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1539

Patterns of larval amphibian distribution along a

wetland hydroperiod gradient
Kimberly J. Babbitt, Matthew J. Baber, and Tracy L. Tarr

Abstract: We investigated the response of pond-breeding amphibian assemblages to wetland hydroperiod and associ-
ated predator changes (invertebrates (abundance and richness) and fish (presence/absence)) in relatively undisturbed
landscapes in southern New Hampshire, U.S.A. We sampled 42 wetlands for larval amphibians in 14 spatial blocks
(each with a short-, intermediate-, and permanent-hydroperiod wetland) in 1998 and 1999. Assemblages in short-
hydroperiod wetlands (<4 months) were depauperate (4 species only) compared with intermediate-hydroperiod (non-
permanent but >4 months) and permanent wetlands, which included 7 and 9 species, respectively. Total amphibian
abundance did not vary among hydroperiod categories. Species distributions along the hydrological gradient also dif-
fered. Rana sylvatica dominated wetlands with short and intermediate hydroperiods, whereas Rana catesbeiana, Bufo
americanus, Rana clamitans, and Pseudacris crucifer dominated in those with a longer hydroperiod. Among permanent
wetlands, amphibian species richness and abundance did not differ with respect to the presence of predatory fish, al-
though there were species-compositional differences. Amphibian species richness and abundance were positively corre-
lated with the abundance and richness of predatory invertebrates, suggesting that both amphibian and macroinvertebrate
predator assemblages may be responding similarly to differences in wetland characteristics (e.g., dissolved oxygen con-
centration). Overall, our results indicate that wetland hydroperiod has an important influence on amphibian distribution
and should be incorporated into regulations and legislation designed to protect biologically diverse isolated wetlands.
Rsum : Nous avons examin la raction dun peuplement damphibiens, qui se reproduisent dans des tangs,
lhydropriode de terres humides et aux changements associs dans la faune des prdateurs ((abondance et richesse)
des invertbrs et (prsence/absence) des poissons) dans des paysages relativement peu perturbs du sud du New
Hampshire, .-U. Nous avons chantillonn les larves damphibiens dans 42 terres humides dans 14 blocs spatiaux
(comprenant chacun une terre humide hydropriode courte, une hydropriode intermdiaire et une hydropriode
permanente) en 1998 et 1999. Les peuplements des terres humides hydropriode courte (<4 mois de mise en eau) ont
une faune rduite (seulement 4 espces) en comparaison des terres humides hydropriode intermdiaire (non perma-
nente, mais avec >4 mois de mise en eau) ou permanente qui contiennent respectivement 7 et 9 espces. Labondance
totale des amphibiens ne varie pas en fonction de lhydropriode, mais la rpartition des espces change le long du
gradient hydrologique. Rana sylvatica domine dans les terres humides hydropriodes courte et intermdiaire, alors
que Rana catesbeiana, Bufo americanus, Rana clamitans et Pseudacris crucifer le font dans les terres humides hy-
dropriode plus longue. Dans les terres humides permanentes, la richesse spcifique et labondance des amphibiens ne
sont pas affectes par la prsence de poissons prdateurs, bien quil y ait des diffrences dans la composition des esp-
ces. La richesse spcifique et labondance des amphibiens sont en corrlation positive avec labondance et la richesse
des macroinvertbrs prdateurs, ce qui laisse croire que les peuplements damphibiens et de macroinvertbrs prda-
teurs ragissent tous deux de faon similaire des diffrences dans les caractristiques des terres humides (e.g.,
concentration de loxygne dissous). Dans leur ensemble, nos rsultats dmontrent que lhydropriode des terres humi-
des a une influence considrable sur la rpartition des amphibiens et que cette variable devrait tre incorpore dans les
rglements et les lois qui visent protger les terres humides isoles forte diversit biologique.

[Traduit par la Rdaction] Babbitt et al. 1552

Introduction
In freshwater lentic habitats, the hydrological gradient
ranges from ephemeral pools to permanent ponds and lakes,
and has long been recognized as a major influence on the
abundance and distribution of organisms. Numerous amphib-
ian species use these habitats for mating, oviposition, and
larval growth and development (Semlitsch et al. 1996). Wet-
land hydroperiod can have a particularly strong influence on
amphibian assemblages (Pechmann et al. 1989; Semlitsch et
al. 1996; Skelly 1997). This is largely attributed to species-
specific differences in the time available to complete larval

Received 2 January 2003. Accepted 15 July 2003. Published on the NRC Research Press Web site at http://cjz.nrc.ca on
29 September 2003.
K.J. Babbitt,1 M.J. Baber, and T.L. Tarr.2 Department of Natural Resources, University of New Hampshire, 226 James Hall,
Durham, NH 03824, U.S.A.
1
Corresponding author (e-mail: kbabbitt@cisunix.unh.edu).
2
Present address: NH Soil Consultants, Inc., Newmarket, NH 03857, U.S.A.

