Climate Driven Population Fluctuations in Rain Forest Frogs
Author(s): Margaret M. Stewart
Source: Journal of Herpetology, Vol. 29, No. 3, (Sep., 1995), pp. 437-446
Published by: Society for the Study of Amphibians and Reptiles
Stable URL: http://www.jstor.org/stable/1564995
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Journal of Herpetology, Vol. 29, No. 3, pp. 437-446, 1995
Copyright 1995 Society for the Study of Amphibians and Reptiles
Climate Driven Population Fluctuations in Rain Forest Frogs
MARGARETM. STEWART
Departmentof BiologicalSciences.StateUniversityof New Yorkat Albany,Albany,New York12222,USA
ABSTRACT.-A deme of Eleutherodactylus coqui was followed from 1979 to 1993 at El Verde, Puerto
Rico, to determine seasonal and annual variation in numbers and activity patterns. All visible frogs and
predatory spiders in a 50 x 2 m transect in the forest were counted for three consecutive nights semimonthly for two years, then annually or biannually thereafter for a total of 255 evening counts. Ten allnight counts were made at five different times of the year to determine time of maximal activity during
the night. Population size varied seasonally, with numbers increasing from June until December followed
by a gradual decline until May. The number of adults varied from 1 to 29/100 m2,whereas the number of
juveniles varied from 0 to 221/100 m2.The maximum single count of all frogs was 244. Counts of >100
juveniles occurredduring October through Januaryin the years 1979 to 1982, and in 1989. A marked drop
in the numbers of frogs occurred in 1984; from 1979 to 1983, 3-50% of the counts yielded >15 adults
whereas the maximum count from 1984until 1989 was 11 adults. The drop in numbers was correlatedwith
an increased number of periods of days with <3 mm of rain. Over the period 1979 to 1989, the number
of frogs observed was negatively correlated with the longest dry period during the previous year.
Population size began to decrease in 1983 and never regained prior levels although numbers were
increasing
early in 1989before HurricaneHugo. Juveniles apparentlycannot survive extensive drought, and extended
dry periods may be lethal to adults who are inhibited from feeding because of potential desiccation.
Predatory ctenid spider populations crashed two years following the decline of frog populations, then
disappearedfollowing the hurricaneas did other arthropodpredators.Ratherthan total monthly or annual
rainfall, it is the distribution of the rain that is important to these subtropical wet forest species.
The perception that many anurans are becoming rare or disappearing (Wake, 1991) provides impetus to understanding natural variations in amphibian population size within ecosystems (Pechmann et al., 1991; Blaustein, 1994;
McCoy, 1994; Pechmann and Wilbur, 1994;
Travis, 1994). Although several temperate zone
amphibians have been studied for up to 24 yrs
(see references in Pechmann and Wilbur, 1994),
little information has been published concerning temporal variation in tropical frog populations (Kluge, 1981; Stewart and Pough, 1983;
Barbault, 1991; Woolbright, 1991; Galatti, 1992).
Studies of the Puerto Rican coqui, Eleutherodactylus coqui, and its congeners at El Verde date
back to the 1960s when H. T. Odum initiated
studies on the Puerto Rican rain forest in the
Luquillo Mountains of eastern Puerto Rico
(Odum and Pigeon, 1970). My observations on
E. coqui began in 1978. Here, I report results of
15 yrs of population censuses.
To understand population changes within and
between years, I followed a population of E.
coqui and other co-occurring anurans in a 2 x
50 m plot. My studies in that plot, called the
Activity Transect (AT), provide basic data on
the composition of a deme of frogs and how
density changed seasonally and annually. The
AT provided baseline data for comparisons with
other field studies conducted in the forest during the period. I was fortunate in having a study
site where current human disturbances were
negligible.
METHODS
Site
and
Study
Species.-The study was conducted in the Luquillo Experimental Forest, Caribbean National Forest, which surrounds the
El Verde Field Station at 350-450 m in the Luquillo Mountains of northeastern Puerto Rico
(18?22'N; 65052'W). The study site lies in a second growth subtropical wet forest (Ewel and
Whitmore, 1973), recovered from a coffee plantation since the 1940s (Odum and Pigeon, 1970).
Eleutherodactyluscoquiis a terrestrial-breeding
species that remains on small territories, and
does not exhibit breeding or seasonal migrations as do aquatic breeding anurans. Although
the climate is mildly seasonal (Odum et al., 1970),
frog activity continues throughout the year albeit with less calling and breeding in cooler
months (Stewart and Pough, 1983; Woolbright,
1985; Townsend and Stewart, 1994). Because
non-aquatic eggs develop directly into small
froglets, there is no distinct difference in the
habitat of pre-adults and adults as there is in
aquatic-breeding species with tadpoles. Adult
males are territorial and exhibit strong site attachment. Calling and brooding males are located primarily in the understory, averaging 1
m above ground (Townsend et al., 1984; Woolbright, 1985), whereas subadults, many females,
438
MARGARETM. STEWART
and non-breeding males climb to the canopy to
forage at night (Stewart, 1985). Frogs are 6-7
mm snout-vent length (SVL) at hatching and
grow rapidly, reaching breeding size in one
year. Size classes use somewhat different levels
in the vertical space of the forest with juveniles
perching on low vegetation. Frogs forage higher in the understory as they grow larger (Stewart, 1985).
