Studies in Larval Amphibian

Habitat Partitioning

W. RONALD HEYER

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 242
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SMITHSONIA N CONTRIBUTION S T O ZOOLOG Y • NUMBE R 242

Studies in Larval Amphibian

Habitat Partitioning

W. Ronald Heyer

SMITHSONIAN INSTITUTION PRESS

City of Washington

1976
ABSTRAC T

Heyer, W. Ronald. Studies in Larval Amphibian Habitat Partitioning. Smithsonian Contributions to Zoology, number 242, 27 pages, 3 figures, 14 tables,

1976.—Habitat partitioning by larval amphibians was studied in two environments. A two-year study was undertaken at the Chesapeake Bay Center for Environmental Studies and a comparative dry and wet season study was completed

at Barro Colorado Island, Panama.

At the Chesapeake site, partial year to year differences in temporal larval

habitat partitioning combined with different year to year population sizes

indicate: (1) different habitat utilization from one year to the next by the larvae,

and (2) different biological interactions involving predator-prey and species associations from year to year.

The stream bed pond habitat on Barro Colorado Island is effectively partitioned by the tadpole community on the basis of space and time. Predation

is an organizing factor in the composition of the tadpole community, interspecific competition apparently is not.

This study concludes that competition among tadpoles does not normally

occur in nature. Bursts of primary productivity provide superabundant food

resources. The habitat partitioning found in tadpole communities reflects the

temporal and microhabitat differences associated with the evolutionary life

history of each of the species occurring in any pond. Tadpole communities are

additive collections of different species, not integrated, interactive superorganizations.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded

in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coral Montastrea

cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data

Heyer, W Ronald

Studies in larval amphibian habitat partitioning.

(Smithsonian contributions to zoology ; no. 242)

Bibliography: p.

Supt. of Docs, no.: SI 1.27:242

1. Tadpoles. 2. Habitat partitioning. 3. Amphibians—Ecology. I. Title. II. Series: Smithsonian Institution. Smithsonian contributions to zoology ; no. 242.

QL1.S54 no. 242 [QL668.E2] 591'.08s [597'.8'0439] 76-608161
Contents

Page

Introduction 1

Acknowledgments 1

Chesapeake Bay Area 2

Methods and Materials 2

Temporal Succession 2

Microhabitat Partitioning 8

Microhabitat Metrics 10

Discussion 13

Barro Colorado Island 15

Methods and Materials 15

Results 15

Habitat Partitioning 17

Discussion 17

Other Studies of Larval Habitat Partitioning 18

Tadpole Community Organization 19

The Generalized Anuran Life Cycle and Its Evolutionary Maintenance . 22

Selection, Population Control, and the Anuran Life Cycle 24

Evolutionary Modifications of the Generalized Anuran Life Cycle 25

Literature Cited 26

in

Studies in Larval Amphibian

Habitat Partitioning

W. Ronald Heyer

Introduction

The single goal of this study was to learn more

about how habitats are partitioned by larval amphibians. Data were gathered from two very different sites, a temperate pond and a series of tropical

stream ponds.

The study of habitat partitioning by larval amphibians has been previously neglected. There are

fewer than a half dozen descriptive studies and

only 4 quantitative studies (cited in Heyer, 1973).

The temperate pond (present study) was followed

for two years to study year to year variability in

habitat partitioning. The tropical stream ponds,

located on Barro Colorado Island, were sampled

once during the dry season and once during the

wet season to determine the effects of seasonality on

habitat partitioning by stream pool larval amphibians.

The studies at the two sites are described separately because the methods and analyses of data

are different. Patterns of habitat partitioning evidenced at the sites are then compared. Any patterns of habitat partitioning common to these two

environmental extremes should be common to

larval amphibia in other environments.

It is necessary to define larval amphibian habitat

partitioning as used in this study. The habitat consists of one or more ponds found at a specific site.

W. Ronald Heyer, Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution,

Washington, D.C. 20560.

The habitat contains the resources utilized by

different species of larval amphibians; different larval species utilize the habitat resources in different

ways. The patterns of habitat usage produced by

different larval species are manifested as a partitioning of the habitat resources. Larvae may partition the habitat in terms of space, time, or food

(among the more obvious categories). Examples of

partitioning include: (1) where the habitat consists

of a series of ponds at a single site, larvae of a

particular species may occur in only a few of the

available ponds; (2) within a pond, larvae of a

single species may be found only in certain microhabitats or they may utilize only certain kinds of

food; (3) two species may use the same pond at

different times as larvae. The studies reported

herein reveal both space and time habitat partitioning by larval amphibians.

ACKNOWLEDGMENTS.—Roy W. McDiarmid, University of South Florida, Richard J. Wassersug,

University of Chicago, and George R. Zug, Smithsonian Institution, carefully read the entire manuscript. Linda R. Maxson, University of Illinois, read

the section discussing the amphibian genetic system. Comments from the reviewers considerably

improved the paper, but the reviewers do not

necessarily agree with all of the conclusions or discussion.

The following persons supplied specific information: Ronald I. Crombie and James F. Lynch,

both of the Smithsonian Institution, William F.

1
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Pyburn, University of Texas at Arlington, and

Kentwood Wells, University of Connecticut.

The Environmental Sciences Program of the

Smithsonian Institution supported the field work

in Panama.

Elena, Laura, and Miriam Heyer participated in

the field work both in Panama and in the Saturday

excursions to the Chesapeake site. Without their

help and cooperation, the study would not have

materialized.

Chesapeake Bay Area

METHODS AND MATERIALS.—Larval samples were

taken once a week from 9 March to 29 June 1974

and from 22 March to 28 June 1975. A sample for

15 June 1974 was not obtained due to illness. An

additional sample of 26 July 1975 was taken to

determine whether any drastic changes occurred

after June, the arbitrarily determined end of the

sampling period. In both years, sampling preceded

the onset of tadpole occurrence. Samples were

taken from a large, shallow pond surrounded by

hardwood forest at the Smithsonian's Chesapeake

Bay Center for Environmental Studies near Annapolis, Maryland. The common trees in the

forest are beeches, hickories, oaks, and tulip trees.

Three microhabitats were sampled by dipnet each

sampling period. The dipnet had a triangular opening. For the surface samples, the base of the triangle was placed just under the surface of the

water. The surface film and about the top 5 cm

of water were swept at the grassy edge of the pond

where the water was about 30-40 cm deep. The

net skimmed the top of the grass. The midwater

sample was taken farther from the shore, in about

60-70 cm water, in grassy and open water areas.

The net opening was completely immersed, then

the net was propelled through the water. Open

water areas were emphasized in the midwater sample. The bottom sample was taken in the same

general area as the midwater samples, but the

grassier areas were emphasized. For the bottom

sample, the net was bumped along the bottom. The

linear distances sampled for the sweep types were

variable, but comparable. Generally, at least a

25 m linear sweep was made for each sample. If

the net had an abundance of tadpoles, no further

sampling was done in that microhabitat. If few or

no tadpoles were collected, additional sweeps were

made. The same microhabitats were sampled each

week in the same way both years. The surface,

midwater, and bottom sweeps sampled three more

or less discrete areas of the pond. The results were

of course only a reflection of the dynamics of the

populations of the entire pond.

The tadpoles of each sweep type were formalin

preserved in separate containers. In the laboratory

the samples were sorted and identified to species

level. Salamanders were measured by vernier calipers, snout-vent and total lengths measured to the

nearest 0.5 mm. Tadpoles were staged (Gosner,

1960). For very large samples (unless all were hatchlings), 50 individuals were staged and the total

sweep sample for that species was extrapolated from

the staged subset. The 1974 sample is represented

by 1182 individuals, the 1975 sample by 2755 individuals. All specimens (total study) are in the

collections of the Division of Reptiles and Amphibians, National Museum of Natural History.

TEMPORAL SUCCESSION.—1974 Pattern: Ambystoma maculatum egg masses were first seen on 16

March, but may have been present (and overlooked)

previously. Hatchlings were not collected until 4

May (Figure 1). The previous week, 27 April, an

empty salamander jelly case was found in the pond,

but no larvae were collected in the sweeps. Many

dead egg masses were found in April and May. At

the end of June, some of the larvae were metamorphic size.

Ambystoma opacum lays its eggs in the fall. Larvae were present in the pond when sampling

started on 9 March. The population demonstrated

a synchronous growth pattern (Figure 1). The last

larvae, of metamorphic size, were collected on 18

May.

Hyla crucifer hatchlings were first collected on

13 April (Figure 1). Hatchlings continued to be

collected through 4 May, indicating a probable

breeding season of about a month for H. crucifer

in 1974. Metamorphic larvae were first collected

on 25 May. Only prometamorphic larvae were collected on 8 June. All larvae apparently completed

metamorphosis prior to 22 June (no sample available for 15 June). The time spreads of hatchling

appearance and metamorphosis are comparable.

Hyla chrysoscelis (not versicolor, James Lynch,

pers. comm.) were first collected on 1 June (Figure
NUMBER 242

1). The two larvae collected were both well beyond

stage 25. Hyla chrysoscelis was not abundant in the

pond; sampling error probably accounts for hatchlings not being collected prior to 1 June. Collections of only large larvae on 22 and 29 June suggest that the breeding period for H. chrysoscelis

ended in early June in 1974.

Rana clamitans were first heard calling on 11

May. Larvae were first collected on 1 June. Larvae

were never abundant, but hatchlings were collected through the entire sampling period (Figure

1).

Rana sylvatica larvae were first collected on 6

April. Population growth appeared rather synchronous; metamorphic larvae were last collected

on 1 June (Figure 1).

Bufo americanus were collected only once, as

hatchlings, on 20 April. Concerted efforts to recollect the species within the sampling areas were

unsuccessful for the remainder of the sampling

year.

