TROPHIC INTERACTIONS in SOUTHEASTERN WETLANDS by RICHARD D. SCHULTHEIS (Under the Direction of Darold Batzer) ABSTRACT Wetlands

TROPHIC INTERACTIONS IN SOUTHEASTERN WETLANDS

RICHARD D. SCHULTHEIS

(Under the Direction of Darold Batzer)

ABSTRACT

Wetlands are naturally dynamic systems. In this study, I explored the effects of predation by a dynamic vertebrate complex on the aquatic invertebrate community of a southeastern wetland. A two-year predator exclusion experiment was used to test for effects of predation by marbled salamanders ( Ambystoma opacum ), spotted salamanders ( Ambystoma maculatum ), red- spotted newts ( Notophthalmus viridescens viridescens ), bluegill ( Lepomis macrochirus ), mosquitofish ( Gambusia sp.) and bullfrogs ( Rana catesbeiana ). Overall invertebrate responses to vertebrate reductions were minimal. Of sixty-five invertebrate taxa observed in the study, abundances of few differed with predator treatments, and these patterns were restricted to mainly

April of both years. These findings suggest that vertebrate predation was only seasonally important in this habitat, and complex interactions within the vertebrate community likely limited our ability to detect a response to predation in the invertebrate community.

INDEX WORDS: Invertebrate, trophic, predation, salamander, fish

TROPHIC INTERACTIONS IN SOUTHEASTERN WETLANDS

RICHARD D. SCHULTHEIS

B.S., Allegheny College, 2002

A Thesis Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment

of the Requirements for the Degree

MASTER OF SCIENCE

ATHENS, GEORGIA

2005

Richard D. Schultheis

TROPHIC INTERACTIONS IN SOUTHEASTERN WETLANDS

RICHARD D. SCHULTHEIS

Major Professor: Darold P. Batzer

Committee: Sara H. Schweitzer Barbara E. Taylor

Electronic Version Approved:

Maureen Grasso Dean of the Graduate School The University of Georgia August 2005

ACKNOWLEDGEMENTS

I would like to thank my committee members, Dr. Barbara Taylor, Dr. Sara Schweitzer, and my advisor Dr. Darold Batzer, with whom this project would have never happened. I would additionally like to thank the ladies of the Batzer lab, Elizabeth Reese, Missy Churchill, and

Jennifer Henke, for all insight, assistance, and entertainment over the last three years. Valuable assistance with amphibians was provided by Scott Connelly, to whom I am grateful. I would like to thank my parents, family, and friends for the support, assistance, and distraction I needed the last few years. v

TABLE OF CONTENTS

Page

ACKNOWLEDGEMENTS...... iv

LIST OF TABLES...... vi

LIST OF FIGURES ...... vii

CHAPTER

1 INTRODUCTION ...... 1

2 METHODS ...... 5

STUDY AREA...... 5

EXPERIMENTAL DESIGN...... 7

STATISTICAL ANALYSIS...... 9

3 RESULTS ...... 11

VERTEBRATE COMMUNITY...... 11

INVERTEBRATE COMMUNITY...... 12

EFFICACY OF VERTEBRATE EXCLUSION...... 12

CAGE EFFECTS ...... 13

INVERTEBRATE RESPONSE TO VERTEBRATE EXCLUSION...... 13

FIGURES AND TABLES...... 16

4 DISCUSSION...... 21

CONCLUSIONS...... 25

LITERATURE CITED ...... 26 vi

LIST OF TABLES

Page

Table 1: SPECIES RICHNESS OF VERTEBRATE AND INVERTEBRATE PREDATORS ...20 vii

LIST OF FIGURES

Page

Figure 1: VERTEBRATE PREDATOR ABUNDANCE...... 16

Figure 2: INVERTEBRATE ABUNDANCE – CAGE EFFECTS ...... 17

Figure 3: SIGNIFICANT TAXA, APRIL 2003 ...... 18

Figure 4: SIGNIFICANT TAXA, APRIL 2004 ...... 19

CHAPTER 1

INTRODUCTION

The effect of fish predation on invertebrate communities has been well documented.

Although recent studies suggest interaction strength varies with habitat complexity (see Dahl and

Greenberg 1998), strong interactions have been demonstrated in lakes (Carpenter et al. 1987,

Bronmark et al. 1992, Diehl 1995, Osenberg and Mittelbach 1996), ponds (Hall et al. 1970,

Hambright et al. 1986, Warren 1989, Diehl 1992), and streams or rivers (Koetsier 1989, Power

1990, 1992, Bechara et al. 1992, 1993).

