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THE REPRODUCTIVE ECOLOGY OF A RANID FROG COMMUNITY
IN POND HABITATS OF WEST JAVA, INDONESIA '

BY

DEAN BARRETTE PRENO

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Zoology

1985

ABSTRACT

THE REPRODUCTIVE ECOLOGY OF A RANID FROG COMMUNITY
IN POND HABITATS OF NEST JAUA, INDONESIA

BY
DEAN GARRETTE PREMO

This dissertation reports a year-long study of the
reproductive biology of five ranid frog species in
human-disturbed habitats of aseasonal west Java. Field
observations and laboratory dissections were conducted on
mw.&w.&m.
hm mdQQLLQQmeJJm-

Field observations revealed no seasbnal partitioning in
calling or mating behaviors. Genetic isolation was promoted
by temporal (over a 24-hour cycle) and microhabitat
partitioning, body size differences and distinctive mating
calls.

Dissections of monthly samples were performed. Sexual
size dimorphism was present in all species (females larger
than males). within the community, the possession of large
fat bodies was not related to size, sexual maturity,
reproductive readiness of females or time of year. External
secondary sexual characteristics of males were an accurate
indicator of sexual maturity. An interspecific positive
correlation existed between female body size and ovum

diameter when four of the five species were considered. An

intraspecific positive correlation between female body size
and ovum diameter existed in two of the species.
Intraspecific positive correlations between live weight and
ovarian weight were present in all five species. An
interspecific positive correlation between mean live weight
and mean ovarian weight was present.

Mean percent body weight contributed by ovarian weight
in reproductively ready females ranged from 6.5% to 11.7%
for the five species. This percentage was not significantly
correlated with body weight among the species. Mean clutch
sizes ranged from 434 to 13,611 for the five species. There
was a pattern of increased clutch size with increased,
species size. No seasonality in male or female reproductive
characteristics was observed.

Four of the five species had large clutch size when
compared to temperate zone Bang or Bornean tropical
rainforest Bang. Net reproductive rates for the west
Javan ranids are likely higher than those of their temperate
zone relatives. Indirect evidence suggested that females
produce more than one clutch per year. In view of their
reproductive characteristics, the five species were
relatively aligned on the 'r-K' selection continuum and
their position on this scale was considered in relation to
the zoogeographical range of each species. The degree of
'r' selectedness was not perfectly related to large.

geographic range among the species.

ACKNONLEDGEMENTS

Many people are due gratitude for their part in the
development, execution and completion of this study.
Special thanks are extended to Dr. SetiJati Sastrapradja,
Director of Lembaga Biologi Nasional, and Dr. Soenartono
Adisoemarto, Director of Museum Zoologicum Bogoriense, for
their advice, courtesy and friendship during my stay in
Indonesia. My days in the museum were made enjoyable by
many friends and colleagues there, especially Arie Budiman
and Pak Boeadi. Dr. Mohammad Eidman, Dean of Fisheries
Faculty at Institut Pertanian Bogor, granted permission to
work at the Darmaga Field Station and always displayed
interest in my work. My life in Bogor was greatly enriched
by the friendship and kindness of the Samsoedin family.

I am indepted to Robert F. Inger, Curator, Division of
Amphibians and Reptiles, Field Museum of Natural History for
valuable discussions during the planning stages of my
research and for the opportunity to view specimens at the
museum. Dr. Inger’s impressive contributions to the
herpetology of Southeast Asia were my constant reference.

Bruce Jayne offered valuable advice concerning
herpetological field work in the tropics.

I wish to thank J. A. Holman, C. D. McNabb, James

Edwards and M. M. Hensley for serving as my doctoral

committee and for their contributions to this work. Dr.
McNabb provided my wife and me with the opportunity to live
and work in Indonesia and gave us our first introduction to
the country. For the many and varied experiences that came
with our stay in west Java we will always be grateful to
him.

As chairman of my doctoral committee, Professor Hensley
demonstrated patience and provided friendship, moral support
and many hours of discussion.

Immeasurable quantities of support were offered by my
family and friends at 'home' through their frequent letters
and words of encouragement. To them, I offer deep thanks.

The greatest thanks is owed Dr. Bette J. Premo, my wife
and friend. Bette spent many hours with me discussing the
course of my research and commenting on techniques and
interpretations. She provided financial support throughout
this study, assisted in nearly every trip into the field,
constructed and typed tables, and critically reviewed

various drafts of the manuscript.

TABLE OF CONTENTS

LIST or TABLES . . . . . . . . . . . . . . . . . vi
LIST OF FIGURES . . . . . . . . . g . . . . . . x
INTRODUCTION . . . . . . . . . . . . . . . . . . I
DESCRIPTION or THE STUDY SPECIES . . . . . . . .

Bag; ghglggggtg (Schlegel) . . . . . . . .
Qggiggzzgg,llmg Kuhl and van Hasselt. . .
Ban; ggzthggga (Schlegel). . . . . . . . .
Ban; gangrivorg Gravenhorst. . . . . . . . 1

Rana llmgggngnig Boie. . . . . . . . . . . 11
DESCRIPTION OF THE STUDY SITES . . . . . . . . . 13

OOGO-B

Bogor Botanical Garden (BBS) . . . . . . . 18
Cibodas Botanical Park (CBP) . . . . . . . 21
Darmaga Field Station (DFS) . . . . . . . 23
METHODS AND MATERIALS . . . . . . . . . . . . . 25
RESULTS . . . . . . . . . . . . . . . . . . . . 30

Breeding habitat partitioning and
courtship behavior . . . . . . . . . . . . 30

Body size relations . . . . . . . . . . . 41
F.t bOdi .s I I I I I I I I I I I I I I I I 53
Male reproductive characteristics . . . . 62

Female reproductive characteristics . . . 70

iv

Seasonality of reproductive
characteristics . . . . . . . . .

DISCUSSION . . . . . . . . . . . . . . .
Reproductive biology . . . . . . .
Reproductive isolation . . . . . .
Reproductive potential . . . . . .
Natural selection and zoogeography

SUMMARY AND CONCLUSIONS . . . . . . . .

LITERATURE CITED . . . . . . . . . . .

109
I45
I45
I49
158
164
173
I78

LIST OF TABLES

Table 1. Habitat type and species assemblages
of the study sites. . . . . . . . . . . . . . . .

Table 2. Anuran species associations at each
’tUd)’ ‘i t.I I I I I I I I I I I I I I I I I I I I

Table 3. Matrix for species calling
sympatrically and synchronously. . . . . . . . .

Table 4. Monthly calling record for males
of the five study species. . . . . . . . . . . .

Table 5. Monthly calling record for males
of the five study species with reference . . . . .

Table 6. Shout-vent length data (in mm)
for mature frogs. . . . . . . . . . . . . . . . .

Table 7. Live weight data (in grams) for
mature frogs. . . . . . . . . . . . . . . . . . .

Table 8. Product-moment correlation between snout-
vent length (SUL) and live weight (Lw). . . . . .

Table 9. Relation between live weight and live
volume for the five study species. . . . . . . .

Table 10. Body size differences and body size
ratios between sexually mature males and females
of each species. . . . . . . . . . . . . . . . .

Table 11. Results of Mann-whitney tests checking
species differences of mean snout-vent length and
mean live weight for mature frogs. . . . . . . .

Table 12. Test results checking differences in
mean snout-vent length (SUL) between frogs with
large fat bodies (LFB) and those without (w/o LFB).

Table 13. Product-moment correlation results for

testis weight vs. testis length and testis weight
vs. calculated testis volume. . . . . . . . . . .

vi

Table 14. Mann-Nhitney test results for difference
between mean testis volumes of mature and immature

”.1.‘I I I I I I I I I I I I I I I I I I I I I I I I

Table 15. Egg diameter data (in mm) for all

ova ‘t.°.‘ I I I I I I I I I I I I I I I I I I I I I I .

Table 16. Nonparametric test results for comparisons
of ovum diameters between ova stages. . . . . . . . .

Table 17. Mean volumes (in cu mm) of the five
stages of ova and increase in volume from one
stage to the next. . . . . . . . . . . . . . . . . .

Table 18. Ovarian weight (in grams) for all
00. ’t.°.'I I I I I I I I I I I I I I I I I I I I I I

Table 19. Nonparametric test results for comparisons
of ova weights between ova stages. . . . . . . . . .

Table 20. Snout-vent length data (in mm) for ova
stage 1-5 females for the five study species. . . . .

Table 21. Nonparametric test results for comparisons
of snout-vent lengths among females of different
OVI ‘t.°.sI I I I I I I I I I I I I I I I I I I I I I

Table 22. Results of Mann-whitney tests for
differences in ovum diameter between species. . . . .

Table 23. Product-moment correlation analysis
of snout-vent length and ovum diameter of
stage 5 females. . . . . . . . . . . . . . . . . . .

Table 24. Left and right ovary weights (in
grams) for reproductively ready females. . . . . . .

Table 25. Product-moment correlation between live
weight (LN) and ovarian weight (ow) and between

live weight and percent live weight contributed by
ovaries (ZOO) in reproductively ready females. . . .

Table 26. Live weight in grams (LN), ovarian weight
in grams (0“) and percent live weight contributed by
ovarian weight <zow> in reproductively ready females.
Table 27. Results of Mann-Uhitney tests for
differences in percent live weight contributed by
ovaries (Z ovarian weight) between species. . . . . .

Table 28. Clutch sizes in females with countable ova.

vii

69

77

79

BI

82

B4

85

BB

91

93

94

97

9B
101

Table 29.

Table 30.

Results of Mann-Uhitney tests for
differences in clutch size between species.

Product-moment correlation between snout-

vent length (SVL) and clutch size (N of Ova) and

live weight (LN) and clutch size. . . . .

Table 31. Snout-vent length (SUL)
and live weight (LN)
countable ova. . . . . . . . . . . . . .

Table 32.
size factors (OSF) for the five species.

Table 33. Mean monthly testis volumes (in

mature male Qgglgglzgg 11mg, . . . . . .

Table 34. Mean monthly snout-vent lengths
mature male Qgglgglzg; llmg. . . . . . .

Table 35. Mean monthly testis volumes (in
mature male ggng limnggharig. . . . . . .

Table 36. Mean monthly snout-vent lengths
mature male Ran; limngchargg. . . . . . .

Table 37. Mean monthly testis volumes (in
mature male Egg; £gztngggg. . . . . . . .
Table 38. Mean monthly snout-vent lengths

mature male Bang ggztngagg. . . . . . . .

Table 39. Mean monthly testis volumes (in

mature male Bag; gaggglggga. . . . . . .

'Table 40. Mean monthly snout-vent lengths
mature male Egg; 5535212953. . . . . . .
Table 41. Mean monthly testis volumes (in

mature male Egg; gnalggggtg. . . . . . .

Table 42. Mean monthly snout-vent lengths
mature male 35;; ghglggnoga. . . . . . .

Table 43. Kruskal-wallis test results for

in millimeters
in grams of females with

Ovarian weight factors (OUF) and ovarian

cu mm) for

(in mm) for

cu mm) for

(in mm) for

cu mm) for

(in mm) for

cu mm) for

(in mm) for

cu mm) for

(in mm) for

differences

in mean monthly testis volumes and mean monthly snout-

vent lengths in mature males. . . . . . .
Table 44.

Table 45.
MI I I I I I I I I I I I I I I I I I I

viii

Monthly percentages of mature males. . . .

Mean monthly clutch sizes for Qgglgglzg;

102

104

105

110

111

112

113

114

115

116

117

118

119

120

124

126

128

Table 46. Mean monthly snout-vent lengths (in mm) for

female Qg;ldg;zgg,llmg with countable ova. . . . . .

Table 47. Mean monthly clutch sizes for Ban;
MI I I I I I I I I I I I I I I I I I I I I

Table 48. Mean monthly snout-vent lengths (in mm) for

female Bag; lflmnggnggls with countable ova. . . . . .

Table 49. Mean monthly clutch sizes for Egg;
”MI I I I I I I I I I I I I I I I I I I I I I

Table 50. Mean monthly snout-vent lengths (in mm) for

female Bang.;£zthgggg with countable ova. . . . . . .

Table 51. Mean monthly clutch sizes for Bang
MI I I I I I I I I I I I I I I I I I I I I I

Table 52. Mean monthly snout-vent lengths (in mm) for

female Bang Englggngtg with countable ova. . . . . .

Table 53. Mean monthly clutch sizes for Rang
MI I I I I I I I I I I I I I I I I I I I I I

Table 54. Mean monthly snout-vent lengths (in mm) for

female 353; gaggglggng with countable ova. . . . . .

Table 55. Kruskal-wallis test results for differences
in mean monthly clutch sizes and mean monthly snout-
vent lengths of females with countable ova. . . . . .

Table 56. Monthly values of number of mature females
(N mature), number of reproductively ready females

(0 repro) and percent of reproductively ready females
(2 repro) for all species. . . . . . . . . . . . . .

Table 57. Summary of reproductive isolating mechan-
isms for species by species combinations. . . . . . .

Table 58. Comparison of predicted and observed
CIUtCh "2.’I I I I I I I I I I I I I I I I I I I I I

Table 59. Correlates of 'r' and 'K' selection
(from Pianka, 1978) and characteristics of the
five study species. . . . . . . . . . . . . . . . . .

:29
130
131
132
133
134
I35
136

137

141

143

155

161

166

LIST OF FIGURES

Figure 1. Location of Java in Southeast Asia
(from Bartstra and Casparie, 1975). . . . . . . . . .

Figure 2. Mean monthly rainfall and temperature
(Fontanel and Chantefort, 1978), total monthly
rainfall and mean monthly maximum-minimum
temperatures (1983-84) for Bogor, west Java. . . . .

Figure 3. Mean monthly rainfall and temperature
for Cipanas, Nest Java (data from Fontanel and
ChIHtIfort, 1978) I I I I I I I I I I I I I I I I I I

Figure 4. Total monthly rainfall and monthly mean
maximum-minimum temperatures for Darmaga Field
StItIOh (‘983-84)e e e e e e e e e e e e e e e e e a

Figure 5. Temporal aspects of advertisement calling
behavior including time of commencement, peak period
(broad portion of trace) and time of completion for
each 24-hour observation bout. . . . . . . . . . . . .

Figure 6. Average time of commencement, peak period
(broad portion of trace) and time of completion of
advertisement calling behavior for the five study
species. . . . . . . . . . . . . . . . . . . . . . .

Figure 7. Means (vertical lines), ranges (horizontal
lines) and 95% confidence intervals (horizontal bars)
of snout-vent length of male and female frogs. . . .

Figure 8. Distribution of large fat bodies (LFB)
across size classes of male frogs of the five study
‘p.CI.‘I I I I I I I I I I I I I I I I I I I I I I I

Figure 9. Distribution of large fat bodies (LFB)
across size classes of females of the five study
.p'Ci.‘I I I I I I I I I I I I I I I I I I I I I I I

Figure 10. Percent frogs with large fat bodies in
matures and immatures of both sexes for the five
study species. . . . . . . . . . . . . . . . . . . .

Figure 11. Percent reproductively ready and non-
reproductively ready mature females with large
f‘t bOdi.’I I I I I I I I I I I I I I I I I I I I I

I4

19

22

22

40

42

46

54

55

5B

60

Figure 12.

Figure 13.

Size-frequency distributions of mature
and immature males of the five study species.

Distribution of testis volumes for

mature and immature males of the five study species.

Figure 14.

Figure 15.

lines) and 95% confidence
rectangles) for ovum diameters of the five ovum

stages.

Figure 16.

Figure 17.

Size-frequency distributions of mature
and immature females of the five study species.

Means (vertical bars), ranges (horizontal
intervals (horizontal

Relationship between mean ovum diameter
and mean snout-vent length for stage 5 females of the
five study species.

Relationship between mean live weight and
mean ovarian weight of reproductively ready females

(ova stages 4 and 5) for the five study species.

Figure 18.

Relationship between mean live weight and

mean clutch size for the five study species.

Figure 19.

Relationship between ovum size and clutch

size for the five study species.

Figure 20.
(vertical

Lime- -
Figure 21.

mn r
Figure 22.
(vertical

SIOELLEQCI-
Figure 23.

122102311-

Monthly means (horizontal bars), ranges
lines), and 95% confidence
(vertical rectangles) for testis volume and monthly
mean snout-vent length (upper line) for Qggigggzg;

Monthly means (horizontal bars), ranges
(vertical lines), and 95% confidence
(vertical rectangles) for testis volume and monthly
mean snout-vent length (upper line) for Bang

Monthly means (horizontal bars), ranges
lines), and 95% confidence
(vertical rectangles) for testis volume and monthly
mean snout-vent length (upper line) for Bag;

Monthly means (horizontal bars), ranges
(vertical lines), and 95% confidence
(vertical rectangles) for testis volume and monthly
mean snout-vent length (upper line) for gang

xi

intervals

intervals

intervals

intervals

64

68

71

76

90

96

106

108

121

121

122

123

Figure 24. Monthly means (horizontal bars), ranges
(vertical lines), and 95% confidence intervals
(vertical rectangles) for testis volume and monthly
mean snout-vent length (upper line) for Rang

gnglggngtg. . . . . . . . . . . . . . . . . . . . . .

Figure 25. Monthly means (horizontal bars), ranges
(vertical lines) and 95% confidence intervals
(vertical rectangles) for clutch size for Qggigggzgg

11mg. . . . . . . . . . . . . . . . . . . . . . . . .

Figure 26. Monthly means (horizontal bars), ranges
(vertical lines) and 95% confidence intervals
(vertical rectangles) for clutch size for Ban;

llmngghgglg. . . . . . . . . . . . . . . . . . . . . .

Figure 27. Monthly means (horizontal bars), ranges
(vertical lines) and 95% confidence intervals
(vertical rectangles) for clutch size for gang

inglggggtg. . . . . . . . . . . . . . . . . . . . . .

Figure 28. Monthly means (horizontal bars), ranges
(vertical lines) and 95% confidence intervals
(vertical rectangles) for clutch size for Egg;

Ir: thrllsI I I I I I I I I I I I I I I I I I I I I I I

Figure 29. Monthly means (horizontal bars), ranges
(vertical lines) and 95% confidence intervals
(vertical rectangles) for clutch size for Bag;

Slug? ngse I I I I I I I I I I I I I I I I I I I I I

Figure 30. The relationship between ovum size and body
size in some frogs (from Salthe and Duellman, 1973),
including the five study species. . . . . . . . . . .

Figure 31. Range of Qgglggzzga lime.
Figure 32. Range of Bag; gangrigorg. . . . . . . . . .

Figure 33. Range of Ban; gn5lggngta. . . . . . . . . .
Figure 34. Range of Bag; ggztngggg. . . . . . . . . .
Figure 35. Range of Ban; 11mgggngglg. . . . . . . . .

xii

123

138

138

139

139

140

147
168
168
169
169
170

INTRODUCTION

In west Java, several species of ranid frogs co-occupy
pond and flooded rice field habitats. The basic question of
this research was: what reproductive isolating mechanisms
and reproductive biology differences among these frogs allow
them to coexist in apparently homogeneous environments? To
answer this question, four species of Bag; and one species
of Qgglggzzgg (Family Ranidae) were examined in their
natural habitat and by laboratory dissections.

The great biotic diversity in the world’s tropical
areas has evoked much scientific interest. Java is a
tropical island that is heavily impacted by humans and their
agriculture. This has resulted in decreased diversity of
the biotic communities, including the anurans. The pond
frog communities of Nest Java are composed of species that
have tolerated human activities. In fact, some of the frogs
have prospered in conJunction with humans. Scott and
Campbell (1982) predict that future herpetological community
studies will inevitably be more concerned with anthropogenic
effects and will focus on such areas as the impacts of
habitat simplification. In the scramble to study the anuran

fauna of the remaining pristine tropical areas, communities

2

of anurans living in close association with humans have been
neglected. This study focused on such a community.

West Java is an aseasonal wet tropical area and
conditions favorable to anuran reproduction prevail
year-round. This study was based on data collected over a
complete annual cycle, from October 1983 to October 1984.
Previously, year-long studies of anuran reproductive biology
in the Asian tropics number only eight: Alcala (1962) and
Brown and Alcala (1970) (Philippine Islands); Berry (1964)
(Singapore); Inger and Greenberg (1963) and Inger and Bacon
(1968) (Borneo); Church (1960a,b) (Java) and Zeller (1960)
(Java). Of these studies, only Inger and Bacon (1968),
Berry (1964) and Alcala (1962) studied the reproductive
biology of a community of frogs; all others were studies on
single species. Other anuran community studies in Asian
tropics have examined community organization in relation to
environmental gradients or competition (Brown and Alcala,
1961; Inger, 1969; Inger and Colwell, 1977; Inger and
Greenberg, 1966). Studies with a community approach to the
reproductive biology of frogs in other tropical localities
are also rare, with Crump (1974), Caldwell (1973) and Bowker
and Bowker (1979) being noteworthy contributions.

Five species of ranid frogs were examined to ascertain
their reproductive coadaptations for life together in
disturbed pond habitats. Seasonal, temporal and spatial
breeding habitat partitioning and reproductive isolating

mechanisms were investigated through field observations.

3

Dissection of monthly samples of males and females allowed
examination of: (1) body size relations, (2) fat body
occurrence, (3) sexual maturity, (4) testis size and
relation to maturity, (5) ovum and ovarian characteristics,
(6) reproductive readiness in females, (7) clutch size and
(8) seasonal aspects of reproductive characteristics. This
information led to a consideration of the species that
departed somewhat from the general reproductive patterns and
an interpretation of anti-mating and courtship isolating
mechanisms. Further, the reproductive potential of the west
Javan species was compared to Bornean rainforest ranids and
temperate ranids, and the relative position of these frogs
on the 'r-K' selection continuum was outlined along with its

relation to the zoogeography of each species.

DESCRIPTION OF THE STUDY SPECIES

Five species of frogs in the family Ranidae were
studied. A description follows along with a brief review of
the published ecological literature for each species.

Unless otherwise cited, the morphological descriptions
follow Inger (1966) with some additional information from

the present work.

Bag; ghglggngt; (Schlegel)
Adult Egg; gnalggggt; have a slender body and legs.

The head is triangular and has a pointed snout and a
conspicuous tympanum. The fingers and toes are dilated into
distinct disks with the disks of the outer fingers at least
twice as wide as the phalanges. The toe disks are smaller
than those of the outer fingers and the web reaches the
disks on the outer edges of the first three toes and on the
inner edge of the fifth toe. The fourth toe has one or two
phalanges free of the broad web. Both an inner and outer
metatarsal tubercle are present.

The dorsal skin of B, gnalggngta is granular and a
dorsolateral skin fold is present although sometimes
obscure. Several small glands occur behind the rictus. A

supratympanic skin fold is absent. The skin of the

4

5

posterior half of the abdomen is granular or rugose, but the
rest of the venter is smooth.

The color of live individuals is yellowish green to
brownish green on the dorsum and cream colored on the
venter. The ventral surfaces of the thigh, groin and tibia
are reddish. The upper lip and glands behind the rictus are
white or yellowish.

The most obvious sexually dimorphic character of B,
gnglggngta is size. Adult females are much larger than
males, often four to six times the mass. The tympana of
males are visibly larger than those of females and males
have paired subgular vocal sacs. The nuptial pads in males
are clusters of yellowish spinules on the mediodorsal
surface of the first finger.

The species occurs from peninsular Thailand to Java,
Bali, and Celdbes (Mertens, 1930).

The published literature on the ecology of 3,
511.115.932.11 is quite mug... It is an inhabitant of
small streams in primary forest and secondary growth and
around swampy areas at edges of clearings (Berry, 1975;
Dring, 1979; Grandison,1972; Inger, 1966). Berry (1975)
observed that it is the upland ecological counterpart of
Ban; gazinggga, but gave no data for support. Inger
(1966) stated that E; ghglggnotg is most abundant below.
300 meters elevation but has been recorded up to 900 meters
in Borneo. Inger (1966) further reported that females with

enlarged pigmented ova were collected in all months from

6

April to August. In a study of community organization of
frogs along small rainforest streams in Sarawak, Inger
(1969) classified 3; ghglggngta as a riparian species

with strong clumping tendencies and found that the maximum
distance from the streambed that adults occurred was ten to
twenty feet. Liem (1971) reported that, in contrast to the
Bornean forms which are forest dwellers, Javan B,
ghglggnota do not occur in forests except in UdJung

Kulon. On Java, the species is found in vegetation up to
1.5 meters high and occurs from sea level to 1500 meters
(Liem, 1971). Liem (1959) studied the breeding habits of
this species in Bandung, West Java, from January to July of
1958. He found eggs were laid in a thin surface layer on
water, but never out of water. This refuted Dunn’s (1928)
statement that‘fi, gnglggggtg lay their eggs out of water

on vegetation; In conjunction with Schistma’s (1932)
findings of tadpoles in Bogor, Java, from October to
January, Liem (1959) concluded that eggs are laid in Java_
throughout the year. Liem (1959) also gave data on clutch

size and egg diameter.

Qggiggzzga,llmg Kuhl and van Hasselt
Members of the species Qggiggzzgg lima are small

aquatic frogs with a maximum size of about 39 mm. The
tongue is elongate and extensively free (Taylor, 1962).
Uomerine teeth are absent and the head is small. The snout

is quite pointed and the nostrils are located on two

7

elevated swellings, raised above the level of the snout.
The tympanum is large and covered with skin (Berry, 1975).
The fingers are slender and acutely pointed. The toes are
entirely webbed (Kampen, 1923). The dorsum, lower surfaces
and legs have numerous small, conical tubercles of unequal
size, the largest ones forming a few longitudinal rows on
the throat and belly (Kampen, 1923).

The color in life is greenish brown above, with small
darker markings. Sometimes a light yellow or green
vertebral stripe is present. The venter is yellow to cream
colored with a dark brown band on the arm and along the back
side of the thigh. Sometimes a brown L-shaped mark is
present on each side at the base of the thighs (Berry.
1975).

Male Q; llm; have an internal vocal sac (Kampen,

1923) and mature females are considerably larger than males.
Nuptial pads are present in males.

The species occurs in Thailand, Burma, Indo-China,
Hainan, Malaysia, and Java (Taylor, 1962).

The number of reports that even briefly mention the
ecology of Q, lflmg are few. Berry (1975) characterized
the species as small aquatic frogs found in lowland swamps
and pools. Schistma (1932) found the tadpoles in rice
fields during October and December in Bogor, west Java.
Inger and Colwell (1977) characterized Q, lime as

riparian-aquatic and nocturnal. The mating call has been

8

described by Heyer (1971) and Heyer (1974) briefly discussed

the ecology of the tadpole.

Egg; grztgragg (Schlegel)

ngg ggzthraga is a slender-bodied (males) to
moderately robust (females) frog. The head is longer than
broad, with a pointed snout. The tympanum is distinct and
about three-quarters of the eye diameter.