No Acris crepitans larvae were collected in 1974.

Tadpoles could be seen easily only in the open

water areas of the pond. In 1974, from mid-April

to mid-May, Rana sylvatica larvae were predominant; the population, estimated visually, appeared

to be very large in the open water. After the R.

sylvatica had metamorphosed, there appeared to be

little tadpole activity in the open water areas of

the pond.

1975 Pattern: Ambystoma maculatum eggs were

found on the first sampling time of 22 March. Larvae were not collected until 26 April (Figure 2).

Small larvae were collected over a long period, from

26 April to 31 May, apparently reflecting differences

in hatching times of the various egg masses. Larvae

were present throughout the remainder of the

sampling period (Figure 2). Only one egg mass

was found in which a noticeable percentage of eggs

was inviable.

Very few Ambystoma opacum larvae were collected in 1975. Sampling errors apparently account

for lack of specimens from the sampling dates of

29 March through 19 April. Larvae were last collected on 26 April (Figure 2).

Hyla crucifer egg masses were first observed on

22 March. Hatchlings were collected from 12 April

to 31 May, an 8 week period (Figure 2). Metamorphs were first collected on 31 May and last

collected on 28 June. Judging by the staging graphs

and relative numbers (Figure 2), the population

had completed, or was in the process of, metamorphosis by 28 June.

Hyla chrysoscelis larvae were first collected on

31 May. The staging graphs (Figure 2) suggest that

the breeding period was short and the tadpole

growth was synchronous through 28 June.

Overwintered Rana clamitans larvae were collected on the first sampling date, 22 March (Figure

2). Calling males were first heard on 10 May, and

the first spring hatched larvae were collected on

10 May as well. Early developmental stages of the

overwintering larvae were much larger than the

same stages of the spring hatched larvae. Larvae

were present throughout the entire sampling period.

Rana sylvatica eggs were observed on 22 March.

Hatchlings were first collected on 19 April and

last collected on 10 May. Late prometamorphic

larvae were first collected on 24 May and last collected on 28 June (Figure 2).

On 3 May, a calling male of Acris crepitans was

captured for identification. Calling males were

heard on sampling dates from 3 May through 21

June. Larvae were never abundant and were first

collected on 21 June (Figure 2).

On 26 July, a sample was taken to determine

whether the sampling time span concluding with

the end of June was adequate to describe the essential tadpole interactions. Larvae of three species

were collected: Acris crepitans (6 individuals), Hyla

chrysoscelis (2), and Rana clamitans (18). Hatchlings were collected only of R. clamitans. This

sample indicated that while larvae were still in the

pond, most of the larval activity had concluded

before the end of June. No additional species were

represented, nor were the species present represented by large numbers.

The sample date of 5 April is notable because

no larvae were collected, although they must have

been present in the pond (Figure 2). The temperature was cold at the sampling time. The air temperature was 0.4° C, the water temperature 3.4°

C, and there was a film of ice on the water. The

cold temperature may have caused the larvae, as a

behavioral response, to leave the sites they normally

inhabited when temperatures were more favorable.

In the open areas of the pond, the predominant
t!

27 APRIL 5 20 APRIL 5 13 APRIL

o 00 00

r ° r

5

 6 APRIL

00

5

 3 0

 MARCH 5 23 MARCH 5

00

5

00

5 16 MARCH

o 9

5 9 

00 
NUMBER 242

100

AMBYST. AMBYST. HYLA

MACUL. OPACUM CRUCIFER

HYLA RANA RANA

CHRYSOSCELIS CLAMITANS SYLVATICA

. 0

. 0

- 0

. 0

. 2

1 1

. 7

I.

. 15

.1

. 2

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-I

-

-

33

33 j

1

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 :

i

7 !

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3

1

0

0

0

45 25 45 25 45 25 45

opacum, left to right, < 15 mm, 16-22 mm, 23-29 mm, > 30 mm. Horizontal axes for tadpoles = Gosner (1960) stages. Dashed vertical lines = metamorphosis. Number within each

graph = total number of individuals per sample.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

species, estimated visually, was Bnfo americanus. two years produces some striking similarities and

Comparison of the 1974 and 1975 Patterns: A striking contrasts (Figure 3).

comparison of the patterns observed during the Each of three species repeated in 1975 the temlOOi

I •

o

I

(VI

lOOi

O

ac

2

a>

<M0

100

100

tr

a.

100

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ac

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AMBYST. AMBYST. HYLA

MACUL. OPACUM CRUCIFER

100

I

100

I

20

. 3 IV

36

50

292

427

514

HYLA RANA

CHRYSOSCELIS CLAMITANS

RANA

SYLVATICA

25

k

45 25 45 25

18

19

1

45 25

L

BUFO ACRIS

AMERICANUS CREPITANS

82

1

42

130

45 25

1

45 25 45
NUMBER 242

poral pattern of 1974: A. maculatum, Hyla crucifer,

and Hyla chrysoscelis (Figure 3). Hyla chrysoscelis

not only had the same temporal pattern but also

had consistently low larval densities in both years.

The relative numbers of larvae for Ambystoma maculatum, as well as for Hyla crucifer, were quite dif100

AMBYST. AMBYST. HYLA HYLA RANA RANA BUFO ACRIS

MACUL. OPACUM CRUCIFER CHRYSOSCELIS CLAMITANS SYLVATICA AMERICANUS CREPITANS

10

10

iv

189

28

Jl

25 45 25 45 25 45 25 45 25 45 25 ^

FIGURE 2.—Larval occurrence in 1975 at the Chesapeake site. (Vertical axes are percent of occurrence of each category per sample. Horizontal axes for salamanders = snout-vent size classes:

Ambystoma maculatum, left to right, < 12 mm, 13-18 mm, 19-24 mm, > 25 mm; Ambystoma

opacum, left to right, < 15 mm, 16-22 mm, 23-29 mm, > 30 mm. Horizontal axes for tadpoles = Gosner (1960) stages. See Figure 1 for further explanation.)

45
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

A. MACULATUM

A. OPACUM

H. CRUCIFER

H. CHRYSOSCEUS

R. CLAMITANS

R. SYLVATICA

B. AMERICANUS

A. CREPITANS

•••••• i

MARCH APRIL MAY JUNE

FIGURE 3.—Presence of larvae in the Chesapeake site pond for 1974 and 1975. (Upper line for

each species = 1974, lower line = 1975. Dates supplied for which no larvae were collected

due to presumed sampling error—see text. Dashed lines = probable presence of larvae prior

to initiation of sampling in 1975—see text.)

ferent in 1975 from what they had been in 1974.

Although data were not collected on egg masses,

visual observation indicated that comparable numbers of A. maculatum egg masses were laid in 1974

and 1975. Egg mortality, high in 1974 and low in

1975, probably accounts for the different densities of

larval population in the two years. The patterns of

Hyla crucifer are similar at the onset of both years

but different at the end. The data presented in

Figures 1 and 2 suggest that the extended breeding

season of Hyla crucifer in 1975 may account for the

larger larval population in that year.

The remaining species show striking temporal

and population density differences when the data

for the two years are compared. Of these, the most

profound differences are found in Rana clamitans,

individuals of which overwintered in 1974-75, but

not in 1973-74. The first appearance of springhatched larvae of R. clamitans also differs: 1 June

in 1974, 10 May in 1975.

In order to understand fully the observed similarities and differences of the patterns of temporal

succession and population density recorded in each

of the two years, climatic patterns will have to be

examined and analyzed in detail together with the

larval data. Long term sampling, over several years,

not just two, is necessary to reveal relationships between climate and larval populations. For this reason, these relationships are not examined in this

paper. Sampling at the Chesapeake site is planned

to continue for the next few years to address these

relationships.

MICROHABITAT PARTITIONING.—The numbers of

individuals of each species were totalled by type of

sweep (Tables 1 and 2) to determine the differences

in abundance for each sweep type.

In both 1974 and 1975, Ambystoma maculatum

individuals were not equally distributed among the

three sweep types, more individuals being found in

the surface sweeps than in any of the other two

sweep types. Ambystoma opacum individuals were

statistically equally distributed among the three

sweep types in both years (based on small-sized

samples). Most Hyla crucifer larvae were collected

TABLE 1.—Distribution of individuals in microhabitats in 1974 (ns = not significant; • = significant at 5% level; •• = significant at or beyond 1% level)

Species Surface Midwater Bottom

Ambyatoma maculatum...

Amby8toma opacum

Hyla crucifer

Hyla chry8OBcelia

Rana clamitans

Rana syIvatica

Bufo americanus

11

6

452

6

3

7

296

2

3

47

17

4

121

0

4

2

2

3

9

48

0

7.88*

2.36 (ns)

575.81**

12.54**

3.88 (ns)

113.67**

592.00**
NUMBER 242

TABLE 2.—Distribution of individuals in microhabitats in 1975 (see Table 1 for key to symbols)

Species Surface Midwater Bottom x

2

Ambyetoma maculatum...

Hyla crucifer

Rana olamitans

Rana sylvatioa

Acris crepitans

59

0

882

1

1

6

4

0

28

1

567

12

67

34

434

1

47

3

426

11

79

38

43

1

10.94**

3.50 (ns)

174.42**

9.25**

72.00**

23.38**

705.41**

1.00 (ns)

in surface sweeps in both years. However, a statistically greater proportion of the population was

collected from midwater and bottom sweeps in

1975 than in 1974 (x

2

 = 1727.69). Most Hyla chrysoscelis larvae were collected from the midwater

sweep in 1974; in 1975 their concentration was divided equally between the midwater and bottom

sweep habitats. In 1974, Rana clamitans individuals were statistically equally distributed among all

three sweep types, while in 1975, almost all individuals came from the midwater and bottom

sweeps. Rana sylvatica larvae came mostly from the

midwater sweeps in both years. All Bufo americanus

larvae came from the surface sweeps in 1974, but

in 1975 their majority came from the midwater

sweeps.

