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PACIFIC HORNED FROG: HUSBANDRY, REPRODUCTION AND DEVELOPMENT
151
Int. Zoo Yb. (2013) 47: 151–162
DOI:10.1111/j.1748-1090.2012.00193.x
Notes on husbandry, reproduction and
development in the Pacific horned frog
Ceratophrys stolzmanni (Anura: Ceratophryidae),
with comments on its amplexus
D. A. ORTIZ1, D. ALMEIDA-REINOSO2 & L. A. COLOMA2
Museo de Zoología, Escuela de Biología, Pontificia Universidad Católica del Ecuador,
Quito, Ecuador, and 2Centro Jambatu de Investigación y Conservación de Anfibios,
Fundación Otonga, San Rafael, Quito, Ecuador
E-mail: [email protected]
1
Aspects related to the natural history and behaviour of
the Pacific horned frog Ceratophrys stolzmanni were
investigated, mostly by observations under laboratory
conditions. Ceratophrys stolzmanni is a poorly known
species of horned frog (Ceratophryinae) that inhabits the
xeric environments of Pacific coast in Ecuador and Peru.
The species has been found only during the rainy season
in western Ecuador. Herein, techniques for husbandry
and reproduction, as well as reproductive and developmental features, are reported. Breeding was nocturnal
and clutches, which were laid on the same night as courtship, contained a maximum of 2100 eggs. Development
time (c. 27°C) from fertilization to hatching was 40
hours and metamorphosis was completed at 20–32 days.
The amplectant position of C. stolzmanni differs from
typical axillary amplexus of other anurans and may be
the result of the unique morphology of Ceratophryinae.
Data presented here are pivotal for captive-management
programmes related to conservation, education and
hobbyist activities.
Key-words: amplexus; Ceratophryinae; development;
Ecuador; husbandry; Pacific horned frog; reproduction;
tadpole.
Se investigaron aspectos sobre historia natural y comportamiento del sapo bocón del Pacífico Ceratophrys
stolzmanni, mayormente basados en observaciones bajo
condiciones de laboratorio. Ceratophrys stolzmanni es
una especie poco conocida de rana cornuda (Ceratophryinae) que habita los ambientes xéricos de la costa del
Pacífico en Ecuador y Perú. La especie ha sido encontrada
únicamente durante la estación lluviosa en Ecuador
occidental. Aquí se reportan técnicas de mantenimiento y
reproducción, así como características reproductivas y de
desarrollo. La reproducción fue nocturna y las puestas de
huevos, que fueron hechas la misma noche del cortejo,
contuvieron un máximo de 2100 huevos. El tiempo de
desarrollo (~27°C) desde la fertilización hasta la eclosión
fue 40 horas y la metamorfosis fue completada entre
20–32 días. La posición de amplexus de C. stolzmanni
difiere del amplexus axilar típico de otros anuros, y puede
ser el resultado de la morfología única de Ceratophryinae.
Los datos presentados aquí son esenciales para programas
de manejo en cautiverio relacionados a conservación,
educación y actividades de afición.
Palabras clave: amplexus; Ceratophryinae;
desarrollo; Ecuador; renacuajo; mantenimiento;
reproducción; sapo bocón del Pacífico.
INTRODUCTION
The genus Ceratophrys is a monophyletic
group from South America, which includes
(at the time of writing) eight formal species
(Frost, 2012). Monophyly of Ceratophrys
was recognized by morphological synapomorphies (e.g. Lynch, 1971, 1982; Fabrezi,
2006) and immunological analyses (Maxson
& Ruibal, 1988). Inter- and intrageneric relationships were hypothesized by Lynch (1982)
and Mercadal de Barrio (1986), but they are
not well supported (Fabrezi, 2006; Frost,
2012). The natural history and reproductive
biology of these frogs are known for species
such as the Ornate horned frog Ceratophrys
ornata (Basso, 1990) and the Amazonian
horned frog Ceratophrys cornuta (Duellman
& Lizana, 1994; Duellman, 2005), whereas
information about husbandry and breeding
of horned frogs is mainly available from
the hobbyist literature (e.g. Obst et al., 1988;
Int. Zoo Yb. (2013) 47: 151–162 © 2012 The Authors. International Zoo Yearbook © 2012 The Zoological Society of London
152
THE DEVELOPING ZOO WORLD
Hunziker, 1994), especially for the Ornate
horned frog C. ornata and the Chacoan
horned frog Ceratophrys cranwelli.
