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Population Decline of the Jambato Toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador

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The Jambato Toad, Atelopus ignescens, is endemic to montane forests, inter-Andean valleys, and paramos in Ecuador. Although formerly abundant and widely distributed, the species has not been recorded in nature since 1988. To determine its population status, data from intensive surveys in 1999-2001 are compared with those from 1967 and 1981. Presence-absence data from several localities also are reported. Temperature and precipitation between 1891 and 1999 were analyzed to determine whether these correlate with population trends. Atelopus ignescens was abundant in 1967 at Paramo de Guamani (47 individuals recorded in 120 pers/min) and in 1981 at Paramo del Antisana (up to 0.75 individuals/m(2)). In the 1999-2001 surveys, A. ignescens was absent despite considerably higher survey efforts. The presence-absence data at several localities also indicate a dramatic decline. Before 1988, A. ignescens was present during 64% of the visits to sites throughout its range. After 1988, A. ignescens was absent at all sites. The results strongly suggest that A. ignescens is extinct. Climatic data show that 1987, the year previous to the last record of A. ignescens, was particularly warm and dry. The reasons for the decline in pristine areas remain unclear, although the available information suggests that a combination of factors such as pathogens and unusual weather conditions may have played an important role.
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Journal of Herpetology, Vol. 37, No. 1, pp. 116–126, 2003
Copyright 2003 Society for the Study of Amphibians and Reptiles
Population Decline of the Jambato Toad Atelopus ignescens
(Anura: Bufonidae) in the Andes of Ecuador
S
ANTIAGO
R. R
ON
,
1,2
W
ILLIAM
E. D
UELLMAN
,
3,4
L
UIS
A. C
OLOMA
,
1
AND
M
ART
I
´
N
R. B
USTAMANTE
1
1
Museo de Zoologı´a, Centro de Biodiversidad y Ambiente, Departamento de Ciencias Biolo´gicas,
Pontificia Universidad Cato´ lica del Ecuador, Apartado Postal 17-01-2184, Quito, Ecuador
3
Natural History Museum and Biodiversity Research Center, and Department of Ecology and Evolutionary Biology,
University of Kansas, Lawrence, Kansas 66045-7561, USA; E-mail: duellman@ku.edu
A
BSTRACT
.—The Jambato Toad, Atelopus ignescens, is endemic to montane forests, inter-Andean valleys,
and paramos in Ecuador. Although formerly abundant and widely distributed, the species has not been
recorded in nature since 1988. To determine its population status, data from intensive surveys in 1999–2001
are compared with those from 1967 and 1981. Presence-absence data from several localities also are reported.
Temperature and precipitation between 1891 and 1999 were analyzed to determine whether these correlate
with population trends. Atelopus ignescens was abundant in 1967 at Paramo de Guamanı´ (47 individuals
recorded in 120 pers/min) and in 1981 at Paramo del Antisana (up to 0.75 individuals/m
2
). In the 1999–2001
surveys, A. ignescens was absent despite considerably higher survey efforts. The presence-absence data at
several localities also indicate a dramatic decline. Before 1988, A. ignescens was present during 64% of the
visits to sites throughout its range. After 1988, A. ignescens was absent at all sites. The results strongly
suggest that A. ignescens is extinct. Climatic data show that 1987, the year previous to the last record of A.
ignescens, was particularly warm and dry. The reasons for the decline in pristine areas remain unclear,
although the available information suggests that a combination of factors such as pathogens and unusual
weather conditions may have played an important role.
R
ESUMEN
.—El sapo jambato, Atelopus ignescens es ende´ mico de bosques montanos, valles interandinos, y
pa´ ramos del Ecuador. A pesar de que anteriormente era abundante y ampliamente distribuido, A. ignescens
no ha sido registrado en la naturaleza desde 1988. Para establecer su estado poblacional, monitoreos inten-
sivos llevados a cabo entre 1999–2001 fueron comparados con muestreos efectuados en 1967 y 1981. Datos
de presencia-ausencia en varias localidades tambie´n fueron considerados. La temperatura y precipitacio´n
entre 1891–1999 fue analizada para encontrar correlaciones con tendencias poblacionales. Atelopus ignescens
era abundante en 1967 en Pa´ramo de Guama´ (47 individuos registrados en 120 pers/min) y en 1981 en
Pa´ ramo del Antisana (hasta 0.75 individuos/m
2
). En los monitoreos 1999–2001 A. ignescens estuvo comple-
tamente ausente a pesar de que hubo un esfuerzo de muestreo considerablemente mayor. Los datos de
presencia-ausencia en varias localidades tambie´ n sugieren una declinacio´n drama´tica. Antes de 1988, A.
ignescens estuvo presente en el 64% de las visitas a localidades a lo largo de su rango. Luego de 1988, estuvo
ausente en todos los sitios. La informacio´n combinada sugiere que A. ignescens esta´ extinto. Los datos
clima´ ticos muestran que 1987, el an˜o previo al u´ltimo registro de A. ignescens, fue inusualmente ca´lido y
seco. Las razones para la declinacio´ n en a´ reas no disturbadas no esta´n claras. Sin embargo la evidencia
disponible sugiere que factores como la accio´n de pato´ genos y condiciones clima´ticas inusuales pueden
haber jugado un rol importante.
During the last two decades, several declines
and extinctions of populations and species of
amphibians have been reported worldwide
(Barinaga, 1990; Blaustein and Wake, 1990; Wy-
man, 1990; Tyler, 1991; Wake, 1991; Vial and
Saylor, 1993; Drost and Fellers, 1996; Lips, 1999;
Young et al., 2001). As in other groups of organ-
isms, some of these extinctions have been the
2
Present address: Texas Memorial Museum and De-
partment of Integrative Biology, University of Texas,
Austin, Texas 78712, USA.
4
Corresponding Author.
consequence of habitat destruction. However, a
unique feature of this global amphibian diver-
sity crisis is that it also has affected species that
lived in apparently undisturbed natural areas.
Research on causes for amphibian declines sug-
gests that there are several factors acting around
the world. Some of these are (1) epidemic dis-
eases (e.g., Blaustein et al., 1994b; Berger et al.,
1998; Lips, 1998); (2) unusual weather patterns
(e.g., Pounds and Crump, 1994; Pounds et al.,
1999); (3) introduced species (e.g., Drost and
Fellers, 1996; Knapp and Matthews, 2000); and
(4) ultraviolet radiation (e.g., Blaustein et al.,
1994a; Broomhall, et al., 2000).
117ATELOPUS POPULATION DECLINE IN ECUADOR
F
IG
. 1. Andean region of Ecuador showing distri-
bution of Atelopus ignescens based on locality data for
specimens deposited in Field Museum of Natural His-
tory, Museo de Zoologı´a Pontificia Universidad Cato´-
lica del Ecuador, Museo de Historia Natural Gustavo
Orce´ s, Museum of Comparative Zoology Harvard
University, Museum of Zoology University of Michi-
gan, Museum of Vertebrate Zoology University of Cal-
ifornia, Natural History Museum University of Kan-
sas, and Natural History Museum of Los Angeles
County. Because of the close proximity of many sites,
the number of dots does not represent all of the lo-
calities. The stars are the locations of the weather sta-
tions that provided information for climate analyses.
Arrows show localities for population surveys: (1) Pa-
ramo de Guamanı´, and (2) Paramo del Antisana (see
text for details).
Changes in climate can influence population
dynamics of amphibians (e.g., Heyer et al., 1988;
Beebee, 1995; Blaustein et al., 2001). Extended
periods of unusual low precipitation and high
temperatures may increase mortality rates and
reduce recruitment (Stewart, 1995). Water avail-
ability is influenced by temperature because
heat generates evaporative water loss through
the skin. Many authors have investigated rela-
tionships between amphibian declines and ex-
treme weather or climate (e.g., Corn and Fogel-
man, 1984; Heyer et al., 1988; Osborne, 1989;
Pounds and Crump, 1994; Beebee, 1995; Don-
nelly and Crump, 1998; Pounds et al., 1999;
Blaustein et al., 2001). However, the cause-and-
effect linkage between weather changes and
amphibian declines have not been explored.
Population declines in amphibians in Ecuador
have been reported since the early 1990s (Vial
and Sailor, 1993; Coloma, 1995, 1996, 2002; Steb-
bins and Cohen, 1995; Lo¨ tters, 1996; Coloma et
al., 2000). These reports have been based on un-
successful efforts to find species in their natural
range by several biologists since the mid-1980s.
Unfortunately, these observations have not been
based on standardized survey techniques, and
for some species and regions, the information is
scant and inconclusive. Such deficiencies in the
data are the most significant obstacle that con-
servationists face in their attempts to delineate
programs to protect endangered species of am-
phibians in Ecuador.
Existing evidence suggests that populations
of at least 25 species of frogs may have declined
in Ecuador (Ron et al., 2000). The greatest num-
ber of species affected belong to the genus Ate-
lopus (Ron et al., 2000); of 18 species of Atelopus
known from Ecuador (Coloma and Quiguango,
2000; Coloma, 2002), 11 apparently have de-
clined during the last 15 years (Ron et al., 2000).
The terrestrial, diurnal toads of the genus Ate-
lopus commonly are associated with streams,
where females deposit eggs and tadpoles de-
velop (Reproductive Mode II, as defined by
Duellman and Trueb, 1994). Habitats of these
toads range from lowland tropical rain forests
to paramos at elevations as high as 4500 m (Lo¨t-
ters, 1996). Atelopus probably is the most spe-
cious genus of toads (family Bufonidae) in the
Neotropical region (Lo¨tters, 1996). The genus is
primarily montane; only 21 of the nearly 70 spe-
cies (Frost, 2000) have populations below 1000
m. Species have restricted areas of distribution
with high regional endemism (Lo¨tters, 1996).
Until the 1980s, one of the most conspicuous
anurans in the highlands of Ecuador was Ate-
lopus ignescens, a diurnal species easily observed
moving slowly on the ground. This species is
endemic to Ecuador and inhabits inter-Andean
valleys and montane forests and paramos be-
tween 2800 and 4200 m (Coloma et al., 2000).
Its latitudinal range (Fig. 1) encompasses Prov-
incia de Imbabura in the north to Provincias del
Chimborazo and Bolı´var in the south (Coloma,
1997; Coloma et al., 2000). Anecdotal informa-
tion suggests that A. ignescens was abundant
throughout most of its range (see Discussion).
Despite its former abundance and extensive
geographic range, no records (published or un-
published) or collected specimens of the species
exist after 1988 (Ron et al., 2000). The absence
of records is puzzling in areas without evident
signs of habitat degradation.
Herein, we summarize and analyze data from
the literature, records in natural history muse-
ums, herpetologistsfield notes, and population
surveys, to assess the magnitude of population
declines of A. ignescens in the Andes of Ecuador.
Additionally, we analyze weather information
within the distribution range of A. ignescens to
118 S. R. RON ET AL.
T
ABLE
1. Abundance of Atelopus ignescens during diurnal visual encounter surveys made at Paramo de
Guamanı´ (1967–2001) and Ingaloma (1968). Relative abundance is expressed as individuals registered per
person per minute of search (ind/pers/min).