For species represented each year by more than

100 individuals in total and by at least 10 individuals per sweep type, occurrence by size classes of

larvae has been determined (Tables 3 and 4). In

1974, statistically more medium-sized Hyla crucifer

larvae were found in the bottom sweep than expected and statistically more large-sized larvae were

found in the midwater sweep than expected (Table

3). There was thus an ontogenetic change in microhabitat preference for H. crucifer in 1974. This was

also true in 1975 when statistically more large larvae

were collected in the bottom sweeps than expected

(Table 4). No other species examined demonstrated

ontogenetic shifts in microhabitat preference.

The sweep abundance data can be directly related

to microhabitat preferences for each species, since

the sweeps sampled different microhabitats. As expected, microhabitat preferences were demonstrated

for each species for which a total sample size per

year was greater than 20 individuals. One would

also expect that species would demonstrate the

same preferences from year to year. The only species

that does not appear to be consistent with this hypothesis is B. americanus. However, the entire

TABLE 3.—Occurrence of larvae of two species (adequate for statistical analysis), arranged by

size classes, from sweeps in 1974 (size classes of tadpoles = Gosner stage groupings; left of

slash = observed figure; right of slash = expected figure based on equal occurrence among

sweep types irrespective of size; see Table 1 for key to symbols)

Species Size Surface Midwater Bottom

By la crucifer

Rana sylvatica

25-30

31-36

37-44

25-30

31-36

37-44

235/217

78/89

139/143

17/21

7/9

23/14

34/38

45/41

42/40

17/27

25/11

15/17

20/15

13/16

16/16

5.96 (ns)

19.62**

6.13*

31771**

"7720" (ns)
10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 4.—Occurrence of larvae of five species (adequate for statistical analysis), arranged by

size classes, from sweeps in 1975 (size classes of salamanders in mm; see Table 1 for key to

symbols and Table 3 for further explanation)

Species

Ambystoma maculatwn

By la crucifer

Rana alamitans

Rana sylvatiaa

Bufo americanus

Size

3=12

13-18

19-24

^25

25-30

31-36

37-44

25-30

31-36

37-44

25-30

37-44

25-30

31-36

Surface

21/15

11/11

16/20

11/13

740/736

48/55

94/90

Midwater

8/7

2/5

10/9

8/6

502/470

31/35

34/58

38/35

17/20

12/12

20/22

10/7

368/371

61/59

Bottom

6/12

12/9

19/16

10/10

324/358

38/27

64/44

39/41

26/23

14/14

30/28

6/9

36/32

3/5

10779" (ns)

5.43 (ns)

5.82 (ns)

19.20**

30.46**

""1720" (ns)

"XoT (ns)

~O9~ (ns)

1974 sample was collected in a single, surface sweep

which passed through hatching egg strings. The

1975 data doubtless demonstrate the larval microhabitat preferences in contrast to the 1974 information, which may indicate nothing more than the

egg deposition sites. Hyla crucifer, while demonstrating a preference for the surface sweep microhabitat, showed a shift toward statistically more

individuals using the midwater and bottom microhabitats in 1975 than in 1974. This may be due to

differences in total population densities for the two

years.

The ontogenetic change in microhabitat preferences for H. crucifer in 1974 and 1975 is interesting. The data for the two years combined suggest

that smaller larvae tend to be in shallow surface

areas and as they grow, they move into deeper, more

open parts of the pond.

MICROHABITAT METRICS.—Commonly used measures of niche breadth and niche overlap can encompass the factors of temporal and spatial partitioning

by the larvae when the measures are based on individual sweeps (see Heyer, 1974, for a previous

analysis and justification).

Microhabitat Breadth: The formula used to determine microhabitat breadth is:

B, -^f'zlpij';

iVt i

where 57 is the microhabitat breadth of species j ,

Ns is the number of sweeps in which individuals

of species ; were collected, Nt is the total number of

sweeps, and pj ; is the proportion of occurrences of

species ; in sweep i (modified from Levins, 1968).

Microhabitat breadths for 1974 and 1975 are presented in Table 5. When the species are ranked

within years by broadest microhabitat width to narrowest, only one species shows the same relative

position. Hyla crucifer had the broadest microhabitat width both years. Relative to H. crucifer, H.

chrysoscelis had narrower microhabitat widths both

years but stood in varying relationship to the other

species. The other congeneric pairs, involving Ambystoma and Rana show reversals of relative rank

of microhabitat widths for 1974 and for 1975.

There are no straightforward, powerful, statistical

tests to apply to measures based on proportions to

determine statistical differences from one year to the
NUMBER 242 11

TABLE 5.—Microhabitat breadths (largest/smallest = largest value divided by

smallest to determine magnitude of difference from one year to next;

see text)

Species 1974 1975 largest/smallest

Ambystoma maculatum,

Arriby8toma opacum....

Hy la erucifer

By la ehrysoaoelis...

Rana olamitans

Rana sylvatica

Bufo amerieanus

Acris arepitans

0.0179

1.3518

6.1109

1.1307

0.3293

5.4228

0.0156

0

0.9711

0.0194

13.5549

0.0181

2.1750

0.2035

0.5850

0.0003

54.2

69.7

2.2

62.5

6.6

26.6

37.5

next. For this reason, the larger value is simply divided by the smaller value to determine the order

of magnitude of difference from one year to the

next. Biologically, there was but a single species

that had the same microhabitat breadth for both

years: Acris crepitans essentially was absent both

years. I interpret the differences between microhabitat widths measured in 1974 and in 1975 to be

biologically significant for all of the other species.

Microhabitat Overlap: The formula used to determine microhabitat overlap (Horn, 1966) is:

ajk = 2Y,pijpik

where jk = overlap of species / and k, and pif is

the proportion of occurrence of species ; in sweep i.

Values range from 0 (no overlap) to 1 (complete

overlap). Larval salamanders and larval anurans

are in different trophic levels. Tadpoles are primarily herbivorous, while salamander larvae are

carnivorous and sometimes eat tadpoles. Co-occurrences in sweeps (which the overlap measure represents in a single value) thus give information on

potential predator-prey and competition relationships between salamander larvae and tadpoles. High

overlap values are interpreted as the potential (but

not necessarily the existence) for predation or competition to occur. Low overlap values are interpreted as indicating that predation or competition

is not important.

Overlap values for all comparisons involving

salamanders are presented in Table 6. The very

low overlap value for 1975 between the two species

of Ambystoma and no overlap in 1974 confirms

previous conclusions (Worthington, 1968; 1969) that

larval Ambystoma maculatum and A. opacum essentially do not co-occur in the same ponds.

In examining the sweep data for possible

predator-prey relationships between the salamanders

and tadpoles, the data for all salamanders (in addition to being compared on a species-species overlap with tadpoles) were combined, on the assumption that both species would be potential tadpole

predators and it would make no difference to tadpole species x whether it was preyed upon by either

salamander species a or b. It is clear from the results (Table 6) that Ambystoma opacum potentially

is not an effective tadpole predator in the study

pond. Almost all potential salamander predation

is accounted for by Ambystoma maculatum. Two

additional generalizations may be drawn from the

overlap values. First, potential salamander predation, on all species of tadpoles, was much greater

in 1975 than in 1974. The differences involved suggest that salamander predation on tadpoles probably did not have much of an effect in 1974, while

salamander predation on tadpoles in 1975 could

have been a strong natural selective force. Second,

predictions can be made about which species of

tadpoles should most likely be affected by salamander predation. In 1974, only Rana sylvatica should

have had any noticeable predation by salamander

larvae. In 1975, Rana clamitans and Rana sylvatica

should have been preyed on extensively by

salamander larvae. Such predictions are best

treated cautiously until more is known about feeding habits in larval salamanders. For example, the

predator-prey size relationships are unknown, but

the Rana tadpoles become quite large and may

escape predation after reaching a certain size.
12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 6.—Microhabitat overlaps for comparisons involving salamander larvae (see Table 5

for further explanation)

Pair comparison

All salamanders - Hyla arucifer

All salamanders - Hyla chrysoscelis

All salamanders - Rana alamitans

All salamanders - Rana sylvatioa

All salamanders - Bufo ameriaanus

All salamanders - Aoria crepitans

Amby8toma maaulatum - Ambystoma opaaum

Ambystoma maculatum - Hyla arucifer

Ambystoma maaulatum - Hyla ahrysoscelis....

Ambystoma maaulatum - Rana aylvatioa

Amby8toma maaulatum - Acris arepitans

Ambystoma opaaum - Hyla aruaifer

Ambystoma opaaum - Hyla dhrysosaelis

Ambystoma opaaum - Rana sylvatiaa

Ambystoma opaaum - Aerie orepitans

1974

0.0583

0.0603

0.0385

0.1111

0.0004

0

0

0.0625

0.0976

0.0612

0.1163

0

0

0.0085

0

0

0.0224

0.0007

0

1975

0.1879

0.1106

0.2920

0.2574

0.1565

0.0168

0.0126

0.1938

0.1149

0.2683

0.2694

0.1619

0.0168

0.0003

0

0.0196

0.0232

0.0012

0

largest/smallest

3.2

1.8

7.6

2.3

391.2

"

-

3.1

1.2

4.4

2.3

-

-

28.3

-

-

1.0

1.7

~

Walters (1975) demonstrated that Ambystoma larvae have definite prey preferences among tadpoles

when offered a choice; however, she did not include aquatic insects in her experiments. Larval

salamanders may prefer insects over tadpoles, even

to the extent that tadpoles are not eaten, although

available. Anderson and Graham (1967) demonstrated that vertical migration and stratification

occur in larval Ambystoma. They found that during

the evening the larval salamanders leave the sites

they have occupied during the day and begin actively feeding. If most feeding is done at dusk, then

the overlap values reported here have little or no

bearing on the predator-prey relationships of larval

salamanders and tadpoles, since all sweeps were

taken during the day. Walters (1975) reported diurnal foraging in Ambystoma larvae, but had no

data to indicate whether most of the foraging takes

place during the day or at dusk.