The Pacific horned frog Ceratophrys
stolzmanni Steindachner (1882) [snout–vent
length (SVL): 웧웧 = 48·4–67·9 mm (mean =
57·5; n = 20); 웨웨 = 53·1–82 mm (mean =
67·6; n = 19)] (Plates 1 and 2) is endemic to
xeric environments of the Pacific coastal dry
shrub and deciduous forest from Manabí
province, surrounding the Gulf of Guayaquil
(south-western Ecuador) to the Tumbes
department (north-western Peru), and is
known from an altitudinal range of 0–100 m
(Frost, 2012). Two subspecies were recognized by Peters (1967): Ceratophrys stolzmanni stolzmanni for Peru and Ceratophrys
stolzmanni scaphiopeza for Ecuador. Presumably, the species lives below ground when not
breeding and it is an explosive breeder during
the rainy season, with reproduction taking
place in water (Angulo et al., 2004). Ceratophrys stolzmanni is rare in nature and poorly
known because of its ecology (active only in
the rainy season). However, its Ecuadorian
populations may be declining as a result of the
destruction and fragmentation of coastal dry
forests. Until 2000, dry scrub comprised 53%
Plate 1. A. Juvenile 웨 Pacific horned frog Ceratophrys stolzmanni within its micro-habitat at Reserva Ecológica
Militar Arenillas, El Oro, Ecuador; B. calling 웧 C. stolzmanni in a terrarium; C. amplectant pair of
C. stolzmanni in a terrarium – note the arm position of the 웧; D. amplectant pair of Amazonian horned
frog Ceratophrys cornuta at Kaw mountain, French Guiana. A–C by Luis A. Coloma; D by Jean-Pierre Vacher.
153
Plate 2. Ontogenic variation of Pacific horned frog Ceratophrys stolzmanni tadpoles according to (Gosner, 1960)
stage system: A. hatchling at Stage 22; B. Stages 25–30; C. Stages 39–40; D, E. individually reared tadpole in
2009: D. Stage 42, 20 days after oviposition; E. Stage 44, 22 days. Note that tadpoles are not to the same scale. For
a more accurate indication of expected size, see Fig. 2. Luis A. Coloma.
and deciduous forest 27% of the original vegetation cover (Ron et al., 2011). The Pacific
horned frog was listed as Vulnerable (according to International Union for Conservation of
Nature and Natural Resources criteria) by
Angulo et al. (2004); nonetheless, its conservation status is in need of revision if additional
data were available.
Until recent times, the natural history and
reproductive biology of the Pacific horned frog
were little known because no detailed field or
laboratory observations have been conducted.
A captive-management programme for the
species began in 2007 at the ‘Life Raft for
Frogs’in the Pontificia Universidad Católica del
Ecuador for conservation purposes (Coloma
et al., 2010) and more recently at the Centro
Jambatu de Investigación y Conservación de
Anfibios for conservation purposes and for the
hobbyist industry (Wikiri, 2012). Here, techniques for husbandry and reproduction are
described, and features and behaviours related
to reproductive biology and development are
reported.
MATERIALS AND METHODS
Collection site and ecology
Adults and subadults of C. stolzmanni
[19.25 (웧웧.웨웨)] were collected at Reserva
Ecológica Militar Arenillas (REMA;
03°36′26″S, 80°09′01″W; 84 m), El Oro
province, Ecuador, between 31 January and 1
February 2007. Three juvenile 웨웨 were collected on 18 March 2011 at Destacamento
Pintag Nuevo, REMA, El Oro, Ecuador.
This protected area comprises the dry-forest
biomes of this eco-region and vegetation is
dominated by shrubs and deciduous trees
(World Wildlife Fund, 2012). In 2007, adults
were collected at 2100–0000 hours in and near
temporary ponds along a trail within the
forest. The forest was surrounded by grass and
deforested areas. Subadults were collected at
0000–0030 hours in a disturbed area with few
trees and furrowed soil. On average, daily air
temperature was c. 30°C and water temperature of ponds was c. 28°C. In 2011, juveniles
were collected at night in a marshy area
(Plate 1A) and at the margin of a pond for
ducks, close to human habitation. Collection
dates coincided with the rainy season which
extends from January to March (World
Wildlife Fund, 2012).
Laboratory maintenance
For adults, two kinds of terrariums were
used: one for maintenance (non-breeding)
and the other for breeding. For tadpoles, two
154
kinds of aquariums were used: one for maintenance and the other for complete metamorphosis (see Tadpole and froglet care section).
