Rothermel for initiation of the Land-use Effects on Amphibian Populations (LEAP) project. Additionally, I would like to extend my gratitude to the rest of the LEAP.
GRAY TREEFROG BREEDING SITE SELECTION AND OFFSPRING PERFORMANCE IN RESPONSE TO FOREST MANAGEMENT
A Thesis Presented to The Faculty of the Graduate School University of Missouri-Columbia
In Partial Fulfillment Of the Requirements for the Degree Masters of Science
By DANIEL J. HOCKING Dr. Raymond D. Semlitsch, Thesis Supervisor
May 2007
The undersigned, appointed by the Dean of the Graduate School, have examined the thesis entitled:
GRAY TREEFROG BREEDING SITE SELECTION AND OFFSPRING PERFORMANCE IN RESPONSE TO FOREST MANAGEMENT
Presented by Daniel J. Hocking A candidate for the degree of Master of Science, and herby certify that in their opinion it is worthy of acceptance.
__________________________________________ Professor Raymond D. Semlitsch
__________________________________________ Professor James Carrel
__________________________________________ Professor Joshua Millspaugh
ACKNOWLEDGEMENTS During my work towards the completion of this thesis I have become indebted to many individuals and organizations. As such, I would first like to thank Gus Raeker and the Missouri Department of Conservation for permissions and help with the forest manipulations. Of course this would not have been possible without the initial idea and planning, so I would like to thank Ray Semlitsch, Mac Hunter, Whit Gibbons, and Betsie Rothermel for initiation of the Land-use Effects on Amphibian Populations (LEAP) project. Additionally, I would like to extend my gratitude to the rest of the LEAP collaborators for insightful discussions and encouragement. I would like to thank all the members of the Semlitsch lab for the discussions and encouragement that have helped me in the endeavor. Special thanks to my advisor, Ray Semlitsch for his encouragement, numerous discussions and help on all aspects of my project. Additionally, Josh Millspaugh, Jim Carrel, John Faaborg, and Aram Calhoun have all provided valuable comments and critiques of my project, challenging me to improve it along the way. The field work necessary to complete my project would not have been possible or nearly as enjoyable without the help of Chris Conner, Eric Wengert, Brett Scheffers, Jaime Sias, John Crawford, Bethany Williams, Sara Storrs, Tim Altnether, Scott Altnether, and Tracy Rittenhouse. A special thank you is extended to John Crawford for the numerous discussions about projects and especially for support during the perilous journey transporting cattle tanks across the bridge. Statistical analysis in this thesis has benefited through discussions with Mark Ellersieck, John Fresen, Ray Semlitsch, and Josh Millspaugh. This thesis and my writing
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in general have improved from the comments so generously provided by Betsie Rothermel, Tracy Rittenhouse, John Crawford and Lesley Hocking. Additionally, I would never have completed everything I needed to do without the technical and logistical support of the Life Sciences Fellowship Program and Division of Biological Sciences, with special thanks to Josh Hartley, Alan Marshall, and Nila Emerich. Finally, I need to thank my family for the support and willingness to listen when things weren’t going as planned. Most of all I would like to thank my wife, Lesley Hocking. This thesis would not have been possible without her loving support and critical review. She deserves all the credit for any parts of my writing that are intelligible and none of the criticism for the rest of it. She also warrants particular thanks for being supportive through long months of field work and the irritability that ensues.
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TABLE OF CONTENTS
ACKNOWLEDGEMENTS…………………………………………………………….....ii LIST OF TABLES……………………………………………………………...………...vi LIST OF FIGURES………………………………………………………...…………....vii ABSTRACT………………………………………………………………………….....viii
CHAPTER 1. INTRODUCTION…………………………………………………….......…………..1 Literature cited…………………………………………………………………….5 2. IMPORTANCE OF LANDSCAPE COMPLEMENTATION: EFFECTS OF FORESTRY TREATMENTS ON THE BREEDING-SITE SELECTION OF GRAY TREEFROGS (HYLA VERSICOLOR)………………………………………10 Abstract……………………………………………………………......................10 Introduction…………………………………………………………....................11 Methods……………………………………………………..........................……14 Study site and experimental forest manipulations………………….........14 Experiment 1……………………………………………………..........…16 Experiment 2……………………………………………………..............17 Results……………………………………………………....................…………19 Results of experiment 1………………………………………............….19 Results of experiment 2………………………...............………………..20
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Discussion……………………………………………………….................…….21 Acknowledgements………………………………………………........................25 Literature Cited…………………………………………………..........................25
3. EFFECTS OF EXPERIMENTAL CLEARCUT LOGGING ON GRAY TREEFROG (HYLA VERSICOLOR) TADPOLE PERFORMANCE……........…….39 Abstract………………………………………………..................………………39 Introduction…………………………………................................………………40 Methods……………………………........................……………………………..43 Study design……………………………….............................…………..43 Data collection………...................................……………………………44 Statistical analyses…………………………...................………………..45 Results…......................…………………………………………………………..47 Discussion……………..............…………………………………………………48 Acknowledgements……………..............………………………………………..52 Literature Cited………………………….........………………………………….53
4. CONCLUSIONS AND FUTURE DIRECTIONS..............…………………………68 Literature cited…………………………………………..........………………….72
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LIST OF TABLES Table
Page
2.1
Analysis of variance (ANOVA) of the number of eggs oviposited per pool in a split-block design…………………………………………………..35
3.1
Abbreviations and descriptions of the variables and 9 a priori models used to analysze tadpole performace…………………………..………………..60
3.2
Univariate analysis of variance testing the differences among habitat treatments for time to metamorphosis, mass at metamorphosis, and percent survival…………………………………………………..………….61
3.3
Linear regression models for survival, time and size at metamorphosis. Model fit was evaluated using Akaike’s Information Criterion for small sample sizes (AICc) and Akaike’s Weight (w)……………………………………………………………..62
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LIST OF FIGURES Figure
Page
2.1
A) The aerial photograph of one study site in the Daniel Boone Conservation Area, Warren County, MO shows the four forest management treatments with a pond at the center. The smaller circles show the placement of the artificial pools in each habitat. B) The expanded view diagrams the arrangement and distances of the low, medium, and high isolation pools within a forest treatment…………………………………………………………………………36
2.2
Interaction diagrams of the A) mean number of eggs laid in each forest and isolation treatment combination and B) eggs per oviposition event in each treatment combination………………………………………..…...38
2.3
Mean number of A) oviposition events and B) male captures per survey night in each of the four forest treatments……………………………..…40
3.1
Periphyton productivity measure upon the addition of tadpoles, at the onset of metamorphosis, and at the end of the experiment. Chlorophyll a (µg/m2) from periphyton samples indicated productivity………………………………………………………………………64
3.2
Tadpole performance in the four treatments based on A) mean time to metamorphosis (days), B) mean mass at metamorphosis, and C) mean percent survival. Bars represent means with standard error bars. Statistical significance among treatments is indicated by letters above each bar as determined using Fisher’s LSD ( = 0.05)………………………………………………………….66
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GRAY TREEFROG BREEDING SITE SELECTION AND OFFSPRING PERFORMANCE IN RESPONSE TO FOREST MANAGEMENT
Daniel J. Hocking
ABSTRACT
Amphibian diversity and abundance are generally reduced following clearcut logging. These impacts often last for decades, but little is know about why diversity and abundance are depressed. Attempts to understand the mechanisms contributing to the observed amphibian responses have focused on the growth and survival of juveniles and adults--the premise being that terrestrial juveniles and adults are susceptible to desiccation through increased wind and temperatures in clearcut habitats. To address other possible mechanisms, I examined gray treefrog breeding site selection and subsequent offspring performance following experimental forest manipulations. Using wading pools and cattle tanks, I found that gray treefrogs select breeding sites in clearcuts more than those in forested habitats. Additionally, females preferred breeding sites close to forest edges over sites farther into clearcuts. To determine the influence of breeding site selection of the offspring, I stocked cattle tanks along a forest-clearcut gradient with gray treefrog tadpoles. Tadpole survival was greatest in the clearcut treatments. However, tadpoles in the clearcuts also had a shorter larval period. Having a shorter larval period can benefit individuals by reducing the time to maturity, thereby potentially increasing lifetime reproduction. But metamorphs were smaller in the clearcuts, which
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can reduce juvenile survival, increase time to maturity, and reduce fecundity as adults. Smaller juveniles may be particularly susceptible to mortality in the clearcuts through decreased dispersal ability and increased risk of desiccation. Despite the preference for open canopy breeding sites, clearcuts can create resistance for females moving between terrestrial forest habitat and aquatic breeding sites. Also, juvenile survival and dispersal success are likely to be reduced in clearcuts. Although reduced canopy cover over breeding ponds provides some benefits for tadpoles, logging operations should avoid isolating aquatic habitat from forested uplands.
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CHAPTER 1
INTRODUCTION
Daniel J. Hocking
Habitat loss and alteration remain the greatest threats to the conservation of biodiversity (Cushman 2006; Stuart et al. 2004; Wilcove et al. 1986). Loss and alteration result from numerous human actions including urban development, habitat conversion to agriculture, and natural resource extraction. Timber harvesting is one type of resource extraction that decreases the amount of available forest habitat at a given time and alters the surrounding habitats. In particular, clearcut logging is a common practice because it is the most cost-effective method of timber extraction. Clearcutting has also been suggested as a necessity for the growth and establishment of many early successional plants (Keenan & Kimmins 1993). Despite the potential benefit of small clearcuts (< 20 ha) for landscape diversity, the practice remains contentious and controversial. In addition to physical habitat alteration through the removal of the canopy trees, clearcutting also affects the microclimate of a site. The surface, soil, and air temperatures in clearcuts are higher on average and experience greater fluctuations than in uncut forests (Keenan & Kimmins 1993). Higher temperatures coupled with increased wind and solar radiation present physiological challenges for many species. Most notably, amphibians are sensitive to changes in microclimate due to their permeable skin that allows gas and water exchange with the environment (Duellman & Trueb 1994).
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Concern about global amphibian declines coupled with their unique physiology has lead researchers to examine terrestrial amphibian responses to clearcutting (e.g. Ash 1997; deMaynadier & Hunter 1995; Petranka et al. 1993; Stuart et al. 2004). This practice has been found to reduce the abundance and diversity of amphibians (e.g. Ash 1997; deMaynadier & Hunter 1995; Herbeck & Larsen 1999; Karracker & Welsh 2006). Although timber harvesting is a temporary alteration, the effects on amphibians can persist for decades (e.g. Ash 1997; Herbeck & Larsen 1999; Semlitsch et al. 2006). We do not understand the mechanisms contributing to these observed patterns despite studies revealing reduced diversity and abundance following clearcutting. In fact, Ash and Bruce (1994) state that “we known they [amphibians] disappear from clear-cuts, but that is all we know.” More mechanistic studies have been conducted since 1994 but have examined a limited number of species and life stages. Most research investigating amphibian declines following timber harvest focuses on terrestrial species or the terrestrial stage of species with complex life cycles (Ash 1997; deMaynadier & Hunter 1995; Johnston & Frid 2002; Karracker & Welsh 2006; Petranka et al. 1993; Todd & Rothermel 2006). However, species with complex life cycles breed in aquatic habitats, including a larval stage restricted to those aquatic habitats until metamorphosis. The use of these aquatic habitats by adults may be influenced by timber harvesting, and logging near aquatic habitats alters the environment for aquatic larvae. Few studies have examined the breeding site selection and subsequent larval performance in response to forest alteration (Cushman 2006; deMaynadier & Hunter 1995).