The tips of the fingers are dilated into disks with
circummarginal grooves. The largest disk is about half of
the tympanum diameter, but less that twice the width of the
phalanges. The disks of the toes are smaller than those of
the fingers. The web usually reaches the bases of the disks
on the outer edge of the first three toes and on the inner
edge of the fifth toe. The fourth toe has two phalanges
free of the web. An inner and, usually, an outer metatarsal
tubercle are present. Ventral and dorsal surfaces are
smooth. A broad dorsolateral fold is present.

Color in life is usually bright green above and on the
sides, with a bright yellow dorsolateral fold. The upper
lip and ventral surfaces are white. The limbs are olive
above with longitudinal black stripes or rows of dots.

As with 3‘ ggalgongtg, adult female 3;
ggzlggggg range four to six times the mass of males.

Males have a relatively larger tympanum and have nuptial

pads on the first fingers and clear asperities on the chin.

9

The geographic range of the species includes eastern
India and Burma to Sumatra, Borneo, Java, Celebes, and the
Philippine Islands (Boulenger, 1920).

Somewhat more literature is available for 3‘

mm than for figmor him-g. It

is a common frog found in rice fields, water around human
habitatations, and swamp forests at low elevations (Berry,
1975; Brown and Alcala, 1961, 1964; Heang, 1972; Inger,
1966; Matsui, 1979; Taylor, 1921, 1962). Inger and Colwell
(1977) classified 3; grzthgggg as a riparian-aquatic

and nocturnal frog.

Alcala (1955) studied 3; erzggraeg on Negros
Island, Philippines, and found males to call throughout the
night and frequently during the day. Eggs and embryos were
collected in all months in permanent ponds, ditches, shallow
creeks, marshy areas and semipermanent shallow ponds. Eggs
were deposited on the leaves of aquatic plants and he
inferred that all eggs were not deposited in one mass.

Brown and Alcala (1970) published on a more extensive
study of the population ecology of B; erythraeg on
Negros Island using mark-recapture techniques. They
reported maximum sizes for males and females and growth
rates for the two sexes.

Inger and Breenberg (1963) reported on the breeding
ecology of B; ggzlggggg in Borneo. Monthly collections

were obtained for one year and they reported on sizes for

10

males and females and on the state of sexual readiness.

They encountered no seasonal patterns.

Egg; §;n§giggr; Gravenhorst

Egg; g;ggglggg; has a stocky body and is a medium to
large-sized frog. The snout is rounded and the tympanum
clearly visible. Limbs are moderate to heavy and fingers
and toes are pointed, without disks. The web reaches almost
to the tips of the first, second, and third toes and to the
middle subarticular tubercle of the fourth toe. An elongate
inner metatarsal tubercle is present, but there is no outer
metatarsal tubercle.

Irregular skin folds are present on the back and a
supratympanic fold extends from the eye to the axilla.

Color in life is brownish-green above with irregular dark
markings. The lips have vertical dark brown bars and the
limbs have dark crossbars or irregular markings. The venter
is marbled with light and dark pigment.

Females are larger than males and males have median
subgular vocal sacs and black patches at the corners of the
throat. Males also have nuptial pads on their first
fingers.

The species is distributed in Thailand, Malaysia, the
Indo-Australian Archipelago and the Philippines (Taylor,
1962).

11

E; ggggriggrg is an economically important species
as it is collected in large numbers to be sold for human
consumption. The species is closely associated with humans
and is found mainly at low elevations, but never in the"
rainforest (Berry, 1975; Brown and Alcala, 1964; Inger,
1966; Liem, 1971). The species has a good tolerance for
salt water and is often found feeding on crabs in tidal
areas (Taylor, 1962). Despite its abundance and economic
importance, very little ecological or reproductive
information has been reported.

Alcala (1962) reported some information on the species
in the Philippines. It is a seasonal breeder on Negros,
avoiding the dry season. Egg masses contained from 50 to 70
ova, but the clutch size in dissected adults was more than
2000.

Church (1960b) reported on the breeding biology of E;
ggncrivggg based on weekly collections of males and
females for one year near Jakarta, Java. The testes of
males and ovaries of females were examined and measured and
body sizes reported. Church (1960b) suggested that part of
a batch of maturing eggs could be ovulated and oviposited.
Ovaries in all stages of development were found in each

month, although a degree of seasonality was reported.

MW Boie

The adult Egg; limgggggglg is a moderately stocky
frog with short limbs. The head is longer than broad and

12

the snout is rounded. A tympanum is visible. The limbs are
short and moderately heavy and the finger tips are pointed
and not expanded into disks. The web of the foot leaves at
least one phalanx of each toe free. Both inner and outer
metatarsal tubercles are present.

Irregular skin folds are present on the back and a
supratympanic fold runs from the eye to the axilla. The
color in life is grey or brownish above, with darker spots
or patches and often a green or tan vertebral stripe is
present. The underside is white and immaculate, except for
the male’s dark throat patch. Usually three dark brown
vertical bars on upper and lower lips are present and the
dorsal surfaces of the limbs have dark crossbars (Liem,
1971).

Adult female E; Luggggggfig are larger than males.
Males have a.mmdian subgular vocal pouch and a black
M-shaped band across the throat. Nuptial pads are present
on the first fingers.

The species is found in Thailand, India, Sri Lanka,
Taiwan, China, Japan, Malaysia, and Indo-Australian
archipelago (Taylor, 1962). The species is also found on
the Philippine islands (Inger, 1954).

E; limggsgggig is found in cleared areas where
humans has destroyed the original vegetation and therefore
is restricted to fairly low elevations (Berry, 1975; Dring,
1979; Dunn, 1928; Brandison, 1972; Heang, 1972; Inger,

1966). Taylor (1962) noted its importance as a human food

13

source in much of its range, although it is generally not
used in this way on Java. It shares the same habitats with
E; ggggglgggg and is never found in the forest (Liem,

1971). Inger and Colwell (1977) classified E;

11mgggggglg as terrestrial and nocturnal and Heyer

(1971) described the mating call. In Thailand, Heyer (1973)
noted mating calls in September, October, July, April, and
August and found larvae during October, September, June and
August. Schistma (1932) found tadpoles near Bogor, Java,
from October through April.

In Singapore, Berry (1964) noted calling males with
developed nuptial pads in every month. Enlarged oviducts
were found only in February, March, June, July, August,
October, November, December, and January. The monthly
average numbers of pigmented ova ranged from 504-2259.

The most‘extensive work on the reproductive biology of
E; 11mgggggg;g has been carried out in Taiwan by Paul
Alexander and g1 g1; (1963, 1979). These papers
discussed the sex ratio, body size and age distribution,
growth rates, life expectancy and reproductive biology of

the species.
DESCRIPTION OF THE STUDY SITES
The study sites for this research were in the vicinity

of Bogor, west Java, Indonesia. Before describing the

actual sites in detail, geographic, biogeographic,

I4

 

 

   
    
 
 

aw
I...
' I I ..'
CHINA
( p
THAILAND 10 ’6. 500'" cm». sn
‘9 2
z
a
“moon: . 1V .. PHILIPPINES
' .
I
I
'1 MALAY PENINSULA

BORNEO

INDIAN 06f“!

 

 

 

Figure 1.

Location of Java in Southeast Asia (from
Bartstra and Casparie, 1975).

15

paleogeographic, climatologic, and agricultural attributes
of Java will be outlined.

Java’s location is approximately 7 degrees south
latitude and between 95 and 115 degrees east longitude.‘ The
island is approximately 1100 kilometers long and 100
kilometers wide. Its surface area is 126,501 square
kilometers (Hammond Atlas, 1980). Java is part of the
Republic of Indonesia as are the islands which flank it:
Sumatra to the west, Borneo to the north, and Bali to the
east (Figure 1). These islands and approximately 14,000
1 others form the world’s largest archipelago (Draine and
Reed, 1982). Javan soils are nutrient-rich because it is an
area of intense volcanism. Java has 121 volcanos, 25 of
which are active (Fontanel and Chantefort, 1978). Indonesia
is the fifth most populous country in the world and sixty
percent of the population lives on Java, which has 70
million people (Hammond Atlas, 1980).

Java is in an extremely interesting and dynamic region
of biogeography and biogeographic history. It is a
“continental island'I which has had connections with the
mainland as recently as the Pleistocene Epoch and is part of
the Eurasian tectonic plate (Brown and Gibson, 1983). A. R.
Uallace (1876) designdted Java as part of the Oriental
Biogeographic Region.

During the Ouaternary Period in Southeast Asia, arid
and semiarid periods alternated with periods of more humid

conditions very similar to events in Africa and Latin

16

America (Uerstappen, 1975). However, Steenis (1935, 1947,
1961) emphasized that the Dipterocarpaceae, typical
representatives of the equatorial rain forest, have occurred
uninterruptedly in Sumatra and Borneo at least since the
Miocene Epoch and cores of tropical rainforest have
persisted throughout.

According to Uerstappen (1975) three factors have
exerted a great influence on the climatic conditions of the
Pleistocene Epoch in S.E. Asia. First of all, marked
changes in the distributional pattern of rainfall occurred
during the glacials and a drop of 30% in precipitation was
likely. Second, the world-wide decrease in air and sea
temperatures during the Quaternary ice ages caused a
lowering of the snow and forest lines and affected the
altitudinal zonation of vegetation in the area. Finally,
emergence of the Sunda shelf during the glacials due to
lowering of sea levels probably produced increased dryness.
During the last glaciaton, the sea level was about 100
meters lower then presently and the land surface area was
much greater. Continental connections existed during this
period (Verstappen, 1975).

Over 90% of the Indonesian Archipelago, the mean
temperature of the coldest month is over 20 degrees C, the
total annual rainfall is more than 2000 mm and the dry
season is absent. Over half of the archipelago receives.
more than 3000 mm of rain annually (Fontanel and Chantefort,

1978). Monsoon effects are felt more in the east than in

17

the west. The constancy of temperature is remarkable, with
the mean thermic amplitude only about two degrees C for most
of the archipelago. December and January are the coolest
and wettest months. Diurnal temperature amplitude is quite
high and ranges between seven and ten degrees C for the
entire area (Fontanel and Chantefort, 1978). The mean
thermic gradient for Java is 0.6 degrees C for each 100
meters; thus it can be estimated that the mean temperature
of the coldest month becomes less than 20 degrees C towards
900 to 1000 meters and 15 degees C towards 1700 to 1800
meters (Fontanel and Chantefort, 1978). Java’s natural
vegetation is tropical rainforest (whittaker, 1975) and is
dominated by the Family Dipterocarpaceae. However, the
natural vegetation is heavily impacted by human activities
and, according to Uerstappen (1975), massive deforestation
on Java has occurred in the last 200 years.

Because human activities have had great impact on the
frog fauna of Java (approximately 30 species), it is
important to briefly characterize the history of Em
ggglggg and agriculture on Java. Hominids have occupied
Indonesia since two million 8P (Jacob, 1975). Around
10,000 years BP, vegetable and root plants were first
domesticated and between 10,000 and 3,000 years 8P, rice and
cattle were domesticated. From 3,000 to 1000 years 8P,
culture developed further and settlements increased in size
and number (Jacob, 1975). For the past two hundred years a

colonial presence has brought about increased agriculture of

18

coffee, tea, and rubber (Draine and Reed, 1982) and an
accompanying deforestation. These factors have contributed
to the success of a few frogs species that do well in the
presence of human agriculture. More recently, the increased
use of pesticides and heavy collection of edible frogs may
affect even these anthropophilic species.

Three specific study sites were utilized in the data
collection for the present study. They were Bogor Botanical
Garden, Cibodas Botanical Park and Darmaga Field Station. A

description of each site is presented below.

0 or hi i rden (886

The Bogor Botanical Garden (888) is a 200 hectare park
located near the center of Bogor, west Java. It is
approximately 250 meters above sea level. Bogor has an
extreme rainforest climate with mean monthly temperatures
varying only between 24.3 C in February and 25.3 C in
October (waiter, 1979). Annual rainfall is approximately
4300 mm with 450 mm in the wettest month (April) and 230 mm
in the driest month (August) (Figure 2). On cloudy days
daily temperature variation is small (two degrees C), but on
sunny days temperature variation may reach nine degrees C.
Rain usually falls at mid-afternoon in the form of short
downpours, after which the sun shines. Clear days are
present in Bdgor even during the rainiest months (walter,
1979). The days are about 12 hours long throughout the year

(ca. 0600-1800 hours) (Church, 1960a).

19

 

 

70-
60-
Total rainfall}
E
{j 50-
H \
"c? A ’\
“E 40- --_ // \\ [I \\\
I; \\// g...“ \
\
m Mean monthl rainfall” ‘ H
30- y [I *0 g
\‘ ~ ” F36 '°
W - 3
20... :32 ,9.
......... Mean mo‘nihly temp\ ____‘____..---.. :28 E,
— Am ~24 “’
lO-i Min-temp/ :20 2»

 

 

 

I I I I I I I I T I I
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

Figure 2. Mean monthly rainfall and temperature (Fontanel and
Chantefort, 1978), total monthly rainfall and mean monthly maximum-
minimum temperatures (1983-84) for Bogor, West Java.

20

According to the Schmidt and Ferguson (1951)
classification system, Bogor has on the average 11.5 wet
months (where precipitation is greater than 100 mm) and 0.3
dry months (precipitation less than 60 mm). Fontanel and
Chantefort (1978) classified Bogor as a hot-hyperhumid
bioclimate which lacks a dry season. Figure 2 also
includes rainfall and temperature data for Bogor for the
duration of this study.

within the 886 are more than ten ponds, several small
streams and a maJor river (Sungai Ciliwung). Most fieldwork
time was spent in the vicinity of Mesjid Pond. This pond
had a surface area of 528 square meters and a maximum depth
of 70 cm. It was surrounded by high ground and trimmed
grass. On the east side of the pond, water from a small
stream entered over a one-meter waterfall. 0n the north
side, overflow water exited by way of a small stream. The
water source was rich in nutrients from human use and this
aided in the production of large amounts of filamentous
algae and an aquatic weed, EZQLLLLQ vggtigillggg. The
pond had up to 40% of its surface area covered by large
water lilies (Ezmggggg‘gg;). On the west side of
the pond, the strip of clipped grass was approximately ten
meters wide and this gave way to leaf litter and brush along
a small ravine and stream. MesJid pond was flanked on the
north and east by two other small ponds which shared the
same water source. On the south side of the pond, the

clipped grass extended 40 meters up a slope to an access

21

road. MesJid Pond was a permanent pond although the water.
level was lower in September and October, when its maximum
depth was about 30 cm and the surface area of the pond was

reduced by about 50%.

i oda nic l Park (C P)

The Cibodas Botanical Park (CBP) is an area of
approximately 50 hectares. It is located on the slopes of
Gede Mountain at the edge of a national forest preserve of
15 square kilometers. CBP is approximately 1400 meters
above sea level.

Schmidt and Ferguson (1951) gave a 20-year average
annual precipitation for CBP of 3380 mm and furthur
indicated that, on average, CBP has 1.4 dry months annually
and 8.5 wet months. Average monthly temperatures hover
around 20 C and diurnal fluctuations range about ten degrees
(from 14-24 C). A climate diagram for the nearby town of
Cipanas (elevation 1070 meters) is given in Figure 3.
Current climate data were not available for CBP. Fontanel
and Chantefort (1978) characterized CBP as a moderately
cool, hyper-humid and montane bioclimate which lacks a dry
season.

CBP contains several ponds and small streams, but field
work was concentrated on a large pond called Papyrus Pond.
This pond had a surface area of 3850 square meters and a
maximum depth of 80 cm. On the south side of the pond, a

brook entered from the adjacent rainforest. Overflow water

.22

 

Rainfall (cm)

 

 

 

 

 

 

-24
10 u mean monthly temperature _ _2.,
F'ZO
1 "18
I T f I T If r fi fi T T F
Oct liov Dec Jan Feb liar Apr May Jun Jul Aug Sep

Figure 3.

Mean monthly rainfall and temperature for Cipanas, West

Java (data from Fontanel and Chantefort, 1978).

 

 

 

 

 

Dashed segments of lines indicate
50 4 months when data were not available.
ao-i \
,\ \ Total monthly rainfall
8
V 30“ \
H ‘ ~..~
H ~~‘~
{u ‘u
‘64
_§ 20-
“ WW ------ ———\_.._
"“ -32
10-
-28
-___\ M1n-temp___-_—__-- {-24
T I r I I 1 r i y T r—T‘
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Figure 4. Total monthly rainfall and monthly mean maximumrminimum

temperatures for Darmaga Field Station. (1983-84).

(30) Sinusiadmal

(3°) Sinusiadmal

23

exited in a small stream at the east end of the pond. The‘
water source was cool and clear and Papyrus Pond had
relatively little filamentous algae and aquatic macrophytes.
The water of the pond was generally clear except after hard
rains when suspended sediments sometimes clouded the water.
Aquatic macrophytes in the pond included small patches of
lilies, Nzgghge; 3g; and the submergent weed,

Egratoghzllum g2; §ggittarig gg;_was an emergent

plant near the perimeter of the pond and patches of
cattails, 112g; gg;, were located at the ends of the

pond. A large patch of nggrus pagzrus was located near

the bank of the north edge. Clipped grass and shrubs
surrounded the pond. On the north edge, large dipterocarp
trees bordered the pond and on the south edge of the pond,
the clipped grass extended 30 meters, giving way to
second-growth rainforest. The ground surrounding the pond
was steep and well drained. The pond was permanent and held
its maximum amount of water in January through March and its

lowest water levels occured June through October.

D r Fie t tio ( F )

The Darmaga Field Station (DFS) is a fisheries field
station and laboratory owned by Bogor Agricultural
University. It is located ten km west of Bogor at an
elevation of 220 meters above sea level. This area consists
of 40 artificial ponds of various sizes. The total surface

area of the ponds was approximately 13,000 square meters.

24

Some of the ponds were used in fish culture, others were
allowed to grow up in natural vegetation. DFS receives, on
average, 3552 mm of rain annually and it has 11.2 wet
months and 0.3 dry months (Schmidt and Ferguson, 1951;
twenty-year average). The mean monthly temperature and
diurnal variations are similar to 88G. Fontanel and
Chantefort (1978) classified the DFS area as a
hot-hyperhumid bioclimate which lacks a dry season. The
temperature and rainfall data over the duration of this
study are presented in Figure 4.

Much of the DFS area was vegetated in grass. The area
was surrounded by agricultural land (mostly ricefields) and
kampung (village) areas. The water source for these ponds
was a small stream which flowed through a village area and
was rich in nutrients from human use. The water hyacinth,
Eigggggig gragsiggg, was a common floating vegetation in
many of the ponds, along with some emergent grasses.
Coconut and banana trees were the only larger vegetation in
the area.

The ponds at DFS were permanent although fluctuations
in level occured as result of research programs at the

laboratory.

METHODS AND MATERIALS

Field work at the three study sites was carried out
from October 1983 - October 1984. At 888 and DFS, one
24-hour observation period was conducted each month. These
observations were supplemented by more frequent, but shorter
visits to both sites. At CBP, one 24-hour observation
period was carried out on an average of every six weeks.

For CBP, all months exceptDecember, April, June and October
were included. A total of 940 worker hours was accumulated
during 50 nights in the field for nocturnal and 24-hour
observation periods. Species present, relative abundance of
each species and male calling activities were recorded on
each outing. Observations were made on temporal and spatial
taspects of the frog community. Observations on behavior of
females and males were recorded.

On daytime visits to the study sites, pond dimensions
and characteristics were measured. The predominant aquatic
plants present at the sites were identified using Pancho and
SoerJani (1978). Maximum-minimum air temperatures in the‘
shade and rainfall accumulation were taken daily in Bogor
and biweekly readings were taken at DFS (no data were taken
at DFS for April and May). weather data were not taken at

CBP.

25

26

Frogs were collected for dissection usually between
1700 and 2400 hours. Each month an attempt was made to
collect ten individuals of each sex of E; ggzgggggg, E;
iimgogggrig and Q; ling. The same number of E;
ghglggngt; was collected approximately every six weeks.
The field technique was to collect the first ten of each sex
that could be located and captured. A long-handled net with
a 14 cm diameter hoop was used. The frogs were processed
within two hours of capture. In the case of E;
gggsgivgrg, 20-30 live frogs were purchased every three
weeks at the local market. Each batch of frogs was
purchased at 0700 hours and had been collected by a
professional catcher the previous night and early morning.
Information on the collection locality was obtained from the
vendor and in all cases the collection site was within 25
kilometers of Bogor. It was assumed that the professional
collector captured adult frogs without bias as to size as
frog prices at the market were calculated per frog, not by
weight. These frogs were processed within two hours of
purchase. E; ggggglgggg_were difficult frogs to capture
because of their wariness. They were purchased in order to
obtain adequate numbers for dissection without inordinate
time ouput. Over the 12 months of this study, a total of
1328 frogs was dissected. The counts for each species were:
E; ggggigggg, 534 (ca. 45 per month); E; ggglgggggg,

198 (ca. 17 per month); E; grzthrggg, 211 (ca. 18 per

27

month); E; limnogharig, 21? (ca. 18 per month); and Q;
ligg, 168 (ca. 14 per month).

Frogs were relaxed in an aqueous chloretone solution.
Each was blotted dry and weighed using a ten gram Pesola
scale calibrated in tenths of a gram or, for larger frogs, a
300 g Pesola scale calibrated in grams. An individual field
tag was then attached to each frog. Snout-vent length
(distance from the tip of snout to farthest extent of the
ischium) was measured with a spreader and millimeter rule
while the relaxed frog was held flat. The volumes of a
subsample of frogs were measured by water displacement.
After measurements were made, the E; ggglgggota, E;
grzgggaeg, E; limnggharig and Q; ling were fixed
and preserved in 4% buffered formalin. The measurements and
the fixing procedures were conducted at the field collection
site. These frogs were dissected within a few days. The E;
ggncrivora were dissected fresh but the gonads were
placed in 4% formalin for one or two days before further
measurements were taken. This procedural difference was
because their large body size made fixing and storing a slow
and space-consuming process. The gonads were preserved in
formalin to be consistent with the way the other five
species were processed.

In males, the presence or absence of secondary sexual
characteristics was noted. The left testis was removed from

each male and its length and diameter measured. Testis

28

volume was calculated by assuming it to be a cylinder. The
presence and relative size of fat bodies were noted.

Each ovary was weighed on the 10 g Pesola scale. The
diameters of ten ova from each frog were measured using a
dissecting microscope fitted with an ocular micrometer. The
ova were staged according to the following scheme after
Church (1960b): Stage 1 - small, unpigmented ova; Stage 2 -
ova small and pigmentation variable; Stage 3 - almost all
ova pigmented, but no animal-vegetal hemisphere apparent;
Stage 4 - a difference in pigmentation between animal and
vegetal hemispheres beginning to develop; Stage 5 - ova with
clearly distinguishable animal-vegetal poles; and Stage 6 -
post-ovulation, distinguished by the condition of the empty
ovary which usually contained some unovulated Stage 5 ova.
It was not possible to categorize Q; lig; ova in Stages
4 or 5 because heavy pigmentation obscured the
animal-vegetal hemispheres. In this case a size criterion
(explained in text) was used to determine ova stage.

In females with sufficiently large ova, fifty ova were
teased from the ovary and their volume measured in a burette
calibrated to hundredths of a milliliter. It was found that
the weight in grams of an ovary was not significantly
different from its volume in milliliters (t-test, 95% level
of confidence, n=15). Using the combined weight in grams of
left and right ovaries and the volume of 50 ova, the total
number of enlarged ovarian ova (clutch size) was calculated.

This procedure was biased in that it could result in a

29

slight overestimate of clutch size. Supportive tissue in
the ovary, as well as a small developing set of ova, added
some weight to the total ovarian weight. This was not
appreciable in an ovary with enlarged ova. The small clutch
size of Q; lim; permitted a direct count.

The size and convolutions of the oviducts were recorded
and the presence and relative size of the fat bodies noted.
Most statistical analyses and tests were performed
using an Apple IIe computer. Prior to use of a parametric

test, variables were tested for normality (Kolmogorov-
Smirnov Test for Goodness of Fit) and homogeneity of
variances (F-max Test and Bartlett’s Test for
Homoscedasticity) (Sokal and Rolhf, 1981). If normality and
homoscedasticity were not demonstrated, nonparametric tests
were applied. Statistical tests used in this research were
Kruskal-wallis Test (nonparametric test for differences
among groups), Mann-whitney Test (nonparametric analog of
the t-test), linear regression, t-tests, product-moment
correlation, F-max Test, Bartlett’s Test for
homoscedasticity, and Kolmogorov-Smirnov Test for goodness

of fit.

RESULTS

The data collected in this study generally fell under
two main categories: (1) qualitative data collected by field
observations and (2) quantitative data collected through
measurements of dissected specimens. The results section.
reflects these two main areas with the first subsection
reporting field observations and the later subsections

reporting quantitative data.

r in i r tioni n court hi eh v'or

It was hypothesized that mechanisms existed to prevent
interbreeding and minimize other interspecific interactions
such as competition for food or space at breeding sites.
Breeding habitat partitioning and discriminatory courtship
behaviors are two potential mechanisms that can be studied
in the field. Observations pertaining to both were made at
the breeding sites of the five species.

Breeding habitat partitioning can take place on three
levels: spatial, seasonal and temporal. Spatial
partitioning can be of two types: (1) coarse spatial
partitioning, which refers to the use of completely
different breeding ponds by different species, and (2) fine

spatial partitioning, which refers to species preferences

30

31

for specific microhabitats within the same breeding pond.
Seasonal partitioning refers to weekly or monthly
differences in breeding activities, for example, dry-season
breeders and wet-season’breeders. Finally, temporal
partitioning refers to breeding activity differences on a
24-hour cycle, for example, day-time breeders and night-time
breeders.

Both coarse and fine spatial breeding habitat
partitioning were apparent within the community. Coarse
spatial partitioning was evidenced by the fact that distinct
species associations occurred at each of the three sites.
Table 1 presents characteristics of the three study sites,
including species assemblages. Only the five study species
were included in Table 1, but each site had larger species
associations (Table 2). The five study species were
selected because of their close taxonomic relation and their
great abundance in the community. E; ggglgggggglwas the
only study species present at Papyrus Pond at CBP. MesJid
Pond at 888 had four of the five study species present. ‘E;

ggngcivogg and E; ggglggggig were not present at
every observation period, whereas E; ggztgrggg and E;

limngcharig were always present. Q; liga was never
found at MesJid Pond. The maximum number of study species
calling synchronously at MesJid Pond was four. Considering

only the study species, the ponds at DFS had E; erythraea,

E; Limggggggig, 0; 11m; and E; cangrivgr; present and

32

Table 1. iiabitat type and species assenblages of the stsdy sites.

