Diet and Nematode Infection Differ Between Coastal and
Inland Populations of Green Treefrogs (Hyla cinerea)
Molly A. Albecker, William B. Brantley Jr., and Michael W. McCoy
Southeastern Naturalist, Volume 17, Issue 1 (2018): 155–165
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M.A. Albecker, W.B. Brantley Jr., and M.W. McCoy
22001188 SOUTHEASTERN NATURALIST 1V7o(1l.) :1175,5 N–1o6. 51
Diet and Nematode Infection Differ Between Coastal and
Inland Populations of Green Treefrogs (Hyla cinerea)
Molly A. Albecker1,*, William B. Brantley Jr.1, and Michael W. McCoy1
Abstract - Progressive salinization of freshwater wetlands is likely to trigger significant
changes in associated animal communities. Understanding how salinization affects fundamental
natural history characteristics, like diet, is necessary to predict consequences of
environmental change. We analyzed dietary patterns of Hyla cinerea (Green Treefrog), a
generalist frog species known to inhabit freshwater and brackish wetlands. The stomach
contents of coastal (e.g., brackish) and inland (e.g., freshwater) H. cinerea differed in both
species variety and abundance of prey items. We also observed nematodes, a common
anuran gut parasite, in inland individuals but did not observe any nematodes in coastal
individuals. Our study shows differences in resource use and parasite load in H. cinerea,
suggesting that wetland salinization may impact trophic dynamics and infectious disease in
anuran amphibians.
Introduction
Little is known about how resource-use and trophic dynamics will be affected
by changes in habitat-defining characteristics such as salinity, or how ecological
relationships will be impacted as habitats are transformed by climate change. As
habitats and prey communities change, generalist consumers may demonstrate
concomitant shifts in diet (Mahan and Johnson 2007). However, some more discriminant
species may maintain dietary preferences despite the changing prey
community (Freed 1980). Understanding diet composition and the factors that affect
diet across disparate habitat conditions is especially important given that rapid
environmental change is expected over the next century. Secondary salinization, or
increasing salt concentrations in freshwater wetlands due to anthropogenic factors,
is becoming a serious environmental concern worldwide (Herbert et al. 2015). Wetlands
along coastal margins are becoming progressively more saline as sea levels
rise, inland tributaries are changed, storm surges are magnified, and shipping canals
are increasingly dredged, facilitating saltwater flow upstream (Kaushal et al. 2005,
Michener et al. 1997, Moorhead and Brinson 1995, Nicholls and Cazenave 2010,
Williams 2013).
Saltwater segregates organisms and limits species distributions, so species
assemblages within saltwater and freshwater wetlands are often distinct, with
few salt-tolerant or euryhaline species occurring across both habitat types. Increasing
salt concentrations in coastal freshwater wetlands is therefore expected to
induce wholesale shifts in species assemblages as freshwater-adapted organisms
1Department of Biology, Howell Science Complex, East Carolina University, Greenville,
NC.*Corresponding author - albeckerm09@students.ecu.edu.
Manuscript Editor: Cathryn Greenberg
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emigrate, or are extirpated, and as salt-tolerant organisms immigrate into habitats
that become brackish or saline (Guccione 1995, Hunter et al. 2015, Kennish 2001,
Morris et al. 2002, Nicholls and Tol 2006, Parkinson 1994, Williams et al. 2003).
Indeed, rising salinities may trigger complex shifts in trophic dynamics, potentially
impacting the structure of wetland invertebrate and vertebrate assemblages (James
et al. 2003).
Amphibians are among the putatively salt-sensitive organisms predominantly
associated with freshwater wetlands, with only 2% of species documented in saline
habitats (Hopkins and Brodie 2015). Amphibians are prominent members of
wetland communities and are implicated as key players in the transfer of energy
between aquatic and terrestrial habitats, and between trophic levels (Burton and
Likens 1975, Gibbons et al. 2006, McCoy et al. 2009). Hyla cinerea (Schneider)
(Green Treefrog) is a generalist consumer that inhabits a variety of different wetland
types in the Southeastern United States including ponds, drainage ditches,
marshes, bogs, and swamps (Engels 1942, 1952; Freed 1980; Lee 2009; Meyers
and Pike 2006; Tuberville et al. 2005), and also is recurrently observed in brackish
wetlands along coastal regions within its native range (Albecker and McCoy 2017,
Johnson and Christensen 1976, Labanick 1976, Oplinger 1976, Wells 2007).