Date Locality Season
Surveye d
area (m)
Surveye d
time
(pers/min)
Absolute
abundance
(number of
individuals
recorded)
Relative
abundance
(ind/pers/
min)
Relative
abundance
(ind/m
2
)
26 March 1967
16 August 1968
13 March 2000
13 March 2000
15 April 2000
15 April 2000
15 April 2000
15 April 2000
15 April 2000
Guamanı´
Ingaloma
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
wet
wet
wet
wet
wet
wet
wet
wet
wet
?
?
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
120
240
60
120
60
60
60
60
60
47
194
0
0
0
0
0
0
0
0.38
0.81
0
0
0
0
0
0
0
?
?
0
0
0
0
0
0
0
18 April 2000
18 April 2000
18 April 2000
18 April 2000
1 May 2000
1 May 2000
26 Nov. 2000
26 Nov. 2000
26 Nov. 2000
26 Nov. 2000
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
wet
wet
wet
wet
wet
wet
dry
dry
dry
dry
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
60
60
60
60
60
60
75
75
75
75
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
identify correlates between population declines
and changes in weather patterns.
M
ATERIALS AND
M
ETHODS
Population Surveys.—Changes in relative abun-
dance of A. ignescens were examined at La Vir-
gen at Paramo de Guamanı´ (78
8
12
9
10.5
0
W,
0
8
19
9
52.3
0
S, 4020 m, Reserva Ecolo´gica Cayam-
be-Coca) and Rı´o Antisana at Paramo del An-
tisana (78
8
12
9
8
0
W, 0
8
29
9
41.6
0
S, 4202 m, Reserva
Ecolo´gica Antisana). Localities were chosen be-
cause they were sampled several years before
population declines were evident. Both localities
are in Provincia del Napo in the Cordillera Ori-
ental. The vegetation at both localities is Her-
baceous Paramo, dominated by grasses Cala-
magrostis spp. and Festuca spp. (Valencia et al.,
1999).
At Paramo de Guamanı´, a diurnal visual en-
counter survey (VES) was done in March 1967
by W. E. Duellman and L. Trueb. Relative abun-
dance from that survey was compared with rel-
ative abundance from 17 diurnal VES carried
out between March and November 2000 by M.
Bustamante, P. Espinosa, L. Lo´ pez, A. Merino,
and S. Ron. At Paramo del Antisana, four 100
3
2 m diurnal transect surveys were done in
June 1981 by J. Black (Black, 1982). Two of the
four transects were along a stream and two
along a trail. Relative abundance from those
surveys was compared with 24 diurnal transect
surveys carried out between July 1999 and Jan-
uary 2001 at Paramo del Antisana by M. Bus-
tamante, L. Coloma, J. Guayasamı´n,A.Merino,
and S. Ron. The transects in 1999–2001 were set
up along a stream and were carried out by one
person. Transect sizes are shown in Tables 1
and 2.
Atelopus ignescens was last recorded in nature
in 1988 (Coloma et al., 2000; Ron et al., 2000).
To test whether the presence or absence of A.
ignescens at six localities (Laguna de Mojanda,
Oyacachi, Papallacta, Paramo de Guamanı´, Pa-
ramo del Antisana, and Volca´ n Cotopaxi) is in-
dependent from collection time (before 1988/af-
ter 1988), Fisher’s exact test for independence
was applied (
a5
0.05). Presence/absence data
were obtained from herpetologists’ field notes.
Climatic Analyses.—Extreme dry and/or
warm conditions can produce hydric stress that
can affect amphibians at the individual, popu-
lation, and community levels (Donnelly and
Crump, 1998). To identify the occurrence of
warm and dry periods, we analyzed climate in-
formation from two weather stations within the
range of A. ignescens: (1) Izobamba, Provincia de
Pichincha, (78
8
33
9
11
0
W, 0
8
21
9
45
0
S, 3058 m) and
(2) Astronomical Observatory of Quito, Provin-
cia de Pichincha, (78
8
29
9
59.9
0
W, 0
8
12
9
59.9
0
S, 2800
m). Airline distance between the two stations is
17 km (Fig. 1).
Climatic data from Quito include 90 years of
annual precipitation and mean annual temper-
atures from 1891 and 1984. There was a signif-
119ATELOPUS POPULATION DECLINE IN ECUADOR
T
ABLE
2. Abundance of Atelopus ignescens during
transect surveys made at Paramo del Antisana. 1864
data from Jime´nez de la Espada (1875); 1981 data from
Black (1982).
Date Season
Surveye d
area (m)
Absolute
abundance
(number of
individuals
recorded)
Relative
abun-
dance
(ind/m
2
)
Dec. 1864
3 June 1981
3 June 1981
9 June 1981
9 June 1981
3 July 1999
3 July 1999
3 July 1999
3 July 1999
3 July 1999
3 July 1999
3 July 1999
3 July 1999
dry
wet
wet
wet
wet
dry
dry
dry
dry
dry
dry
dry
dry
?
100
3
2
100
3
2
100
3
2
100
3
2
200
3
2
200
3
2
200
3
2
200
3
2
100
3
2
100
3
2
100
3
2
100
3
2
‘‘thousands’’
5
84
84
150
0
0
0
0
0
0
0
0
?
0.025
0.42
0.42
0.75
0
0
0
0
0
0
0
0
29 April 2000
29 April 2000
29 April 2000
29 April 2000
29 April 2000
24 June 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
8 Aug. 2000
25 Nov. 2000
27 Jan. 2001
wet
wet
wet
wet
wet
wet
dry
dry
dry
dry
dry
dry
dry
dry
wet
dry
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
500
3
2
250
3
2
250
3
2
250
3
2
250
3
2
250
3
2
250
3
2
250
3
2
250
3
2
500
3
2
500
3
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
icant linear relationship in annual precipitation
between Quito and Izobamba (F
5
31.04, P
,
0.0001). The relationship also was significant for
mean annual temperature (F
5
65.67, P
,
0.0001). The equations of both linear regressions
were used to predict annual precipitation and
mean annual temperature in Quito from 1985 to
1999 (data for this period were not available).
Standardized values for annual precipitation
and for mean annual temperature were ob-
tained to determine what years had the greatest
difference, expressed in standard deviation
units, between temperature and precipitation
(i.e., the years that were simultaneously warm-
est and driest).
Climate information from Izobamba includes
a shorter period (1962–1999) but is more de-
tailed. The variables considered at Izobamba are
(1) annual precipitation, (2) mean annual tem-
perature, (3) number of dry days (precipitation
5
0) per year, (4) monthly precipitation, and (5)
mean monthly temperature. Mean annual and
monthly temperatures are the average of daily
temperatures. Daily temperatures are the aver-
age between maximum and minimum daily
temperatures.
R
ESULTS
Population Surveys.—Relative abundance of A.
ignescens decreased drastically at Paramo de
Guamanı´ and Paramo del Antisana. At Paramo
de Guamanı´ in 1967, relative abundance was
0.38 ind/pers/min (individuals registered per
person per minute of search) during one VES.
In 2000, relative abundance was 0 ind/pers/min
in 17 VES (Table 1). In 1967, 120 pers/min,
yielded 47 individuals, whereas in 2000, A. ig-
nescens was completely absent despite a search
effort 9.5 times higher (1140 pers/min).
In surveys at Paramo del Antisana in 1981,
Atelopus ignescens relative abundance was mean
(
6
SE)
5
0.34 ind/m
2
(0.025–0.75, N
5
4). In
1999–2001 relative abundance was 0 (N
5
24,
Table 2). In 1981, 323 individuals were recorded
during four transect surveys. In 1999–2001, A.
ignescens was absent during 24 transect surveys
(1465 pers/min; Table 2). No tadpoles or egg
masses of A. ignescens were observed during the
1999–2001 surveys. At both localities during the
1999–2001 surveys, a total search effort of 2665
pers/min yielded no A. ignescens.
Presence or absence was not independent of
time of visit (before 1988/after 1988) to five lo-
calities (Fisher’s exact test P
,
0.0001). Between
1967 and 1987, A. ignescens was present in nine
of 14 visits; between 1988 and 2001, A. ignescens
was present in one (1988) out of 30 visits (Table
3). Presence or absence was not independent of
time of visit to Paramo de Guamanı´ (Fisher’s
exact test P
5
0.002). From 1967 to 1987, A. ig-
nescens was present in five of eight visits, where-
as from 1988 to 2001, it was absent in all 15
visits.
Climatic Analyses.—Annual precipitation and
mean annual temperatures at Izobamba and
Quito are shown in Figures 2 and 3. Mean an-
nual precipitation at Izobamba was 1422.03 mm
(SD
5
239.95, N
5
38); at Quito it was 1230.1
mm (SD
5
214.7, N
5
105). At Izobamba, the
years with the least precipitation were 1985
(983.6 mm), 1987 (994.6 mm), and 1992 (1027
mm). At Quito, the years with the least precip-
itation were 1926 (692.2 mm), 1985 (882.3 mm),
and 1987 (890.4 mm).
Mean annual temperature at Izobamba was
11.33
8
CSD
5
0.62, N
5
38); at Quito it was
13.4
8
C (SD
5
0.7, N
5
105). At Izobamba, the
warmest years were 1998 (x¯ temperature
5
12.56
8
C), 1987 (x¯ temperature
5
12.48
8
C), and
1997 (x¯ temperature
5
12.26
8
C). At Quito, the
warmest years were 1998 (x¯ temperature
5
120 S. R. RON ET AL.
T
ABLE
3. Presence/absence of Atelopus ignescens at
six localities in Andean Ecuador.
Date Locality Occurrence
26 March 1967
1 Dec. 1983
1 March 1984
1 June 1984
20 Oct. 1984
1 May 1985
1 Dec. 1985
1 May 1986
8 July 1986
1 Oct. 1986
1 June 1987
5 Dec. 1987
1 Dec. 1987
13 Dec. 1987
30 March 1988
Guamanı´
Volca´n Cotopaxi
Volca´n Cotopaxi
Volca´n Cotopaxi
Guamanı´
Papallacta
Papallacta
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Laguna de Mojanda
Guamanı´
Oyacachi
present
absent
absent
present
present
present
present
present
present
absent
present
absent
present
absent
present (last
record)
14 April 1988
1 May 1988
1 June 1988
26 June 1988
21 June 1989
5 July 1989
12 July 1991
17 Aug. 1991
1 Oct. 1991
18 May 1993
25 Nov. 1993
1 Sept. 1994
30 Jan. 1999
21 April 1999
3 July 1999
2 Oct. 1999
11 Nov. 1999
13 March 2000
Papallacta
Guamanı´
Guamanı´
Guamanı´
Guamanı´
Cotopaxi
Cotopaxi
Papallacta
Cotopaxi
Guamanı´
Papallacta
Guamanı´
Guamanı´
Cotopaxi
Antisana
Laguna de Mojanda
Cotopaxi
Guamanı´
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
16 March 2000
15 April 2000
18 April 2000
29 April 2000
1 May 2000
24 July 2000
1 Oct. 2000
26 Nov. 2000
27 Jan. 2001
7 Dec. 2001
7 Dec. 2001
Guamanı´
Guamanı´
Guamanı´
Antisana
Guamanı´
Antisana
Guamanı´
Guamanı´
Antisana
Papallacta
Guamanı´
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
F
IG
. 2. Mean annual temperature and annual pre-
cipitation at Izobamba, Provincia del Pichincha, Ec-
uador. Note that the year before 1988, when Atelopus
ignescens was recorded in the field for the last time,
weather was unusually warm and dry.