 

 

 

 

 

 

 

 

 

 

 

 

CD 888 IFS
Habitat type then area Open area ilpen area,
and elevation at forest edge adjacent dis- adjacent
1m neters tnrbed forest agri-land
m gig; m netgg
iii-her of ponds one pond, one pond, nany ponds,
and approxinate 3,850 se.n. 528 se.n. 13,100;
grface area an,
Pernanence semi mung; ”Eggs;
Total noeber of
species found 1 4 ii
at site
lotal amber of
species calling 1 ii 4
a ite ‘
iiaxinine iii-tier of
species calling 1 4 t
synchronously
at site
ll, cancrivggg if Q AP
ll. linnocliaris l0 AP AP
, it. erzthraea ill AP AP
ii. chalcongtg AP 3’ if
0. lig Elf; i0 AP

 

'CI” =- Papyrns Pond at Cibodas Botanical Part.
'HS' =- liesjid Pond at Bogor Botanical Garden.
'DFS' 8 easy ponds at the Darnaga Field Station.
'AP' indicates alvays present.

'0!” indicates occasionally present.

“ll” indicates never present.

33

Table 2. Anuran species associations at each study site.

 

Locality

Family

Species

 

Bogor Botanical
Garden,
Mesi id Pond

Bufonidae

Microhylidae

Ranidae

Rhacophoridae

E219 mglanggtigtgg
E; gipgrgatgg

am H 351mm

Rgga cangrivggg
E; chalggnotg
E; erzthraea
E; limnochari;
E; macrodgg

WW

 

Darmaga Field
Station

Bufonidae

Microhylidae

Ranidae

Rhacophoridae

Bufo melggggtigggg
E; bipgrcgtg;

Miggohzla achggiga

e lima

i
an 52mm
. erztgrae;

limnocharis
. macrodon
' ob r'

W01 at was;

E

 

 

PPPI”

 

Cibodas Botan-
ical Park,
Papyrus Pond

Bufonidae

Microhylidae

Pelobatidae

Ranidae

Rhacophoridae

Egig|melanggtigggg

Miggohzla gghggina
[13.293.953.293

flegophrz; mggtigglg'

hal
nicogarigggig

Polypeggggs lgggggzglg;

E; reinwgrggi
Rhagophogg; jgvagus

FIFE

 

34

calling synchronously at every visit to the site. E;
ggglggg93g was never observed at DFS.

Over the course of this study, all combinations of
species pairs were observed calling sympatrically and
synchronously at the same site except for Q; ligg/E;
ghgiggngta (Table 3).

Fine spatial habitat partitioning was maintained both
in situations where only one species called alone and where
two or more of the species called simultaneously.
Microhabitat preferences were most readily observed by
noting the calling sites of the males. Male E;
grzthrgea preferred positions over the water and usually
perched on floating Ezgggggg pads or on emergent Eiggggnia
leaves up to 25 cm above the water surface. Individual male
‘E; grzghrgeg were fairly evenly spaced, although
male-male interactions to maintain specific calling sites
were not observed. Male 9; 11g; called while floating
in open water or on mats of floating algae. water depth at
the calling sites ranged from 5 to 30 cm. Individual males
were spaced over the entire pond. Male E; ggglgggggg
most frequently called from emergent vegetation up to one
meter above the water surface or from the grassy banks of
the pond up to three meters from the water’s edge.
Occasionally they called from floating Ezggggg; pads and
frequently formed dense aggregations of 20-100f individuals
calling from the same patch of papyrus or cattails. Male E;

gagggivora called from ground level on exposed mud flats

35

Table 3. liatria for species calling synpatrically and synchronoesly.

 

 

 

SPECIES
5m 1m 1m Mm

SPECIES mscim limits stalemate ML!!! line
i. memos! X + . i i
1.. new i X t t t
I. missed; * t X t N
1.. cumin * . i X t
9.. lies * + N t X

Ratio: in m m m 313
m

Percent: my 1m 1m my not

 

'N' indicates that the tun species nere never observed calling at the sue site.
'0' indicates that the bio species were found calling synpatrically

and synchronously.

'AP' indicates the ratio of acteal species associations (idiere species

called synpatrically and synchronously) to potential species associations

(where species called at the sue site but nere segregated seasonally).

36

or clumps of grass on the pond’s perimeter. They were not
observed calling while sitting in water and sometimes called
several meters from open water. Males were evenly spaced,
but behavioral interactions between males were not observed.
Male E; limnoggggis called from exposed positions on mud
flats or short grass on the edge of the pond. Like male E;
ggggg;ggg;, they did not call from the water or from
elevated positions. They were usually located within one or
two meters of open water and called while facing the water.
Males were fairly evenly spaced.

For the five study species, breeding ponds were also
the living and feeding areas. All five species were
observed at the ponds during daytime visits. During periods
of non-calling (daytime), microhabitat preferences were also

observed. E; ggncrivgrg and E; lignocharis hid in

damp grass or in soil crevices and depressions, E
grzthraea and E; chalcgnggg perched above the water
in vegetation in hidden positions and 9; 11m; were
partly submerged in wet mud or floating algae. Field
observations at CBP, BBB and DFS and other areas in the
Bogor area indicated that E; grzthraea and E;
£legggg$g most frequently utilized permanent ponds as
living-breeding habitat whereas Q; ligg, E;

im ris and E; ggnggivorg were frequently
observed in the more temporary ricefield habitats.

Males of all five species gave advertisement calls in

every month of the year (Table 4) when the three study sites

37

were considered collectively. The gap in Table 4 for E;
chglggggg; resulted from a month where no observations
were made at CBP.

when studied from the viewpoint of individual sites
(Table 5), no seasonality was observed in calling behaviors
at CBP or DFS. E; chglggnota were heard calling each
month that observations were made at CBP. E; erythraea, E;
leggggggig, E; gancrivgr; and Q; 11g; were present and
calling at every visit to the DFS site for nocturnal
observations. At MesJid Pond in 886, some seasonality was
observed. E; grzthrae; and E; limnocgggig were
present and calling during each month, but E; gggcgivora
and E; ggalcgnota were not present at all times. E;
gancgigora was observed calling at BBB during September,
October and July. E; ghalcongt; were present and
calling at 888 during March, April, May, June, July and
August.

Figure 5 illustrates the temporal patterns of
advertisment calling behaviors for each of the study
species. Each trace in Figure 5 represents calling
commencement time, peak calling period and calling
completion time for each observation bout. Because the
twelve-hour pattern of daylight and darkness varied only a
few minutes on an annual cycle, it was possible to use
absolute time. Generally, the calling activities of all
species were restricted to the hours of twilight and

.darkness. E; ghalggnot; had two rather equal periods in

38

Table i. Nonthly calling record for nales of the fine study species.

 

 

2&5
Nonth fig; l igmgh er i g .5392... 93;an Mil-gem
k tober i e f i e
None-her : t f i i
Decenher f f f N i
January i f + i f
february f f i i f
March 0 f f f i
“N l t f e f f
Nay e f f e i
hine f i f f f
July e i f f f
Myst e f f i e
Septenber e f e f f

 

'f' indicates nale frogs called airing the nooth.
11' indicates no record for the nooth.

Table 5.

reference to locality.

39

Noethly calling record for sales of the fine study species uith

 

 

 

 

 

 

 

 

 

 

 

 

 

egos

Lane to; 1m to:
Mt Lil: gagging: ligggharig gm; chalcongta jig;
888 e e - ..
ET DFS f f - f
m .. .. - 4; ..

BS - e f -

W DFS f e s -

E - - - i
888 - f f - -
EC DFS I I 0 .- g
99! N N N N
m - f i - -
JAN OPS f f f - e
E! .. g - -
nee - i i - -

FEB DFS f f -
m - - - Q -

188 f f f

Mil DFS e e -
fl - - Q -
BBS - e e e -
A°it DFS t i i - t
99!! N N N N N
I88 - f t e -
MY DFS e e f - f
92 . - - p -
386 - f f p -
Mi DPS e f i - -
993 N N N it N
188 f i e i -
Jll DFS e e f - i
Q! - - .. g -
886 e f f e -
AB N8 0 i e - e
m - - .. s -
I86 f f i - -
SEP DFS e e e - e
m - - - g ..

 

'386'= Bogor Botanical Garden; 'DfS'a Darnaga Field Station;
'CD'I- Cibodas Botanical Part.
't' indicates nale frogs called during the nonth.
'-' indicates nales uere not heard calling during the nonth.
'N' indicates no record for the nonth.

40

 

Rana cancrivorq

 

 

 

 

 

 

Rana Zimnocharis

 

 

 

 

 

 

 

 

 

 

 

 

 

 

ana erythraea

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Rana chalconota

 

 

 

—*—-
-—-—————

 

 

 

 

 

 

 

Ooeidozyga Zima

 

 

 

 

 

 

 

 

 

 

 

 

-———:

IIITIFIIIIIfiIIIIFsIIIIrI

OOOOOOOOOOOOOOOOOOOO

NMQMO-NwC‘OF‘NMQHNMQVIONQQOH

e—tr-iF-tn—te—ir—fv—iv—iNNNNNOOOOOOOOOHH
Time of Day

 

 

Figure 5. Temporal aspects of advertisement calling behavior
including time of commencement, peak period (broad portion of
trace) and time of completion for each 24-hour observation bout.

41

terms of calling activites during a 24-hour cycle. At
Papyrus Pond (CBP), calling usually occurred from Just
before sunrise and continued until mid-morning. At MesJid
Pond (886), E; chalgongt; called during an evening

period only.

Temporal partitioning of calling activities was present
in the community. Figure 6 is a composite of the individual
species traces of Figure 5. The single trace for each
species was generated by averaging calling commencement
time, peak calling period, and calling completion time for
each species over all observation periods. E;
ligngghagis and E; gaggcivora had nearly complete
overlap in their calling periods. Q; lig; and E;
chglconota also showed great overlap in the evening
calling period. E; erzghraea essentially called from
dusk until dawn and therefore overlapped all four species to
some extent. However, there was a period from midnight to
0300 hours when the peak calling period of E; grzggrggg
did not overlap that of the other species. E; cancrivora
and E; chalconota, E; limnocharis and E; chalconota, Q; LEE;
and E; cancrivora and Q; Lia; and E; limnocharis had fairly

distinct peak calling activity periods.

Eggz gig; relations

The five species ranged over a large spectrum of sizes.
‘ Tables 6 and 7 give snout-vent length (SUL) and live weight

(LN) data for sexually mature individuals of each sex and

42’

 

l Rana cancrivora
———@E- emthmea

Rana chalconota
——-—— —_———

__—____ Ooeidozyga Zima

\

 

 

 

 

VIIjITIII'jI'IIWIIIVT—vvr
UUOOOOOOOOOOOOOOOOOOOOOO
OOOOOOOOOOOOOOOOOOOOOOOO
NMQMONQC‘O—dNMQ-HNMQIAONQO‘C—f
e-(e-tr—tn—tn—(r—ir—te—fNC‘JNNNOOOOOOOOOo—d—dy

Time of Day
Figure 6.

Average time of commencement, peak period (broad
portion of trace) and time of completion of advertisement
calling behavior for the five study species.

Table 6. Snout-eent length data (in I) for nature frogs.

43

 

 

Species Se: N- llean 952 6.1. Range M then
m m ' ii 99 76.7 75.5-77.9 59.1-17.1 7.9 YES
M M F 68 91.9 95.6-112.1 61.1-119.1 13.6 YES
3.1!! 111111.!!! ll 64 42.1 41.3-42.9 36.1-51.1 7.7 YES
Lag; 1:23.131! F 39 66.7 65.3-61.2 56.1-78.1 6.7 YES
211.! 11.11.539.11 if 61 43.3 42.3-44.2 35.1-53.5 1.5 YES
M $1115.11!!! P 64.2 61.9-66.6 52.1-77.7 11.7 YES
m m; if 61 45.6 44.1-46.4 35.5-51.5 6.1 YES
M W F 27 52.5 51.4-54.6 41.1-62.5 11.1 YES
m Lia if 44 24.9 24.4-25.5 21.1-29.5 7.4 YES
m jig; F 29 31.1 8632.9 25.5-36.5 9.4 YES

 

'c.l.' is confidence interval.
'M' is coefficient of variation.

‘Norn' is nornality as deternined by Kolguoron-hirnoe test.

44

Table 7. Line ueight data (in was) for nature frogs.

 

 

Species Se: N- iiean 95% 1.1. Range M then
Egg gangrieggg ll 99 41.1 38.3-41.8 21.1-61.1 21.7 YES
Egg gangrivorg F 68 97.8 88.6-117.1 29.5-216.1 39.2 YES
gm 1.2M N 64 4.6 4.3-4.8 2.7-6.7 21.8 YES
Lag; m P 39 21.4 19.2-21.7 11.1-31.6 19.1 YES
35;; My}; if 61 4.7 4.4-5.1 2.4-7.9 23.6 YES
itgn; ghalconota F 35 18.6 16.7-21.5 9.5-31.5 31.1 YES
3g; iinnggharis if 61 7.8 7.4-8.1 3.8-11.3 15.9 YES
3113 HMS F 27 13.5 12.1-15.1 8.1-21.1 14.8 YES
Mag; ijg; if 44 1.8 1.7-1.9 1.1-2.6 19.3 YES
My; jig; F 29 3.7 3.3-4.1 2.1-5.4 27.6 YES

 

'c.I.' is confidence interval.
'M' is coefficient of variation.

'Norn' is nornality as deternined by Kolguorov-fiirnoo test.

45
each species (sexual maturity is defined on pages 62 and
70). The SUL data are presented graphically in Figure 7.
The data for these measurements were normally distributed,
but variances among the groups were unequal. Nonparametric
statistics were used for comparative description.

SVL and Lu were highly correlated in males and females
of all five species (Table 8).

A one-to-one relationship existed between L“ and live
volume for all the study species (Table 9).

All five species demonstrated sexual dimorphism in size
(both SUL and LN), with statistically significant
differences between the sexes (Table 10). In all cases,
females were larger than males. The sexual dimorphism
ratios (female size/male size) for each species are given in
Table 10.

Shine (1979) reported that female anurans grow to a
larger size in 89.6% of 589 anuran species that he reviewed
and species where males were larger than females tended to
be those where male-male combat takes place. Both Shine
(1979) and Crump (1974) outlined possible reasons for female
anurans being larger than males of a species. Both authors
suggested that, since larger females can accomodate more or
larger eggs, there should be selective pressures for females
to be large. Shine (1979) suggested that female fecundity
increases more rapidly with increasing body size than does
male reproductive success and Crump (1974) stated that there

is an energetic advantage for being small. These two

46

 

 

Rana cancrivora (females) +

Rana cancrivora (males) IL

 

Rana erythraea (fem.) It

 

——dh—- Rana erythraea (males)

Rana chalconota (fem.) ————4lhr————-
._—_‘}———— Rana chalconota (males)

 

* Rana limnocharis (females)

-———4I——- Rana limnocharis (males)

-——IP—-Ooeidozyga Zima (females)

-I- Ooeidozgga Zima (males)

 

 

2316 I 2b ' 50"46 ' 56 ' 60 ' f0 riéoj 9b ‘166 'ifo '120'
Snout-vent length (mm)
Figure 7. Means (vertical lines), ranges (horizontal lines)

and 95% confidence intervals (horizontal bars) of snout-vent
length of male and female frogs.

47

Table 8. Product-nuent correlation betueen snout-vent
length (M) and live ueight (111).

 

Species Sex 11- SA. 111 it

 

3mm ii 51 YES YES 1.12“

M51191!!! F 58 YES YES 1.93 as
MW if 51 YES YES 1.75 ea

mm P 27 YES YES 1.91 as

mm ll 51 YES YES 1.75"
818.158.153.931 F 35 YES YES 1.94"

Egg rae ii 51 YES YES 1.72 it
3m erzthrge; F 39 YES YES 1.91“

mm ll 44 YES YES 1.74"
mm; P 29 YES YES 1.96"

 

'Norn' is nornality is as deternined by iiolguorou-hirnou test.
'fl' indicates simificant at P(1.11.

48

Table 9. Relation between live weight and live volume for the
five study species.

 

 

Species N 8 Regression Equation R -

Oogigozzg; 11g; 9 Y = -0.04 + 1.00 X 0.97 in
Egg; grzthrgg; 10 Y = _0.08 f 0.99 X 0.98 an
Egg; iimggghgrig 11 Y I -0.21 + 0.99 X 1.00 an
Egg; ggggrivgr; (males) 11 Y = -0.26 f 1.00 X 0.99 an
Egg; gangrivorg (females) 11 Y 8 0.82 f 0.97 X 1.00 an
Egg; Egglgggggg 11 Y I 0.08 e 0.99 X 1.00 as

 

'ii' indicates significant at P(0.01.

49

Table 11. Sudy size differences and body size ratios betueen sexually nature sales and
fenales of each species.

 

'0' '0' Se: Range 931 81 Sex Range 951 CI
Species value value Ratio of Sex of Sex Ratio of Sex of Sea
(1.11) (Sit) Peel Ratio Ratio Feel Ratio Ratio
liale (1.8) (111) liale (941) (971.)
(Of) (801.)

 

mus; 333: 331: 2.1 1.3-4.9 1.7-2.4 1.3 1.9-1.7 1.2-1.4
mm; 313: 342: 1.7 1.3-5.5 1.5-2.1 1.2 1.3-1.3 1.1-1.2
mm 411: 411: 3.9 1.2-13.1 3.3-4.7 3.9 1.1-2.2 1.4-1.1
il_an_a__e_i;Ltggg_;_a_ 401: 411: 4.4 1.1-11.3 4.1-5.1 4.4 1.1-2.2 1.5-1.6
Mimi-avg; 349: 354: 2.4 1.5-9.3 2.2-2.3 2.4 1.3-2.1 1.2-1.4

 

'0 value' indicates Nann-ihitney test statistic for checking for significant difference
in size betueen nature males and nature fenales;

'1' indicates significant at P(1.15 (2-tailed test);

'Lii‘ is live Heidit; 'M' is Soont-iient Length;

'951 01' is 951 confidence interval.

50
factors, combined with a potential for reduced competition
for resources between a male and female of different sizes,
may contribute to selection for sexual dimorphism in size
with the female being larger than the male. Shine
suggested, as an alternate or contributing factor, that
males probably die younger (and therefore smaller) because
of the I'high risk' mating strategies they employ. This
suggestion would seem to be supported by Turner (1960) for
Egg; grggiogg, but Brown and Alcala (1970) found a
similar longevity for male and female E; grztgrge; in
the Philippines.

Shine (1979) and Crump (1974) came to opposite
conclusions regarding the relationship of sexual size
dimorphism and taxonomic relatedness. The former author
concluded that the direction of sexual size dimorphism does
not follow taxonomic lines, whereas the latter author
suggested that sex size dimorphism is determined more by
systematic relationships than by reproductive
considerations. Undoubtedly, both sexual size dimorphism
and reproductive attributes of species are influenced by
systematic relationships. In this study, the sexual size
dimorphism ratio for the five species was not correlated
with mean clutch size, mean ovum diameter, mean female size,
ovarian weight factor or ovarian size factor.

A Kruskal-Uallis test indicated that both LN (H-83.4**,
P(0.01) and SVL (H-87.3**, P(0.01) were significantly

different among females of the study species. The order of

51

increasing mean size (SUL or LN) for mature females is Q;

lima (.3; limnochgris ( E; chalconota ( E; erythraea ( E;

 

cancrivora. Mann-Nhitney tests for adjacent frogs on the
SUL or LN spectrum (Table 11) indicated that female E;
ghglconota and E; grzthraea were not significantly
different from each other, but the pairs Q; llgg/E;
limnocharis, E; limnocharis/E; chalgonoga, E; erztgraga/E;
cancrivora, and E; limnocharis/E; erythraea were
significantly different.

A Kruskal-Nallis test indicated that both LN (H-89.5**,
P(0.01) and SUL (H-81.4**, P(0.01) were significantly
different among males of the study species. The order of
increasing mean size (SUL or LN) for mature males is Q; 11g;
( E; erythraea ( E; chalconota ( E; limnocharis ( E;
Eggsglgggg; Mann-Nhitney tests (Table 11) indicated that

male E; chalcggoga and E; iimgggharig were not
significantly different in SUL, but were different in LN.
Male E; grzihgge; and E; ghglggnggg were not
significantly different in LN, but were different in SVL.
The pairs Q; leng; r rae , E; limnocharis/E;
cancrivora, and E; limnocharisAE; erythraea were
significantly different in SUL and LN. In effect, mature
males of each species were significantly different in either
SUL, LN or both.

It is possible that species differences in size within

thb community are determined, in part, by interspecific

partitioning of food resources based on size, as has been

52

Table 11. Results of Nann-hhitney tests checking species differences of
nean snout-vent length and nean live ueidit for nature frogs.

 

 

Species pair . '8' value for '1' value for
for cnparison of cnparison of

cuparison Se: live ueidit snout-vent length
Mm _l_iga_ - Egg; linngghggig F 411 I 411 I
Eggligggharig-Emgggigm F 336! 383!
Egg; ghglcggotg - Egn; MILE! F 214 NS 223 NS
Egg gthgggg - Em gancrivgg F 411 i 392 I
has m - Em mum F 35' ' ' 391 '
9911112111! lg; - Egg; 121111.111 if 411 s 411 1
Egg 9111.113; - Egg; gigggggig ii 311 e 214 NS
Egg; giglgongtg - Egg 1mg 11 251 NS 391 3
Egg; linnociiarig - Egg; gggrivga ii 411 e 411 I
Emligigiarig-Eggggziigm N 331: 399i

 

'3' indicates significant at P(1.15 (tun-tailed test).
'NS' indicates not significant, ”-1.”.

53

suggested by Caldwell (1973) and Toft (1980). However,
Inger (1969) found only a weak correlation between frog size
and prey size in Bornean ranids. Species recognition is
also a potential factor involved with evolution of species
size differences within a community, with such differences

contributing to maintenance of species isolation.

Fgg gogigg

Each frog was qualitatively scored as to whether the
fat body associated with the gonad was large (usually
whitish in color and often larger than the gonad) or small
(usually yellowish in color and smaller than the gonad).
Fat bodies are presumably energy-storage tissue and it could
be hypothesized that younger frogs store energy in these fat
bodies until it is needed in the production of gametes at
sexual maturity. To test this, male and female frogs were
scored on their SVL (an indicator of relative age) and size
of fat body, and size-frequency histograms were plotted for
each sex and species (Figures 8 and 9). The assumptions of
normality and equality of variances were met on the SUL data
for all groups except male Q;,l;gg and male E;
ligngggaris. In general, large fat bodies were
distributed across all size classes of the frogs with no
significant differences in mean size between frogs with

large fat bodies and those without large fat bodies (Table
12). However, in female E; grzghrge; and E;

gggggiggg; and in male E; ggggrivora, there was a

54

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A. Rana chalconota B. Ooeidozyga Zima
: w/LFB ; w/LFB
14: 14;
10- 10 : F
,3 62 1' .3 6 1
g 2‘ , W1 :3 21 F a
“a 2; J 'O 2; L-i
w-i g ”'1 .1
73 6: r5 6:
,5 10: ,fi 10 3 J
«1414‘ “-4141
c j _ 0 j -
3 :8‘ 5 18 q
2- 22 -
.o ‘ -° .
S 26- 5 2 4
z “ z -4
30j 30 :
344 34 -
. _ .
383 w/o LFB 38 1 w/o LFB
IlrlIl'III IIIIIIIFTT
30 50 10 30 .S
Shout-vent length Snout-vent length
D. Rana Zimocharis
30j w/LFB
261
22:
.318: "l .E.’
314- 3
3 3 3
> 10- F >
'9'. 6-1 H
'o 1 'o
F 2. c
'1'. h '1 ‘1'1
n4 2. “{JLL+ _] a.
o 4 o
u 6: 3
3 ' 3
Iz 14? L =2
18: *
22-
26;
3° w/oLFB
ri'i'i'rrfi
15 35 55

Snout-vent length

Number of individuals

C. Rana eggthraea
w/LFB

p—n
.I.\
JLAL

0‘
IILI

3.1
b
J

 

 

 

H
(I)
L4IJILJAIIILLJIIJJ

 

 

La

w/o LFB

I I rW ITI
35 45 55
Snout-vent length

 

E. Rana cancrivora

30

26
22

18
14

10

 

 

 

 

 

 

 

 

 

 

: w/LFB _

1

j i"

I a

. LJLLL J—I

I L

.i

1

iw/oLFB "
T'lfil'i‘i'l’i

4O 60 80 100
Snout-vent length

Figure 8. Distribution of large fat bodies (LFB) across size
classes of male frogs of the five study species. Snout-vent

length in mm.

55

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A. Rana limnocharis B. Ooeidbzyga Zima C. Rana chalconota
m 22 w/LFB m w/LFB m w/LFB
”.314; "3143 7.314;
310: _. €102 3103
H 3 — H
.3 63 >' 6- >' 6-
'0 d :3 4 J :8 d
g 23 mn-n— "L 5 2~ g 22 I}.
O 6‘ L c: 6‘ o» 6'
4 -w ‘
E102 310« L 310«
1 .0 1 .0 "
314: 314 glé‘
218‘ w/o LFB 218;w/o LFB 2.13: w/o LFB
‘I‘T'I'T'l' IfiTTr 1 WWW
20 40 60 15 35 30 7o
Snout-vent length Snout-vent length Snout-vent length
D. Rana erythraea E. Rana cancrivora
m l w/LFB a: I w/LFB
"3143 1.3142
€103 €102
w-l ‘H d
23 2 H“
5 2‘ [-111th "I E‘ 2‘ ['1
“-0 d “-0 q
o 6- o 5. _
“10‘ “101
3 J ,2 . L.
51": 91“: L.
218‘ w/o LFB _ 218-4 w/o LFB
'ITng-JWI' 'I'IFWI'I‘IFIFAUI
25 4 65 25 45 65 85 1 5
Snout-vent length Snout-vent length

Figure 9. Distribution of large fat bodies (LFB) across size
classes of females of the five study species. Snout-vent
length in mm.

56

lable 12. Test results checking diiierences in nean snout-vent length
(811.) hetueen frogs with large iat bodies (LFB) and those nitlioot (in/o LFB).