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The gray treefrog is an ideal species to test the impacts of forest alteration on breeding site selection and offspring performance because individuals require both terrestrial and aquatic habitats, and they readily breed in artificial ponds that can be experimentally manipulated (Johnson & Semlitsch 2003; Resetarits & Wilbur 1989). Gray treefrogs live and forage in trees but make annual migrations to small ponds to mate and lay eggs (Johnson 2005). They often oviposit in small isolated ponds that receive little or no legal protection from logging in proximity to the pond. Additionally, gray treefrogs are selective in their use of oviposition habitats and prefer breeding habitats devoid of competitors and predators (Resetarits & Wilbur 1989). Gray treefrog tadpoles are vulnerable to multiple predatory taxa including odonate larvae (Caldwell et al. 1980; Semlitsch & Gibbons 1988), fish (Fauth 1990; Semlitsch & Gibbons 1988), and salamanders (Caldwell et al. 1980; Fauth 1990). These past studies reveal that gray treefrogs have evolved mechanisms to select oviposition habitats that maximize their fitness through increased offspring survival. Therefore, it is important to examine both breeding site selection and the implications of site selection on the offspring (larvae). Depending on both biotic and abiotic conditions, larvae may alter the length of their larval period as well as their size at metamorphosis. The time and size at metamorphosis are directly related to fitness, as individuals that metamorphose earlier and at a larger size reach maturity sooner and have larger clutch sizes (Berven 1990; Semlitsch et al. 1988; Smith 1987). Clearcutting around ephemeral ponds opens the forest canopy, which can alter the resources available for amphibian larvae. As such, tadpoles grow faster and have greater survival in open canopy ponds compared with closed canopy ponds (Skelly et al. 2002; Werner & Glennemeier 1999). Additionally,
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Schiesari (2006) found that higher temperatures and food quality in open canopy ponds improved tadpole performance. Therefore, clearcutting around ponds may be expected to improve the habitat quality for the aquatic stage of many anuran species. However, the open canopy created by clearcutting can also alter the predator community in the pond. Anisopteran (Odonata) larvae are known to prey upon tadpoles (Petranka & Hayes 1998; Semlitsch 1990; Skelly & Werner 1990), and many anisopteran species prefer to breed in open canopy ponds, resulting in higher predator densities than closed canopy ponds (Corbet 2004; McCauley 2005). Predators can directly affect on tadpole survival but can also have indirect impacts including costly behavioral and morphological responses (Relyea 2002a; Relyea & Hoverman 2003; Skelly 1992; Skelly & Werner 1990). Behaviorally, tadpoles may reduce foraging activity in response to these predators, resulting in reduced growth and subsequent size-specific mortality (Lawler 1989; Semlitsch 1990). Morphological responses to predators include deeper, more muscular tails with increased coloration. These morphological antipredator responses have fitness costs that can persist after metamorphosis (McCollum & Leimberger 1997; McCollum & Van Buskirk 1996; Relyea 2003). Despite the fitness costs of defense, tadpoles that survive can potentially benefit through reduced competition (Alford 1999; Fauth 1990; Relyea 2002b). My studies examine gray treefrog breeding site selection in response to experimental forest management and subsequent larval performance. Specifically, Chapter 2 addresses breeding site selection among four experimentally altered forest habitats. We also examine how distance from a forest edge changes breeding site selection in clearcuts and control forests. In Chapter 3, we test the impact of clearcutting
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on gray treefrog tadpoles along the same forest-clearcut gradients. We use cattle tanks as experimental mesocosms to examine tadpole growth and survival along the gradient. Although we expect the open canopy in clearcuts to benefit gray treefrog tadpoles, we also expect greater colonization of predatory invertebrates in the clearcut ponds. The abundance of predators may hinder the ability of tadpoles to exploit open canopy resources in recent clearcuts.
LITERATURE CITED Alford, R. A. 1999. Ecology: resource use, competition, and predation. Pages 189-214 in R. W. McDiarmid, and R. Altig, editors. Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago. Ash, A. N. 1997. Disappearance and return of plethodontid salamanders to clearcut plots in the southern Blue Ridge Mountains. Conservation Biology 11:983-989. Ash, A. N., and R. C. Bruce. 1994. Impacts of timber harvesting on salamanders. Conservation Biology 8:300-301. Berven, K. A. 1990. Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599-1608. Caldwell, J. P., J. H. Thorp, and T. O. Jervey. 1980. Predator-prey relationships among larval dragonflies, salamanders, and frogs. Oecologia 46:285-289. Corbet, P. S. 2004. Dragonflies: Behavior and Ecology of Odonata. Cornell University Press, Ithaca. Cushman, S. A. 2006. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128:231-240.
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deMaynadier, P. G., and M. L. Hunter, Jr. 1995. The relationship between forest management and amphibian ecology: a review of the North American literature. Environmental Review 3:230–261. Duellman, W. E., and L. Trueb 1994. Biology of Amphibians. Johns Hopkins University Press, Baltimore. Fauth, J. E. 1990. Interactive effects of predators and early larval dynamics of the treefrog Hyla chrysoscelis. Ecology 71:1609-1616. Herbeck, L. A., and D. R. Larsen. 1999. Plethodontid salamander response to silvicultural practices in Missouri Ozark forests. Conservation Biology 13:623-632. Johnson, J. R. 2005. Multi-scale investigations of gray treefrog movements, patterns of migration, dispersal, and gene flow. Page 246. Division of Biological Sciences. University of Missouri, Columbia. Johnson, J. R., and R. D. Semlitsch. 2003. Defining core habitat of local populations of the gray treefrog (Hyla versicolor) based on choice of oviposition site. Oecologia 137:205-210. Johnston, B., and L. Frid. 2002. Clearcut logging restricts the movements of terrestrial Pacific giant salamanders (Dicamptodon tenebrosus Good). Canadian Journal of Zoology 80:2170-2177. Karracker, N. E., and H. H. Welsh, Jr. 2006. Long-term impacts of even-aged timber management on abundance and body condition of terrestrial amphibians in Northwestern California. Biological Conservation 131:132-140. Keenan, R. J., and J. P. Kimmins. 1993. The ecological effects of clear-cutting. Environmental Review 1:121-144.
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Lawler, S. P. 1989. Behavioural responses to predators and predation risk in four species of larval anurans. Animal Behaviour 38:1039-1047. McCauley, S. J. 2005. Species distributions in anisopteran odonates: effects of local and regional processes. Page 224. Ecology and Evolutionary Biology. University of Michigan, Ann Arbor. McCollum, S. A., and J. D. Leimberger. 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615-621. McCollum, S. A., and J. Van Buskirk. 1996. Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583-593. Petranka, J. W., M. E. Eldridge, and K. E. Haley. 1993. Effects of timber harvesting on southern Appalachian salamanders. Conservation Biology 7:363-370. Petranka, J. W., and L. Hayes. 1998. Chemically mediated avoidance of a predatory odonate (Anax junius) by American toad (Bufo americanus) and wood frog (Rana sylvatica) tadpoles. Behavioral Ecology and Sociobiology 42:263-271. Relyea, R. A. 2002a. Costs of phenotypic plasticity. The American Naturalist 159:272282. Relyea, R. A. 2002b. The many faces of predation: how induction, selection, and thinning combine to alter prey phenotypes. Ecology 93:1953-1964. Relyea, R. A. 2003. Predators come and predators go: the reversibility of predatorinduced traits. Ecology 84:1840-1848. Relyea, R. A., and J. T. Hoverman. 2003. The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596-604.
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Resetarits, W. J., Jr., and H. M. Wilbur. 1989. Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220-228. Schiesari, L. 2006. Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biology 51:412-423. Semlitsch, R. D. 1990. Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology 68:1027-1030. Semlitsch, R. D., and J. W. Gibbons. 1988. Fish predation in size-structured populations of treefrog tadpoles. Oecologia 75:321-326. Semlitsch, R. D., T. J. Ryan, K. Hamed, M. Chatfield, B. Drehman, N. Pekarek, M. Spath, and A. Watland. 2007. Salamander abundance along road edges and within abandoned logging roads in Appalachian forests. Conservation Biology 21: 159167. Semlitsch, R. D., D. E. Scott, and J. H. K. Pechmann. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. Skelly, D. K. 1992. Field evidence for a cost of behavioral antipredator response in a larval amphibian. Ecology 73:704-708. Skelly, D. K., L. K. Freidenburg, and J. M. Kiesecker. 2002. Forest canopy and the performance of larval amphibians. Ecology 83:983-992. Skelly, D. K., and E. E. Werner. 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology. 71:2313-2322. Smith, D. C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344-350.
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Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman, and R. W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786. Todd, B. D., and B. B. Rothermel. 2006. Assessing quality of clearcut habitats for amphibians: effects on abundances versus vital rates in the southern toad (Bufo terrestris). Biological Conservation 133:178-185. Werner, E. E., and K. S. Glennemeier. 1999. Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999:1-12. Wilcove, D. S., C. H. McLellan, and A. P. Dobson. 1986. Habitat fragmentation in the temperate zone. Pages 237-256 in M. E. Soule, editor. Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates Inc., Sunderland, MA.
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CHAPTER 2
IMPORTANCE OF LANDSCAPE COMPLEMENTATION: EFFECTS OF FORESTRY TREATMENTS ON THE BREEDING-SITE SELECTION OF GRAY TREEFROGS (HYLA VERSICOLOR)
Daniel J. Hocking and Raymond D. Semlitsch
ABSTRACT Despite numerous studies showing reduced amphibian abundance and diversity following habitat modification, little is known about the mechanisms causing these observed patterns. We examined the effects of four experimental forest management treatments on breeding site selection by gray treefrogs (Hyla versicolor) in Missouri. Our study of four management treatments included a clearcut with the high amounts of coarse woody debris (CWD), a clearcut with lower amounts of CWD, a partial timber cut, and an uncut control. To examine gray treefrog breeding site selection, we placed five plastic wading pools in each treatment replicated at three sites. We found that treefrogs laid significantly more eggs in the clearcuts (low-CWD 77 185 eggs; high-CWD 51 990 eggs) than in either the partial (13 553 eggs) or the control (14 068 eggs) treatments. In a second experiment, we further examined the importance of spatial relationships between breeding sites and mature forest habitat by placing cattle tanks 50 m into a clearcut, 10 m into a clearcut, 10 m into a forest, and 50 m into a forest. Gray treefrogs oviposited eggs on more occasions in the clearcut-edge tanks (17 occasions) than in the clearcut (7),
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forest (8), or forest edge (3) tanks, but eggs were not counted. Despite the preference for open canopy breeding sites, clearcuts can create resistance for females moving between terrestrial forest habitat and aquatic breeding sites. Although reduced canopy cover over breeding ponds may be beneficial for some amphibians, logging operations should avoid isolating aquatic habitat from forested uplands.