We capitalized on the ability of Green Treefrog to inhabit both freshwater and
brackish wetland habitats to investigate how salinity of wetlands affects adult frog
diets. We did so by comparing the stomach contents of Green Treefrog populations
inhabiting brackish wetlands with those of populations inhabiting freshwater
wetlands in North Carolina. Understanding how resource use varies with habitat salinity
is important when investigating the natural history of an organism, its habitat
requirements, and the trophic dynamics within an ecosystem, as well as how each
of these may be affected by environmental change.
Methods
Study area
We made field collections in eastern North Carolina (NC) between May and
July of 2014. We collected “inland” Green Treefrog from freshwater wetlands in
and around Greenville, NC. Greenville is situated on the coastal plains of North
Carolina ~190 km east (inland) of the coastal collection sites. Inland, freshwater
wetlands contained a wider diversity of plants including sedges, emergent grasses,
and hardwood trees such as Taxodium distichum (L.) Rich (Bald Cypress), Liquidambar
styraciflua L. (Sweet Gum), Nyssa aquatica L. (Water Tupelo), and Acer
rubrum L. (Red Maple). The salinity of the freshwater habitats never exceeded 1
part per thousand (ppt) and were slightly acidic, with pH varying between 5.0 and
6.5. We collected “coastal” Green Treefrogs from salt marsh habitats dominated by
Spartina alterniflora Loisel (Smooth Cordgrass) and Phragmites australis (Cav.)
Trin. Ex Steud. (Common Reed), which were the only source of shade and structure
available in these locations. Individuals collected from coastal populations were
calling on emergent vegetation in brackish water with salinities varying between 3
and 24 ppt and a pH of 7.5–8.8.
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Field collections
We collected 5–7 male Green Treefrogs from each of 4 discrete, freshwater
wetlands near Greenville, NC, and 5–7 males from each of 5 discrete, brackish
wetlands along North Carolina’s outer banks (Table 1). We placed each captured
frog into a small, moistened container for transport back to the laboratory for processing.
In total, we sampled the gut contents via stomach dissections from 25 male
Green Treefrogs from 4 coastal populations, and 20 males from 4 discrete inland
populations (n = 45 individuals; Table 1). At each collection site, we measured
salinity (in parts per thousand (ppt)) and pH using a YSI Professional Plus multiparameter
meter (Xylem, Inc., Yellow Springs, OH).
Dietary analyses
The day after collection, we recorded each frog’s weight and snout–vent length
(SVL) and then humanely euthanized individuals via 2% MS-222 overdose (all
protocols approved by ECU IACUC #D302) (Gentz 2007). Stomachs and intestines
were excised and placed in labeled 2-mL micro centrifuge tubes containing
70% ethanol. We identified stomach contents using a Leica Dissection microscop e
(Model MDG41). To characterize diets, we sorted and arranged the contents of
each stomach and identified contents within the stomach to taxon omic Order, with
the exception of Gastropoda, which could only be identified to Class. We limited
our taxonomic discrimination to the level of Order, as the majority of the gut contents
were partially or mostly digested, leaving only shells or incomplete, small
remnants, thereby making a finer resolution impractical. After identification, we
conservatively enumerated prey items by determining the minimum number of prey
organisms that could be represented by the fragments present (e.g., 8 ant legs would
be recorded as 2 ants). We took photos of all contents using Leica Application Suite
X software.
Statistical methods
We excluded nematodes from our diet analyses because nematodes are gut
parasites; although they can be transferred via ingestion, they typically are not
considered to be prey for adult frogs (Campião et al. 2015). We collected males
from chorusing populations, i.e., during reproductively active periods. Because
Table 1. Collection sites and dates of coastal and inland Hyla cinerea (Green Treefrog) used for gut
contents analysis.
