). Uniparental care of eggs
and froglets or no care are characteristic of die Neotropical,
terrestrially reproducing, direct-developing frogs in die genus
Eleuthtrodactjhis (Crump, 1977; Schwartz and Henderson,
1991; Townsend, 1996; Townsend et aL, 1984). The sex providing die uniparental care differs in various species (Diesel
et al., 1995; Duellman, 1992; Duelhnan and Trueb, 1986;
Schwartz and Henderson, 1991; Townsend, 1986,1996; Townsend et al., 1984). Female attendance of eggs and froglets
(yiuti Crump, 1995; refers to die parent remaining with die
eggs or froglets at a fixed site) is associated with ground oviposition sites and is most commonly found in Jamaican (West
Indies) and continental species (Townsend, 1996). On the
other hand, male attendance is not associated with any spe-
Behavioral Ecology Vol. 9 No. 1
cdfic oviposition site but is strongly associated with the eastern
archipelago of the West Indies (Townsend, 1996).
Although many species of Eleuthtrodactylus are leaf litter
and cavity breeders, their natural histories offer biologists unlimited opportunities for studying functions and effects of sexual selection when problems of conducting continuous, unobstructed observations can be overcome. While studying the
reproductive ecology of the frog E. johnstonti by employing
modified planters with windows (Bourne, 1997), I noted that
some females provided care at some nests in a species that
also has male care (Beckwith, 1986; Townsend, 1996). According to dutton-Brock (1991), when desertion by one sex affects parental care by the other sex, game theory models are
appropriate for specifying the conditions under which maternal or paternal care are likely to evolve. Earner, Maynard
Smith (1977) developed an evolutionarily stable strategy
(ESS) hypothesis to account for situations where breeding is
continuous, individuals reproduce many times a year, and
there is pair formation with external fertilization. These conditions are exhibited by the reproductive biology of E. johnstotm (Bourne, 1997). Maynard Smith's (1977) continuous
breeding model m indicates that either maternal or paternal
care can evolve from either no care or biparental care. However, if no care is the initial state, then male care is more likely
to evolve when females do not provide care, because females
can produce additional clutches, and one parent attending
progeny is better than none, but two parents are not much
better than one. If the initial condition is biparental care,
then male abandonment is more probable when the absence
of males affects progeny survival less than the absence of females. I tested these predictions with observations and field
experiments to determine social and ecological conditions under which either sex provided parental care (i.e., amphisexual
care, stnsu Simon, 1983) in K johnstonti, primarily by focusing on the relative benefits of care.
METHODS
Subjects and study cites
Eltuthtrodactyhis johnstonti is a small, brownish member of the
Leptodactylidae. This frog is an island species native to the
lesser Antilles of the West Indies (Frost, 1985; Hardy and Harris, 1979; Schwartz and Henderson, 1991) that was introduced
unintentionally to Guyana at an unknown date (Frost, 1985;
Hardy and Harris, 1979; Lynch JD, personal communication). '
ElexUhtrodactyhts johnstonti adapted well to human habitation and is now abundant in urban areas of Greater Georgetown, New Amsterdam, and Linden, Guyana (Bourne, 1997).
In Guyana, individuals are highly iteroparous, with males siring 3.3 ±1.2 clutches and females producing 4.3 ±1.3 clutches
yearly; clutches contain 14±6 eggs on average and hatch into
froglets in 13.2±2.1 days (Bourne, 1997).
I studied parental care in E. johnstonti on two adjacent residential lots (06°48'78" N, 58°08'99* W; Magellan GPS navigator) in Queenstown, Georgetown, Guyana, from 8 May to
17 June 1988, 20 May to 16 June 1990, 14 May to 15 June
1992, and 28 May to 3 August 1994. A phenological study of
parental behavior was also conducted, and operational sex ratios (OSRs; Emlen and Oring, 1977; Kvamemo and Ahnesjd,
1996) were monitored at a residence in Albouystown
(06°48'10* N, 58°10'25" W) Georgetown, from 1 July 1995 to
30 June 1996 (ftouraa GR, manuscript in prccaraPpn).
Georgetown, the capital of Guyana, occupies 24 km* of eroded floodplain on the east bank of the mouth of the Demerara
River. Georgetown and coastal areas of Guyana usually experience two rainy seasons, a long season from mid-May to midAugust, and a short one from mid-November to mid-January
(Bourne and Osborne, 1978).
The primary Queenstown study site was 782 m1. The yard
was covered by grasses and sedges (66% coverage) and a herbaceous layer (32%) that was dominated by horticultural
plantings, especially Philodtndrvn ladniatum and Alocasia macrorhixa. These plantings were used by male E. johnstonti as
calling sites. Other members of the anuran community were
the aquatic breeding treefrogs, Sdnax rubra and Phrynohyas
vtnukaa, the leptodactylid, Ltptodactyhis fuscus, and die giant
toad, Bufb marmus (Bourne, 1997). The Albouystown site was
602 m1 and had 31 potted plants on shelves adjacent to the
house along its north wall.
A female initiates courtship with a railing male by making
physical contact; the male then leads her to one to four cavities for oviposition (Bourne, 1997). Male E. johnstonti have
access to several potential oviposition sites, and females "decide" about tile suitability of a given cavity after considerable
inspection; males have not been observed to attend nests with
more than one clutch (Bourne, 1997). I categorized male
frogs as "female chosen" {stnsu Bourne, 1993) when a female
approached and successfully amplexed and oviposited with a
vocalizing male in a nest cavity that was provided by the male.