Can. J. Zool. 81: 15391552 (2003) doi: 10.1139/Z03-131 2003 NRC Canada

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1540
development (desiccation stress), and the fact that predators
are also influenced by these hydrological processes (Wood-
ward 1983; Skelly 1996).
General models predict a unimodal pattern of species
richness for assemblages of larval amphibians and aquatic
invertebrates, with a peak in ponds with intermediate hydro-
periods (Wilbur 1987; Wellborn et al. 1996). This hypothesis
is supported by field studies of species richness of both
larval amphibians and invertebrates (Heyer et al. 1975;
Wilbur 1984; Snodgrass et al. 2000a, 2000b). In ephemeral
wetlands, low species richness is attributed to the increased
likelihood of desiccation and, thus, the exclusion of amphib-
ians with slow rates of development. In permanent wetlands,
low species richness is primarily attributed to the high abun-
dance and diversity of predators, which may be avoided by
some breeding amphibians. Thus, amphibian species rich-
ness may be maximized at intermediate positions along the
hydrological gradient, because both desiccation and preda-
tion risks are relatively low.
Amphibians that breed in permanent habitats tend to have
a prolonged larval period but are able to coexist with preda-
tors, owing to the possession of defensive mechanisms, in-
cluding attaining a large body size (Travis et al. 1985;
Richards and Bull 1990), behavioral changes such as reduc-
ing activity (Lawler 1989; Skelly and Werner 1990) or
selecting microhabitat (Hews 1995), use of structurally com-
plex habitats (Babbitt and Jordan 1996; Babbitt and Tanner
1997), and toxicity and unpalatability (Brodie and Formano-
wicz 1983). In contrast, amphibians that breed in temporary
aquatic habitats develop rapidly but generally lack or have
diminished antipredator defenses. Larval amphibian assem-
blages found in temporary aquatic environments, therefore,
are often distinct from those that utilize permanent aquatic
habitats.
Predators are known to be a major cause of mortality for
amphibian larvae (Calef 1973; Smith 1983). Fish are partic-
ularly efficient predators of larval amphibians and often
cause the local extirpation of species (Bradford et al. 1993;
Hecnar and MCloskey 1997; Smith et al. 1999). While fish
are typically more voracious amphibian predators than inver-
tebrates or other amphibians (e.g., adult newts), they are
generally excluded from wetlands that dry periodically (an-
nually or semiannually), whereas non-fish predators range
broadly across the hydrological gradient (Wellborn et al.
1996). Nevertheless, predation pressure by non-fish preda-
tors may be lower in wetlands with short hydroperiods, ow-
ing to the inability of some species to colonize or complete
their larval development in such habitats (Woodward 1983;
Skelly 1996).
Our objective was to investigate how amphibian assem-
blages respond to changes in wetland hydroperiod and
aquatic predators (specifically invertebrates and fish) in
southern New Hampshire, U.S.A. Furthermore, we examined
the influence of other potential abiotic correlates (e.g., wet-
land size, depth, pH, conductivity, dissolved oxygen concen-
tration, and temperature) on amphibian assemblages. We
predicted that amphibian assemblages would vary along the
hydrological gradient predominantly as a result of species-
specific development-rate limitations and changes in predator
species richness, abundance, and composition. Although the
importance of hydroperiod in influencing the structure of as-
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Can. J. Zool. Vol. 81, 2003
semblage of many aquatic taxa is well recognized (Wellborn
et al. 1996), few empirical studies have actually been con-
ducted to examine patterns of amphibian species distribution
across the gradient of ephemeral to permanent wetlands (see
Collins and Wilbur 1979; Snodgrass et al. 2000a). Our goal
in conducting this study is to improve our current under-
standing of the local-scale processes that influence amphib-
ian species distributions along the hydrological gradient, and
thus complement recent efforts to predict assemblage struc-
ture from processes operating at landscape and regional
scales (Hecnar and MCloskey 1996; Knutson et al. 1999;
Lehtinen et al. 1999). Together, such studies serve to in-
crease the ability of biologists to predict amphibian distri-
bution and abundance, and thus optimize conservation
management.
Methods
Study area
Field research was conducted in public and privately
owned wetlands at 14 sites in southern New Hampshire
(Fig. 1). Wetlands were predominantly surrounded by
closed-canopy secondary growth (>50 years old) oakpine
forest. Dominant tree species included white pine (Pinus
strobus), red maple (Acer rubrum), red oak (Quercus rubra),
and eastern hemlock (Tsuga canadensis). Following Skelly
(1996), we classified wetlands as short, intermediate, or long
in hydroperiod. Short-hydroperiod wetlands (<4 months
after ice out, drying in MayJuly) were generally small
(0.053 0.0143 ha; mean SE). Buttonbush (Cephalanthus
occidentalis) was common in most vernal pools, and these
wetlands often had downed logs, shrubs, and leaf litter as
vegetative structure with little to no emergent or floating
vegetation. Intermediate-hydroperiod wetlands (>4 months
after ice out, drying in late July September (n = 10) or
only in dry years (n = 4); 0.27 0.081 ha) were similar in
vegetation to short-hydroperiod wetlands; however, a few
(4 of 14) did have emergent or floating vegetation. This veg-
etation consisted primarily of waterlily (Nuphar variegata),
three-way sedge (Dulichium arundinaceum), rattlesnake grass
(Glyceria sp.), and bladderwort (Utricularia sp.). Most long-
hydroperiod wetlands (i.e., permanent wetlands) were large
(2.52 0.974 ha) and appeared to have more vegetative di-
versity than short- or intermediate-period wetlands. All but
two long-hydroperiod wetlands had abundant woody debris
and well-developed aquatic-plant assemblages. Common
plants found in permanent wetlands included bur-reed (Spar-
ganium sp.), coontail (Ceratophyllum sp.), milfoil (Myrio-
phyllum sp.), pondweed (Potamogeton sp.), cattail (Typha
