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R. Tumlison and B. Serviss
22001133 SOUSToHuEthAeSaTstEeRrnN N NaAtuTrUaRlisAtLIST 12V(o3l). :1527,9 N–5o8. 83
Novel Food Habits of Branchiate Mole Salamanders
(Ambystoma talpoideum) from Southwestern Arkansas
Renn Tumlison1,* and Brett Serviss1
Abstract - Branchiate Ambystoma talpoideum (Mole Salamanders) in fishless ponds can
be large enough to act as predators, rather than competitors, during the spring breeding
season of other amphibians. Food habits of high-density Mole Salamander populations
from 2 proximate woodland ponds in Clark County, AR were examined before and after
egg-laying by frogs, with an expectation that the salamanders likely would consume
hatching tadpoles. However, salamanders instead commonly fed on the novel item of
freshly-laid frog eggs. Results from both ponds indicated that the salamanders, perhaps
due to food limitation, consumed smaller prey items than would be expected and heavily
consumed frog eggs, a novel item.
Introduction
Many amphibians reduce risk of predation by breeding in fishless ponds
(Semlitsch 1988). Species that either breed early (e.g., Ambystoma opacum
Gravenhorst [Marbled Salamander], Boone et al. 2002) or grow quickly (e.g.,
Ambystoma tigrinum Green [Tiger Salamander], Wilbur 1972) may achieve a
body size advantage for predation. In Arkansas, both the metamorphic and paedomorphic
forms of Ambystoma talpoideum Holbrook (Mole Salamander) breed
in winter, whereas many other amphibians breed in the same ponds in the spring
(Trauth et al. 2004). Resulting syntopic occurrence of branchiate Mole Salamanders
and larvae of other amphibian species in such ponds is often characterized
by differences in size and ontogeny (Nyman 1991), which might allow predation
by the larger species (Stenhouse 1985, Stenhouse et al. 1983), facilitated by
the larger gape of the mouth (Freda 1983, Taylor et al. 1988). Although fishless
ponds provide breeding sites for several potentially competing species of amphibians,
“priority effects” can change the relationship from one of competition
to one of predation (Blaustein and Mar galit 1996).
During the winter of 2002, we located two fishless ponds that supported
populations of branchiate Mole Salamander at the periphery of their known distribution
(Trauth et al. 1993) in Clark County, AR. Shoreline seine samples in
both ponds averaged 20 individuals/m2—a value considered by Semlitsch (1987)
to represent a high density population. High population densities of aquatic
salamanders can create food limitation in their environments, possibly causing
increased predation on other amphibians (Morin 1981, Stenhouse et al. 1983,
Taylor et al. 1988).
Few studies of food habits of larger branchiate Mole Salamanders exist. Larval
Mole Salamanders are known to feed mostly on pond invertebrates (Petranka
1Department of Biology, Henderson State University, Arkadelphia, AR 71999. *Corresponding
author - tumlison@hsu.edu.
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2013 Southeastern Naturalist Vol. 12, No. 3
580
1998) although paedomorphic individuals are known to take occasional conspecific
ova (McAllister and Trauth 1996). The Mole Salamander is an aggressive
species, a superior competitor to other larval salamanders (Walls and Jaeger
1987), and the facultative paedomorphosis it exhibits may allow the exploitation
of productive but transient resources within the pond environment (Semlitsch
1987). We hypothesized that the high density of the populations we found could
cause food limitation within the environment and result in shifts in prey selection
as new prey become available.
The spring breeding season produces a surge in availability of potential amphibian
prey as other salamanders and frogs begin to oviposit. Thus, our field
situation presented an opportunity to evaluate whether the high-density population
of branchiate Mole Salamanders would consume large numbers of hatchling
larvae of other amphibians. High occurrences of amphibian prey are undocumented
in studies of Mole Salamander food habits.