All were stacked on shelves inside a room
with controlled environmental conditions.
The daily light cycle was 12 hours (0630–
1830 hours) and room temperature was maintained at 25–30°C using electric heaters.
Maintenance terrariums Frogs were maintained individually in SmallWorld SW03
plastic terrariums (which were only large
enough to support one frog) and in small
groups of five to ten individuals in glass
terrariums (70 cm ¥ 40 cm ¥ 50 cm high).
The terrariums were filled with chlorine-free
water to a depth of 2 cm in plastic terrariums
and 5 cm in glass terrariums. The water was
covered with a false bottom (a plastic net over
a solid plastic grid, the latter elevated from the
bottom of the terrarium by pieces of styrofoam). This reservoir of water was advantageous for the maintenance of substrate
humidity. A layer of autoclaved and rehydrated Sphagnum sp moss was placed over the
false bottom, with leaf litter and plants
(Philodendron sp), to provide the substrate.
The substrate was c. 3–4 cm deep, which the
frogs require in order to burrow and blend in.
During initial assays, a gravel layer was used
as a substrate over the false bottom but the
frogs ingested the gravel while eating. Since
then, gravel has not been used as a substrate.
Terrariums were covered with a plastic grid in
the middle of two glass plates, which provided
aeration through the plastic grid and good
conditions of humidity. A fluorescent lamp
over the terrariums provided UVB light to
frogs. Substrate temperature was maintained
at 28·6–29·2°C and relative humidity was
65–75%. Frogs were fed three times a week on
a diet of 7 week-old crickets Gryllus sp assimilis complex, which were dusted with RepCal (calcium and vitamin D3) supplement
once a week. In addition, frogs were occasionally fed with Mealworms Tenebrio molitor
and baby Mice Mus musculus (pinkies).
Breeding terrariums The optimal arrangement consisted of glass terrariums, measur-
ing 70 cm ¥ 40 cm ¥ 50 cm high, filled with
chlorine-free water to a depth of c. 5 cm.
Large and flat rocks of c. 20–25 cm diameter
placed inside the terrariums let the frogs
climb above the water line. Water temperature was maintained between 27 and 30°C,
air pumps provided aeration and the terrariums were covered completely with two glass
plates.
Reproduction trials
General observations on reproduction were
carried out in 2007, 2008, 2010 and 2011.
Between February and April of 2009, ad
libitum observations (Altmann, 1974) were
conducted during six reproduction trials in
order to describe courtship, amplexus and
oviposition. Trials were carried out under different conditions (Table 1), but the same
kinds of rocks and aeration described earlier
for breeding terrariums were used. Frogs
were fed with crickets 1 or 2 days before
reproduction trials. Individuals for trials were
randomly selected from the plastic and glass
maintenance terrariums. Amplectant pairs in
maintenance terrariums were separated and
placed in breeding terrariums in order to
observe and describe their courtship. In
trial 6, a playback of the advertisement call
of C. stolzmanni was used. A Sony DCRTRV340 video camera was used to record (2
seconds minute–1 intervals) the activity of
frogs and egg development during day and
night, then the videos were analysed. Eggs
were measured using ImageJ 1·41 software.
Air and water temperature, and relative
humidity were recorded during the trials.
Tadpole and froglet care
When the oviposition was completed, adults
were removed from the breeding terrariums.
Neither eggs nor tadpoles were removed from
breeding terrariums until they reached Stage
25 (Gosner, 1960) (Plate 2B). To reduce problems caused by food competition and cannibalism, tadpoles were kept in groups of up
to ten individuals in 60 cm ¥ 30 cm ¥ 30 cm
high aquariums. In addition, a tadpole was
17:50/1070
16
Trial finished
33:05/1985
No record
Trial finished
88:19/5299
No record
Trial finished
No
No
No
06:34/394
60 ¥ 30 ¥ 30
10
25·5
26·5
50–59
P: 1.2
3
18:12/1092
No record
Individuals split up
No
No
Yes
10:02/602
60 ¥ 30 ¥ 30
9
26·3
30·1
50
P: 1.1
4
30:54/1854
2
Individuals split up
Yes
No
No
Not separated
60 ¥ 30 ¥ 30
9
25·9
26·8
49
P: 1.1
5
12:00/720
9
Clutch
70 ¥ 40 ¥ 50
6
28·9
28·8
68
P: 2.1
F1: 0.1
No
Yes
Yes
00:16/16
6
Table 1. Summary of reproduction trials for Pacific horned frog Ceratophrys stolzmanni in 2009: F1. filial 1 individuals from 2008 captive breeding; P. parents.