The effect of fish predation on invertebrates in wetlands, however, has received less attention. Batzer (1998) found that small insectivorous fish in a New York marsh strongly influenced the benthic midge community in open water habitat. A similar study in weedy habitats, however, suggested that the influence of fish predation was more complex, with midge abundance actually increasing with fish presence in some areas (Batzer et al. 2000). In semi- permanent prairie pothole wetlands of North America, fathead minnows ( Pimephales promelas ) affected the composition, abundance, and biomass of benthic invertebrate communities (Hanson and Riggs 1995, Zimmer et al. 2001a, 2001b, 2002a, 2002b). These and other fish have been implicated as a possible cause for a decline in abundance of a number of waterfowl species that rely on invertebrate prey (Anteau and Afton 2004). Overall, it appears that patterns of fish predation in wetlands are similar to results in other aquatic habitats.

In many wetlands, the presence of fish is restricted by periodic drying, winter-kill events, or limitations to colonization. In these habitats, the important vertebrate predators on 2 invertebrates are amphibians. Diet analyses (see review in Schultheis and Batzer 2005) indicate that a number of salamander species feed primarily on invertebrate fauna as maturing larvae and/or adults. The effects of this predation, however, are not well understood, and have been focused within the family Ambystomatidae. In subalpine wetlands of central Colorado, the tiger salamander ( Ambystoma tigrinum nebulosum ) plays a keystone role in determining macroinvertebrate community composition (Wissinger et al. 1999). In prairie pothole wetlands, tiger salamanders alter the macroinvertebrate community to the extent that they may deter use by migrating waterfowl (Benoy et al. 2002). In a South Carolina temporary wetland, increases in larval abundance of marbled ( Ambystoma opacum ) and mole salamanders ( Ambystoma talpoideum ) are proposed as a cause for annual variations in chironomid abundance (Leeper and

Taylor 1998). When present in a more complex community with dwarf salamanders ( Eurycea quadridigitata ) and red-spotted newts ( Notophthalmus viridescens viridescens ) in a similar habitat, however, mole salamanders consumed chironomid larvae with no visible impact on the chironomid assemblage (Taylor et al. 1988).

There has been much research done on density-dependent life history traits of salamander larvae. Although these studies do not directly address the effects of salamander predation on invertebrates, most of the studies monitored some aspects of invertebrate abundances with varying densities of salamander larvae. They therefore provide a reasonable estimate of the effects of varying salamander predation on invertebrate communities. In a study on marbled salamander density in southeastern wetlands, Scott (1990) monitored zooplankton abundance in an experimental setup of large enclosures that varied in salamander density. Zooplankton densities were lowest in treatments with the highest density of salamanders, but showed no significant pattern across all treatments. In a similar study with marbled salamanders, the 3 abundance of zooplankton in an experimental setup in natural ponds did not differ as salamander abundance changed (Petranka 1989). In a study on blue-spotted salamanders ( Ambystoma laterale ), Van Buskirk and Smith (1991) manipulated salamander abundance in natural splash pools on Lake Michigan. No associated differences in zooplankton abundance were detected between salamander density treatments. A weakness of these studies, however, was their failure to monitor benthic invertebrate populations. Both of the latter studies admit that their conclusions on the role of food limitation in the habitat were limited by their failure to monitor benthic prey items. Although these studies may suggest that salamander predation on zooplankton communities shows little density-related variation, their application on the overall effects of these salamanders on invertebrates is limited.

A unique characteristic of many wetlands is a constantly changing predator complex.

The dynamic physical conditions of wetlands often affect the vertebrate fauna. In semi- permanent prairie potholes, salamander larvae are typically the only vertebrate predators present.

However, fish colonize wetlands during high water events as connections develop with permanent water habitats. This colonization may result in a predator complex of both fish and amphibians, or perhaps the elimination of amphibians from the habitat by the fish. These fish only remain, however, until the next winter-kill or drying event (Zimmer et al. 2001b).

Similarly, periodic fish colonization and extinction in wetlands has been observed in isolated

Carolina bay wetlands (Snodgrass et al. 1996) and floodplain swamps (Patrick et al. 1967).

These kinds of variable habitats provide a unique opportunity to explore trophic interactions in aquatic systems.

In this study, we attempted to expand our knowledge on the effects of salamander predation, as well as a complex and dynamic vertebrate predator community on invertebrate 4 communities in wetland habitats. To address these issues, we experimentally manipulated the abundances of vertebrate predators using cage structures, and observed how the invertebrate community responded. Over the two-year study, the predator complex naturally varied from one dominated by marbled salamanders, to a diverse community of bluegill, mosquitofish, marbled salamanders, spotted salamanders ( Ambystoma maculatum ), red-spotted newts, and bullfrogs

(Rana catesbeiana ). The goals of this project were to asses and compare the effects of amphibian and fish predation on the invertebrate community, and gain insight into how macroinvertebrate communities respond to a changing vertebrate complex. 5

CHAPTER 2

METHODS

Study Area

The experiment was conducted in a seasonal oxbow wetland on the floodplain of the

North Oconee River, in the Georgia Piedmont. The wetland is located near Athens, Georgia, in the University of Georgia’s Whitehall Experimental Forest, a facility managed to limit outside human impact. The wetland typically floods during heavy precipitation events of late fall or early winter, and often dries in mid to late summer when evapo-transpiration rates are highest.