Date Area Specific location Latitude Longitude
28-May-14 Coastal Coastal Studies Institute 35º52'26.14"N 75º39'38.54"W
6-June-14 Inland Bellamy Pond 35º33'28.50"N 77º20'55.85"W
10-June-14 Inland Lowe's Retention Pond 35º35'26.49"N 77º19'09.89"W
11-June-14 Inland Oakwood School 35º37'15.80"N 77º26'45.29"W
14-June-14 Coastal Pea Island Highway 12 Ditches 35º41'33.42"N 75º29'07.43"W
25-June-14 Inland Wheat Field 35º37'28.40"N 77º20'32.80"W
28-June-14 Coastal New Inlet Pond 35º41'11.50"N 75º29'03.92"W
3-July-14 Coastal Bodie Lighthouse 35º49'12.48"N 75º33'45.04"W
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reproductive activities may affect prey consumption (Hirai and Matsui 2000), we
compared the individuals whose stomachs held contents against individuals whose
stomachs had no contents to determine any differences in probability of containing
prey between coastal and inland populations. For this test, we used a general linear
mixed-effects model and a binomial family error distribution (Bates et al. 2015).
Presence or absence of stomach contents and location (e.g., coastal or inland) were
treated as fixed effects, with population treated as a random effect to account for
non-target variation due to differences among sites. For those individuals with
items in their stomachs, we tested whether total number of prey items for each individual
differed according to habitat salinity using a general linear model with a
Poisson error distribution (Bates et al. 2015). In this analysis, prey item abundance
and location were considered fixed effects, with specific collecting sites treated as
random effects. All analyses were conducted in the R statistical programming environment
(2014).
To assess differences in the gut contents between coastal and inland Green Treefrogs,
we compared both the variety and abundance of different prey items between
the groups. To compare variety in dietary content, we standardized the data in a
binary presence/absence data frame, while abundance analyses were performed on
the abundance of prey items present within individuals. We omitted unidentifiable
prey items and individuals with empty stomachs from these analyses.
We used permutational multivariate analysis of variance (PERMANOVA) to
assess differences in prey variety and abundance between the groups. We further
explored PERMANOVA results by conducting similarity percentages analyses
(SIMPER) to identify which prey orders were most commonly shared between
coastal and inland populations. Each of these analyses utilized the R package
“vegan” (Oksanen et al. 2016).
Results
Inland individuals had an average weight of 4.13 g (± 0.75 g) with an average
SVL of 43.39 mm (± 3.03 mm). Coastal individuals weighed an average of 4.25 g
(± 1.02 g) with an average SVL of 43.07 mm (± 3.86 mm).
We observed differences in the number of stomachs with contents vs. stomachs
with no contents between inland and coastal locations (Z = 2.23, P = 0.026). Indeed,
85% (95% confidence interval [C.I.] = 0.53–0.96) of inland frogs contained
items in their stomachs compared to 56% (C.I. = 0.37–0.74) of the coastal frogs
(Fig. 1). However, for the individuals with items in stomachs, there were no differences
in the total number of items in the stomachs of coastal and inland Green
Treefrogs (Z = -0.03, P = 0.92). On average, coastal frogs had 1.6 (C.I. = 0.94–
2.50) items in their stomachs, whereas inland frogs had 1.55 (C.I. = 0.48–1.93)
items in their stomachs.
We identified organisms from a total of 10 different Orders in the stomachs
of Green Treefrogs across both habitat types, including nematodes (Table 2). We
observed that 7 of 22 inland Green Treefrog individuals contained nematodes, a
common anuran gut parasite (Bursey and Brooks 2010). Each infected individual
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2018 Vol. 17, No. 1
contained an average of 4 (± 3.31 std. dev.) nematodes. No nematodes were observed
in any coastal individuals.