Male-male competition as a mate acquisition tactic was defined as a successful fertilization of a crutch that resulted after
another amplexed male was displaced following physical
and/ or vocal combat. Males that bypassed female choice by
male-male competition were always vocally advertising individuals (Bourne, 1997). Clutch production with a small satellite male (SSM) occurred when a female that approached a
vocalizing male was followed into a cavity by the nonvocalizing
small satellite that was associated with die female's original
choice (Bourne, 1997).
General procedure*
I made observations and conducted experiments on individually tagged (Ryan, 1980) E. johnstonei using red-filtered highintensity flashlights and headlamps (Bourne, 1993). Frogs
were sexed by morphological criteria such as snout shape,
presence/absence of vocal sacs, vocal behavior, visibility of
eggs in die lower abdomen (Ovaska, 1991), and body size
(females 32.1 ±3.2 mm, males 23.8 ±2.4 mm long, snout-tovent length). Behavioral observations usually were made at 10
specially constructed observational planters (described below) . However, clutches were also located through systematic
diurnal searches of typical laying sites such as curled dead
leaves in leaf litter, root masses of orchids (Orchidaceae), rhizomes of hanging ferns (Poh/podiceae), or small chambers
under decaying logs, boards, coconut (Corns nuaftro) husks,
and rocks (Bayley, 1950; Blankenship, 1990; Bourne, 1997).
Clutches for which I had no history were aged according to
staging criteria (Bayley, 1950; Bourne GR, unpublished data;
Townsend and Stewart, 1985). To determine whether male
absence from die nest led to female parental care, I temporarily removed randomly female-chosen males (diey were released at die end of die experiment at die site of capture),
from 20 nests of varying ages (Bayley, 1950; Townsend and
Stewart, 1985) from May to August 1994 and documented
their fates. As controls, I observed 10 nests with males in attendance.
To ascertain whether rainfall was correlated with patterns
of OSRs and with paternal and maternal behaviors, I obtained
data on the phenology of parental behavior of individually
tagged frogs from 1 Jury 1995 to 30 June 1996 at die Albouystown residence. Males and females ready to mate (Emlen and
Oring, 1977; Kvamemo and Ahnesjo, 1996) and clutches were
Bourne • Parental behavior in terrestrial frogs
censused at weekly intervals on a randomly selected day, and
nightly observations were made for one week (randomly selected) each month. During these censuses and observational
periods, identification numbers and sexes of dutch-attending
frogs or of mating pairs during opposition were recorded.
Data on rainfall were recorded at the Queenstown residence.
All statistical tests were two-tailed, and I accepted p s .06
as stathficaDy significant. Descriptive statistics are expressed as
means ± 1 SD. All analyses were performed with the
GraphPad InStat version 2.0 package for Macintosh
(GraphPad Software, 1993).
Ob
al plant.
To study parental behavior of E. johnstonti, I constructed 10
observational planters using small Rubbermaid Design Planters measuring 150 mm highX155 mm top diameterXl20 mm
inside bottom diameter. Each planter consisted of a large outer pot with observation windows (acetate cells measuring
225X118 mm), and a small inner pot (plastic nursery planters
95 mm high X112 mm top diameterX76 mm inside bottom
diameter) to keep frogs awayfromthe interior recesses of the
outer pot and to keep them visible. Each inner pot was provided with a single dwarf canna, Carma mdica. A loose mixture of two parts orchid medium, one part medium-sized cobble stones, and one part sphagnum moss between the large
and small pots, leaving relatively large accessible spaces
(13±S/planter), served as oviposition chambers for the frogs,
especially dose to the windows (see Bourne, 1997:Figure 1).
The outside of each planter was draped with dark polyethylene sheets held in place by black plastic tape on the lips of
planters. The loose ends of these privacy shields were tucked
under the bottoms of planters to provide frogs with dark retreats and nest sites. I randomly distributed the 10 planters
among 18 established 1-m* quadrants on the southeast side of
the Queenstown residence. Each planter was situated in the
center of its assigned quadrant on a 60-cm high lumber pedestal. At the Albouystown residence, the same 10 planters were
similarly distributed among 12 quadrants on the north side of
the house. Frog occupancy of observational planters usually
began 36 h after the pots were set out
RESULTS
Natural history of parental care
Parental care by E. johnstonti in Guyana was uniparental by
either sex (Table 1) and was characterized by egg attendance
that began at opposition and lasted 1-8 days after hatching.
Both parents remained in the nest cavity with the eggs on the
first day after oviposition. During the long wet season (MayJune 1988), males that provided paternal care were all femalechosen individuals that had their nest cavities selected after
one or two inspections by the female (Table 1). Males attended dutches immediately after oviposition by staying on egg
masses after females moved out from under the males. Attending males also gave aggressive calls by 1830 h on the evening that the clutch was laid and bit the hind limbs of the
females; these aggressive behaviors usually drove the female
from the nest by dusk.