 

 

Mean 81L ltean 81L F-nax Test
Species Sex vith LFB NI Nora u/o 1.178 N- Norn stat stat
(I) (In)

W Lin 31.2 24 Y8 28.4 24 Y8 1.7 NS 1.88 N8
m Lia 24.6 32 Y8 24.4 31 Y8 2.2 s 287 us
888.! 1.11M 46.1 21 Y8 42.7 36 Y8 1.8 148 1.18 118
Lug m 45.7 38 Y8 43.8 53 Y8 7.8 as 213 148
M M 63.3 5 ,Y8 61.8 33 Y8 1.7 118 1.83 148
393 m 46.2 13 Y8 44.8 78 Y8 1.8 N8 1.61 NS
33;; 2838—“; 81.8 13 Y8 63.1 48 Ml 1.6 NS -3.87 as
33;; m 41.7 23 Y8 41.9 56 Y8 1.2 N8 -.24 us
320—! mm 88.3 64 Y8 88.6 99 Y8 1.4 N8 2.68 as
m m 76.2 96 Y8 72.7 111 Y8 1.2 148 2.94 as

 

'Norn' is nornality as deternined by Kolguaorov-Sairnov test (Y8Iyes).
'F-Iax stat' checks for equality oi variances; us indicates variances
are equal; I! indicates variances are onegoal at “8.81; s indicates

variances are vnequal at No.85.

'Test stat' is Student’s 't' test in all cases except nale 8,, fig and
nale L linnocliaris where a Hann-ilitney '8' is presented, NS

indicates not significant at PH.85; *5 indicates significant at “8.81
and 5 indicates significant at P(8.88.

57

significant difference in mean SUL between the frogs with
large fat bodies and those without (Table 12). In female 3;
grztgrggg, the group with large fat bodies had a smaller
mean SVL. In both male and female 3; gancrivorg, the

frogs with large fat bodies had a higher mean SUL. By this
analysis, it seems the hypothesis of large fat bodies in
young frogs is generally not supported (with the exception
of female 3; erzthraeg). Working with Taiwanese B;
limggghggig, Alexander g5 $1; (1979) reported a

large variation in fat body weights among individuals of a
sample and found no correlation between fat body weight and
SUL in mature individuals.

To determine whether there was a relation between the
existence of large fat bodies and sexual maturity (defined
on pages 62 and 70), percentages of mature and immature
individuals possessing large fat bodies were calculated
(Figure 10). In female 8; gancrivgrg, B;
limnoghgris and Q 11mg, a small percentage of immature
females possessed large fat bodies. This supported
rejection of the above hypothesis. However, in female 3;

r h a, a large percentage of immatures (53%)

possessed large fat bodies when compared to mature
individuals (11%). In B; chglgonotg, mature females
possessed a comparable percentage of large fat bodies (13%)
to mature female 3; erzthrgeg, but no immature female 3*

gnglgonota were available for comparison.

58

 

 

I | l
l immature n852:
m
a e mature In=155
Rana cancrivora l |
immature ln=92 |
female ‘71
mature In- |
I I
l I I
immature I n=10 l
male I =73
mature n |
Rana limnocharzs I I
' immature n=26|
female n=31|
mature I I
l I I
immature n=1 l I I
a1
m e mature =78I |
Rana erythraea I
f 1 immature n=15
ema e mature I n=46I I
I I I
. I |
immature n=0 I
male I |
mature n=83| I
Rana chalconota . l |
f l immature ‘n=0 I |
ema e mature I n=38| |
' I
I
immature n=4
male _—
mature n=59
Ooeidozyga Zima i I 11 I
mmature n= |
IIIIII
female mature n=37l
l I l
l l I
I l I I I 6 I"I I
20 40 6 80

 

Percent with large fat body

Figure 10. Percent frogs with large fat bodies in matures and
immatures of both sexes for the five study species.

59

Immature and mature male 3; ggngrivgrg possessed
similar percentages of large fat bodies (48% and 46%,
respectively). In male 3; limnogharis, a small
percentage of immatures possessed large fat bodies (10%)
when compared to matures (40%). In male 9; limg, a
large percentage of the immatures had large fat bodies
(75%), compared to matures (49%). when comparing mature
males between the five species, high percentages of B;
ggngrivorg (46%), B; iimgggngrig (40%) and Q;
llm£_(49%) possessed large fat bodies, whereas
relatively small percentages of B; grzthrggg (28%) and
B; ghglcongtg (16%) possessed large fat bodies. In 3;
gingcivorg, g; limnggharig and Q; llmg, very
similar percentages of mature males and females possessed
large fat bodies (differences range from 2-13% of the
total), whereas in mature fig grzthrgg; and 3;
ghglggngta, quite different percentages of males and
females possessed large fat bodies (23% difference in 3;
ghglgggotg and 173% difference for 3; erythpaga).

To examine the relation between fat body size and
reproductive status of females, 'reproductively ready'
females for each species were scored as to possession of
large fat bodies and percentages were calculated (Figure
11). Criteria for Judging reproductively ready females are
described on page 83; essentially these females have mature
or nearly mature egg clutches. No clear trend was evident.

A higher percentage of reproductively ready female 3;

Rana cancrivora

Rana limnocharis

Ooeidozyga Zima

Rana erythraea

Rana chalconota

non

non

DOD

non

non

60

 

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

repro-ready

 

I
n=53 I
I
n=18I I
I | I
I I
n=29 l
I I I
n=2
I | I
I I I
n=26
l I I
n=11
' |
I I
I I
n=37 I I
ln=9 I
I I I
I |
In=38 I I
n=0 I l I
I I I
I I I
r f I 1 I I T
20 40 60 80

Percent with large fat body

Figure 11. Percent reproductively ready and non—reproductively

ready mature females with large fat bodies.

 

61

ggngniggpg contained large fat bodies than
non-reproductively ready 3; ggncrivgra. In 3‘
limgoghggig and Qg_lim;, the reverse situation
occurred. Perhaps the most obvious features of this

histogram are the low percentages of reproductively ready 3;

erythrggg and g; gnglggngtg that had large fat
bodies.

Very little study has been done on the possession of
fat bodies in relation to sexual maturity or reproductive
readiness of frogs. Alexander gt 5;; (1979) stated that
a negative correlation existed between fat body weight and
reproductive maturity in female 3; Iimggghgrig, although
no data were presented in support. In a west Javan study of
g; ggncrivorg, Church (1960b) reported that there was
great variation in possession and size of fat bodies in
females and no correlation between the presence of fat
bodies and the stage of the ovaries was found. In the
present study, it did not appear that younger frogs stored
energy in fat bodies to be used later in the production of
gametes. Perhaps the young frogs utilized all available
energy in body growth and had none to spare for an energy
reserve tissue. Further, it did not appear that females
necessarily depleted their fat body reserves with the‘
production of an egg clutch. Both Alexander g; gig
(1979) and Church (1960b) demonstrated seasonality in the
size and presence of fat bodies and this aspect will be

examined in a later section.

62

We

Males were considered sexually mature if they possessed
secondary sexual characteristics. Specifically, mature male

B... W and it limmshatia possessed

dark-pigmented throat patches and nuptial pads on their
thumbs. Mature male 3; gnzth;ggg and 3&Icnalggnogg
possessed nuptial pads on their thumbs and mature male Q;
llm; had nuptial pads on their thumbs and yellowish,
distended and wrinkled throats. Inger and Greenberg (1963)
found all Bornean male 3; ggzgngggg_with secondary
sexual characteristics had active sperm production.
Alexander 1; 3;; (1979) reported that male 3‘
llmgggngnlg without secondary sex characteristics had
small, white testes compared to the larger, yellowish testes
of frogs with secondary sex characteristics. The same
relationship was evident in the present study. Androgens
secreted by testes influence neuro-effector mechanisms for
mating calls and nuptial pad development (Rabb, 1973; Lofts,
1974), which indicates the direct relationship between
testis “maturity“ and presence of secondary sexual
characteristics in males. This Justifies the use of
secondary sexual characteristics as easily recognizable
indicators of sexual maturity.

Figure 12a presents a size-frequency histogram of
mature and immature male 3; ggnggigggg. The largest
immature male was 86 mm 80L and the smallest mature male was

59 mm SVL. There was great overlap in SVL of mature and

63

immature male 3; gangrivgrg. g; ggggrivgrg

metamorphosed from the larval state at approximately 16 mm
va.

Figure 12b presents the size-frequency histogram for
mature and immature male 3; limngghapig. The largest
immature was 40 mm SUL and the smallest mature male was 35.5
mm SUL. Alexander :1 $1; (1979) found the smallest
mature male 3‘ lfmggghgrig in Taiwan was about 28 mm
SUL. The Taiwanese males reached a size of sexual maturity
about two months after metamorphosis and were about 17 mm I
SUL at metamorphosis. B&_limnocgaris in West Java
metamorphosed at about 16 mm SVL.

Figure 12c is a size-frequency distribution for mature
and immature male 3; grzthgggg. The largest immature
individual was 48 mm SOL and the smallest mature male was 36
mm SVL. .8; enghrggg metamorphosed at approximately 20
mm SVL. Brown and Alcala (1970) considered 34-35 mm SUL as
the approximate minimum size for sexually mature males in
Philippine 3; gczthrgeg and, based on mark-recapture
technique, determined that males reached this size in
approximately 6-7 months post-metamorphosis. Brown and
Alcala (1970) found all males between 35 and 48 mm SUL
possessed well-developed nuptial pads and those 26-33 mm
long did not. Inger and Greenberg (1963) found secondary
sex characters and active spermatogenesis in all male 3‘
gnztnnggg collected in Sarawak, Borneo (SUL 31.6-44.7

mm).

A. Rana cancrivora

 

68: Mature

601
52‘;I
441
q
36:
28:
20
.22
4+
4.
12‘
20

 

 

Number of individuals

 

 

 

 

.3 .J'
“LLIII
Immature

2. r7 2'0” 183' "

Snout-vent length

 

 

 

C. Rana erythraea

: Mature
38:
34:
30‘
263
221
131
143
10-

 

I-I

 

 

 

Number of individuals
Number of individuals

 

LJ’
2 Immature

3‘brl 8458 lT

Shout-vent length

 

 

 

Figure 12.

males of the five study species.

64

Number of individuals

D. Ooeidozyga Zima

 

-

38-
34:
30:
26:
22‘
183
11.3
10:

5.

2%

Mature
"I

 

 

r.

 

24

6:

 

10“

 

TiJJ

Immature

 

 

Ill '.2'4'
Snout-vent length

B. Rana limnocharis

 

34: Mature

so? P

263
22?
18-
141

d

101
'I

 

 

 

 

 

 

LLL-J

 

r4“
“LI—T

 

Immature

 

 

T'l‘ IIT 'IVTFIT
21133145 57

Snout-vent length

E. Rana chalconota

 

: Mature
382
32.1

.I
30:
26:
22- '—
18:
14-

10“

63
2. ,.

 

 

 

 

Number of individuals

2.

6:
4 Immature
10

 

 

 

2' r2! r'S'o’“
Snout-vent length

Size-frequency distributions of mature and immature
Snout-vent length in mm.

65

Figure 12d is the size-frequency distribution for
mature and immature male 9; ling, The largest immature
male was 19.5 mm SUL and the smallest mature male was 20.8
mm SUL. Q;_llm3 metamorphosed at approximately 13 mm
SUL.

Figure 12e is a size-frequency distribution for mature
male 3;,gnglggggtg. Only mature males and new metamorphs
were found at the pond. The smallest mature male was 35 mm
SUL. B; ggglggngthmetamorphosed at approximately 20 mm
SUL.

Subsamples of testes from each species were weighed on a
Hettler electronic pan balance. The relationship between
testis weight and calculated testis volume was not
one-to-one and in all cases calculated testis volume
overestimated weight. The testis shape was slightly
flattened and departed from a cylindar, thus contributing to
the overestimation. Product-moment correlation was
performed to determine the relationship between actual
testis weight and the variables testis length and calculated
testis volume (Table 13). All data sets were distributed
normally. Correlation between testis weight and length and
testis weight and calculated testis volume were significant
in all species except Qg_llm;. However, the correlation
was greater between testis weight and calculated volume and
therefore calculated testis volume was considered a better

index of actual testis size.

66

Table 13. Proud-scent correlation results for testis veidIt vs. testis
length and testis weight vs. calculated testis vol-e.

 

 

'8' valve for '8' valve for

testis veifit testis newt
Species vs. vs. N :-

testis length calc. test. vol.
3.18.! caucuses '-75 *8 0-39 5* 53
BE! linnghggig 8.62 as 8.86 as 31
m m 8.49 s 8.79 a 18
388.! m 8.78 as 8.78 as 27
W li_a 8.87 NS 8.17 NS 17

 

'fl' indicates significant at P(8.81.
'5' indicates significant at P(8.85.
'NS' indicates not simificant, ”-8.88.

67

Figure 13 presents size-frequency distributions of
calculated testis volume for mature and immature males. No
immature male 3;,gnglggggtg,were available for this
analysis. There was a significant difference in testis size
between mature and immature males (Table 14). Inger and
Greenberg (1963) and Alexander gt gl; (1979) reported
histological data on testes for mature males only and no
histological examination was performed in the present study.
However, since the small testes of the immature males were
not producing sufficient androgens for the development of
secondary sexual characteristics, it is quite likely that
they contained only early stages of spermatogenesis.

The fact that there are different distributions of
testes sizes for frogs with and without secondary sexual
characteristics lended further support to the use of
secondary sexual characters as criteria for judging sexual
maturity. In a later section, testis size will be examined
as to any seasonality the males display in reproductive
readiness.

There was significant positive correlation (P(0.01)

between SUL and calculated testis volume in mature 3;

ggzthgggg (R-.43), 9; 11m; (R-.46), 3‘
gnglggggtg (R-.52) and B; ggncrigggg (R-.63). There

was no significant correlation found in mature B;

llmnggngglg (R-.18, P>-0.05)).

68

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A. Rana limnocharis B. Rana cancrivora
: Hatu_re _I Nature,
30 "‘ 60-1
m 26 - H m 523
.-I :1 r-I ._
g 22 -+ I— gm} L
3414 « 3. 28~
"2 - 'g 2 r
.5310 2 .,.I 20:
“a 6 ‘ —I‘I—I “a 12; Tl-L-rLI-L
: _ 7'
3 2 f k 3 4 - —
2g 2: g 41 L.
z 6 : 2:12:
10:I 20: ._II‘
14.: Immature 28: Immature
'I'I'ITF I‘I'i'riTT'lriT
4122028 15 45 75 135 195
Testis volume Testis volume
C. Ooeidozyga Zima D. Rana chalconota E. Rana erythraea
_ Mature. 2 Mature .. Mature
38- .. 38* 38-I
m 343 «:341 m 341 7
H J I; a '3 d
3 26- 326- 3 26-1 I‘
5 .1 .5 ‘ 5 ‘
-o 22. .022: .0 22:
5181+ 518j 5113f
11.. 14- 4.1144 11.14-
0 '1 ' 0 d O -l
I”.10:I I“10" H 10.
o o 1 o r
g 2-I - .3 2* g 2-
z 2; g 2; z 2‘LI‘
63 6d 6-
~ . I -I "i I .
10 Immature 10'1 Immature. 10 Immature
Irl‘I' 'I'I'I'I'lri P'Irlfi
2610 4 81216202428 26101418
Testis volume Testis volume Testis volume

Figure 13. Distribution of testis volumes for mature and immature
males of the five study species. Testis volume in cu m.

69

Table 14. lane-timer test results for diiiereece beteeee
eeae testis values at nature and i-ature sales.

 

 

lbae Testis Heaa ‘lestis Hane-
Species Volt-e VON-I Ilium
Mature Hale l-atere Hale '0'
(ca D) (co I)
m 5.19.91!!! 94.0 24.7 395!
Mm lie! 5.: - 0.9 m
m; 11m 15.3 2.3 200!
m m 7.7 0.! 20!
m mum 9-6 “- “-

 

'e' indicates significant at NO.” (tun-tailed test).
'--' indicates no data for imtere 3m ml -

70

r h t r' t

Following Inger and Greenberg (1963), female frogs were
considered immature if their oviducts were not convoluted.
Females with oviducts convoluted such that loops folded back
and contacted each other were considered mature. In the
five study species, only females with convoluted oviducts
carried enlarged ova.

Figures 14a-e present size-frequency histograms for
mature and immature females of all species. The largest
immature female 3; gangrivgrg was 106.5 mm SUL and the
smallest mature female was 68 mm SUL (Figure 14d). There
was considerable size overlap between mature and immature
female 3; ggngnlggni. This reflected natural variation
in the population and indicated there was not an absolute
size at which female 3; gagcriggcg became mature.

The largest immature female 3; limnggnggig was 51 mm
SUL and the smallest mature female was 41 mm SUL (Figure
14a). There was somewhat less overlap in size of mature and
immature female 3; limnggngglg then there was for g;
gggggiggng. In Taiwan the smallest mature female 3;
llmggsngnlg were 30-34 mm and the largest immature was
49mm (Alexander et al., 1979).

The largest immature female fi&_gnztn£ggg was 65.5 mm
SUL and the smallest mature female was 56 mm SUL (Figure
14e). As with B; limnggngcig, very little overlap in
size between mature and immature females existed. In

Borneo, Inger and Greenberg (1963) found all female 3;

Number of individuals

Number of individuals

71

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A. Rana Zimnocham's B. Ooeidozyga Zima C. Rana chalconota
16: .Mature 161 Mature l6: Hhture
-i q
12* 212- 2312.
1 T 'U -1 'C q
10: :10; 2101
s « S 84 33 8-
1 1: ' a q
6 *1 61 *1 63
4‘; t3 4: t3 44
2- —t1 La 2‘ L1 2.1
' m f: 7
2: '2 2: "LUA g -:
4. g 4: z 4:
6 « 6: 5:
8: Immature 34 Immature 3< Immature
I T1 I I l I I l l l I TI [ii I 7' T] T I Y—IV I I
20 40 80 15 35 55 75
Snout-vent length Snout-vent length Snout-vent length
D. Rana cancrivora E. Rana erythraea
12 . Nature 12 : Mature
“ 1""
10} 310 1
81 cg 8:
6 1 A :3 6 j
4 1 n—J‘ 3; 4 :
2 . _ E 2 -
w-i
zj “U I” m 2:
4 at A O 4 .-
. _ H a
6: ~ — 3 6:
8 - g Sid
a L— z j
10‘: _ 10 .
12 ‘ Immature 12 - Immature
14 . 141
I It r I1]! r T [T4 '5 TT' l T
J) 6 ' do oo'ufo 25 's ' 8'3
Snout-vent length SnoutA—vent length

Figure 14. SiZe—frequency distributions of mature and immature
females of the five study species. Snout—vent length in mm.

72

ggztngggg larger than 59 mm were mature and the smallest
mature female was 48.2 mm SVL.

The largest immature female 9; 11m; was 27.3 mm SUL
and the smallest mature female was 25.5 mm SUL (Figure 14b).
Sexual maturity in female 9; 119; was reached between 25
and 28 mm SUL. There was little overlap in SUL of mature
and immature females.

No immature female 3; gnglggggtg were collected
during any month. Figure 14c presents a size-frequency
histogram of mature female 3‘ ghglggngtg. The smallest
mature female was 52 mm SVL. It is not known why smaller
females were not found at the pond. Only mature and newly
metamorphoslng frogs of both sexes were found near the pond.
The immatures either selected another habitat or behaved in
such a way as to be less suseptible to collection.

As previously outlined, ova were classified into five
stages based primarily on pigmentation (and a sixth stage
based on whether or not ovulation had occurred). A female’s
ovaries were accordingly classified depending on the
predominant egg stage they contained. 3; cancrivora,.§;
limnocharis, B; erythraea and B; chalconota had normally
pigmented eggs with a clear distinction evident between
animal and vegetal hemispheres in enlarged ova. Large Q;
11m; ova were uniformly dark and no clear distinction
between animal and vegetal hemispheres was evident. This
made it impossible to differentiate stages 3, 4 and 5 for Q;

limg based on pigmentation.

73

Egg deposition site and presence of egg pigment are
often associated. Pigmented eggs are usually deposited in
sites that are exposed to sunlight. The dark pigmentation
may function in protection from ultraviolet radiation or
absorption of infrared radiation (Salthe and Duellman,
1973). Oviposition sites of 3; cancrivora,_ig4 limnocharis,
.34 erzthraga and 3; chalconota were often exposed to direct
sunlight and each of these species showed pigmentation in
the animal hemisphere. The exact oviposition site of Q;
11m; is unknown, but the ponds utilized for breeding
were totally exposed to direct sunlight. why the ova were
completely pigmented is a mystery. It is possible that a
countershading function is also adaptive in frogs with
distinct animal-vegetal hemispheres. g, cancrivora, g;
limnocharis, 3; erythraea and g; chalconota laid their eggs
in masses near the water surface. After fertilization, the
eggs rotate so the darker animal hemisphere is uppermost.
Potential egg predators viewing from beneath would have to
detect the light vegetal hemisphere against a light sky
background and those viewing from above would have to see a
dark egg against a dark substrate. If the highly aquatic g;
‘lflmg deposits ova at the sediment surface or at a
mid-depth, perhaps a uniformly pigmented ovum provides
better concealment.

In all species, ovaries with a complement of enlarged,
pigmented ova also contained numerous small, unpigmented

ova. These small ova were presumably the next developing

74

clutch. In stage 4 and 5 ovaries, the small white eggs were
hardly detectable, being obscured by the larger, developing
ova. Frogs which had ovulated, but not yet oviposited (that
is, contained a clutch of eggs in the oviducts), were never
encountered in 3; erythraea and were found in only one
instance each in 3; limggchgri; and Q, limg. In
these two cases, the ovaries contained stage 1 ova. Seven
3; gnglggngtg had oviducal ova and in these individuals
the ovaries contained stage 1 or 2 ova. These were the
newly developing clutch. Five individual 3; ggngciggra
had oviducal ova. One of these had ovaries that contained
stage 2 ova and another had stage 3. Three of these 3;
ggngrigggg had ovaries with stage 4 ova, suggesting that
partial ovulation had occurred. In other words, female 3;
gangrivgc; were apparently able to ovulate and oviposit
part of a clutch of eggs.

Ovaries with two or more stages of developing ova have
been noted in several tropical frogs (see Alexander :1
al;, 1963; Church, 1960a; Duellman, 1970; Inger and
Bacon, 1968; Inger and Greenberg, 1963). Partial ovulation

is likely in female figglzgnnlg galligrzag (Duellman,

1970) and was a common occurrence in Taiwanese B;
11mggghgrig (Alexander gt al,, 1963). The

observations on west Java ranids suggest that ovarian cycles
occurred continuously and provided some indirect evidence

for multiple breeding per female in an annual cycle.

75

Egg stages 1-5 were based on pigmentation, but analysis
of the diameters showed that the egg stages were distinctive
based on size as well. Figure 15 illustrates the means, 95%
confidence intervals and ranges for ovum diameter of each
stage in all five species. In general, the ova diameter
data were not normally distributed (Table 15) and
nonparametric tests were used. Kruskal-Nallis analyses
(Table 16) indicated significant differences in diameters
among the egg stages of each species. Mann-Whitney tests
for egg diameter differences between adjacent egg stages
were significant in all cases where sample sizes were
sufficient (Table 16).

In a few cases, egg diameters for ovulated eggs (stage
6) were available. On average, little growth occurred
between a stage 5 and a stage 6 ovum. Five individual 3,

nc iv r stage 6 ova measurements (mean = 1.44 mm)
were Just slightly outside the 95% confidence interval for
stage 5 B; gansrivggg egg diameter. In seven individual
a; gnglggggtg, the egg diameters of two ova were outside
the 95% confidence interval for stage 5 a; chglgongtg
egg diameter, but the mean for all seven (8 1.46) was inside
the confidence interval. In single observations for B,
Limnggngnlg and Q, 11mg, the stage 6 ovum
measurement (1.37 mm and 1.13 mm, respectively) were Just
outside the confidence intervals for stage 5 ova of these
species. These data indicated that a stage 5 female of any

species was very close to ovulation.

76

 

 

 

 

 

 

 

 

 

 

5 Hana cancrivora
- -————E$E+———-
4 - -————————45$Ee—————-
3 ' ———-£EE$EEs——————-
2 - -—-—£EE$EE!*
1‘4
5 Rana erythraea
- -——————4E$a————————
4 - ,___+___,
3,. C———===__——:|'
2 - -£E§EB—
1- Eli—
3 5 Hana chalconota
' —$———
314% ———~EE———
‘531- +
s 2 ' i
51" "
5 Rana limnocharis
- -—+:E$EE§———
4. —¢—-—.
3 . __p_
2- l
1. $—
5 Ooeidozyga Zima 1
- —_$__
3- $—
2 b fEEEFEEB—-———
1- $—

 

 

 

' I’j’I ' I ' I ' I ' I I I I I7'7I’r I I I ' I ' I ' l I I ‘ I r“I
0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6

Ovum diameter (mm)
Figure 15. Means (vertical bars), ranges (horizontal lines) and 95%
confidence intervals (horizontal rectangles) for ovum diameters of
the five ovum stages.

77

Table 15. Egg dineter data (in I) for all oea stages.

 

 

lbaa
Species Stage 00- Dia 9510.1. ltaege M finality
gm cancrim! 5 14 1.29 1.25-1.34 1.13-1.44 5.6 ill
he; cancrivora 4 43 1.05 1.01-1.10 0.77-1.26 13.2 M
Mgaecrieorg 3 13 0.74 0.66-0.03 0.54-1.01 10.4 00
£00.! cangrivga 2 14 0.51 0.43-0.59 0.32-0.07 20.4 Ml
£20.! ‘00:"!!! 1 90 0.16 0.14-0.17 0.05-0.37 44.2 ill
malimggbaris 5 11 1.24 1.16-1.32 1.11-1.41 9.2 101
3.40! limgharis 4 22 1.04 1.01-1.00 0.05-1.17 6.6 ill
33E limnocharis 3 2 0.51 - 0.46-0.55 12.6 -
gm limggm’s 2 1 0.32 :-- -- -- -
Mlimgbgis 1 32 0.12 0.11-0.12 0.11-0.2 17.0 ill
Mgrztbrna 5 30 1.50 1.46-1.54 1.27-1.75 7.0 ill
_ii_a_n_a_ erzthraga 4 10 1.14 1.03-1.25 0.77-1.27 13.3 YES
3.0!! erzthraea 3 3 0.79 0.40-1.09 0.60-0.92 15.5 -
3m erzthrgeg 2 7 0.50 0.44-0.56 0.40-0.50 12.3 ill
gag; erzthrag! 1 22 0.12 0.10-0.13 0.11-0.21 23.6 00)
Mchalcmgta 5 14 1.44 1.30-1.50 1.27-1.67 7.2 M
m; chalcmotg 4 13 1.20 1.09-1.30 0.09-1.44 14.0 00)
BM; chalcgggta 3 2 0.62 - 0.57-0.67 11.5 -
EB chalconota 2 3 0.53 0.15-0.90 0.37-0.67 20.6 -
Lag; sgalgongtg 1 1 0.27 - - - -
My!” 5 32 1.04 1.01-1.07 0.06-1.13 7.0 00
Ooeidozzgg ii 3 5 0.66 0.54-0.79 0.59-0.04 14.9 -
ggidozzgg ii 2 9 0.43 0.34-0.52 0.33-0.66 27.0 ill
9931932213.! 1 13 0.13 0.11-0.14 0.11-0.21 25.1 Ml

 

'0.I.' is confidence interval.