Number of observations corresponds to number of intervals (2 seconds minute-1) analysed from each video.
Yes
No
Yes
00:57/57
Yes
No
Yes
00:54/54
Amplexus previously in maintenance terrarium
C. stolzmanni playback
Vocalization of 웧 during courtship
Time since start of trial to amplexus (hours:minutes)/number
of observations
Amplexus duration (hours:minutes)/number of observations
Number of records of pressing reproductive behaviour
Fate of amplexus
60 ¥ 30 ¥ 30
11
25·5
25·5
50–59
P: 1.1
60 ¥ 30 ¥ 30
11
25·5
30
50–59
F1: 1.1
2
Terrarium size (cm ¥ cm ¥ cm high)
Level of water (cm)
Air temperature (°C)
Water temperature (°C)
Relative humidity (%)
Individuals (웧.웨)
1
TRIAL
155
156
reared individually to record its ontogeny.
Aquariums were filled with 27 litres of
chlorine-free water and water temperature
fluctuated between 25 and 29·4°C. Air pumps
provided aeration and water was changed
at 2 day intervals. Tadpoles (from Stage 25)
were fed with SAR II (Super Alimento Renacuajos type II for carnivorous tadpoles;
protein: 42·6%; humidity: 9·6%) and occasionally crickets were placed in the aquariums. Two glass plates (10 cm ¥ 15 cm),
smeared with SAR II and dried, were placed in
each aquarium twice a day. The Gosner (1960)
staging system was used to describe main
tadpole features. Tadpoles and juveniles were
measured using a Tresna EC05 digital caliper,
and juvenile frogs were weighed using a
Boeco BLC electrical balance. Tadpoles at
Stages 42–43 (forelimbs emerge) were placed
in aquariums with low water levels (c. 1 cm)
and rocks, to ensure that they did not drown
while completing metamorphosis. Then, tadpoles at Stages 44–45 (tail stub) were installed
in maintenance terrariums and fed with small
crickets and Mealworms. Cricket size was
increased according to frog growth. A halogen
lamp over the terrarium was used to provide
additional heat for juveniles.
RESULTS
Courtship
In all 2009 trials, the frogs (웧웧 and 웨웨)
were markedly active at night, moving and
swimming across the breeding terrariums.
During the day, the frogs were observed
resting on the rocks or in the water. In the late
afternoon and at night, the 웧 sat on the rocks
and began to vocalize strongly (Plate 1B) in
the direction of the 웨, which was in the water
(in trial 3, the 웧 amplexed the 웨 without
previous vocalization; whereas in trial 5,
individuals were already amplexed). A trial in
2011 with a large 웨 (SVL = 76 mm) and a
calling 웧 (SVL = 61 mm) ended with the 웧
dead because overnight the 웨 bit the hind
limb of the 웧 and he could not escape. The
advertisement call of 웧 C. stolzmanni was a
loud ‘baaaaa’ similar to those mentioned for
C. cornuta (Duellman & Lizana, 1994).
Advertisement calls during the courtship
were simple and occasional or in series with
a maximum of 48 calls recorded in 1 minute
47 seconds (trial 2). Silence intervals
between a series of calls ranged 10–20
seconds. A detailed description of this call is
not given because its physical and spectral
parameters under laboratory conditions and
at high altitude (2800 m) might show differences if compared to calls recorded in situ.
Amplexus occurred when the 웨 passed close
to the 웧, and he jumped into the water and
amplexed her. However, we could not determine whether the amplexus was the result of
an active response by the 웨 or it was an
opportunistic action by the 웧 when the 웨
casually passed near him.
Amplexus and oviposition
Males obtained amplexus in all 2009 trials.
The amplectant position was similar for all
pairs and is defined as ‘웧 clasps firmly on
both sides of the 웨’s anterior region of body
(at level of scapular region), with the dorsal
surface of his hands pressing underneath the
posterior angle of her mandible and with his
forearms pressing against the 웨’s suprascapular region’ (Plate 1C). If the 웨 was not
receptive or the required conditions were
not adequate, the amplectant pair remained
in amplexus for c. 2–3 days and then they
just split up or the trials were ended. A different, pressing reproductive behaviour was
recorded in 2009 during trial 2, trial 5 and
trial 6 during amplexus: while the 웧 was
climbing on the back of the 웨, he pressed
downward on the 웨’s head to submerge it
and the cloaca of each frog thus rose to the
water line (Fig. 1). This behaviour took 2–3
seconds and was recorded a maximum of 16
times during amplexus (Table 1).