Water input is typically from precipitation and groundwater seepage from adjacent uplands.

Overbank inputs from the North Oconee River occur sporadically. Although river water had not likely entered the site for a number of years prior to this study, the wetland received river input on two occasions during the first year of the experiment. When flooded, approximate maximum depth of the wetland was 2 m, and wetted area was 0.6 ha. Conductivity in the wetland was very low, ranging from 10 to 40 µs/cm. The pH was circumneutral (6.1 to 8.2) and water temperatures ranged from 10 to 25°C.

The wetland had an open canopy, and was dominated by herbaceous plants. Common species included panic grass ( Panicum sp.), smart weed ( Polygonum sp .), Asiatic dayflower

(Murdannia keisak ), and soft rush ( Juncus effusus). During year two of the experiment, a stand of submersed muskgrass ( Chara sp.) developed.

The study wetland also supported a rich amphibian community. Marbled salamanders, spotted salamanders, and red-spotted newts were collected during this study. Marbled 6 salamanders are a unique salamander species in that they lay eggs in dry basins before wetlands flood. They are thus typically the first species to appear in newly flooded habitats (Petranka

1989). Diet analyses suggest that they typically prey on small zooplankton species in their early larval period, and increase the proportion of larger macroinvertebrate species as they mature

(Petranka and Petranka 1980). Spotted salamanders typically migrate to breeding sites later in the spring, and as a result, larvae tend to be present in aquatic habitats through much of the summer. Feeding habits are similar to marbled salamanders (Freda 1983, Trauth et al. 2004), although it has been suggested that size selective predation on zooplankton fauna is common

(Lannoo 1986). Eastern newts have three life stages: the aquatic larvae, terrestrial eft, and aquatic adult. Diets of the aquatic larval and adult stages include an array of micro and macroinvertebrates, as well as other amphibians (Ries and Bellis 1966, Burton 1977, Brophy

1980, Stewart 2001). Although most anurans present in Georgia do not typically consume much macroinvertebrate prey, during the second year of the experiment, we collected bullfrog ( Rana catesbeiana ) tadpoles, a common consumer of aquatic invertebrates as well as other amphibian larvae (Stewart and Sandison 1972, Korschgen and Moyle 1976, Tyler and Hoestenbach 1979,

Hirai 2004).

Late in the first flood season of the experiment, overbank flow from the adjacent North

Oconee River introduced fish into the wetland. Although initial fish densities were low, the fish apparently spawned, and by late the following summer, a fish community dominated by mosquitofish (Gambusia sp .) and bluegill sunfish ( Lepomis macrochirus ) became established.

The diet of bluegill typically incorporates zooplankton (Mittelbach 1981, Harris et al. 1999), macroinvertebrates (Schramm and Jirka 1989, Dewey et al. 1997, Olson et al. 2003), and other fish (Flemer and Woolcott 1966, Applegate et al. 1967, Engel 1988). The diet of mosquitofish is 7 typically dominated by zooplankton and small insects within the water column. Their feeding on benthic inhabiting invertebrate fauna is typically limited (Hurlbert et al. 1972, Bence and

Murdoch 1986, Linden and Cech 1990, Oliver 1991, Garcia-Berthon 1999, Blanco et al. 2004).

Thus, during the first flood season (2002-2003), the only common vertebrate predators on invertebrate fauna were salamanders, while in the second season (2003-2004), bullfrogs and fish also joined the predator community.

Experimental Design

To test the effects of salamander and fish predation on invertebrates, we designed an exclusion experiment using wire mesh cages. 1.5 x 1.5 x 1 m cages were constructed from a

PVC pipe frame covered with 4-mm wire mesh. The cages were constructed with an open bottom and top, to allow use of natural benthic substrate and limit the effects of reduced sunlight or inhibited insect colonization. The 1-m height allowed the cage to extend above the water surface. Six cages were constructed with four sides completely covered with wire mesh. The mesh on each side panel extended below the frame into the mud to help seat the cage to the bottom substrate and limit vertebrate passage. These cages allowed the invertebrate community to develop without vertebrate predators. Six additional cages were constructed with half of each side covered in mesh. These cages allowed vertebrate entry and enabled us to test for physical or biological effects of the cage structure not relating to predator exclusion (i.e., cage effects). A final six 1.5 x 1.5 m areas of open cageless habitat served as ambient controls. The twelve cages and six open habitats were randomly arranged within two rows of nine units each; hence, there were 18 cells from which we sampled. Each cell was placed at least 1.5-m apart, and the location of the treatment array was changed between year one and year two of the experiment. 8