'M' is coefficieet of variation.
'Nnrsality' is as deternined by Kolguorov-aeirroe test.

'--' indicates ssall saple si

78

Mean ovum volumes for each egg stage were calculated
from egg diameters, assuming an egg to be spherical (Table
17). Ovum volume changes drastically from stage 1 to stage
2 (mean for the five species is 37 times). The change from
stage 2 to stage 3 (mean I 3x), stage 3 to stage 4 (mean I
5x) and stage 4 to stage 5 (mean = 2x) is smaller and fairly
consistent among the species (Table 17).

Despite absolute differences in egg size between
species, the ova of each species matured in a similar manner
in terms of pigment deposition and size increases between
stages of development. Presumably, these were
characteristic egg maturation patterns of ranids in general.

As eggs mature and increase in mass there should be a
concomitant increase in the mass of the ovaries. Ovarian
weight data for the five ovum stages are presented in Table
18. The data were not normally distributed. The weight of
each stage ovary was significantly different from the
adjacent stages for all species (Table 19). The only
exceptions were in instances where sample size was small.
These findings paralleled the differences between stages of
egg diameter.

It is important to consider frog size when analyzing
egg diameters and ovarian weights because there is
frequently a positive correlation between body size and
these reproductive parameters (Kaplan and Salthe, 1979;
Salthe and Duellman, 1973). SUL data for females containing

each egg stage are presented in Table 20. The data were not

79

Table 16. Nonparaetric test results for cuparisoos of ova diaaeter
betueee ova stages.

 

 

Krvslal-tiall is Test Hun-Hitoer Test Statistic

Species Stages '0' Stages Stages Stages Stages
statistic 4/5 3/4 2/3 112

mm 1-5 73.42' 269! 2454163! 200!
BE lisogllgis 1-5 40.3 I 214 l 40 I --- 20 2
M m H 47.4 a zoo in 29 e 21 a 140 a
3,9; mm 1-5 22.3 e 162 as 26 a 5 a --
ggggmg L113 14,: 41.3 a m a 41 a m a

 

'l' indicates simificant at P(0.05 (two-tailed test).
'--' iedicates saall sable size.
First haee-thitoey cuparisoo for m 1.5;! is between stages 3 ad 5.

80

Table 17. been values (in ca u) of the 5 stages of one and increase in value
iru one stage to the neat.

 

Species Stg 1 Stg 2 Stg 3 Stg 4 Stg 5 Val Inc. Vol lac. Val Inc. Vol inc.
Val Val Val val Vol 1-2 2-3 3-4 4-5

 

mm 2.141147 1.21 1.32 1.14 33.» 3.0x 3.0x 1.011
mm 1.911 1.12 1.17 1.59 1.» 22.3: 3.33 0.4a 1.7:
mm 1.91. 1.17 0.26 0.70 1.77 77.11: 3.7x 3.0x 2.3x
03115331593933 1.11 1.111 1.12 1.91 1.56 0.0x 1.5x 7.6x 1.7:
mm v.94: e.e4 11.15 -- 1.59 43.0: 3.3: 13.9111

 

'Stg' indicates stage; 'Val' indicates value. .'1nc.' indicates increase.
'e' indicates naltiply the preceedieg 11qu by 0.001 for the actual value.
'1 l'; Vol.1nc. fru stage 3-5 for My; lina

81

Table 10. Ovarian neigbt (in was) for all ova stages.

 

 

Species Stage li- llean 952 0.1. Range 002 Narnality
Lag; cancrivorg 5 14 15.9 11.2-20.6 5.6-40.0 51.2 ill
gm cancrivora 4 43 9.1 6.7-11.4 0.7-42.7 04.1 ill
m; gacrivgfl 3 13 2.9 1.6-4.2 0.7-6.6 73.1 ill
30!! cgncrivggg 2 14 1.1 0.6-1.6 0.2-2.9 75.9 ill
39; m 1 90 0.2 0.2-0.3 .02-1.0 01.4 M
£00! linnggliaris 5 11 1.4 0.9-1.9 0.5-3.1 52.5 M
3m linnocnarig 4 22 0.9 0.7-1.2 0.4-2.5 63.0 10)
BE! linngbari; 3 2 0.4 -- 0.2-0.7 70.7 --
39.03. linnggharig 2 1 0.1 - -- - -
In; linnghgis 1 32 0.1 .04-.07 .01-0.2 7 .7 ill
li_ang erztnrgea 5 30 1.6 1.4-1.0 0.9-2.7 31.0 ill
no; erzthragg 4 10 0.0 0.7-1.0 0.4-1.0 23.9 10)
Lan_a erztltraeg 3 3 0.6 - 0.3-0.0 45.6 -
fig; erztnrggg 2 7 0.4 0.3-0.5 0.2-0.5 35.6 ill
Lag; erztbragg 1 22 .06 .04-.00 .01-0.1 73.2 ill
Lam chalcongtg 5 14 2.7 2.2-3.2 1.6-4.5 32.0 Ml
fig; chalconota 4 13 1.6 1.2-2.0 0.6-2.0 41.5 140
fig; chalconota 3 2 0.6 -- 0.5-0.6 12.9 -
Lag; chalconota 2 3 0.3 0.1-0.9 0.3-0.6 32.7 N0
m; chglcongtg 1 1 0.3 - -- -- -
m ii; 5 32 0.3 0.2-0.3 0.1-0.5 7.0 010
m l!!! 3 5 0.3 0.1-0.4 0.1-0.4 47.0 -
hidozzga Li; 2 9 0.1 .04-0.1 .04-0.1 52.5 ll
Qgidazzgg li_a; 1 13 .03 .02-.04 .02-.04 35.5 00)

 

'0.1.' is confidence interval; 'M' is coefficient of variation.
'anality' is as deternined by Kolguorae-uirnav test.
'--' indicates snall suple size.

82

Table 19. Nonparaeetric test results for cuparisons of ovarian newts
betveee ova stages.

 

Kreslal-tiall is Test Hann-tibitney Test Statistic

Species Stages '0' statistic Stages Stages Stages Stages
4/5 3/4 2/3 1/2

 

mm 1-3 60.0! 24111 2411 15011 2354
3311; linnacbaris 1-5 41.3 a 162 1 34 us «- 17 4
mm 1-5 52.31 1331 22113 16145 67!
gm 5131:9961; 1-5 19.7 a 1511 4 26 1 4 a --
m m; 1-3,5 36.0 a 52 113 43 a 112 a

 

'1' indicates significant at P(0.05 (two-tailed test).

'NS' indicates nan-significant at ”80.05.

'--" indicates snail sable size.

First Hann-tluitney cuparisan for W 112; is between stages 3 and 5.

83

distributed normally and Kruskal-Uallis and Mann-whitney
tests were used for comparison (Table 21). In general,
Stage 2, 3, 4 and 5 females did not differ in SUL (except
for stage 3 and 4 g; caggriggrg). Stage 1 and 2 frogs
usually differed significantly in size because the stage 1
group also contained immature females which were of smaller
size. Any correlation between frog body size and ovarian
weight or egg diameter would be evident only in frogs with
enlarged ovarian eggs. The fact that stage 3, 4, and 5
frogs were similar in size within each species allowed an
unbiased analysis of egg diameters and ovarian weights
between the egg stages with frog size controlled.

Female frogs were classified as 'reproductively ready“
if their ovaries contained predominantly stage 4 or 5 ova.
In Taiwan, Alexander gt film (1979) used a similar
staging process for ovaries with their classes 4 and 5
roughly equivalent to stages 4 and 5 of the present study.
These workers designated females of classes 4 and 5 as
reproductives based on the fact that pituitary injections
induced ovulation in class 5 females, resulting in class 4
or 5 ovaries. Further, their class 4 females contained eggs
that were under 0.8 mm diameter. Stage 4 female 3;
limngsngnlg in the present study had a mean ovum
diameter of 1.04 mm, considerably larger, and presumably
closer to breeding than the class 4 Taiwanese frogs that
were considered reproductives by these researchers. Inger

and Greenberg (1963) designated female 3‘ ggztnnggg as

84

Table 20. Scoot-vent length data (in u) for ova stage 1-5 fenales for

the five study species.

 

 

Species Stage N- ltean 952 0.1. liange 1100 than
RA; cancrivggg 5 14 107.9 102.1-113.0 00.0-119.0 9.4 M
3333 cangrivorg 4 43 90.0 94.2-101.9 75.0-110.0 12.7 M
3m cancrivorg 3 13 00.6 77.7-99.5 62.0-110.0 20.3 ill
5m cancrivgg 2 14 90.6 04.0-97.2 76.0-114.5 12.6 10
gm cangrivggg 1 90 72.0 60.0-75.2 29.0-100.0 21.1 10
5;” linnocbggi; 5 11 54.6 49.0-59.4 41.0-62.5 13.0 10)
m linnacngis 4 22 51.0 50.5-53.1 47.0-57.0 5.7 M
3.92! linnocbarig 3 2 56.2 -- 53.5-59.0 6.9 --
33g; linnacbaris 2 1 44.0 - - - -
gm linnggbggis 1 32 35.4 32.2-30.6 10.0-51.0 25.1 10)
Lag; erythraea 5 30 67.3 65.7-69.0 50.5-70.5 6.6 ill
gm erzthragg 4 10 67.6 64.4-70.0 60.0-72.0 6.5 ill
3.3.0.3. erzthraeg 3 3 65.7 44.5-06.0 56.0-72.0 13.0 -
£02! erzthrggg 2 7 64.4 59.2-69.6 55.0-69.0 31.5 140
EL! erztbrgea 1 22 39.5 33.9-45.0 21.0-65.5 31.0 10)
300.4. ctalcggtg 5 14 66.7 62.4-71.0 56.0-77.7 11.3 no
3M! chalcgotg 4 13 63.0 60.3-67.4 53.6-72.5 9.2 ill
£0.02 chalgonotg 3 2 61.0 -- 57.0-65.0 9.3 -
90.4 chalgggta 2 3 67.2 60.0-73.5 65.0-70.0 3.0 -
3m cbglcgggtg 1 1 70.5 -- -- -- --
My; 1.!!! 5 32 32.6 31 .0-33.4 27.2-36.5 6.0 ill
Mm Ii 3 5 31.3 25.3-37.3 25.5-36.5 15.4 --
Mm ii 2 9 29.9 27.2-32.7 26.5-35.0 12.7 101
Mm ii 1 13 22.0 20.0-25.5 14.0-29.5 21.1 101

 

'0.I.' is confidence interval; 'M‘ is coefficient of variation.
'Narn' is nornality as deternined by llalguarov-uirnov test.

'--' indicates snail suple size.

85

Table 21. Nonparuetric test resalts for cuparisans of snout-vent lengths
uoeg fenales of different ova stages.

 

Krastal-lfall is Test Hann-tibitney Test Statistic

Species Stages '0' statistic Stages Stages Stages Stages
V5 3/4 2/3 1/2

 

Lag; gggrivora 1-5 33.3 I! 177 NS 202 I 101 NS 227 4
11333111111951.3113 1-5 34.3 a 149 143 34 143 -- 16 11
0433222112313 1-3 37.413 1211143 16143 14143 1364
m; 91.1ch 1-5 3.3 143 1111 14s 17 143 -- --
m li_na 1-3,5 24.3 as 61 NS 20 NS 102 a

 

'50' indicates significant at P(0.01.

'3' indicates significant at P(0.05 (tun-tailed test).

'NS' indicates non-significant at 9180.05.

'--' indicates snail suple size.

First Hun-Unite" cuparison for m Hg is between stages 3 and 5.

86

'ready to breed' if they contained “enlarged ova" (using
four stages of egg size).

The criteria for judging reproductively ready females
are obviously artificial, but hopefully follow some law of
parsimony. Designating stage 4 and 5 females as
reproductively ready was justified because the polarized ova
are easy to recognize, appear in coloration and size as the
ova that will be deposited during breeding and, based on the
work of Alexander gt 5;, (1979), are close to breeding
time. The actual time until breeding for a stage 4 femaie
is not known and would be difficult to determine without
surgical techniques. Further, the surgical technique itself
would undoubtedly affect the egg maturation process as part
of the frog’s available energy would be devoted to wound
repair.

As previously mentioned, separation of stages 3, 4 and
5 in Q‘,llm; was precluded because of heavy ovum
pigmentation. As a result, female 9; 11m; were
categorized as reproductively ready based on ovum diameter.
The criterion for this classification was determined as
follows. For B; cancrivora, g; limnocharis, 3; erythraea
and fl; chalcgnota, the ovum diameter of the lower end of the
stage 4 95% confidence intervals (Table 15) is an
approximate ovum size at which these frogs enter the
reproductively ready category. A relative index of this
size is a percentage of mean stage 5 ovum diameter for each

species (Idlameter of lower end stage 4 95% CI] / (mean

87

stage 5 diameter) x [100]). The percentages for g;
cancrivora, 3; limgocharis, 3, gnztnnggg and B; gnglggngtg
are 78%, 81%, 69% and 76% respectively (mean for all four is
76%). The largest Q; limg ovum diameter was 1.13 (from
Table 15), and 76% of this diameter is 0.86 mm. Thus, any
female Q;_llm; with ova whose mean diameter was equal to

or greater than 0.86 mm was considered reproductively ready.
These ova were designated as stage 5 and no stage 4 category
was applied to Q; 11mg.

The mean stage 5 ovum diameters in ascending size
(Table 15) were Q; 11m; (1.04 mm), B; limnocharis (1.24 mm),
3; ggncrivora (1.29 mm), 3; chalconota (1.44 mm) and 3;
erythraea (1.50 mm). Ovum diameters were significantly
different for the five species (Kruskai-wailis test, H I
61.23, P(0.01), but pairwise comparisons using Mann-whitney
tests (Table 22) showed that mean ovum diameters were not
significantly different for the pairs 3; limnocharis/B;
cancrivora and 3; erythraea/B; chalconota. It would appear
that ovum diameter similarities between these species
followed taxonomic relatedness.

Terentyev (1960), working with Eurasian 3533, and
Salthe (1968, 1969), working with saiamanders, demonstrated
interspecific positive correlations between female body size
and ovum size. Salthe and Duellman (1973) found that,
within a reproductive mode, a positive correlation existed
between ovum diameter and SUL among anuran species. Figure

16 is a plot of mean stage 5 ovum diameter against mean

88

Table 22. Results of Mann-Uhitney tests for
differences in ovum diameter between species.

 

 

Species Compared U 8
Qogidggzga lima / Rana limnogharis 209.0 *
Bgna limnocharis / Rang gangriggr; 101.5 NS
Rana cancrivgrg / Rgng ghglcoggtg 178.5 a
Rgna gnalcoggta / Ran; erzthrgea 182.0 NS

 

'e' indicates significant at P(0.05 (two-tailed test).
'NS' indicates not significant, P>=0.05.

89

stage 5 female SUL for the five study species. Considering
all five, the product-moment correlation coefficient is 0.47
and not significant (P>-0.05). The point for g;

ggngnigggg lies along quite a different line than that

for the remaining four species. In fact, the correlation
coefficient for g;_limnocharis, 3; erythraea, B; chalconota
and Q; leg_aione is 0.98 and significant (P(0.01). The
regression line and equation for these four species are also
presented in Figure 16.

Crump (1974) stated that, within the generalized
reproductive mode (frogs that deposit eggs directly in
water), species with the largest clutch sizes also have the
largest ovum diameters and that this relation was probably
due to larger body size. In contrast, 3; gangrigor; is
by far the largest frog in this study, yet its ovum diameter
is not significantly different from the second smallest frog
(Bl MW)-

Salthe and Duellman (1973) stated that an intraspecific
correlation between body size and ovum size must precede an
interspecific correlation of the same kind if the notion is
accepted that intrapopuiation variability is the ultimate
source of raw material for adaptive evolution. To check for
an intraspecific correlation between body size and ovum
size, product-moment correlation analysis was performed on
SUL and ovum diameter of stage 5 females of each species

(Table 23). B; limnggharig and Q; lima were the

only species that showed a significant positive correlation.

Ovum diameter

90

 

 

 

 

 

 

 

 

_ Dotted line is the //
1-60‘1 regression for all spp. /
4 except Rana cancrivora /
1.50-1 y = 0.61 + 0.01(x) +/ Rana erythraea
' 7+’Rana chalconota
1.40 - /
1 /
1.30 - // Rana cancrivora +
' /'-f Rana limnocharis
1.20 - /r
‘ /
1.10- /
- .f/'Ooeidozyga Zima
*‘1 1' r 1 1 r T 1"r T'1 i i l i T l T I l i T’T
10 20 30 40 50 60 70 80 90 100 120

Snout-vent length (mm)

Figure 16. Relationship between mean ovum diameter and mean
snout-vent length for stage 5 females of the five study species.

91

Table 23. Product-moment correlation analysis
of snout-vent length and ovum diameter of
stage 5 females.

 

 

Species N- R- Significant
‘ggg; limnocharis 11 0.75 ** YES
Egg; ghalcgnotg 14 0.34 N8 N0
3911; erzthragg 30 0 .20 NS N0
gggg caggriggra 14 -0.23 NS N0
Oogiggzzga 1393 32 0.41 * YES

 

'nn' indicates significant at P(0.01.
'4' indicates significant at P(0.05.
'NS' indicates not significant, P)=0.05.~

92

McAlister (1962) showed that larger female Egg; gigiggg
have larger ova within a given population. In two species
of hylids, Crump (1974) found a significant intraspecific
negative correlation between body size and egg diameter.
Table 24 summarizes ovarian weight data for
reproductively ready females of the five species. The data
were not normally distributed. In 3; cancrivora,.3;
limnocharis, B;_erzthraea and 3; chalconota the left ovary
was frequently larger than the right, but the mean weight of
left and right ovaries was not significantly different in
any of the species (Table 24). Working with g;
ggngcivgrg, Church (1960b) also found the left ovary was
heavier than the right in most instances. These findings
indicate the importance of measuring both ovaries when
calculating clutch size or total ovarian weight. Inger and
Bacon (1968) assumed left and right ovaries equal in size
and used only the left ovary volume when calculating number
of ova in Bornean frogs. Had the same assumption been made
in the present study, it would have would resulted in up to
a 17 percent overestimation in clutch size.

Correlation analysis was performed between body weight
and ovarian weight for reproductively ready females of each
species (Table 25). The correlation was positive and
significant for each species, indicating that a larger
individual was able to accomodate a larger mass of eggs.
This relationship was also examined among species, using

mean live weight and mean ovarian weight for reproductively

93

Table 24. Left and riut ovary heights (in mus) for repradnctively ready fenales.

 

 

itt.or Lt. lfean 21H» Tines 14-41
59. W01" 14' “1’0 WEI. I” MI L72 L32 UR I
hump-11m L 57 3.9 4.7-7.1 1.4-24.9 14a
46 4 11 224.518
3.14% it 57 4.9 3.0-5.9 0.3-19.7 16
13931111951311; 1 33 .51 .4o-.72 .22-1.6 14a
61 27 1. 227.5143
mm R 33 150 .39'.“ 120-416 m
mm In 27 412 19‘74e3 .34'2.3 m
74 4 22 235.506
m m R 27 41‘ 183-1 e2 .39'1 n, m
11mm 1 41 1.3 .67-.07 .21-1.4 14a
09 5 15 253.0045
mm R ‘0 0.7 157’s?“ e45-1e3 m
0111112221111!!! 1 32 .14 .12-.1s .13-.21 140
22 63 16 2.6.4045
mm R 32 e13 n42‘e15 .45'.” m

 

'Sp.‘ indicates species; '01. or Lt.‘ indicates right or left ovary.
'0.1.' indicates confidence interval.
'Norn' is nornality as deternined by Kolguorov-Sairnov test.
'11-0 0' is the liann-thitney test 11, 16 indicates not significant at ”-0.05.

94

Table 25. Product-moment correlation between live
unight (LH) and ovarian weight (0") and between live
weight and percent live weight contributed by ovaries
(ZOU) in reproductively ready females.

 

 

Species N- LU vs. 0“ Lu vs. 20“

Egg; gbalggngta 27 R I 0.618 ** R =-0.270 NS
By”, ggncrivgrg 57 R =- 0.692 *4! R = 0.219 NS
55g; limngchgrig 33 R a 0.647 in R a 0.276 NS
33.0.! grzggrgeg 40 R = 0.512 5* R a 0.093 NS
Qgglgggzgg_llmg, 32 R = 0.815 in R 8 0.325 NS

 

'ii' indicates significant difference at P(0.01.
'NS' indicates no significant difference at P(0.05.

95

ready females. The data were transformed to their natural
logarithms to minimize the spread of data points. There was
a significant positive correlation (R-0.99, P(0.01) and the
regression line is plotted in Figure 17. The larger species
accomodated larger egg masses. Crump (1974) reached a
similar conclusion in a community of Ecuadoran anurans.

The percent body weight contributed by ovarian weight
(“percent ovarian weight') was calculated for reproductively

ready females. The order of increasing mean percent ovarian

weight was: L ggzthgagg (6.57.) ( _O_L lim; (6.87.) <

B; limnggharis (7.9%) < 3‘ gangrivgrg (10.1%) < B;
chglcgnggg (11.7%). The data are given in Table 26.

The mean percent ovarian weights are significantly different
for the five species (Kruskal-wallis test, H - 25.3 is,
P(0.01). Pairwise comparisons using Hann-Uhitney tests
indicated that B; gnzthgggg, g;_llmg and a;
limnggngcig are not significantly different in percent ovary
weight (Table 2?). 3; limggcharig and 3; ggggnlggra
are significantly different, but 3; gancrivgr; and 3;
snglgggota are not (Table 27).

Percent ovarian weight was not significantly correlated
with body weight in any of the five species (Table 25).
Further, mean percent ovarian weight was not significantly‘
correlated with mean live weight (R=0.43 NS, P>=0.05) among
species. This contrasted with Crump’s (1974) findings where
there was a significant negative correlation between body

size (SUL) and percent clutch volume among species. She

‘96

 

 

 

: Regression equation: 7
; y = -2.82 + 1.12(x)
j R a 0.99
2.0‘1
«l
1
1

e ovarian weight (a)
P i-
c> c>

Log

I
H
O

.nIALnnLLuLLJaJLlnieeILLn

l

/

 

Rana chalconota '1’

Hana limnocharis

/

Rana cancrivora '1’

  
    

.f

"1' Ooeidozyga Zima

4' Hana erythraea

 

'f""rT"IU_T—_FITIII‘ITVI

1.0

Figure 17. Relationship between mean live weight and mean ovarian

2.0

IIUITT'UIUU'IT'V

3.0

Loge live weight (g)

Ulf

4.0

rrfl'nfi

weight of reproductively ready females (ova stages 4 and 5) for

the five study species.

 

97

Table 26. Live ueifit in was (Lil), ovarian ueidit in gras (ill) and
percent live weight contributed by ovarian ueifit (1110f) in reproductively
ready fenales.

 

 

Species 11- Variable hean 9502.1. Range Nasal
310.1. cangrivgg 57 LB 102.4 92.6-112.3 42.0-206.0 101
gm linngtgrig 33 Lil 13.3 12.1-14.5 0.1-21.0 ill
33g; erythraea 40 Lil 21.3 20.1-22.6 14.0-33.0 M
£10.! 9.3199393! 27 Lil 19.1 16.6-21.6 9.5-35.0 ill
Mm flu 32 Lil 3.9 3.6-4.2 2.3-5.4 ill
M cgngrivgn 57 02 10.7 0.6-12.9 0.7-42.7 ill
£00! lisngglgig 33 (II 1.1 0.0-1.3 0.4-3.1 Ml
Lag; erzthrae; 40 ill 1.4 1.2-1.6 0.4-2.7 101
gm chalcgggtg 27 (It 2.2 1.8-2.5 0.6-3.0 110
mm Lia 32 W .27 .24-.30 0.1-.45 M)
3m gancrivgg 57 mi 10.1 0.7-11.4 1.7-26.5 10)
Lap; linnocbari; 33 2111 7.9 6.5-9.2 11.5-19.2 ill
Lag erythraea 40 lef 6.5 5.7-7.2 2.3-10.0 10
gm cbalcongtg 27 ZN 11.7 10.3-13.2 3.2-16.3 110
Mm fig 32 201 6.0 6.3-7.3 3.4-9.1 YES

 

'CJ.’ is confidence interval; 'M' is coefficient of variation.
'Noreal' is nornality as deternined by Kolgnorov-hirnov test.

98

Table 27. Results of Mann-Hhitney tests for
differences in percent live weight contri-
buted by ovaries (Z ovarian weight) between
species.

 

 

Species Compared U =-
34.0.1 gczthragg / Ooeigggzgg j_i__rn_a_ 228.5NS
Oogidgzzga 11m; / Egg; limggchgrig 212.0 NS
Egg; limggghgrig /‘g;gg gangrivgrg 282.0 !
figgg ggggrivor; / gig; ghglconota 229.5 NS
$.03 grzthrgga I 3m limnggharis 243.0 NS

 

'i' indicates significant at P(0.05 (2-tailed test).
'NS' indicates not significant, P>=0.05.

99

concluded that, as body size among species increased,
proportionately less of the total frog volume was devoted to
egg mass, reasoning that larger species had proportionately
larger amounts of supportive tissue. In contrast, in the
present study, the largest frog (3; gangcivgra) had

a percent ovarian weight that was not significantly
different from the frog with the highest percent ovarian
weight (3; gnglggggtg) and the smallest frog (Q;

limg) had a percent ovarian weight that was not
significantly different from the frog with the smallest
percent ovarian weight (3; erzthrgeg). The west

Javan ranid frogs did not follow the same relationship noted
by Crump (1974).

Two other studies that presented information for
percent ovarian weight were Alexander :3 3;; (1963),
working with g; i no r , and Church (1960b) working
with 3; ggnggivorg. The Taiwanese 3, limnggngpig
had a mean percent ovarian weight (8%) very similar to the
Nest Javan g; limnggnggig, Church studied 3‘
gangglgggg from Jakarta, Nest Java and reported a mean
percent ovarian weight (4.3%) that was considerably smaller
than for the Bogor area 3, 5535512923. This small value
resulted from Church using all classes of females in his
calculations. In the present study, only reproductively
ready females were used.

Table 28 contains means and other descriptive

statistics for clutch size (number of enlarged ovarian ova)

100

for each species. The order of increasing mean clutch size
was: 9; lim; (434) < 34 erythraea (1,304) < B; limnocharis
(1,750) < 3; chalconota (2,207) < 3; cancrivora (13,611).
The data were not normally distributed. A Kruskal-wallis
test indicated that clutch sizes for the five species were
significantly different in terms of number of ova (H -
75.3**, P(0.01). Pairwise comparisons using Mann-Whitney
tests indicated that the pairs 9, Lima / 3; erythraea, B;
Limnggngplg / 3; ghalconota and B: chalconota /.§;
cancrivora were significantly different in mean clutch size,
but 3; erythraea and 3; limnocharis were not (Table

29).