F
IG
. 3. Mean annual temperature (squares) and
annual precipitation (diamonds) at Quito, Provincia
del Pichincha, Ecuador. The smooth line shows world
mean annual temperature (from Goddard Institute for
Space Studies, 2002). Note that the year before 1988,
when Atelopus ignescens was recorded in the field for
the last time, weather was unusually warm and dry.
15.4
8
C), 1987 (x¯ temperature
5
15.3
6
C), and
1997 (x¯ temperature
5
15.1
8
C).
At Quito, between 1891 and 1999, the warm-
est decades were 1991–1999 (x¯ annual temper-
ature
5
14.81
8
C, SD
5
0.39, N
5
9) and 1981–
1989 (x¯ annual temperature
5
14.47d
8
,SD
5
0.49, N
5
10). The 1981–1990 decade was sig-
nificantly warmer than all previous decades (all
P-values for t-tests
,
0.001). The 1990–1999 pe-
riod also was significantly warmer than all pre-
vious decades (all P-values for t-tests
,
0.001)
except 1981–1990 (t
52
1.66, P
5
0.115).
There is a significant positive correlation be-
tween year and temperature in Quito (Spear-
man’s Rho
5
7.98, P
,
0.0001). The increase in
mean annual temperature is also evident in Fig-
ures 2 and 3. Mean annual temperatures after
1985 are significantly higher from those be-
tween 1891 and 1907 (t
52
13.118, one tail P
,
0.0001). Between 1891 and 1907, x¯ mean annual
temperature
5
12.764 (SD
5
0.418). Between
1986 and 1999, x¯ mean annual temperature
5
14.771 (SD
5
0.391).
At Quito, between 1891 and 1999, the driest
decades were 1951–1960 (mean annual precipi-
tation
5
1095.4 mm, SD
5
117.9, N
5
10) and
1931–1940 (mean annual precipitation
5
1162.3
mm, SD
5
117.9, N
5
10). At Quito, the years
121ATELOPUS POPULATION DECLINE IN ECUADOR
F
IG
. 4. Difference between standardized values of
temperature and precipitation at Quito. High values
represent climate conditions simultaneously warm
and dry. Note that of 90 years of climate records, 1987
shows the highest value.
F
IG
. 5. Mean monthly temperature and precipita-
tion for 1987 compared with mean values for 1962–
1999 at Izobamba, Provincia del Pichincha, Ecuador.
T
ABLE
4. Wilcoxon signed rank test values for the
comparison between average monthly precipitation
and average monthly temperature between 1962 and
1999 with monthly precipitation and monthly tem-
perature for the years 1981–1988; weather data from
Izobamba, Provincia del Pichincha, Ecuador. Bold
characters show significant differences.
Monthly precipitation
ZP
Monthly temperature
ZP
1981
1982
1983
1984
1985
1986
1987
1988
2
1.02
2
0.86
2
0.23
2
0.47
2
1.88
2
0.16
2
2.35
2
1.96
0.308
0.388
0.814
0.638
0.06
0.875
0.019
0.05
2
3.06
2
2.27
2
2.59
2
1.72
2
0.71
2
2.35
2
3.06
2
1.73
0.002
0.023
0.009
0.086
0.48
0.019
0.002
0.084
F
IG
. 6. Number of dry days (precipitation
5
0) at
Izobamba, Provincia del Pichincha, Ecuador. Sixty
days of data are missing from 1996.
with the highest difference between the stan-
dardized values of mean annual temperature
and annual precipitation were 1987 (4.125 SD
units) and 1994 (3.466 SD units; Fig. 4).
At Izobamba, average monthly precipitation
from 1962 to 1999 was significantly different
from monthly precipitation in 1987 and 1988
(Table 4). Average monthly temperatures from
1962 to 1999 were significantly different from
those in 1981, 1982, 1983, 1986, and 1987 (Table
4). The combined weather information shows
that 1987 (the year before A. ignescens was re-
corded for the last time) was unusually warm
and dry (Figs. 2–3, Table 4). Monthly precipita-
tion and mean temperature for 1987 are shown
in Figure 5.
The mean number of dry days per year at Izo-
bamba was 149.51 (SD
5
24.42, N
5
35; Fig. 6).
The years with the most dry days were 1985
(192 days) and 1967 (181 days). Years with low
number of dry days are associated with El Nin˜o
events (e.g., 1982, 1988, 1998). There are not ev-
ident abnormalities in the number of dry days/
year between 1962 and 1999 (Fig. 6).
D
ISCUSSION
There is strong evidence of a drastic popula-
tion decline of A. ignescens. This can be inferred
from (1) the population data presented, (2) an-
ecdotal information indicating that before 1988
A. ignescens was an abundant species (see be-
low), and (3) the absence of records after 1988.
It is unlikely that the complete absence of re-
cords during the 1999–2000 population surveys
is an artifact of unfavorable environmental con-
ditions. The surveys in 1999–2001 encompassed
a longer period and a wider set of environmen-
tal conditions than those in 1967 and 1981. In
spite of the high search effort (2665 pers/min),
the absence of A. ignescens is a clear indication
of a severe population decline at the surveyed
localities.
Anecdotal information shows that A. ignescens
formerly was abundant. In December 1864, the
Spanish naturalist M. Jime´nez de la Espada ob-
served at Paramo del Antisana (Laguna de la
Mica) the occurrence of ‘‘thousands of individ-
uals in the herbaceous and humid prairies close
122 S. R. RON ET AL.
to streams, pools, and lakes’’ (Jime´nez de la Es-
pada, 1875:146). Field parties from the Univer-
sity of Kansas documented high densities of A.
ignescens in the 1960s and 1970s (e.g., 194 indi-
viduals (0.81 ind/pers/min) at Ingaloma, Prov-
incia de Pichincha, 3780 m on 16 August 1968).
At Paramo del Antisana, densities were as high
as 50 individuals/m
2
in 1981 (Black, 1982). Also,
there are reports of mass migrations that re-
sulted in large numbers of individuals smashed
across 1–8 km of highways in Provincia del
Tungurahua and Provincia de Bolı´var in 1958
and 1959 (Peters, 1973). Atelopus ignescens has
been recorded in human disturbed areas, such
as backyards in Quito in 1959 and 1983 and in
Latacunga in 1979 (J. A. Peters, L. A. Coloma,
field notes).
Population data are not available for the pe-
riod 1982–1988, and therefore it is difficult to
determine the timing and rate of the decline.
However, evidence suggests that A. ignescens
was still abundant at some localities between
1984 and 1986. In October 1984, 19 A. ignescens
were collected at Paramo de Guamanı´ (Museo
de Zoologı´a, Pontificia Universidad Cato´ lica del
Ecuador 264–270; Muse´um d’Histoire Naturelle
Geneva 2273.48, 2273.81–82, 2273.84, 2273.86,
2273.88–93, 2273.96). On 15 May 1985, a mass
migration at Paramo del Chimborazo (border
between Provincia de Bolı´var and Provincia de
Tungurahua) left thousands of smashed toads
along 1 km of the Guaranda-Ambato highway
(L. A. Coloma, field notes). On 8 March 1986,
29 A. ignescens were collected at Papallacta
(Provincia de Pichincha, Museo de Historia Nat-
ural Gustavo Orce´s 3261–3289). In August 1986,
64 A. ignescens were collected in Zumbahua
(Provincia de Cotopaxi, Muse´um d’Histoire Na-
turelle Geneva 2385.001–010, 2384.047–100).
The complete absence of records after 1988
indicates that population declines of A. ignescens
have occurred throughout its geographic range.
The absence of records does not seem to be an
artifact of low search effort. A considerable por-
tion of the range of A. ignescens is easily acces-
sible and repeatedly visited by herpetologists.
The available evidence suggests that A. ignes-
cens is extinct. However, the possibility of its
presence in areas of difficult access cannot be
ruled out.
The decline of A. ignescens seems to be part
of a generalized process that has affected sev-
eral species of the genus. Atelopus declines have
been reported from Costa Rica (Lips, 1998),
Panama (Lips, 1999), Venezuela (La Marca and
Lo¨tters, 1997), Ecuador (Ron et al., 2002), and
Peru (Vial and Saylor, 1993). Atelopus is the am-
phibian genus with the most declines reported
from South America. Declines from Andean Ve-
nezuela, Ecuador, and Peru include a total of 43
species, of which 21 are Atelopus (48.8%; Ron et
al., 2002). Possible causes for the population de-
clines of A. ignescens are discussed below.
Habitat Degradation.—During the last two de-
cades, significant portions of the geographic
range of A. ignescens have been modified by hu-
man activities. By 1996, 27.1% of the paramo
and 33.3% of Andean forests had been cleared
in Ecuador (Sierra, 1999). Brandbyge and Holm-
Nielsen (1991) estimated that only 3.5% of na-
tive forest remained in the inter-Andean region.
Habitat degradation in some parts of its range
may be a factor for population declines in A.
ignescens. However, A. ignescens can withstand
some degree of habitat degradation, as seen by
its presence in cities such as Quito and Latacun-
ga.
The most puzzling declines are those that
have occurred in places such as Paramo del An-
tisana and Paramo de Guamanı´, where human-
mediated habitat destruction has been minor.
Both localities are located within protected ar-
eas. Although more detailed habitat analyses
may reveal subtle forms of degradation (e.g.,
chemical contamination), at present it seems un-
likely that habitat destruction is the cause for the
disappearance of A. ignescens in apparently un-
disturbed regions.
Introduced Species.—Presence of introduced
predatory fishes have been identified as a pos-
sible factor linked with declines of several am-
phibian species in many regions (e.g., La Marca
and Reinthaler, 1991; Bro¨nmark and Edenhamn,
1994; Drost and Fellers, 1996; Adams, 1999;
Knapp and Matthews, 2000). Two exotic species
of salmonids (Onchorhynchus mykiss and Salmo
trutta) are present in streams and lakes in the
highlands of Ecuador. Onchorhynchus mykiss is
present in Paramo del Antisana (Laguna de la
Mica) and Paramo de Guamanı´. However, it was
never observed in the streams where the inten-
sive surveys took place.
Although there are no studies on the impact
of salmonid predation on the tadpoles or eggs
of Atelopus, it is reasonable to assume that intro-
duced fishes may have contributed to popula-
tion declines at least in some parts of the dis-
tribution range. However, it is unlikely that sal-
monid predation is the driving cause for the de-
cline of A. ignescens throughout its entire range.
Salmonids have been established in aquatic eco-
systems of Ecuador since the 1950s (R. Barriga,
pers. com.), decades before A. ignescens declines
were evident.
Pathogen Outbreak.—Chytridiomycosis is a
deadly fungus disease that attacks amphibians.