Methods and Materials
Laboratory study
We conducted laboratory experiments to develop predictions for the field
study. Because it is commonly known that feeding in amphibians is often initiated
by movement, we placed four branchiate Mole Salamanders (snout–vent
lengths [SVL] from 30–35 mm) individually in 1-gallon plastic containers and
supplied each with 12 hatchling Lithobates sphenocephalus Cope (Southern
Leopard Frog) tadpoles to evaluate feeding attempts on motile amphibian prey.
These salamanders were taken from the field the previous day and were selected
because they did not have either distended or shrunken stomachs (they were neither
full nor starving). A similar trial was conducted with a different set of four
Mole Salamanders and egg masses of L. sphenocephalus, in which there would
be little or no movement.
Further, another set of 4 novice branchiate Mole Salamanders were placed
in separate aquaria with egg masses of Ambystoma maculatum Shaw (Spotted
Salamander). Though unhatched, the embryos in these egg masses were already
elongated, and moved upon stimulation.
We closely observed each of these trials for 30 minutes, recording the behavior
and positioning of the salamanders in relation to the potential prey, and
the frequency and results of each predation attempt. This portion of the study
allowed us to examine whether and how the salamanders fed on nonactive, unhatched
larvae versus active larvae or motile hatchlings.
Field study
The field study site was a woodland area located 8 km NW of Gurdon, Clark
County, AR (Sec. 27, T9S, R21W). The forest was a pine (Pinus)–hardwood
(mostly Carya [hickory] and Quercus [oak]) mix. Two ponds, located about 0.5
km apart, were present within this forest managed by the Ross Foundation, Arkadelphia,
AR. Both ponds were permanent: the area of pond 1 was 300 m2 at low
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2013 Southeastern Naturalist Vol. 12, No. 3
water and 340 m2 at high water; and the area of pond 2 was 340 m2 at low water
and 390 m2 at high water.
Lithobates palustris LeConte (Pickerel frogs) and Spotted Salamanders were
beginning to lay eggs in the ponds by very late February. On 7 March 2002, before
many of the available Pickerel Frog eggs hatched (which usually occurs within
about 10 days of oviposition, Trauth et al. 2004), a sample of 59 salamanders was
collected from pond 1 by use of long-handled dip nets and seines (sample 1), and
preserved for stomach analysis. Specimens were taken as randomly as possible,
without selection based on body size or degree of distension of the abdomen. We
allowed one week for the bulk of the increasing number of frog eggs to hatch,
and on 15 March we collected an additional 31 in the same manner (sample 2),
and preserved them for comparison analysis of food habits, size, and sex ratio.
We also sampled with a benthic net to detect amphibian hatchling s.
Just after the first sampling period, pond 2 was discovered and found to support
a large population of branchiate Mole Salamanders, and we sampled the
pond on 15 March to allow comparison of food habits between ponds on the
same date. As with pond 1, we minimized shoreline disturbance in pond 2 while
collecting 40 specimens (sample 3) with long-handled dip nets a nd seines.
These samples allowed comparison of food habits of branchiate Mole Salamanders
from one pond before and after the hatching of the spawn of other
amphibians, and a comparison of food habits within 2 local ponds on the same
date, and under similar environmental conditions. Other than the qualitative
assessment of the increase in amphibian eggs, no food availability data were
obtained for potential invertebrate prey items in the ponds.
We measured SVL of preserved specimens and determined the sex by internal
examination of gonads, aided by a dissecting microscope. Stomachs were removed
and opened, and food items were separated, counted, and identified to the
lowest taxonomic level possible (Pennak 1989, Thorp and Covich 1991).
We summed the number of different taxa consumed by each salamander, then
performed ANOVAs to determine whether diversity of foods varied by pond and
date. Separate ANOVAs were used to examine differences between dates within
pond 1, and between ponds 1 and 2 on the same date, evaluating total numbers
of each major food item as the dependent variable. To reduce error with multiple
tests, Bonferroni adjustments were made in analyses comparing ponds on the
same date, and separately when comparing dates for the same pond (Rice 1989).