I grouped frogs into three size classes by SVL:
juveniles <18 mm; subadults 18-23 mm; and
adults > 23 mm (maximum of 55 mm at this
site). The adult status was determined by the
size at which the internal opening of the vocal
sac is visible.
Activity Transect.-The AT was a meter-wide
strip on both sides of a 50 m trail in the forest
so that a total of 100 m2 was sampled. Counts
were made from 2000-2100 h. By 2000 h frogs
leave their diurnal retreats on or near the forest
floor and are on their nocturnal sites with little
additional movement unless major weather
changes occur (Woolbright, 1985). Observers
counted frogs from ground to canopy by systematically scanning visible surfaces of leaves,
vines, rocks, and tree trunks. Individuals are
not disturbed by flashlight as they sit on top of
understory leaves, so direct observations and
counts are relatively easy. Frogs were not captured during counts. I recorded all species of
frogs seen or heard in the transect, and all predators known to feed on coquies (Stewart and
Woolbright, in press).
Counts were made by two people to complete
the census as quickly as possible. Observers were
trained with several trial runs comparing their
counts with those made by an experienced observer (counts differed by less than 5%).Counts
were made for three consecutive nights to account for the influence of weather on frog activity. Because some frogs may climb to the canopy before 2000 h (Stewart, 1985), subadult and
adult counts were often lower than the actual
numbers present in the AT. Because these factors could reduce the number of frogs visible
from the ground, I considered the maximum
number of frogs seen in a three-night sequence
of counts the closest approximation to actual
frog density. Counts were made semi-monthly
from 20 June 1979 for two years, then twice or
more in each of the following years. Thirty-two
individual counts were made in 1979, 59 in 1980,
25 in 1981, 18 in 1982, 30 in 1983, 12 in 1984,
12 in 1985, 12 in 1986, 15 in 1987, 7 in 1988, 5
in 1989, 4 in 1990, 3 in 1991, 9 in 1992, and 12
in 1993, for a total of 255 evening counts.
To determine how population density
changed from year to year, I compared the maximum number of frogs counted during the same
season throughout the study. I used the Decem-
ber-January census period because population
maxima occur at that time. To determine the
time of maximum frog activity during the night,
10 all-night counts were made with a census
every two hours. All-night counts were made
at 2000, 2200, 2400, 0200, 0400, and 0600 h during February and March 1980, July 1979, 1981,
1982, 1983, August 1979, and November 1981.
I recorded temperature and relative humidity
1 m above ground at the start of each count. I
obtained rainfall and temperature data from a
weather station 100 m from the field site. Approximately 50-60% of rainfall is intercepted by
the canopy, and 1.5 mm is insufficient to wet
the litter (Odum et al., 1970;Scatena, 1990). Based
on this information, I chose three mm of rainfall
as the threshold below which frogs are critically
stressed (Pough et al., 1983; Beuchat et al., 1984).
Ground slope of the AT was measured using
a Brunton compass. Ground slope varied from
0-16?. The vegetation along the transect consisted of open forest with a shrub understory
and groundcover of seedlings and non-woody
plants; these were underlain with fallen leaves
in different stages of decay. The AT contained
11 trees >15 cm diameter at breast height with
canopy closure at approximately 15 m. Species
included both broad leaved trees and palms,
small saplings, shrubs and a few lianas. There
was abundant ground cover of tree seedlings,
forbs, and grasses. Before hurricane disturbance, ground cover was 5 to 15 cm high. Understory shrub height was 1 to 1.5 m.
The area of the AT was shaded except for
small sunflecks. Fifty readings of light levels
(UDT-40 x Opto-meter photometer, United Detector Technology, Inc.) were taken on a clear
day at 1-m intervals throughout the transect at
1225 h 19 February 1980. The sensor was placed
at ground level and pointed vertically. Light
levels averaged 27.9 (1.9-241.5) lux. An occasional treefall altered light and cover. Hurricane David, September 1979, although not severe, resulted in much leaf and twig fall, hence
deep litter. The major impact on the site was
Hurricane Hugo, 18 September 1989, which
felled or topped most of the trees on the site
and removed leaves from remaining trees
(Lodge et al., 1991; Walker, 1991).