In year one of the study, initial flooding of the wetland occurred in mid-November 2002, and cages were installed by early December. Although the wetland did not dry completely between year one and year two of the study, the water receded from the area of our treatment array in July 2003. The water level returned to full pool levels in late January 2004, and cages were reinstalled by early February. Water remained in the cages until May 2004. Each year, we allowed the cage array to remain undisturbed for one day after installation, then we surveyed all

18 cells for vertebrates using D-frame sweep nets. If any were found, they were removed from the cage or open habitat, identified, and released outside of the study array. The habitat was then left undisturbed for an additional two weeks, after which routine invertebrate and vertebrate sampling was initiated.

Invertebrates were sampled monthly while cages were flooded, with the exception of

March 2003, when high water levels would not permit wetland access. Samples consisted of three 1-m sweeps of a D-frame sweep net (30-cm diameter, 1-mm mesh size). The three sweeps were pooled together so each sample represented 0.9-m2 of the benthic habitat. Samples were preserved in the field with 90% ethanol and brought back to the lab for processing and identification. Keys in Pennak (1989), Thorpe and Covich (1991), and Merritt and Cummins

(1996) were used to identify invertebrates to family, subfamily, or genus. The monthly invertebrate sweep samples also provided a survey of the amphibian community, but they failed to collect fish. Instead, we surveyed fish species using standard funnel-style minnow traps.

Each fish sampling consisted of one trap in each of the 18 units for a period of 48 hours (checked every 24 hours). Fish surveys were also conducted monthly for the duration of the experiment.

Traps also caught amphibians and provided an additional survey of that community. Due to the 9 differences in sampling methods between vertebrates, however, we did not make observations on relative abundances across vertebrate taxa.

Statistical Analysis

All comparisons between experimental treatments were done using analysis of variance

(ANOVA). For all tests, 0.05 was the a priori level of significance. To test for physical or chemical effects of the cage structures, a 2-way ANOVA was done for total invertebrate abundance across all sampling dates in half cages and open-ambient habitats. Because we detected a significant interaction between treatment and sample date, 1-way ANOVAs were then done for invertebrate abundances in each sampling date. We also tested the success of cages at excluding vertebrate predators by comparing the abundance of each taxon across all sampling dates using a 2-way ANOVA. This analysis was done between the 6 full cage exclosures and the

12 combined half cages and open-ambient habitats. In the taxa with a significant date-treatment interaction, treatment differences were analyzed for each month using 1-way ANOVAs.

To test for differences in invertebrate abundance by predator treatment, we first compared the total abundance of invertebrates in the 6 full cage exclosures to the 12 half cages and open habitats across all sampling dates using a 2-way ANOVA. However, because we suspected that response to vertebrate predation would differ both taxonomically and temporally, the abundances individual taxa were then compared in the 6 full cage exclosure and the 12 half cages and open ambient habitats within each sampling date using 1-way ANOVAs. Although some would argue the repeated nature of these tests suggests that Bonferroni adjustments are necessary, others (Perneger 1998) indicate that these corrections are overused and not valid when 10 hypotheses differ for each comparison (i.e., impacts of predation are not expected on every sample date for every taxon). Thus, we use a significance level of 0.05 for each comparison.

CHAPTER 3

RESULTS

Vertebrate community

A diverse vertebrate community developed over the two years of the experiment (Figure

1). From when cages were first installed in December 2002 through April 2003, larvae of the marbled salamander was the only vertebrate observed, and its abundance did not significantly differ among those months. The highest mean abundance observed was 0.75 salamanders/sweep in December, and the lowest was 0.27 salamanders/sweep in April. In the final May 2003 sample, mosquitofish, juvenile bluegill, and adult newts first appeared in the wetland, and marbled salamander larvae were absent.

In year 2 of the experiment, marbled salamanders were rare, with only one marbled larva detected in February in an open habitat. Bullfrogs, newts, and mosquitofish were present in

February, but in relatively low abundances (mean abundances: bullfrogs 0.50 larvae/trap sample: newts 0.08 adults/trap sample: mosquitofish 0.25 fish/sweep sample). In March 2004, bluegill were again collected (mean abundance: 1.33 fish/trap sample). Also in March, low numbers of bullfrogs (0.75/trap sample) and mosquitofish (0.58/sweep sample) persisted, while newts became abundant (2.08/trap sample). In April, spotted salamander larvae first appeared and were relatively abundant (mean abundance: 3.75 salamanders/sweep sample). Moderate to high numbers of bluegill (2.88/trap sample), bullfrogs (1.41/trap sample), mosquitofish (.33/sweep sample), and newts (2.92/trap sample) also occurred in April. Thus, a general trend of increasing richness of vertebrate predators occurred over the two years of study (Table 1). 12

Invertebrate community

Overall, we identified sixty-five invertebrate taxa (families, subfamilies, or genera).