Only trial 6 resulted in oviposition. In this
trial, some factors were different in comparison to the other five trials in 2009 (Table 1).
The clutch was laid in the early morning after
the courtship night. The amplectant pair swam
slightly in the terrarium during the night, then
they deposited multiple masses of eggs in the
157
Clutch and egg hatching
The clutch was a group of multiple egg
masses stuck to rocks and the terrarium
bottom. The clutch was laid on 16 April 2009
at 0040 hours and contained 2100 ⫾ 50 eggs,
with a non-viable portion of 17·5% (eggs
without any pigmentation and unusual
appearance). Additionally, one clutch was
obtained in 2008 (Almeida-Reinoso, 2008)
and eight clutches in 2010 with 200–780
eggs (Table 2). Mean egg diameter without
egg capsules was 2·11 mm (SD = 0·2; n = 15)
and the eggs had a dark-brown animal pole
and a light-cream vegetal pole. During development, the embryos rotated continuously
inside the egg capsule and hatching was produced by muscular contractions of embryos.
Egg hatching occurred at Stage 22, c. 40
hours after the clutch was laid, and it corresponded to an early hatching stage.
Development
Fig. 1. Sequence of pressing reproductive behaviour during the amplexus of Pacific horned frog
Ceratophrys stolzmanni. Pressing behaviour took
2–3 seconds and could be inducing oviposition.
water. Eggs were pushed away from the 웨’s
cloaca by both frogs gently using their hind
limbs, while both were moving across the
terrarium. Finally, the 웧 released the 웨 after
oviposition. No indication of parental care
was recorded after oviposition.
Tadpoles had a voracious appetite during
their entire development and the first food
was the mucilage capsules and the non-viable
eggs. For the 2009 offspring, metamorphosis was attained between 25 and 32 days
(mean = 29 days) at c. 27·2°C. The mean
number of days to complete metamorphosis
for the 2008 and 2010 offspring ranged from
20 to 32 days (Table 2). Tadpole total length
according to developmental time and Gosner
(1960) stage is indicated in Fig. 2 (see also
Plate 2). The individually reared tadpole in
2009 was the first to metamorphose (Stage
46); its growth was better than the tadpoles
reared in groups (both in size and time)
(Plate 2D,E). In the clutch, a single white
tadpole was found and it was reared individually. However, its development was slower
than the others and, at 44 days after oviposition, it was still at Stage 39. This tadpole did
not reach metamorphosis and died.
Juvenile frogs were measured at 44 days
after oviposition: weight averaged 12·58 g
(SD = 1·9; n = 15) and SVL averaged
42·86 mm (SD = 2·1; n = 15). The frogs were
then measured at 146 days after oviposition:
weight averaged 52·17 g (SD = 2·6; n = 12)
158
100
tadpole total length (mm)
100
A
90
90
80
80
70
70
60
60
50
50
40
40
30
30
20
20
10
10
B
0
0
0
5
10
15
20
25
16 22 25 26 27 28 29 30 31 32 33 34 35 36 37 39 40 42 43 44 45
30
Gosner stage
development time (days)
Fig. 2. A. Total length of tadpoles (n = 160) of Pacific horned frog Ceratophrys stolzmanni according to development time (from oviposition to metamorphosis) and B. according to development stage (Gosner, 1960) from the
clutch of trial 6 in 2009. Star symbol indicates hatchlings. Tadpole data are provided and discussed by M.
Morales-Mite (pers. comm.).
CLUTCH
YEAR
1
2
3
4
5
6
7
8
9
10
MEAN (SD)
2008
2009
2010
2010
2010
2010
2010
2010
2010
2010
WATER
TEMPERATURE (°C)
NUMBER
OF EGGS
METAMORPHOSIS
AT (DAYS)
29·7 ⫾ 1·1
27·2 ⫾ 2·2
26·8 ⫾ 0·5
27·2 ⫾ 0·3
27·1 ⫾ 0·1
26·7 ⫾ 0·3
26·3 ⫾ 0·1
26·7 ⫾ 0·1
26·0 ⫾ 0·6
26·0 ⫾ 0·8
27·0 (1·1)
NA
2100
300
400
200
500
780
700
550
450
664·4 (567·9)
20
29
22
22
23
23
29
25
28
32
25·3 (3·9)
Table 2. Number of eggs per clutch and mean number of days to complete metamorphosis (Stage 46: Gosner,
1960) for Pacific horned frog Ceratophrys stolzmanni tadpoles. All offspring were fed with Super Alimento
Renacuajos type II (SAR II): NA. no available data.