INTRODUCTION Habitat alteration and destruction remain the greatest threat to amphibians (Lannoo 2005; Semlitsch 2003). Therefore, it is essential to understand the multiple habitat needs of species to ensure population persistence in an increasingly fragmented landscape. Due to their biphasic life cycle, pond-breeding amphibians require terrestrial habitat for juvenile and adult growth and maturity, in addition to aquatic habitat for larval growth and development. Some species require additional habitat types for over-wintering (Johnson et al. In review; Lamoureux & Madison 1999), and foraging (Johnson et al. In review; Lamoureux et al. 2002). Further, amphibians require these complementary habitats in proper spatial and temporal relationship to allow for movement between them. Landscape complementation refers to both the amount of different habitat types in a given area and the spatial relationships among them (Dunning et al. 1992). Consideration of landscape complementation is essential for amphibian conservation because many human-altered habitats create significant resistance to amphibian migration and dispersal (Chan-McLeod 2003; Gibbs 1998; Rittenhouse & Semlitsch 2006; Rothermel 2004; Rothermel & Semlitsch 2002). Even if forests offer sufficient quantities
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of required habitats, the spatial relationships among them could render some habitats unavailable. Forestry practices can create patchy, fragmented forests, separated by an inhospitable habitat matrix for some species. In particular, clearcutting generally reduces the abundance and diversity of amphibians (e.g. Ash 1997; deMaynadier & Hunter 1995; Herbeck & Larsen 1999; Karracker & Welsh 2006). Although timber harvest is a temporary alteration, the effects on amphibians can persist for decades (e.g. Ash 1997; Herbeck & Larsen 1999; Semlitsch et al. 2006). Individuals residing in recently clearcut terrestrial habitats face greater risks of mortality due to desiccation (Rittenhouse unpublished data). In clearcuts, individuals may also have stunted post-metamorphic growth rates (Todd & Rothermel 2006) which can reduce total lifetime reproduction (Berven 1990; Semlitsch et al. 1988; Smith 1987). Clearcutting can also impact the terrestrial stages of pond-breeding amphibians by creating inhospitable habitat that impedes the movement of migrating individuals. Altered habitats have greater resistance for adults migrating to or from a breeding pond (Chan-McLeod 2003; Mazerolle & Desrochers 2005; Rittenhouse & Semlitsch 2006). Additionally, non-forested habitat creates significant resistance for emigrating juveniles following metamorphosis. Even juveniles of the American toad (Bufo americanus), considered a habitat generalist as an adult, are limited in emigration ability in nonforested habitats (Rothermel 2004; Rothermel & Semlitsch 2002). Clearcut habitats may restrict juvenile dispersal events, thereby altering the metapopulation dynamics and restricting the rescue effect (Brown & Kodric-Brown 1977; Gill 1978; Pope et al. 2000; Rothermel 2004).
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Despite the detrimental impacts of logging on the terrestrial stage, opening the canopy over a pond through logging can be beneficial for the aquatic larvae of some amphibian species. Open canopy ponds have greater primary productivity, which increases high quality food resources for herbivorous tadpoles. Additionally, the increased solar radiation warms the water, resulting in increased developmental rates beneficial to aquatic larvae (Halverson et al. 2003; Schiesari 2006; Skelly et al. 2002; Werner & Glennemeier 1999). However, open canopy ponds have greater abundances of dragonflies, increasing the risk of predation on amphibian larvae (Gunzburger & Travis 2004; McCollum & Leimberger 1997; Semlitsch 1990). In the absence of parental care, adults must choose breeding habitats that balance the benefits and risks to the offspring with the risks to themselves. The gray treefrog is an ideal species to consider because individuals require both terrestrial and aquatic habitats, and they readily breed in artificial ponds that can be experimentally manipulated (Johnson & Semlitsch 2003; Resetarits & Wilbur 1989). Gray treefrogs live and forage in trees but make annual migrations to small ponds to mate and lay eggs (Johnson 2005). They often oviposit in small isolated ponds that receive little or no legal protection from logging in proximity to the pond. Additionally, gray treefrogs are selective in their use of oviposition habitats by preferring breeding habitats devoid of competitors and predators (Resetarits & Wilbur 1989). Gray treefrog tadpoles are vulnerable to multiple predatory taxa including odonate larvae (Caldwell et al. 1980; Semlitsch & Gibbons 1988), fish (Fauth 1990; Semlitsch & Gibbons 1988), and salamanders (Caldwell et al. 1980; Fauth 1990). These past studies reveal that gray treefrogs have evolved mechanisms to select oviposition habitats that maximize their
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fitness through increased offspring survival. However, in a fragmented landscape, adult anurans have to balance the optimal conditions for their offspring with their own risks in an altered forest environment. Understanding the mechanisms causing the patterns observed in forest landscape studies is critical in understanding how to mitigate for the detrimental effects on amphibians (Cushman 2006; Rittenhouse & Semlitsch 2006). Our study addresses adult use of habitat for oviposition in an altered forest environment. Specifically, we examine gray treefrog (Hyla versicolor) breeding site selection in response to four different forestry treatments and determine how distance from a forest patch affects breeding site use in recently clearcut habitats. We experimentally test the importance of spatial relationships between aquatic breeding sites and terrestrial habitat in an altered forest. This information will help elucidate how forest alteration impacts the connectivity between terrestrial and aquatic habitats essential for amphibian persistence.
METHODS Study site and experimental forest manipulations Our research was conducted as part of an experiment examining the impacts of different forest management practices on pond-breeding amphibians. The Land-use Effects on Amphibian Populations (LEAP) project compares amphibian responses to four forest management treatments surrounding ephemeral ponds. All sites used in our study are located within the Daniel Boone Conservation Area (1,424.5 hectares) in Warren County, Missouri. The sites are situated in a secondary growth oak-hickory forest (80 – 100 years old) in the upper Ozark Plateau. The pond at the center of each of three sites were
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selected from approximately 40 ponds in the conservation area to be greater than 1000 m apart and similar in size (high water area 160 – 330 m2). These ponds were originally built for wildlife and are greater than 50 years old. The four treatments consist of a clearcut with high levels of coarse woody debris (High-CWD), a clearcut with less CWD (Low-CWD), a partial canopy removal, and an unmanipulated control forest (Fig. 2.1). In the clearcuts, all marketable timber greater than 25 cm diameter at breast height (DBH) was removed for sale. The clearcuts with the high CWD had the remaining trees (< 25 cm DBH) felled and left on the ground. In the clearcuts with low CWD, the remaining trees (< 25 cm DBH) were left standing to reduce the CWD on the ground, but were killed by girdling. The partial cut treatment was thinned to a basal area of 5.6 m2 per acre which is approximately 60% stocking level. This was achieved by girdling or felling poor quality trees and undesirable species (such as Acer saccharum). This type of partial cut treatment is a common part of timber stand improvement in central Missouri. The two clearcut treatments were designed to test the potential for retaining more CWD to mitigate negative effects of clearcutting on amphibians. CWD has the potential to benefit amphibians by providing moisture retaining refugia. To delineate the treatments, the circular area with a radius of 164 m from a pond was divided into four equal quadrants. A radius of 164 m was used because this distance represents the core habitat for pond breeding salamanders (Semlitsch 1998). The control treatment was randomly assigned to one quadrant, the clearcut treatments were randomly assigned to the two quadrants adjacent to the control, and the partial treatment was fixed
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in the quadrant opposite the control (Fig. 2.1). All forest treatment manipulations were performed between March 2004 and February 2005.
Experiment 1 To test how different forest management treatments affect oviposition habitat selection by gray treefrogs, we used artificial pools located in each of the forest management treatments. Five plastic wading pools (1.5 m diameter) were placed in each treatment at three levels of isolation within the treatments in February 2005. Pools filled with rainwater by 1 April, prior to gray treefrogs emerging from over-wintering. Because we expected more adult treefrogs to be concentrated near the pond and in the forested treatments, we defined degree of isolation with respect to both distance from the pond and from treatment edges. At low isolation, the pools were 10 m from the pond and 1012 m from each treatment edge. The pools at medium isolation were 64 m from the pond edge and 10-12 m from the treatment edge. The pools at high isolation were placed 115 m from the pond edge and 45 m from the treatment edge. There was one pool in each treatment at low isolation, and two pools in each treatment at each of the medium and high isolation levels (Fig. 2.1). We replicated this design at three study sites each separated by greater than 800 m. Pools were checked for treefrog eggs for 47 days following the first oviposition event on 7 May 2005, with no greater than 48 hrs between monitoring periods. Hyla versicolor is the only treefrog (genus: Hyla) that occurs in the Daniel Boone Conservation Area, and females lay their eggs in distinctive floating packets of 20-90 eggs, allowing for reliable identification. Using artificial wading pools prevented the use
16
of pools by other amphibians, with one exception. Two American toads (Bufo americanus) were found with eggs in one pool on 10 June. The individuals and their eggs were removed, and no additional eggs from other species were found in any pool. Treefrog eggs were counted, removed from the pools, and transferred to the pond at the center of each site. Any tadpoles that hatched from missed eggs were removed and assigned to a previous oviposition event based on tadpole development. All leaves and debris were consistently removed from the pools to ensure all the eggs in a pool could be located and counted. To test for differences in oviposition habitat selection among forest treatments and isolation levels we used an analysis of variance (ANOVA). Our experiment was set up as a balanced split-block design with the main plots (forest treatments) arranged in complete blocks (sites). The subplots (isolation) were in the same location within each forest treatment, therefore separate error terms were used for the forest treatment, isolation, and forest treatment by isolation interaction effects. The number of eggs was square-root transformed to meet the assumptions of normality and homogeneity of variance. For comparison with the second experiment, the number of eggs divided by the number of times eggs were found in a pool (oviposition events) was compared among treatments using a split-block ANOVA.
Experiment 2 We designed a second experiment to examine breeding site selection in relation to a forest-clearcut edge with distance from existing breeding ponds held constant. In this experiment cattle tanks (2 m diameter) were placed in clearcut, clearcut edge, forest edge,
17
and forest habitats in February 2006. Tanks in the clearcut treatment were 50 meters from the nearest forest edge. Clearcut edge treatments had tanks 10 m from the forest edge, forest edge tanks were in a forest 10 m from a clearcut, and forest treatments were 50 m from the nearest clearcut. All tanks an equal distance (65 m) from the nearest pond. This design was replicated using three forest-clearcut edges separated by more than 800 m. All clearcuts were 12 to 18 months old at the start of the experiment. Each tank was filled with 570 liters of tap water and allowed to dechlorinate for greater than 48 hours before the addition of 1 kg of dry deciduous leaf litter. Additionally, one liter of pond water was added to each tank as phytoplankton and zooplankton inoculum. Tanks were checked for eggs following rain events and at a minimum of once per week from 17 April until 13 July 2006. Each tank was classified as used or unused during each census. Each time a tank was used was considered one oviposition event. Litter in the bottom each tank and the large size of the tank increased breeding site realism but prevented enumeration of eggs. Therefore, we used the number of oviposition events as the response variable for analysis. Eggs were not counted and were left in the tanks to account for the influence of conspecific attraction or density dependent avoidance on breeding site selection (i.e. Marsh & Borrell 2001; Resetarits & Wilbur 1989; Spieler & Linsenmair 1997). Additionally, we visited each tank on 38 nights between 17 April and 29 June. Calling males were hand captured and given a unique toe-clip. All woody branches (>1 cm diameter) within three meters radius of the tank and below three meters from the ground were searched using a headlamp. We compared the number of nights males were captured and mean number of males captured per night to examine if males and females
18
respond to the treatments in the same way. If males respond as females do, then it is possible that females are responding to the habitat choices of the males rather than making habitat choices for oviposition preference. Single factor analysis of variance was used to test for differences in response variables among treatments. All statistical procedures for both experiments were performed using Statistical Analysis Software (SAS) version 9.1 and tested at a significance level of α = 0.05.
RESULTS Results of experiment 1 We counted a total of 156 796 eggs laid in the artificial pools across all treatments. The mean number of eggs laid differed significantly among the forest treatments (P = 0.0141, Table 2.1) and among isolation levels (P = 0.0194, Table 2.1). Treefrogs preferred to oviposit in the clearcuts (low CWD 77 185 eggs; high CWD 51 990 eggs) compared with the partial (13 553 eggs) or the control (14 068 eggs) treatments. The two clearcut treatments did not differ significantly, nor was there a significant difference between the partial cut and the control treatments (Fig. 2.2). The number of eggs tended to decrease with increasing isolation (Fig. 2.2). Pairwise comparisons of isolation levels revealed significant differences in the mean number of eggs laid among the low and high isolation treatments (P = 0.0234) and among the medium and high treatments (P = 0.0088), but not among the low and medium treatments (P = 0.2921). The forest treatment by isolation level interaction effect was marginally significant (P = 0.0624). In the two clearcut treatments oviposition decreased with increasing isolation (Fig. 2.2). The partial cut and
19
control treatments both had few eggs and an isolation effect was not found in either the partial or control treatments. The number of eggs per oviposition event did not differ among forestry treatments (P = 0.4283) or isolation treatments (P = 0.6527). However, there was a significant interaction effect (P = 0.0053). The number of eggs per oviposition event increased with isolation within the control and partial cut treatments. The opposite was true in both of the clearcut treatments where the number of eggs per event decreased with increasing isolation.