Little information is available from the literature on
clutch sizes for the five study species. Berry (1964)
reported a range in clutch size of g; limnocharis in
Singapore of 504-2259, similar to the range of west Javan E;
1i ggcharig. Alexander ;; 5L; (1963) reported that
.3; limnoghgrig oviposited between 30 and 2400 ova. Liem
(1959) gave a mean of 1575 and range of 1000-3250 for clutch
size of West Javan 3; chalcongta and Alcala (1955)
reported that Philippine 3; erythraea had a clutch size
of 1200 to 1900. These figures are similar to the present
study’s finding of clutch sizes for 3; chalconota and B;

r hr , respectively.

The coefficients of variation for clutch size (Table
28) indicated that 3; cagcrivora, B; limnocharis and
Q; ling had high variability in the clutch size, 3;

101

Table 20. Clutch sizes in feeales vitb covntable ova.

 

 

Species 10- ilean Clutch Size 9510.1. Range Noreal M
3m gangrivora 59 13611 11733-15409 3333-35503 Ml 52.9
3:3 mm; 26 1750 1368-2132 667-4167 101 54.0
M Eli-”LE! 34 1304 1154-1454 503-2400 ill 33.0
5.000 13.33321! 30 2207 2030-2383 1417-3000 10) 21.4
M1291!!! 11;; 23 437 353-515 150-900 101 43.0

 

'0.1.' is confidence interval; 'LVZ' is coefficient of variation.
'liornal' is nornality as deternined by Kolgcnorov-hirnov test.

102

Table 29. Results of Mann-Whitney tests toe
differences in clutch size between species.

 

 

Species Compared . U i
agglgggzg; lima / gang grzthrgg; 279.5 a

3193, 32.23.0133 / Rgng lignggharis 216.5 NS
ggng limngchggig / 3391 ghalggggt; 272.0 !
Bang ghalgonotg / 33g; gangriggrg 400.0 3

 

'i' indicates significant at P(0.05 (2-tailed test).
'NS' indicates not significant, P)-0.05.

103

gnglsgngt; had the lowest variability and 3;
ggztnngg; was intermediate.

Within a population, increasing female size is often
associated with increased clutch size (Henderson, 1961;
Kaplan and Salthe, 1979; Oplinger, 1966; Pettus and
Angleton, 1967), but Crump (1974) found a significant
positive relation between female body size and clutch size
in only 11 of 41 species she studied. In the present study,
4 of 5 species had significant positive correlations between
body size and clutch size (Table 30). B; cangpivgrg,

Q; Lim; and fl; erythraea demonstrated a significant .
positive correlation between clutch size and both LN and
SUL, 3; limgggnggig had a significant positive

correlation between clutch size and LN only, and 3*
gnalggngtg showed no significant relationship between

clutch size and body size (Table 30). Table 31 presents the
data on mean SUL and Lu for females with enlarged ova that
were used in these correlation analyses.

Clutch size-body size relationship can also be examined
among species. Salthe and Duellman (1973) concluded that,
within a reproductive mode, larger species produced more
eggs and Crump (1974) supported their conclusion with her
work. Figure 18 is a plot of the regression between mean
live weight and mean clutch size for each species. Data
were transformed to their natural logarithms to reduce the
.spread of data points. The correlation coefficient was

positive and significant (R - 0.97**, P(0.01). Thus, these

104

Table 30. Productfimoment correlation between snout-
vent length (SUL) and clutch size (0 of Ova) and
live weight (LH) and clutch size.

 

 

Species 30L vs. 0 of Ova LU vs. 0 of Ova
31g; giggrivgr; R I 0.62 n! R I 0.66 *5
355; linngghgrig R I 0.31 NS R a 0.44 !!
Rgga grzthrggg R 8 0.37 e R I 0.42 O
m; 5313352093.! R --0.07 NS R --0.01 NS

0211991191131 R=O.55es Its-0.513

 

'i!‘ indicates significant at P(0.01.
'n' indicates significant at P(0.05.
'NS' indicates not significant, P)=0.05.

105

Table 31. Scoot-vent length (311.) in nillineters and live weight (Lil) in was of
feeales vitb countable ova.

 

 

Species ii- Uar iable hean 9540.1. Range lioreal M
m M 59 ill 100.2 96.0-103.6 76.0-119.0 ill 13.1
m linnggbarig 26 M 53.0 50.9-55.1 41 .0-62.5 101 9.0
li_ag grztbrgeg 34 svc 67.0 65.5-60.4 60.0-72.0 Ml 6.2
gm cgalcongtg 30 30. 64.2 61.4-66.9 52.7-77.7 N0 11.3
Qidozzga ii 23 311. 31.7 30.4-32.9 25.5-36.5 141 9.3
£a_ng sancrivgg 59 Lil 102.4 92.6-112.2 42.0-206.0 no 36.0
BE! linnocharis 26 1.0 13.9 12.4-15.4 0.1-21.0 ill 14.5
m erzthrgeg 34 Lil 20.0 19.6-22.0 15.0-30.7 101 16.0
8303. ghalcmgt! 30 Lil 10.9 16.7-21.1 9.5-31.5 NO 35.5
m L191 23 Lil 3.7 3.3-4.1 2.3-5.2 YES 25.2

 

'0.1.' is confidence interval; 'M' is coefficient of variation.
'Nornal' is nornality as deternined by Kolguorov-Snirnov test.

106

 

    

Rana cancrivora 4*

   

\O
O

lull:tJiltiiJlitJillittliitiltnitltjtilt;tiliiii

 
   
  

m
N 8.0
"-4
m 1
Rana cnalconota
': e 1 e
3, Hana sznocnarts '1-
.3
U + Rana erythraea
w 7.0
a
o
p:

 

4F Ooeidozyaa Zima Regr9951°n equation:

 

 

 

 

6.0
y = 4.6 + 1.02(x)
R = 0.97
TVTITT'IIII'TTIIIrY'lItrITrrllrIrrlfiIIrIYrtv'vvifi
2.0 3.0 4.0 5.0

Loge live weight(g)

Figure 18. Relationship between mean live weight and mean clutch
size for the five study species.

107
pond-dwelling Asian ranids followed an interspecific pattern
of increased clutch size with increased body size. It is
interesting to note that the slope of the clutch size-LN
regression line (Figure 18) is very similar to the slope of
the ovarian weight-Lu regression line (Figure 17). In fact,
the slopes of each of these regressions do not differ
significantly from 1.0. This indicates that clutch size and
ovarian weight were quite similar measurements for
reproductively ready individuals of these five frogs.

Salthe and Duellman (1973) predicted that within a
given range of body size, species with relatively large ova
produce relatively few eggs at each reproduction. This also
occurs in salamanders (Kaplan and Salthe, 1979; Salthe,
1969). Figure 19 plots the 95% confidence interval of
number of ovarian ova and ovum diameter for each species.
The relationship suggested by Salthe and Duellman (1973) did
not seem to hold true for the five study species. Perhaps
the body size range is too great and the range of ovum
diameters is too small for the relationship to become
evident.

Duellman and Crump (1974) presented an index called the
'ovarian size factor“ which is an index of egg mass relative
to body size. The ovarian size factor in its original form
was t(CS)(OD)1/SUL in which CS - mean clutch size, OD I mean
ovum diameter and SUL = mean snout vent length of gravid
females. Since live weight is a more realistic measure of

actual frog size than SUL, live weight was used to construct

Loglo 95% confidence interval clutch size

108

 

 

L 1

Hana cancrivora

b

w

Rana chalconota

l ‘ [ 1
Hana limnocharis 7

Hana erythraea

 

 

 

PiJniitltlTLIIliitJifit'iiii

Us)

[:3

Ooeidozyga Zima

N
U1
LIIILJLIJIIILILILIL

5?.

 

 

 

111‘r111 11'1’111’1111'Ifr1 1111*111 '111’1111 1111 111 1111’111 1111*

1.10 1.20 1.30 1.40 1.50

95% confidence interval ovum diameter (mm)

Figure 19. Relationship between ovum size and clutch size for the five
study species.

109
a similar index, called, for convenience, the ovarian weight
factor. Table 32 gives the computed ovarian weight factor
for each species as well as Crump and Duellman’s (1974)
ovarian size factor. Using LN instead of SUL in this index

causes a switch in the relative positions of Q; limg and

3‘,g:zghr§ea.
11 r 'v rl

Seasonality in male reproductive characteristics was
examined by using mean monthly testis volumes for mature
males. Since testis volume was correlated with SUL (page
67), it was necessary to analyze the mean monthly SUL for
mature males. Data for mean monthly SUL and testis volume
of the five species are presented in Tables 33-42 and
illustrated in Figures 20-24. In general, the data were not
normally distributed and a Kruskal-uallis test was used to
check for significant monthly differences (Table 43).
Mature male 9; 11m; showed no significant differences in

testis volume or SUL during the 12 months of this study

(Figure 20). B; limggghgris (Figure 21), B;

sanscigm (Figure 22>. B... macs». (Figure 23> and
3;,gnglggngtg (Figure 24) each demonstrated significant

monthly differences in testis volume; however, all, except
fi‘_limnggngnig, also showed significant monthly
differences in mean SUL. Examination of Figures 22-24
suggests that the monthly peaks and troughs of SUL and

testis volume coincided for each of these three species.

110

Table 32. Ovarian veigbt factors (ill?) and ovarian size factors (03’) for the five species.

 

 

Species llean Egg Din. liean Clntcb llean all. llean Lil If 05F
Stage 5 Size 0ravid Fee. 0ravid Fee.

31;; ggcrivgfl 1.29 13611 100.2 102.4 171 175

Lag! mm 1.44 . 2207 64.2 10.9 160 50

393 linnglmig 1.24 1750 53.0 13.9 156 41

992.199.2200 Lia 1.04 434 31.7 3.7 122 14

32; £210.02; 1.50 1304 67.0 20.0 94 29

 

'0ia.‘ indicates egg diaeter in II.

'Sil' indicates snout-vent length in n of gravid fesales ('Fes.').

'111' indicates live weight in grass of gravid fesales ('Fen.').
'N'-linen civtcb size)(nean egg dimstage 5)) / (eean 31L gravid Fem).
'M'riinean clvtcb size)(nean egg dia.stage 5)] / (nean Lii gravid Fem).

111

Table 33. Mean monthly testis volumes (in cu mm) for mature

 

 

male Ogeiggzzggllflmg.

Mo. N- Mean 9528.1. Range CUZ Normal
OCT 10 5.1 3.1-7.1 1.8-11.4 54 NO
NOV 16 5.3 3.8-6.7 3.1-13.5 53 NO
DEC 5 6.9 2.9-10.8 2.8-11.3 46 YES
JAN 8 4.0 2.5-5.5 1.8-6.3 44 NO
FEB 6 3.6 3.3-3.9 3.2-4.0 8 NO
MAR 10 4.2 3.0-5.4 1.7-7.5 39 NO
APR 8 3.7 2.7-4.6 1.8-5.0 31 NO
MAY 6 3.8 2.6-5.0 1.9-5.0 30 NO
JUN 10 3.5 2.4-4.6 1.4-4.4 45 NO
JUL 6 4.1 2.2-6.1 2.0-6.3 45 NO
AUG 12 3.8 2.5-5.0 1.4-8.6 53 NO
SEP 12 4.2 3.2-5.3 3.2-8.0 39 NO

 

'No.‘ indicates nonth.

'C.l.' indicates confidence interval.

'CUZ' is coefficient of variation.

'Nornai' is nornality as deternined by iiolgunorov-kirnov test.

112

Table 34. Mean monthly snout-vent lengths (in mm) for mature male

Mme ___iima-

 

 

Mo. N= Mean 95%C.I. Range CUZ Normal
OCT 10 25.8 24.2-27.3 22.5-29.0 9 NO
NOV 16 25.6 24.7-26.4 22.3-28.5 6 NO
DEC 5 24.9 22.6-27.2 23.0-28.0 8 NO
JAN 8 24.0 21.6-26.6 20.8-29.5 12 YES
FEB 6 24.9 24.1-25.8 24.0-26.0 3 NO
MAR 10 24.3 23.7-25.3 22.5-26.2 6 NO
APR 8 24.5 23.0-26.0 22.0-28.0 7 N0
MAY 6 26.7 23.6-29.8 22.5-30.0 11 NO
JUN 10 25.3 23.8-26.9 22.0-29.0 8 NO
JUL 6 24.6 21.0-28.2 20.5-29.5 14 NO
AUG 12 25.2 24.0-26.4 21.5-29.0 8 NO
SEP 12 24.8 23.9-25.8 23.0-28.0 6 NO

 

'Ho.’ indicates nonth.

'C.i.' indicates confidence interval.

'DUZ' is coefficient of variation.

'Noreal' is nornality as deternined by Kolguorov-hirnov test.

113

Table 35. Mean monthly testis volumes (in cu mm) for mature

male 33n;,limngghgri .

 

 

Mo. N= Mean 95%C.I. Range CUZ Normal
OCT 10 18.6 12.6-24.6 10.4-32.9 45 NO
N00 11 13.5 11.2-15.9 8.0-18.1 26 NO
DEC 3 13.0 4.4-21.6 9.0-15.0 27 NO
JAN 15 17.9 14.3-21.5 10.7-29.5 36 YES
FEB 11 15.4 13.6-17.1 11.6-20.1 17 NO
MAR 11 16.0 12.0-20.1 9.8-27.7 38 NO
APR 10 12.7 10.4-15.1 8.4-19.3 26 NO
MAY 12 14.5 11.5-17.5 9.9-26.7 32 NO
JUN 9 11.9 9.3-14.5 5.8-16.0 28 NO
JUL 9 21.0 15.0-27.0 12.0-29.5 37 NO'
AUG 9 16.7 12.7-20.7 11.3-28.4 31 NO
SEP 8 13.4 8.2-18.5 6.4-25.6 46 NO

 

'No.‘ indicates nonth.
'C.l.' indicates confidence interval.

'OUZ' is coefficient of variation.

'tfornal' is nornality as deternined by Kolgtmorov-fiirnov test.

Table 36.
Ran; limnocharis.

114

Mean monthly snout-vent lengths (in mm) for mature male

 

 

Mo. NB Mean 9520.1. Range CV2 Normal
OCT 10 47.5 46.0-49.0 44.0-50.5 4 ‘NO
N00 11 44.6 42.2-47.0 40.0-51.5 8 N0
DEC 3 45.2 36.0-54.0 41.0-48.0 8 YES
JAN 15 45.7 44.2-47.2 41.5-49.3 6 N0
FEB 11 47.0 45.8-48.3 44.2-49.7 4 NO
MAR 11 44.4 41.2-47.6 35.5-51.0 11 N0
APR 10 45.6 44.3-46.8 43.0-48.0 4 N0
MAY 12 46.2 44.2-48.2 42.0-49.5 7 NO
JUN 9 43.4 40.7-46.1 37.5-49.0 8 N0
JUL 9 45.2 42.6-47.8 40.0-51.0 7 N0
AUG 9 46.1 44.3-48.0 43.0-49.5 5 NO'
SEP 8 45.9 43.3-48.5 43.0-51.7 7 N0

 

'No.’ indicates nonth.

'C.I.' indicates confidence interval.

'OUZ' is coefficient of variation.

'Nornal' is nornality as deternined by Kolgnnorov-Sirnov test.

Table 37.
male Rgng grzthraga.

115

Mean monthly testis volumes (in cu mm) for mature

 

 

Mo. NB Mean 952C.I. Range C02 Normal
OCT 8 7.9 5.3-10.5 4.1-12.8 40 NO
N00 16 8.3 6.9-9.7 4.5-13.5 31 NO
DEC 10 7.5 4.5-10.5 2.0-16.9 56 NO
JAN 9 6.8 5.7-7.8 4.5-8.8 20 NO
FEB 12 6.8 5.5-8.0 4.2-10.7 29 NO
MAR 12 6.0 3.6-8.3 2.3-15.8 62 NO
APR 9 7.4 6.7-8.1 6.2-8.9 12 NO
MAY 10 9.2 6.7-11.8 6.2-16.3 39 NO
JUN 10 4.1 2.9-5.3 2.0-7.9 40 NO
JUL 8 6.1 3.7-8.6 2.8-10.4 48 NO
AUG 13 5.5 4.4-6.6 3.4-8.5 32 NO
SEP 9 6.0 3.9-8.0 2.6-10.5 45 NO

 

'Nb.‘ indicates nonth.

'C.1.' indicates confidence interval.

'Ufl'iscuflfkhmtofvufiafidm

‘Nornal' is nornality as deternined by Kolgworov-tirnov test.

116

Table 38. Mean monthly snout-vent lengths (in mm) for mature male

Rana erzthrgg .

 

 

Mo. N= Mean 952C.I. Range CU2 Normal
OCT 8 40.5 37.8-43.2 36.5-45.0 8 NO
N00 16 41.2 40.4-41.9 39.0-43.5 3 NO
DEC 10 41.0 38.8-43.1 36.0-46.0 7 NO
JAN 9 ‘ 41.7 39.9-43.5 39.0-46.0 6 NO
FEB 12 43.6 41.4-45.7 37.7-49.2 8 NO
MAR 12 41.0 39.0-43.1 38.0-48.5 8 NO
APR 9 44.3 41.1-47.6 40.0-50.0 10 NO
MAY 10 40.3 38.7-41.9 36.0-44.0 6 NO
JUN 10 37.1 34.5-39.7 29.0-41.0 10 NO
JUL 8 39.1 36.8-41.3 35.0-42.5 7 NO~
AUG 13 38.7 36.9-40.4 35.0-45.5 8 NO
SEP 9 39.4 36.6-42.2 32.5-46.0 9 NO

 

'Nb.‘ indicates nonth.
'C.l.' indicates confidence interval.
'002' is coefficient of variation.

'Norsal' is nornality as deternined by Kolguorov-hirnov test.

117

Table 39. Mean monthly testis volumes (in cu mm) for mature

male Rgng ggngrivgrg.

 

 

Mo. N- Mean 9520.1. Range CU2 Normal
OCT 55 74.5 63.2-85.8 27.1-203.1 56 NO
NOV 17 98.1 77.5-118.7 37.3-158.9 41 NO
DEC 22 50.4 41.3-59.5 15.9-79.2 41 NO
JAN 17 72.7 55.0-90.5 31.1-152.9 47 NO
FEB 17 77.0 59.3-94.7 27.0-120.6 45 NO
MAR 6 71.7 37.6-106.0 43.2-132.2 45 NO
APR 10 69.5 47.2-91.8 32.0-119.5 45 NO
MAY 24 63.9 53.6-74.1 28.7-131.2 38 NO
JUN 13 75.8 65.5-86.2 46.9-102.0 23 NO
JUL 40 71.0 60.9-81.1 29.4-199.1 44 NO
AUG 18 81.4 64.0-98.8 41.9-151.5 43 NO
SEP 12 80.7 61.0-100.4 36.1-143.8 38 NO

 

'No.‘ indicates nonth.

'C.1.' indicates confidence interval.

'002' is coefficient of variation.

'lfornal' is nornality as deternined by Kolguorov-Gnirnov test.

118

Table 40. Mean monthly snout-vent lengths (in mm) for mature male
Rgng gangrivorg.

 

 

Mo. N: Mean 952C.I. Range CU2 Normal
OCT 55 75.1 73.0-77.1 63.0-92.5 10 NO
NOV 17 78.6 76.2-81.0 66.7-85.5 6 NO
DEC 22 75.3 72.8-77.7 66.0-85.5 7 NO
JAN 17 77.2 74.0-80.5 66.5-85.0 8 NO
FEB 17 76.8 74.2-79.5 66.0-83.5 7 NO
MAR 6 79.4 75.2-83.7 74.0-86.5 5 NO
APR 10 80.3 78.4-82.1 76.0-83.5 3 NO
MAY 24 79.7 77.1-82.3 71.0-88.0 8 NO
JUN 13 78.0 75.0-81.1 69.5-86.5 6 NO
JUL 40 76.9 74.8-78.9 64.9-94.0 8 NO
AUG 18 79.5 77.1-81.9 73.0-90.0 6 NO
SEP 12 79.2 75.0-83.4 70.0-89.5 8 NO

 

'llo.‘ indicates nonth.

'C.1.' indicates confidence interval.

'002' is coefficient of variation.

'Nornal' is nornality as deternined by Kolgtmorov-Sirnov test.

Table 41. Mean monthly testis volumes (in cu mm) for mature

male Rgna chalcoggtg.

 

 

Mo. 1*! Mean 952C.I. Range C02 Normal
OCT 11 14.3 12.4-16.2 10.2-19.5 20 NO
NOV 18 12.1 10.5-13.7 7.2-18.7 26 NO
JAN 12 13.6 9.4-17.7 6.2-24.8 48 NO
FEB 13 7.1 5.9-8.4 4.2-11.1 29 NO
MAR 19 9.9 8.5-11.1 5.7-14.8 28 NO
MAY 20 17.4 15.2-19.6 12.6-26.3 27 NO
JUL 11 11.2 8.8-13.3 6.2-17.3 30 NO
AUG 10 20.8 15.8-25.6 11.9-35.0 33 NO

 

'No.‘ indicates nonth.
'C.1.' indicates confidence interval.

'002' is coefficient of variation.

'Nornal' is nornality as deternined by Kolganorov-Snirnov test.

120

Table 42. Mean monthly snout-vent lengths (in mm) for mature male
Rana chalconota.

 

 

'Mo. N= Mean 952C.I. Range CU2 Normal
OCT 11 48.4 46.6-50.3 44.0-52.5 6 NO
NOV 18 43.7 42.2-45.3 35.2-48.7 7 NO
JAN 12 43.5 41.3-45.7 37.0-46.6 8 NO
FEB 13 41.2 39.1-43.4 35.0-49.0 9 NO
MAR 19 44.3 42.3-46.3 39.0-53.5 9 NO
MAY 20 46.8 45.2-48.5 41.0-54.5 8 NO
JUL 11 45.2 43.3-47.2 41.0-50.5 6 NO
AUG 10 48.6 46.8-50.4 43.5-52.5 5 NO

 

'Ho.‘ indicates nonth.

'C.i.' indicates confidence interval.

'002' is coefficient of variation.

'Nornal' is nornality as deternined by Kolguorov-Snirnov test.

121

 

 

 

 

 

 

 

28:3
’3 C265.
5 15. I 4
3 _24,,
3 .2253,
m IOJ P,
g. g
F. in
° 9-
: 5- ii ‘51 i. A
2: 3 {ii 1‘3 it a
U) v
0)
E" 1 1 l 1 1 1 1 l l l r F
Oct Nov Dec Jan Feb Mar Apr May Jun Jul A23 §g2|

 

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and 95% confidence intervals (vertical rectangles) for testis

volume and monthly mean snout-vent length (upper line) for
Ooeidozyga Zima.

 

30 J [4
7
_.__ 1-
323\//\/\/fl/ :45
25 4 i; :43

20 q i F1

 

 

(mm) qnfluat nuaA-unous

 

 

 

 

 

 

 

 

 

 

 

 

10'

 

 

 

 

 

Testis volume (cu mm)
p—n
U1
r-4——1
L—f—l
l
1*
r—t—t
L—Qf—J
i
E;,
r —1
.J
}

 

 

 

5‘ L.

 

I I I l l l 1 l I l T F
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep].

 

 

Figure 21. Monthly means (horizontal bars), ranges (vertical lines),
and 95% confidence intervals (vertical rectangles) for testis

volume and monthly mean snout-vent length (upper line) for

Rana limnocharis.

122

 

 

 

 

 

 

 

 

 

 

 

 

 

 

:82 ‘é’
:30 5.
K76 g
1 ’74 H
'3
3°
8
A 150‘
E A
s E
U V
V 4
0) M
*3
.—i F0
g 100‘l Tr-
0‘) ma
°r-i
U uni-I
. * ~~+— 1} i} H
H
504 {} L
L H

 

 

 

 

 

 

U I V I I T I I I T U '

Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Se

 

 

 

Figure 22. Monthly means (horizontal bars), ranges (vertical lines),
and 95% confidence intervals (vertical rectangles) for testis
volume and monthly mean snout-vent length (upper line) for

- Rana cancrivora.

123

 

 

 

 

 

 

 

I 8
r 8
“:45 n
,.204 . A
E t a
a ”:40
315- . '5'
. 5
<1) .. 3;
,5 P35 3'
010'1 A
> .E&' {h- .4} {3. g
0‘) v
wt
0
$4
5 l I r v n v T I —T I 0
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

 

 

 

Figure 23. Monthly means (horizontal bars), ranges (vertical lines),
and 95% confidence intervals (vertical rectangles) for testis

volume and monthly mean snout-vent length (upper line) for

Rana erythraea.

 

 

 

 

 

 

 

 

 

 

 

 

 

' 3
35 :47 3
it '45 T
25- " ~43 3
- :41 3
e ..
e _ l-‘
3 20. “HP 39 g
U 39
v F" g.
3 11 Li A
o 15- a
'3 ]. ‘€}. ~4+ El
>
.5 104 Li 1H- }
U
U)
01
Ft
5!

 

‘— T I T T

l r' ’1 *1 1’ I r
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

 

 

 

Figure 24. Monthly means (horizontal bars), ranges (vertical lines),
and 95% confidence intervals (vertical rectangles) for testis

volume and monthly mean snout-vent length (upper line) for

Rana chalconota.

124

Table 43. Kruskal-Uallis test results for differ-
ences in mean monthly testis volumes and mean
Inonthly snout-vent lengths in nature males.

 

Species Kruskal-Uallis 'H'

testis volume

Kruskal-Uallis 'H'
snout-vent length

 

Whigs 9
mum 19
MW 38
Egg; gczghraeg 27
33g; gingrivgrg 22

NS
s

as
as

{NI

18
24

18

NS

NS

*5
ifi

*I’

 

'NS' indicates not significant, P>-0.05.
'i' indicates significant at P(0.05.
'**' indicates significant at P(0.01.

125

Between species, the peaks and troughs showed little
coincidence. It was concluded that no seasonality in testis
volume occurred for the five study species.

Table 44 gives numbers and percents of mature males
collected each month. The majority of males collected in
this study were mature. In 3; ggztnnggg and 3;
gnglggngtg, nearly 100% were mature. In a;
limnggngglg and nglimg, approximately 90% of those
collected were mature. In 3; ggggglgggg, 74% of the
males collected were mature. Some monthly variation of
percent mature males occurred in B; gaggcivgra, B;
limgoghgcig and Q; ling but these fluctuations did not
coincide. Apparently, no large influx of immatures occurred
during any month that would have influenced the percent
mature frogs and indicated seasonality in breeding. It is
possible that the high percentage of mature males found was
not a true reflection of the respective population
percentages. This would be true if the immature frogs had
different habits or habitat that rendered them less
susceptible to collection.