Males that did not provide paternal care (small satellite
males and larger competitive displacer males) sat to one side
in the nest chamber. They did not attempt to chase females
from the chambers at dusk but instead left to feed, rehydrate,
explore, and/or call. All females after oviposition, whether
driven from the nest or not, returned within 28-73 min (n «•
12) after foraging and/or rehydration and, if a male was not
present on the eggs, sat on clutches. Two attending males that
Table 1
Mate acquhldu tactic
b
p
of potential
nesti
indrvidaal female* before ovipositing, and the sex uiotkUug
parental o r e in terrestrial breeding frogs ElmHurodaetyba
je/mtto—i in Georgetown, Guyana, May-June 1988 and July 1995Junel996
Mating tactic*
FC
FC
FC
FC
FC
FC
MMC
MMC
MMC
SSM
Nests visited"
Parental
sex
Ps
1
M
M
M
F
F
F
F
2
3
1
3
4
1
2
3
2
F
F
F
No. of
occurrences
14
12
1
1
2
2
2
2
5
1
* FC female choice; MMC, male-male competition; SSM, small
satellite male.
b
Each male has access to several potential oviposition cavities and a
female chooses a nest site after inspecting a cavity of a particular
male (Bourne, 1997).
left the nest for periods of about 0.75 h returned to find females sitting on the dutches. Both males gave aggressive calls
and bit the females until the females left the cavities.
on survivorship of pjogeuy
Effect! of
Of the 20 nests where parental males were temporarily removed, females provided care at the 12 nests up to 3 days old
but showed no interest in the 8 nests more than 3 days old
(Fisher's Exact test, df - 1, p < .0001). At the 42 nests where
histories were known (Table 1), only three females returned
to nest cavities past the third day (fifth and sixth days) of
oviposition (x2 " 152.37, df - 3, p < .0001), and the 27 females that did not provide parental care eventually occupied
their premadng diurnal retreats. Nests older than 3 days
where tending males were temporarily removed went unattended and suffered high mortality (100% of the dutches,
93±2% of the eggs, n - 8 nests/109 eggs). Only males provided parental care to dutches in control nests (n ** 10 nests).
Furthermore, differences in progeny survival were not detected in nests attended by females (n - 15) or males (n 27; If = 214.5, p -.76) at the 42 nests where histories were
documented (Table 1).
The dominant activity of paternal and maternal care consisted of the adult sitting on the dutch, with its venter in contact with the uppermost eggs. Most of the clutch was covered
by the attending parent Obvious hydration occurred when
either maternal or paternal caregivers periodically moistened
dutches with dear fluid from their doacae (n •» 23). When
attending froglets after hatching, adult E. johnstonti elevated
themselves over the egg capsules to shield froglets that remained in a dump. I observed three sources of mortality in
1994. All eight unattended experimental dutches succumbed
to cockroadi (Blaberus spp. and PeripUxntta sp.) predation
(13%), desiccation (25%), and fungal growth (62%), which
began in unfertilized eggs and spread to eggs with developing
embryos. In situations where full nest histories were known
(Table 1; 42 clutches), nests with an attending parent suffered
little or no mortality (5%). Although not witnessed directly
during 1995-1996, embryo loss was attributed to invertebrate
predation. Unfertilized eggs in 39% of the dutches (n = 41
clutches) disappeared from nests with an attending parent I
Behavioral Ecology VoL 9 No. 1
Tablet
care (see Simon, 1983). To my knowledge, facultative compensatory maternal behavior of free-ranging amphibians is
known for only two odier anurans, E atticola (Lynn, 1937;
females, operational •ex ratios (OSJU), and numbers of parental'
Townsend, 1996) and Cophixahu parkeri (Simon, 1983), and
_ ties by i fof terrestrial breeding fiuca
for a caudate amphibian, the aquatic salamander, Proteus anEUmA*n>doctybBJ<</mittm*i bx Georgetown, Guyana, July 1995-Juue
guineus (Durand and Vandel, 1968; Vandel and Bouillon,
1996
1959). Amphisexual parental behavior is also known for other
anurans under captive conditions (Mudrack, 1969; Myers and
Rainfall Males/ OSR
Paternal Maternal No
Daly, 1983; SUverstone, 1976; Vaz-Ferrera and Gehrau, 1975;
Date
(mm)
Females (%)'
frogs
frogi
care
Woodruff; 1977; Zweifel, 1956). Males of many anuran spedes, including E johnstonei, are likely to provide parental care
Jun 1996
96
10
14
1
454
2V1
in association wim high confidence of paternity following ex95.7
11
11
2
May 1996
22/1
448
ternal fertilization of dutches (Chitton-Brock, 1991; Crump,
95.7
267
8
8
4
Novl995
22/1
1995; Dueuman and Trueb, 1986; Ridley, 1978; Wells, 1981).
95.7
8
10
0
Jan 1996
224
22/1
Males are also likely to be parental when females oviposit in
95.7
8
0
Jull995
11
223
22/1
Febl996
95.8
8
8
0
222
23/1
limited nest sites controlled by territorial males (Qutton6
0
1
Dec 1995
95
180
19/1
Brock, 1991; Crump, 1995; Huge, 1981; Wells, 1981). Both of
5
0
0
Mar 1996
77
12/1
92.3
these ecological correlates are present in the natural histories
Augl995
90.9
6
0
0
72
10/1
of E johnstontL On me odier hand, females usually provide
Apr 1996
0
2
0
1
34
0/1
care when they construct dieir own nests or when die nest is
Octl995
0/0
0
2
0
0
19
made of foam by the amplectant pair (Wells, 1981). Support
Sept 1995
0
0
0
2
12
0/1
for the prediction that either maternal or paternal care can
evolve from no care (Maynard Smidi, 1977) was equivocal be• OSR is the number of calling males/(calling males + gravid
cause, akhough males cared for die majority of dutches, fefemales) (Kvamemo and Ahnesjo. 1996).