and SVL averaged 64·24 mm (SD = 2·4;
n = 12). From this information, the growth
rate for C. stolzmanni was established as
0·39 g day–1 and 0·21 mm day–1 during the
first 4 months of life (since metamorphosis)
under the captive conditions described. Eventually c. 60 metamorphosed frogs and c. 230
preserved tadpoles at various stages were
obtained for larvae description (M. MoralesMite, pers. comm.). Presumably, sexual
maturity was attained after about 1 year in
captivity, because F1 individuals (2008 offspring) were found in amplexus in maintenance terrariums.
DISCUSSION
Data presented herein suggest that C. stolzmanni possess ecological and reproductive
features similar to those reported for other
horned frogs. In nature, adult C. stolzmanni
were observed in temporary ponds only
during the rainy season; while under laboratory conditions, the presence of water in
breeding terrariums appeared to stimulate
activity and reproduction in the frogs. That
rainfall triggers the activity and breeding has
been reported for C. ornata in gallery forest in
Argentina (Basso, 1990), for C. cornuta in the
Amazon basin in Peru (Duellman & Lizana,
1994; Duellman, 2005), and for C. ornata and
the related Paraguay horned frog Chacophrys
pierottii and Lepidobatrachus spp in the
Chaco region and xeric plains in northern and
central Argentina (Cei, 1955, 1968). Hunziker
(1994) also mentioned that an increase of
water level in combination with hormonal
induction (luteinizing hormone-releasing
hormone) can be used to induce reproduction
in horned frogs in captivity. The activity of
C. stolzmanni was markedly higher at night
(in nature and during reproduction trials),
similar to C. ornata (Basso, 1990) and C. cornuta (Duellman & Lizana, 1994). During the
day, frogs were motionless in both breeding
and maintenance terrariums. In the latter, the
frogs were partially buried in the substrate
waiting to ambush prey. This behaviour
(ambush) seems to be a common foraging
strategy for sedentary predators such as
Ceratophrys (Duellman & Lizana, 1994),
although a behaviour involving a display for
luring prey has been reported for captive Venezuelan horned frog Ceratophrys calcarata
(Murphy, 1976).
Only one clutch (trial 6) was obtained from
the 2009 reproduction trials. Because there
were some differences between trial 6 and
trials 1–5 (e.g. terrarium size, use of playback
and presence of a second 웧), conclusions
about which factor(s) contributed to oviposition are limited. Additionally, the reproductive condition of the 웧웧 and 웨웨 was not
evaluated during selection of individuals for
trials. However, all 웧웧 attained amplexus
indicating that they were mature. On the
other hand, 웨웨 in trials 1–5 were probably
not mature enough and amplexus may only
have occurred opportunistically when the 웨
casually passed close to a 웧.
Water level could have contributed significantly to oviposition in trial 6. During the
eight reproduction trials in 2010, a water
level of c. 5 cm (similar to trial 6 in 2009)
was used, resulting in clutches for all trials. It
is probable that the 웨웨 need to be able to
reach the bottom of terrarium with their hind
limbs to maintain a stable position during
amplexus (Plate 1C), thus concentrating
159
energy expenditure on oviposition. During
trials 1–5 in 2009, the water level was excessive (> 6 cm) so the 웨웨 could not reach the
bottom of the terrarium and, therefore, during
amplexus, they spent the time swimming
desperately.
For future studies, it would be advantageous to evaluate one factor (variable) at a
time and include replicates for each trial, in
order to obtain more confident results. In addition, some external variables (e.g. barometric
pressure) should be recorded when reproduction trials in captivity are carried out, as
these may help us to determine whether these
factors contribute to breeding. However, on
the basis of the experiences and successes
attained, the features of the breeding terrarium
described herein (see Laboratory maintenance section) appeared to be optimal for
captive breeding of C. stolzmanni.