We found differences in the variety of prey items between coastal and inland
populations (F1 = 2.8, P = 0.03; Fig. 2). SIMPER analysis revealed that the prey
items most commonly shared across coastal and inland frogs were Coleoptera
(shared average = 28%), Aranae (15%), and Orthoptera (15%), wheras Mesostigmata
(3%), Gastropoda (3%), and Odonata (3%) contributed the least to similarities
(Table 2).
Coastal and inland populations contained different abundances of prey items
(F1 = 2.8, P = 0.025; Fig. 3). The prey items that contributed the most to observed
similarities between in diet abundance between the 2 locations were Coleoptera
(38%), Aranae (13%), and Orthoptera (13%), whereas Odonata (3%), Gastropoda
(3%), and Mesostigmata (3%) contributed the least to observed similarities (Table 3).
Figure. 1. Mean
proportion of individuals
whose
stomachs contained
dietary
items across
coastal and inland
Hyla cinerea
(Green Treefrog)
populations. Error
bars represent
95% confidence
intervals.
Table 2. Prey items present within the stomachs of coastal and inland Hyla cinerea (Green Treefrog).
The presence per coastal individual shows the average presence (in percent) that each prey was observed
within coastal and inland populations of Green Treefrogs. Contribution to similarities reflects
the results of the SIMPER analysis showing average shared contribution to similarities in diet abundance
between coastal and inland populations.
Average presence (in percent) in
Prey Coastal frogs Inland frogs Contribution to similarities
1. Coleoptera 20% 73% 0.283
2. Aranae 30% 9% 0.147
3. Orthoptera 30% 9% 0.147
4. Hymenoptera 10% 0% 0.048
5. Lepidoptera 10% 0% 0.048
6. Mecoptera 0% 9% 0.042
7. Mesostigmata 10% 0% 0.033
8. Gastropoda 10% 0% 0.033
9. Odonata 0% 9% 0.028
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Discussion
We examined how the stomach contents of male Green Treefrogs differed according
to wetland type (e.g., coastal, brackish wetlands or inland, freshwater
Figure. 2. Stacked
bar plot showing
differences in average
prey presence
(shown in
percent) within
stomachs of coastal
and inland Hyla
cinerea (Green
Treefrog; see Table
2 for actual
values).
Figure. 3. Stacked
bar plot demonstrating
differences
in average
prey abundance
between coastal
and inland Hyla
cinerea (Green
Treefrog; see Table
3 for actual
estimates). Although
Nematoda
abundance is
shown here, it was
not included in the
statistical analyses
on these data.
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2018 Vol. 17, No. 1
wetlands). This species is considered a dietary generalist, but studies are mixed
about whether or not Hylid consumption patterns are opportunistic and non-preferential,
or whether individuals maintain dietary preferences across environments
(Freed 1980, Leavitt and Fitzgerald 2009). We found that stomach contents of
coastal and inland Green Treefrogs differed in both variety and abundance of prey
consumed (Tables 2, 3). These findings provide preliminary indications that as
environments change, we may expect shifts in trophic dynamics among generalist
anuran species that could ultimately impact wetland invertebrate communities.
Our study corroborates an investigation of the diets of invasive Green Treefrogs
that had been introduced in the Chihuahuan desert in which the authors reported
scorpion remnants in frog stomachs, indicating that Green Treefrogs are capable of
exploiting novel prey types in new environments (Leavitt and Fitzgerald 2009).
One of the most interesting observations that emerged from this study is the
complete absence of nematodes (Order Nematoda) from the stomachs of coastal
Green Treefrog populations. Nematodes are well-known gut parasites in frogs, so
it is likely that their presence in freshwater Green Treefrogs indicates gut-parasite
infection (Campião et al. 2015). Infection occurs when nematodes are incidentally
consumed via invertebrate vectors, or via direct contact with substrate. In some
severe cases, nematode infection can debilitate or kill individuals (Bursey and
Brooks 2010, Johnson et al. 2007, Schotthoefer et al. 2003). The lack of nematode
infection in individuals inhabiting brackish water may be due to an inability of
nematodes, or their vectors, to withstand the increased osmotic stress of brackish
environments, resulting in lower gut-parasite infection rates (Thurston et al. 1994).
