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Keywords Abstract
Diversity, mesocosm, temporary ponds,
zooplankton. In temporary pond ecosystems, it is hypothesized that the two dominant
structuring forces on zooplankton communities are predation and demographic
Correspondence constraints due to wetland drying. Both of these forces are deterministic pro-
Marcus Zokan, Odum School of Ecology, cesses that act most strongly at opposing ends of a hydroperiod gradient. Our
University of Georgia, Athens, GA 30602. objective was to test how these two processes affect a- and b-diversity of zoo-
Tel: (706) 542-2968;
plankton communities derived from a diverse temporary pond system. We
Fax: (706) 542-4819;
E-mal: zokanm@gmail.com
hypothesized that decreased hydroperiod length and the presence of salamander
larvae as predators would decrease b-diversity and that intermediate hydroperi-
Funding Information od communities would have the greatest species richness. Our 1-year mesocosm
This experiment was funded through the experiment (n = 36) consisted of two predation treatments (present/absent)
small grant program of the Odum School of and three hydroperiod treatments (short/medium/long) fully crossed, seeded
Ecology, University of Georgia. from the resting egg bank of multiple temporary ponds. In total, we collected
37 species of microcrustacean zooplankton from our mesocosms. A reduction
Received: 22 January 2015; Revised: 3 June
2015; Accepted: 10 June 2015
in hydroperiod length resulted in lower a-diversity, with short-hydroperiod
treatments affected most strongly. Endpoint community dissimilarity (b-diver-
Ecology and Evolution 2015; 5(15): sity) was greatest in the medium-hydroperiod treatment with regard to species
3066–3074 presence/absence, but was greatest in the long-hydroperiod treatment when
abundances were included. Predation by salamander larvae led to reduced b-
doi: 10.1002/ece3.1593 diversity with respect to species presence/absence, but not among abundant spe-
cies, and had no effect on a-diversity. Our results suggest that environmental
changes that reduce hydroperiod length would result in reduced a-diversity;
however, intermediate hydroperiod length appear to enhance b-diversity within
a group of wetlands.
3066 ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
M. Zokan & J. M. Drake Effect of Hydroperiod and Predation
Strength
of effect
Weak
Ephemeral Permanent
Hydroperiod gradient
Figure 1. A conceptual diagram of the predation-permanence gradient in temporary wetlands, developed from Wellborn et al. (1996). The
strength of the environmental constraint on life history due to wetland drying is greatest when hydroperiod is short and alleviates as hydroperiod
increases. On the other hand, the strength of predation is greatest in long-hydroperiod ponds and diminishes in shorter hydroperiod wetlands due
to fewer predators capable of sustaining populations in these habitats. The intersection of these two relationships suggests that the pressure
exerted by these two processes may be lessened in moderate hydroperiods, although the true shape of these relationships is unknown.
wetland drying. For those that produce resting stages, • H2 – zooplankton community similarity increases in the
they must produce them prior to a dry down and in suf- presence of predation. We predict endpoint communities
ficient quantities for their population to survive the dry in the treatment exposed to predation by salamander
phase and truncated wet phases. Because wetland drying larvae will have lower b-diversity among replicates than
and predation are considered deterministic processes and those in which salamander predation is absent; and
act in opposing directions, community similarity should • H3 – intermediate hydroperiods will have the greatest
be greatest at both ends of the predation-permanence zooplankton species richness (a-diversity). We predict
gradient. endpoint communities in medium-hydroperiod treat-
Empirical studies by Chase (2003, 2007) found that ments will have the greatest species richness. The pres-
community dissimilarity, or b-diversity, is greater in per- sures of predation and wetland drying are reduced in
manent ponds than temporary wetlands, suggesting that intermediate hydroperiods, leading to the possibility of
b-diversity increases with hydroperiod length, but that greater species richness when both of these pressures
predation increases similarity (decreases b-diversity) in are lessened.
permanent wetlands (Chase et al. 2009). Thus, it remains
The goal of this experiment was to address whether
unclear what the net effect of these processes will be when
and how the impacts of salamander predation and the
both are acting together. Because predation and wetland
demographic constraints imposed by wetland drying
drying act most strongly at opposing ends of the hydro-
reduce a large species pool to the smaller communities
period gradient and are reduced in intermediate hydrope-
observed in natural wetlands. Our results indicate that hy-
riods, dissimilarity could be increased at intermediate
droperiod length and the frequency of drying have impor-
levels of both. This greater dissimilarity could result from
tant effects on both a- and b-diversity; however,
greater species richness or a-diversity at some level of
salamander predation at the densities tested had only
intermediate hydroperiod. Because these predictions have
minor impacts on the zooplankton community.