Its presence has been linked to declines in sev-
eral species in Australia (Berger et al., 1998),
Central America (Berger et al., 1998; Lips ,1999;
Young et al., 2001), and Europe (Bosch et al.,
123ATELOPUS POPULATION DECLINE IN ECUADOR
2000), and its has been found in frogs in zoos
in North America (Nichols et al., 1998; Pessier
et al., 1999). The first report of the disease in
South America is from five Ecuadorian species
(Berger et al., 1999; Ron and Merino Viteri,
2000). The species positive for chytridiomycosis
are Atelopus bomolochos, Atelopus sp. (from Prov-
incia del Carchi, Ecuador), Gastrotheca pseustes,
Hyla psarolaima,andTelmatobius niger (Ron and
Merino Viteri, 2000). The last records in the field
of A. bomolochos and Atelopus sp. were in 1994
and 1993, respectively. The first record of chy-
tridiomycosis in Ecuador is from an A. bomolo-
chos collected in Provincia del Can˜ar in 1980.
This indicates that chytridiomycosis was present
in Ecuador several years before the disappear-
ance of highland Atelopus. So far, 89 museum
specimens of A. ignescens have been examined
for chytridiomycosis. All specimens have tested
negative (Merino Viteri, 2001). Of the 89 speci-
mens, 53 were collected after the first record of
the disease: one in 1983, seven in 1984, three in
1985, 29 in 1986, 11 in 1987, and two in 1988
(Merino Viteri, 2001). However, extensive anal-
yses may reveal the presence of chytridiomy-
cosis in A. ignescens. This is a likely scenario be-
cause chytridiomycosis has low host specificity
(Speare and Berger, 2000) and is present in A.
bomolochos and Atelopus sp. Both species are par-
apatric to A. ignescens (Ron and Merino Viteri,
2000).
Five A. bomolochos infected with chytridiomy-
cosis were collected in January 1991. The spec-
imens (Museo de Zoologı´a, Pontificia Universi-
dad Cato´lica del Ecuador 2911, 2913, 2923, 2939,
2949) were examined because when found in
the field they were either dead or evidently un-
healthy and died within a few hours after col-
lection. Similar observations are available for A.
ignescens. In November 1987, three females were
found dead 20 km SE of Latacunga (Provincia
del Cotopaxi) by G. Onore and LAC (Coloma et
al., 2000). The three specimens tested negative
for chytridiomycosis (Merino Viteri, 2001).
A pathogen outbreak during the late 1980s
could have been mediated by favorable environ-
mental conditions (e.g., dry and/or warm cli-
mate; see below). Additional pathological diag-
noses of preserved specimens are needed to un-
derstand the geographic and temporal distri-
bution of chytridiomycosis and other pathogens
within the range of A. ignescens.
Changes in Climate and UV Radiation.—A sharp
increase in mean annual temperature during the
last 15 years is evident within the distribution
range of A. ignescens. Of 90 years of climatic
data analyzed in this study, 1987 has the most
extreme combination of dry and warm condi-
tions (Fig. 4). Concomitantly, in the period 1987–
1989 six species of Atelopus were recorded for
the last time in the Ecuadorian Andes (Ron et
al., 2003). Climate may have affected the toads
directly (by increasing adult mortality and/or
reducing reproductive success) and/or indirect-
ly (e.g., by weakening the immune system facil-
itating pathogen outbreaks). Unusually dry and
warm conditions during 1987 also may have
played a roll in the decline of several species of
frogs in Monteverde, Costa Rica (Pounds and
Crump, 1994; Pounds et al., 1999).
There are an increasing number of reports of
changes in population sizes (including extinc-
tions), reproductive cycles, and distribution
ranges of vertebrates as a consequence of global
warming (e.g., Pounds et al., 1999; Sæther et al.,
2000; Sillett et al., 2000; Wuethrich, 2000). Global
warming has increased worldwide tempera-
tures an average of 0.5
8
C (Hasselmann, 1997).
Our data show that the temperature increase in
the equatorial Andes is four times higher than
the global average increase (approximately 2
8
C
during the last century; Fig. 3). Accordingly,
changes in population sizes in the equatorial
Andes are expected to be more drastic than in
other regions. Extinctions also are predicted to
be more numerous, and the disappearance of
several species of amphibians from the Andes
of Ecuador may be a manifestation of this cli-
matic trend.
An additional factor on the decline A. ignes-
cens may be UV radiation. A number of studies
have demonstrated that UV radiation can affect
amphibian survival, specially during early de-
velopment (e.g., Blaustein et al. 1994a, 1995,
1999; Anzalone et al., 1998; Lizana and Pedraza,
1998). Satellite measurements show that annu-
ally averaged UV-B radiation has increased sig-
nificantly in South America since 1979 (Middle-
ton et al., 2001). According to Middleton et al.
(2001), of 20 sites in Central and South America
where annual UV-B levels were measured be-
tween 1979 and 1998, the site with the highest
values was the one with the highest altitude
(Cordillera de Me´rida at 4000 m in Venezuela).
This site also shows the highest rate of increase
in UV-B when compared to other South Amer-
ican localities (Middleton, 2001). In Cordillera
de Me´ rida, Atelopus oxyrhynchus, Atelopus carbo-
nerensis, Atelopus mucubajiensis,andAtelopus so-
rianoi have declined (La Marca and Lo¨tters,
1997).
Ultraviolet radiation levels are considerably
higher in highlands than at sea level (Blumthal-
er et al., 1997). Atelopus ignescens is a highland
species that must have been exposed to high
levels of UV-B radiation. Increased UV-B radia-
tion may have exceeded the limits of tolerance
of some highland species; further increases
would be expected to result in more adverse ef-
fects on populations.
124 S. R. RON ET AL.
Conclusions.—There has been a severe popu-
lation decline and extinction of the formerly
abundant toad A. ignescens. The causal factors of
the decline need further research, although pos-
sible causes are (1) a pathogen outbreak, (2) un-
usual climate patterns including increased levels
of UV-B radiation, (3) habitat modification, (4)
the presence of exotic predatory salmonid fish-
es, and/or (5) synergistic interactions among
factors.
Acknowledgments.—This investigation was
funded by the Declining Amphibian Popula-
tions Task Force, Earthwatch Institute, and the
Lincoln Park Zoo Neotropical Fund. The Min-
isterio de Medio Ambiente del Ecuador issued
the research permit (049-IC-DFP). G. Romero, G.
Onore, J. M Guayasamı´n,L.E.Lo´pez, P. Mene´n-
dez, A. Merino, S. Padilla, and A. Quiguango
assisted with the fieldwork. WED thanks L.
Trueb for her assistance in the field in 1967;
fieldwork was supported by the Natural History
Museum, the University of Kansas. A. Almen-
da´riz provided information from the Museo de
Historia Natural Gustavo Orce´s database. The
Instituto Ecuatoriano de Climatologı´a e Hidrol-
ogı´a (INHAMI) and the Observatorio Astron-
o´mico de Quito made available climatic infor-
mation. A. Merino provided data on chytridi-
omycosis and compiled climatic information. C.
Graham georeferenced Atelopus ignescens muse-
um records. K. Lips, W. R. Heyer, and an anon-
ymous reviewer provided helpful comments on
earlier versions of the manuscript.
L
ITERATURE
C
ITED
A
DAMS
, M. J. 1999. Correlated factors in amphibian
decline: exotic species and habitat change in west-
ern Washington. Journal of Wildlife Management
63:1162–1171.
A
NZALONE
, C. R., L. B. K
ATS
,
AND
M. S. G
ORDON
.
1998. Effects of solar UV-B radiation on embryonic
development in Hyla cadaverina, Hyla regilla,and
Taricha torosa. Conservation Biology 12:646–653.
B
ARINAGA
, M. 1990. Where have all the froggies
gone? Science 247:1033–1034.
B
EEBEE
, T. J. C. 1995. Amphibian breeding and cli-
mate. Nature 374:219–220.
B
ERGER
, L., R. S
PEARE
,P.D
ASZAK
,D.E.G
REEN
,A.A.
C
UNNINGHAM
,C.L.G
OGGIN
,R.S
LOCOMBE
,M.A.
R
AGAN
,A.D.H
YATT
,K.R.M
C
D
ONALD
,H.B.
H
INES
,K.R.L
IPS
,G.M
ARANTELLI
,
AND
H. P
ARKES
.
1998. Chytridiomycosis causes amphibian mortal-
ity associated with population declines in the rain-
forests of Australia and Central America. Proceed-
ings of the National Academy of Sciences USA 95:
9031–9036.
B
ERGER
, L., R. S
PEARE
,
AND
A. H
YATT
. 1999. Chytrid
fungi and amphibian declines: overview, implica-
tions and future directions. In A. Campbell (ed.),
Declines and Disappearances of Australian Frogs,
pp. 23–33, Environment Australia, Canberra, Aus-
tralian Capital Territory, Australia.
B
LACK
, J. 1982. Los pa´ramos de Antisana. Instituto
Geogra´ fico Militar Revista Geogra´ fica 17:25–52.
B
LAUSTEIN
,A.R.,
AND
D. B. W
AKE
. 1990. Declining
amphibian populations: a global phenomenon?
Trends in Ecology and Evolution 5:203–204.
B
LAUSTEIN
,A.R.,P.D.H
OFFMAN
,D.G.H
OKIT
,J.M.
K
IESECKER
,S.C.W
ALLS
,
AND
J. B. H
AYS
. 1994a.
UV repair and resistance to solar UV-B in amphib-
ian eggs: a link to population declines? Proceed-
ings of the National Academy of Sciences USA 91:
1791–1795.
B
LAUSTEIN
,A.R.,D.G.H
OKIT
,
AND
R. K. O’H
ARA
.
1994b. Pathogenic fungus contributes to amphib-
ian losses in the Pacific Northwest. Biological Con-
servation 67:251–254.
B
LAUSTEIN
, A. R., B. E
DMOND
,J.M.K
IESECKER
,J.J.
B
EATTY
,
AND
D. G. H
OKIT
. 1995. Ambient ultra-
violet radiation causes mortality in salamander
eggs. Ecological Applications 5:740–743
B
LAUSTEIN
,A.R.,P.D.H
OFFMAN
,D.P.C
HIVERS
,J.M.
K
IESECKER
,W.P.L
EONARD
,A.M
ARCO
,D.H.O
L
-
SON
,J.K.R
EASER
,
AND
R. G. A
NTHONY
. 1999.
DNA repair and resistance to UV-B radiation in
western spotted frogs. Ecological Applications 9:
1100–1105.
B
LAUSTEIN
, A. R., L. K. B
ELDEN
,D.H.O
LSON
,D.M.
G
REEN
,T.L.R
OOT
,
AND
J. M. K
IESECKER
. 2001.
Amphibian breeding and climate change. Conser-
vation Biology 15:1804–1809.
B
LUMTHALER
,M.,W.A
MBACH
,
AND
R. E
LLINGER
.
1997. Increase in solar UV radiation with altitude.
Journal of Photochemistry and Photobiology (B: Bi-
ology) 39:130:134.