sp.), arrowhead (Sagittaria sp.), waterlily (Nymphaea and
Nuphar sp.), bladderwort, watershield (Brasenia schreberi),
pickerelweed (Pontederia cordata), and three-way sedge.
Finally, short-hydroperiod wetlands were also likely to have
relatively high canopy cover, whereas intermediate- and
long-hydroperiod wetlands generally had open canopies.
Site selection
Fourteen permanent wetlands in southern New Hampshire
were selected from National Wetland Inventory (NWI) maps
using a stratified random approach, with the constraint that
the surrounding landscape must consist of relatively undis-
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Babbitt et al.
Fig. 1. Locations of study sites. At least one short-, one intermediate-, and one long-hydroperiod wetland was sampled in each cluster
(). Scale is 1 : 2 500 000 (modified from U.S. Geological Survey, map collection, PerryCastaneda Library, University of Texas).
turbed forested habitat. The areas surrounding each of the 14
study-site wetlands were ground-surveyed from April to
early June 1998 for smaller, seasonally inundated wetlands,
which generally failed to show up on NWI maps. Several of
these wetlands were selected at each of the 14 permanent
wetland study sites, resulting in a cluster of study wetlands
with short, intermediate, and permanent hydroperiods. Once
hydroperiod was verified for each wetland (wetlands were
checked for standing water monthly), we dropped excess
wetlands from our study so that a total of 42 wetlands
(1 short-hydroperiod, 1 intermediate-hydroperiod, and 1 per-
manent wetland in each of the 14 clusters) were selected for
continued sampling. Each wetland cluster was treated as a
block for statistical analyses.
Sampling methods
We sampled each wetland for predaceous aquatic inverte-
brates and amphibian larvae four times during the summers
of 1998 and 1999. In 1998, we sampled wetlands from
17 June to 24 July and from 26 August to 20 September. In
1999, we sampled wetlands from 24 May to 11 June and
from 26 July to 3 August. Sampling time periods were dic-
tated by preliminary sampling and accounted for temporal
differences in breeding activity among species and ensured
that all species breeding in wetlands were captured (breed-
ing events began later in 1998 than in 1999). Wetlands
within a cluster were sampled within a 2-day period to avoid
temporal effects. Wetlands and surrounding upland areas
were characterized by determining the numerically dominant
vegetation during site selection and at the end of sampling in
1999 using standard references (Petrides 1986; Gleason and
Cronquist 1995). These were qualitative habitat descriptions
and were not designed for statistical analyses. The size of
large wetlands was determined from digitized NWI maps us-
ing ArcInfo software (Environmental Systems Research In-
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1541
stitute Inc. 1999). The maximum area of small wetlands not
identified on NWI maps was measured with a meter tape.
We sampled larval amphibians and predacious inverte-
brates using a 30 cm 45 cm dip net. Standardized (approx-
imately 1 m2) dip-net sweeps were conducted to obtain relative
species densities (herein species abundance) for each wet-
land. Dip-netting is a standard technique used to sample
both amphibian and invertebrate assemblages in lentic habi-
tats (Heyer et al. 1994). A minimum of 5, 10, and 15 dip-net
sweeps were taken in each microhabitat in short-, intermedi-
ate-, and long-hydroperiod wetlands, respectively. These
sweep numbers were based on a preliminary survey in which
we quantified the sweeps required to obtain no new inverte-
brate genera or amphibian species in wetlands with different
hydroperiods. Because water at study sites was generally
clear, we determined fish presence through visual surveys
(i.e., walking the shoreline looking for nesting centrarchids)
in addition to dip-net captures. Fish collected from dip-net
sweeps were identified and released. The purpose of fish
sampling was to detect the presence of predatory fish; we
did not attempt to quantify fish abundance. Fish-presence es-
timates were considered robust because wetlands categorized
as fishless in 1998 were also found to be fishless in 1999.
Moreover, a subsequent study (M.J. Baber and K.J. Babbitt,
unpublished data) confirmed that these wetlands contained
no predatory fish, although an additional predatory fish spe-
cies was recorded in one of the wetlands that contained
predatory fish in this study.
Four coarsely defined microhabitats were identified to ac-
count for species-specific distribution among microhabitats
(Heyer et al. 1994). Microhabitats included shallow non-
vegetated areas, shallow vegetated areas, deep nonvegetated
areas, and deep vegetated areas. Preliminary sampling re-
vealed that vegetation zones often changed to deep-water
plant assemblages (e.g., B. shreberi, Nuphar sp., Nymphaea
sp.) at a depth of approximately 0.6 m. Therefore, we
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defined deep water as 0.6 m and shallow water as <0.6 m
in depth. Depth was measured at the deepest point within
each wetland at the time of sampling. Vegetated areas in-
cluded aquatic submerged and emergent vegatation and
shrubs (e.g., C. occidentalis), or floating plants. Non-
vegetated areas were either totally devoid of any living
plants or were very sparsely vegetated (as described in
Mitsch and Gosselink 1993).
In the field, all specimens were preserved in 10% buffered
formalin. Invertebrates were transferred to 70% ethanol in
the laboratory and identified to the generic level (except
Trichoptera larvae, which were identified to order only) us-
ing standard identification keys (Walker 1958; Peckarsky et
al. 1990; Merritt and Cummins 1996) and reference samples
from the University of New Hampshire invertebrate collec-
tion. Only invertebrates known to prey on vertebrates (am-
phibians or fish) were considered (reviewed in McCormick
and Polis 1982). In the case of Dytiscidae, only genera with
adults >4 mm in length were included because smaller gen-
era are likely to be ineffective predators. Amphibians were
identified to the species level using standard larva-identification
keys (Orton 1939; Altig 1970; Travis 1981).