Mean taxa richness per sample of open habitat increased from 6 taxa in December of year 1, to

24 in the last sample of year 2. Similarly, mean number of invertebrates varied from a low of 60 per sample in December 2002 to a high of over 3000 per sample in March 2004. In December

2002, a month after initial flooding, the community was dominated by Aedes mosquitoes and isopod and amphipod macrocrustaceans. In January and February 2003, copepods and ostracods became the most abundant organisms. By April and May 2003, chironomid midge larvae dominated collections. In year 2, chironomid and ceratopogonid midges were the most abundant organisms in February, but during the rest of year 2, cladoceran, copepod, and ostracod crustaceans were the most abundant organisms. Like vertebrates, invertebrate predator richness increased steadily over the two years (Table 1).

Efficacy of vertebrate predator exclusion

The effectiveness of cages at excluding vertebrate predators varied by taxa. Newt, marbled salamander, and spotted salamander abundances were effectively reduced by complete cages throughout the experiment (newts F = 10.20, p = 0.002, Figure 1e; marbled salamanders, F

= 7.052, p = 0.009, Figure 1c; spotted salamanders, F = 5.12, p = 0.042, Figure 1b). Exclusion of bullfrogs, mosquitofish, and bluegill was less consistent. As juvenile fish hatched late in the first year of the study, their small size allowed them to colonize the exclusion cages. Bluegill abundance did not differ between complete cages and open habitats during May 2003 ( F = 1.20, p = 0.29, Figure 1f). By the second year of the experiment, however, the larger size of the 13 bluegill limited access to complete cages, and bluegill abundance was significantly reduced by exclosures ( F = 9.72, p = 0.003). Bullfrog and mosquitofish densities were not affected by exclusion cages throughout the experiment (bullfrogs F = 1.19, p = 0.28, Figure 1d, mosquitofish

F = 0.80, p = 0.38, Figure 1a). However, neither bullfrog larvae nor mosquitofish were particularly abundant.

Cage effects

We tested for cage effects by comparing invertebrate abundances within the six half cages to the six open habitats. There were no differences across all dates ( p = 0.91), although a significant interaction existed ( p = 0.02), indicating that dates should be analyzed independently

(Figure 2). Of the 8 months tested, invertebrate abundance was greater in half cages during May

2003 ( F = 8.31, p = 0.018) but lower in March 2004 (F = 7.50, p = 0.021). Because of the lack of any consistent differences across dates that would suggest cage effects affected ecological patterns, we felt justified in pooling the six half-cage exclosures with the six open habitat samples to represent ambient conditions.

Invertebrate response to predator exclusion

Total invertebrate abundance did not differ significantly between caged and open- ambient habitats across all dates ( F = 3.05, p = 0.083) or within any single sampling date. There were, however, differences between treatments for some individual taxa on certain dates, and these responses will be reviewed chronologically. In December and January of the first year of the experiment, when vertebrate predation was likely low, no taxa significantly differed between exclusion cages and open-ambient habitats, and in February, only Hydroporus water beetle 14 abundance was higher in exclusion cages than open habitats ( F = 5.33, p = 0.035). In April,

Hesperocorixa water boatmen ( F = 11.32, p = 0.004) and Lestes damselfly ( F = 6.01, p = 0.026) abundances were significantly higher in exclusion cages than in open habitats (Figure 3).

Additionally, predatory Agabus beetles and Buenoa backswimmers were present, although not abundant, in exclosure cages, but were absent in open habitats. Conversely, abundances of

Ceriodaphnia ( F = 2.65, p = 0.012) and chydorid ( F = 4.51, p = 0.050) crustaceans were higher in open habitats than in exclusion cages (Figure 3). Orthocladiinae, Tanypodinae, Tanytarsini,

Ceratopogonidae, and Chaoborus fly larvae were all present in open-ambient habitats but absent from cages.

In May, larval fish first colonized both exclusion cages and open-ambient habitats, and marbled salamanders disappeared. The patterns in invertebrate abundance that were apparent earlier disappeared or changed. Ceratopogonidae fly larvae, absent from exclosure cages in

April, were modestly more abundant in exclosure cages than open habitats ( F = 4.56, p = 0.049), and Tanypodinae, Tanytarsini, and Chaoborus dipterans also appeared in exclosure cages.

Conversely, Hydroporus beetles and Hesperocorixa water boatmen, two common predators in exclosure cages in April, were largely absent from the wetland in May.