All sweeps were taken when tadpoles were active,

so the overlap values represent potential competition when tadpole species-tadpole species comparisons are made. All of the tadpoles in this study

have the same gross feeding morphology. Thus,

competition may be potentially occurring among all

individuals of all species. For this reason, overlaps

have been calculated for each species compared

with all other tadpoles in addition to speciesspecies overlap comparisons (Table 7). There is no

experimental evidence with which to relate overlap

values to potential competition among and within

species. Does a value of 0.1062 mean that competition is strong enough so that selection will operate

to reduce the overlap? For purposes of this paper,

the following common-sense hypothesis will be used

to evaluate the overlap values. The range of values

from about 0.1 to 0.25 represents the degree of potential competition that the process of natural selection would operate to reduce the microhabitat

overlap. Values below 0.1 indicate potential competition is not significant, and values above 0.25

indicate potential competition is significant.

Each of three species had roughly the same

amount of overlap with all other tadpoles in 1975

that it had in 1974: Hyla chrysoscelis, Rana sylvatica, and Acris crepitans. Of these, potential competition was a marginal factor only for Rana

sylvatica, and that for only 1974. For each of the

other three species, the degree of overlap with all

other tadpole species was different in 1975 from
NUMBER 242 IS

TABLE 7.—Microhabitat overlaps for comparisons involving only tadpoles (see Table 5 for

further explanation)

Pair comparison 1974 1975 largest/smallest

Hyla crucifer - All other tadpoles....

Hyla chry808celi8 - All other tadpoles

Eana alcanitans - All other tadpoles...

Rana aylvatica - All other tadpoles...

Bufo americanus - All other tadpoles..

Aaris crepitans - All other tadpoles..

Hyla aruaifer -Hyla chrysoscelie

Hyla crucifer - Rana clamitans

Hyla aruaifer - Rana sylvatica

Hyla aruaifer - Bufo americanus

Hyla aruaifer r Aarie orepitans

Hyla chry8O8celi8 - Rana clamitans....

Hyla chrysoscelis - Rana eylvatiaa....

Hyla chrysosaelis - Bufo americanus...

Hyla chrysoecelie - Aaris arepitane...

Rana clamitans - Rana sylvatica

Rana clamitans - Bufo americanus-.

Rana clamitans - Acris arepitans

Rana sylvatiaa - Bufo americanus

Rana sylvatica - Aaris arepitans

Bufo americanus - Aaris arepitane

0.1531

0.0564

0.0395

0.1062

0.0096

0

0.0305

0.0204

0.1385

0.0146

0

0

0.0336

0

0

0.0189

0

0

0

0

0

0.3225

0.0438

0.1519

0.0679

0.0967

0.0076

0.0704

0.1665

0.1137

0.1215

0.0074

0.0980

0.0436

0.0215

0.0585

0.2231

0.1060

0.0189

0.1699

0.0232

0

2.1

1.3

3.8

1.6

10.1

-

2.3

8.2

1.2

8.3

-

-

1.3

-

-

11.8

-

-

-

-

what it had been in 1974. For Hyla crucifer, potential competition was important both years but

more significant in 1975. For Rana clamitans, potential competition was a factor only in 1975, as it

also was (marginally) for Bufo americanus. At the

community level it would appear that larvae of

Hyla crucifer are the only ones that would experience potential competition from the rest of the

tadpole community on a year to year basis.

Although feeding morphologies of all tadpoles

under consideration are similar, interspecific competition might be most important between certain

species pairs. Each of the following species pairs

showed the same overlap in 1974 that they did in

1975 (Table 7): Hyla crucifer-Rana sylvatica, Hyla

crucifer-Acris erepitans, Hyla chrysoscelis—Rana

sylvatica, and Bufo americanus-Acris erepitans.

Among these, only the Hyla crucifer-Rana sylvatica

pair shows an overlap value that indicates potential competition as a factor. All of the other species

pair overlap values are very different for 1974 as

compared to those for 1975. For the following pairs

potential competition is not a factor in either year:

Hyla crucifer-Hyla chrysoscelis, Hyla chrysoscelisBufo americanus, Hyla chrysoscelis-Acris erepitans,

Rana clamitans-Acris erepitans, and Rana sylvaticaAcris erepitans. For the following pairs, potential

competition is significant for only one of the two

years: Hyla crucifer-Rana clamitans, Hyla cruciferBufo americanus, Hyla chrysoscelis-Rana clamitans,

Rana clamitans-Rana sylvatica, Rana clamitansBufo americanus, Rana sylvatica-Bufo americanus.

Thus, based on the two consecutive years of this

study, 8/15 of the total species-species overlaps

probably do not have competitive interactions,

while in only 1/15 of the species-species overlaps

is competition potentially a year to year factor.

DISCUSSION.—The aquatic larval community appears to have distinct temporal patterns each year.

Some of the species show the same temporal patterns each year and others show different temporal

patterns each year.

Each species of larvae has essentially the same

microhabitat preference for the two years.

The analyzed microhabit breadths reflect temporal and spatial partitioning with population densities, thereby illustrating the comparative habitat

utilization each year. The overall picture is that
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the total habitat utilization was very different in

each of the two years studied and would likely be

different every year.

The microhabitat overlap analyses allow insights

into the biological interactions occurring in the

pond. Overlaps of salamander larvae and tadpoles

give indications of predator-prey relationships,

while overlaps of species in the same trophic level

give insights into potential competition.

Salamander larvae can prey heavily on tadpoles

in nature (Anderson, 1968). Even if most prey cap

ture is done at twilight in microhabitats other than

those occupied by the salamanders in daylight, the

overlap data presented herein exemplify the kinds

of relationships that occur between predators and

tadpole prey. The overlap data indicate that the

tadpole populations in 1974 were in very different

predator environments from those in 1975.

The lack of competition between Ambystoma

maculatum and A. opacum in Maryland due to

temporal partitioning has been documented and discussed previously (Worthington, 1968; 1969). The

role of competition among tadpoles has not been as

well documented. Wilbur and Collins (1973) and

Brockelman (1969) demonstrated that intraspecific

competition among tadpoles may occur at high experimental densities. Brockelman (1969) found no

evidence for intraspecific competition in natural

pond habitats. De Benedictis (1974) was unable to

demonstrate conclusively that interspecific competition occurs in field simulated experiments. An analysis of the available literature suggests that while

competition is a theoretical possibility among tadpoles, the densities found in nature fall well below

the densities required to demonstrate competition

experimentally. For example, comparative figures

extrapolated from Wilbur and Collins (1973) and

Turnipseed and Altig (1975) indicate a density of 1

tadpole per 192 cm3 of water as being necessary for

tadpole competition to occur (based on the results

of 300 larvae density runs in Wilbur and Collin's

experimental pens), while the greatest recorded

tadpole population density found in nature was

identified in a pond edge in Mississippi as 1 tadpole

per 285 cm3 water (conservative estimate, using 5

cm water depth to Turnipseed and Altigs' density/

area data).

In order to demonstrate the occurrence of actual

competition among tadpoles, it would be necessary

to determine a limiting factor in the environment.

Tadpoles are not territorial; many species freely

form association groups and/or schools (Wassersug,

1973). Thus, it appears unlikely that space would

be a limiting factor. The pond has abundant submerged vegetation and a deep organic silt bottom;

all indications are that it is a productive pond and

that food would not be limiting. The tadpole

species-species overlap values indicate potential competition, not the existence of competition. Most of the overlap values are low, indicating

that there is little potential competition within

most of the tadpole community. The highest consistent values involve Hyla crucifer (Table 7). Hyla

crucifer has a small tadpole, and although the numbers of individuals may be high, the biomass may

not be appreciable, especially compared to Rana

clamitans and R. sylvatica. The overall results of

this study indicate that if interspecific competition

is occurring, it most likely is occurring between

Hyla crucifer and Rana sylvatica. Until experiments

are performed to determine the density levels required to demonstrate competition between these

two species, the most reasonable assumption is that

competition is not important for these populations

at the study pond. The only other overlap value

really indicative of potential competition is that of

Rana clamitans-Rana sylvatica for 1975 (Table 7).

While individuals of both species were occupying

the same microhabitats, the total number of individuals collected were not great: 148 R. clamitans

and 79 R. sylvatica. These numbers came from a

reasonable volume of habitat sampled. I conclude

that the total densities involved are of such a magnitude that competition was not a factor for Rana

clamitans and Rana sylvatica in 1975. In the absence of any demonstrated limiting factor, the overlap analysis provides no evidence that competition

among tadpoles was occurring in the pond in either

year. Since the search for evidence of competition

produced such generally negative results, it appears

that competition was not likely limiting population

growth in any of the tadpole species in the study

pond. What the overlap values do demonstrate is

that the temporal and spatial relationships within

the biological larval community were quite different in 1974 from what they were in 1975.