not been tested experimentally, we conducted a meso-
cosm experiment in which predation and hydroperiod
were manipulated to test the following hypotheses within Methods
temporary wetland zooplankton communities:
The experiment was conducted at the Savannah River Site
• H1 – zooplankton community dissimilarity (b-diversity) Ecology Laboratory (SREL), South Carolina, between 19
increases with hydroperiod length. More specifically, we September 2012 and 4 September 2013. Experimental
predict that endpoint communities in long-hydroperiod mesocosms consisted of 189-L plastic containers with
treatments will have greater b-diversity among replicates overall dimensions of 108 cm 9 55 cm 9 45 cm (Fig. 2).
than those in short-hydroperiod treatments. This is Treatments consisted of three hydroperiod manipulations
because the constraint on life history due to wetland of different duration (short, medium, and long) and two
drying is lessened as hydroperiod length increases; predation treatments (salamander larvae present vs.
ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 3067
Effect of Hydroperiod and Predation M. Zokan & J. M. Drake
3068 ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
M. Zokan & J. M. Drake Effect of Hydroperiod and Predation
failed to produce another individual. Additional larvae Chao1 estimator (Chao et al. 2005). Two additional mea-
were added as needed to maintain the treatment density. sures of a-diversity, estimators of Shannon’s index (Chao
Our experimental protocol was in accordance with the and Shen 2003) and the Simpson index (minimum vari-
procedures of and approved by The University of Georgia ance unbiased estimator) (Magurran 1988) that account
Institutional Animal Care and Use Committee. for unseen species, were calculated for each sample using
abundances of the same taxonomic units used for species
richness calculation. Species richness, Shannon’s index,
Sample collection
and the Simpson index represent the three levels of a-
One zooplankton sample per mesocosm was taken diversity (q) recommended by Chao et al. (2012) to char-
monthly using a tube trap sampler (Paggi et al. 2001). acterize a community of species. Species richness reflects
One mesocosm in the short-hydroperiod/no-predator the number of species present, but gives no information
treatment group was damaged and drained out between on species abundances. A higher Shannon’s index indi-
the penultimate and final sampling day and was removed cates a higher number of species in more equal abun-
from all analyses for that date. Cladocerans, cyclopoid co- dances, whereas a high Simpson index value represents a
pepods and calanoid copepods were identified to the spe- community low in species in which only a few species
cies level where possible. Other individuals of Calanoida, dominate the total community abundance. These metrics
Harpacticoida, Ostracoda, and Anostraca were identified can be converted to Hill numbers, with the interpretation
to class level and were also counted and designated as of species richness (q = 0) as the number of species,
pseudospecies. Water conditions (pH, conductivity, tem- exponential of Shannon’s index (q = 1) as the number of
perature) were monitored in conjunction with each sam- average species, and inverse Simpson index (q = 2) as the
pling using a YSI Professional Plus. number of dominant species (Chao et al. 2012). The lev-
els of diversity (q) in measures of both a- and b-diversity
are equivalent regarding the weights given to species fre-
Statistical analysis
quencies. Richness and diversity estimates were calculated
To examine the effect of experimental treatments on using the program SPADE (Chao and Shen 2010). Differ-
community similarity, the abundances of each species ences in a-diversity between treatments for each sampling
present on the final sampling date were converted to a date were analyzed using Welch’s ANOVA due to unequal
community matrix. Following Chao et al. (2012), two group sizes and heteroscedasticity in some comparisons;
pairwise measures of b-diversity (Sørensen–Dice index pairwise differences between hydroperiod treatment
and Morisita’s overlap index) were calculated from each groups were tested using a post hoc Games–Howell test.
matrix, reflecting dissimilarity in presence/absence and
relative abundances, respectively. These measures can be
Results
derived from the classical definition of b-diversity and are
themselves transformations of a single diversity metric, Over 40,000 individuals of at least 37 species were col-
but with different weights given to species frequencies lected during this study (Table 1), representing 46% of
(Jost et al. 2011; Chao et al. 2012). The Sørensen–Dice taxa known from the wetlands from which the mesocosm
index represents differences in species presence (q = 0) communities were derived. Total mesocosm sample spe-
and the Morisita’s overlap index represents differences in cies richness ranged from 12 to 23 species (x = 16.19,
dominant species (q = 2) in the Hill number diversity SD = 2.86). The endpoint communities held 19 total spe-
framework (Jost et al. 2011). The Sørensen–Dice index cies and ranged from 1 to 8 species per mesocosm (x
and Morisita’s overlap index were calculated using the = 3.37, SD = 1.97). There were no species present in the
“vegan” package in R. To compare differences between short-hydroperiod treatment that were not present in the
treatment groups, we used Welch’s ANOVA due to other two hydroperiod treatments.