Early in year 2 of the experiment, differences in individual taxa abundances between treatments were again minimal. In February 2004, Ptilostomis caddisfly abundance was higher in cage exclosures than open habitats ( F = 5.12, p = 0.038), but otherwise no significant differences were detected. In March, all invertebrate abundances were similar in exclusion and open-ambient habitats. However, as in year 1, the first widespread effects of exclusion on invertebrate abundance was apparent in April. The abundances of Orthocladiinae ( F = 8.06, p =

0.001), Ceratopogonidae ( F = 4.74, p = 0.045), Anopheles ( F = 5.06, p = 0.039), Pseudosida ( F 15

= 8.71, p = 0.0094), and Cyclopoida ( F = 6.02, p = 0.026) were all greater in exclosure cages than in open-ambient habitats (Figure 4).

Figures and Tables

6 a b 2 5

4 1.5

3 1

sample 2

Fish/sweep .5 1 Salamanders/sweep 0 0 1.2 c d 2 1

.8 1.5

.6 Cage 1 .4 Open .5 .2 Bullfrogs/48 hours Bullfrogs/48hours Salamanders/sweep

0 0 4 12 e f 10 3 8

2 6

1 Bluegill/48 hours Newts/48hours 2

0 0

8/03 8/03 4/ 4/ 2/26/04 4/29/04 4/29/04 3/29/04 2/18/03 1/28/03 2/18/03 5/24/03 3/29/04 1/28/03 5/24/03 2/26/04 12/16/02 ______12/16/02 ______Year 1 Year 2 Year 1 Year 2

Figure 1. Mean abundance (±1 SE) of a) mosquitofish, b) spotted salamanders, c) marbled salamanders, d) bullfrogs, e) newts, and f) bluegill at each sampling date. Cage samples are full enclosures (n=6). Open samples (n=12) are six half exclosures and six open habitats. Marbled salamander, spotted salamander, and mosquitofish abundances are per three one- meter sweeps of a D-frame net (30-cm dia, 1-mm mesh). Newt, bullfrog, and bluegill abundances are per one minnow trap set for 48 hours. Abundance differed across all sampling dates significantly with treatment for spotted salamanders ( F = 5.12, p = 0.042), marbled salamanders ( F = 7.05, p = 0.009), newts ( F = 10.20, p = 0.002), and bluegill (yr 1 F = 1.20, p = 0.29; yr 2 F = 9.72, p = 0.003), but not for bullfrogs ( F = 1.19, p = 0.28) or mosquitofish ( F = 0.80, p = 0.38).

4 * * 3

2 Half Cage Open Habitat 1

log invertebrate abundance log invertebrate

4/8/03 4/29/04 1/28/03 2/18/03 5/24/03 2/26/04 3/29/04 ______12/16/02 ______Year 1 Year 2

Figure 2. Invertebrate abundance (±1 SE) in half cages and open habitats for each sampling date (date F = 60.12, p < 0.0001; treatment F = 1.70, p = 0.19; interaction F = 2.61, p = 0.018). Asterisks indicate months in which treatments differed (May 2003 F = 8.31, p = 0.018; March 2004 F = 7.50, p = 0.021). Abundance values are log transformed abundance per three 1-m sweeps of a D-frame net (30-cm dia, 1-mm mesh size). 18

1.6

1.2 Cage Open .8 log(abundance+1) log(abundance+1)

0 Lestes Chydoridae Ceriodaphnia Hesperocorixa

Figure 3. Invertebrate for which abundance (±1 SE) significantly differed between exclosure cages and open habitats in April 2003. Abundance values were log(abundance+1) transformed per three 1-m sweeps of a D-frame net (30-cm dia,1-mm mesh). Hesperocorixa F = 11.32, p = 0.004; Lestes F = 6.01, p = 0.026; Ceriodaphnia F = 2.65, p = 0.012; Chydoridae F = 4.51, p = 0.050.

2 Cage Open

log(abundance1) + 1

0 Anopheles Pseudosida Cyclopoida Orthocladiinae Ceratopogonida

Figure 4. Invertebrate taxa for which abundance (±1 SE) significantly differed between exclosure cages and open habitats in April 2004. Values are log +1 transformed abundance per three 1-meter sweeps of a D- frame net (30-cm dia, 1-mm Mesh). Orthocladiinae F = 8.06, p = 0.0011; Ceratopogonidae F = 4.74, p = 0.045, Anopheles F = 5.06, p = 0.039; Pseudosida F = 8.71, p = 0.0094; Cyclopoida F = 6.02, p = 0.026.