Church (I960b) found an increase in mean testis volume
from March to July in west Javan 3; gangcivorg, however,
he did not document the body size of the males and this may
have been a factor in the observed trend. working with 3‘
grithrggg in Borneo, Inger and Greenberg (I963) found
that all males collected were sexually mature and every

testis examined from each month showed all stages of

126

labie 44. Monthly percentages of nature sales.

 

 

Species mummmrsammmvmmmsvmu
31113111111111

11.111113517221717 1112413411112231

11111111212723229213321472212327

z 911312747712491941131211177
121mm

leatvre i. 12 3 15 ii ii 10 12 9 9 9 8 119

111111 11 14 1 11 11 12 11 14 11 11 11 9 131

211111319411192111111291911911
82111213313

1mm 1 11 11 9 12 12 9 11 11 1 13 9 121

111111 11 12 11 9 12 12 11 11 11 11 13 9 132

z 11 94 111 111 111 111 91 111 111 11 111 111 95
3.111111111111211

1mm 11 11 12 13 19 21 11 11 114

Total 1 11 11 12 13 19 21 11 11 114

z 111 111 111 111 111 111 111 111 111
99019222931121

11111111111 5 1 111 1 11171212111

111111 1119 1 9 111 1 711 11212117

1 111 14 13 19 111 111 111 11 111 11 111 111 94

 

127

spermatogenesis, indicating these frogs had the ability to
breed year-round. Alexander g3_;l& (1979) found that

male 3; limnocharis in Taiwan did not differ

significantly in mean testis weight each month nor did
secondary sexual characters regress totally in the
off-breeding season. They concluded that, on the population
level, males were reproductive year-round, even in Taiwan’s
seasonal climate.

Seasonality in the female reproductive cycle was
examined by analysis of mean monthly clutch sizes. Since
clutch size and body size were correlated (page 103), it was
necessary to analyze the mean monthly SUL of females. The
data for the five species are presented in Tables 45-54 and
data for clutch size are plotted in Figures 25-29. The
Kruskal-Wallis test was used to check for significant
differences among the monthly means (Table 55).

Only 3; ghglconotg showed significant differences
in monthly SVL means, so significant differences in clutch

size can be considered as independent of female size in 9;

1.1.1111. B... sanctum. B... __z_t____er bran and 8.4.
n ri . As previously stated, 3; ghglggggt;

showed no significant correlation between body size and
clutch size, so significant differences in mean clutch size
can be considered independent of body size in this species
also.

94 Ling, g; chalconota, 3; erythraea and B; limnocharis

showed no significant differences in mean monthly clutch

128

 

 

Table 45. Mean monthly clutch sizes for W Ml-

Mo. NI Mean 9520.1. Range CV2 Normal
OCT 6 408 274-542 165-540 31 N0
NOU 9 420 302-538 250-666 37 NO
DEC 4 450 88-812 150-700 50 N0
JAN 3 355 --- 195-496 43 YES
FEB 4 615 240-990 360-900 38 YES
MAR 6 454 293-615 195-566 34 YES
APR 2 333 218-447 ' 324-342 4 YES
MAY 4 421 99-744 268-716 48 N0
JUN 6 464 327-600 317-668 28 YES
JUL 6 489 360-618 345-715 25 N0
AUG 5 423 218-629 265-700 39 YES
SEP 5 348 157-539 185-585 44 N0

 

'No.‘ indicates nonth.

'C.I.' indicates confidence interval.
'M' is coefficient of variation.

'Noreai' is nornality as deternined by Kolguorov-hirnov test.

129’

Table 46. Mean monthly snout-vent lengths (in mm) for female
gogidgzzga lima with countable ova.

 

 

Mo. N= Mean 9520.1. Range CV2 Normal
OCT 6 29.2 24.7-33.6 25.0-33.0 14 N0
nov 9 32.4 30.4-34.5 30.0-36.5 3 N0
DEC 4 32.0 24.2-39.1 25.5-36.5 15 N0
JAN 3 30.0 23.6-36.3 27.2-32.2 3 YES
FEB 4 31.6 ‘ 29.6-33.6 30.0-33.0 4 N0
MAR 6 32.6 29.0-36.2 26.5-36.0 11 N0
APR 2 30.2 --- 23.5-32.0 8 ---
MAY 4 34.4 31.8-36.9 32.0-35.5 5 YES
JUN 6 32.5 30.6-34.5 31.1-36.0 6 N0
JUL 6 34.6 33.0-36.2 33.0-37.0 4 N0
AUG 5 32.3 29.7-35.9 29.0-35.5 7 YES
SEP 5 31.4 27.5-35.3 26.5-34.0 10 N0

 

'Nb.‘ indicates nonth.

'C.I.' indicates confidence interval.

'UUZ' is coefficient of variation.

'Noraal' is nornality as deternined by Kolguorov-Sairnov test.

130

 

 

Table 47. Mean monthly clutch sizes for figgg_ligng§ngglg.

Mo. NB Mean 9520.1. Range CV2 . Normal
OCT 9 1481 1221-1742 1125-2083 23 YES
N00 4 996 427-1565 733-1500 36 N0
DEC 4 2661 931-4391 1583-4167 41 YES
JAN 5 1428 463-2394 667-2667 54 YES
FEB 6 1511 646-2377 667-2583 55 N0
MAR 4 2375 446-4304 1833-4167 51 YES
APR 3 1722 1090-2355 1500-2000 15 YES
MAY 4 1344 871-1817 1083-1750 22 N0
JUN 4 1354 556-2152 917-2000 37 YES
JUL 6 1625 675-2575 625-3000 56 N0
AUG 5 979 706-1252 750-1250 22 YES
SEP 6 1569 1093-2046 917-2125 29 N0

 

'Ho.‘ indicates nonth.

'0.I.' indicates confidence interval.

'OUZ' is coefficient of variation.

‘Nornal' is nornality as deternined by itolgaaorov-Sairnov test.

131

Table 48. Mean monthly snout-vent lengths (in mm) for female
Ring limnogharis with countable ova.

 

 

Mo. N- Mean 9520.]. Range CUM Normal
OCT 9 52.5 49.7-55.3 47.5-58.0 7 N0
N00 4 48.0 37.4-58.6 41.0-57.0 14 N0
'DEC 4 53.8 43.5-64.0 48.0-62.5 12 YES
JAN 5 52.9 48.7-57.2 50.2-58.3 6 YES
FEB 6 53.3 48.9-57.7 48.0-59.0 8 N0
MAR 4 54.6 46.6-62.6 52.0-62.0 9 YES
APR 3 56.0 41.0-70.9 50.0-62.0 11 N0
MAY 4 50.5 48.4-52.6 49.0-52.0 3 YES
JUN 4 54.5 47.5-61.4 54.0-60.5 8 N0
JUL 6 52.0 48.7-55.3 48.0-57.0 6 N0
AUG 5 50.0 43.3-56.7 42.0-57.0 11 N0
SEP 6 51.2 48.3-54.0 49.0-55.0 5 N0

 

'No.‘ indicates nonth.

-c.1.' indicates confidence interval.

'GUZ' is coefficient of variation.

'Nornal' is nornality as deternined by Kolguorov-Sairnov test.

132

 

 

 

Table 49. Mean monthly clutch sizes for Rana erythraea.

Mo. N= Mean 95%C.I. Range CUZ Normal
OCT 7 1345 1204-1487 1167-1571 11 NO
NOU 7 1044 727-1361 719-1469 33 YES
DEC 4 1390 1291-1490 1312-1458 4 NO
JAN 4 1214 763-1665 938-1607 23 YES
FEB 4 1117 532-1701 900-1667 33 NO
MAR 7 1160 819-1502 821-1929 32 NO
APR 8 1715 1365-2137 1100-2400 26 NO
MAY 4 1214 903-1525 1063-1500 16 NO
JUN 3 1361 1045-1677 1250-1500 9 YES
JUL 6 1137 838-1437 708-1500 25 NO
AUG 5 1400 1201-1599 1167-1583 11 YES
SEP 7 1583 1320-1847 1250-2000 18 NO

 

'No.’ indicates nonth.
'0.I.' indicates confidence interval.

'CUZ' is coefficient of variation.

'Nornal' is nornality as deternined by Kolguorov-Birnov test.

133

Table 50. Mean monthly snout-vent lengths (in mm) for female
Rang erythraea with countable ova.

 

 

Mo . NB Mean 957.0 . I . Range W7. Normal
OCT 7 61.1 56.2-66.1 53.0-68.0 9 NO
N00 7 66.0 62.5-69.4 62.0-71.5 6 NO
DEC 4 67.9 62.6-73.2 64.5-72.0 5 YES
JAN 4 64.5 59.2-69.7 60.0-67.5 5 YES
FEB 4 65.8 54.6-76.9 62.0-74.5 11 NO
MAR 7 69.9 65.3-74.4 62.0-78.0 7 NO
APR 8 66.7 65.0-68.4 64.0-70.0 3 NO
MAY 4 69.9 59.3-80.5 63.5-71.5 10 YES
JUN 3 70.3 66.5-74.2 69.0-72.0 2 NO
JUL 6 63.2 55.4-70.9 57.0-73.0 12 NO
AUG 5 67.6 65.6-69.5 65.5-69.0 2 NO
SEP 7 67.4 63.9-70.8 64.0-70.5 6 NO

 

'No.’ indicates nonth.

'C.I.' indicates confidence interval.

'DUZ' is coefficient of variation.

'Nornal' is nornality as deternined by Kolguorov-Sairnov test.

134

Table 51. Mean monthly clutch sizes for Rang ghglggngta.

 

 

Mo. N= Mean 95%C.I. Range 00% Normal
OCT 10 2749 2289-3210 1857-3917 23 N0
NOV 8 2075 1473-2677 1417-3550 35 N0
JAN 6 2270 1810-2728 1500-2800 19 NO
FEB 9 2159 1762-2556 1550-3000 24 NO
MAR 7 2508 2208-2809 2000-2917 13 NO
MAY 5 2123 1570-2675 1813-2813 21 NO
JUL 6 2602 2147-3059 2000-3167 17 NO
AUG 5 2898 1811-3984 1833-3857 ‘ 30 NO

 

'No.‘ indicates nonth.
'0.l.' indicates confidence interval.

'OUZ' is coefficient of variation.

'Nornal' is nornality as deternined by Kolgaorov-Sairnov test.

135

Table 52. Mean monthly snout-vent lengths (in mm) for female

Rgna ghglgonot; with countable ova.

 

 

Mo. NB Mean 9520.1. Range 0U2 Normal
OCT 10 66.7 64.2-69.2 62.0-72.5 5 NO
N00 8 70.7 67.5-73.9 64.0-75.5 5 NO
JAN 6 61.3 55.3-67.2 52.7-67.5 9 NO
FEB 9 61.5 55.3-67.6 53.6-77.7 13 N0
MAR 7 62.6 56.3-68.8 52.0-71.0 11 NO
MAY 5 69.5 62.5-76.5 64.5-78.0 8 NO
JUL 6 68.5 64.4-72.6 63.0-75.0 6 NO
AUG 5 68.1 61.9-74.3 61.5-74.5 7 YES

 

’No.‘ indicates nonth.
'0.1.' indicates confidence interval.
'002' is coefficient of variation.

'Nbrnal' is nornality as deternined by Kolgonorov-Snirnov test.

136

 

 

Table 53. Mean monthly clutch sizes for gang gancrivora.

Mo. N= Mean 9520.1. Range 0U2 Normal
OCT 23 10942 7938-13946 4667-33833 64 NO
NOV 2 13000 --- 6500-19500 71 ---
DEC 13 13724 8902-18546 5333-35583 58 NO
JAN 5 18422 6030-30814 5000-28571 54 N0
FEB 8 16093 11400-20788 10500-25000 35 NO
MAR 5 16202 9950-22454 8500-22333 31 YES
APR 3 15041 9213-20871 12500-17125 16 NO
MAY 2 9625 --- 6000-13250 53 ---
JUN 3 7528 2558-12498 5250-9000 27 YES
JUL 6 17660 9459-25861 9000-32000 44 NO
AUG 11 9993 8374-11611 5167-13500 24 NO
SEP 9 13107 8520-17695 6500-23667 45 NO

 

'No.‘ indicates nonth.
'0.l.' indicates confidence interval.
'002' is coefficient of variation.

'Nornal' is nornality as deternined by Kolgneorov-fiirnov test.

137

Table 54. Mean monthly snout-vent lengths (in mm) for female
33;; gangrivgra with countable ova.

 

 

Mo . N- Me an 9520 . I . Range 0U2 Normal
OCT 23 94.6 88.9-100.4 74.5-119.0 14 N0
NOV 2 102.0 --- 97.7-106.4 6 ---
DEC 13 103.5 95.3-111.7 80.0-119.0 13 NO
JAN 5 98.0 76.3-119.7 68.0-110.0 18 YES
FEB 8 104.5 95.2-113.9 86.0-118.0 11 N0
MAR 5 104.8 95.6-114.0 96.5-112.0 7 YES
APR 3 111.2 99.1-123.0 107.0-116.5 4 NO
MAY 2 98.5 --- 94.0-103.0 6 ---
JUN 3 109.2 93.2-125.2 102.0-114.5 6 NO
JUL 6 105.4 92.7-118.1 90.5-119.0 11 NO
AUG 11 103.2 96.9-109.5 84.0-114.0 9 NO
SEP 9 96.7 89.1-104.3 80.5-112.0 10 NO

 

'No.‘ indicates nonth.

'0.1.' indicates confidence interval.

'002' is coefficient of variation.

'Nornal' is nornality as deternined by Kolguorov-birnov test.

Clutch size

Clutch size

138

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

1000-
F1
800 1 F
F
600- -»L Ff
M
400- ““- - #- Jem-
cit-1T.
200- ‘ -
.1 L ‘
U V I V f I 1 I r T I r
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

 

 

Figure 25. Monthly means (horizontal bars), ranges (vertical
lines) and 95% confidence intervals (vertical rectangles) for
clutch size for Ooeidozyga Zima.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

5000-
40004
30001
fl” F” .1... ..
2000-
$ q-I‘F --__ dihh
1000- J _H1
.. 1
I r r I T I I I l I I I
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

 

 

Figure 26. Monthly means (horizontal bars), ranges (vertical
lines) and 95% confidence intervals (vertical rectangles) for
clutch size for Rana limnocharis.

Clutch size

Clutch size

3500

3000

2500

2000

1500

Figure
lines)
clutch

2500

2000

1500

1000

500

Figure
lines)
clutch

139

 

3

L

A‘A‘

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

l
r
f

 

T I V T U 7 T

Jan

r r

Feb Mar Apr May Jun Jul Aug Sep

1 1

Oct

I
Nov Dec

 

 

27. Monthly means (horizontal bars), ranges (vertical
and 95% confidence intervals (vertical rectangles) for
size for Rana chalconota.

 

 

l

1

 

as;

 

 

 

 

 

 

 

 

 

1 I I I U I' r j F r I 1—
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
28. Monthly means (horizontal bars), ranges (vertical
and 95% confidence intervals (vertical rectangles) for

size for Rana erythraea.

Clutch size

140

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

40000
35000- '
300004 1
25000- 7
+0
20000- “i 3
[-1- Inm-
qp-n-I- 1'1"
4""- all-L41-
15000- - F
-—o— 11“- L ""'"’
1 1 1 ~ 1 1. £1 1
5000‘ '
fl I I I I I I I I I I I
Oct Nov Dec Jan Feb far Apr May Jun Jul Aug Sep

 

 

Figure 29. Monthly means (horizontal bars), ranges (vertical
lines) and 95% confidence intervals (vertical rectangles) for
clutch size for Rana cancrivora.

141

Table 55. Kruskal-Uallis test results for differences \
in mean monthly clutch sizes and mean monthly snout-vent
lengths of females with countable ova.

 

 

Species Kruskal-Nallis 'H' Kruskal-Nallis 'H'
clutch size snout-vent length

Ogeidgzzga 11!; 5 NS 5 NS

figg; limngghgris 12 NS 7 NS

Egg; ghglgongtg 6 NS 12 !

gggg erzthrggg 13 NS 9 NS

Bang gangrivgra 17 11 1 12 NS

 

'NS' indicates not significant, P>=0.05.
'4' indicates significant at P(0.05.

142

size and this is taken as evidence of non-seasonality. B;
ggngrivggg did show significant differences in mean
monthly clutch size. A decrease in mean clutch size
occurred from April to June. Unfortunately, these three
months were represented by small sample sizes and it is
possible, since 3; ggngciggrg may partially ovulate
(Church, 1960b and the present study), that, by chance, the
females obtained during these months had already oviposited
part of their clutch.

In Church’s (1960b) study of west Javan 3L
ggngniggng, he cited high ovarian weight (an indicator
of clutch size) in September through November as indicative
of the peak breeding season for this species. However, both
ovarian weight and clutch size are positively correlated
with body size and Church did not account for this in his
analysis. In fact, during the months that Church found high
ovarian weight, he also had females with high body weights.
A further problem, and perhaps more critical, with Church’s
analysis was that he included all ovarian weights (mature
and immature females), so the number of frogs with stage 1-3
ovaries (and therefore small weight ovaries) in his sample
would have effected his results drastically. His data on
relative abundance of the five egg stage ovaries in each
month indicate that this probably was the case.

The percentage of mature females that were
reproductively ready (Table 56) was high for all species in

almost all months, although some fluctuations occurred. The

143

Table 56. Monthly valves of n-ber of natvre fenales (I nature), nder of reprohctively
ready fenales (I repro) and percent of reproductively ready fenaies (2 repro) for all species.

 

 

becies MWDECMFHNMMYMMMSEPTMM
Museum

Imatvre 28 3 13 5 11 5 3 5 5 9 11 9 188

I repro 22 2 13 4 4 5 3 2 2 6 11 9 fl

Zrepro 79 67 188 88 36 188 188 48 48 67 188 188 77
323W

Inatere II 4 5 5 6 5 3 4 5 6 5 65

I reprn 9 4 4 5 6 4 3 4 4 6 5 6 56

Xrepro 98 188 88 100 188 88 188 188 88 188 III 86 86
Merztbrgg

Inatvre 1| 7 6 6 6 7 8 7 4 8 8 7 84

I repro 7 7 4 4 4 7 8 4 2 6 5 7 65

2 repro 74 111 67 67 67 188 188 57 58 75 63 188 77
83315131131931

I natvre 18 18 6 18 9 6 18 15 76

I repro 18 8 6 9 7 5 6 5 56

1 repro 188 88 180 98 78 83 68 33 74
99311911131131

Inatvre 6 9 4 4 5 5 2 8 8 7 5 6 69

I repro 5 8 2 3 4 5 1 4 5 6 5 5 54

Irepro 83 89 50‘ 75 88 1“ 58 58 62 86 180 83 78

 

144

high percentages indicate that in most months the majority
of mature females was ready to breed. The overall annual
percentages of mature females that were reproductively ready
were also high (Table 56).

Several researchers (Alexander g; 51;, 1979;

Church, 1960b; Inger and Bacon, 1968; Inger and Greenberg,
1963) have presented information on the percent of
reproductively ready females out of the entire sample of
collected females, without regard to sexual maturity. Any
influx of immatures into the population would tend to
depress these percentages. In the current study, a more
accurate picture of the portion of the breeding-age frogs
(i.e., sexually mature) which are ready to breed is
presented. This information is more valuable in discussing
the reproductive potential of a population.

The percent of males and mature females with large fat
bodies was calculated for each month to check for
seasonality. All species showed fluctuation from month to
month, but peaks and troughs did not coincide between the

species.

DISCUSSION

r iv iol

The present study has taken a close look at a community
of frogs within a narrow range of reproductive diversity.
The five study species all have a 'generalized mode' of
reproduction (Crump, 1974; Salthe, 1969; Salthe and
Duellman, 1973). That is, their eggs are deposited in open
water and the larvae develop in this environment. This
reproductive mode places similar restrictions on the frogs,
but each species has a distinctive set of reproductive
characteristics to meet these restrictions.

Salthe and Duellman (1973) and Crump (1974) made
cergain generalizations regarding reproductive patterns of
frogs that are within a single reproductive mode. The frogs
in the present study did not always fit these patterns.

Salthe and Duellman (1973), Salthe (1969) and Kaplan
and Salthe (1979) presented evidence that suggested that an
interspecific increase in body size is accompanied by an
interspecific increase in ovum size for frogs and
salamanders. However, they pointed out that inclusion of
data from a variety of reproductive modes disrupts this
pattern. 3; gggggigggg is a standout from this pattern

in that it has a large body size, but small ovum diameter.

145

146

Salthe and Duellman (1973) noted that the genera figig and
33g; are in the same reproductive mode yet figig have
consistently smaller ovum diameters at all body sizes than
3‘33. Associated with this, is the fact that, at all
body sizes, the clutch sizes of 9912 are consistently larger
than 355;. figig have a reproductive strategy that
involves many more smaller ova than Eggs. Salthe and
Duellman (1973) even suggested the possibility of
subdividing the general mode of reproduction based on these
differences. 3; cgggrivgrg more closely follows the
reproductive strategy of ggig and 34 Limgggngnig, B;
grzthrgga, B; chalconota, and Q: Lia; fall within the Egg;
group (Figure 30). If body size is held constant, reducing
ovum diameter is one way of increasing fecundity. Natural
selection has presumably favored, in 3; ggggrivgrg, a
small ovum diameter (and smaller energy investment per ovum)
and an increased clutch size. It may be that B;
ggggnlgggg is approaching maximum clutch size (or
ovarian weight) allowed by body size constraints, as was
postulated for em2113gmg,tlgglggm,by Kaplan and Salthe
(1979).

fig gnztngggg has also departed somewhat from the
reproductive strategy of the generalized mode frogs. Crump
(1974) found that ovarian size factor increased with
increasing female size within a reproductive mode. In
general, this occurred with the five species in this study

(Table 32) with the exception of g; ggztngggg which was

147

 

Helioporus
EZeutherodactyZus
Ansonia
Pseudophryne -
Bufb
Ascaphus
Barbourula
Pond Hyla
AgaZychnis -
Rana

Platymantis

Rana cancrivora
Rana limnocharis
Rana erythraea
Ooeidozyga Zima

OOG$QIO<>§ODME§HHI

Rana chalconota

!
2 . "is- 4;: T: -

Ovum diameter (mm)

 

 

 

 

 

 

 

 

l a l n

I I l I
20 40 60 80 100 120 140 160

 

Female snout—vent length (mm)

Figure 30. The relationship between ovum size and body size in
some frogs (from Salthe and Duellman, 1973) including the five
study species. The data for various species of Bufg are plotted
as unshaded rectangles for individual species.

148

the second largest frog, but had the smallest ovarian weight
factor value, or in other words, the smallest egg mass
relative to body size.

The lack of reproductive seasonality that is evident
from both field observations and dissection of adults was
striking. One could go into the field on any night of the
year and expect to find all of the five species breeding.
Darlington (1957) considered the tropics as the center of
origin for the anurans and Inger and Greenberg (1963)
suggested that an acyclic reproductive pattern (possible
only in a uniformly equable climate) may represent the
characteristic pattern of most stocks from which modern frog
species have evolved. The latter authors stated further
that the cyclic behaviors of species in the temperate zones
and of seasonal tropics can be considered derived patterns.

3; limggghagig has been studied in the seasonal
environment of Taiwan (Alexander gt gl, 1963, 1979), as
well as in aseasonal tropics (Berry, 1964; and the present
study). This species demonstrates that breeding seasonality
can be variable within a species depending on the
environmental conditions of a specific locality. It is
interesting that, in Taiwan, the females display a distinct
seasonality in their reproductive biology, but the males are
apparently ready to breed at any time, even in that seasonal
climate. Following Inger and Greenberg (1963), if the
aseasonal pattern was the original pattern for B;

in ari , it may represent a reproductive phenomenon

149

which has had a differential rate of evolution in the two
sexes. Perhaps the selective pressures were stronger for
female 3; limggghgcig to become seasonally reproductive

than they were for males. Certainly the energy investment
is greater in females. An alternate explanation is that
cyclic reproductive behavior is environmentally produced and
not genetically set. The remaining four species have not
been studied in seasonal environments, but perhaps future
studies will reveal a similar intraspecific variation in

breeding seasonality.

R r ti e ' ti n

The obvious fact that distinct species existed in this
community indicated that mechanisms were operative which
maintained genetic isolation. Fouquette (1960) presented a
classification of anuran isolating mechanisms which has
three major categories: (1) anti-mating isolating
mechanisms, (2) courtship isolating mechanisms and (3)
post-mating isolating mechanisms. In the present study,
anti-mating isolating mechanisms and courtship isolating
mechanisms are examined for their relative contributions to
maintaining genetic isolation. Under the category of1
anti-mating isolating mechanisms are five criteria: (a)
geographic isolation (allopatry), (b) habitat isolation
(differences in breeding site), (c) seasonal isolation
(differences in breeding season), (d) temporal isolation

(different times of day when breeding occurs) and (e)

150

psychological or climatic isolation (differences in response
to climatic or physical environment). Under Fouquette’s
category of courtship isolating mechanisms are two main
criteria: ethological isolation (differences in courtship
behavior) and mechanical isolation (structural differences
which prevent interbreeding). Duellman (1967) outlined four
criteria under the category of ethological isolation: (I)
calling site of male, (2) mating call, (3) position of
amplexus (axillary or not) and (4) ovipostion site.

The ranges of the five study species overlap
extensively, so geographic isolation was not operative in
maintaining genetic isolation among these frogs.

Habitat isolation (coarse habitat partitioning) was
operative only between 3; ghglcgngtg and Q; lymg in
the cases studied. All other species were found together in
the same breeding habitat.

A frequently observed type of habitat partitioning by
breeding frogs is seasonal partitioning. This is especially
evident in temperate and seasonal tropical environments (for
examples see Blair, 1961; Heyer, 1973; and wiest, 1982).
However, a main feature of the West Javan community was its
lack of reproductive seasonality. All five species were
heard calling in all twelve months of the year. A
sufficient rainfall and suitable temperature in all months
allowed continuous breeding by the populations. On a

site-by-site basis, Mesjid Pond in BBC showed the only

seasonality, with g; ggngrlvorg and a; gnalggngtg

151

not present in all months. flgpgggggigggg called at the
site during times of relatively low water levels. Exposed
mudflats at these times provided desirable microhabitat for
the calling males. The reason for the absence of 3‘
gnglggngtg during some months is unknown. In general,
seasonal habitat partitioning was not operative in
maintaining specific isolation among the five species of
frogs.