The conclusions drawn with respect to habitat

partitioning for the study pond are as follows. An-
NUMBER 242 15

nual differences in larval temporal habitat partitioning combined with different annual population

densities result in: (1) differential habitat utilization

each year by the larvae, and (2) different biological

interactions involving predator-prey and species

associations each year. Generally low microhabitat

overlap values for tadpole species indicate that competition was not regulating the tadpole community,

but that larval spatial and temporal distributions

effectively partitioned the habitats. Overall, each

larval species was in a different environment with

respect to natural selection in 1974 from what it

experienced in 1975.

Barro Colorado Island

The stream habitats at Barro Colorado Island

(BCI) consist of semi-isolated or completely isolated stream bed pools. Sampling was done once in

the dry season (11 February to 5 March 1975) and

once in the wet season (1-20 July 1975) to determine gross temporal patterns of tadpole occurrence.

Sampling procedures were designed to determine

how fish (predators) and tadpoles spatially occupy

the habitat.

METHODS AND MATERIALS.—Each stream bed pool

was measured by length, breadth, and greatest

depth. The measured pool was then sampled by a

large or small dipnet appropriate to the size of

the pond. Presence or absence of fish was noted.

Fish were not collected, so the assumption that the

fish were all predators probably overestimates the

real situation. In the dry season, the presence or

absence of tadpoles by species was noted. In a few

samples the individuals were preserved for confirmation of identifications. In the wet season, all tadpoles collected were preserved. Efforts were made

to collect all individuals in the small ponds. In the

laboratory, all specimens were identified, counted,

and staged (Gosner, 1960).

RESULTS.—Few larvae were collected in any

single pond; for this reason, only the presence or

absence of larvae was noted in the dry season. The

wet season sampling, in which quantitative counts

were taken, probably reflects the same quantitative

relationships as the dry season sampling. During

the wet season the greatest number of tadpoles collected in a pond was 18, the average number of

tadpoles in a pond that had tadpoles was 3.6.

Ninety-seven ponds were sampled in the dry season, 80 were sampled in the wet season (Table 8).

The ponds were larger in the wet season (x

 2 =

21.17, P<.01) as might be expected. Fish occurred in

a total of 63 ponds, tadpoles occurred in a total of

47 ponds. Fish and tadpoles co-occurred in only 1

pond.

TABLE 8.—Size classes of ponds (volume in m*) sampled by

seasons at Barro Colorado Island

Pond size

1 - 9....

0.1 - 0.9..

0.01 - 0.09.

0.001 - 0.009

Dry season Wet season

2

22

52

21

6

43

24

7

Distribution of fish among pond size classes is

presented in Table 9. Fish occurred in the larger

ponds. This aspect of habitat preference was evident only in the dry season when there were more

small ponds available to choose from. During the

wet season, when ponds were larger, the fish distribution among size classes of ponds was random.

The distribution of all tadpoles among pond size

classes is presented in Table 10. Tadpoles occurred

in a random sample of the available pond sizes in

both the dry and wet seasons.

In the dry season, tadpoles of Bufo typhonius,

Colostethus nubicola, and Smilisca sila were collected from the stream bed ponds. Bufo typhonius

were collected in only one pond where they were

completing metamorphosis. The sampling period

included the very end of the reproductive season

of Bufo typhotiius. The Colostethus nubicola and

Smilisca sila larvae were at all stages of develop

ment since the sampling period was during the

breeding season of these species. Although sample

sizes are not large enough for statistical analysis,

the raw data clearly suggests that Colostethus

nubicola occurred randomly in the available ponds

during the dry season when small ponds were more

abundant (Table 11). The same applies to Smilisca

sila larvae (Table 12). Colostethus nubicola tadpoles were found in 6 ponds where Smilisca sila

tadpoles did not occur, S. sila tadpoles occurred in

7 ponds were C. nubicola did not occur, and C.

nubicola and 5. sila co-occurred in 8 ponds. The
16 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 9.—Fish occurrence among size classes of ponds (volume in m1) sampled by seasons at

Barro Colorado Island (for x5 determination, sample sizes are grouped so that expected values

> 5; expected values are determined by multiplying percent occurrence of all fish in all ponds

by number of ponds sampled in each size category; see Table 1 for key to symbols)

Pond size

Dry season Wet season Total

Observed Expected Observed Expected Observed Expected

1 - 9

0.1 - 0.9..,

0.01 - 0.09.

0.001 - 0.009,

1

17

28

2

1

11

26

in

= 9.55** X

2

 =

4

1

2.00 (ns)

3

24

34

2

2

23

27

10

8.37**

TABLE 10.—Tadpole occurrence among size classes of ponds sampled by seasons at Barro

Colorado Island (for x2 determination, sample sizes are grouped so that the expected values

> 5; expected values are determined by multiplying percent occurrence of all tadpoles in all

ponds by number of ponds sampled in each size category)

1

0

n

n

Pond

1

01 -

001 -

size

9

0.9

0.09

0.009

Dry

Observed

1

2

10

8

x

2

season

Expected

0

5

11

5

= 2.69 (ns)

Wet

Observed

1

11

12

2

x

2

season

Expected

2

14

8

2

= 2.60 (ns)

Total

Observed

2

13

22

10

x

2 -

Expected

2

17

20

7

2.33 (ns)

TABLE 11.—Occurrence of Colostethus nubicola tadpoles among size classes of ponds sampled

by seasons at Barro Colorado Island (for x2 determination, sample sizes are grouped so that

the expected values > 5; expected values are determined by multiplying percent of occurrence of all C. nubicola larvae in all ponds by number of ponds sampled in each size category)

Pond size

Dryi

Observed

0

2

8

4

season

Expected

0

3

8

3

Wet

Observed

0

3

8

2

season

Expected

1

7

4

1

Total

Observed

0

5

16

6

Expected

1

10

12

4

1 - 9

0.1 - 0.9..

0.01 - 0.09.

0.001 - 0.009

X

2

8.12** X

2 5.52*

two species were randomly associated with each

other (x2 = .28,P>.05).

Colostethus nubicola, Centrolenella fleischmanni,

and Physalaemus pustulosus larvae were collected

in the stream ponds in the wet season. All stages of

larvae were present indicating the sampling period was within the breeding season of all three

species. Physalaemus pustulosus larvae were collected in 6 ponds, in 1 pond it was the only species

collected, in 1 pond Physalaemus pustulosus cooccurred with Colostethus nubicola, in 3 ponds

Physalaemus pustulosus co-occurred with Centrolenella fleischmanni, and in 1 pond Physalaemus

pustulosus co-occurred with Centrolenella fleisch-
NUMBER 242 17

TABLE 12.—Occurrence of Smilisca sila larvae

among size classes of ponds sampled in one season at Barro Colorado Island (expected values

are determined by multiplying percent occurrence of all S. sila larvae in all ponds by number of ponds sampled in each size category)

Pond size

1 - 9

0.1 - 0.9

0.01 - 0.09

0.001 - 0.009

Dry season

Observed Expected

1 0

2 3

7 8

5 3

manni and Colostethus nubicola. In the wet season,

Colostethus nubicola demonstrated a greater occurrence in smaller ponds than expected (Table 11).

This preference was evident only in the wet season,

when there were fewer small ponds than in the dry

season. Over all, Colostethus nubicola tadpoles were

associated with smaller ponds (Table 11). Centrolenella fleischmanni tadpoles were distributed

randomly among the pond sizes (Table 13). Colostethus nubicola tadpoles were found in 10 ponds

where Centrolenella fleischmanni tadpoles were

not found, Centrolenella fleischmanni tadpoles were

found in 12 ponds where Colostethus nubicola tadpoles were not found, and both Centrolenella

fleischmanni and Colostethus nubicola tadpoles

were found in 3 ponds. The two species tend to

mutually exclude each other, but the statistical

evidence for this is not strong (x2 = 5.36, . 1 >

P>.05):

TABLE 13.—Occurrence of Centrolenella fleischmanni larvae among size classes of ponds sampled in one season at Barro Colorado Island

(for x1 determination, sample sizes are grouped

so that the expected values > 5; expected values

determined by multiplying percent occurrence

of all C. fleischmanni larvae in all ponds by number of ponds sampled in each size category)

Pond

1

0.1

0.01

0.001

size

- 9.

- 0.

- 0.

- 0.

9

09

009

Wet

Observed

1

9

5

0

season

Expected

1

8

4

1

- .11 (ns)

HABITAT PARTITIONING.—In terms of habitat partitioning, the habitat is considered as the entire collection of stream bed ponds.

Temporal Partitioning: The habitat is clearly partitioned temporally over a seasonal cycle. Only one

species, Colostethus nubicola, was present as tadpoles in the two seasonal sampling periods.

Spatial Partitioning: Space partitioning is evident

in the total pond system. Of all the ponds with tadpoles present, 68% had but a single species. Where

more than one species occurred in a pond, I found

no evidence for microhabitat partitioning within

the pond. All species were found in the leaf litter

that had accumulated in the pond bottoms.

The stream bed tadpole community was effectively partitioning the available habitat on the

basis of time and space.

DISCUSSION.—While the effective habitat partitioning evidenced in the BCI stream tadpoles seems

to be the product of selective forces acting previously upon the species making up the community,

the possible roles of predation and competition

invite speculation.

Fish predation in the tropics recently has been

hypothesized to be a major organizing factor in

tadpole communities (Heyer, McDiarmid, and

Weigmann, 1975). Two observations, in addition to

the data already presented, are pertinent to the

question of possible fish predation as a factor in

the BCI study. The single pond sampled in which

tadpoles and fish co-occurred had a small surface

area, but was a deep crevice pond, in the bottom of

which had accumulated a deep layer of leaf litter.