Prior to dip-netting, pH, conductivity (S), water tempera-
ture (C), and dissolved oxygen concentration (mg/L) were
recorded at three random locations in each microhabitat at
each site, between the approximate hours of 0900 and 1500,
using an Orion model 230A pH meter and a YSI model 85
conductivity meter. These abiotic parameters were measured
to determine which of these variables were correlated with
hydroperiod and could thereby potentially influence compo-
sition and abundance of predators and amphibian larvae.
Statistical analyses
Total counts for each amphibian species and invertebrate
genus captured in each wetland were divided by the number
of dip-net sweeps taken in each wetland. This yielded an av-
erage number of specimens per sweep (i.e., abundance based
on catch per unit effort) for each year, and both years com-
bined, which could be compared across hydroperiod types.
Sample sizes differed in the two years for short-hydroperiod
wetlands (n = 14 and 8), owing to drier conditions in 1999
(six short-hydroperiod wetlands dried before the first sam-
pling in 1999). We performed Spearmans rank correlations
on abiotic factors (wetland size, pH, conductivity, dissolved
oxygen concentration, depth, and temperature) to determine
if these variables covaried with respect to hydroperiod. Wa-
ter-chemistry data from 1999 were not analyzed because of
the low number of complete blocks
To examine the relationships among larval amphibian as-
semblages, hydroperiod, and concomitant changes in abiotic
and biotic (predator) characteristics, we used nonmetric
multidimensional scaling (NMDS), with the Bray and Curtis
(1957) dissimilarity metric on a wetland variable by wetland
site matrix overlaid on a larval amphibian species density by
wetland site matrix. This analysis is an ordination method
based on ranked distances and is well suited to data that are
nonnormal or are on an arbitrary or otherwise questionable
scale (McCune and Mefford 1997). Furthermore, axes are
independent and do not result in the complex curvilinear dis-
tortions that often appear in hierarchical correspondence
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axes even after recommended detrending and rescaling
(Minchin 1987). The lack of fit between matrices (stress)
is measured by a loss function that the procedure minimizes.
We started the NMDS analyses with six ordination axes,
then later eliminated axes that had a small incremental
reduction in stress. Two ordination axes were sufficient
to achieve low values of stress. Subsequently, 10 two-
dimensional ordinations were performed using 100 iterations
each. The ordination with the lowest final stress (0.191) was
selected for use in further statistical analyses in this study.
Ordinations with stress levels <0.2 are considered interpret-
able (Clarke 1993).
We used varimax rotation based on maximizing the rela-
tionship between axis 1 and hydroperiod, which showed the
strongest relationship to ordination space. Furthermore, to
test whether larval amphibian assemblages varied among
hydroperiod categories, we performed one-way ANOVAs
on NMDS axis 1 and axis 2 scores. Bonferroni pairwise
comparisons were used to test for differences in larval
amphibian assemblages between hydroperiod groups (short,
intermediate, and long).
We used generalized linear models (GLMs; McCullagh
and Nelder 1989) to determine the relative influence of
hydroperiod and concomitant changes in abiotic and biotic
characteristics (invertebrate abundance and richness, and
the presence/absence of fish) on larval amphibian species
richness, total abundance, and species abundances. These
models present a major advantage over classical multiple re-
gression approaches in that they integrate data from different
statistical distributions with the appropriate modeling of sta-
tistical error (e.g., normal as in multiple regression, binomial
for presence/absence data, ordinal for classes of abundance,
Poisson or negative binomial for species or individual
counts). The response variables larval amphibian species
richness and larval amphibian abundance were fitted assum-
ing a normal error and identity link (equivalent to a multiple
linear regression), whereas species abundances were best
represented by a Poisson regression and logarithmic-link
function (McCullagh and Nelder 1989). To determine the
most appropriate subset of combinations of explanatory vari-
ables we used a subjective approach (Collet 1994). We ob-
served changes in deviance (explained variance) when fitting
single variables, and the change in deviance was tested by a
2 test (McCullagh and Nelder 1989). Only variables that
were significant (p < 0.05) were retained in the final model.
Moreover, to avoid collinearity, when variables where
strongly correlated (>0.7; Table 1), only the variable with
the greatest change in deviance was used.
We conducted repeated-measure ANOVAs to determine if
amphibian richness and abundance differed between years or
varied among hydroperiod categories between years. We
performed Students t tests to determine if amphibian or in-
vertebrate richness, amphibian abundance, or species abun-
dances were influence by the presence of fish in long-
hydroperiod wetlands. NMDS was conducted using the ordi-
nation software PC-ORD (McCune and Mefford 1997). All
other statistical procedures were analyzed using SAS (ver-
sion 8; SAS Institute Inc. 2001). Where necessary, data were
transformed to improve normality, and Bonferroni adjust-
ments were made to account for multiple testing.
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Table 1. Spearmans rank correlations of independent variables recorded for each wetland.
Wetland Max. water
size Hydroperiod IAB ISR pH Conductivity Temp. DOC depth
Wetland size 1.00
Hydroperiod 0.78 1.00
IAB 0.63 0.65 1.00
ISR 0.84 0.77 0.71 1.00
pH 0.26 0.38 0.01 0.16 1.00
Conductivity 0.07 0.07 0.03 0.09 0.26 1.00
Temp. 0.43 0.53 0.40 0.46 0.05 0.11 1.00
DOC 0.36 0.56 0.42 0.45 0.16 0.18 0.53 1.00
Depth 0.82 0.87 0.55 0.81 0.43 0.03 0.45 0.67 1.00
Note: Correlations >0.70 were considered collinear. IAB, invertebrate abundance; ISR, invertebrate species richness; DOC, dis-
solved oxygen concentration. Numbers in boldface type denote strong correlations (>0.7).