Further, percent of salamanders ingesting each food item was calculated to evaluate
how commonly individuals consumed a prey taxon, and the total number of
each item was calculated to rank the overall importance of the item as a food.
Results
Laboratory study
The lab trials with eggs and tadpoles of Southern Leopard Frogs provided different
results. When placed in containers with frog eggs, all Mole Salamanders
positioned themselves near the eggs, but only occasionally attempted to ingest
R. Tumlison and B. Serviss
2013 Southeastern Naturalist Vol. 12, No. 3
582
an egg. Some eggs, including their gelatinous envelopes, were ingested then spit
out (2 of the 4 Mole Salamanders attempted to feed on eggs, temporarily ingesting
one and two eggs in those two cases). When presented with mobile tadpoles,
however, the salamanders consumed 66–100% (8–12) of the prey within 30 minutes
in each of the four trials.
During the lab trials using Spotted Salamander eggs with elongated embryos,
all four Mole Salamanders positioned themselves on top of the egg masses and
pushed their heads into the mass. The embryos, which moved within their eggs
on disturbance, were consumed from within the gelatin of the egg masses with
apparently little or no intake of gelatin. Mole Salamanders consumed 1–3 Spotted
Salamander embryos within the four 30-minute trials. A l l s u c c e s s f u l
feeding observed in lab trials was in response to motion of prey. Based on these
laboratory observations, we anticipated that the large number of branchiate Mole
Salamanders in the ponds would commonly consume hatchlings, but not eggs, of
other amphibians.
Field study
Temperature of pond 1, which had a maximum depth of 75 cm, was 17.0° C
on 7 March. Elongated larvae were already present in numerous, large Spotted
Salamander egg masses, which were green with the symbiotic algae Oophila
amblystomatis Lambert Ex Printz. A few scattered masses of Pickerel Frog eggs
had recently been laid, and elongation of the embryos was not e vident.
On 15 March, the previously deposited eggs of the Pickerel Frogs had disappeared,
which we presumed to have hatched, and new eggs had been laid.
However, no tadpoles were found during benthic net sampling of the pond. Some
of the Spotted Salamander egg masses contained no embryos, but none of their
hatched larvae were found during benthic sampling.
Primary foods detected during this study included a variety of small crustaceans,
insects, and frog eggs (Table 1). Unexpectedly, however, no tadpoles were
found in stomachs or in benthic-net-collected samples from the ponds. Instead,
many salamanders had distended their stomachs with eggs of Pickerel Frogs,
including the gelatinous matrix.
Analysis of variance (ANOVA) indicated no differences in any food taxa
consumed based on sex (P > 0.05), therefore sexes were combined for further
analysis. All but three of the 130 specimens (97.7%) had food items in the stomach.
The number of different taxa of food items in a stomach ranged from 0–7 in
sample 1 (mean = 2.6), 3–8 (mean = 5.2) in sample 2, and 1–8 (mean = 5.2) in
sample 3. A significantly greater diversity of foods was taken by individuals in
pond 1 on the latter sample date (sample 1 vs. sample 2: ANOVA, F = 65.54; d.f.
= 1, 88; P < 0.0001), yet the diversity of foods taken by individuals on the same
date but in different ponds was the same (sample 2 vs. sample 3: F = 0.03; d.f. =
1, 69; P > 0.05).
The comparison of foods taken in pond 1 on different dates demonstrated
fewer differences than in the comparison between ponds. The only significant
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2013 Southeastern Naturalist Vol. 12, No. 3
differences detected were increases in the frequency of isopods, zygopterans,
chaoborids, and frog eggs (Table 2). In the field, we observed that the number of
frog egg masses consumed increased between the sampling periods, and presume
that all the increases in consumed taxa were either due to increases in availability
due to reproduction of the prey or by increased activity (either of the prey
or predator). A higher percentage of salamanders were eating almost every food
category on 15 March compared with 7 March. On average, stomachs contained
twice as many prey taxa on 15 March.