The most evident temporal aspect of the community
members was the general avoidance of daytime hours for
calling and other breeding activities. The high daytime
temperatures are likely a primary factor involved. During
daytime rain storms, calling was sometimes stimulated, but
usually these storms took the form of hard downpours of
short duration. There was likely not enough time for
breeding activity other than calling during these periods.
Approximately 18 hours of the 24-hour cycle were used by the
frog community members for calling. Each species
demonstrated a preferred time for the peak calling activity
and no species used the entire 18-hour segment.

Psychological or climatic isolation was not detected in
the community. Calling activites of the study species were
observed on nearly every nocturnal visit to the ponds,
regardless of prevailing weather.

Fine spatial habitat partitioning in calling site

preference was evident among all community members with

152

little overlap in calling site preferences except between 3;
limgggngglg and 3; ggncrivorg.

Advertisement calls were not electronically analyzed,
but a few observations are worthy of mention. An acoustical
partitioning of the breeding environment was apparent. Both
3; grzthrggg and 3; chalcongtg had high-pitched
calls with a low intensity (loudness). The calls of neither
species carried very far, at least to the human ear.

Neither B; ggzthrgeg nor 3; chglggngtg had apparent

organization to the chorus. Individual males called
frequently. The calls of 3; ggggrivggg, 3;

l’ n c r’ and Q; 119; were quite loud and were heard

at great distances (ZOO-300 meters). Male g; 1.ng

called non-synchronously, but often the calls of a few males
stimulated calling by many males. Male 3; limggghgrig
called in bursts of synchronous calling lasting several
minutes, followed by periods of silence. Male 3‘
ggggrivgrg did not call synchronously, but the calls of

one male often stimulated other males to call and individual
male Bg‘gggggigggg seemed to take turns calling. Being
predominantly inhabitants of permanent water sites, 3;
ggzthrggg and B; chglconotg were probably more

concerned with advertising their relative position within
the pond to females and not in attracting females from great
distances to come to the breeding pond. 1n the case of Q;

11mg, 3‘ limngcnggig and 3; cangrigogg, which

tended to utilize transient, non-permanent breeding sites,

153

their loud and synchronous calls were perhaps important for
advertising a new site to individuals that were some
distance away.

Axillary amplexus was observed in all five study
species. Oviposition was so infrequently observed that
analysis of oviposition site differences was not possible.

Mechanical isolation by way of size differences is
likely operative in the community. The five pond-dwelling
ranids formed a continuum of sizes from a very small species
to a relatively large one. This size partitioning may have
resulted from selection for partitioning of food resources
according to size (Caldwell, 1973: Crump, 1974: Toft, 1980)
or through selection for the mechanical isolating mechanism
itself. whatever the origin, the size differences were
presently an effective cue available for species
recognition. Correct species recognition is more important
to the female since the energy loss for her, in the event of
a mismating, is higher than for the male. Mature males of
all five species were significantly different in either SUL,
Lu or both. 3; chglgggota and 3‘ grzthcggg males
were not significantly different in Lu, but were
significantly different in SUL. 3; ghglggnotg and 3*
limggghggig males were not significantly different in
SVL, but were in Lu. Females presumably had to assess SVL V
in order to discriminate between male 3; grzthggeg and
,nggnglggngtg, and consider Lw in order to discriminate

male 3; ghglgonota and B; limnogharig.

154

Table 57 presents a summary of isolating mechanisms
between all combinations of species pairs within the
community. Factors included in this matrix are adult size,
temporal habitat partitioning, coarse and fine spatial
habitat partitioning and advertisement calls.

It is interesting to note that there was little
temporal overlap between the peak calling periods of B;
ghglsgggtg and g; ggzthrggg. These two species were
similar in size and shape and had quite similar advertisment
calls. They apparently relied on temporal differences and a
degree of fine spatial habitat partitioning to maintain
isolation. B; chalggggta had a distinctive odor and
this could have been involved in species recognition.
Further, male 3‘ grzthraeg had small asperities on their
chins and it is possible that these were used as a tactile
cue in species recognition. As previously stated, SUL
separated 3; grzthraea and B; chglgonotg males as a
size cue. '

The pairs 3; erythraea/34 limnocharis and B;
erythraea/B; cancrivora had high temporal overlap in their
calling periods and apparently relied on fine spatial
habitat partitioning, size differences and distinct
advertisment calls to maintain isolation.

.33 [imngchgrig and 3; gancrivgrg were greatly
overlapping in their peak calling‘periods and in
microhabitat preferences for calling site. Both species had

skin rugosities which eliminated possible tactile

‘E’

15555

Table 57. Smary of reproactive isolating nechanisns for species by
species cubinations.

 

it. chalconota

 

 

1. size sinilar

2. little temp.
overlap

3. found at
sue site

4. partial fine
spatial part.

5. call inil

 

8.4.0.4
claim-3.3

spatial part.

spatial part.

R. m R. cancrivora o, Iina

1. size differs 1. size differs 1. size differs

2. tenporal 2. temporal 2. little ten.
overlap overlap overlap

3. found at 3. found at 3. found at
sane site sue site sane site

4. conpiete fine 4. conpiete fine 4. cuaplete fine

spatial part.

 

 

_§;_ggll differs, 5. call differs 5. call differs
1. size differs 1. size differs 1. size differs
2. little ten. 2. little tenp. 2. temporal
overlap overlap overlap

3. found at 3. found at 3. not found at
sue site sue site sane site

4. conpiete fine 4. caplete fine 4. conpiete fine
spatial part. spatial part. spatial part.

 

 

 

5, gall giffgrs 5. call differs 5. call differs
1. size differs 1. size differs
2. tenporal 2. little tenp.
B!!! overlap overlap
. - 3. found at 3. found at
11312513112 sane site sane site
4. little fine 4. conpiete fine
spatial part. spatial part
5. call differs, 5. call diffg;g_q
1. size differs
2. little tenp
overlap
352’ . 3. found at
53555139£3 sane site
4. conpiete fine

 

5.

spatial part.
call differs

 

 

156

recognition other than size. Size and call differences
likely function to maintain genetic isolation.

3, ghglgoggtg and Q;,llm3,were completely
isolated by coarse spatial habitat partitioning, that is,
they never occurred at the same site. Beyond this,
microhabitat preferences, advertisement calls and size were

also distinctive.

The combinations of BJ gnalggngta/BJ limnocharis, 3;

ghalgonota/B; cancrivora, B; erythraea/Q; lima, g;

limnocharis/9h lim§_and B4 cancrivora/Q4 leg_were well
isolated by fine spatial habitat partitioning, temporal
habitat partitioning, size differences and distinctive calls.
In a study of ten sympatric hylid species, Duellman
(1967) concluded that, although mechanical isolation
(principally size) between some species was obvious, the
most important isolating mechanisms were behavioral. He
reasoned that even though each species had characteristic
calling and oviposition sites, the sites were not exclusive
and could not be regarded as primary ethological isolating
mechanisms. Duellman (1967) concluded that the distinct
mating calls of the species were the 'primary' isolating
mechanisms. Among the five species of west Javan ranids
studied, mating calls were certainly an important isolating
factor, but to call them the primary factor may not be
Justified. Certainly all reproductive isolating mechanisms
within the available repertoire were important from the

standpoint that precious time and effort was not wasted in

157

attending to a frog of the wrong species. The breeding call
is but one of these.

Several other investigations have examined existing
reproductive isolating mechanisms in frog communties.
Bowker and Bowker (1979) evaluated spatial and temporal
habitat partitioning for ten species of African anurans.
They concluded that, because these explosive breeders were
restricted to breeding within a short time period of
available water, seasonal isolation did not occur. Habitat
isolation (Ifine spatial habitat partitioning) and temporal
isolation were present in the African frog community.
Temporal separation of breeding activities was not complete,
but it reduced the number of frogs breeding at any one time
from ten to five. when spatial and temporal aspects were
considered together, the four most abundant species were
completely separated. Heyer (1973) reported that the rainy
season frogs he studied in Thailand subdivided the available
breeding sites by (1) utilizing different ponds, (2)
occupying a single pond at different times and (3) dividing
up the living space within a pond spatially. Channing
(1976) concluded that three species of South African Kgsgin;
depended primarily on differences between mating calls and
calling sites of the males for premating reproductive
isolation, but did not examine the other anti-mating
isolating mechanisms such as temporal or spatial factors.

In the present study, each species exhibited continuous

breeding and the densities of breeding frogs were never as

158

high as might be encountered at the breeding congresses of
explosive breeders. Breeding was not a frenzied activity
and some breeding behaviors (especially vocalizations) were
observed on every nocturnal trip to the ponds. Because the
species live and breed at the same site, it is doubtful that
the carrying capacity of the habitat in terms of availabilty‘
of food and space is exceeded as it might be at the
temporary breeding habitat of an explosive breeder. Crump
(1982) stated that, in the Ecuador frog community she
studied, calling site specificity seemed to be less rigid
when many species called sympatrically and synchronously.
if this is generally true, then the calling microhabitat
specificities observed in the present study, where the
densities were consistently low, were probably the true
preferences of the frogs.

A suite of variables were involved in maintaining
reproductive isolation among these five secies. The
relative importance of each is difficult to assess, but it
is likely that temporal habitat partitioning, fine spatial
habitat partitioning, body size and breeding call acted in
concert in maintaining genetic isolation among these five

ranids.

WM;
Pianka (1978, p104) defined net reproductive rate as
'the average number of age class zero offspring produced by

an average newborn organism during its entire lifetime.‘

159

Margalef (1963) generalized that an inverse relationship
exists between species diversity and reproductive rate.
Inger and Bacon (1968) tested Margalef’s generalization
using Bornean rainforest 3553. They made the basic
assumption that the tropical rainforest contains the most
diverse faunas and used an empirical relationship
(Terentjev, 1960) between clutch size and female size for
predominantly temperate zone 33g; to generate expected
clutch sizes for the Bornean 353;. The expected clutch
size was always greater than the observed for the rainforest
figg; and the authors considered this evidence in support of
Hagalef’s generalization. Inger and Bacon (1968) did
acknowledge that the possibility of multiple clutches per
year was an additional unknown factor. In fact, mean clutch
size and mean number of clutches per lifetime are equally
important in consideration of net reproductive rate.

Even though the five species in the present study were
tropical species, they differed from the rainforest frogs
that Inger and Bacon (1968) studied in that they were from
disturbed, human-impacted habitats. Margalef (1963)
generalized that in such changing, early-successional
environments, the reproductive rate should be high. For
purpose of comparison, TerentJev’s (1960) formula was
applied to the west Javan ranid frogs to determine their
expected clutch sizes. The formula is:

log N - -1.7423 + 2.1670 log L

where 'N' - number of ova in thousands and 'L' - maximum

160

size of female in centimeters. The maximum sizes of the
females were taken from Table 31. In contrast to Inger and
Bacon’s (1968) findings, the mean observed clutch size was
the same (in 3; erzthraga) or greater than the expected
clutch size (3.5 times greater for 3, gangriggrg). The
data are shown in Table 58.

For these five west Java species the potential for high
reproductive rate is present and this supports Margalef’s
generalization. Actual data on number of clutches per
lifetime are not available, but can be estimated using
information from the literature.

The clutch sizes of the west Javan ranids are high
compared to their temperate zone counterparts, but how do
their net reproductive rates compare? Growth to maturity
and longevity were not examined in this study, but
information is available from the literature for B,
grzthragg and B; limnggnggls. Female 3,
ggztngagg in the Philippines reached sexual maturity in
approximately nine months post-metamorphosis and males in
six to seven months after metamorphosis (Brown and Alcala,
1970). In the same study, the maximum life span for 3,
ggzjnnggg_was determined to be three to four years.
Alexander ;; Ala (1963) reported female 3, -
llmnggnggig in Taiwan reached sexual maturity in four
months after metamorphosis and survival fell off drastically
after the second and third years of life. In the present

study, male 3,,gnalggggta reared from fertilized ova in

161

Iahie 5C. Cuparison of predicted and observed clutch sizes.

 

 

Species Predicted tbserved Clutch Size Ratio of ibsereed to
Clutch Size! lfean 951 C.I. Predicted Clutch Size

3.14.! SMELL!!! 3871 13611 11733-15489 3.5

m M 959 1750 1368-2132 1.8

M m 1303 1304 1154-1454 1.0

m m 1537 2207 2030-2383 1.4

m m 299 437 353-513 1.5

 

il’redicted clutch size uas deternined b7: log N 8 4.7423 f 2.1670 log i.
den N is umber of ova in thousands and i. is naxinu size of fenale in
centineters (Terentieu, 19ft).

162

\

Bogor, west Java had secondary sexual characteristics,
including vocalization, in approximately six months. No
information is available for 3; ggggglggga or Q,

11mg, but it is reasonable to assume that they reach
sexual maturity within one year or less. Even the large
introduced species, gang gggggggiana, which is cultured
in Java, reaches sexual maturity in less than one year
post-fertilization.

The overall and monthly percentages of mature females
that were reproductively ready (Table 56) were surprisingly
high in all of the species. These percentages can be
interpreted to mean that, on average, 77% of the population
of mature female 3; ggggrigora are reproductively ready
at any given time. Samples of females were taken at regular
monthly intervals in order to obtain a realistic picture of
the reproductive readiness of the populations. Individual
females were not followed over time to determine what
percentage of an annual cycle they were reproductively
ready, but an indication of this percentage can be
extrapolated from the population data. In order for the
populations to demonstrate such high percentages of
reproductively ready females during all 12 months of the
year, individual females in each population would have to
spend a large portion of their time in the reproductively
ready state. Unfortunately, the number of clutches produced
per year, the time it takes for one clutch to become mature

(reproductively ready), or how long a female with a

163

reproductively ready clutch goes before ovipositing, are
unknown. However, it seems implausible that an individual
female would spend the major portion of a year carrying the
same clutch of mature ova. Therefore, these data lend
evidence for the probability being high of more than one
clutch being produced by a female on an annual basis and
perhaps several actually being produced. 'Double clutching"
has even been reported for some temperate ranids (Emlen,
1977; wells, 1976).

Multiple clutches per year are probably the rule rather
than the exception in the west Javan species, which start
breeding at an earlier age than their temperate zone
counterparts. However, temperate zone frogs tend to live
longer and therefore net reproductive rate, ggggg Pianka
(1978), of tropical and temperate ranids may be nearly
equal. At least the picture is more complicated than a
simple comparison of clutch sizes.

Demographic information from the literature allows
comparisons to be constructed between the west Java ranids
and their temperate counterparts. These comparisons require
several assumptions, as actual data are lacking, but provide
some interesting questions for future work. Longevity data
for anurans other than captive animals are rare, but Hartof
(1956) reported a maximum life span of three to six years
for 359; glgmitans in Michigan and Turner (1960)
reported that female 353; grgtiosg can live ten to

twelve years in the wild. If six to ten years is allowed as

164

a maximum life span for temperate Bang, the potential
exists for five to nine clutches being produced per
reproductive life time (assuming a single clutch per year
and sexual maturity at age one). It is likely that all of
the west Javan ranids breed for the first time before or at
age one and if we allow a maximum life span of four years
(Alexander :3 31;, 1963; Brown and Alcala, 1970), this
gives a maximum breeding lifetime of three years. In order
for the net reproductive rate of the west Javan ranids to
equal that of the temperate ranids, the tropical forms would
have to produce only two or three clutches per year
(assuming equal clutch size). However, four of five of the
Nest Javan ranids have larger clutch sizes than
similar-sized temperate forms, so it is likely that their
net reproductive rate exceeds that of the temperate ranids

in general.

N r l i an o o r

The model of 'r and K selection“ can be used for
comparing the members of the west Javan ranid frog
community. MacArthur and wilson (1967) used the terms 'r
selection' and 'K selection“ after the two terms in the
logistic equation for population growth where 'r' is the
intrinsic rate of natural increase and 'K' is the carrying
capacity. Pianka (197B) stressed that an organism can be
considered an 'r' strategist or a 'K' strategist only

relative to some other organism. Based on several

I65

generalized attributes of 'r' and 'K' selection, the five
Nest Javan species can be relatively aligned along the 'r-K'
continuum. Crump (1974) used clutch size alone to position
Ecuadoran anurans on this spectrum. Clutch size is a very
important criterion in this regard, but actually several
factors should be considered together as criteria. Clutch
size alone may not be adequate information if the frogs
being compared differ as to number of clutches per year or
per reproductive life time.

Table 59 outlines some of the characteristics of the
five species in relation to 'r' and 'K' strategies. Based
on the information in this table, 3; ggnggigggg should
be positioned as the most 'r' selected species and B,
ggztnnaga as the most 'K' selected. B,_llmnggflgLLg
falls into the 'r' selected part of the spectrum and 3‘
ghglggngga is more 'K' selected. Information is limited
for Q; llmg, but it is placed near B;_1lmng§ngglg.

Salthe and Duellman (1973) considered the goal of any
reproductive strategy to be the production of adequate
genetic variability per unit time. One characteristic of
'r' selected organisms is that they are opportunistic forms,
that is, good colonizing species rather than 'equilibrium'
type species. Inherant variability would be a favorable
attribute to a colonizing species which encounters new
environmental conditions. 3; ganggivgca, B,

limngghgcig and Q; lflma all have high coefficients of
variation (CUZ) for clutch size (Table 28) when compared to

166

 

 

 

 

 

 

 

 

 

 

 

 

 

 
 

 

 

 

 

 

 

 

 

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167

3; gnglggflgtg and g, grzthraga. This may indicate

more variability within their populations and lends extra
support for designating them as relative 'r' strategists.
Can the extent of the ranges of each of the five west
Javan ranids be explained by their relative 'r' selectedness
(that is, their 'weediness' or colonizing ability)? Species
that are 'r' strategists tend to be good colonizing species
and it could be hypothesized that this attribute should
allow these species to disperse and extend their ranges more
readily. Range maps for each of the five species (compiled
from previously cited literature) are given in Figures
31-35. Peninsular Thailand and Malaysia are near the center
of distribution of each species, so many of the same
physical barriers to dispersal have confronted these frogs.
The five species should also be comparable from the
standpoint that they are all generalized mode breeders
(Salthe and Duellman, 1973) and therefore have similar
requirements for breeding habitat. Inger (1966) designated
Q, Li a (Figure 31) as a transitional species probably
of Indo-Chinese origin, 3, gaggriggrg (Figure 32) a
transitional species probably of Malaysian origin, 3;
ghalggngta (Figure 33) an exclusive Malaysian species,
and B; grzthragg (Figure 34) and 3, limggcngrig
(Figure 35) shared species between Malaysian and Indochinese
areas. Inger (i966) designated several members of the

Bornean frog fauna as 'commensals of man", including 3;

cancrivora, fl; iimnogharig and g, erythraea.

168

 

40° -_ ’
3ooh- ”’ a [I

I ’I/ A
.- ///Mé¢, ii: ”’
10° P-- _.-.— — --"é$

0°.

 

 

 

10°

 

Figure 31. Range of Ooeidozyga Zima.

 

40°

30°

20°

10°

0°

10°

 

 

 

 

Figure 32. Range of Rana cancrivora.

169

 

40° ~_

30° ~-

20° — _ _._

10° ~— ..

 

 

 

 

 

 

 

 

0°’
10°

Figure 33. Range of Rana chalconota;
30° ~.- _.‘

20° ~ _

//‘/
10...._/._
0

oo ______ _ _ ____ -—

100 ___________

Figure 34. Range of Rana erythraea.

 

170

 

V, ([4 7
400‘... ,/ U%’/

30°

  

20°

V/a

" I
9"
-

”

10°

“
-fi’

’
..

0° L—-

 

10°

../ ”in ////’,;// /

v I
,o’

 

 

Figure 35. Range of Rana ‘Zimnocharis.

171

g; ghglgongt; did not behave in this way in Borneo
(lnger, i966), but it did in Java, occurring frequently in
disturbed habitats near human habitation. 9; lim; also
occurred most frequently in flooded agricultural fields.
For these species, it is likely that human-induced
environmental perturbations have not provided a dispersal
barrier and, in fact, with the possible exception of B;
ghglggnotg, the dispersal of these frogs has probably
been enhanced by humans. Inger (1954) suggested that a;
grzthrae; has probably reached Celebes and the

Philippine islands through accidental human transport.
Alexander ££.LL; (1979) noted that g; limgggnarig in
Taiwan has a strong attraction for freshly plowed and
flooded soil and this phenomenon is also evident in west
Java for 3; limggcharig and g; giggcivorg. This is
probably an adaptive characteristic for living in close
association with humans.

3; limnocharis (Figure 35) has, by far, the most
extensive range. It extends to 36 degrees north (Pope and
Boring, 1940) and eastward to Flores. 3; erzthrag;
(Figure 34) has the next most extensive range; however, if
Celebes and the Philippines are disregarded as areas of
possible accidental introduction by man (Inger 1954), the
longest axis through the total range is not much greater
than that of B; gangrivgca or Q; 11mg. ‘3;
ggnggiggng (Figure 32) and g; Lia; (Figure 31) have

quite similar-sized ranges although 9; lima has extended

172

farther north into Asia and 3‘ gaggnigggg has extended
further east into the Indonesian archipelago and north into
the Philippines. The existence of Q; llm; in Sumatra

has not yet been reported. 3; ghglconotg has the least
extensive range, although interestingly it was able to cross
the Makassar Straits from Borneo to Celebes.

The relationship between degree of 'r' selectedness and
large range is not perfect. However, the second most 'r'
selected species (3; limngghggig) has the largest
range and the second most 'K' selected species (B;
gnglggggtg) has the smallest range. 3, erzthragg,
the most 'K' selected species, has a fairly extensive range,
but if areas of probable anthropogenic distribution are
disregarded, the range is quite similar to Q; llmg_and
3; cggcrivgrg (both 'r' selected species).

Perhaps the tendency for 'K' selected species to be
good competitors has allowed them some advantage in becoming
established in new localities. This may have tended to
equalize the dispersal abilities (those related to 'r-K'
selection attributes) between 'r' selected species and 'K'
selected species (thus, the relatively large range of 3;
.ggztngggg). Assuredly, other physiological, behavioral
and ecological factors are involved with the dispersability

of these species.

SUMMARY AND CONCLUSIONS

Five species of ranid frogs living in pond habitats of
West Java were studied through an annual cycle to ascertain
their mechanisms for reproductive coexistence in relatively
uniform, man-impacted environments. Both field observations
and dissection of monthly samples of each species provided
information for evaluatLon of their reproductive biology.
west Java has an aseasonal tropical climate with a natural
vegetation of tropical rainforest. However, its natural
vegetation has been heavily altered by human and human
agriculture.

Field studies elucidated seasonal, temporal and spatial
attributes of the community members’ reproductive behaviors.
No seasonality was observed in the calling activities of
males. Every month was utilized for breeding. All five
species called predominantly between the hours of dusk and
dawn, but temporal partitioning of calling activities was
apparent. Species divided the available habitat on both a
coarse level (different species choosing different ponds)
and a fine level (each species having characteristic
microhabitat preferences within a pond).

An evaluation of anti-mating and courtship isolating
mechanisms revealed that temporal partitioning, microhabitat

partitioning, body size differences, and distinctive mating

173

174

calls acted together to maintain genetic isolation.

Quantifiable variables were recorded from dissected
specimens. The results are summarized as follows.
I. - Shout-vent length and live weight were highly
correlated for each species and a one-to-one relationship
existed between live weight and live volume.
2. - Sexual dimorphism in size was present in each species
(males smaller than females). Female live weight was
greater than male live weight by 1.7 to 4.4 times depending
on the species. Possible reasons for sexual size dimorphism .
are discussed.
3. - Mean sizes for males of all five species were
significantly different. Mean sizes for females of the five
species were significantly different except for the pair
Bag; chalconota and 3; grzghrgga.
4. - Large fat bodies were distributed across all size
classes of male and female frogs. There was no apparent
trend for small or large frogs to more frequently possess
large fat bodies. In either sex, no clear trends were
present among the species as regarded possession of large
fat bodies in relation to sexual maturity. In three of five
species, similar percentages of mature males and females
possessed large fat bodies. In the remaining two species, a
higher percentage of mature males possessed large fat
bodies. No trend was observed between possession of large
fat body and possession of enlarged ovarian ova in any of

the species. Seasonality with respect to possession of

175

large fat bodies was not observed.

5. - It was concluded that external secondary sexual
characteristics in males were accurate indicators of sexual
maturity, as Judged by testis size. Calculated testis
volume (assuming cylindrical shape) was Judged to be a more
accurate index of actual testis size than was testis length
alone. There was significant positive correlation between
testis volume and snout-vent length for four of the five
species.

6. - Partial ovulation occurred in Bag; gancrivora, but

was not observed in the other four species.

7. - Developing ova and ovaries were classified using an egg
pigmentation criterion, but it was found that the ova stages
were distinctive on a size basis as well.

8. - An interspecific positive correlation existed between
female body size and ovum diameter for four of the five
species. 35g; cancrivora did not follow the same
relationship. Two of the five species showed a significant
positive correlation between female body size and ovum
diameter within the species.

9. - In most cases the left ovary was found to be heavier
than the right ovary in four of the five species.

10. - Intraspecific correlations between live weight and
ovarian weight of reproductively ready females were present
in all five species. Larger females carried larger egg
masses. An interspecific correlation between mean live

weight and mean ovarian weight existed among the five

176

species with the larger species accomodating larger egg
masses.

11. - The means for percent body weight contributed by
ovarian weight (percent ovarian weight) for reproductively
ready females ranged from 6.5% to 11.7%, depending on the
species, and the mean percent ovarian weights were
distinctive for each species. Percent ovarian weight was
not significantly correlated with body weight within or
among species.

12. - Mean clutch size ranged from 434 to 13,611. Four of
five species demonstrated a significant positive correlation
between body size and clutch size. Among species there was
a pattern of increased clutch size with increased species
size which was very similar to the ovarian weight-live
weight interspecific relationship.

13. - No seasonality in testis volume occurred in males. No
seasonality in clutch size or in the percentage of mature
females that were reproductively ready was observed.

A consideration of the quantitative variables indicated
that 353; gaggrivgrg is more similar to the ggig mode of
reproduction than it is to the Bag§_mode. It tends to have
a large clutch size composed of small ova. 3553
grzthgaea also stands out in that it devotes a
relatively small proportion of its body mass to egg mass.

Ban; limgggharig is a species that demonstrates

reproductive seasonality in parts of its range that are

177

seasonal and does not in areas where equable conditions
exist year-round.

The five frog species studied do well in disturbed,
early successional habitats. They have a high fecundity
when compared to temperate zone Egg; or Bornean tropical

rainforest Rana. Reproductive rates of the west Javan

 

ranids and their temperate zone counterparts were compared.
It is likely that net reproductive rates for the west Javan
forms are higher. Indirect evidence indicated that multiple
clutches per year are likely with the frogs studied.

The west Javan frogs were aligned on the 'r-K'
selection continuum and their relative position on this
scale is considered in relation to the geographic range of
each species. The degree of 'r' selectedness is not
perfectly related to large geographic range among the study

species.

LITERATURE C I TED

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