Fig. 2. Nonmetric multidimensional scaling (NMDS) scores based on a larval amphibian abundance (number/m2) by wetland site ma-
trix. R2 cutoff = 0.2. Short hydroperiod is <4 months, intermediate hydroperiod is >4 months (nonpermanent), and long hydroperiod
denotes permanent wetlands. Depth refers to maximum wetland depth and DOC is dissolved oxygen concentration. NMDS scores var-
ied significantly among hydroperiod categories for axis 1 (F[2] = 38.4, p < 0.0001) but not axis 2 (F[2] = 1.42, p = 0.24).

Results curred in 20 of the 42 wetlands sampled (48%), with an

Description of the amphibian assemblages
Nine amphibian species totaling 2918 individuals were
collected during 1998 and 1999. Species richness was 2.7
0.29 (mean SE) and ranged from 0 to 7 species per wet-
land. Larval amphibian abundance in wetlands was 1.04
0.24/m2 and ranged from 0 to 15.6/m2. Species collected
were the red-spotted newt (Notophthalmus viridescens), spot-
ted salamander (Ambystoma maculatum), wood frog (Rana syl-
vatica), green frog (Rana clamitans), bullfrog (Rana cates-
beiana), pickerel frog (Rana palustris), American toad (Bufo
americanus), spring peeper (Pseudacris crucifer), and gray
treefrog (Hyla versicolor). The most common (frequently
occurring) and abundant species was R. sylvatica, which oc-
abundance of 0.48 0.2/m2. The least common species were
R. palustris and B. americanus, which were each found in
only 4 of the 42 wetlands, and the least abundant species
was R. palustris, which attained an abundance of only
0.007 0.005/m2.
Factors influencing amphibian assemblages
NMDS revealed ecologically interpretable patterns of as-
semblage structure (Fig. 2). NMDS axis 1 accounted for
23.0% of the variation in amphibian-assemblage structure
and separated out amphibian assemblages primarily on the
basis of hydroperiod (which was strongly correlated with
depth, wetland size, and invertebrate richness (>0.7);
Tables 1, 2) and dissolved oxygen concentration. Long-

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1544 Can. J. Zool. Vol. 81, 2003

Table 2. Abiotic factors (mean SE) recorded for wetlands with short (<4 months), intermediate (>4 months; nonper-
manent), and long (permanently inundated) hydroperiods.
Abiotic variable Short hydroperiod Intermediate hydroperiod Long hydroperiod
Area (ha) 0.0530.014 a 0.270.078 b 2.530.972 c
pH 5.10.21 a 5.20.17 a 5.70.19 b
Conductivity (S) 288175 6829 189121
Temperature (C) 19.10.9 a 19.71.0 a 22.50.8 b
Dissolved oxygen concentration (mg/L) 2.30.49 a 2.10.30 a 4.40.54 b
Depth (cm) 121.9 a 232.8 b 668.0 c
Note: Water-chemistry data were not analyzed in 1999, owing to low block numbers. Values followed by a different letter are signifi-
cantly different, based on statistical pairwise comparisons.

Fig. 3. Larval amphibian species richness (A) and abundance (B) in short- (<4 months), intermediate- (>4 months; nonpermanent), and
long-hydroperiod (permanently inundated) wetlands sampled during 1998 and 1999.

hydroperiod wetlands were dominated by R. catesbeiana and
R. clamitans and generally contained more species and
higher species abundances. Conversely, short-hydroperiod
wetlands were dominated by R. sylvatica and contained few
species.
NMDS axis 2 accounted for 18.6% of the variation in
amphibian-assemblage structure and separated out amphib-
ian assemblages on the basis of invertebrate abundance
(which was strongly correlated with invertebrate genus rich-
ness (0.71), herein referred to as invertebrate abundance/
genus richness). Wetlands with high invertebrate abundance/
richness contained more species and higher abundances of
R. sylvatica, H. versicolor, B. americanus, and P. crucifer,
whereas wetlands with low invertebrate abundance contained
fewer amphibian species and lower amphibian species abun-
dances.
NMDS axis 1 scores varied among hydroperiod categories
(F[2] = 38.4, p < 0.0001). Amphibian assemblages in long-
hydroperiod wetlands differed significantly from those in
short- (p < 0.0001) and intermediate-hydroperiod (p < 0.0001)
wetlands, whereas larval amphibian assemblages in short-
and intermediate-hydroperiod wetlands did not vary signifi-
cantly. NMDS axis 1 scores did not differ with respect to the
blocking factor (F[2,13] = 0.45, p = 0.38), indicating that
amphibian-assemblage structure was not significantly influ-
enced by the spatial position of the study sites. NMDS axis
2 scores did not differ significantly with respect to hydro-
period (F[2] = 1.42, p = 0.24) or the blocking variable

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Babbitt et al. 1545

Table 3. Relationship between dependent (amphibian) and independent variables (abiotic and bi-
otic characteristics) in study wetlands.
Dependent variable Independent variable 2 p
Amphibian species richness Hydroperiod 12.52 0.0004*
Invertebrate abundance 7.86 0.005*
Amphibian abundance Invertebrate abundance 8.33 0.0039*
Rana catesbeiana Invertebrate abundance 4.48 0.034
Rana clamitans Hydroperiod 3.98 0.046
Invertebrate abundance 5.7 0.017
Rana palustris Insufficient occurrence
Rana sylvatica Hydroperiod 5.50 0.019
Bufo americanus Hydroperiod 5.96 0.0146
Invertebrate abundance 30.01 <0.0001*
Pseudacris crucifer Invertebrate abundance 36.2 <0.0001*
Hyla versicolor Invertebrate abundance 21.8 <0.0001*
Notophthalmus viridescens Hydroperiod 8.25 0.0041*
Invertebrate abundance 3.79 0.0514
Ambystoma maculatum Invertebrate abundance 3.2 0.074
Note: Analyses were based on GLMs using SAS Institute Inc. (2001).
*Significance after Bonferroni adjustments.