Lestes Lestes Newts Newts Gerris Gerris Buenoa Buenoa Spotted Berosus Berosus Gyrinus Gyrinus Bluegill Dineutus Dineutus Libellula Bullfrogs Pelocoris Pelocoris 4/04 4/04 Hirudinea Hirudinea Peltodytes Peltodytes Enallagma Hydroporus Hydroporus Laccophilus Tropisternus Tanypodinae Tanypodinae Mosquitofish Hesperocorixa Hesperocorixa Ceratopogonidae Ceratopogonidae

Lestes Lestes Newts Newts Gerris Gerris Bluegill Libellula Bullfrogs 3/04 3/04 Hirudinea Hirudinea Peltodytes Peltodytes Chaoborus Ptilostomis Hydroporus Hydroporus Tropisternus Tanypodinae Tanypodinae Mosquitofish Hesperocorixa Hesperocorixa Ceratopogonidae Ceratopogonidae

Newts Newts Marbled Marbled Libellula Bullfrogs 2/04 2/04 Hirudinea Enallagma Ptilostomis Hydroporus Mosquitofish Tanypodinae Ceratopogonidae ected for all sampling dates. allected sampling for Marbled Anax Anax Lestes Lestes Newts Newts Gerris Gerris Bluegill Dineutus Dineutus 5/03 5/03 Peltodytes Peltodytes Chaoborus Sympetrum Sympetrum Hydroporus Hydroporus Pachydiplax Pachydiplax Tropisternus Tanypodinae Tanypodinae Mosquitofish Hesperocorixa Hesperocorixa Belostomatidae Belostomatidae Ceratopogonidae Ceratopogonidae bled salamanders, Spotted = spotted salamanders, =bled Spotted spotted ators net via samples, sweep collected

Lestes Lestes Agabus Agabus Buenoa Buenoa Marbled Marbled 4/03 4/03 Hirudinea Hirudinea Chaoborus Sympetrum Sympetrum Hydroporus Hydroporus Tanypodinae Tanypodinae Hesperocorixa Hesperocorixa Ceratopogonidae Ceratopogonidae

Agabus Agabus Marbled Marbled 2/03 2/03 Ptilostomis Hydroporus Hydroporus

Agabus Agabus Marbled Marbled 1/03 1/03 Notonecta Notonecta Ptilostomis Hydroporus Hydroporus

Marbled Marbled Ptilostomis Hydroporus Hydroporus 12/02 12/02 Hesperocorixa Hesperocorixa

predators predators Vertebrate Invertebrate Invertebrate bluegill, newts, and bullfrogs collected via minnow traps.marbluegill,minnow andcollected viabullfrogs= newts, (Marbled salamanders, spottedandsalamanders, allinvertebrate mosquitofish, salamanders, pred Table coll invertebrate vertebrate 1. Community composition and of predators salamanders) salamanders)

CHAPTER 4

DISCUSSION

In this experiment, we attempted to test the effects of vertebrate predation by comparing the invertebrate community in predator free exclosure cages to that in open ambient habitats with a natural vertebrate predator complex. Although full exclosure cages did not completely exclude all vertebrate predators, they significantly reduced the abundance of all common vertebrate predators throughout the experiment, suggesting our predator treatment was successful.

Additionally, minimal differences in invertebrate abundances between half cages and open habitats suggests that cage structures were not likely responsible for any patterns in the invertebrate community that developed between the predator treatments. In addition to suggesting that cage effects were not responsible for patterns that developed in the invertebrate community, this lack of differences also allowed us to combine our half cages and open habitats to increase the sample size of open-ambient habitats from 6 to 12.

Overall, differences between the invertebrate communities in cage exclosures and ambient habitats were minimal. Of eight sampling dates, only April 2003 and April 2004 had a number of taxa with abundances significantly differing between exclosures and open-ambient habitats. Of these months, the abundances of only four taxa differed in April 2003, and only five in April 2004. A number of conclusions could be made from these results.

First, these results could develop from an experimental design flaw. The lack of a reduction of both mosquitofish and bullfrogs during year two of the experiment may have limited our ability to detect patterns in invertebrate abundance. This possibility, however, seems 22 unlikely. The relatively low densities of both mosquitofish and bullfrogs throughout the experiment were probably insufficient to structure invertebrate communities. In addition, similar effect of mosquitofish and bullfrog predation between the two habitat types should not preclude our ability to detect responses to common predators. It is also possible that cage artifacts limited our ability to detect patterns in the invertebrate community. However, the lack of significant differences in invertebrate abundances in completely open habitats and half-cage exclosures

(Figure 2) suggests this was not the case. Statistical issues related to repeated analysis could also have affected interpretations, but applying a Bonferroni correction would have reduced our ability to detect differences, further supporting the idea of weak interactions.

The lack of widespread invertebrate responses to vertebrate exclusion may also suggest that predation is not a particularly strong factor in this habitat. The virtual lack of differences between invertebrate abundances in exclosures and open-ambient habitats early in year 1

(December, January, February) and year 2 (February, March) likely suggest that predation was not an important factor in structuring the invertebrate community during winter and early spring.