Frogs, unless in transit, were never found on
the ground and rarely on rocks. Perch sites were
smooth upper leaf surfaces, stems, or trunks.
Juveniles perched most frequently on the low
broad leaves of the grass Panicum adspersum.
Perches of visible adults were most often leaves
of the shrub Piper glabrescens,and sierra palm,
Prestoea montana. From measurements made in
1979, juvenile perches averaged 14 cm above
ground, subadults 33 cm, and visible adults 74
cm (Townsend, 1985).
439
PUERTO RICAN FROGS
150
-
ILn
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z
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Juvenile
D
Subadult
*
z
cn
100
z
0
c
Adult
0
O
U.
Subadult
-
u)
-
Juvenile
2
200
Adult
150
0
0IL
m
100
z
50
z
Ii- l l
';1
EM
ff
|
0 I'"
'
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I
x
ii1, IIl
i,
z
m
n
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l i 11 ilii
'-
i-
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z
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-1
I .1 II
D
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0
.
-
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0
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0
Z
0
w
a
MONTHS
FIG.1. Seasonal variation in density of juvenile,
coquiin the Acsubadult,and adult Eleutherodactylus
tivity Transectas shown by monthly maximacounted
during 1980. No data were collected September-November.
RESULTS
varied from 0 to 221/100
m2.
Subadults were usually the least numerous (034/100
m2). Numbers
of calling
- C
CO
M
O_
__ CD
_
C
_
C
v
@
C
C0 000-
9
, i
_
_
O
N
lHi
^
O
MONTH
OFYEAR
FIG.2. Maximaldensity of frogs in Activity Transect throughoutthe study, from June 1979to November 1993.
ulation decline) were significantly higher than
those during the years 1984-1985 to 1988-1989
(Fig. 3; t = 2.47, df = 7, P <0.05 for preadults;
t = 8.34, df = 7, P <0.001 for adults; two-sample
Population Variation.-Population density of
the three size classes varied seasonally (data from
1980 shown in Fig. 1). Throughout the year there
was a marked increase in total number of frogs
from June until December followed by a gradual decline through May. Juvenile density varied the most with season and adult density varied the least. Coefficients of variation for the
years 1980 and 1981, respectively, were as follows: juveniles 69.5% and 50.0%; adults 43.2%
and 34.8%. Monthly maximal counts for the entire survey period showed even greater fluctuations (Fig. 2). Throughout the pre-Hurricane
Hugo years, adults varied from 1 to 29 /100 m2,
whereas juveniles
-
'
i
i 1 Jiiii
Iii
II
males varied
from 0 to 8 (x = 2 when any frogs called, N =
167 calling nights). The maximum count of visible frogs was 244/100 m2 in October 1982 with
a juvenile count 17 times greater than the adult
count.
Numbers of all size classes of frogs declined
during 1983 with a marked decrease during 1984
(Table 1; Figs. 2, 3). From 1979 to 1983, 3-50%
of the counts yielded >15 adults whereas from
1985 to 1989, the maximum number of adults
was eight. All counts of >100 juveniles occurred during October through January in the
years 1979 to 1982, and in 1989. When the maximum number of frogs per census during December-January counts were compared among
years, counts during the years 1979-1980 to
1983-1984 (the years prior to the marked pop-
t-test).
Abiotic Conditions.-The climate is mildly seasonal with lowest temperatures from December
to March (Odum and Pigeon, 1970). From 1978
until 1989, total annual rainfall varied from 475
cm in 1979 to 284 cm in 1980 (Fig. 4). Data from
1975 to 1993 document rainfall just prior to, as
well as during my study. There was less rainfall
from January to April than in other months
(Fig. 5). Relative humidity was high in the forest. Measurements taken in the transect prior
to counts during 1980 averaged 88% (73-100%;
SD = 6.2; N = 66). Weather had obvious
effects
on frog activity, especially on the smaller size
classes. Adults remained exposed and visible
unless there was a drenching rain, but on windy
nights they switched from an active body posture to a water-conserving posture (Heatwole
et al., 1969; Pough et al., 1983) and did not call.
When temperatures fell below 20 C, almost all
calling ceased, especially if it were dry. No frogs
called at temperatures below 18 C. Few juveniles were visible on windy nights or during
rain unless the rain was light. After prolonged
periods without rain, activity declined and few
frogs, mostly adults in water-conserving posture, were visible. One such example occurred
in October, 1979. After five days without rain,
humidity dropped from 90% to 73%. The juvenile count decreased from 186 to 61 (67% decline), and the adult count decreased from 16
to 12 (25% decline). The following night there
was a shower at 1800 h. At 2000 h the humidity
was 90% and I counted 143 juveniles.