Results of experiment 2 We recorded 35 oviposition events on 18 occasions. Eggs were laid in all tanks except one tank in a forest-edge treatment. There was a marginally significant difference among the four treatments (P = 0.0773). Comparison using Fisher’s Least Significant Difference (LSD) reveals more oviposition events in the clearcut-edge treatment than in any of the other treatments (Fig. 2.3A). Although these results are only marginally significant, we believe that they are biologically meaningful. Due to the scale of this project, we only used three replicates which resulted in low power to detect a significant difference (power = 0.676). Additionally, we used oviposition events as our response variable rather than number of eggs, which is not as precise a measure of reproductive output. There was a marginally significant effect of treatment on the mean number of males captured per night (P = 0.0711). Contrast comparisons between the clearcut treatments and the forest treatments indicate that the forest and forest-edge treatments had fewer males captured on average compared with the clearcut and clearcut-edge
20
treatments (P = 0.0134, Fig. 2.3B). Unlike the female response, there was no difference between the clearcut and clearcut-edge treatments using Fisher’s LSD. There was no difference among the treatments in the number of nights males were captured at the tanks (P = 0.2476).
DISCUSSION Gray treefrogs strongly selected pools for oviposition located in clearcuts compared with pools in partial cut treatments or control forests. The preference for breeding sites located in clearcut treatments is likely a response to open canopy. Open canopy ponds are beneficial for the larval stage of many anurans because of higher quality food resources and higher temperatures result in increased growth and developmental rates (Schiesari 2006; Skelly et al. 2002; Werner & Glennemeier 1999). Increased growth and development benefits the larvae by reducing the time they are vulnerable to gape-limited predators (Semlitsch & Gibbons 1988; Skelly 1996) and decreasing the risk mortality due to pond drying (Babbitt et al. 2003; Skelly 1996). Additionally, larger size and shorter time to metamorphosis allows individuals to reach maturity sooner and have greater lifetime fitness (Semlitsch et al. 1988; Smith 1987). Although, breeding adults favored open canopy ponds, females oviposited fewer eggs at high isolation in the clearcut treatments, but this same pattern did not occur in the partial cut or control treatments. This treatment interaction effect suggests that treefrogs were less willing to breed in pools farther into clearcuts. Additionally, fewer eggs were found per oviposition event in high isolation clearcut pools in experiment one. Differences in the number of eggs per oviposition event can be explained by multiple
21
females ovipositing in preferred pools on a favorable breeding night (i.e. high humidity, wet leaf litter, warm air temperatures, etc) or it may be due to individual females laying more eggs per clutch in preferred pools. Distance from the pond and distance from the treatment edge were confounded in experiment one. However, the distance from the pond is unlikely to cause the decrease in the number of eggs per oviposition event observed in the clearcuts because the same trend was not observed in the control or partial cut treatments. Experiment one indicated that the location of the open canopy breeding sites in relation to mature forest could be important for gray treefrogs and the importance of this relationship was confirmed by the second experiment. The preference for breeding sites in clearcuts in close proximity to forested habitat indicates that females from the forested treatments likely moved into the clearcuts to breed. Given that we did not record individual treefrog movements, greater use of clearcut edge sites may be due to treefrogs residing in the clearcuts. But, because more eggs in clearcuts were oviposited near forest edges than in the pools further into the clearcuts, this latter explanation is unlikely. Johnson (2005) found that gray treefrogs use large trees for foraging and tree cavities for diurnal refuges and are known to make single-night breeding migrations longer than 100 m in a forested habitat (Johnson & Semlitsch In review). Females are capable of moving from a refuge in a forested treatment to pools in the clearcuts, and although we observed some frogs in clearcuts, we believe it is unlikely they can subsist for prolonged periods in clearcut habitats due to risk of desiccation (Johnson et al. In review; Perison et al. 1997). Like females gray treefrogs, males appear to prefer the open canopy breeding sites of the clearcut and clearcut edge treatments. However, neither the number of males
22
nor the frequency of male captures differed between the clearcut and clearcut-edge treatments. This indicates that males are likely not limited by the 50 m isolation distance, even though the risk of desiccation for adult anurans is significantly greater in clearcuts than in mature forests (Rittenhouse unpublished data). Males may be more willing risk desiccation to use the 50 m breeding sites in the clearcut to reduce competition for mating opportunities at the clearcut edge sites (Fellers 1979; Wells 1977). Females likely had similar opportunities for mating at either clearcut site, suggesting that females were primarily responsible for selecting the breeding sites closer to the forest edge instead of those 50 m into the clearcut. Future studies should examine if there are difference in the size or acoustic attractiveness of males using breeding sites different distances into a clearcut. The difference in male and female breeding site selection has implications for anuran surveys, which often focus on calling males at the breeding site because they are more conspicuous (e.g. Heyer et al. 1994; Royle 2004; Stevens et al. 2002). Researchers should use caution when drawing conclusions about habitat use from observations of only one sex. Ultimately, we found that clearcutting can disrupt the connectivity between breeding and non-breeding habitats for gray treefrogs. Breeding was reduced at sites only 50 m from the nearest forest indicating that even relatively small clearcuts can create resistance to migrating females. Altered habitat between essential habitats reduces landscape complementation and could be potentially detrimental to populations where alternative breeding sites are not available. Although clearcuts are only a temporary form of habitat alteration, most species of anurans have a maximum longevity of much less than 15 years (Lannoo 2005). Specifically, the gray treefrog is not known to live more
23
than four years in natural populations (Roble 1985). If breeding ponds are located in clearcuts greater than 50 m from a forest it is possible that the local population would substantially decline due to reduced recruitment over five years. Therefore, future studies should examine this isolation effect for other species with short population turnover times. Although timber harvest that opens the canopy over ponds may be beneficial for some species, it is essential to have mature forest nearby for forest dependent species (Johnson 2005). Not all species benefit from open canopy ponds, and some ponds should be maintained within a closed-canopy forest for species such as woodfrogs (Skelly et al. 2002). Additionally, although the lack of difference in breeding site use between the two clearcut treatments in experiment one indicates that CWD does not influence breeding site use, CWD could still affect the vital rates of individuals via desiccation or altered foraging, especially for males that spend multiple nights calling around breeding sites in clearcuts. In addition to examining the effects of CWD on adult vital rates, future studies should examine the performance of eggs and larvae in recent clearcuts and mature forest ponds. Information on egg and larval responses will help determine the mechanisms controlling population level responses to clearcutting and adult breeding site selection in a fragmented landscape. Testing the fate of emigrating juveniles from ponds in clearcuts at different distances from mature forests will help toward understanding the total effects of clearcutting on landscape complementation. Finally, while some amphibian populations can be impacted by forest alteration for decades (e.g. Ash 1997; Karracker & Welsh 2006), others may respond more quickly to forest regeneration (Marsh et al. 2004).
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It will be important to determine how long the clearcuts function as a barrier to female breeding site use and how selection and habitat resistance change with succession.
ACKNOWLEDGEMENTS We would like to thank C. Conner, J. Sias, and D. Sattman, and for their help in the field, and to M. Ellersieck, J. Toms, and J. Crawford for discussions on experimental design and analysis. Appreciation is extended to L. Hocking, J. Crawford, C. Conner, B. Rothermel, T. Rittenhouse, J. Faaborg, and two anonymous reviewers for comments on earlier drafts of this manuscript. This project would not have been possible without the support of G. Raeker and the Missouri Department of Conservation. Financial support was provided by the National Science Foundation (DEB-0239943). D. J. Hocking was supported by a Life Sciences Fellowship through the University of Missouri.
LITERATURE CITED Ash, A. N. 1997. Disappearance and return of plethodontid salamanders to clearcut plots in the southern Blue Ridge Mountains. Conservation Biology 11:983-989. Babbitt, K. J., M. J. Baber, and T. L. Tarr. 2003. Patterns of larval amphibian distribution along a wetland hydroperiod gradient. Canadian Journal of Zoology 81:15391552. Berven, K. A. 1990. Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599-1608. Brown, J. H., and A. Kodric-Brown. 1977. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445-449.
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Caldwell, J. P., J. H. Thorp, and T. O. Jervey. 1980. Predator-prey relationships among larval dragonflies, salamanders, and frogs. Oecologia 46:285-289. Chan-McLeod, A. C. A. 2003. Factors affecting the permeability of clearcuts to redlegged frogs. Journal of Wildlife Management 67:663-671. Cushman, S. A. 2006. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128:231-240. deMaynadier, P. G., and M. L. Hunter, Jr. 1995. The relationship between forest management and amphibian ecology: a review of the North American literature. Environmental Review 3:230–261. Dunning, J. B., B. J. Danielson, and H. R. Pulliam. 1992. Ecological processes that affect populations in complex landscapes. Oikos 65:169-175. Fauth, J. E. 1990. Interactive effects of predators and early larval dynamics of the treefrog Hyla chrysoscelis. Ecology 71:1609-1616. Fellers, G. M. 1979. Mate selection in the gray treefrog, Hyla versicolor. Copeia 1979:286-290. Gibbs, J. P. 1998. Distribution of woodland amphibians along a forest fragmentation gradient. Landscape Ecology 13:263-268. Gill, D. E. 1978. The metapopulation ecology of the red-spotted newt, Notophthalmus viridescens (Rafinesque). Ecological Monographs 48:145-166. Gunzburger, M. S., and J. Travis. 2004. Evaluating predation pressure on green treefrog larvae across a habitat gradient. Oecologia 140:422-429.
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Halverson, M. A., D. K. Skelly, J. M. Kiesecker, and L. K. Freidenburg. 2003. Forest mediated light regime linked to amphibian distribution and performance. Oecologia 134:360-364. Herbeck, L. A., and D. R. Larsen. 1999. Plethodontid salamander response to silvicultural practices in Missouri Ozark forests. Conservation Biology 13:623-632. Heyer, W. R., M. A. Donnelly, R. W. McDiarmid, L.-A. C. Hayek, and M. S. Foster, editors. 1994. Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington. Johnson, J. R. 2005. Multi-scale investigations of gray treefrog movements, patterns of migration, dispersal, and gene flow. Page 246. Division of Biological Sciences. University of Missouri, Columbia. Johnson, J. R., R. D. Mahan, and R. D. Semlitsch. In review. Terrestrial microhabitat use by gray treefrogs (Hyla versicolor) in oak-hickory forests. Forest Ecology and Management. Johnson, J. R., and R. D. Semlitsch. 2003. Defining core habitat of local populations of the gray treefrog (Hyla versicolor) based on choice of oviposition site. Oecologia 137:205-210. Johnson, J. R., and R. D. Semlitsch. In review. The effect of matrix habitat and inter-pond distance on amphibian movements in an experimental metapopulation. Landscape Ecology. Karracker, N. E., and H. H. Welsh, Jr. 2006. Long-term impacts of even-aged timber management on abundance and body condition of terrestrial amphibians in Northwestern California. Biological Conservation 131:132-140.