Other pathogens such as Batrachochytrium dendrobatidis (Longcore, Pessier &
D.K. Nichols) (Amphibian Chytrid Fungus) and saprolegnia fungal infections are
also lower in anurans exposed to salt, which suggests that saltwater may provide a
refuge, protecting hosts from certain parasites and pathogens (Karraker and Ruthig
2009, Stockwell et al. 2015).
Table 3. Abundance of prey items present within the stomachs of coastal and inland Hyla cinerea
(Green Treefrog). The average number per coastal individual represents the average number of prey
items of each Order observed within coastal and inland populations of Green Treefrogs. Contribution
to similarities reflects the results of the SIMPER analysis showing average shared contribution to
similarities in diet abundance among coastal and inland populations.
Average abundance per
Prey Coastal individual Inland individual Contribution to similarities
1. Coleoptera 0.5 1.080 0.38
2. Aranae 0.3 0.083 0.13
3. Orthoptera 0.3 0.083 0.13
4. Lepidoptera 0.2 0.000 0.06
5. Hymenoptera 0.1 0.000 0.04
6. Mecoptera 0.0 0.083 0.04
7. Mesostigmata 0.1 0.000 0.03
8. Gastropoda 0.1 0.000 0.03
9. Odonata 0.0 0.083 0.03
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We know relatively little about how consumption patterns vary throughout
breeding and non-breeding phases in frogs, and our study provides important
insights into what adult, male frogs are consuming during reproductively active
months. We found that more coastal frogs had empty stomachs, which may impact
breeding behavior, fecundity, or the male’s ability to establish and defend breeding
territories and calling perches (Li et al. 2009, Martínez et al. 2004).
Although frogs are credited as providing important ecosystem services by
controlling pest species like mosquitos (Hocking and Babbitt 2014, Premo and
Atmowidjojo 1987), little is known about the degree to which this occurs. We did not
find any mosquito species in frog stomachs, despite an abundance of mosquitos in
all wetlands sampled (M.A. Albecker, pers. observ.). It is possible that mosquitos
were consumed by these individuals, but were digested and unidentifiable at the
time of collection. Alternatively, previous research has shown that Green Treefrogs
preferentially consume larger, more active prey than mosquitos, which may explain
their absence (Freed 1980).
A wide variety of factors likely influence dietary patterns in adult frogs observed
in this study. For example, there may be differences in prey abundances, prey type,
and prey availability between brackish and freshwater habitats. Alternatively, habitat
type may modify the ability of frogs to effectively navigate through different
substrates between habitat types. There may be different metabolic needs due to
increased salt stress in coastal wetlands that requires additional energy to process
and eliminate excess salts by coastal individuals (Bernabò et al. 2013, Giunta et al.
1984). Additionally, differences in diet may stem from differences in the nutritional
value among prey items (Freed 1980), which may be particularly important during
the energetically taxing breeding season or in brackish environments that require
extra energy to maintain internal ionic balances.
As habitats continue to change from anthropogenic modifications and global
climate change, research focused on revealing basic biology and natural history
of organisms inhabiting both current and impending environments is crucial to
accurately predict consequences, and effectively manage impacted communities.
Our analyses of dietary patterns of a common, dietary generalist frog species
(H. cinerea) documented that abundance and variety of dietary items differed
according to habitat salinity. Our results provide valuable insights into how an
emerging environmental stressor, secondary salinization, may impact the diets of
freshwater species.
Acknowledgments
We are grateful to R. Trone for assistance with arthropod identification. We also thank
A. Stuckert, T. McFarland, C. Thaxton, and J. Touchon for field assistance. Funding for this
project was supplied by North Carolina Sea Grant (Project No. 2014-R/14-HCE-3) awarded
to M.W. McCoy and M.A. Albecker, as well as research grants from the North Carolina
Herpetological Society, ECU’s Coastal Maritime Council, and Explorer’s Club. The authors
declare no conflicts of interest.
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