The drop in numbers of frogs after 1983 was
v-
MARGARETM. STEWART
440
1. Numbersand lengths of prolonged dry
TABLE
periodsat El VerdeField Station.Forthe years 19781993are given: total numberof periods with five or
more days with <3 mm of rainfall;number of dry
periodsexceeding10d;maximumnumberof drydays/
yr; maximumnumberof all E. coqui(maximumnumber of adults); and maximum number of spiders
counted in any census in the Activity Transect.
200
~~_-~~
cn
-
Preadults
*
Adults
O
oo
zSw
100
1
50
....
............... ............... .............. ................
........
Dry
Year
No.dry
periods > 10 d dry days (adults) spiders
1984
9
8
9
12
7
10
9
1985
8
1986
8
16
6
11
7
11
12
9
1978
1979
1980
1981
1982
1983
1987
1988
1989
1990
1991
1992
1993
Totals
Means
Max.no
periods
of Max.no frogs Max.no.
152
9.5
1
1
1
1
1
4
1
4
2
1
2
1
0
1
3
0
24
1.5
12
13
14
11
12
22
28
25
13
13
23
30
8
16
26
10
17.3
..................................
230 (16)
171 (29)
171 (27)
244 (22)
125 (22)
82(14)
57 (7)
54 (8)
17
32
25
20
15
28
6
60 (7)
6
90 (7)
156 (6)
36 (16)
21 (14)
28 (7)
40(8)
1
8
0
0
0
0
104 (14)
11
0
o
co
d?
a-
coo
co
a)
T
o14
co
co
C0
Co
CO
co
CD
co
c0
CO
00
co
a,
v-
a)
v-
CD
co
0)
-
rp(0
oD
0)
DECEMBER- JANUARYDENSITIES
FIG.3. Yearlyvariationin frog density as shown
by maximumnumber of frogs counted during Decemberand Januarycensus periods from 1979-1980
to 1988-1989.
2, 3), but conditions were disrupted severely by
Hurricane Hugo in September 1989.
Litter depth was influenced primarily by hurricanes. Litter depth in July 1982 was 0-13 cm
(x = 4.6 cm, N = 29). After Hurricane David in
not accompanied by a drop in total rainfall. In
fact, total rainfall from 1984 to 1988 was slightly, though not significantly, greater than that
from 1979 to 1983. Mean monthly rainfall for
the years 1979 to 1983 (years of population highs)
was not significantly different from the years
1984 to 1988, years of population lows (t = 0.66,
df = 22, P > 0.50; Fig. 5). However, after 1982,
periods with little or no rain lengthened and
became more numerous (Table 1). Longer periods without rain were correlated with a decrease in frog density. When the maximum
number of days with <3 mm of rain during a
year for the years 1978 to 1989 was compared
to the maximum number of frogs the following
year, the number of frogs was negatively correlated with the longest dry periods during the
previous year (r, = 0.700, P < 0.01). Following
the longest dry period, 28 d, in March and April
1984, there was a large drop in the numbers of
all size classes, and populations never regained
densities found prior to those years. The years
1983, 1984, and 1985 had the longest dry periods
(22, 28, 25 d) during the pre-Hurricane Hugo
period (Table 1). More than twice as many of
the prolonged dry periods occurred from January to June than from July to December (103
vs. 49; Fig. 6). The numbers of juveniles increased in December 1988 to January 1989 (Figs.
September 1979, litter was especially heavy, up
to 30 cm deep in some spots. After treefall and
canopy loss from Hurricane Hugo, herbaceous
vegetation flourished and provided complete
groundcover. In May, 1990, mean height of nonwoody vegetation (primarily Panicum adspersum) was 51 cm (30-86, N = 9), and of shrubs
(primarily Piper spp.) was 92 cm (38-158, N =
17). In October 1993, four years following Hurricane Hugo, the area had been invaded by Heliconiaand 20-cm seedlings; there was little Panicum. Litter depth was 4.7 cm (0-9); the ground
was covered with small tree seedlings 17.4 cm
(10-29) high, and an intermediate layer of saplings and shrubs, mostly Piperglabrescens,85 cm
(55-122) high. Plant heights were continuous
thereafter, without a distinct layer, to the canopy 10-20 m above ground.
All-night Activity.-The maximum number of
frogs was counted at the 2000 h census. Most
adults remained visible on vegetation until late
in the night. Numbers of juveniles decreased
steadily during the night (Fig. 7). All frogs disappeared by 0600 h having returned to their
daytime retreats. Light showers during the night
resulted in an increase in visible juveniles, but
heavy showers resulted in the disappearance of
most juveniles and a marked decrease in larger
frogs as well. Temperature dropped little during the night (0-2.2 C change; N = 10 nights).
441
PUERTO RICAN FROGS
25
500
z
450
C400
350
L
U 300j
20
250
u-200
150
z 100
E
a
so0
X
eC
Cu
C
D
Cu
C
C Cu
Cu
Cu
Cu
u
u
C
C
15
I.