(F[2,13] = 0.33, p = 0.57). Thus, the effect of invertebrate
abundance on amphibian assemblages was similar among
hydroperiod categories and was not influenced by the spatial
position of study sites.
Amphibian species richness was positively influenced by
2
hydroperiod ([2,41] = 12.52, p = 0.0047) (Fig. 3A).
Bonferroni pairwise comparisons indicated that species rich-
ness was significantly lower in short-hydroperiod than in
long-hydroperiod wetlands (p < 0.0001). Amphibian species
richness was also higher in intermediate- than in short-
hydroperiod wetlands, although this difference was not sig-
nificant after Bonferroni adjustments (p = 0.029). Species
richness did not differ significantly between intermediate-
and long-hydroperiod wetlands. Species richness increased
from 1.3 0.29 in short-hydroperiod wetlands to 3.9 0.45
in long-hydroperiod wetlands. Total amphibian abundance
(Table 3) did not vary significantly among hydroperiod cate-
gories, although it was highest in intermediate-hydroperiod
wetlands (Fig. 3B). Relative abundances of larval amphibi-
ans varied among hydroperiod categories (Figs. 4A, 4B) and
abundances of most amphibian species were significantly in-
fluenced by hydroperiod (Table 3). Rana catesbeiana,
R. clamitans, B. americanus, and N. viridescens were influ-
enced positively by hydroperiod, whereas R. sylvatica was
negatively influenced by hydroperiod. Ambystoma macula-
tum attained higher abundance in wetlands with intermediate
hydroperiods. Rana palustris abundance was not signifi-
cantly influenced by hydroperiod, despite the fact that it was
found only in long-hydroperiod wetlands. The nonsignificant
result was due to the small sample size for this species.
Fish occurred in 9 of 14 long-hydroperiod wetlands. Pred-
atory species caught or observed while dip-netting included
the bullhead catfish (Ameiurus sp.), pickerel (Esox sp.), and
sunfish (Lepomis sp.). Although both amphibian species
richness and abundance were numerically lower in wetlands
with fish, the differences were not significant (t = 1.78, p =
0.17 (Fig. 5A), and t = 2.44, p = 0.11 (Fig. 5B), respec-
tively). Several species were influenced by the presence of
fish (Fig. 5C). Most notably, A. maculatum and R. sylvatica
were not found in permanent wetlands with fish. Rana
catesbeiana was positively associated with fish presence (t =
3.45, p = 0.042), whereas B. americanus (t = 6.49, p = 0.01)
and H. versicolor (t = 4.11, p = 0.033) were negatively asso-
ciated with fish presence; however, with Bonferroni adjust-
ments these results were not significant.
Larval amphibian species richness, total abundance, and
abundance of most species were correlated with predatory
invertebrate abundance / genus richness. Amphibian species
2 2
richness ([41] = 12.5, p = 0.0004) and abundance ([41] =
8.3, p = 0.0039) were positively correlated with invertebrate
abundance / genus richness (Table 3). For 3 of the 9 amphib-
ian species (B. americanus, P. crucifer, and H. versicolor)
this correlation was significant, and for 3 others (R. cates-
beiana, R. clamitans, and N. viridescens) the relationship
was strong but not significant (Table 3).
Assemblage differences between years
Nonpermanent wetlands had shorter hydroperiods in 1999
than in 1998, owing to less rainfall in 1999, and this resulted
in amphibian-assemblage differences between years. Am-
phibian species richness was significantly lower (F[1] =
17.65, p < 0.0001) in 1999 (1.5 0.22) than in 1998 (2.3
0.27) (Fig. 6A), although amphibian abundance did not dif-
fer (F[1] = 1.04, p = 0.31) (Fig. 6B). The interaction between
year and hydroperiod was not significant for either species
richness (F[1,2] = 0.63, p = 0.54) or abundance (F[1,2] = 2.34,
p = 0.54), suggesting that variation in species richness and
abundance among hydoperiod categories was not influenced
by year. In 1998, 3 species (R. sylvatica, P. crucifer, and
A. maculatum) were found in short-hydroperiod wetlands,
7 species (P. crucifer, H. versicolor, R. sylvatica, R. clamitans,
N. viridescens, B. americanus, and A. maculatum) in
intermediate-hydroperiod wetlands, and 8 species (all but
R. sylvatica) in long-hydroperiod wetlands. In 1999, only
1 species (R. sylvatica) was found in short-hydroperiod
wetlands, 6 species (P. crucifer, H. versicolor, R. sylvatica,

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1546 Can. J. Zool. Vol. 81, 2003

Fig. 4. (A) Relative abundances of species in short- (<4 months), intermediate- (>4 months; nonpermanent), and long-hydroperiod (per-
manently inundated) wetlands sampled during 1998 and 1999 (Amac, Ambystoma maculatum; Nvir, Notophthalmus viridescens; Hver,
Hyla versicolor; Pcru, Pseudacris crucifer; Bame, Bufo americanus; Rsyl, Rana sylvatica; Rpal, Rana palustris; Rcla, Rana clamitans;
Rcat, Rana catesbeiana). (B) Relative abundance of each species with respect to wetland hydroperiod.

R. clamitans, N. viridescens, and A. maculatum) in
intermediate-wetlands, and 8 species (all but R. sylvatica) in
long-hydroperiod wetlands.
There were no significant differences in the abundance of
any species between years, although relative abundances of
species in each hydroperiod category differed (Fig. 7). In
1998, R. sylvatica attained the highest relative abundance
(79%) in short-hydroperiod wetlands, B. americanus and
P. crucifer larvae had the highest relative abundance (26%
and 22%, respectively) in intermediate-hydroperiod wet-
lands, and R. catesbeiana larvae had the highest relative
abundance (31%) in long-hydroperiod wetlands (Fig. 7A). In
1999, R. sylvatica larvae (99%) dominated short-hydroperiod
wetlands, whereas R. sylvatica (77%) and P. crucifer (17%)
larvae were most abundant in intermediate-hydroperiod
wetlands. Bufo americanus larvae attained the highest abun-
dance in long-hydroperiod wetlands (48%), despite being
present in only two of these wetlands (Fig. 7B).
Discussion
Our goal was to better understand the relative influence of
hydroperiod and associated changes in predator composition
and abundance on larval amphibian assemblages. We were
able to achieve this goal by selecting relatively undisturbed
wetlands and successfully factoring out spatial differences
attributed to landscape characteristics (i.e., we spatially
blocked our study sites).
Hydroperiod was the most important variable influencing
amphibian assemblages in this study. Long-hydroperiod wet-
lands contained 2 species that bred exclusively in these habi-
tats (R. catesbeiana and R. palustris), and the most abundant