This pattern was likely due to low predator sizes and activity rates early in the year.

However, in both April 2003 and April 2004, relatively widespread differences in invertebrate abundance were observed between exclusion cages and open-ambient habitats. In

April 2003, large predatory invertebrate taxa ( Hesperocorixa, Lestes ) were less abundant or absent from open-ambient habitats where salamanders were abundant. Conversely, a number of small planktonic invertebrates were more common in habitats with salamanders. These patterns could suggest that direct predation of marbled salamanders was sufficient to reduce the abundances of large mobile taxa, and indirectly reduce invertebrate predation to the benefit of smaller invertebrate fauna (microcrustaceans, fly larvae). In April of 2004, however, a different 23 pattern developed. A number of small planktonic species were less abundant in open-ambient habitats with vertebrate predators than in exclusion cages, suggesting a direct predatory effect of the vertebrate community. Together, these observations suggest that vertebrate predation was a relatively important force in late spring.

The diverse vertebrate and invertebrate predator community, especially in year 2, may make responses in the invertebrate community difficult to detect. In his keystone paper on trophic cascades, Strong (1992) argued that systems where predation effects propagate through trophic levels to primary resources (Brett and Goldman 1996) tend to be species poor. He argued that as communities become speciose, the likelihood of strong interactions decreases. In this study, species richness of both vertebrate and invertebrate predators increased steadily over the duration of the project (Table 1). A number of interactions could have complicated the effects of vertebrate predation. One likely interaction was intraguild predation within the vertebrate complex. Elsewhere, bluegill have eliminated or significantly reduced the survival of a number of amphibian species, including marbled salamanders (Semlitsch 1987), spotted salamanders (Semlitsch 1987, Semlitsch 1988, Figiel 1990), and red-spotted newts (Smith et al

1999). Mosquitofish have also been suggested as a predator on amphibians (Goodsell and Kats

1999).

Vertebrates also interact with invertebrate predators. In wetland habitats, both the eggs and larvae of amphibians and fish can be consumed by large, predatory insects (Van Buskirk

1988, Kehr and Schnack 1991, Gascon 1992, Miad 1993, Tejedo 1993, Blaustein and Margalit

1994, Rowe et al. 1994, Batzer and Wissinger 1996). Those predatory insects are then subject to reciprocal predation by the amphibians and fish after they mature. Interactions within the 24 vertebrate complex and between vertebrates and invertebrates likely complicate community interactions and limit our ability to detect the consequences on invertebrate prey.

One objective of this study was to assess the interaction strength of amphibian predators on the invertebrate community. Due to the complexity of the vertebrate community in year 2, we are unable to isolate the effects of spotted salamander larvae predation on invertebrates.

However, it may be noteworthy that we only saw widespread differences in the invertebrate community between exclosure cages and ambient habitats in year 2 after spotted salmanders appeared in April.

The effects of marbled salamander predation, however, were more obvious in year 1, when marbled salamanders were for the most part the only vertebrate predator present

(December-April). In winter, marbled salamander larvae were small, and predation was likely restricted to small microcrustacean and dipteran taxa (Petranka and Petranka 1980). However, we did not detect any response by those small prey. The effects of marbled salamander predation only became evident in April 2003. Large invertebrate predators as a group appeared to be suppressed by marbled salamander predation. This finding is somewhat surprising because diet analyses elsewhere suggest a preference for smaller prey (see Schultheis and Batzer 2005).

Additionally, feeding behavior of marbled salamander and many other Ambystomatid larvae is thought to be opportunistic and not size selective. Salamander predation also apparently indirectly benefited small invertebrate consumers, suggesting that amphibian predation has the potential to structure invertebrate communities over multiple trophic levels.

Conclusions

Overall, the effects of vertebrate predation on invertebrate abundances in this study were not dramatic. This is surprising given the widespread effects of fish in other aquatic habitats

(Weir 1972, Blois-Heulin et al. 1990, Strayer et a. 1991, Rasmussen 1993, Batzer and Wissinger

1996, Wellborn et al. 1996). Weaker interaction strength in our study may be caused by a combination of seasonally variable predator densities and complex interactions within a diverse vertebrate predator complex. Our findings highlight the importance of amphibian predation, indicating that these animals should be considered in the analysis of vertebrate predation in wetland habitats. Other vertebrate predators with a similar transient nature include migrating waterfowl and shorebirds (Batzer et al. 1993, Weber and Haig 1996, Dabbert and Martin 2000), and fish migrating into floodplains to feed or spawn (Ross and Baker 1983). Like amphibian predation, the effects of these predators on invertebrate communities have received little attention, but have the potential to be seasonally important predators of aquatic invertebrates.

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