0
YEARS
10
UJ
FIG.4. Totalannual precipitation(cm)at El Verde
Field Station, Puerto Rico, for 19 years (1975-1993).
Any changes in temperature were associated
with showers or with gusts of wind that broke
the subcanopy air cell. Numbers of visible juveniles declined throughout the night even
when temperatures did not change.
Other Species of Frogs. -Eleutherodactylus
wightmanae (0-3 per count) and E. portoricensis
(0-8 per count) called regularly in the plot during the early years of the study. The small litter
species, E. wightmanae, called near the ground.
Eleutherodactylus portoricensis, similar to but
smaller than E. coqui, was nearly always observed in the AT through 1984 after which it
was seen only twice. Bufo marinus(six sightings)
and Leptodactylusalbilabris(four sightings) moved
through the transect rarely.
Predators.-The most abundant predators seen
in the AT during counts were sparassid crab
spiders (Olios antiguensis and Stasina portoricensis). Other predators included wolf spiders Oligoctenus ottleyi, tarantula Avicularia laeta, amblypygid Phrynus longipes, forest crab Epilobocerasituatifrons, screech owl Otus nudipes, and black
rat Rattus rattus. Anolis gundlachi and A. stratulus,
m
Z
5
0
C i
-
. C -
>
L
'
m~~~p~~~~~,:
MONTHS,1978-1993
FIG.6. Numbers of prolonged dry periods by
month, at El VerdeField Station,PuertoRico.Periods
with five or more days with <3 mm of rainfall from
1978-1993. Total periods: Jan. to June: 103; July to
Dec.: 49 (total = 152).
diurnal frog predators, lived in and around the
transect. The cricket Amphiacusta caraibea, a
predator on frog eggs, was often present. Numbers of predators varied dramatically during the
study, especially after Hurricane Hugo, when
none were seen except in July 1992 (1-11 crab
spiders, N = 6 counts).
The annual maximum number of crab spiders
averaged 22.8/100 m2 (15-32 spiders, 12-49
E
Juvenile
O
Subadult
*
Adult
120
600
100
U)
O
0o
E
E
500
U.
(T
400
a)
.-j
_1
G
80
60
1
I
LU
z
UJ
L.
-J
300
40
200
20
100
0
_
I
z
z
I.
fi
I
2000
Z
,
a
UL
m
m
0:
<
>
Z
-J
(
n
n
<
.
0
>
F
O
0
I
2200
_: I
2400
I
200
400
600
TIMEOF NIGHT
Z
MONTHS
FIG.5. Mean monthly rainfall (mm) at El Verde
Field Station,PuertoRico,for the periods 1979to 1983
and 1984 to 1988.
FIG.7. All night activitylevels of E.coquias shown
by average number of frogs (+ 1 SE)counted every 2
h during the night in February1980,July 1981, 1982,
1983 (2) and November 1981 (N = 6). No frogs were
visible by 0600 h.
442
MARGARETM. STEWART
counts/yr). Numbers of crab spiders declined
after midnight (e.g., July 14-15, 1981, seven spiders were visible at 2200 and 2400 h, but only
two at 0200 h). Through the years 1980 to 1985,
spiders reached much higher densities during
the months June to November (0-32; N = 77
counts) than from December to May (0-19; N
= 70 counts). Wolf spiders were rarely seen. A
marked decline in sparassid spiders occurred
after 1985 (Table 1). The annual maxima (1532) during the years 1980-1985 far exceeded the
maxima (1-8) found during years 1986-1989.
From 1986 to 1993 the maximum number each
year averaged 3.7 (0-11 spiders; 3-12 counts/
yr). After Hurricane Hugo spiders were seen on
only seven of 28 counts.
Phrynus longipes, the guava, is a major frog
predator, catching them as frogs climb trees
(Stewart and Woolbright, in press). One to three
were observed in the AT (seen in 26 counts).
Tarantulas are also major frog predators; at least
five different tarantula "hides" were built on
tree trunks in the transect. Neither large predator was seen in the AT following Hurricane
Hugo.
DISCUSSION
Eleutherodactyluscoqui is one of the most important species in Puerto Rican forests. It constitutes the largest component of the nocturnal
biomass of all vertebrates in the rain forest.