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Babbitt et al.
Fig. 5. Larval amphibian species richness (A), abundance (number/m2) (B), and individual species abundances (number/m2) (C) in
wetlands with and without predatory fish. Wetlands were sampled during 1998 and 1999.
species were R. catesbeiana, R. clamitans, B. americanus,
and P. crucifer. Intermediate-hydroperiod wetlands were im-
portant for A. maculatum, contained high abundances of
R. sylvatica, and were suitable breeding habitats for most
amphibians. Furthermore, intermediate-hydroperiod wetlands
are important breeding habitat for the blue-spotted salaman-
der (Ambystoma laterale), which occurs in the region but is
not common in the study area and was not recorded. Short-
hydroperiod wetlands were most important for R. sylvatica,
which breeds in spring when competitors and predators are
relatively few and the species is able to reach metamorpho-
sis in as little as 68 weeks (Hopey and Petranka 1994).
Nevertheless, it is also important to note that metamorphosis
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1547
of even the fastest developing species may not occur in
short-hydroperiod wetlands during dry years; 6 of the 14
short-hydroperiod study wetlands dried before mid-May (the
first sampling period) in 1999.
Species richness was significantly lower in short-
hydroperiod wetlands (<4 months) than in intermediate- and
long-hydroperiod wetlands. Only 4 amphibian species were
found in these wetlands, whereas intermediate- and long-
hydroperiod wetlands contained 7 and 9 species, respec-
tively. Moreover, total abundance was higher in intermediate-
hydroperiod wetlands, although this difference was not
statistically significant. Empirical evidence suggests that
amphibian species richness is often highest at intermediate
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Fig. 6. Differences in larval amphibian species richness (A) and larval amphibian abundance (B) between 1998 (a wet year) and 1999
(a dry year).
periods along the hydrological gradient (Heyer et al. 1975;
Wilbur 1984; Snodgrass et al. 2000a, 2000b). Intermediate-
hydroperiod wetlands may have higher amphibian species
richness than either ephemeral or permanent wetlands be-
cause they are inundated long enough to permit metamor-
phosis for most species, but short enough to prevent
colonization by predatory fish (Wellborn et al. 1996). This
trend was not evident in our study. We did not find a signifi-
cant difference in species richness between intermediate-
hydroperiod and permanent wetlands, and overall we found
an increase in species richness across the hydrological gradi-
ent. We attribute this to the ability of longer hydroperiod
wetlands to accommodate species with lengthy development
(e.g., R. clamitans and R. catesbeiana), and to the increased
depth in long-hydroperiod wetlands that allows some species
to overwinter without freezing. Moreover, compared with
other regions (e.g., the southeastern United States), a large
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Can. J. Zool. Vol. 81, 2003
proportion of species in this study (7 of 9 recorded) are
known to coexist with predatory fish.
Predatory fish
Neither amphibian species richness nor abundance in per-
manent wetlands was significantly influenced by the pres-
ence of predatory fish, although both parameters were
numerically lower in wetlands containing fish. In addition,
of the 9 amphibian species captured during this study, all but
2 (R. sylvatica and A. maculatum) occurred in wetlands con-
taining predatory fish. Ambystoma laterale (not captured in
this study) is also known to avoid permanent wetlands con-
taining predatory fish. Abundances of H. versicolor and
B. americanus were lower in wetlands with predatory fish.
Conversely, the abundance of R. catesbeiana tadpoles tended
to be higher in such wetlands and this was possibly due to
reduced competition from other larval amphibians (Werner
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Babbitt et al.
Fig. 7. Relative abundance of amphibian species in short- (<4 months), intermediate- (>4 months; nonpermanent), and long-
hydroperiod (permanently inundated) wetlands in 1998 (a wet year) (A) and 1999 (a dry year) (B). See Fig. 4 for species abbrevia-
tions.
and McPeek 1994) coupled with antipredator defenses (e.g.,
toxic skin; Kats et al. 1988).
In contrast to our findings, other studies have demon-
strated a negative correlation between the presence of preda-
tory fish and amphibian-assemblage parameters (e.g., Heyer
et al. 1975; Hayes and Jennings 1986; Hecnar and
MCloskey 1997). Hecnar and MCloskey (1997) found a
negative correlation between the presence of predatory fish
and larval amphibian species richness in southwestern
Ontario, Canada. Similarly, M.J. Baber, K.J. Babbitt, F. Jor-
dan, H.L. Jelks, and W.H. Kitchens (unpublished manu-
script) reported that only 4 of the 12 native anuran species in
southern Florida occur in permanent wetlands containing
predatory fish. Variation among regions in the effect of pred-
atory fish on amphibian species richness may depend largely
on the predator and prey species pool (Hecnar and
MCloskey 1997). Perhaps most importantly, the northern
New England amphibian species pool includes a high pro-
portion of species known to utilize permanent wetlands with
predatory fish, whereas other regions (e.g., the southeast)
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contain a higher proportion of species (e.g., treefrogs, Hyla
spp.) whose larvae are vulnerable to predatory fish (Kats et
al. 1988; Smith et al. 1999; Baber 2001). Alternatively, be-
cause our study included only 14 permanent wetlands and
because we measured only fish presence, we may have
lacked the statistical power to uncover more subtle effects
and we were unable to examine possible relationships be-
tween predatory-fish abundance and patterns of larval am-
phibian assemblages. Nevertheless, our results suggest that
there was no dramatic impact of predatory fish on larval am-
phibian species richness in permanent wetlands in this study,
although predatory fish seemingly contribute to variation in
species composition and abundance among permanent
wetlands.
Predatory invertebrates
The richness and the abundance of several amphibian spe-
cies were positively correlated with invertebrate richness and
total invertebrate abundance. Specifically, wetlands with low
amphibian species richness and abundance also had depaup-
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erate predatory-invertebrate assemblages, whereas wetlands
with species-rich and abundant amphibian assemblages sup-
ported species-rich and abundant invertebrate assemblages.
This suggests that species-rich and abundant predatory in-
vertebrate assemblages do not lower amphibian species rich-