B
OSCH
, J., I. M
ARTINES
-S
OLANO
,
AND
M. G
ARC
ı´
A
-
P
AR
ı´
S
. 2000. Evidence of Chytrid fungus infection
involved in the decline of the common midwife
toad in protected areas of central Spain. Froglog
40:1.
B
RANDBYGE
,J.
AND
L. B. H
OLM
-N
IELSEN
. 1991. Refo-
restacio´n en los Andes ecuatorianos con especies
natives. CESA. Quito, Ecuador.
B
RO
¨NMARK
,C.,
AND
P. E
DENHAMN
. 1994. Does the
presence of fish affect the distribution of tree frogs
(Hyla arborea)? Conservation Biology 8:841–845.
B
ROOMHALL
, S. D., W. S. O
SBORNE
,
AND
R. B. C
UN
-
NINGHAM
. 2000. Comparative effects of ambient
ultraviolet-B radiation on two sympatric species of
Australian frogs. Conservation Biology 14:420–427.
C
OLOMA
, L. A. 1995. Ecuadorian frogs of the Genus
Colostethus (Anura: Dendrobatidae). Miscellaneous
Publications of the Natural History Museum, Univ.
of Kansas 87:1–72.
. 1996. Systematics, morphology, and relation-
ships of Atelopus (Anura: Bufonidae). In Program
Notes and abstracts of the 39th Annual Meeting of
the Society for the Study of Amphibians and Rep-
tiles, p. 47. Univ. of Kansas, Lawrence.
. 1997. Morphology, Systematics, and Phylo-
genetic Relationships among Frogs of the Genus
Atelopus (Anura: Bufonidae). Unpubl. Ph.D. diss.
Univ. Of Kansas, Lawrence.
. 2002. Two new species of Atelopus (Anura:
Bufonidae) from Ecuador. Herpetologica 58:229–
252.
C
OLOMA
,L.A.,
AND
A. Q
UIGUANGO
. 2000. Anfibios
de Ecuador: lista de especies y distribucio´ n alti-
125ATELOPUS POPULATION DECLINE IN ECUADOR
tudinal. [on line]. Vers. 1.2 (9 Marzo 2000). Museo
de Zoologı´a, Pontificia Univ. Cato´ lica Ecuador. Qui-
to, Ecuador.
,
http://www.puce.edu.ec/Zoologia/
anfecua.htm
.
[Inquiry: 9 October 2000].
C
OLOMA
, L. A., S. L
O
¨TTERS
,
AND
A. W. S
ALAS
. 2000.
Taxonomy of the Atelopus ignescens complex (An-
ura: Bufonidae): designation of a neotype of Ate-
lopus ignescens and recognition of Atelopus exiguus.
Herpetologica 56:303–324.
C
ORN
,P.S.
AND
J. C. F
OGELMAN
. 1984. Extinction of
montane populations of the northern leopard frog
(Rana pipiens) in Colorado. Journal of Herpetology
18:147–152.
D
ONNELLY
,M.A.,
AND
M. L. C
RUMP
. 1998. Potential
effects of climate change on two Neotropical am-
phibian assemblages. Climatic Change 39:541–561.
D
ROST
C. A.,
AND
G. M. F
ELLERS
. 1996. Collapse of a
regional frog fauna in the Yosemite area of the Cal-
ifornia Sierra Nevada, USA. Conservation Biology
10:414–425.
D
UELLMAN
,W.E.,
AND
L. T
RUEB
. 1994. Biology of
Amphibians. John Hopkins Univ. Press. Baltimore,
MD.
F
ROST
, D. R. 2000. Amphibian Species of the World:
An online reference. [on line]. Vers. 2.20 (1 Septem-
ber 2000). American Museum of Natural History,
New York.
,
http://research.amnh.org/herpetolo-
gy/amphibia/index.html
.
[Inquiry: November
2000].
G
ODDARD
I
NSTITUTE FOR
S
PACE
S
TUDIES
. 2002. Sur-
face Temperature Analysis. [on line]. Goddard In-
stitute for Space Studies.
,
http://www.giss.nasa.
gov/data/update/gistemp/
.
[Inquiry: December
2001].
H
ASSELMANN
, H. 1997. Are we seeing global warm-
ing? Science 276:914–915.
H
EYER
, W. R., A. S. R
AND
,C.A.C
ONC¸ALVEZDA
C
RUZ
,
AND
O. L. P
EIXOTO
. 1988. Decimations, extinctions
and colonization of frog populations in southeast
Brazil and their evolutionary implications. Biotro-
pica 20:230–235.
J
IMENEZ DE LA
E
SPADA
, M. 1875. Vertebrados del viaje
al Pacı´fico verificado de 1862–1865 por una comi-
sio´ n de naturalistas enviada por el Gobierno Es-
pan˜ ol. Batracios. Imprenta Miguel Ginesta, Ma-
drid, Spain.
K
NAPP
,R.A.,
AND
K. R. M
ATTHEWS
. 2000. Non-native
fish introductions and the decline of the mountain
yellow-legged frog from within protected areas.
Conservation Biology 14:428–438.
L
A
M
ARCA
,E.,
AND
S. L
O
¨TTERS
. 1997. Monitoring of
declines in Venezuelan Atelopus (Amphibia: Anura:
Bufonidae). In W. Bohme, W. Bischoff, and T. Zie-
gler (eds.), Herpetologia Bonnensis, pp. 207–213.
Societas Europaea Herpetologica, Bonn, Germany.
L
A
M
ARCA
,E.,
AND
H. P. R
EINTHALER
. 1991. Popu-
lation changes in Atelopus species of the Cordillera
de Me´rida, Venezuela. Herpetological Review 22:
125–128.
L
IPS
, K. R. 1998. Decline of a tropical montane am-
phibian fauna. Conservation Biology 12:106–117.
. 1999. Mass mortality and population declines
of anurans at an upland site in western Panama.
Conservation Biology 13:117–125.
L
IZANA
,M.,
AND
E. M. P
EDRAZA
. 1998. The effects of
UV-B radiation on toad mortality in mountainous
areas of central Spain. Conservation Biology 12:
703–707.
L
O
¨TTERS
, S. 1996. The Neotropical toad genus Atelo-
pus, Checklist-Biology-Distribution. M. Vences and
F. Glaw Verlags, Ko¨ ln, Germany.
M
ERINO
-V
ITERI
, A. 2001. Ana´lisis de posibles causas
de las disminuciones de poblaciones de anfibios en
los Andes del Ecuador. Licenciatura thesis, Ponti-
ciaUniv.Cato´lica Ecuador, Quito, Ecuador.
M
IDDLETON
, E. M., J. R. H
ERMAN
,E.A.C
ELARIER
,J.
W. W
ILKINSON
,C.C
AREY
,
AND
R. J. R
USIN
. 2001.
Evaluating ultraviolet radiation exposure with sat-
ellite data at sites of amphibian declines in Central
and South America. Conservation Biology 15:914–
929.
N
ICHOLS
, D. K., A. P. P
ESSIER
,
AND
J. E. L
ONGCORE
.
1998. Cutaneous chytridiomycosis: an emerging
disease? Proceedings of the American Association
of Zoo Veterinarians 1998:269–271.
O
SBORNE
, W. S. 1989. Distribution, conservation sta-
tus of corroboree frogs, Pseudophryne coroboree
Moore (Anura: Myobatrachidae). Australian Wild-
life Research 16:537–547.
P
ESSIER
, A. P., D. K. N
ICHOLS
,J.E.L
ONGCORE
,
AND
M.
S. F
ULLER
. 1999. Cutaneous chytridiomycosis in
poison dart frogs (Dendrobates spp.) and White’s
tree frogs (Litoria caerulea). Journal of Veterinarian
Diagnosis and Investigation 11:194–199.
P
ETERS
, J. A. 1973. The frog genus Atelopus in Ecuador
(Anura: Bufonidae). Smithsonian Contributions in
Zoology 154:1–49.
P
OUNDS
,J.A.,
AND
M. L. C
RUMP
. 1994. Amphibian
declines and climate disturbance: the case of the
golden toad and the harlequin frog. Conservation
Biology 8:72–85.
P
OUNDS
, J. A., M. P. L. F
OGDEN
,
AND
J. H. C
AMPBELL
.
1999. Biological response to climate change in a
tropical mountain. Nature 398:611–615.
R
ON
,S.R.,
AND
A. M
ERINO
-V
ITERI
. 2000. Amphibian
declines in Ecuador: overview and first report of
chytridiomycosis from South America. Froglog 42:
2–3.
R
ON
, S. R., L. A. C
OLOMA
,A.M
ERINO
,J.M.G
UAY
-
ASAM
ı´
N
,
AND
M. R. B
USTAMANTE
. 2000. Informa-
cio´ n sobre declinaciones de anfibios en el Ecuador.
[on line].
,
http://www.puce.edu.ec/Zoologia/
infodecl.html
.
[inquiry 5 October 2001].
R
ON
, S. R., A. M
ERINO
-V
ITERI
,L.A.C
OLOMA
,
AND
M.
B
USTAMANTE
. 2003. Amphibian declines in the
Andes of Venezuela, Colombia, Ecuador, and Peru:
an overview. Amphibian and Reptile Conservation
In press.
THER
, B.-E., J. T
UFTO
,S.E
NGEN
,K.J
ERSTAD
,O.W.
STAD
,J.E.S
KA
˚TAN
. 2000. Population dynamical
consequences of climate change for a small tem-
perate songbird. Science 287:854–856.
S
IERRA
, R. 1999. Vegetacio´ n remanente del Ecuador
continental, Circa 1996, 1:1’000.000. Proyecto INE-
FAN/GEF and Wildlife Conservation Society, Qui-
to, Ecuador.
S
ILLETT
,T.S.,R.T.H
OLMES
,
AND
T. W. S
HERRY
. 2000.
Impacts of a global climate cycle on population dy-
namics of a migratory song bird. Science 288:2040–
2042.
S
PEARE
,R.,
AND
L. B
ERGER
. 2000. Global distribution
of chytridiomycosis in amphibians. [on line].
126 S. R. RON ET AL.
,
http://www.jcu.edu.au/school/phtm/PHTM/
frogs/chyglob.htm
.
[inquiry 1 December 2000].
S
TEBBINS
,R.C.,
AND
N. W. C
OHEN
. 1995. A Natural
History of Amphibians. Princeton Univ. Press,
Princeton, NJ.
S
TEWART
, M. M. 1995. Climate driven population
fluctuations in rainforests frogs. Journal of Herpe-
tology 29:437–446.
T
YLER
, M. J. 1991. Declining amphibian popula-
tions—a global phenomenon? An Australian per-
spective. Alytes 9:43–50.
V
ALENCIA
, R., C. C
ERO
´N
,W.P
ALACIOS
,
AND
R. S
IERRA
.
1999. Las formaciones naturales de la Sierra del
Ecuador. In R. Sierra (ed.), Propuesta preliminar de
un sistema de clasificacio´n de vegetacio´ n para el
Ecuador continental, pp. 79–108. Proyecto INE-
FAN/GEF-BIRF and Ecociencia, Quito.
V
IAL
,J.L.,
AND
L. S
AYLOR
. 1993. The status of am-
phibian populations. Working document No. 1. De-
clining Amphibian Populations Task Force, World
Conservation Union, Gland, Switzerland.