Stewart and Woolbright (in press) estimated that
it occurs in densities of up to 3265 adults/ha,
or totals of 20,570 frogs/ha. As a secondary and
tertiary consumer, it eats at least 101 species as
prey, mostly arthropods. It consumes 114,000
prey/night/ha, and serves as food for both invertebrate and vertebrate predators. The pattern of population variation in E. coquifollows
that of small ectothermic vertebrates with a short
life span (Zug, 1993). The great variation in population density is due in part to the short generation time of the frogs. The 15 years of this
study spans several generations of coquies. Since
some hatchlings are produced throughout the
year, the population consists of individuals of
several different ages at any one time. Most
adults live less than two years. Stewart and
Woolbright (in press)calculated that 94%of adults
do not survive to the following year, and survivorship of the smaller frogs is surely much
lower. For example, in one population of 172
coquies marked in 1983, 8%were recaptured in
1984 and 3%were recaptured in 1985 (Stewart,
unpubl.).
During the first five years of this study, seasonal changes in the amount of breeding accounted for most variation in frog density. Lower temperatures in winter months are sufficient
to reduce, but not eliminate, reproduction. Maximum juvenile counts occurred from October to
December and were eight times that of the maximum adult counts. After that time juveniles
decreased markedly as they grew rapidly into
the next larger size class and as predators took
their toll. Within one year (1980), seasonal variation accounted for a four-fold difference in
monthly maxima of adults, the most stable group
numerically. Although some of the variation
between counts may result from differences in
canopy use on census nights (Stewart, 1985),
seasonal population lows or highs showed repeatability over sampling periods regardless of
weather on any one night.
Population changes within a year were influenced by abiotic factors such as seasonal changes
in daylength, temperature, and rainfall. Days
are two hours longer in June than in January.
The highest monthly average temperatures occurred from May to September. Rainfall is less
during January to March than in other months
of the year (Odum et al., 1970), but monthly
rainfall seldom drops below 100 mm during
those months (Fig. 5). Even though rainfall may
be heavy during May, twice as many of the
prolonged dry periods occurred from January
to June as occurred from July to December (Fig.
6). Frogs begin breeding actively in late February (Townsend and Stewart, 1994) so hatchlings during those extended dry periods could
suffer desiccation. Females are less likely to oviposit after even 24 h without rain (Townsend
and Stewart, 1994). Fewer extended dry periods
and greater frequency of rain in the latter half
of the year can result in an increased amount
of breeding and increased survival rate of juveniles, thereby augmenting high densities following the time of maximum reproduction. Although E. coquihas a broad tolerance to varied
moisture and temperature regimes, it cannot
tolerate extreme water loss; a 30% loss of body
water in adults is fatal (Pough et al., 1983; Beuchat et al., 1984). The lethal dehydration limit
for juveniles has not been determined, but with
their greater surface to volume ratio, long
droughts could have serious consequences
without moist soil and litter for rehydration.
A physical factor related to seasonal changes
and important to frogs is litter depth. Leaf fall
is maximal from April to June as new leaves
emerge. Litter depth changes as litter decays or
is washed down slope during heavy rains. Litter
replaces itself in approximately six months, although less dense leaves deteriorate in six weeks
(LaCaro and Rudd, 1985; Reagan et al., 1982;
pers. obs.). Litter is not only important in providing cover for frogs, especially juveniles, but
it prevents dense fine clay soils from excessive
drying during rainless periods. Majorprey, such
PUERTO RICAN FROGS
as tiny ants (e.g., Solenopsis spp.) and oribatid
mites live in the litter as well (Townsend, 1985;
W. J. Pfeiffer, pers. comm.).
Annual changes in population density were
influenced by rainfall pattern. The maximum
annual rainfall during the study fell during 1979
(474.7 cm; Fig. 4). During that year, the maximum period without rain was 13 d. Likewise,
during 1982, with the maximum number of frogs
counted during the study, there was only one
long dry period (12 d) during the year even
though total rainfall was less than average during 19 yrs (Fig. 4). Years with the most rain
were not the years of greatest population density.
Numbers of frogs remained relatively stable
before 1983 (Fig. 3), after which there was a
significant drop in numbers of all size categories. From 1979 to 1989, adult maxima differed
by five-fold (6 vs. 29, Table 1). I attribute the
drop in numbers, starting in 1983, to a series of
relatively long dry periods. In 1983 the length
of the longest dry period was nearly double that
in the previous five years. During an extended
dry period February to May, 1984, litter moisture declined from 211% to 17% and moisture
in the upper 5 cm of soil declined from 88% to
45% (W. J. Pfeiffer, pers. comm.). From 1984 to
1988, there were 47 periods of five or more days
with no rain or less than 3 mm of rain/day and
10 periods of 11-28 d with little or no rain (Table 1). The forest biota is adapted to frequent
showers. After five days with no rain, shrubs
wilt and the forest litter becomes crispy dry.