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Lamoureux, V. S., and D. M. Madison. 1999. Overwintering habitats of radio-implanted green frogs, Rana clamitans. Journal of Herpetology 33:430-435. Lamoureux, V. S., J. C. Maerz, and D. M. Madison. 2002. Premigratory autumn foraging forays in the green frog, Rana clamitans. Journal of Herpetology 36:245-254. Lannoo, M. J., editor. 2005. Amphibian Declines: The Conservation Status of Unites States Species. University of California Press, Berkeley. Marsh, D. M., and B. J. Borrell. 2001. Flexible oviposition strategies in tungara frogs and their implications for tadpole spatial distributions. Oikos 93:101-109. Marsh, D. M., K. A. Thakur, K. Bulka, C., and L. B. Clarke. 2004. Dispersal and colonization through open fields by a terrestrial, woodland salamander. Ecology 85:3396-3405. Mazerolle, M. J., and A. Desrochers. 2005. Landscape resistance to frog movements. Canadian Journal of Zoology 83:455-464. McCollum, S. A., and J. D. Leimberger. 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615-621. Perison, D., J. Phelps, C. Pavel, and R. Kellison. 1997. The effects of timber harvest in a South Carolina blackwater bottomland. Forest Ecology and Management 90:171185. Pope, S. E., L. Fahrig, and H. G. Merriam. 2000. Landscape complementation and metapopulation effects on leopard frog populations. Ecology 81:2498-2508. Resetarits, W. J., Jr., and H. M. Wilbur. 1989. Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220-228.
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Rittenhouse, T. A. G., and R. D. Semlitsch. 2006. Grasslands as movement barriers for a fores-associated salamander: migration behavior of adult and juvenile salamanders at a distinct habitat edge. Biological Conservation 131:14-22. Roble, S. M. 1985. A study of the reproductive and population ecology of two hylid frogs in northeastern Kansas. Page 242. Department of Systematics and Ecology. University of Kansas. Rothermel, B. B. 2004. Migratory success of juveniles: a potential constraint on connectivity for pond-breeding amphibians. Ecological Applications 14:15351546. Rothermel, B. B., and R. D. Semlitsch. 2002. An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conservation Biology 16:1324-1332. Royle, J. A. 2004. Modeling abundance index data from anuran calling surveys. Conservation Biology 18:1378-1385. Schiesari, L. 2006. Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biology 51:412-423. Semlitsch, R. D. 1990. Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology 68:1027-1030. Semlitsch, R. D. 1998. Biological delineation of terrestrial buffer zones for pondbreeding salamanders. Conservation Biology 12:1113-1119. Semlitsch, R. D., editor. 2003. Amphibian Conservation. Smithsonian Institute Press, Washington D.C.
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Semlitsch, R. D., and J. W. Gibbons. 1988. Fish predation in size-structured populations of treefrog tadpoles. Oecologia 75:321-326. Semlitsch, R. D., T. J. Ryan, K. Hamed, M. Chatfield, B. Drehman, N. Pekarek, M. Spath, and A. Watland. 2006. Salamander abundance along road edges and within abandoned logging roads in Appalachian forests. Conservation Biology. Semlitsch, R. D., D. E. Scott, and J. H. K. Pechmann. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. Skelly, D. K. 1996. Pond drying, predators, and the distribution of Pseudacris tadpoles. Copeia 1996:559-605. Skelly, D. K., L. K. Freidenburg, and J. M. Kiesecker. 2002. Forest canopy and the performance of larval amphibians. Ecology 83:983-992. Smith, D. C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344-350. Spieler, M., and K. E. Linsenmair. 1997. Choice of optimal oviposition sites by Hoplobatrachus occipitalis (Anura: Ranidae) in an unpredictable and patchy environment. Oecologia 109:184-199. Stevens, C. E., A. W. Diamond, and T. Shane Gabor. 2002. Anuran call surveys on small wetlands in Prince Edward Island, Canada restored by dredging of sediments. Wetlands 22:90-99. Todd, B. D., and B. B. Rothermel. 2006. Assessing quality of clearcut habitats for amphibians: effects on abundances versus vital rates in the southern toad (Bufo terrestris). Biological Conservation 133:178-185.
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Wells, K. D. 1977. The social behaviour of anuran amphibians. Animal Behaviour 25:666-693. Werner, E. E., and K. S. Glennemeier. 1999. Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999:1-12.
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TABLE 2.1. Analysis of variance (ANOVA) of the number of eggs oviposited per pool in a split-block design. The main plots (forest treatment) and subplots (isolation) are arranged in strips and therefore each has their own error term for the F-test. Treatments are also arranged in three blocks (site).
Source
df
MS
F-value
P-value
Site
2
315.15
0.8100
0.4673
Forest treatment
3
6135.48
8.4700
0.0141
Site x treatment (treatment error)
6
724.80
1.8700
0.1686
Isolation
2
466.90
12.3500
0.0194
Site x isolation (isolation error)
4
37.81
0.1000
0.9813
Treatment x isolation
6
1078.75
2.7800
0.0624
Error
12
388.54
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FIG. 2.1. A) The aerial photograph of one study site in the Daniel Boone Conservation Area, Warren County, MO shows the four forest management treatments with a pond at the center. The smaller circles show the placement of the artificial pools in each habitat. B) The expanded view diagrams the arrangement and distances of the low, medium, and high isolation pools within a forest treatment.
33
34
FIG. 2.2. Interaction diagrams of the A) mean number of eggs (± 1 SE) laid in each forest and isolation treatment combination and B) mean number of eggs per oviposition event (± 1 SE) in each treatment combination (forest treatment x isolation level).
35
A. Control
Mean number of eggs per pool
10000
Partial
9000
High-CWD
8000
Low-CWD
7000 6000 5000 4000 3000 2000 1000 0 Low
Medium
High
Isolation level
B.
Mean number of eggs per oviposition event
2500
2000
1500
1000
500
0 Low
Medium
Isolation level
36
High
FIG. 2.3. Mean number of A) oviposition events and B) male captures per survey night in each of the four forest treatments. Bars represent means + SE.
37
A.
8
Mean number of oviposition events
7
6
5
4
3
2
1
0 Clearcut
Clearcut Edge
Forest Edge
Forest
B.
Mean number of males captured per night
2.50
2.00
1.50
1.00
0.50
0.00
Clearcuts
Clearcut Edge
Forest Edge
Forest treatments
38
Forest
CHAPTER 3
EFFECTS OF EXPERIMENTAL CLEARCUT LOGGING ON GRAY TREEFROG (HYLA VERSICOLOR) TADPOLE PERFORMANCE
Daniel J. Hocking and Raymond D. Semlitsch
ABSTRACT Clearcutting detrimentally affects the populations of many amphibian species. Gray treefrogs, however, have shown a preference for breeding sites located in clearcuts near forested habitat. To test the implications of this preference, we examined gray treefrog tadpole performance in cattle tanks along a gradient from clearcut to forest habitat. We replicated this design at three experimental clearcut sites. Tadpole performance was measured as length of the larvae period, size at metamorphosis, and survival. We also examined the influence of temperature, periphyton productivity, and invertebrate predator abundances on tadpole performance. Time to metamorphosis was shorter in the clearcuts, but those metamorphs tended to be smaller than metamorphs in the forest tanks. Survival was also greater in the clearcuts than in the forest treatments. There was no strong edge effect on either side of the forest-clearcut ecotone. Higher temperatures and greater periphyton productivity in the clearcuts primarily contributed to tadpole performance while invertebrate predators did not appear to influence
39
performance. Although clearcuts benefited tadpoles through higher survival and shorter larval periods, smaller sized metamorphs in clearcuts may reduce post-metamorphic survival and fecundity. Additionally, smaller metamorphs in the clearcuts may have reduced dispersal success. Small scale disturbances such as clearcutting around ephemeral ponds may benefit gray treefrogs, but large clearcuts that leave ponds isolated from forested habitat should be avoided.
INTRODUCTION Habitat loss and alteration are among the greatest threats to biodiversity and are a major cause of amphibian declines (Lannoo 2005; Semlitsch 2003; Wilcove et al. 1986). With the rapidly increasing human population, the need for natural resources including timber is also increasing. The need for timber products necessitates logging practices that often result in reduced amphibian diversity and abundance (Cushman 2006; reviewed in deMaynadier & Hunter 1995). Despite the negative impacts forestry on many amphibians, the mechanisms creating the observed patterns remain poorly understood (Cushman 2006). Most studies focus on terrestrial species and the terrestrial stage of pond-breeding species because they are exposed to hotter, drier conditions that can cause mortality or decreased growth and development (Ash 1995; Chazal & Niewiarowski 1998; Karracker & Welsh 2006; Todd & Rothermel 2006). Few have investigated the potential impacts on the aquatic larval stage of amphibians (but see Wahbe & Bunnell 2001). However, both the terrestrial and aquatic stages of pond-breeding amphibians are important in population dynamics and can be influenced by timber harvest.
40
The larvae of pond-breeding amphibians are confined to the pond until metamorphosis, subjecting larvae to the changing aquatic conditions. The larval stage is dedicated to growth and evolved to exploit transient aquatic resources (Wilbur 1980; Wilbur & Collins 1973). Species differ in the length of their larval stage depending on the predictability of the aquatic resources, particularly the hydroperiod (Alford 1999; Alford & Harris 1988; Ryan & Winne 2001; Skelly 2001). There is also individual variability in the length of the larval period. Depending on both biotic and abiotic conditions, individuals may alter the length of their larval period as well as their size at metamorphosis. The time and size at metamorphosis are directly related to fitness as individuals that metamorphose earlier and at a larger size reach maturity sooner and have larger clutch sizes (Berven 1990; Semlitsch et al. 1988; Smith 1987). Clearcutting around ephemeral ponds opens the forest canopy, which can alter the resources available for amphibian larvae. Tadpoles grow faster and have greater survival in open canopy ponds compared with closed canopy ponds (Skelly et al. 2002; Werner & Glennemeier 1999). Additionally, Schiesari (2006) found that higher temperatures and food quality in open canopy ponds affected tadpole performance and not dissolved oxygen (DO) which also varied with canopy cover. Therefore, clearcutting around ponds may be expected to improve the habitat quality for the aquatic stage of many anuran species. However, the open canopy created by clearcutting can also alter the predator community in the pond. Anisopteran (Odonata) larvae are known to prey upon tadpoles (Petranka & Hayes 1998; Semlitsch 1990; Skelly & Werner 1990), and many anisopteran species prefer to breed in open canopy ponds resulting in higher predator densities than
41
closed canopy ponds (Corbet 2004; McCauley 2005). Predators can have direct effects on tadpole survival but can also have indirect impacts including costly behavioral and morphological responses (Relyea 2002a; Relyea & Hoverman 2003; Skelly 1992; Skelly & Werner 1990). Behaviorally, tadpoles may reduce foraging activity in response to these predators, resulting in reduced growth and subsequent size-specific mortality (Lawler 1989; Semlitsch 1990). Morphological responses to predators include deeper, more muscular tails with increased coloration. These morphological antipredator responses have fitness costs that can persist after metamorphosis (McCollum & Leimberger 1997; McCollum & Van Buskirk 1996; Relyea 2003). Despite defensive fitness costs, the tadpoles that avoid predation can potentially benefit through reduced competition (Alford 1999; Fauth 1990; Relyea 2002b). Gray treefrogs (Hyla versicolor) often use small ephemeral ponds that may be logged around with little or no legal protection (Semlitsch & Bodie 1998). In a previous study, we found that gray treefrogs prefer to breed in ponds in recent clearcuts rather than in forested ponds or ponds in clearcuts isolated long distances from forest edges (Hocking and Semlitsch in review). We evaluate the implications of this oviposition selection by examining gray treefrog tadpole performance along a clearcut-forest gradient. Additionally, we examine how biotic and abiotic factors influence tadpole performance. We expect the higher temperature and periphyton productivity in clearcuts will benefit tadpoles while invertebrate predator abundance will reduce tadpole survival. Tadpole performance in aquatic habitats can significantly affect adult fitness and must be considered when evaluating the complete effects of clearcutting terrestrial habitats.