The comparison of foods consumed on the same date (15 March) demonstrated
differences between ponds. In pond 1, Mole Salamanders consumed
significantly more isopods, amphipods, zygopterans, chaoborids, and frog eggs,
Table 1. Food items recovered from stomachs of 130 branchiate Ambystoma talpoideum from
southwestern Arkansas, March 2002. Sample 1 = pond 1, 7 March; sample 2 = pond 1, 15 March;
sample 3 = pond 2, 15 March. Miscellaneous category includes unidentified Hemiptera. For each
sample, percent of salamanders consuming each item is given. Also, the total number of individuals
of each prey item (and the percent of the total foods represent ed) is provided per sample.
% of salamanders
eating item in sample Total # (%) per sample
Prey taxon 1 (n = 59) 2 (n = 31) 3 (n = 40) 1 2 3
Annelida
Oligochaeta - 3.2 - - 3 (0.4) -
Crustacea
Cladocera 27.1 32.3 70.0 210 (25.9) 46 (5.7) 1773 (63.2)
Copepoda 27.1 67.7 77.5 104 (12.8) 104 (12.9) 366 (13.1)
Ostracoda 6.8 9.7 42.5 16 (2.0) 3 (0.4) 61 (2.2)
Isopoda 13.6 54.8 22.5 14 (1.7) 24 (3.0) 9 (0.3)
Amphipoda 54.2 64.5 17.5 50 (6.2) 41 (5.1) 7 (0.2)
Decapoda 1.7 - 2.5 1 (0.1) - 1 (less than 0.1)
Insecta
Ephemeroptera 13.6 6.5 - 8 (1.0) 2 (0.3) -
Odonata
Anisoptera 3.4 3.2 - 2 (0.2) 1 (0.1) -
Zygoptera - 16.1 - - 5 (0.6) -
Heteroptera
Corixidae 18.6 25.8 60.0 13 (1.6) 9 (1.1) 74 (2.6)
Lepidoptera - - 2.5 - - 1 (less than 0.1)
Coleoptera 13.6 35.5 5.0 14 (1.9) 13 (1.6) 28 (1.0)
Diptera
Chironomidae 8.5 19.4 70.0 8 (1.0) 9 (1.1) 62 (2.2)
Chaoboridae 8.5 77.4 47.5 6 (0.7) 76 (9.4) 37 (1.3)
Hymenoptera
Formicidae - 3.2 - - 1 (0.1) -
Gastropoda (limpet) - - 2.5 - - 1 (less than 0.1)
Amphibia
Ranidae 50.8 96.8 77.5 363 (44.8) 469 (58.1) 383 (13.7)
Miscellaneous 1.7 3.2 2.5 1 (0.1) 1 (0.1) 14 (less than 0.1)
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2013 Southeastern Naturalist Vol. 12, No. 3
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but in pond 2 significantly more copepods, corixids, and chironomids were consumed
(Table 2). Food items most commonly taken from either pond tended to
be taken by a higher percentage of Mole Salamanders in that pond (Table 1),
with the exception of amphipods, which were taken more often in pond 1 but by
a higher percentage of salamanders in pond 2.
The presence of enlarged, yolk-filled follicles confirmed that 2 of the 72
females were paedomorphic (Semlitsch 1985). The remaining females in the
samples were developing follicles, and we observed some metamorphosis
occurring in salamanders in the ponds; thus we could not determine if the population
consisted of all paedomorphs, or of a mix of paedomorphic and larval
metamorphic individuals. In external appearance, our specimens most closely
matched the series of images of paedomorphic individuals provided by Trauth
et al. (2004).
Table 2. P-values for ANOVAs of the effects of pond and date on food items recovered from
stomachs of 130 branchiate Ambystoma talpoideum from southwestern Arkansas, March 2002. *
= significant difference (P < 0.05) after Bonferroni adjustment (Rice 1989) was applied separately
to analysis by pond and by date.