Normally during a year there are 30-60 d without showers sufficient to penetrate to the ground,
but they are not contiguous (Briscoe, 1966; Odum
et al., 1970). Scatena (1990) estimated that 3040% of all showers generate no throughfall. I
propose that juveniles cannot survive extensive
drought, and that extended dry periods are
sometimes lethal to adults who are inhibited
from feeding because of desiccation. During
January 1987, 1988, and 1989, we found several
dead frogs, emaciated with empty stomachs, on
the forest floor and in retreats. Woolbright and
Stewart (1987) found 20% of the frogs sampled
in the dry season with empty stomachs whereas
only 2% of frogs examined during the wet season had empty stomachs. The more rainfall on
the previous three days, the fewer frogs with
empty stomachs were found. Changes in population densities that I describe were not limited to the AT. I observed similar declines of E.
coqui populations in six 100 m2 study plots in
other parts of the forest (Stewart [unpubl.]). The
amount of rainfall during the prior three days
also has a significant influence on the amount
of canopy use by these frogs in several parts of
443
the forest (Stewart, 1985) and on the amount of
breeding (Townsend and Stewart, 1994).
These data on E. coqui are timely, important,
and especially critical because Puerto Rico is far
from a continent. Although islands are especially vulnerable to anthropogenic impacts,
and Puerto Rico is no exception, its biota in the
montane preserves should be less affected by
regional environmental pollutants, such as acid
rain, than most continental sites where such
impacts are being shown to affect amphibian
declines. Puerto Rico lies in an airshed where
the northeastern flow of air comes from the
broad reaches of the Atlantic Ocean. Atmospheric effects would be either global or locally
generated.
The year 1982-1983 was an extremely severe
El Nifio Southern Oscillation event in the Pacific followed by an Atlantic La Nifia in 1984
(Philander, 1989). Another El Nifio event occurred in 1987 followed by an Atlantic La Nifia
in 1988, a year of unusual heat and drought in
North America. Those events may have influenced rainfall patterns in Puerto Rico as well.
Prolonged droughts have been implicated in
population oscillations and extinction of several continental anuran populations and species
(e.g., Corn and Fogleman, 1984; Caldwell, 1987;
Crump et al., 1992; Dodd, 1992; Donnelly and
Guyer, 1994; Pounds and Crump, 1994). Caldwell (1987), Corn and Fogleman (1984), Pechman et al. (1991), and Kagarese Sherman and
Morton (1993) found drying of ponds in some
years to be a major factor producing large year
to year population fluctuations in pond breeding amphibians. Pounds and Crump (1994) suggest alterations in patterns of rainfall and temperature as possible reasons for the disappearance and decline of montane frogs in Costa Rica.
For species with short life spans, years with
reduced recruitment can have a substantial impact on population size.
I know of no other comparable long-term
population study of terrestrial breeding anurans for comparison with E. coqui,a subtropical
island species. However, studies of anoline lizards provide comparative information regarding seasonal and annual population fluctuations. Gorman and Licht (1974) found that temperature was the main factor influencing seasonal reproductive cycles in several species of
Puerto Rican anoline lizards. Although low
temperatures influence calling and breeding in
the coqui, both nightly and seasonally (Pough
et al., 1983; Stewart, 1985; Townsend and Stewart, 1994), there is no evidence that annual temperatures have changed during the period of
this study. Andrews and Rand (1982) and Andrews (1991) found populations of Anolis limifrons in Panama over 10-yr and 20-yr periods to
444
MARGARETM. STEWART
fluctuate largely with length of the dry season
and amount of rainfall that may regulate food
supply and influence predation. Major fluctuations in population density of E. coqui from
year to year at El Verde are associated with rainfall as expressed in periods without rain.
All-night Activity.-Nocturnal activity observations confirmed that 2000 to 2100 h were indeed the periods of maximal activity. Numbers
of visible adults declined little during the night;
most remained out to take advantage of foraging opportunities (Pough et al., 1983; Woolbright, 1985). Because of the small size of juveniles, returning to the litter early in the night
protects them from both desiccation and predation. Their stomachs are filled early in the
evening (Townsend, 1985). The decline in spiders visible during the night indicates that they
too have physiological or foraging constraints
as do juvenile frogs.
Other Species of Frogs.-Other frog species in
the AT also showed declines following 1984.
Eleutherodactylusportoricensis,a sibling species
of E. coqui, is adapted to cool moist conditions
(Beuchat et al., 1984). It calls during cooler nights
when E. coquiis silent. Abundant in and around
the study site from 1978, its numbers were
greatly reduced from 1985 to 1988 when I found
it only at higher elevations and in moist ravines.
Eleutherodactyluswightmanaewas heard rarely in
the area in 1985 and 1986. It increased in 1987
only to disappear again after Hurricane Hugo.