males also provided care. However, individual females tend to
breed more often dian males in a given year (Bourne, 1997),
and because nests widi an attending parent suffered only 5%
found no gender differences in number of unfertilized eggs
mortality, two parents could not be much better than one at
that disappeared at parental-care nests (males: 1.67±0.71; feprotecting progeny.
males: 2^9±0.76 eggs, U' - 45J5, p - .14).
nnwiiniy fainiaii aiiaugeo ni aescenatoa; aimwnra,
A chi-square test of Tnariiniim likelihood comparisons of tbe
combined May-June 1988 and July 1995-June 1996 data sets
(Table 1) indicated that the sexes did not differ significantly
in providing care (\2 • 3.42, df = 1, p •* .06). Care differed
significantly among the three mating tactics of males that fertilized clutches (x 2 -33.85, df - 2, p< .0001), and a highly
significant association also existed between the tactics of mate
acquisition and the sex (Table 1) of the attending parent (x2
- 16.65, df = 1, p < .0001, Fisher's Exact test). Additionally,
the number of visits to potential nests was rignificantly associated with the sex (Table 1) of the attending parent (x 3 *•
16.87, df - 2, p - .0002), and a significant linear trend occurred among the ordered number of visits to potential nests
and the proportion of dutch-attending males (x 3 ™ 12.18, df
- 1, p - .0005).
The phenology of parental behavior relating monthly rainfall to the sex of an attending parent over a 12-month period
suggested that females were not associated with clutches when
monthly rainfall was <200 mm (Table 2). Additionally, rainfall
amounts conveniently separated into operationally wetter (>
200 nun/month) and drier (< 200 mm/month) periods,
each 6 months long (Table 2). The OSRs for wet and dry
months (wet 95.8+0.1 %; dry: 46.4+50.8 %, V » 36, p .0023, n " 6) were significantly different. Forward stepwise
regression analysis of appropriately transformed data of OSR
on the independent variables paternal (B = 10.42) and maternal care (B = —1.62) revealed significant linear relations
for paternal and maternal care (/"» 71.53, r*» .96, p < .005).
However, rainfall was not related to OSR (B =• - 0 3 4 , p «
.61).
DISCUSSION
Amphiaexaal pi
sntal behavior
These are the second detailed, quantitative observations of a
free-ranging frog species where either sex provided parental
Westneat and Sargent (1996) suggested that sexual conflict
over parental care ensues because females and males employ
different mating tactics. Thus, from die perspective of die potential reproductive rate paradigm (Andersson, 1994; ChittonBrock and Vincent, 1991; Kvamemo and Ahnesjo, 1996), lack
of parental care was more understandable in males diat bypassed female choice and employed alternative mating tactics—satellite or male-male competitive displacement behaviors (Andersson, 1994; Bourne GR, unpublished data; Ovaska
and Hunte, 1992). However, die proximate cue triggering
male parental desertion after alternative male mating tactics
were employed in mate acquisition may be lack of familiarity
widi die oviposition site. It is not dear why some female-chosen male E johnstonei abandoned parental duties. In most of
diese cases (Table 1) females mated widi die males only after
a diird or fourth visit to die males' controlled potential laying
sites. Female E johnstonei chose their mates in two stages: by
vocalization* and dien by die absence of direct contact with
soil in die potential nest cavity (Bourne, 1997). Some males
diat showed females more dian two cavities before being chosen as mates widiheld paternal care, thereby causing die females to protect their dutches (Table 1). Females reflected
conflict about parental care by initially returning to nests up
to 72 h after oviposition, just in case males abandoned their
eggs. It appears diat some male E johnstonei may widihold
paternal care because die costs to males for attracting additional mates may be relatively low (Andersson, 1994; Crump,
1995; Durand and Vandel, 1968; Gross and Shine, 1981;
Simon, 1983; Townsend, 1986; Wells, 1981). Use of an alternative tactic, diat of caring for multiple dutches was not observed. Thus, eidier males cannot care for more dian one
dutch at a time, or females do not mate widi males if they
aljoady attond-a dutch. Moreover, the coats to males attracting
anodier mate are further reduced because females are apt to
provide care when males fail to do so (Myers and Daly, 1983).
However, because female E johnstonei responded to male absence from dutches by exhibiting facultative brooding behavior, they were able to increase dieir own reproductive success
following dutch abandonment by dieir mates. Thus, amphi-
Bourne' Parental behavior in terrestrial frogs
sexual care b expected to evolve only if progeny survival is
enhanced when the other parent provides care following offspring abandonment by the "traditional" parent (Crump,
1995; Simon, 1983).