42
METHODS Study Design We conducted our study in the Daniel Boone Conservation Area (DBCA; 1425 ha) in Warren County, Missouri. Replicate 2.3 ha clearcuts were established in 2004 (Hocking and Semlitsch in review). We set up cattle tanks in clearcuts and control forests at three replicate sites. We placed three replicate cattle tanks in the clearcuts at 10 m and 50 m from the nearest forest-edge, and in the forest 10 m and 50 m from the same edge. Tanks at these locations represent four habitat treatments: clearcut, clearcut-edge, forestedge, and forest treatments. Three tanks were used as subsamples in each treatment at each replicate site (36 total tanks). Tanks were each filled with 570 l of tap water in February 2006. After allowing one week to dechloronate, we added 1 kg of dry deciduous leaf litter to each. We added zooplankton inoculum and one liter pond water strained through a 100 µm net the first week of April and again the first week of May. Tank covers made of fiberglass window screen prevented unwanted oviposition by treefrogs. A minimum of three days per week, we removed the covers from the tanks during the day to allow invertebrate colonization and natural solar radiation. On 29 May, we collected 15 pairs of gray treefrogs from five ponds in the DBCA. Each pair was placed in a plastic container with water and allowed to oviposit overnight. We removed the pairs the following morning and checked the eggs daily; removing any dead eggs. On 7 June, we pooled all clutches and haphazardly selected tadpoles (Gosner
43
stage 25) and added 100 to each of 36 distribution containers. These 36 distribution containers were then randomly assigned and added to the cattle tanks.
Data collection Tadpoles were observed daily for forelimb emergence, at which point they were removed and kept in plastic containers until the completion of metamorphosis (tail stub < 2 mm). Upon metamorphosis, we weighed tadpoles to the nearest 0.001 g using an electronic balance. We monitored the tank for 60 days following the addition of tadpoles. Afterwards, we removed all leaf litter from the tanks and recorded the number of surviving tadpoles and number of anisoptera larvae. Percent survival was calculated by adding the number of remaining tadpoles plus the number of metamorphs from each tank, dividing by the initial number of tadpoles (100) and multiplying by 100%. Our measures of tadpole performance were length of the larval period, size at metamorphosis, and survival. To examine the influence of invertebrate predators, we swept each tank with a dipnet (3 mm mesh) immediately prior to adding the tadpoles. The total number of dyticid beetle larvae and adults were quantified; however, no anisoptera dragonfly larvae were found. Additionally, we measured temperature, DO, and pH in each tank the week tadpoles were added, after three weeks to correspond with the start of metamorphosis, and at the end of the experiment. Measurements were taken 10 cm below the surface of the water. We also sampled periphyton productivity at the same three times. Three weeks prior to the start of the experiment, we hung glass slides (25 mm x 75 mm) 10 cm below the surface of the water. Three slides were hung on the south facing wall of each
44
tank. To sample the periphyton, we randomly selected one slide from each tank and scrapped any periphyton off with a razor blade and cotton swab. We placed the cotton swab in buffered acetone and kept the samples in a refrigerator for 24 hours. Samples were allowed to come to room temperature prior to chlorophyll analysis. We determined chlorophyll a concentration following EPA Method 445.0 (Arar & Collins 1992) using a Turner Designs Model 10-AU digital fluorometer.
Statistical analyses We used the tadpole survival, mean number of days and mean size at metamorphosis for each tank as our dependent variables for measuring tadpole performance. The mean of each cluster of tanks in a treatment was used for statistical analysis, because habitat treatment is our experimental unit. The individual tadpoles in tanks and the tanks were subsamples of each experimental unit. Therefore, we had four treatments replicated at three sites for a total of 12 experimental units. We tested the effect of treatment on our dependent variables using analysis of variance at a significance level of α = 0.05. Pairwise comparisons were examined using Fisher’s Least Significant Difference (LSD). Predator densities did not meet the assumptions required for ANOVA, and replication was low for using Kruskal-Wallis test. Therefore, we used the Goodnessof-Fit G-statistic to test whether invertebrate predator colonization was random among treatments. We used linear regression analysis to help understand the factors that influenced tadpole performance in the treatments. We developed 9 a priori models to determine the relative importance of variables predicted to impact tadpole growth, development, and
45
survival (Table 3.1). We used the mean temperature, DO, and pH from the three sampling periods for analysis. Initial periphyton productivity was used in our models rather than mean productivity. Tadpoles consumed the majority of periphyton in the first three weeks in all treatments (Fig. 3.1), indicating that the difference in initial periphyton should have the greatest influence on the tadpoles. Additionally, the final periphyton levels would be dependent upon the timing of metamorphosis and tadpole survival as well as the proportion of edible periphyton. We also used dyticid abundance at the start of the experiment in our models because predators present early in tadpole development should have a greater impact on tadpole performance (Fauth 1990; Relyea 2002b, 2003). Anisopteran abundance at the end of the study was used for analysis because no anisopteran larvae were found initially. The 9 models were compared using Akaike’s Information Criterion for small sample sizes (AICc). This model selection technique is based on the Kullback-Leibler distance and compares how well models fit the data while balancing the number of terms in the model (model complexity). Models are ranked by AICc values and Akaike’s weight (w), with the lowest AICc and highest weights representing the models that best approximate the data. We performed all statistical tests using SAS v9.1 (SAS Institute), except the Goodness-of-Fit test which we calculated using Microsoft Excel 2003 (Microsoft Corporation). Two tanks did not hold water for the duration of the study and were not used for analysis. During the study, adult treefrogs or eggs were found under the net covers in three additional tanks and were also excluded from the study. One tank in a clearcut and one tank in a clearcut-edge treatment developed a thick unknown algae that covered the leave litter and walls of the tanks. These two tanks had 5 and 40 % survival, respectively,
46
while the rest of the tanks had a mean percent survival of 78.2 (1.7 SE). These two tanks were therefore excluded from all statistical analyses. Excluding these tanks did not alter the total replication, as at least one tank remained in each replicate treatment (29 total tanks). RESULTS In the remaining tanks (n=29), mean time to metamorphosis ranged from 26.3 to 46.8 days. Mean mass at metamorphosis ranged from 0.193 to 0.642 g, while percent survival ranged from 5 to 93 %. Time to metamorphosis was significantly shorter in the clearcut and clearcut-edge treatments than in the forest-edge and forest treatments (Table 3.2; Fig. 3.2a). Fisher’s LSD multiple comparisons test revealed no difference between the clearcut and clearcut-edge treatments or between the forest and forest-edge treatments. There was no significant difference in size at metamorphosis among treatments. However, comparing the two clearcut treatments to the two forest treatments revealed a significant difference (Table 3.2). Metamorphs were larger in the forest treatments than in the clearcut treatments (Fig. 3.2). There was a marginally significant difference in survival among the treatments (Table 3.2). However, we believe that these results are biologically significant. In a large-scale experiment such as this, limited replication reduces the power to detect differences among treatments. There was a significant difference when the clearcut and clearcut-edge treatments were contrasted against the forest and forest-edge treatments (Table 3.2). Neither dyticid beetle larvae (χ20.05,3 = 106.5, P < 0.0001) nor dragonfly larvae (χ20.05,3 = 569.9, P < 0.0001) were found randomly distributed among the habitat treatments. The mean number of beetles per tank was 8.4, 11.6, 0.7, and 0 for the
47
clearcut, clearcut-edge, forest-edge, and forest treatments, respectively. Although zero dragonfly larvae were present at the start of the experiment, means of 42.3, 65.4, 0.7, and 0 were found in the clearcut, clearcut-edge, forest-edge, and forest treatments, respectively, at the end of the study. Despite far greater predator abundances in the two clearcut treatments than in the two forest treatments, there was no apparent influence on tadpole performance. Analysis of the multiple linear regression using AIC revealed the best models predicting time to metamorphosis were Temperature and Temperature-Chlorophyll, accounting for 48.5 and 51.3 percent of the variation, respectively (Table 3.3). The other models did not perform as well and were unlikely to be the best predictors of time to metamorphosis. The same two models were also the best predictors of size at metamorphosis and survival to metamorphosis (Table 3.3). However, the support for these two models was not clear for either size or survival. Models predicting size that included beetle and dragonfly predators had low to moderate support as indicated by ΔAICc and Akaike’s weight (Table 3.3). However, none of the models accounted for a large portion of the variation (Table 3.3; R2). Temperature was the best predictor of survival to metamorphosis, but models including chlorophyll, water quality, and predators had moderate support using AICc analysis. As with size, none of the models accounted for a large portion of the variation in survival (Table 3.3).
DISCUSSION Tadpoles in the two clearcut treatments metamorphosed in an average of 6.9 fewer days than in the two forest treatments. Even small differences in time to
48
metamorphosis can result in large differences in recruitment, especially in rapidly drying ephemeral ponds (Pechmann et al. 1989; Ryan & Winne 2001). Gray treefrog tadpoles are moderately weak competitors (Morin 1987; Wilbur 1987) and are susceptible to predators that require long hydroperiods (Morin 1983; Relyea 2003; Semlitsch 1990) making the use of ephemeral ponds advantageous for this species. With an extended summer breeding season (late April to July), gray treefrog tadpoles are subjected to ponds drying in the heat of the summer. Small closed canopy ponds can also have shorter hydroperiods due to higher evapotranspiration (Brooks 2004). The ability to metamorphose quickly from ephemeral ponds located in clearcuts likely increases survival. Despite emerging earlier, tadpoles in clearcuts tended to be smaller in size at metamorphosis. Although the comparison among all habitat treatments was not significant, the comparison between the two clearcut and two forest treatments was significant (Table 2). The metamorphs from the clearcut treatments were 15.5% smaller than metamorphs from the forested treatments. Smaller size at metamorphosis can reduce fitness through delayed reproductive maturity and reduced fecundity of females (Semlitsch et al. 1988; Smith 1987). Additionally, smaller body size increases the surface area to volume ratio and may make small individuals more susceptible to desiccation. Smaller size at metamorphosis significantly reduces post-metamorphic survival and dispersal success (Chelgren et al. 2006). Smaller size could be especially problematic in clearcut habitats where higher temperatures and winds increase the likelihood of desiccation during dispersal (Chan-McLeod 2003; Keenan & Kimmins 1993; Wahbe et al. 2004). Dispersing metamorphs have been shown to have lower
49
success in old fields than in forested habitat (Rothermel & Semlitsch 2002). Dispersal success would also be lower for metamorphs leaving ponds farther from forested edges (Rothermel 2004; Rothermel & Semlitsch 2002). Although post-metamorphosis survival is known to be lower in old fields (Rothermel 2004), survival of tadpoles to metamorphosis was 8.5 % greater in ponds in the clearcut treatments than in the forest treatments. Thus, higher larval survival and shorter time to metamorphosis may offset any potential consequences of smaller size at metamorphosis. However in a previous study, we found that gray treefrogs preferred to oviposit in ponds along a clearcut-edge but also bred in forest, forest-edge, and clearcut ponds (Hocking and Semlitsch in review). This variability in breeding site selection may serve as a form of bet hedging. Although breeding in open canopy ponds might be advantageous in some circumstances because of higher productivity, using a variety of breeding habitats along a canopy or disturbance gradient could ensure some recruitment in at least one habitat each year, depending on predation, competition and hydroperiod. Having some annual recruitment may benefit short-lived species that breed in highly variable aquatic habitats, such as the gray treefrog which lives less than five years (Johnson 2005; Roble 1985; Wright & Wright 1995), whereas long-lived species like mole salamanders can persist even after several years of recruitment failure (Semlitsch et al. 1996). In the second part of our study, we examined the biotic and abiotic factors that contributed to tadpole performance in the different treatments. We found that higher temperatures alone and in combination with increased periphyton productivity in clearcuts contributed most to tadpole performance. This lends strong support to previous
50
research indicating that temperature and food quality are the most important factors for tadpoles along a gradient of canopy cover (Schiesari 2006; Skelly et al. 2002; Werner & Glennemeier 1999). In contrast to our expectations, predatory invertebrates had no detectable influence on any aspect of tadpole performance. Dyticid beetle larvae and adults prey upon gray treefrog tadpoles, as do anisoptera dragonfly larvae. In cattle tanks, anisopteran larvae can reduce tadpole survival by 50 % more than in controls (Relyea 2002b). McCollum and van Buskirk (1996) found that anisopteran larvae in the genus Anax (family: Aeshnidae) reduced tadpole survival more than Pantala (family: Libellulidae). Anax oviposit into aquatic macrophytes and therefore were not present in our tanks. Instead, only anisopteran larvae of the family Libellulidae were present. Gray treefrogs have been shown to exhibit behavioral and morphological antipredator defenses in response to anisoptera (Relyea 2003; Relyea & Hoverman 2003). These defenses may be sufficient to prevent predation by some species of dyticids and anisoptera. More research is needed to determine the impact of different anisoptera species on tadpoles and the generality of antipredator responses in gray treefrogs. In addition to tadpole behavioral and morphological defenses, breeding site selection and breeding phenology may reduce exposure to many predators. Breeding in ephemeral ponds prevents exposure to predators that accumulate in more permanent ponds, including species of anisoptera dragonflies, such as Aeshnidae that overwinter as larvae and require long hydroperiods. Additionally, breeding during the late spring to early summer allows gray treefrog tadpoles to avoid the highest densities of late instar anisoptera larvae. Many anisoptera metamorphose in the early summer and adults breed
51
synchronously or slightly after gray treefrogs (McCollum and van Buskirk 1996, Hocking unpublished data). Therefore, tadpoles may be able to complete their larval period before dragonfly larvae get large enough to inflict significant mortality. Gray treefrogs are known to avoid ovipositing in cattle tanks containing fish and predatory newts but show no avoidance of anisoptera larvae (Resetarits & Wilbur 1989). The lack of avoidance coupled with our data showing little or no effect suggests that dyticids and anisoptera larvae may not strongly impact tadpole performance in many habitats. Gray treefrog tadpoles appear to benefit from clearcutting and likely from other small scale disturbances that open the canopy over breeding ponds. This benefit may be limited to ephemeral ponds where predators are not able to accumulate. The advantages may also be offset by reduced juvenile survival if ponds are isolated some distance from forest habitat, but this remains to be tested. It is essential to consider the impacts of logging on amphibian aquatic larvae but also terrestrial juvenile stages as the latter is predicted to have the greatest influence on population regulation (Biek et al. 2002; Vonesh & De la Cruz 2002). Future studies should also examine competitive and predatory interactions among amphibians, in addition to predatory invertebrates, that might be altered through clearcutting. Finally, it will be important to examine tadpole performance during forest succession to better understand deterministic change on species persistence and its relationship to restoration efforts.