W
AKE
, D. B. 1991. Declining amphibian populations.
Science 253:860.
W
UETHRICH
, B. 2000. How climate change alters
rhythms of the wild. Science 287:793–795.
W
YMAN
, R. 1990. What is happening to the amphib-
ians? Conservation Biology 4:350–352.
Y
OUNG
, B. E., K. R. L
IPS
,J.K.R
EASER
,R.I
BA
´N
˜EZ
,A.
W. S
ALAS
,J.R.C
EDEN
˜O
,L.A.C
OLOMA
,S.R
ON
,E.
L
A
M
ARCA
,J.R.M
EYER
,A.M
UN
˜OZ
,F.B
OLAN
˜OS
,
G. C
HAVES
,
AND
D. R
OMO
. 2001. Population De-
clines and Priorities for Amphibian Conservation
in Latin America. Conservation Biology 15:1213–
1223.
Accepted: 10 June 2002.
Journal of Herpetology, Vol. 37, No. 1, pp. 126–131, 2003
Copyright 2003 Society for the Study of Amphibians and Reptiles
Intra- and Interspecific Competition among the Water Snakes
Nerodia sipedon and Nerodia rhombifer
J
OHN
G. H
IMES
1
Department of Biological Sciences, Box 5018, University of Southern Mississippi,
Hattiesburg, Mississippi 39406-5018, USA
A
BSTRACT
.—I investigated the potential role of intra- and interspecific competition for food in Midland
Watersnakes (Nerodia sipedon pleuralis) and Diamond-Backed Watersnakes (Nerodia rhombifer rhombifer)
during the summers of 1999 and 2000. Snakes offered prey (juvenile spotted bass, Micropterus punctulatus)
at low densities (five fish/enclosure/week) had significantly lower proportional changes in mass than snakes
offered prey at high densities (10 fish/enclosure/week). However, differences in mass changes of N. sipedon
were not significant at constant relative densities of prey to snakes. Nerodia sipedon and N. rhombifer that
were offered 10 fish per week and tested individually had significantly higher mass changes than snakes
tested in intraspecific pairs. For snakes maintained in interspecific pairs and offered 10 fish per week, N.
sipedon had higher mass changes than N. rhombifer, although the difference was not significant. I lab-tested
the potential for exploitation as a mechanism of competition between N. sipedon and N. rhombifer by com-
paring rates of gastric breakdown after feeding snakes a goldfish (Carassius auratus), forcing regurgitation
at six, 12, and 18 h after ingestion, and comparing ash-free dry masses (AFDMs) of the digested fish. Rel-
atively higher AFDMs of digested fish were obtained from N. sipedon than from N. rhombifer at six and 12
hours after ingestion. Thus, the former species exhibited a faster rate of gastric breakdown than the latter.
These differences in competitive abilities may potentially contribute to the higher abundance of N. sipedon
than N. rhombifer in the upper Pascagoula River system of southeastern Mississippi.
Relative to most organisms that inhabit fresh-
water communities, the ecological role of snakes
has been little-studied, and few studies con-
ducted on aquatic snakes have focused on the
1
Present address: Nevada Division of Wildlife,
Southern Region Headquarters, 4747 Vegas Drive, Las
Vegas, Nevada 89108-2135; E-mail: jhimes@ndow.
state.nv.us
comparative ecology of coexisting species.
Moreover, I am not aware of any studies in
which the primary objective was to determine
the role of snakes as potential intra- and inter-
specific competitors in freshwater communities.
Nonetheless, some community-level ecological
studies on activity patterns, dietary preferences,
habitat selection, and abundances of aquatic
snakes have been conducted, particularly in the
southeastern and south-central United States
127COMPETITION IN WATER SNAKES (NERODIA SPP.)
(Clark, 1949; Diener, 1957; Preston, 1970; Kof-
ron, 1977, 1978; Mushinsky and Hebrard, 1977;
Hebrard and Mushinsky, 1978; Mushinsky et al.,
1980). The baseline data provided by these stud-
ies indicate that freshwater assemblages of
snakes often consist of several species and that
snakes frequently are abundant top predators in
freshwater communities. Thus, snakes may sig-
nificantly influence the structure of freshwater
communities, because of their roles as top pred-
ators and as potential intra- and interspecific
competitors.
Two of the most abundant species of snakes
in freshwater communities of the southeastern
United States are the Midland Watersnake (Ner-
odia sipedon pleuralis) and Diamond-Backed Wa-
tersnake (Nerodia rhombifer rhombifer). These spe-
cies have broadly overlapping distributions (Co-
nant and Collins, 1998); their diets consist pri-
marily of fishes (Diener, 1957; Laughlin, 1959);
they are primarily nocturnal during the summer
and diurnal during the spring and fall (Diener,
1957; Mushinsky et al., 1980); and they frequent-
ly occur in syntopy (pers. obs.). Because these
species are upper-level predators that have sim-
ilar habits and may occupy the same areas, their
coexistence and relative abundances are poten-
tially influenced by intra- or interspecific com-
petition for the same vital resources.
Both N. sipedon and N. rhombifer have periph-
eral distributions in southeastern Mississippi
(Conant and Collins, 1998), where they fre-
quently occur in sympatry (pers. obs.). Howev-
er, along the upper Pascagoula River system of
southeastern Mississippi, N. sipedon is approxi-
mately five times more abundant than is N.
rhombifer (pers. obs.). The far greater abundance
of N. sipedon in this area may imply that it has
a competitive advantage over N. rhombifer in pe-
ripheral areas. Moreover, N. rhombifer is most of-
ten associated with larger water bodies (Preston,
1970; Kofron, 1978) and is not as inclined to
wander overland as is N. sipedon (Preston, 1970;
Tiebout and Cary, 1987). Therefore, N. rhombifer
may not be as capable of colonizing areas at the
periphery of its distribution or of sustaining
populations in nonpermanent water-bodies as is
N. sipedon.
According to the principles of competition
theory, when putative competitors occur at high
densities and food is therefore limited, intraspe-
cific food competition should be more intense
than when the organisms occur at low densities.
Also, when prey occurs at high densities (per
capita) and is not limited, intraspecific food
competition should be less intense than when
prey occurs at low densities. However, before
concluding that competition is potentially a ma-
jor factor, one must first determine whether the
organisms share vital resources that are limited.
If competition (either intra- or interspecific) oc-
curs, then one may proceed in an attempt to
determine the mechanism (exploitation vs. in-
terference) by which it occurs.
To test the potential for competition as a fac-
tor influencing community relationships among
and between N. sipedon and N. rhombifer in the
upper Pascagoula River system, I studied these
species in the field and in the laboratory. I tested
for intraspecific food competition: (1) in N. si-
pedon at constant relative densities of prey to
snakes; (2) in N. sipedon at low prey densities;
and (3) among N. sipedon and N. rhombifer at
high snake densities. In addition, I tested for in-
terspecific food competition between N. sipedon
and N. rhombifer at constant relative densities of
prey to species of snake and tested for food ex-
ploitation as a mechanism of such competition.
M
ATERIALS AND
M
ETHODS
For all experiments, I used adult male snakes
collected from tributaries of the Bouie River and
adjacent portions of the Leaf River in Jones and
Forrest Counties, Mississippi. All snakes were
within 5 cm (snout–vent length; range
5
51–56
cm) and 20 g (range
5
136–156 g) of each other
to minimize difference in rates of mass change
or gastric breakdown attributable to body size.
Field experiments were conducted on privately
owned land in Jones County, Mississippi, where
snakes were tested in enclosures (1.22
3
1.22
3
0.91 m) constructed of a wooden frame and re-
movable lid and fiberglass screen walls. Enclo-
sures were placed half on land and half in water
at the edges of a series of ponds, to simulate the
natural riparian habitat of Nerodia. Enclosures
were arranged according to a randomized block
design (each pond represented a block), and
snakes were randomly placed in enclosures.
For all field experiments, I recorded snout–
vent length (cm), total length (cm), and mass (g)
of each snake the day before (31 May; Mass #1)
and after (1 September; Mass #2) testing to de-
termine changes in body condition. I considered
body condition to be a correlate of fitness, which
enabled me to determine whether intra- and/or
interspecific competition may have taken place.
The testing variable was proportional change in
mass: (Mass #1 to Mass #2)/(Mass #1) of snakes
from 31 May to 1 September. For treatments in-
volving two individuals of the same species, I
sketched the unique ventral pattern of dark
markings of each snake to identify individuals.
To test the potential for intraspecific food
competition among individuals of N. sipedon,I
calculated proportional changes in mass of sim-
ilarly sized snakes through experimental ma-
nipulation of snake and prey densities. I collect-
ed 35 snakes during May 2000. For 14 weeks
(June to August 2000), I tested snakes in the en-
128 JOHN G. HIMES
closures under three treatments: (1) one snake
per enclosure and five juvenile spotted bass
(Micropterus punctulatus) added as prey (total
length
5
2–3 cm); (2) two snakes per enclosure
and five juvenile M. punctulatus; and (3) two
snakes per enclosure and 10 juvenile M. punc-
tulatus. For each treatment, fish were added into
the water section of each enclosure once a week.
The first and third treatments were replicated
five times each; the second treatment was rep-
licated 10 times; and different snakes were used
for each replicate. Data were analyzed (with
a
set at 0.05) with a one-way ANOVA and a Tu-
key’s HSD test (posthoc to ANOVA).
To test the potential for interspecific food
competition between N. sipedon and N. rhombifer,
I collected 12 individuals of each species of
snake during May 1999. For 14 weeks (June to
August 1999), I tested snakes in the enclosures
and had five treatments: (1) one N. sipedon per
enclosure; (2) one N. rhombifer; (3) one N. sipedon
and one N. rhombifer together; (4) two N. sipedon
together; and (5) two N. rhombifer together. Ten
juvenile M. punctulatus were added as prey into
the water section of each enclosure once a week.
Each treatment was replicated N
5
3 times for
a total of 15 tests and different snakes were
used for each replicate. Data were analyzed
(with
a
set at 0.05) with a 2
3
3 ANOVA (spe-
cies
3
treatment): species
5
N. sipedon, N. rhom-
bifer; treatment
5
1 snake per enclosure, 2
snakes (heterospecifics) per enclosure, 2 snakes
(conspecifics) per enclosure.
To determine whether N. sipedon and N. rhom-
bifer may compete by exploitation, I measured
differential rates of gastric breakdown in snakes
in the laboratory. I collected snakes during Sep-
tember 1998. During October 1998, I maintained
five N. sipedon and five N. rhombifer alone in plas-
tic containers (59.1
3
43.2
3
15.2 cm). Snakes
were maintained at 25 C
6
2 C (cloacal tem-
peratures of active individuals of N. sipedon and
N. rhombifer in the summer generally range from
23–27
8
C; pers. obs.), provided with fresh water
daily, and fed ad libitum on goldfish (Carassius
auratus; total length
5
4.2–5.2 cm, wet mass
5
0.65–0.85 g) prior to testing. Snakes were not fed
within two days of testing to ensure that their
stomachs did not contain any remains of a prior
meal.