unequal group sizes and heteroscedasticity; ANOVA com- b-diversity within hydroperiod treatments measured
parisons used within-treatment b-diversity. Pairwise dif- using the Sørensen–Dice index differed between treat-
ferences between hydroperiod treatment groups were ments (F = 22.10, df = 119.8, P < 0.001) and was greatest
tested using a post hoc Games–Howell test. Statistical within the medium-hydroperiod treatment (Fig. 3), which
tests were performed in R 3.2.0, R Foundation for Statis- differed from both the short (Cohen’s d = 1.22,
tical Computing, Vienna, Austria. P < 0.001)- and long-hydroperiod treatments (Cohen’s
Sample species richness was calculated for each sample d = 0.81, P < 0.001). The long-hydroperiod treatment
as total number of species and pseudospecies, omitting was also more dissimilar than the short-hydroperiod
immature and male cyclopoids. The lower bound of true treatment (Cohen’s d = 0.51, P = 0.02). The same analy-
species richness was estimated using the bias-corrected sis performed on Morisita’s overlap index also found dif-
ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 3069
Effect of Hydroperiod and Predation M. Zokan & J. M. Drake
3070 ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
M. Zokan & J. M. Drake Effect of Hydroperiod and Predation
ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 3071
Effect of Hydroperiod and Predation M. Zokan & J. M. Drake
(A)
(B)
(C)
dominant species, it had some effect on the presence of they can decrease zooplankton density and biomass and
rare species, leading to more similar communities when increase periphyton, bacteria, and chlorophyll a (Scott
salamander larvae were present. This result partially sup- 1990; Holomuzki et al. 1994; Blaustein et al. 1996). In
ports the prediction that predation should increase com- addition, salamander predation can reduce species
munity similarity. However, there were no significant richness (Blaustein et al. 1996; Urban 2013), or increase it
differences on a-diversity due to predation. This lack of in situations where two salamander species are present
difference suggests that salamander predation, at least at (Urban 2013).
the densities used in this experiment had little effect on The third prediction that species richness would be
diversity, but these effects might have been observed had greater in intermediate hydroperiod treatments was not
we used higher predator densities. Studies that have noted supported by the results, although this pattern has been
effects of salamander larvae predation on zooplankton observed in natural wetland systems (DeBiase and Taylor
densities had predator densities that were two to eight 2005; Frisch et al. 2006). Mean species richness per meso-
times greater than the density we used (Scott 1990; Blau- cosm was lower in the medium-hydroperiod treatment
stein et al. 1996). Despite the small effect observed here, than the long-hydroperiod treatment, although this differ-
mesocosm studies of salamander predation indicate that ence was small and not statistically significant. The model
3072 ª 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
M. Zokan & J. M. Drake Effect of Hydroperiod and Predation
Acknowledgments
We wish to thank Rebecca Sharitz (SREL/UGA) and Linda
Figure 6. Number of species represented as Hill numbers. Mean Lee (SREL) for the use of laboratory space, equipment, and
values were calculated within each hydroperiod treatment for logistical support. We also wish to thank David Scott
endpoint communities at three diversity levels, Chao 1 species (SREL) and Stacy Lance (SREL/UGA) for collecting the sal-
richness (q = 0), estimated exponential Shannon’s index (q = 1), and
amander larvae used in this experiment, advising us in sala-
estimated inverse Simpson index (q = 2). The colored polygons
mander care and with logistical support in mesocosm
enclose regions bounded by 2 SE.
setup. We thank the Odum School of Ecology for funding
that led to this prediction suggested that dissimilarity may this research through two OSE Small Grants. We also thank
be greater in intermediate hydroperiods. Our interpretation the two anonymous reviewers, whose positive and con-
was that greater species richness would be the cause. Dis- structive comments greatly improved our manuscript. Our
similarity was indeed greater within the medium-hydrope- experimental protocol was approved by The University of
riod treatment, but species richness was not. Instead, it Georgia Institutional Animal Care and Use Committee
appears that the greater dissimilarity was the result of dif- under Animal Use Protocol # A2012 04-024-A2 and UGA
ferences in species presence/absence between mesocosms. Animal Welfare Assurance # A3437-01.
The predation-permanence gradient model predicts that
the processes of predation and demographic constraint due Conflict of Interest
to wetland drying are greatest at opposite ends of the
hydrologic gradient (Wellborn et al. 1996). Our data None declared.
strongly support the latter, but provide only minor support
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