Reynolds (1996) suggested that sexual selection may influence parental care rather than vice versa, and my results confirm *hi» assumption. Even though individual mal^* and females did not provide parental care with each breeding bout
(Table 1), only males attended clutches and froglets during
the drier months (Table 2). Males were apparently sensitive
to variation in OSRs. The significant differences in OSRs during wetter and drier months and the fact that OSR was predicted by paternal and maternal care suggested that during
the drier months there were significantly fewer gravid females
and r^Kng males ready to mate (Table 2). Equivalent behavior is exhibited by a ticnKd fish HtrotUapia muttupmosa,
where .males forego parental duties when more gravid females
are available as potential mates (Keenkyside, 1983). Furthermore, advertisement calling by male anurans is energetically
expensive (Bevier, 1995, 1997; Schwartz et aL, 1995; Taigen
and Wells, 1985). Thus, the few males that mated during drier
months had to be efficient foragers and in good condition to
maintain the high call rates that females prefer (Bourne GR,
manuscript in preparation; Halliday and Tejedo, 1995; Lopez,
1996; Schwartz et aL, 1995). These dry-season breeders probably increased their reproductive success by providing care
i ^ of immediately seeking additional mating*
Many benefits attributable to parental care have been identified in diverse animal taxa (Blumer, 1986; CaldwelL 1997;
Qutton-Brock, 1991; Crump, 1995; Lack, 1968; McDiarmid,
1978; Shine, 1988; Tinkle and Gibbons, 1977; Wittenberger
and Tilson, 1980). In the anurans, individual frogs that sit on
clutches hydrate eggs through osmosis and/or reduce the rate
of water loss by decreasing exposed surface areas of dutches
(Crump, 1995; Taigen et aL, 1984). Frogs that conspicuously
wet their dutches by emptying their bladder contents onto
eggs not only hydrate them (Crump, 1995; Weygoldt, 1987;
Zimmermann and Zimmermann, 1984), but may inhibit phycomycete fungal outbreaks (Bayley, 1950; Beckwith, 1986). Although at least one eleutherodactyline spedes, E. planirostris,
has fungal-resistant eggs and no parental care (Coin, 1947),
many spedes of EUuthtrodactytus have eggs that are susceptible to fungal attacks (Diesel et aL, 1995). EUuthtmdactyhu
johnstonti is one such spedes; females take great care to avoid
cavities that have direct contact with soil (Bayley, 1950;
Bourne, 1997), probably because these conditions forititatc
fungal growth. I observed no cases of fungal outbreaks in
nests with an adult attendant; however, unattended dutches
with unfertilized eggs suffered high mortality of developing
embryos due to fungus that began growing on unfertilized
eggs before spreading to eggs with embryos, as described by
Simon (1983) and Diesel et aL (1995). The disappearance of
unfertilized eggs from nests with care may have been due to
parental removal or ingestion to minimi^ fungal growth
(Crump, 1995). Although invertebrate predation of E. johnstontCs eggs and froglets were witnessed (Bourne GR, personal observation), I did not observe conspecific egg predation
that Townsend et aL (1984) indicated was so prevalent in E.
coquL This study suggests that the presence of an attending
parent in E johnstonti served to protect dutches against desiccation, fungal pathogens, and invertebrate predators, because nests with parental care were more successful than nests
without care. Moreover, Maynard Smith's (1977) hypothesis
that either female or male care can evolve from biparental
care is supported, because male desertion was evident when
no sexual differences were found in survivorship of dutches.
Although I corroborated Maynard Smith's (1977) ESS hypothesis that biparental care is the initial condition from
which amphisexual parental care evolved in E. johnstonti, die
data also suggested that other functions and effect! (stnsu
Williams, 1966) may have influenced its parental behavioral
ecology. To speculate on the evolution of amphisexual behavior in E. johnstonti, I begin by evaluating Dawkins' and Carhse's (1976) idea that a female's investment in eggs could only
be replaced at great cost In E. johnstonti, time constraints on
breeding could delay dutch replacement for an average of 2.8
months (Bourne, 1997). Such time constraints on fecundity
could influence female participation in caregiving (Barlow,
1984; Blumer, 1986; Outton-Brock, 1991; Crump, 1995). However, such extreme investment by females in oviposition during a short time interval makes partial or complete termination of female parental investment a reality (Blumer, 1986).
According to Blumer (1986), this notion is contrary to the
idea that large replacement costs predispose a parent to continue investing in progeny (Dawkins and Cariise, 1976; Maynard Smith, 1977). Thus, in E. johnstonti the difference between die net benefits of nest attending and die net benefits
of leaving dutches to feed may be dose to zero for most females. Additionally, diis net benefit difference should vary depending on die sizes and reproductive histories of females
(Blumer, 1986; Outton-Brock, 1991; Crump, 1995; Wells,
1981) and might account for die variation I observed in compensatory maternal behavior in E. johnstontL
Although costs of parental care to males and females were
not measured for E. johnstonti in my study, paternal E. coqui
weight, condition, and fat bodies measurably decrease (Lopez,
1996; Townsend, 1986). The biological significance of these
costs—die effect of paternal care on male survival and future
reproduction—has not been determined (Townsend, 1986).
Males could avoid die costs of parental care by leaving soon
after oviposition (Blumer, 1986; Qutton-Brock, 1991; Crump,
1995), and several male E. johnstonti abandoned dutches they
fertilized on die first evening after oviposition. However, die
fact diat most males provided care suggested that die net benefits of abandonment were small compared to the net benefits
of paternal care. This cost-benefit model is similar to Maynard Smith's (1977) discrete breeding seasons model. In Maynard Smith's (1977) ESS model, die behavior of each sex depends on die number of progeny that survive when one or
bodi parents attend and on die probability of a deserting
adult finding a mate during die current breeding season. In
E. johnstonti, die benefits of abandonment were increased
feeding (Bourne GR, personal observation), and on die potential of increased future reproduction. The costs were
dutdi mortality and decreased current reproduction. The
benefits of paternal or maternal care were increased dutch
survival, and die costs are expected to be weight loss and its
consequent negative effects on survival and future reproduction (Blumer, 1986; Chitton-Brock, 1991; Crump, 1995; Townsend, 1986). Fungal growth was die major agent of dutch
mortality, and amphisexual parental care in £. johnstonti had
an antifungal function. Moreover, although males may be capable of replacing dieir current reproductive investment
more easily than females if abandonment resulted in dutdi
failure, enough males found odier gravid females during die
wet seasons to produce die pattern of abandonment during
die wet mondis only (Table 2).