To begin testing for exploitation, each snake
was fed a goldfish (range of total lengths and
wet masses of fish were 4.5–5.0 cm and 0.70–
0.80 cm, respectively, thereby minimizing vari-
ability in surface area to volume ratio) and ex-
amined three times (one time per test): six, 12,
and 18 h after ingestion, when snakes were pal-
pated to obtain the goldfish regurgitant (with a
48-h recovery period between feedings/tests),
resulting in five replicates per species of snake
for each hour and a total of 30 tests (3 treat-
ments [
5
hours after feeding]
3
5 replicates
3
2 species). The regurgitants were dried (to re-
move moisture content) and ashed (to remove
organic matter; Paine, 1971) to determine their
ash-free dry mass (AFDM).
The net mass of 20 goldfish not used in the
feeding trials was determined. These fish were
then dried and ashed to determine their
AFDM. I produced a regression of the result-
ing AFDMs and WMs; the slope of the regres-
sion line (AFDM
52
0.004018
1
0.154 WM; r
2
5
0.6406; P
,
0.001) enabled me to calculate
the initial AFDM (
5
mass before digestion) of
the experimental goldfish. By subtracting the
AFDM
regurgitant
(
5
mass after digestion) from
the AFDM
initial
, I calculated the amount of
AFDM that had been digested, which was used
as an indicator of the rate of gastric break-
down. Data were analyzed (with
a
set at 0.05)
with a two-factor repeated-measures ANOVA
(time [six, 12, 18 h]
3
species [N. sipedon, N.
rhombifer]).
R
ESULTS
All snakes gained mass from the time of first
measurement (on day preceding study) to the
time of second measurement (on day following
study), and thus all proportional changes in
mass were positive. The experiment on intra-
specific competition in N. sipedon indicated that
proportional changes in mass of snakes were
significantly different between the three treat-
ments (F
2,17
5
12.56, P
,
0.001; Fig. 1). Mass
changes did not significantly differ between
snakes that were maintained at low densities
(one snake per enclosure) and offered five fish
per week and snakes that were maintained at
high densities (two snakes per enclosure) and
offered 10 fish per week (q
1,8
5
3.26, P
5
0.69;
Fig. 1). However, mass changes were signifi-
cantly higher in snakes that were maintained at
high densities and offered 10 fish per week than
in snakes that were maintained at high densities
and offered five fish per week (q
1,13
5
3.06, P
5
0.007; Fig. 1).
Again, all snakes gained mass from the time
of first measurement to the time of second mea-
surement, and thus all proportional changes in
mass were positive. The experiment on inter-
specific competition between N. sipedon and N.
rhombifer indicated that snakes of both species
tested individually had significantly higher pro-
portional changes in mass than snakes tested in
intraspecific pairs (F
2,18
5
9.73, P
5
0.002; Fig.
2). For snakes maintained in interspecific pairs,
N. sipedon had higher mass changes than N.
rhombifer, although the difference was not sig-
nificant (F
1,18
5
0.01, P
5
0.94; Fig. 2). In addi-
tion, the species
3
treatment interaction effect
129COMPETITION IN WATER SNAKES (NERODIA SPP.)
F
IG
. 1. Proportional change in mass (
6
1 SE) in
Nerodia sipedon maintained at low (one snake/enclo-
sure) and high (two snakes/enclosure) densities and
offered prey at low (five juvenile Micropterus punctu-
latus/enclosure/week) and high (10 juvenile Microp-
terus punctulatus/enclosure/week) densities. The first
(one snake and five fish) and third treatments (two
snakes and 10 fish) were replicated five times each
and the second treatment (two snakes and five fish)
was replicated 10 times for a total Nof 20 tests. Dif-
ferent snakes were used for each replicate for total N
of 35 snakes. All snakes gained mass, and thus all
mass changes were positive. Proportional change in
mass
5
(snake mass [g] before testing
2
snake mass
[g] after testing)/(snake mass [g] before testing); f
5
fish; s
5
snake.
F
IG
. 2. Proportional change in mass (
6
1 SE) in
Nerodia sipedon (N. s.) and Nerodia rhombifer (N. r.)
maintained at low densities (one snake/enclosure)
and high intra- and interspecific densities (two
snakes/enclosure). For all tests, 10 juvenile Micropte-
rus punctulatus/enclosure/week were added as prey.
Each treatment was replicated three times for a total
Nof 15 tests. Different snakes were used for each rep-
licate for a total Nof 12 N. sipedon and 12 N. rhombifer.
All snakes gained mass, and thus all mass changes
were positive. See Figure 1 for calculation of propor-
tional change in mass.
F
IG
. 3. Ash-free dry mass (AFDM; mean [
6
1 SE])
of the digested meal of five Nerodia sipedon and five
Nerodia rhombifer at six, 12, and 18 h after ingestion of
a goldfish by each snake. Each individual snake was
tested once under each treatment, resulting in five
replicates per species of snake for each hour and a
total Nof 30 tests. For procedures used in the removal
of moisture and organic matter, see Paine (1971).
was not significant (F
2,18
5
1.63, P
5
0.23; Fig.
2).
The experiment on interspecific food exploi-
tation indicated that, for snakes of both species,
the mass of the goldfish that had been digested
through gastric breakdown was significantly
higher at 18 h than at 12 h after ingestion, and
was significantly higher at 12 h than at six hours
(time F
2,7
5
135.36, P
,
0.001; Fig. 3). Nerodia
sipedon had relatively faster gastric breakdown
rates at six and 12 h after ingestion than N.
rhombifer (F
1,8
5
8.51, P
5
0.19; Fig. 3). Moreover,
the time
3
species interaction was significant
(F
2,7
5
7.00, P
5
0.02; Fig. 3).
D
ISCUSSION
The results of these experiments indicate that
(1) food competition does not occur in N. sipedon
at constant relative densities of prey to snakes;
(2) intraspecific food competition in N. sipedon
at low prey densities may occur; (3) intraspecific
food competition among N. sipedon and N. rhom-
bifer at high snake densities may occur; (4) N.
sipedon may be a superior food competitor to N.
rhombifer at constant relative densities of prey to
species of snake; and (5) N. sipedon maybea
superior exploitative food competitor to N.
rhombifer.
The results indicating that intra- and inter-
specific food competition may occur, respective-
ly, among and between N. sipedon and N. rhom-
bifer may seem untenable in freshwater com-
munities that are typified by a generally high
diversity and abundance of potential prey spe-
cies to the snakes. However, water levels of the
Pascagoula River system became very low dur-
ing the period when snakes were collected for
this study (summers of 1998–1999). Because of-
this multiyear drought, the water became re-
stricted to a series of small pools (usually
,
1
m in depth). During nights when snakes were
130 JOHN G. HIMES
collected, up to 10 individuals of N. sipedon and
N. rhombifer combined were observed actively
foraging in the same pools for fishes and frogs.
Moreover, on several occasions, multiple indi-
viduals of snakes were observed attacking the
same fish or frog. Although the snakes were
‘‘free’’ to move overland to search for food after
they had exhausted the supply of fishes and
frogs in the pools, neither N. sipedon nor N. rhom-
bifer are inclined to do so except during periods
of heavy rain (Preston, 1970; Meyer 1992). Thus,
it does appear that the snakes are competing for
a limited/limiting food source, at least during
low water periods.
The faster digestion rate in N. sipedon may al-
low it to resume feeding more rapidly, leading
to the consumption of more prey per unit time
relative to N. rhombifer during periods of food
limitation. This may translate into higher
growth rates and greater reproductive potential
in N. sipedon, ultimately resulting in the greater
overall abundance of this species. Nonetheless,
it is unknown whether N. sipedon actually
spends more time foraging than does N. rhom-
bifer. Moreover, a comparison of foraging suc-
cess by both species is needed to determine
whether the hunting skills of N. sipedon enable
it to capture and consume more prey. The abun-
dances and types of prey present (Mushinsky
and Hebrard, 1977; Kofron, 1978; Miller and
Mushinsky, 1990), habitat complexity (Mullin
and Mushinsky, 1995, 1997), and climatic con-
ditions (Mushinsky et al., 1980) may dictate in
part the foraging success of Nerodia spp. Thus,
the ability of N. sipedon to capture more prey
than can N. rhombifer is probably subject to geo-
graphical and temporal variation.
The competitive relationships of N. sipedon
and N. rhombifer should be further tested to de-
termine whether interference competition may
potentially occur as well. Exploitation and in-
terference are frequently coexisting in the same
community (e.g., Fellers, 1987; MacIsaac and
Gilbert, 1991; Deslippe and Savolainen, 1995)
and thus, although the results indicate that ex-
ploitation may be occurring, interference may
also potentially occur between snakes. More-
over, although the results also indicate that in-
terspecific competition may potentially occur
for food, snakes may compete for other vital re-
sources, regardless of the mechanism(s) in-
volved. For example, in the upper Pascagoula
River system, N. sipedon and N. rhombifer appear
to have a strong preference for basking only on
objects overhanging or partially submerged in
the water (pers. obs.). Thus, the availability of
suitable basking sites, especially for gravid fe-
males, may be a limited resource for which
snakes may potentially compete.
To further substantiate the finding that N. si-
pedon and N. rhombifer may potentially compete
for food, the diets of snakes should be deter-
mined and assessed for the degree of similarity.
Moreover, the foraging habits of free-ranging
snakes should be carefully observed and com-
pared. For example, N. sipedon and N. rhombifer
may forage in different microhabitats or during
different times of the night, although I have
found these two species repeatedly within the
same area and foraging at the same time. Re-
garding foraging tactics, I have observed N. si-
pedon to attack live fishes only from the water’s
edge, whereas N. rhombifer attacks live fishes
from the water (Savitsky, 1989). If these obser-
vations are accurate descriptors of these species
normal foraging tactics, then the two species
may encounter and consume different species or
size classes of fishes, with N. sipedon taking
more fishes that inhabit the land-water interface
than does N. rhombifer.
The potential importance of N. sipedon and N.
rhombifer as competitors in freshwater commu-
nities may be underestimated if adults are stud-
ied to the exclusion of neonates and juveniles.
The smaller head and body size of young N.
rhombifer limits the range of food sources avail-
able to them by inhibiting the consumption of
large fishes, which are preferred by the adults
(Mushinsky et al., 1982). These differences in
diet between size classes may therefore lessen
food competition between young and adult
snakes. However, N. sipedon pleuralis and N.
rhombifer rhombifer give birth annually to an av-
erage of 21 and 37 offspring, respectively (Ten-
nant and Bartlett, 2000). Thus, until or unless
the neonates disperse from their parturition site
or their numbers are lowered by predation or
other factors, the high density and more ste-
nophagous diet (relative to adults) of young
snakes may lead to increased food competition
by individuals within this size class.
Assuming that competition is a major factor
in communities that include N. sipedon and N.
rhombifer, competition may be strongest not be-
tween species of snakes, but between snakes
and other predators, such as piscivorous fishes.