The single Centrolenella fleischmanni larva collected in this pond was in the deep leaf litter. One

of the streams sampled had a weir type dam constructed on it with a pond behind it. Data from this

large pond (7 x 6 x 1 m) have not been included

herein previously, since the pond is not part of the

natural stream bed habitat. In the dry season, fish

were in the pond and no tadpoles were collected

although Physalaemus foam nests were often observed on the periphery of the pond. In early

March, the pond was completely drained, and the

accumulated silt shoveled out. In the following

July, in numerous observations, no fish were seen

but a dense tadpole community was present consisting of Agalychnis callidryas and Physalaemus

pustulosus. The data presented herein are consist-
18 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ent with the following conclusions. Fish are effective predators on tadpoles, completely eliminating

them from certain pond habitats. The tadpoles

have two patterns of occurrence in response to the

fish: (1) Colostethus nubicola demonstrates a habitat preference, using ponds smaller than those

usually occupied by fish; (2) the remaining species

apparently exploit the patchy occurrence of fish in

the total pond habitat system. That is, tadpoles are

deposited in enough ponds so that some of such

ponds will be fish free. For such an accommodation

to be effective, either a single egg clutch would

have to be partitioned among several ponds or the

individuals would have to have multiple clutches

during their reproductive life. Relative to the

anuran species identified in the BCI study, the only

clutch deposition patterns available are for Centrolenella fleischmanni, in which the male has been

shown to fertilize several clutches (data for females

unknown, McDiarmid, 1975) and Physalaemus

pustulosus, in which the female can produce up to

four clutches a year with as little as six weeks between clutches (Davidson and Hough, 1969).

The very low numbers of tadpoles collected in

the individual ponds strongly suggests that competition is not operating. The existence of many

ponds with neither fish nor tadpoles, which appeared similiar to the ponds containing tadpoles

suggests that there was no competition for space

as a limiting factor by itself. It is very difficult, however, to rule out competition (at least intraspecific)

for a combination of space and food. In contrast to

the many temperate zone temporary ponds that are

highly productive, many tropical streams have extremely low productivity (Fittkau, et. al., 1975). No

data are available for the productivity of the

streams on BCI, but the productivity is probably

low, judging by the clearness of the water. Productivity may be higher during the dry season, when

tapir feces remain in the ponds rather than being

continually flushed from them. Interspecific competition for food resources is not a likely factor, since

the species which most often co-occur with each

other have very different feeding morphologies.

Colostethus nubicola larvae have large funnel

mouths; the larvae often feed on the surface film.

The species that co-occur with Colostethus in the

same ponds, Smilisca sila in the dry season and

Centrolenella fleischmanni in the wet season, are

substrate feeders with scraping and chewing mouthparts. Each pond, however, may well have limited

resources. The tadpoles are certainly capable of

moving from pond to pond during rains when the

ponds are interconnected. The low numbers of

individuals in each pond may represent movement

of individuals reflecting competition. The total distribution pattern of larvae would then be a combination of the pond site where eggs were deposited

and a radiation to adjoining ponds.

The data and analysis from the BCI study allow

the following general conclusions to be drawn. The

stream bed pond habitat system is effectively partitioned by the tadpole community on the basis of

space and time. Predation is an organizing factor in

the composition of the tadpole community, interspecific competition apparently is not.

Other Studies of Larval Habitat Partitioning

Larval salamander population dynamics have

been the focus of study by several workers, most

notably Anderson and his coworkers (1967, 1968,

1971), Shoop (1974), Wilbur (1972), Wilbur and

Collins (1973), and Worthington (1968, 1969). Most

of these studies have dealt with predation, competition, survival, and temporal organization of larval

salamander communities. Wilbur (1972), combined

experimental manipulations and field observations

to demonstrate that predation and competition

were important factors in the functioning and organization of the larval salamander communities of

Michigan.

I am aware of only four studies in which quantitative data were taken to deal with questions concerning habitat partitioning by anuran larvae.

Dixon and Heyer (1968) followed a pond in western

Mexico for two weeks. Since all microhabitats sampled were combined, no information was available

on possible spatial partitioning within the pond.

The data strongly indicated temporal partitioning

of the habitat by the larvae.

I previously reported on habitat partitioning of

the temporary pond environment by the tadpole

community for a seasonal tropical site in northeastern Thailand (1973, 1974). Quantitative sweeps

were taken from a series of ponds to determine the

temporal partitioning patterns and a series of microhabitat sweeps were taken from a single pond to
NUMBER 242 19

determine spatial partitioning within a pond. Gut

contents were analyzed to determine any obvious

partitioning patterns of the available food resources.

The study concluded that the available pond habitats were partitioned by the tadpole community

on the basis of time and space, not food.

Calef (1973a) reported on the population dynamics of a single anuran species system in a lake

in British Columbia. The study is of interest as

it is the only reported study of tadpole population

dynamics that covered two years (consecutive) and

the study represents an extreme situation in terms

of anuran diversity. Calef (1973a) found similar results in both years: almost identical numbers of egg

masses were laid in both years and survivorship was

essentially the same both years. Food was not a limiting resource; the tadpoles grew at the maximum

rate set by the aquatic habitat temperature. The

tadpole populations were regulated by predation

(primarily salamander).

In an unpublished study, Wiest (1974), reported

on a series of ponds in Brazos County, Texas. Wiest

quantitatively sampled the larvae of a series of

ponds and reported the individual results from

four of them. He did not sample for microhabitat

differences within ponds. Each of the four ponds

had different combinations of species of larvae.

Within each pond a temporal succession of species

was demonstrated.

The results of all studies that have examined the

entire anuran larval communities are similar and

consistent with the following conclusions. Habitats

are partitioned by space and time, not food. Predation, not competition, has a strong role in controlling and organizing the tadpole communities.

Tadpole Community Organization

A tadpole community is defined as an assemblage

of anuran larval species at a single site. Two extreme levels of organization are possible: (1) a community with no interspecific interactions between

or among any of the component populations, or (2)

a community with either symbiotic relationships

that tie the community together, or competition

that partitions the community into component

parts. With this spectrum of tadpole communities

in mind, I have examined the Chesapeake and BCI

systems to see what type of community organization

they most closely resemble.

The three predominant species collected at BCI

are all stream breeding frogs: Centrolenella fleischmanni, Colostethus nubicola, and Smilisca sila. The

evolutionary history of each of the three species is

distinct. All members of the genus Centrolenella

for which larvae are known have rheocolous larvae

with long, thin tails, bodies flattened dorsoventrally,

and a strong body and tail musculature capable of

continued, powerful flipping movements. The morphology is typical of larvae adapted to life in running water. Mouthparts consist of a scraping and

chewing apparatus. Breeding activities for all species that have been studied coincide with the onset

of the rainy season in those areas with seasonal rainfall patterns. Centrolenella fleischmanni occurs from

southern Mexico to Panama, westward to Ecuador,

and eastward to Surinam (Starrett and Savage,

1973). Colostethus nubicola larvae resemble Centrolenella larvae in body and tail shape, strong musculature, and flipping movements when out of

water. Colostethus nubicola larvae differ from

Centrolenella larvae in that the mouthparts form a

pronounced funnel, adapted for feeding on the

surface film. Colostethus nubicola extends from

Costa Rica through Panama into western Colombia

(Savage, 1968). The tadpole of Smilisca sila has a

typical pond morphology in contrast to the stream

morphologies of the other two species. The body

and tail are weakly muscled, the body is globose

and the tail relatively short but broad, with high

fins. The primitive reproductive pattern for the

genus Smilisca involves pond larvae (Duellman and

Trueb, 1966). Smilisca sila has become adapted to

breeding in quiet stream bed pools. Such pools

predictably exist only during the dry season, which

is the breeding season for Smilisca sila. The mouthpart morphology is the typical scraping and chewing

kind. They are known only from Costa Rica and

Panama (Duellman, 1970).

In each of the seasons (dry and wet) there are two

co-occurring species in the community composed of

the three predominant species. In the dry season,

the surface film feeding C. nubicola larvae coexist

with the substrate processing S. sila larvae. In the

wet season, the surface film feeding C. nubicola

larvae coexist with the substrate processing C.

fleischmanni larvae. The community organization

of these three species can be explained in two very

different ways. First, it may be that competition for
20

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

resources was the source of natural selective forces

which led to the morphological divergence of

mouthparts of Colostethus and the temporal partitioning of the substrate feeding Centrolenella and

Smilisca larvae. The evolutionary result would thus

be a competition free, compartmentalized stream

bed larval community. The second explanation is

that the three species occur as larvae in a community in the way they do because there happen to

occur in the same area three species of frogs that

have stream breeding adaptations. The organization

of the community is due to the way the components

coexist, no further evolutionary adjustments being

necessary. I favor the last explanation for the following reasons. (1) The associations of the species as

larvae appear to be due to similar choices of pond

habitats by the three species. If the associations

were biologically mediated (e.g., competition) one

would not expect the random associations found in

this study. (2) The geographic distributions of the

species argue against long term, species wide interspecific interactions. Divergence in morphology or

temporal use of the habitat would almost have to

be a one sided divergence involving only Smilisca

sila, as it is the only species which throughout its

entire range would consistently encounter the other

two species. (3) The partitioning of the habitat by

the stream tadpole community can be better explained in terms of other features of the life histories of the species involved. The reason that C.

nubicola larvae have funnel mouthpart stream

adapted larvae is likely that the species evolved in

an environment characterized by streams lacking

standing algal growths or deteritus and the food

resources were concentrated in the surface film. The

reason that Smilisca sila breeds during the dry season is likely that the ancestral stock, having a typical pond life history, became isolated in an area

where the only quiet ponds in the environment

were in the stream beds during the dry season. The

reason that Centrolenella fleischmanni breeds in the

rainy season is likely because the exposed egg

clutches that are placed on undersides of leaves

over streams are prone to desiccation during the dry

season and rains frequently are needed to insure

that the hatchlings reach an appropriate stream

habitat.