The pressing reproductive behaviour
during amplexus (Fig. 1) could produce
abdominal contractions in the 웨 as a signal or
stimulus to induce oviposition (Duellman &
Trueb, 1986). Because of the uncertainty of
the recordings (only 2 seconds per minute),
we could not obtain a more accurate frequency of this pressing behaviour; however,
the scant data here (Table 1) indicate that it
occurred during reproduction in captive
C. stolzmanni. However, the possibility that
this behaviour was learned rather than innate
remains. According to features of clutch,
larval development and type of habitat,
C. stolzmanni can be assigned to ‘reproductive mode one’ as defined by Duellman &
Trueb (1986), with eggs and feeding tadpoles
in lentic water. The clutch differed from
C. ornata, which laid isolated eggs (Basso,
1990) not forming masses as seen in captive
C. stolzmanni.
The ecology of tadpoles of C. stolzmanni is
similar to that in other horned frogs. The foraging mode was defined as ‘tadpoles grab a
prey item and with their massive jaw muscles
rip into it, tearing out a hunk’ [C. cornuta
(Duellman & Lizana, 1994), C. ornata
(Crump, 2000), C. cranwelli (Vera Candioti,
2005) and C. stolzmanni (this study)]. This
foraging mode is defined by morphological
160
features of the buccal apparatus (i.e. hypertrophied jaw muscles, terminal position of the
mouth, and strong and keratinized jaw sheaths
and keratodonts) correlated to a carnivorous
diet and tending to achieve a great suction
force inside the buccal cavity (Vera Candioti,
2005). For tadpoles of C. stolzmanni, competition, cannibalism and development could be
high in nature as a result of limiting factors,
such as fast-drying ponds and the availability
of aquatic food sources in those ponds
(e.g. invertebrates, algae and other tadpole
species). Cannibalism was also observed in
captivity by bigger tadpoles on those smaller
than themselves and also between juvenile
individuals, but it can be reduced with
adequate isolation and food resources (see
Tadpole and froglet care section). However, it
is recommended that tadpoles are reared individually. Like other members of Ceratophrys,
tadpoles of C. stolzmanni seem to be facultative carnivores in nature and they play an
important role in regulating the communities
in the temporary ponds where they develop
(Vera Candioti, 2005).
Development time from oviposition to metamorphosis was fast, averaging 25·3 days for
tadpoles of C. stolzmanni (Table 2), which is
similar to that reported for C. ornata (Hunziker, 1994). Therefore, development time for
captive horned frogs could be c. 20–30 days,
and mainly depends on water temperature and
food resources. Metamorphs of C. stolzmanni
at Stage 45 (tail stub) started to feed on an insect
diet. This behaviour seems to be unique to
members of the Ceratophryinae because most
captive-bred anurans reabsorb the tail completely before they start to feed. However, tadpoles of the related Lepidobatrachus spp feed
throughout metamorphosis because they
possess a digestive system similar to that of
adults and little reorganization occurs (Ruibal
& Thomas, 1988). After metamorphosis, juveniles of C. stolzmanni continued growing at a
high rate; but growth was higher in weight (0·39
g day–1) than length (0·21 mm day–1) for the first
few months under laboratory conditions.
This study confirms the importance of
captive-management programmes for the
knowledge of poorly known species, such as
C. stolzmanni, as well for the development of
ex situ protocols for conservation of threatened amphibians. However, further research
on this species must involve a complementary association between field and captive
studies. Field research is needed to determine
the current distribution and conservation
status in nature, seasonal population dynamics, and ecology of adults and tadpoles.
Besides, captive-management programmes
should focus on the viability of populations
in captivity, through genetic, pathological
and behavioural studies, to ensure an efficient
reintroduction of this species into its former
habitats in the future.
COMMENTS ON AMPLEXUS OF
C. STOLZMANNI
Amplectant position is recognized as an evolutionary trend passing from pelvic to axillary
amplexus (Tihen, 1965). Duellman & Trueb
(1986) defined three types of amplexus:
(1) pelvic: for ‘primitive frogs’, including all
archaeobatrachians, myobatrachids, some
telmatobiine leptodactylids and sooglossids;
(2) axillary: for most neobatrachians; (3)
cephalic: for some dendrobatids. Each one of
these types shows variation. These slight variations in clasping position probably reflect
selected modifications to increase fertilization economy and most anuran families
present a uniform type of amplexus (Lynch,
1971); however, individual genera may
deviate to a highly specialized degree (Tihen,
1965). Recent and more detailed descriptions
of amplectant positions interpreted in the
context of a phylogeny have added complexity
to the analyses of general trends within and
among clades of anurans (e.g. Castillo-Trenn
& Coloma, 2008).