Although a snake-fish competitive interaction
has not been documented to my knowledge,
competition between taxonomically disparate
species may be more prevalent than is common-
ly assumed, perhaps because most researchers
do not test for competition between species that
they assume a priori not to be likely competi-
tors. For example, Resetarits (1991, 1995) found
that the demography of a stream-inhabiting
population of spring salamanders (Gyrinophilus
porphyriticus) was strongly influenced by com-
petitively asymmetrical interactions with brook
trout (Salvelinus fontinalis).
131COMPETITION IN WATER SNAKES (NERODIA SPP.)
Acknowledgments.—I thank D. Beckett, F.
Moore, S. Ross, S. Secor, and S. Walls for their
advice and support throughout the duration of
this project. In addition, D. Beckett, F. Moore, S.
Ross, and S. Walls lent me lab equipment, as did
P. Biesiot. J. Johnson assisted with statistics. I am
especially grateful to K. Rushing, who gener-
ously allowed me to conduct my field studies
on her land, and C. Qualls, who reviewed an
earlier version of this manuscript. Numerous
graduate and undergraduate students assisted
with various field and lab components of this
project, including A. Lee, A. Wilberding, A. For-
et, A. Trousdale, B. Alford, E. Ducote, L. Yates,
M. O’Connell, R. Wells, S. Pierce, and T. Rauch.
L
ITERATURE
C
ITED
C
LARK
, R. F. 1949. Snakes of the hill parishes of Lou-
isiana. Journal of the Tennessee Academy of Sci-
ence 24:244–261.
C
ONANT
,R.,
AND
J. T. C
OLLINS
. 1998. A field guide
to reptiles and amphibians of eastern and central
North America. 3rd ed. exp. Houghton Mifflin Co.,
Boston, MA.
D
ESLIPPE
,R.J.,
AND
R. S
AVOLAINEN
. 1995. Mecha-
nisms of competition in a guild of formicine ants.
Oikos 72:67–73.
D
IENER
, R. A. 1957. An ecological study of the plain-
bellied water snake. Herpetologica 13:203–211.
F
ELLERS
, J. H. 1987. Interference and exploitation in a
guild of woodland ants. Ecology 68:1466–1478.
H
EBRARD
,J.J.,
AND
H. R. M
USHINSKY
. 1978. Habitat
use by five sympatric water snakes in a Louisiana
swamp. Herpetologica 34:306–311.
K
OFRON
, C. P. 1977. Feeding, Reproduction, and Oth-
er Habits of Aquatic Snakes in the Atchafalaya Riv-
er Basin, Louisiana. Unpubl. master’s thesis. Univ.
of Southwestern Louisiana, Lafayette.
. 1978. Foods and habitats of aquatic snakes
(Reptilia, Serpentes) in a Louisiana swamp. Journal
of Herpetology 12:543–554.
L
AUGHLIN
, H. E. 1959. Stomach contents of some
aquatic snakes from Lake McAlester, Pittsburgh
County, Oklahoma. Texas Journal of Science 11:83–
85.
M
AC
I
SAAC
,H.J.,
AND
J. J. G
ILBERT
. 1991. Discrimi-
nation between exploitative and interference com-
petition between Cladocera and Keratella cochilearis.
Ecology 72:924–937.
M
EYER
, C. S. 1992. Foraging, Thermal and Spatial
Ecology of the Northern Water Snake (Nerodia si-
pedon). Unpubl. master’s thesis. Central Michigan
Univ., Mount Pleasant.
M
ILLER
,D.A.,
AND
H. R. M
USHINSKY
. 1990. Foraging
ecology and prey size in the mangrove water
snake Nerodia clarkii compressicauda. Copeia 1990:
1099–1106.
M
ULLIN
,S.J.,
AND
H. R. M
USHINSKY
. 1995. Foraging
ecology of the mangrove salt marsh snake, Nerodia
clarkii compressicauda: effects of vegetational densi-
ty. Amphibia-Reptilia 16:167–175.
. 1997. Use of experimental enclosures to ex-
amine foraging success in water snakes: a case
study. Journal of Herpetology 31:565–569.
M
USHINSKY
,H.R.,
AND
J. J. H
EBRARD
. 1977. Food par-
titioning by five species of water snakes in Loui-
siana. Herpetologica 33:162–166.
M
USHINSKY
,H.R.,J.J.H
EBRARD
,
AND
M. G. W
ALLEY
.
1980. The role of temperature on the behavioral
and ecological associations of water snakes. Copeia
1980:744–754.
M
USHINSKY
,H.R.,J.J.H
EBRARD
,
AND
D. S. V
ODOPICH
.
1982. Ontogeny of water snake foraging ecology.
Ecology 63:1624–1629.
P
AINE
, R. T. 1971. The measurement and application
of the calorie to ecological problems. Annual Re-
view of Ecology and Systematics 2:145–164.
P
RESTON
, W. B. 1970. The Comparative Ecology of
Two Water Snakes, Natrix rhombifera and Natrix er-
ythrogaster, in Oklahoma. Unpubl. Ph.D. diss.,
Univ. of Oklahoma, Norman.
R
ESETARITS
J
R
., W. J. 1991. Ecological interactions
among predators in experimental stream commu-
nities. Ecology 72:1782–1793.
. 1995. Competitive asymmetry and coexis-
tence in size-structured populations of brook trout
and spring salamanders. Oikos 73:188–198.
S
AVITSKY
, B. A. C. 1989. Aquatic Foraging in Two In-
dependently Evolved Species of Snake: Nerodia
rhombifera (Colubridae) and Agkistrodon piscivorus
(Viperidae). Unpubl. Ph.D. diss., Univ. of Tennes-
see, Knoxville.
T
ENNANT
,A.,
AND
R. D. B
ARTLETT
. 2000. A field
guide to snakes of North America; Eastern and
Central regions. Gulf Publishing Co., Houston, TX.
T
IEBOUT
III, H. M.,
AND
J. R. C
ARY
. 1987. Dynamic
spatial ecology of the water snake, Nerodia sipedon.
Copeia 1987:1–18.
Accepted: 10 June 2002.
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One of the major causes of worldwide amphibian declines is a skin infection caused by a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). This study documents the interactions between this pathogen and a susceptible amphibian host, the boreal toad (Bufo boreas). The amount of time following exposure until death is influenced by the dosage of infectious zoospores, duration of exposure, and body size of the toad. The significant relation between dosage and the number of days survived (dose-response curve) supports the hypothesis that the degree of infection must reach a particular threshold of about 107–108 zoosporangia before death results. Variation in air temperature between 12°C and 23°C had no significant effect on survival time. The infection can be transmitted from infected to healthy animals by contact with water containing zoospores; no physical contact between animals is required. These results are correlated with observations on the population biology of boreal toads in which mortalities associated with B. dendrobatidis have been identified.
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Global warming is considered to be a major threat to biodiversity and to have an erosive effect on the survival of endangered species. Amphibians are known as a vulnerable group of vertebrates that live and reproduce in both terrestrial and aquatic habitats. The subtropical regions of the world are among the land areas where amphibians will suffer the most from climate change. In the present study, the effect of climate change on Bufo eichwaldi inhabiting Hyrcanian forests was investigated. According to our results, the lowest temperature in the coldest season is the most important variable for the presence of this species. Due to the beginning of reproductive activity and mating taking place in late January until the end of February, this variable will have a direct effect on the rate of breeding and thus on the conservation of this species, because the species can find a new suitable area outside of high humanisation and increase its chance of successful breeding. Of course, climate change will cause the average annual temperature to rise by 2070, and this will favour the early onset of reproduction. Therefore, according to the analysis and scenarios considered in this study, global warming cannot have a negative effect on the toad species. However, a careful assessment of the status of other competing species in conjunction with the Talysh toad could provide a better explanation of the impact of climate change.
Article
On the basis of surveys conducted between 1991 and 1996, I report a decline of the amphibian fauna at Las Tablas, Puntarenas Province, Costa Rica. I propose that the reduction in the abundance of Atelopus chiriquiensis and Hyla calypsa, the presence of dead and dying individuals of six species of frogs and salamanders, and changes in population sex ratios of A. chiriquiensis and H. calypsa are evidence for 'atypical' population fluctuations. Species with both aquatic eggs and aquatic larvae were most affected (e.g., Rana vibicaria, Hyla rivularis), whereas species with direct development or those that lack tadpoles, such as rainfrogs (Eleutherodactylus spp.) and some salamanders (e.g., Bolitoglossa minutula), do not seem to have declined in numbers. In light of this evidence and in comparison with other declines in tropical upland Australia, Brazil, and Costa Rica, I conclude that environmental contamination (biotic pathogens or chemicals) or a combination of factors (environmental contamination plus climate change) may be responsible for declines in the amphibian populations at this protected site.
Article
Between 1973 and 1982 nine populations of the northern leopard frog in the Red Feather Lakes region of Larimer County, Colorado, failed to reproduce. These failures all resulted in extinction of the populations. One area formerly supporting a population was recolonized in 1980, but no frogs were observed at any of the nine sites in 1981 or 1982. Six of the populations went extinct because the breeding ponds dried up. The remaining populations were small enough to be susceptible to random events, but the nature of these events is unknown.
Article
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 semi-monthly for two years, then annually or biannually thereafter for a total of 255 evening counts. Ten all-night 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 m(2), whereas the number of juveniles varied from 0 to 221/100 m(2). The maximum single count of all frogs was 244. Counts of >100 juveniles occurred during October through January in 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 greater than or equal to 15 adults whereas the maximum count from 1984 until 1989 was 11 adults. The drop in numbers was correlated with an increased number of periods of days with less than or equal to 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 1989 before Hurricane Hugo. Juveniles apparently cannot 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 disappeared following the hurricane as did other arthropod predators. Rather than total monthly or annual rainfall, it is the distribution of the rain that is important to these subtropical wet forest species.
Article
Ontogenetic changes in prey consumption are most striking in Nerodia erythrogaster and N. fasciata. Prey of these 2 species changes from fish to frogs as the snakes exceed a snout-vent length of 50 cm. Nerodia rhombifera and N. cyclopion primarily eat fish throughout their life. However, with maturity and increased body size both species change portions of their diets. Nerodia rhombifera preys upon larger fish which occupy deeper, open-water habitats, when the snakes exceed 80 cm. Nerodia cyclopion eats a larger proportion of centrarchid fish as its body size increases. Small prey are found in the stomachs of most size-classes of all 4 snake species. All 4 species eat larger prey as they mature. However, the largest individuals are females, and in 2 of the 4 species the large females eat a different array of prey than smaller conspecific males. The size sexual dimorphism does not reduce the overlap in the diets of the 2 species that eat anurans as adults.-from Authors
Article
Competition between colonies often explains patterns of nest spacing in social insects, but the way in which it produces regular spacing has rarely been studied experimentally. We conducted three field experiments in Elk Island National Park, Alberta, Canada, to examine potential spacing mechanisms across four species of Formica ants. Space preemption of founding queens and asymmetric interference between established colonies were key processes in all species but F. podzolica. The relative importance of these mechanisms was contingent upon the neighboring species, and understood in terms of their activity levels, aggressiveness and development of recruitment systems. Exploitative competition for food may account in part for abundance and distribution of F. podzolica. However, a removal experiment failed to produce significant differences in reproductive output and sex allocation between control and neighbor-removed colonies.