P-values
Prey taxon Pond (d.f. = 1, 69) Date (d.f. = 1, 88)
Annelida
Oligochaeta 0.2589 0.1690
Crustacea
Cladocera 0.0306 0.1687
Copepoda 0.0102* 0.1089
Ostracoda 0.0160 0.4959
Isopoda 0.0066* 0.0027*
Amphipoda 0.0001* 0.0682
Decapoda 0.3825 0.4716
Insecta
Ephemeroptera 0.1061 0.3133
Odonata
Anisoptera 0.2589 0.9676
Zygoptera 0.0079* 0.0013*
Heteroptera
Corixidae 0.0009* 0.5345
Lepidoptera 0.3825 -
Coleoptera 0.6794 0.1364
Diptera
Chironomidae 0.0001* 0.2869
Chaoboridae 0.0034* 0.0001*
Hymenoptera
Formicidae 0.2589 0.1690
Gastropoda (limpet) 0.3825 -
Amphibia
Ranidae 0.0303* 0.0001*
Miscellaneous 0.3825 0.4716
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Sex ratios were female-biased in pond 1 (sample 1: 0.63 males/female; sample
2: 0.82 males/female) but slightly male-biased in pond 2 (1.11/1). Raymond and
Hardy (1990) found a sex ratio bias favoring males in some years, while Petranka
(1998) observed no sex ratio bias.
The mean SVL of Mole Salamanders from pond 1 was 36.8 mm on both dates
sampled (range = 33–41 mm on 7 March and 33–40 mm on 15 March), just large
enough to begin metamorphosis (Semlitsch 1987). From pond 2, mean SVL was
34.4 mm (range 28–40 mm), which is slightly less than Semlitsch’s (1987) critical
value of 35 mm for metamorphosis.
Discussion
Based on preliminary laboratory observations, it was expected that salamanders
would consume tadpoles in the field. However, the evaluation of stomach
contents revealed that many frog eggs never developed to the hatchling stage. Of
the 1215 frog eggs found in all stomachs, none was found in which the embryos
had begun to elongate, and the gelatinous matrix was present along with the embryo
in the stomachs. Likewise, the intact, unwrinkled membranes apparently did
not have adequate time to expand via absorption of water, which begins immediately
upon egg deposition (Duellman and Trueb 1986), thereby corroborating the
conclusion that eggs were eaten during or just after oviposition. To that end, we
conjecture that the motion of the eggs being extruded by the frog was enough to
elicit a feeding response by the salamanders; otherwise they had learned to take
motionless deposited eggs as food.
Several field-collected egg masses of frogs hatched successfully after removal
to the lab; thus, all eggs were presumed to be fertile and capable of elongation.
Although numerous egg masses had been present, no larval Spotted Salamanders
or frog tadpoles were found during benthic net sampling of the ponds. Therefore,
it is likely that predation by the Mole Salamanders essentially nullified reproductive
success of other species of amphibians about the time of oviposition. No
tadpoles were found during additional field sampling over succes sive weeks.
Interspecific predation in amphibians has been known to cause total spawn
failure (Banks and Beebee 1987, Walters 1975), but this level of predation has
not been suggested for sub-metamorphic or paedomorphic Mole Salamanders
such as we observed. McAllister and Trauth (1996) found that paedomorphic
Mole Salamanders consumed a few conspecific ova as well as congeneric larvae.
The gelatinous matrix probably is of low nutritional value (Petranka et al.
1998), although the egg itself contains useful nutrients. Regester et al. (2008)
noted that energetic importance of amphibian prey is underestimated in studies
that measure abundance of prey items; thus, the high levels of occurrence
of amphibian prey reported herein were likely of even greater energetic importance
to the salamanders.