The same kinds of arguments can be made for

the Chesapeake tadpole community. Table 14 presents the major species wide characteristics of breeding habitats and seasons for those species comprising

the tadpole community at the Chesapeake study site

(data from Conant, 1975; R. I. Crombie and G. R.

Zug, pers. comms.). Most of the species have unique

combinations of breeding seasons and types of

ponds primarily used for breeding. These data suggest that each species has a unique reproductive

pattern reflecting the conditions in which that

species occurred at the time of its genetic isolation.

If interspecific competition had been the major

evolutionary force in the habitat partitioning between congeners, their segregation should remain

apparent today, although they would no longer be

in competition. The essentially complete partitioning of larvae of Hyla crucifer from Hyla chrysoscelis and Rana clamitans from Rana sylvatica

could be interpreted as competition having occurred between congeneric pairs historically, with

natural selection operating to reduce larval interspecific competition. The present almost complete

habitat partitioning within the species pairs would

be the result of natural selection operating to reduce competition. The alternate explanation of

larval habitat partitioning within congeneric

TABLE 14.—Major characteristics of breeding habitats and seasons for species comprising the

tadpole community at the Chesapeake site (C = common, r = rare)

Species

Aavie crepitans....

Bufo americanua....

Hyla aruaifer

By la chry808celie..

Rana clamitans

Rana ayIvatica

Breeding season Types of breeding ponds

Early Late Temporary Permanent Sluggish

wooded open wooded open streams

C r C C

C C C r r

C C C r r

C r r C r

C r C C

C C r
NUMBER 242 21

pairs seems more plausable. The ancestral stock

of Hyla crucifer likely was isolated in and became

adapted to an environment in which the only available breeding ponds were temporary ones which

appeared in the spring. The ancestral stock

of Hyla chrysoscelis was likely isolated in and

became adapted to an environment in which the

only available breeding ponds were permanent ones

and in addition, the breeding season was associated

with late spring and summer warm rains. Similarly,

the ancestral stock of Rana sylvatica was likely isolated in and became adapted to an environment

in which the only available breeding ponds were

temporary wooded ponds appearing in the spring.

The ancestral stock of Rana clamitans was likely

isolated and became adapted to an environment in

which the only breeding sites were streams and

open, permanent ponds and also the breeding season was associated with late spring and summer

warm rains. Since the early adaptive histories of the

several species, the geographic ranges have expanded and contracted according to major climatological changes so that the species ranges now

broadly overlap. Each pond in the species range

will have (more or less) some of the major characteristics associated with the primary adaptive

pond type of each species. Thus, certain wooded

permanent ponds will contain the essential features of the temporary wooded ponds to which

Rana sylvatica is primarily adapted. When such

ponds are encountered, they will be utilized by

R. sylvatica in the spring, while the same pond may

also be used by Rana clamitans in the late spring

and early summer. The habitat partitioning of the

larvae of these two species is thus most likely not a

result of biological interactions at the larval stages,

but rather a passive reflection of different adaptive

reproductive patterns of the species involved. A

similar observation may be made for the entire

community of frogs utilizing the same ponds. If

biological interactions at the larval stage were

important in the control and organization of the

tadpole community, the interactions would have to

be reasonably predictable for natural selection to

be effective. The Chesapeake community organization argues against this. Each component species

present as larvae was in an essentially different selective environment in each of the two years

studied.

Although the role of competition among tadpoles

has implicitly (e.g., Wiest, 1974) or explicitly

(Wilbur and Collins, 1973) been accorded major

importance in the control and organization of tadpole communities, this present study concludes

that interspecific competition among tadpoles is

not important in the control or organization of tadpole communities. Further circumstantial evidence

arguing against significant tadpole competition in

nature is relevant to this conclusion. If interspecific

tadpole competition had occurred historically,

selection should have operated to displace the competing species either with respect to space, time, or

feeding morphologies. If this were true, a prediction

could be stated that tadpoles with the same feeding

morphologies feeding on the same foods within the

same type microhabitat should not occur in the

same pond at the same time. Data are available

from two pond studies which do not support this

prediction. For tadpoles with scraping and chewing

mouthparts, the best test is to look for co-occurring,

similar size larvae belonging to the same genus.

Wiest (1974) did not sample for microhabitat differences, but one of the ponds he reported had

only one microhabitat. This was pond D, which was

a uniform, shallow grassy pond in a heavily grazed

pasture. The same larval stages of Pseudacris clarki

and P. streckeri, which have the same mouthparts,

occurred together in this pond. The beakless midwater feeding microhylid genera at Sakaerat,

Thailand, all have morphologically similar larvae,

of the same size, and all feed on the same food in

the same way (Heyer, 1973). Three ponds there

that had a single uniform microhabitat were sampled. For all practical purposes, the ponds were

dirt aquaria. There was no standing vegetation in

the water. If competition had been important historically, no two species of any of the midwater

feeding genera should have occurred together in

these ponds, however, the following pairs did occur

together, refuting the importance of the potential

for interspecific tadpole competition in nature:

Glyphoglossus molossus and Microhyla pulchra,

Glyphoglossus molossus and Kaloula mediolincata,

Kaloula pulchra and Microhyla pulchra (Heyer,

1973). In another pond which was sampled by

microhabitats, Glyphoglossus molossus and Microhyla ornata larvae occurred in the same sweeps.

Interspecific behavioral adjustments appear to be
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

rare among tadpoles, indicating that generally,

interspecific competition among tadpoles is evolutionarily unimportant. In field experiments,

Agalychnis larvae occupied the water column and

the pond floor when it was the only species present,

but when Hyla rosenbergi, a bottom dwelling tadpole species, was in the same pond, the Agalychnis

larvae all occupied the water column (McDiarmid,

pers. comm.). Two partially exclusive explanations

may account for the type of behavioral shift evidenced by the Agalychnis larvae. First, there is

competition for space when Agalychnis is present

with bottom dwelling tadpoles which may occasion

a behavioral response by Agalychnis: partitioning

the habitat to avoid competition. Second, the response by Agalychnis may be purely density dependent. Individual Agalychnis larvae may occupy the

bottom if there are less than a given number of

larvae already present on the bottom (including

other Agalychnis individuals). If there are many

tadpoles on the bottom, at least some of the

Agalychnis larvae will occupy the water column.

If all the bottom larvae belong to another species,

the results would appear to be habitat partitioning

in response to another species, not just other individual tadpoles, but with so little data, it is impossible to choose among the alternatives. Larval

behavioral shifts in response to other species appear

to be rare, however, and they appear to be part of

the total adaptive set of the species that evidences

the behavioral switch. Thus the response is completely one sided; there are no accompanying behavioral shifts in other members of the same

community. My prediction is that behavioral

changes in response to other tadpoles will be found

in relatively specialized larvae, such as midwater

adapted Agalychnis, such behavioral flexibility

allowing greater exploitation of the habitat. Thus,

when no other bottom dwelling tadpoles are present, Agalychnis larvae will utilize the bottom, even

though their adaptive morphology is specialized

for midwater feeding (Starrett, 1973).

Another factor that would refute larval competition as the origin of temporal partitioning by

tadpoles is the following. At the point in the speciation process where reproductive isolation is being

reinforced by selection, one premating isolating

mechanism that can undergo character displacement

is temporal partitioning of the breeding season. If

selection operates to displace the breeding season

of two closely related taxa, the larvae would also

demonstrate temporal habitat partitioning.

Finally, a theoretical model based on a community analagous to a tadpole community predicts

that several phytoplankton cropping species may

coexist without competitive exclusion (Smith, et.

al., 1975).

The available evidence indicates that communities of tadpoles represent nothing more than a

collection of species co-occurring as larvae. A tadpole community is not an integrated whole; biological interactions within the community are not

important evolutionarily; there is no natural selection operating directly to integrate or partition the

community. Similar conclusions have been reported

recently in other aquatic communities, involving

predatory fish (Mendelson, 1975) and dragonfly

larvae (Benke and Benke, 1975).

The Generalized Anuran Life Cycle

and Its Evolutionary Maintenance

Wassersug (1975), from a morphological analysis

of tadpole adaptive types, proposed that the tadpole stage evolved to exploit the bursts of primary

productivity characteristic of temporary ponds. The

temporary food resources are exploitable because

the tadpole stage is temporary, coinciding with the

bursts of primary productivity.

Heyer, McDiarmid, and Weigmann (1975) proposed a model that from an ecological viewpoint

presents reasons why the generalized anuran life

history should be maintained in temporary ponds

during the larval stage. As long as there are temporary ponds with bursts of primary productivity, selection will favor the maintenance of

the generalized anuran life cycle which includes the

herbivorous tadpole stage. The total environment

for which the tadpole stage is adapted is marked

by extreme variability and unpredictability. The

environment is unpredictable from a climaticphysical aspect. Ponds may be present in a location

in one year and absent the next (Wiest, 1974;

Collins, 1975). The biological environment varies

in the same pond from one year to the next

(Chesapeake data). For any species found in a

series of ponds, the biological environment varies

from pond to pond (Heyer, 1973; Wiest, 1974;

BCI data).
NUMBER 242 23

One evolutionary response designed to exploit

unpredictable environments is to maximize both

reproductive effort and genetic variability simultaneously. The amphibian genetic system appears

to be well suited to maximize genetic variability in

its reproductive effort. Polyploidy is not known to

occur in higher vertebrates (parthenogenetic lizards

excluded), possibly because the higher vertebrate

is a complexly integrated machine that can not

function if the genetic controls are changed to any

great degree. Having an extra chromosome set may

be too much of a genetic change to allow the higher

vertebrate cell to function properly. Polyploidy is

known for lower vertebrates, including frogs, and

could be interpreted to mean that the amphibian

cell can tolerate considerable genetic changes and

still function. (This argument does not imply that

mammals are more highly evolved than frogs. It

does imply that frogs have more evolutionary

mechanisms available than mammals.) Wilson,

Sarich, and Maxson (1974) have shown that closely

related species of frogs have much larger genetic

differences than similar pairs of mammal species.