ness or necessarily lead to low amphibian abundances.
Rather, invertebrates and amphibians may be responding
similarly to differences in abiotic or productivity-related fac-
tors.
Variation in amphibian assemblages among wetlands has
been attributed to the degree of canopy cover (Werner and
Glennemeier 1999; Skelly et al. 1999, 2002). Wetlands com-
pletely enclosed by canopy may have lower dissolved oxy-
gen concentrations, less algal food because of lower light
levels, and cooler water, all of which may limit growth and
prevent metamorphosis before drying events occur (Werner
and Glennemeier 1999; Skelly et al. 2002). For example,
Skelly et al. (1999) suggested that forest canopy closure lim-
ited the breeding of H. versicolor (and other species) to
open-canopy wetlands, which tend to be intermediate and
long in hydroperiod. Clearly, further field and experimental
studies are necessary to determine the underlying cause of
the complementary richness/abundance patterns of amphib-
ian larvae and aquatic insect predators.
Conservation implications
There is considerable interest among conservation biolo-
gists in modifying existing wetland regulations to ensure
better protection of amphibians and associated organisms.
Current regulations do not adequately protect the breeding
habitat of many amphibian species, and may fail to protect
nonbreeding habitat (surrounding upland areas). Federal and
state regulations designed to protect isolated wetlands of
high conservation value are largely based on wetland size,
although three states in New England (Massachusetts, New
Hampshire, and Connecticut) regulate the filling of isolated
depressions that contain surface water for at least 2 continu-
ous months during spring and summer (Colburn 1995;
Donahue 1995; Tappan 1997; Paton and Crouch 2002). Nev-
ertheless, several researchers have recently pointed out the
limited practical use of using wetland size as a basis for wet-
land protection (Semlitsch and Bodie 1998; Snodgrass et al.
2000a, 2000b; Paton and Crouch 2002).
Based on the relationship between larval amphibian as-
semblages and hydroperiod in this study, hydroperiod is
likely a better indicator of amphibian species richness and
probably amphibian productivity (the successful develop-
ment of metamorphs) than wetland size. Although we did
find that wetland hydroperiod and size were strongly and
positively correlated in this study, hydroperiod had a stron-
ger influence on larval amphibian assemblage structure
than did wetland size. Intermediate- and long-hydroperiod
wetlands had higher species richness than short-hydroperiod
(<4 months) wetlands, which were relatively depauperate.
From the standpoint of amphibian conservation, this high-
lights the importance of differentiating between ephemeral
wetlands (classified as short-hydroperiod wetlands in this
study) and wetlands with hydroperiods >4 months (classified
as intermediate-hydroperiod wetlands in this study). Simi-
larly, Paton and Crouch (2002) concluded that amphibian
species in southern Rhode Island require hydroperiods of at
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Can. J. Zool. Vol. 81, 2003
least 4 continuous months to meet the habitat requirements
for most pond-breeding amphibians.
It must be noted that wetlands with hydroperiods
>4 months are still ecologically and functionally important
components of a the landscape. These wetlands are impor-
tant breeding sites for R. sylvatica and P. crucifer and may
support unique invertebrate assemblages and provide critical
habitat for some species (e.g., fairy shrimp, Eubranchipus
spp.). Moreover, seasonally inundated wetlands have hydro-
periods that vary among years, and wetlands that typically
have hydroperiods >4 months may support more species-rich
assemblages during extremely wet years. Finally, these
wetlands serve as stepping stones for dispersing amphibians,
and thus contribute to metapopulation dynamics (Hanski and
Gilpin 1991; Gibbs 1993).
Based on the above, when landowners and agencies at-
tempt to manage woodlands for pond-breeding amphibians,
the presence of ponds should not be used as a single predic-
tor. Our results demonstrate that hydroperiod strongly influ-
ences larval amphibian assemblage parameters, particularly
species richness and composition. Protective measures de-
signed to retain a diversity of wetlands that span the hydro-
logical gradient are therefore necessary to ensure the long-
term persistence of amphibian biodiversity. Other factors
such as wetland density, upland-habitat suitability, and land-
scape connectivity are also important (Semlitsch 2000). We
recommend that attempts be made to broadly classify ponds
with respect to hydroperiod because such efforts may ulti-
mately minimize the negative impacts of development on lo-
cal and regional amphibian species richness.
Our results suggest that, all else being equal, modifying
wetlands with hydroperiods <4 months may have less impact
on amphibian species richness than modifying seasonally in-
undated wetlands with longer hydroperiods. We expect that
our conclusions will apply to the northeastern United States
and southeastern Canada. However, this scenario is unlikely
to apply universally, and, in a specific region, is largely de-
pendent on the number and proportion of species that are
able to rapidly develop to metamorphosis (which is typically
higher in warmer climates) and the impact of predatory fish
on larval amphibian assemblages. For example, wetlands in
Florida with hydroperiods less than 4 months may contain a
relatively high proportion of the regional species pool be-
cause most species are able to reach metamorphosis in less
than 4 months (Babbitt and Tanner 2000). Efforts to broadly
classify wetland hydroperiods will also enable conservation
planners to minimize impacts on relatively underrepresented
wetland types. For example, in regions where ephemeral
ponds are rare, alternative development projects that modify
wetland(s) with longer hydroperiods may be less damaging
overall. This may hold true in many regions where mitiga-
tion efforts are essentially substituting seasonal wetlands for
permanent water bodies (Pechmann et al. 2001).
Acknowledgments
Funding for this project was provided by the New Hamp-
shire Fish and Game Department, the New Hampshire De-
partment of Environmental Services, the Environmental
Protection Agency, and the University of New Hampshire
Graduate School. We sincerely thank S. Callaghan, B. Wright,
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Babbitt et al.
T. Ayer, M. Tarr, M. Cole, and C. Meaney for assisting with
data collection and invertebrate sorting. This is Scientific
Contribution No. 2178 from the New Hampshire Agricul-
tural Experiment Station.
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