Male E. johnstonti invested in their mate's progeny by at-
Behavioral Ecology VoL 9 No. 1
tending dutches, probably because the costs of parental behavior are envisioned to be small and the potential benefits
of leaving the clutch may also be small (Blumer, 1986; QuttonBrock, 1991). Also, the predisposition of males to remain with
their clutches is independent of female "decisions" to abandon or attend (Blumer, 1986; Qutton-Brock, 1991; Wells,
1981). A female is, as Blumer (1986) suggested, likely to behave differently, and female E. johnstorui behaved differently
in the presence or absence of her mate in the nest cavity.
Females I~an accrue considerable benefits from either parental
behavior or leaving, unlike males (Blumer, 1986; Townsend,
1986). The cost of clutch loss before the termination of parental care was probably greater for females than males. Females made the bulk of their investment early, during oviposition, whereas males invested in progeny more evenly
throughout this time span. Thus, brood loss is more likely to
occur before a male has fully invested in a particular clutch
but after a female has made most of her investment (ChittonBrock, 1991). A female is therefore in a "cruel bind" (struu
Dawkins and Carlise, 1976) when her mate abandons the
clutch (Blumer, 1986). Apparently, under these conditions,
female E. johnstorui assumed the parental care that I observed.
Although there is support for Maynard Smith's (1977) continuous breeding model, it b difficult to determine whether
observation and manipulation of current populations can reveal anything about the initial evolution of parental care
(Qutton-Brock, 1991). This is because parental behavior of
females and males and development of progeny may have become coadapted since initial conditions—biparental care or
no care (Chitton-Brock, 1991). Even though E. joknstontiwas
an ideal model species for a study of the evolution of amphisexual parental care, it is apparently too late to elucidate
antecedent conditions of the evolution of parental car without, perhaps, resorting to a comparative phylogenctic study
(e.g.. McKitrick, 1992).
I thank John and Peter Ferriera, Trica Forte (also for July 1999-June
1996 phonological data), and Oswald Frater for assistance in the field,
John D. Lynch for identifying voucher specimens (deposited at the
Museum of Zoology, University of Michigan), L. George Bourne (also
for rainfall data), the Gerald Frasers, and the late UU Nautb-Misir for
use of their properties. Debbie D. Boege provided technical assistance
and German translations, and the late John J. Boswell suggested the
chi-square test of linear trend. Teri C Bergquist, Carol M. Bourne,
Stan H. Braude, A. Chris Collins, James H. Hunt, Maureen A. Donnelly, and Seth Isenberg provided constructive comments. Comments
by referees Martha L. Crump and Tun R. Halliday and by Larry L.
Wolf improved the manuscript and are gratefully acknowledged. This
work was supported in part by three grants from Florida Atlantic University (FAU) Division of Sponsored Research, FAU Foundation Small
Grants Program, University of Missouri-St. Louis (UMSL) Research
Award, UMSL Set-up Grant, and personal funds. Preliminary studies
in 1984 and 1985 which influenced this study were supported by National Science Foundation grant RII-8307132. Data analysis and writing benefi tted from research leave funded by a University of Missouri
system research board grant
REFERENCES
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Barlow- OW, M84. Patterns of monogamy among teleost fishes. Arch
Fischer 35:75-123.
Bayley I, 1950. The whisding frogs of Barbados. J Barbados Mus Hist
Soc 17:161-172.
Beckwith P, 1986. A note on the whistling frog in captivity. Br Herpetol Soc Bull 17:34-36.
Bevier CR, 1995. Biochemical correlates of calling activity in neotropical frogs. Phvaol Zool 68:1118-1142.
Bevier CR, 1997. Breeding activity and chorus tenure of two neotropical hyiid frogs. Herpetologica 53:297-311.
Riank.ri.hip JR, 1990. The wildlife of Montserrat Montsemt, West
Indies: Montserrat National Trust.
Blumer LS, 1979. Male parental care in the bony fishes. Q Rev Biol
54.149-161.
Blumer LS, 1986. Parental care sex differences in the brown bullhead
Ictahmis ntbulosus (Pices, Ictaluridae). Behav Ecol Sodobiol 1 9 4 7 104.
Bourne GR, 1993. Proximate costs and benefits of mate acquisition
at lekt of me frog Olofygon mbra. Anim Behav 45:1051-1059.
Bourne GR, 1997. Reproductive behavior of terrestrial breeding frogs
EUuVurodactyfyj Johnston* in Guyana. J Herpetol 31:221-229.
Bourne GR, Oiborne DR, 1978. Black-bellied whistling duck utilization of a rice culture habitat Interciencia 3:152-159.
CaldweU JP, 1997. Pair bonding in spotted poison frogs. Nature 385:
211.