They assumed constant rates of protein evolution

and concluded the frog species are much older

than the mammal species. Another interpretation

is that many mutations in albumin structure may

be deleterious in the homeostatic mammalian system although such can be tolerated in the less well

regulated amphibian system. These inferences suggest that compared to the mammalian genetic system, the anuran genetic system is preadapted to,

and continually selected for, maintenance of large

amounts of variability. One of the reasons large

clutch size may be adaptive in frogs is that a wide

variety of genotypes can be expressed in every

reproductive effort. Some of the genotypes likely

would be adaptive in the situation in which any

egg clutch was laid, but due to the unpredictability

of the pond environments, there is no way for

natural selection to operate to select a genotype

that will always work best. Natural selection would

operate to select those individuals that maximized

genetic variability in each reproductive effort. It is

not necessary to postulate an increased mutation

rate; selection would maintain, rather than reduce,

the variability present.

There are no available direct data on the

amounts of genetic variation present in a single

large frog egg clutch, but there is circumstantial

evidence to suggest that the amount of variation is

considerable. Many frog egg clutches brought in

from the field and raised under laboratory conditions experience heavy mortality, particularly at

three stages: gastrulation, hatching, and metamorphosis. These three times represent periods when

different parts of the genotype are activated for the

first time. Death may be due to defective genotypes. High genetic variability would account for

this high rate of genetic death as many of the

combinations are lethal in some egg clutches. Thus,

it would appear that the number of genotypes is

maximized within a single clutch. The larger the

clutch, the more possible genotypes can be exposed

and selected in the pond where the clutch is laid.

In addition to the maximizing of individual

clutch size, breeding adults should produce multiple

clutches in order to ensure reproductive success in

an unpredictable environment. Crump (1974) found

this to be true for the single gravid female recapture she reported: Hyla rhodopepla is a small,

pond breeding hylid which produced 2 clutches in

31 days. This is the only known data on tropical

pond breeding frogs other than that for Physalaemus previously discussed (Davidson and Hough,

1969). To achieve maximum reproductive effort,

frogs in the temperate zones could either be long

lived, producing one clutch a year, or if short

lived, produce multiple clutches in one year. Some

species of temperate frogs are known to be long

lived, reproducing over several seasons (Collins,

1975). Rana clamitans combines long life and the

production of multiple clutches within a reproductive season (literature summarized in Collins,

1975). There are no data on number of clutches

laid per season by small species; in Michigan,

most individuals of small frog species have only

one reproductive season, but some individuals

breed over at least two reproductive seasons

(Collins, 1975). Thus frogs exploiting temporary

ponds with large clutch size and multiple clutches

would have selective advantages over frogs with

smaller clutch sizes and/or single clutches. Salthe

and Duellman (1973) demonstrated that, of all the

frogs they studied, pond breeding frogs have egg

clutches with the most eggs.

The generalized anuran life cycle involving large,

multiple clutches with essentially random popula-
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

tion control at the larval level should occasionally

result in great densities of frogs when, due to the

random character of tadpole population control,

there is little or no tadpole population reduction.

Such outbreaks of frogs have been reported in

newspapers and at least once in scientific journals

(Scott and Starrett, 1974).

In some ways, the situation Calef (1973a) described is not consistent with the conclusions

reached in this paper (see "Other Studies of Larval

Habit Partitioning" above). The larval population

dynamics were very similar in the two consecutive

years studied by him. At the northern distributional

limit of frog occurrence, one would not expect to

find a system where larval population structures

are the same from one year to the next. If the larval

populations are as stable as the two year study

indicates, the simplicity of the system may well

account for this stability. There is one species of

frog which breeds in permanent water in British

Columbia. The predatory salamanders are permanent residents of the lake in which these frogs

breed. Calef (pers. comm.) found salamanders in

all ponds and lakes where Rana aurora bred. The

system is apparently in a steady state and predictable; ponds are effectively permanent, predator and

prey interaction always occur between the same

predator and the same prey. Under these predictable conditions, Calef (1973a) concluded that

the biological interactions (predator-prey) control

and stabilize the community structure and population density of Rana aurora larvae. Calef's study

adds support to the hypothesis that modifications

of the anuran generalized life cycle only occur in

relatively predictable environments (see "Evolutionary Modifications of the Generalized Auran

Life Cycle" below). His study also indicates that

not all predictable environments are limited to

tropical wet forests.

Selection, Population Control,

and the Anuran Life Cycle

The data, analyses, and conclusions presented

here are summarized in terms of features of the life

cycle where natural selection and population control likely are most effective.

Calling Sites: Competition for calling sites is

most evident in those species with long breeding

seasons. In those species for which calling sites have

been a limiting factor, territoriality has been a common evolutionary response (for example: Rana

clamitans, Wells, pers. comm.; dendrobatids,

Duellman, 1966, Silverstone, 1975; centrolenids,

McDiarmid and Adler, 1974). Territoriality involving male calling sites can be an important population control mechanism.

Egg Deposition Sites: Egg deposition sites may

be the same as calling sites (e.g. centrolenids,

McDiarmid, 1975) or within the defended territory

but not identical with calling sites (e.g. dendrobatids, Crump, 1972; Silverstone, 1973). Territoriality may have arisen in response to limited

availability of egg deposition sites. Some nonterritorial frogs have specific egg deposition sites,

the availability of which may control the population size of the species (e.g. some Phyllomedusa lay

their eggs on leaves of particular species of plants,

Pyburn, pers. comm.).

Clutch Size and Number: As discussed above,

selection should favor large clutch size and multiple

clutches in frogs with generalized life cycles. A

most effective population control at this level is

climatic uncertainty, such as ponds drying up or

egg masses freezing. Egg predation can be important

within ponds (Walters, 1975) but unpredictable

among ponds or from year to year. In these situations, selection will favor large, multiple clutches.

Larvae: Certain kinds of predator-prey interactions can have an evolutionary effect on type of

pond choice by species of frogs. As argued elsewhere (Heyer, McDiarmid, and Weigmann, 1975),

for selection to operate, the predator must eliminate, not reduce, tadpole populations. Predation by

fish (Heyer, McDiarmid, and Weighmann, 1975)

and turtles (Heyer and Muedeking, in prep.) has

been identified as a factor that has likely produced evolutionary change in terms of choice of

ponds; the smaller, temporary ponds, free of fish

and turtles being favored. The relationship between

pond size and occurrence of (either, but not both)

fish and Colostethus larvae in the BCI stream ponds

is consistent with this hypothesis.

Salamander and invertebrate predators within
NUMBER 242 25

temporary ponds may effectively reduce population

sizes (Calef, 1973a; Walters, 1975), but the level of

predation usually is variable among ponds or from

year to year. In these situations, selection will favor

maximizing variability of reproductive efforts; that

is, large, multiple clutches will be favored.

Adults: Direct data are not available, but it

seems likely that all effective population control

occurs in the stages already listed. Competition for

resources (other than calling or egg deposition sites)

is probably not important. Scott and Starrett (1974)

reported on an unusual situation where the number

of adult Agalychnis spurrelli was several times

greater in one area than normally encountered.

This suggests that adult frog populations are normally well below the carrying capacity of the

environment. Calef (1973a) suggested that if survivorship from juvenile to adult Rana aurora were

similar to the rate of larval survival, the adult

population would be sufficient to maintain the

population, but he found adult populations to be

3 to 6 times as large as those needed to maintain

the population (Calef, 1973b). Thus, for Rana

aurora, most population reduction is occurring in

the larval stage.

Evolutionary Modifications of the

Generalized Anuran Life Cycle

Temporary ponds that are characterized by bursts

of primary productivity occur in seasonal environments. The appearance and duration of such ponds

is highly variable. By contrast, environments with

little seasonality do not have bursts of primary

productivity in their ponds, the ponds are long

lived, and the biological communities more predictable and stable. In relatively aseasonal, stable

environments, selection 'should operate to finely

adapt the organism to the environment. There

would not be a selective advantage to maximizing

genetic variability within a clutch. In fact, selection

should operate to reduce genetic variability to the

optimum genotype(s) for the stable environment

in which the species occurs. Large clutch size and

multiple clutches would not have selective advantages per se. Evolution could operate on other

parameters involving smaller clutch sizes that would

adapt the life cycle to stable environments, such as

parental care, brooding, and increase of yolk per

egg, which is a prerequisite for direct development

in most frogs (Salthe and Duellman, 1973; also see

Heyer, 1975).
Literature Cited

Anderson, J. D.

1968. A Comparison of the Food Habits of Ambystoma

macrodactylum sigillatum, Ambystoma macrodactylum croceum, and Ambystoma tigrinum californiense. Herpetologica, 24:273-284.

Anderson, J. D., and R. E. Graham

1967. Vertical Migration and Stratification of Larval

Ambystoma. Copeia, 1967:371-374.

Anderson, J. D., D. D. Hassinger, and G. H. Dalrymple

1971. Natural Mortality of Eggs and Larvae of Ambystoma

t. tigrinum. Ecology, 52:1107-1112.

Benke, A. C, and S. S. Benke

1975. Comparative Dynamics and Life Histories of Coexisting Dragonfly Populations. Ecology, 56:302-317.

Brockelman, W. Y.

1969. An Analysis of Density Effects and Predation in

Bufo americanus Tadpoles. Ecology, 50:632-644.

Calef, G. W.

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