Knowledge about the evolution of the
amplectant position in Ceratophrys is hampered by controversy regarding the relationships among Ceratophryidae subfamilies
(Frost, 2012), as well as the lack of detailed
descriptions of amplexus in most species of
Ceratophrys and other ceratophryines. Lynch
(1971) stated that Ceratophrys posses
axillary amplexus, which is common for
neobatrachians. However, it is relevant to note
that the amplectant position of C. stolzmanni
does not fit well, neither as axillary nor as
cephalic amplexus, because the main grasping
feature is related to the 웨’s shoulder and posterior jaw (Plate 1C). A similar position has also
been recorded in C. cornuta (Plate 1D). We
propose the name ‘neck amplexus’for this kind
of amplectant position because it does not have
grasping components related to the gular region
(e.g. cephalic amplexus of dendrobatids) or
armpits (e.g. axillary amplexus of Atelopus) of
the 웨 (see Amplexus and oviposition section).
This neck amplexus is determined by the robust
short arms in the 웧, which cannot attain an
axillary amplexus, and also by the macrocephalia and skull width of the 웨.
Whether the neck amplexus of C. stolzmanni is closely related, derived or ancestral
to axillary or inguinal positions remains to be
demonstrated when the phylogeny has been
better resolved. Considering an adaptive point
of view, this neck amplexus is an effective
position to ensure optimal grasping and oviposition in this species and could be result of
evolution of its morphology. Ceratophryinae
frogs indubitably have a particular body plan,
and skulls of Ceratophrys and Lepidobatrachus are the consequence of a wide divergence
from development patterns of the typical
anuran (Fabrezi, 2006; Fabrezi & Quinzio,
2008). This body plan also includes a
series of features with ecological, reproductive and evolutionary points of view. The neck
amplexus of C. stolzmanni could have been
evolved from an ancestral condition as a consequence of morphological changes during
the origin of the ceratophryines.
Although variations in amplexus position
seem be common for neobatrachians with
globular bodies where axillary amplexus is
not entirely possible (Duellman & Trueb,
1986), closer attention needs to be placed on
intraspecific, interspecific and outgroup variation of amplectant position in future studies
of reproductive biology of Ceratophryinae.
ACKNOWLEDGEMENTS
We are indebted to REMA personnel, who permitted
access to the military facilities and coordinated logistics
161
during our stay. Fernando Nogales, Italo Tapia and Elicio
Tapia assisted with field collections. Collecting, research
and management of C. stolzmanni were carried out
under permits FAU-001-DNB/VS, 008–09-IC-FAUDNB/MA, 2009-011-FAU-DPAP-MA and 03–2011FAU-DPAP-MA issued by Ministerio del Ambiente of
Ecuador. Manuel Morales kindly provided tadpole data
to elaborate Fig. 2. D.A.O. thanks Santiago Ron, who
provided access to equipment and to the collection in the
Museum of Zoology QCAZ, Pontificia Universidad
Católica del Ecuador. Morley Read generously reviewed
grammar and style in a preliminary version of the manuscript. Tatiana Armas helped to record data of the 2010
offspring. Eduardo Toral and Alejandro Janeta assisted
to elaborate Plate 1 and Fig. 1. Two anonymous reviewers improved this document with objectivity and criticism. This research was funded by Saint Louis Zoo, MO,
USA, and Pontificia Universidad Católica del Ecuador
(in 2010) and Wikiri SA (in 2011) in Ecuador. We are
greatly indebted to Jeff Bonner and Eric Miller (Saint
Louis Zoo) for their commitment and sustained support
for our research and the conservation programme for
Ecuadorian threatened frogs.
PRODUCTS MENTIONED IN THE TEXT
Boeco BLC: electric balance, manufactured by Boeco,
Hamburg 20422, Germany.
ImageJ 1·41: software for image processing and analysis in Java, developed by National Institutes of Health,
Bethesda, MD 20892, USA.
Rep-Cal: calcium and vitamin D3 supplement for
reptiles and amphibians, manufactured by Rep-Cal
Research Labs, Los Gatos, CA 95031, USA.
SAR II: Super Alimento Renacuajos type II, food for
carnivorous tadpoles, produced Diego Almeida-Reinoso,
Quito, Ecuador.
SmallWorld SW03: two-gallon plastic terrarium, manufactured by Penn Plax, Inc., New York, NY 11788, USA.
Sony DCR-TRV340: video camera, manufactured by
Sony Corporation of America, Sony Electronics, Inc.,
San Diego, CA 92127-1708, USA.
Tresna EC05: digital caliper, manufactured by Tresna,
Guilin, Guangxi Province 541004, People’s Republic
of China.
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- Wiley Online Library

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