ACKNOWLEDGEMENTS We would like to thank J. Crawford, B. Peterman, and B. Williams for help moving tanks. We also appreciate the field work provided by E. Wengert, B. Scheffers,
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C. Conner, and A. Barlows. This manuscript has benefited from the thoughtful comments provided by L. Hocking. We thank G. Raeker and the Missouri Department of Conservation for permission and help with the site preparation. Financial support was provided by the National Science Foundation (DEB-0239943). D. J. Hocking was supported by a Life Sciences Fellowship and TWA Scholarship through the University of Missouri.
LITERATURE CITED Alford, R. A. 1999. Ecology: resource use, competition, and predation. Pages 189-214 in R. W. McDiarmid, and R. Altig, editors. Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago. Alford, R. A., and R. N. Harris. 1988. Effects of larval growth history on anuran metamorphosis. The American Naturalist 131:91-106. Arar, E. J., and G. B. Collins. 1992. Method 445.0: In vitro determination of chlorophyll a and Pheophytin a in marine and freshwatrer phytoplankton by fluorescence in Methods for the Determination of Chemical Substances in Marine and Estuarine Environmental Samples, EPA/600/R-92/121. Ash, A. N. 1995. Effects of clear-cutting on litter parameters in the southern Blue Ridge Mountains. Castanea 60:89-97. Berven, K. A. 1990. Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599-1608.
53
Biek, R., W. C. Funk, B. A. Maxell, and L. S. Mills. 2002. What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conservation Biology 16:728-734. Brooks, R. T. 2004. Weather-related effects on woodland vernal pool hydrology and hydroperiod. Wetlands 24:104-114. Chan-McLeod, A. C. A. 2003. Factors affecting the permeability of clearcuts to redlegged frogs. Journal of Wildlife Management 67:663-671. Chazal, A. C., and P. H. Niewiarowski. 1998. Responses of mole salamanders to clearcutting: using field experiments in forest management. Ecological Applications 8:1133-1143. Chelgren, N. D., D. K. Rosenberg, S. S. Heppell, and A. I. Gitelman. 2006. Carryover aquatic effects on survival of metamorphic frogs during pond emigration. Ecological Applications 16:250-261. Corbet, P. S. 2004. Dragonflies: behavior and ecology of odonata. Cornell University Press, Ithaca. Cushman, S. A. 2006. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128:231-240. deMaynadier, P. G., and M. L. Hunter, Jr. 1995. The relationship between forest management and amphibian ecology: a review of the North American literature. Environmental Review 3:230–261. Fauth, J. E. 1990. Interactive effects of predators and early larval dynamics of the treefrog Hyla chrysoscelis. Ecology 71:1609-1616.
54
Johnson, J. R. 2005. Multi-scale investigations of gray treefrog movements, patterns of migration, dispersal, and gene flow. Page 246. Division of Biological Sciences. University of Missouri, Columbia. Karracker, N. E., and H. H. Welsh, Jr. 2006. Long-term impacts of even-aged timber management on abundance and body condition of terrestrial amphibians in Northwestern California. Biological Conservation 131:132-140. Keenan, R. J., and J. P. Kimmins. 1993. The ecological effects of clear-cutting. Environmental Review 1:121-144. Lannoo, M. J., editor. 2005. Amphibian Declines: The Conservation Status of Unites States Species. University of California Press, Berkeley. Lawler, S. P. 1989. Behavioural responses to predators and predation risk in four species of larval anurans. Animal Behaviour 38:1039-1047. McCauley, S. J. 2005. Species distributions in anisopteran odonates: effects of local and regional processes. Page 224. Ecology and Evolutionary Biology. University of Michigan, Ann Arbor. McCollum, S. A., and J. D. Leimberger. 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615-621. McCollum, S. A., and J. Van Buskirk. 1996. Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583-593. Morin, P. J. 1983. Predation, competition, and the composition of larval anuran guilds. Ecological Monographs 53:119-138.
55
Morin, P. J. 1987. Predation, breeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology 68:675-683. Pechmann, J. H. K., D. E. Scott, J. W. Gibbons, and R. D. Semlitsch. 1989. Influence of wetland hydroperiod on diversity and abundance of metamorphosing juvenile amphibians. Wetland Ecology and Management 1:3-11. Petranka, J. W., and L. Hayes. 1998. Chemically mediated avoidance of a predatory odonate (Anax junius) by American toad (Bufo americanus) and wood frog (Rana sylvatica) tadpoles. Behavioral Ecology and Sociobiology 42:263-271. Relyea, R. A. 2002a. Costs of phenotypic plasticity. The American Naturalist 159:272282. Relyea, R. A. 2002b. The many faces of predation: how induction, selection, and thinning combine to alter prey phenotypes. Ecology 93:1953-1964. Relyea, R. A. 2003. Predators come and predators go: the reversibility of predatorinduced traits. Ecology 84:1840-1848. Relyea, R. A., and J. T. Hoverman. 2003. The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596-604. Resetarits, W. J., Jr., and H. M. Wilbur. 1989. Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220-228. Roble, S. M. 1985. A study of the reproductive and population ecology of two hylid frogs in northeastern Kansas. Page 242. Department of Systematics and Ecology. University of Kansas.
56
Rothermel, B. B. 2004. Migratory success of juveniles: a potential constraint on connectivity for pond-breeding amphibians. Ecological Applications 14:15351546. Rothermel, B. B., and R. D. Semlitsch. 2002. An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conservation Biology 16:1324-1332. Ryan, T. J., and C. T. Winne. 2001. Effects of hydroperiod on metamorphosis in Rana sphenocephala. American Midland Naturalist 145:46-53. Schiesari, L. 2006. Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biology 51:412-423. Semlitsch, R. D. 1990. Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology 68:1027-1030. Semlitsch, R. D., editor. 2003. Amphibian Conservation. Smithsonian Institute Press, Washington D.C. Semlitsch, R. D., and J. R. Bodie. 1998. Are small, isolated wetlands expendable? Conservation Biology 12:1129-1133. Semlitsch, R. D., D. E. Scott, and J. H. K. Pechmann. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. Semlitsch, R. D., D. E. Scott, J. H. K. Pechmann, and J. W. Gibbons. 1996. Structure and dynamics of an amphibian community: evidence from a 16-year study of a natural pond. Pages 217-248 in M. L. Cody, and J. A. Smallwood, editors. Long-Term Studies of Vertebrate Communities. Academic Press, San Diego.
57
Skelly, D. K. 1992. Field evidence for a cost of behavioral antipredator response in a larval amphibian. Ecology 73:704-708. Skelly, D. K. 2001. Distributions of pond-breeding anurans: An overview of mechanisms. Israel Journal of Zoology 47:313-332. Skelly, D. K., L. K. Freidenburg, and J. M. Kiesecker. 2002. Forest canopy and the performance of larval amphibians. Ecology 83:983-992. Skelly, D. K., and E. E. Werner. 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313-2322. Smith, D. C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344-350. Todd, B. D., and B. B. Rothermel. 2006. Assessing quality of clearcut habitats for amphibians: effects on abundances versus vital rates in the southern toad (Bufo terrestris). Biological Conservation 133:178-185. Vonesh, J. R., and O. De la Cruz. 2002. Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325-333. Wahbe, T. R., and F. Bunnell. 2001. Preliminary observations on movements of tailed frog tadpoles (Ascaphus truei) in streams through harvested and natural forests. Northwest Science 75:77-83. Wahbe, T. R., F. Bunnell, and R. B. Bury. 2004. Terrestrial movements of juvenile and adult tailed frogs in relation to timber harvest in coastal British Columbia. Canadian Journal of Forest Resources 34:2455-2466.
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Werner, E. E., and K. S. Glennemeier. 1999. Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999:1-12. Wilbur, H. M. 1980. Complex life cycles. Annual Review of Ecology and Systematics 11:67-93. Wilbur, H. M. 1987. Regulation of structure in complex systems: experimental temporary pond communities. Ecology 68:1437-1452. Wilbur, H. M., and J. P. Collins. 1973. Ecological aspects of amphibian metamorphosis. Science 182:1305-1315. Wilcove, D. S., C. H. McLellan, and A. P. Dobson. 1986. Habitat fragmentation in the temperate zone. Pages 237-256 in M. E. Soule, editor. Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates Inc., Sunderland, MA. Wright, A. H., and A. A. Wright 1995. Handbook of Frogs and Toads of the United States and Canada. Comstock Publishing Associates, Ithaca.