Considering the abundance of salamanders in the ponds, food limitation
(Morin 1981, Stenhouse et al. 1983, Taylor et al. 1988) may have forced the
ingestion of some of the foods documented during our study. Under the stress
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2013 Southeastern Naturalist Vol. 12, No. 3
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of food limitation, tadpoles of Lithobates sylvaticus LeConte (Wood Frog) prey
upon embryos of the Spotted Salamander (Petranka et al. 1998). Furthermore,
hard-bodied prey in the diet (e. g., Coleopteran adults and corixids) require more
energy to digest (Secor and Boehm 2006), which should make those prey less
desirable if softer-bodied prey were available, further supporting the hypothesis
of food limitation.
If food limitation were occurring, predators would be expected to adjust
search images toward whatever prey was available and to consume multiple
individuals of sub-optimally sized prey. Our samples included individual salamanders
that had consumed up to 52 frog eggs, 641 cladocerans, 37 copepods, 10
corixids, 16 ostracods, or 10 amphipods. Cladocerans, copepods, and ostracods
are particularly small compared to the gape and size of the salamanders studied.
Cladocerans are so small that they would seem to be of little value as food for the
larger submetamorphic or paedomorphic salamanders that we examined. The fact
that 641 individuals of this sub-optimally-sized prey were found in one stomach
(several other salamanders also had consumed large numbers of cladocerans) indicates
that their availability, coupled with a probable search image, made them
an often-taken food for a hungry salamander. Taylor et al. (1988) also reported
consumption of large numbers of cladocerans by a few, but much smaller, larval
Mole Salamanders.
Copepods, even when abundant, are thought to occur infrequently among the
foods of larger aquatic salamanders due to the copepods’ rapid darting abilities
(Taylor et al. 1988); however, they were common in our samples. Most of the
copepods we found also possessed enlarged egg sacs, which may have made
them larger as well as slower, thereby increasing both their caloric value and susceptibility
to predation. Copepods and cladocerans were taken more commonly
in pond 2, in which salamanders were smaller on average. Common foods of
smaller Mole Salamanders include copepods and cladocerans (Branch and Altig
1981, Taylor et al. 1988) but older larvae shift their diets to include larger prey
such as chironomids (Taylor et al. 1988).
Ostracods also are common foods for smaller larval salamanders (Taylor et al.
1988), and under experimental conditions, they seem to be more common in the
absence of salamanders (Holomuzki et al. 1994). Ostracods were not common
foods in the present study, but, like cladocerans and copepods, they were taken
more commonly in pond 2. No food availability data were obtained in this study,
but the higher presence of ostracods, copepods, and cladocerans as food in pond
2 could reflect take by smaller food-limited salamanders.
At the beginning of our study, we anticipated that the high density of salamanders
would limit food resources, thereby resulting in a shift toward hatchling
amphibian prey. Instead, we discovered that consumption of amphibian eggs
became prevalent, which apparently led to general spawn failure for the Pickerel
Frog. In a prey-depleted environment, the nutrient flush appearing with the hatch
of other amphibians could provide the energy necessary to fuel metamorphosis.
Ryan and Semlitsch (2003) noted that Mole Salamanders were more likely
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2013 Southeastern Naturalist Vol. 12, No. 3
to metamorphose when growth rates were high later in development. Under
stressful conditions, larger larvae metamorphose to escape unfavorable aquatic
habitats (Doyle and Whiteman 2008). Consumption of eggs by branchiate Mole
Salamanders could supply the requisite energy (Regester et al. 2008) for metamorphosis,
but eggs had been reported previously only once for the Mole Salamander
(McAllister and Trauth 1996). Additional research is needed to evaluate
the effect of food limitation followed by a nutrient flush of amphibian prey on
metamorphosis of high-density populations of larval ambystomatid salamanders.
Acknowledgments
We thank M. Karnes and the Ross Foundation for access to the study site. The Arkansas
Game and Fish Commission provided collecting permits.
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