Glutton-Brock TH, 1991. The evolution of parental care. Princeton,
New Jersey: Princeton University Press.
Chuton-Brock TH, Vincent ACJ, 1991. Sexual selection and die potential reproductive rates of males and females. Nature 351:58-60.
Crump ML, 1977. The many ways to beget a frog. Nat Hist 8638-45.
Crump ML, 1995. Parental care. In: Amphibian biology: social behaviour, vol 2 (Heatwole H, Sullivan BK, eds). Chipping Norton, New
South Wales: Surrey Beany and Sons; 518-567.
Dawkins R, raHiii* TR, 1976. Parental investment, mate desertion
and a fallacy. Nature 262:131-133.
Diesel R, Baurle G, Vbgel P, 1995. Cave breeding and froglet transport: a novel pattern of anuran brood care in the Jamaican frog,
EUuVumdadyhu cundaOL Copeia 1995:354-360.
Duellman WE, 1992. Reproductive strategies of frogs. Sd Am 267:8087.
Duellman WE, Trueb L, 1986. Biology of amphibians. New \fort: McGraw-Hill.
DurandJ, Vandel A, 1968. Protnu. an evolutionary relict S d J 1968:
44-49.
Emlen ST, Oring LW, 1977. Ecology, sexual selection, and evolution
of mating systems. Science 197:215-223.
Frost D (ed), 1985. Amphibian species of the world. Lawrence, Kansac Association of Systematic Collections.
Coin CJ, 1947. Studies on the life history of EUutktrvdactjlus ricovda
plonimtris (Cope) in Florida. Univ Florida Stud Biol Sci Ser 4:167.
GraphPad Software, 1993. GraphPad insm mac version 2.0. San Diego, California: GraphPad Software Inc.
Gross MR, Shine R, 1981. Parental care and mode of fertilization in
ectothennic vertebrates. Evolution 35:775-793.
Halliday T, Tejedo M, 1995. Intrasexual selection and alternative mating behaviour. In: Amphibian biology: social behaviour, vol 2 (Heatwole H, Sullivan BK, eds). Chipping Norton, New South Wales:
Surrey Beatty and Sons; 419-468.
Hardy JD Jr, Harris HS Jr, 1979. Occurrence of the West Indian frog
EUutMtrodactytus Johnston*, in South America and on the Island of
Curacao. Bull Md Herpetol Soc 15:124-133.
Houston AI, Dovies NB, 1985. The evolution of cooperation and life
history in the dunnock Prunttta modularis. In: Behavioral ecology:
ecological consequences of adaptive behavior (Sibly RM, Smith RH,
eds) Oxford: BlackweU Scientific; 771-487.
Keenleyside MHA, 1983. Mate desertion in relation to adult sex ratio
in the biparental cichlid fish Hrrotilapia multispmosa. Anim Behav
31:683-688.
Kleiman DC, 1977. Monogamy in mammals Q Rev Biol 5239-69.
Huge AC, 1981. The life history, social organization, and parental
behavior of Hyla rostnitrgi Boulenger, a nest-building gladiator
frog. Misc Publ Mus Zool Univ Mich 160:1-170.
Kvarnemo C, Ahnesjd L 1996. The dynamics of operational sex ratios
and competition for mates. Trends Ecol Evol 11:404-408.
Lack D, 1968. Ecological adaptation for breeding in birds. London:
RKOTOCTL
Lessels CM, 1991. The evolution of life histories. In: Behavioral ecol-'
ogy: an evolutionary approach (Krebs JR. Davies NB, eds). Oxford:
BlackweU Scientific; 32-68.
Lopez PT, 1996. Mate selection in the Puerto Rican frog, EUiUhtrodactyha aquL In: Contributions to West Indian herpetology: a tribute to Albert Schwartz, vol 12 (Powell R, Henderson RW, eds). Ith-
Bourne • Parental behavior in terrestrial frogs
aca. New 'fork; Society for the Study of Amphibians and Reptile*;
241-250.
Lynn WG, 1937. Two new frogs from Jamaica. Herpetologica 1:8890.
Maynard Smith J, 1977. Parental investment: a prospective analysis.
Anim Behav 25:1-9.
Maynard Smith J, 1978. The evolution of sex. Cambridge: Cambridge
University Press.
McOiarmid RW, 1978. Evolution of parental care in frogs. In: The
development of behavior comparative and evolutionary aspects
(Burghardt CM, Bekoff M, eds). New York: Garland STPM Press;
127-147.
McKitrick MC, 1992. Phyiogenetic analysis of avian parental care. Auk
109-.828-846.
Mudrack W, 1969. Pflege und Zucht des Blansteigerfrosches der Gattung PhjOobatts au* Ecuador. Salamandra 5:81-84.
Myers CW, Daly JW, 1983. Dartpoison frogs. Sd Am 248:120-133.
Nusfbaum RA, 1985. The evolution of parental care in salamanders.
MUc Publ Mus Zool Unlr Mich 169:1-50.
Ovaska K, 1991. Reproductive phenology, population structure, and
habitat use of the frog EUuAirodactjhu jolmstonti in Barbados, West
Indies. J Herpetol 25:424-430.
Ovaika K, Hume W, 1992. Male mating tactics of the frog EinUhtrodactjhu johnstotui (LeptodactyUdae) in Barbados, West Indies. Herpetologica 48:40-49.