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TABLE 3.1. Abbreviations and descriptions of the variables and 9 a priori models used to analyze tadpole performance. Model Variables
Description
1 Temperature (Temp)
Mean temperature (C)
2 Anisoptera
Abundance of anisoptera larvae and exuviae
3 Dyticid
Abundance of dyticid larvae and adults
4 Chlorophyll (Chloro)
Initial cholorphyll a (u g/m2)
5 Temp Chloro
Temperature and high quality food level
6 Temp DO pH
Water quality: temp, dissolved oxygen, pH
7 Temp Chloro Anisoptera Dyticid
Temperature, food, and predation
8 Anisoptera Dyticid
Invertebrate predator abundances
9 Temp DO pH Anisoptera Dyticid Chloro
Global model
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Table 3.2. Univariate analysis of variance testing the differences among habitat treatments for time to metamorphosis, mass at metamorphosis, and percent survival. We also used a contrast to compare clearcut and clearcut-edge treatments combined to the forest and forest-edge treatments combined. Source
df
SS
MS
F
P
3
142.91914
47.63971
5.18
0.0280
1
141.74622
141.74622
15.41
0.0044
Error
8
73.56805
9.19601
Total
11
216.48719
3
0.02301
0.00767
2.90
0.1015
1
0.01716
0.01716
6.49
0.0343
Error
8
0.02115
0.00264
Total
11
0.04416
3
318.72917
106.24306
3.77
0.0593
1
223.89120
223.89120
7.94
0.0226
Error
8
225.68519
28.21065
Total
11
544.41435
Time to Metamorphosis Treatment Clearcut vs Forest
Mass at Metamorphosis Treatment Clearcut vs Forest
Survival Treatment Clearctu vs Forest
61
TABLE 3.3. Linear regression models for survival, time and size at metamorphosis. Model fit was evaluated using Akaike’s Information Criterion for small sample sizes (AICc) and Akaike’s Weight (w). Model, Mi
a
R
2
AICc
Δi
L(Mi|Y)
wi b
Time to metamorphosis Temp
0.485
74.80
0.00
1.000
0.59
Temp Chloro
0.513
75.89
1.09
0.581
0.34
Temp DO pH
0.485
80.45
5.65
0.059
0.04
Temp Chloro Anisoptera Dyticid
0.525
81.33
6.53
0.038
0.02
Anisoptera Dyticid
0.276
87.42
12.61
0.002
0.00
Dyticid
0.178
88.38
13.58
0.001
0.00
Temp DO pH Anisoptera Dyticid Chloro
0.530
88.41
13.61
0.001
0.00
Anisoptera
0.143
89.60
14.80
0.001
0.00
Chloro
0.131
89.99
15.19
0.001
0.00
Temp Chloro
0.285
-153.26
0.00
1.000
0.34
Temp
0.212
-153.13
0.12
0.940
0.32
Chloro
0.154
-151.08
2.17
0.337
0.12
Dyticid
0.129
-150.22
3.04
0.219
0.07
Anisoptera Dyticid
0.183
-149.39
3.87
0.144
0.05
Anisoptera
0.084
-148.76
4.50
0.106
0.04
Temp Chloro Anisoptera Dyticid
0.319
-148.50
4.76
0.093
0.03
Temp DO pH
0.231
-148.19
5.07
0.079
0.03
Temp DO pH Anisoptera Dyticid Chloro
0.358
-142.84
10.42
0.005
0.00
Size at metamorphosis
62
Survival
a
Temp
0.219
123.68
0.00
1.000
0.60
Temp Chloro
0.224
126.22
2.54
0.281
0.17
Temp DO pH
0.266
127.55
3.87
0.145
0.09
Anisoptera
0.073
128.65
4.98
0.083
0.05
Dyticid
0.046
129.51
5.83
0.054
0.03
Chloro
0.040
129.68
6.00
0.050
0.03
Anisoptera Dyticid
0.102
130.43
6.75
0.034
0.02
Temp Chloro Anisoptera Dyticid
0.225
132.33
8.65
0.013
0.01
Temp DO pH Anisoptera Dyticid Chloro
0.292
137.09
13.41
0.001
0.00
Models are ranked in ascending order of Akaike’s Information Criterion for small
sample sizes (AICc) b
Akaike’s weight
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Figure 3.1. Periphyton productivity measured upon the addition of tadpoles, at the onset of metamorphosis, and at the end of the experiment. Chlorophyll a (µg/m2) from periphyton samples indicated productivity. Clearcut, clearcut-edge, forest-edge, and forest treatments are represented by solid lines with diamonds, solid lines and squares, dashed lines with triangles, and dashed lines with circles, respectively.
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3000
Chlorophyll a (ug/m2)
2500
2000
1500
1000
500
0 15-Jun
22-Jun
29-Jun
6-Jul
13-Jul
Date
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20-Jul
27-Jul
Figure 3.2. Tadpole performance in the four treatments based on A) mean time to metamorphosis (days), B) mean mass at metamorphosis, and C) mean percent survival. Bars represent means with standard error bars. Statistical significance among treatments is indicated by letters above each bar as determined using Fisher’s LSD (α = 0.05).
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A.
45
Mean days to metamorphosis
40
a
a
Clearcut
Clearcut Edge
b
b
Forest Edge
Forest
35 30 25 20 15 10 5 0
B.
Mean mass at metamorphosis (g)
0.60
C.
0.50
a
a , b
Clearcut
Clearcut Edge
a,b
b
0.40 0.30 0.20 0.10 0.00
Forest Edge
Forest
100 90
b a,b
a
a
Mean percent survival
80 70 60 50 40 30 20 10 0
Clearcut
Clearcut Edge
Forest Edge
Habitat Treatment
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Forest
CHAPTER 4
CONCLUSIONS AND FUTURE DIRECTIONS
Daniel J. Hocking
My studies examined gray treefrog (Hyla versicolor) breeding site selection and subsequent offspring performance in response to experimental forest alterations. Breeding site selection was tested using wading pools located in recent clearcuts with high and low amounts of coarse woody debris, partial cuts (canopy thinning), and control forest treatments. The number of eggs oviposited in pools was compared among the four treatments. The next experiment more directly tested the breeding site selection across a forest-clearcut gradient. Gray treefrogs were allowed to breed in cattle tanks and the number of oviposition events was compared along the gradient. I also examined the number of males captured around the tanks at night. Finally, I tested the offspring (tadpole) performance along the same gradient from forest to clearcut. The primary conclusions of these studies are:
1. Gray treefrogs preferred breeding sites located in clearcuts over forested sites. Coarse woody debris did not influence the use of breeding sites in recent clearcuts. 2. Gray treefrog females preferred tanks in clearcuts close (10 m) to forest edges. Gray treefrog adults reside in tree holes during the day, therefore I suggest that females
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were moving from the diurnal retreats in the forest to the nearby tanks in the clearcut. Male captures did not differ between clearcut and clearcut edge tanks. Males’ behavior may differ from females’ because they spend multiple nights at breeding sites, whereas females are known to move from their diurnal retreat to the breeding site and back to the retreat in a single night (Johnson 2005). It may be physiologically stressful for females to travel to isolated breeding sites in clearcuts in one night. In contrast, males can spend multiple days in clearcuts if there is suitable microhabitat (personal observation). Some males may benefit from moving to tanks in the clearcut farther from the forest thereby reducing competition for mates. 3. The necessity of multiple habitat types highlights the need for habitat complementation. Gray treefrogs use forest habitat for foraging and diurnal retreats. They also used clearcuts (open canopy) habitats for breeding. Although clearcut habitat can benefit gray treefrogs, large clearcuts can disrupt the connectivity between breeding and non-breeding habitats. 4. Gray treefrog tadpoles had greater survival and shorter larval periods in tanks located in clearcuts compared with tanks in forest habitat. These benefits arise from the increased temperature and periphyton production in open canopy ponds. However, gray treefrogs were smaller at metamorphosis in the clearcuts than in the forest tanks. Small size at metamorphosis can reduce lifetime fitness (Semlitsch et al. 1988; Smith 1987) and may be particularly costly for small individuals in clearcuts where higher temperatures and wind increase the risk of desiccation (Ash 1995; Keenan & Kimmins 1993; Rothermel 2004).
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My research highlights the need for future studies to fully understand how habitat alterations can impact amphibian populations. Future directions include examining:
1. The effects of density dependence (intraspecific competition). Gray treefrogs continued to oviposit in tanks in the clearcut edge despite increasing density of conspecifics. Females should be expected to shift to breeding in other sites once the larval density reduces the quality of the breeding site below that of other preferred sites. Additionally, experiments are needed to examine the effects on tadpoles at high density in open canopy habitats compared with tadpoles at low density in closed canopy habitat. 2. How gray treefrogs (and other species) respond to pools created by logging operations. My work demonstrates that frogs can alter their breeding behavior in response to clearcutting; future research needs to be conducted on how frogs are reacting to logging at other sites. Logging roads and skidder operation often create ditches and pools that frogs can use for breeding (Cromer 1999; Cromer et al. 2002). More work needs to be done on how the use of these created pools influence breeding behavior and recruitment. Ultimately, it will be important to determine the effects these breeding choices have on population dynamics. 3. The physiological and potential fitness costs of adult travel and calling in different habitats. Specifically, we must determine how costly is it for males and females to use breeding sites in clearcuts compared with forest habitat. This will help to determine the costs and benefits of individual decisions for the population.
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4. Differences in male traits among the treatments. Are smaller males or males with less attractive calls forced to use less preferred, lower quality habitat (i.e. closed canopy breeding sites or sites located in clearcuts far from forested habitat)? 5. Most importantly, how growth and survival differ among juveniles emigrating from ponds in the different treatments. Knowledge of aquatic carry-over effects in different habitats is the crucial information that is missing for understanding amphibian population dynamics. 6. Finally, the effects of context dependent predator-prey interactions between tadpoles and dragonfly larvae (Wilbur 1988). Through a few laboratory and mesocosm studies, it has been assumed that dragonfly larvae exert a strong influence on tadpole (including gray treefrog) growth and survival (McCollum & Leimberger 1997; Relyea 2003; Relyea & Hoverman 2003; Semlitsch 1990). However, gray treefrogs breed as many of the Ashnidae dragonfly larvae are emerging from the ponds. This reduces the large predator density; many species of dragonflies are breeding synchronously with gray treefrogs, thereby increasing the density of small potential predators. Depending on the habitat and timing of breeding, gray treefrogs may face predators of different sizes, different densities, and even different species. Gray treefrog larvae may be in a size race with dragonfly larvae (Wilbur 1988). Although dragonfly larvae are not gape limited, small individuals will have difficulty capturing large tadpoles that can swim away quickly.
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LITERATURE CITED Ash, A. N. 1995. Effects of clear-cutting on litter parameters in the southern Blue Ridge Mountains. Castanea 60:89-97. Cromer, R. B. 1999. The effects of gap creation and harvest-created ruts on herpetofauna in a southern bottomland hardwood forest. Page 74. Forest Resources. Clemson University, Clemson. Cromer, R. B., J. D. Lanham, and H. H. Hanlin. 2002. Herpetofaunal response to gap and skidder-rut wetland creation in a southern bottomland hardwood forest. Forest Science 48:407-413. Johnson, J. R. 2005. Multi-scale investigations of gray treefrog movements, patterns of migration, dispersal, and gene flow. Page 246. Division of Biological Sciences. University of Missouri, Columbia. Keenan, R. J., and J. P. Kimmins. 1993. The ecological effects of clear-cutting. Environmental Review 1:121-144. McCollum, S. A., and J. D. Leimberger. 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615-621. Relyea, R. A. 2003. Predators come and predators go: the reversibility of predatorinduced traits. Ecology 84:1840-1848. Relyea, R. A., and J. T. Hoverman. 2003. The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596-604.
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Rothermel, B. B. 2004. Migratory success of juveniles: a potential constraint on connectivity for pond-breeding amphibians. Ecological Applications 14:15351546. Semlitsch, R. D. 1990. Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology 68:1027-1030. Semlitsch, R. D., D. E. Scott, and J. H. K. Pechmann. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. Smith, D. C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344-350. Wilbur, H. M. 1988. Interactions between growing predators and growing prey. Pages 157-172 in B. Ebenman, and L. Persson, editors. Size-structured populations. Springer-Verlag, Berlin.
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