Although not present in the AT, other species
in eastern Puerto Rico declined or disappeared
during these years of extended dry periods. I
observed the range of E. richmondi,that lives
under and around boulders, and was common
around El Verde near my study site, contract to
higher elevations during the latter 1980s. Conditions during the mid-1980s became less favorable to those species, including E. portoricensis, that prefer more moisture. Eleutherodactylus jasperi, the live-bearing bromeliad-dwelling species from the Cayey Mountains with
limited range, disappeared completely during
that time (R. Thomas, R. Joglar, pers. comm.).
Predators.-Both vertebrates and invertebrates prey on coquies. Therefore, frog populations would decline rapidly if there were not
constant recruitment. Crab spiders sit on upper
surfaces of leaves of understory vegetation as
do juvenile frogs and spider populations track
those of the frogs (Formanowicz et al., 1981,
Townsend, 1985). Spider population highs occurred during the latter half of the year when
juvenile frogs were most dense. Spider population maxima lagged behind frog population
maxima so that a marked decrease in spider density occurred in 1986, two years after frogs decreased. Tarantulas were last seen in the plot
during 1985. No Phrynus longipeswas seen during 1986 and only once in January 1987. Neither
has been seen since.
HurricaneEffects.-Hurricane Hugo had a major effect on the forest and its fauna (Walker,
1991; Woolbright, 1991). In addition to the direct effects of habitat disturbance, an extended
period of 28 d without rain in November and
December following the hurricane may have
caused the local disappearence of species that
are intolerant of the combined effect of drought
and accompanying high temperatures. The major change in E. coqui populations was a manyfold drop in juveniles and an increase in adults
both in the AT and in larger plots monitored
by Woolbright (1991). After Hurricane Hugo,
numbers of adults attained higher levels than
in the five years prior to the hurricane. Decrease
in numbers of juveniles probably resulted from
severe droughts that followed the hurricane
(Table 1). Litter increased dramatically as the
felled canopy limbs dropped their leaves. With
the loss of the canopy, temperatures increased
near the forest floor, understory vegetation
flourished, and insects were noticably more
dense. Increased food and somewhat higher
temperatures were no doubt desirable for adults,
though less predictable rainfall and higher temperatures may have been lethal to juveniles, too
small to tolerate the warmer, dryer conditions.
Abundant litter provided ample retreat sites for
adults. The species that prefer cool moist conditions, such as E. portoricensis,disappeared almost completely from the area and are just beginning to be heard again at El Verde. The small
E. wightmanae likely had problems similar to
juvenile coquies after the hurricane. Its populations, although not yet in the AT, are recovering at nearby sites.
Predator populations also crashed, and are
just now beginning to reappear. The disappearance of spiders following the hurricane indicates that spiders were either physiologically
intolerant of dry conditions, dependent on small
frogs as a major food source, or both. The direct
correspondence of spider populations with those
of frog populations suggests physiological determinants in density changes for both predator
and prey.
Rainfall is a powerful determinant of frog
activity. My study shows that for E. coqui and
other congeneric species, it is the distribution
of rainfall that significantly influences population densities. Rather than total monthly or
annual rainfall, it is prolonged dry periods that
have a major impact on E. coqui, especially juveniles.
Acknowledgments.-I thank R. B. Waide and
A. Estrada of the Center for Energy and Envi-
PUERTO RICAN FROGS
ronment Research of the University of Puerto
Rico for permission to use facilities of the El
Verde Field Station. A. R. Figueroa (Dept. Natural Resources, Commonwealth of Puerto Rico)
and C. Noble (U.S. Forest Service) kindly issued
permits for our work in the forest. For field
assistance I thank K. Barbehenn, P. Bishop, D.
Bishop, C. Crines, D. Falls, C. Farmer, M. Flynn,
R. Gonser, P. Gutierrez, U. Grafe, J. Hanken, D.
Hencha, R. Joglar, S. Kuhnholz, J. Lasher, N.
Humphrey, G. Martin, B. Milne, G. Preston, S.
Rand, G. Rapp, D. Reagan, R. Roca, N. Sapio, E.
Smith, T. Toklar, K. Townsend, D. Townsend,
B. Verbeck, J. Wilson, and L. Woolbright. K.
Townsend and A. Estrada assisted with plant
identifications. A. Estrada and E. C. Melendez
provided rain data. M. Bowerman, S. Newell,
and J. Rubinoff assisted with data compilation.
G. Martin gave statistical advice. I am especially
grateful to Karyn and Dan Townsend and Larry
Woolbright for their insights about coqui biology, for making so many counts in the transect in my absence, and for suggestions on this
manuscript. I also thank Robin Andrews and
Bob Waide for many helpful comments on the
manuscript. Partial funding was provided by
NSF DEB 77-21349 (to F. H. Pough, M. M. Stewart, and P. Brussard), Oak Ridge Institute for
Science and Education, State University at Albany Faculty Grant-in-Aid, The State University of New York United University Professions
Experienced Faculty Travel Award, and the
Center for Energy and Environment Research.
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