Parker GA, Baker RR, Smith VGF, 1972. The origin and evolution of
gamete dimorphism and die male-female phenomenon. J Theor
Biol 3&529-55S.
Perrone M, Zaret TM, 1979. Parental care patterns of fishes. Am Nat
113:351-361.
Reynolds JD, 1996. Animal breeding systems. Trends Ecol Evol 11:6872.
Ridley M, 1978. Paternal care. Anim Behav 26.-904-932.
Ryan MJ, 1980. Female mate choice in a neotropical frogs. Science
209^23-525.
Schwartz A, Henderson RW, 1991. Amphibians and reptiles of the
West Indies. Gainesville: University of Florida Press.
Schwartz JJ, Ressel SJ, Bevier CR, 1995. Carbohydrate and calling:
depletion of muscle glycogen and chorusing dynamics of the neotropical treefrog Hjla microaphala. Behav Ecol Sodobiol 37:125135.
Shine R, 1988. Parental care in reptiles. In: Biology of the reptilia,
vol 16 (Cans C, Huey RB, eds). New York: Alan R. Lin; 275-329.
Silventone PA, 1976. A revision of the poison-arrow frogs of the genus
PhjUobatts Blbron from Sagra (Family Dendrobandae). Nat Hist
Mus Los Angeles Co Sci Bull 27:1-53.
Simon MP, 1983. The ecology of parental care in a terrestrial breeding
frog from New Guinea. Behav Ecol Sociobiol 14:61-67.
Slagsvold T, Amundsen T, Dale S, 1994. Selection by sexual conflict
for evenly spaced offspring in blue tits. Nature 370:136-138.
Taigen TL, Pough FH, Stewart MM, 1984. Water balance of terrestrial
anuran EUuAtrodactjhts coqui eggs: importance of parental care.
Ecology 65:248-255.
Taigen TL, Wells KD, 1985. Energetics of vocalizations by an anuran
amphibian. J Comp Physiol 155:163-170.
Thompson RL, 1996. Larval habitat, ecology, and parental investment
of Osttopilus brunntus (Hyiidae). In: Contributions to West Indian
herpetology: a tribute to Albert Schwartz, vol 12 (Powell R, Henderson RW, eds). Ithaca, New York: Society for die Study of Amphibians and Reptiles; 259-269.
Tinkle DW, Gibbons JW, 1977. The distribution and evolution of viviparity in reptiles. Misc Publ Mus Zool Univ Mkh 154:1-55.
Townsend DS, 1986. The costs of male parental care and its evolution
in a neotropical frog. Behav Ecol Sociobiol 19:187-195.
Townsend DS, 1996. Patterns of parental care in frogs of die genus
EUuAtrodactjhis. In: Contributions to West Indian herpetology: a
tribute to Albert Schwartz, vol 12 (Powell R, Henderson RW, eds).
Ithaca, New York: Society for the Study of Amphibians and Reptiles;
229-239.
Townsend DS, Stewart MM, 1985. Direct development in EUuthmdaajtus txtqui a staging table. Copeia 1985:423-436.
Townsend DS, Stewart MM, Pough FH, 1984. Male parental care and
its adaptive significance in a neotropical frog. Anim Behav 32:421431.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual
selection and the descent of man (Campbell BG, ed). Chicago: Aldine; 136-179.
Vindel A, Bouillon M, 1959. La reproduction du protee (Prottus angimuus). Compt Rend Acad Sci Paris 248:1267-1272.
Viz-Ferreira R, Gehrau A, 1975. I. Anendon de la cria y acnvidade*
alimentarias y agresiva reladonades. Physu Secc B Aguas Cont Sus
Org 34:1-114.
ViegaJP, 1990. Sexual conflict in die house sparrow: interference
between polygynously mated females versus asymmetric male investment. Behav Ecol Sociobiol 27:345-350.
Weus KD, 1977. The social behaviour of anuran amphibians. Anim
Behav 25:666-693.
Wells ED, 1981. Parental behavior in male and female frogs. In; N a t
ural selection and social behavior recent research and new theory
(Alexander RD, Tinkle DW, eds). New York: Chiron Press; 184-197.
Westneat DF, Sargent RC, 1996. Sex and parenting: the effects of
sexual conflict and parentage on parental strategies. Trends Ecol
Evol 11:87-91.
Weygoldt P, 1987. Evolution of parental care in dart poison frogs (Amphibia: Dendrobatidae). Z zool Syst Evolut-forsch 25:51-67.
Williams GC, 1966. Adaptation and natural selection: a critique of
some current evolutionary thought Princeton, New Jersey: Princeton University Press.
Williams GC, 1975. Sex and evolution. Princeton, New Jersey: Princeton University Press.
Wittenberger JK, Tilson RL, 1980. The evolution of monogamy: hypodieses and evidence. Annu Rev Ecol Syst 11:197-232.
Woodruff DF, 1977. Male postulating behavior in three Australian
Pitudophyrn* (Anura: Leptodactylidae). Herpetologica 33:296-303.
Zimmermann E, Zimmermann H, 1984. Durch Nachtzucht erhalten:
Baumsteigerfrdsche DtndrobaUs quinquevittatus und D. nticulatut,
Aquar Mag 18(1):35-41.
Zweifel RG, 1956. Results of die Archbold Expedition no 72. Microhylid frogs from New Guinea with descriptions of new spedes. Am
Mus Novit 1766:1-49.