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Abstracts to papers from the Rohr Lab

Jennings, D.E.*, Krupa, J.J., Raffel, T.R.†, Rohr, J.R. in press. Evidence for competition between carnivorous plants and spiders. Proceedings of the Royal Society B - Biological Sciences.

Several studies have demonstrated that competition between disparate taxa can be important in determining community structure, yet surprisingly, to our knowledge, no quantitative studies have been conducted on competition between carnivorous plants and animals. To examine potential competition between these
taxa, we studied dietary and microhabitat overlap between pink sundews (Drosera capillaris) and wolf spiders (Lycosidae) in the field, and conducted a laboratory experiment examining the effects of wolf spiders on sundew fitness. In the field, we found that sundews and spiders had a high dietary overlap with each other and with the available arthropod prey. Associations between sundews and spiders depended on spatial scale: both sundews and spiders were found more frequently in quadrats with more abundant prey, but within quadrats, spiders constructed larger webs and located them further away from sundews as the total sundew trapping area increased, presumably to reduce competition. Spiders also constructed larger webs when fewer prey were available. In the laboratory, our experiment revealed that spiders can significantly reduce sundew fitness. Our findings suggest that members of the plant and animal kingdoms can and do compete.


Keywords: competition; Drosera capillaris; Lycosidae; plant–animal interactions

 

 

Rohr, J.R., McCoy, K.A.† 2010. Preserving environmental health and scientific credibility: A practical guide to reducing conflicts of interest. Conservation Letters. 3: 143-150

Conflicts of interest, situations where personal or organizational considerations have compromised or biased professional judgment and objectivity, can weaken scientific credibility, pose threats to biodiversity and ecosystem services, and are often precursors to corruption. Here, we review historical and international examples of conflicts of interest and their impacts on global biodiversity. We present a contemporary example of a conflict of interest that might have implications for the U.S. Environmental Protection Agency's re-evaluation of the safety of the herbicide atrazine. To help scientists, natural resource managers, policy makers, and judicial officials identify and thwart conflicts of interest, we review strategies used by individuals and organizations with conflicts of interest to evade environmental and public health decisions, discuss the role of the scientific and governmental review processes in maintaining scientific integrity, and offer recommendations to reduce bias and facilitate sound and swift decision making for enhanced environmental health.

Keywords: Atrazine; biodiversity; chemical registration; ecotoxicology; junk science; manufacturing uncertainty; peer-review process

 

 

Rohr, J.R., Raffel, T.R.† 2010. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America. 107: 8269-8274

The role of global climate change in the decline of biodiversity and the emergence of infectious diseases remains controversial, and the effect of climatic variability, in particular, has largely been ignored. For instance, it was recently revealed that the proposed link between climate change and widespread amphibian declines, putatively caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), was tenuous because it was based on a temporally confounded correlation. Here we provide temporally unconfound edevidence that global El Niño climatic events drive widespread amphibian losses in genus Atelopus via increased regional temperature variability, which can reduce amphibian defenses against pathogens. Of 26 climate variables tested, only factors associated with temperature variability could account for the spatiotemporal patterns of declines thought to be associated with Bd. Climatic predictors of declines became significant only after controlling for a pattern consistent with epidemic spread (by temporally detrending the data). This presumed spread accounted for 59% of the temporal variation in amphibian losses, whereas El Niño accounted for 59% of the remaining variation. Hence, we could account for 83% of the variation in declines with these two variables alone. Given that global climate change seems to increase temperature variability, extreme climatic events, and the strength of Central Pacific El Niño episodes, climate change might exacerbate worldwide enigmatic declines ofamphibians, presumably by increasing susceptibility to disease. These results suggest that changes to temperature variability associated with climate change might be as significant to biodiversity losses and disease emergence as changes to mean temperature.

Keywords: chytridiomycosis; climate change; conservation; El Niño; emerging infectious disease

 

 

Rohr, J.R., McCoy, K.A.† 2010. A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives. 118: 20-32

Objective: The biological effects of the herbicide atrazine on freshwater vertebrates are highly controversial. In an effort to resolve the controversy, we conducted a qualitative meta-analysis on the effects of ecologically relevant atrazine concentrations on amphibian and fish survival, behavior, metamorphic traits, infections, and immune, endocrine, and reproductive systems.
Data sources: We used published, peer-reviewed research and applied strict quality criteria for inclusion of studies in the meta-analysis.
Data synthesis: We found little evidence that atrazine consistently caused direct mortality of fish or amphibians, but we found evidence that it can have indirect and sublethal effects. The relationship between atrazine concentration and timing of amphibian metamorphosis was regularly nonmonotonic, indicating that atrazine can both accelerate and delay metamorphosis. Atrazine reduced size at or near metamorphosis in 15 of 17 studies and 14 of 14 species. Atrazine elevated amphibian and fish activity in 12 of 13 studies, reduced antipredator behaviors in 6 of 7 studies, and reduced olfactory abilities for fish but not for amphibians. Atrazine was associated with a reduction in 33 of 43 immune function end points and with an increase in 13 of 16 infection end points. Atrazine altered at least one aspect of gonadal morphology in 7 of 10 studies and consistently affected gonadal function, altering spermatogenesis in 2 of 2 studies and sex hormone concentrations in 6 of 7 studies. Atrazine did not affect vitellogenin in 5 studies and increased aromatase in only 1 of 6 studies. Effects of atrazine on fish and amphibian reproductive success, sex ratios, gene frequencies, populations, and communities remain uncertain.
Conclusions: Although there is much left to learn about the effects of atrazine, we identified several consistent effects of atrazine that must be weighed against any of its benefits and the costs and benefits of alternatives to atrazine use.

Keywords: aromatase, behavior, disease, gonads, immunity, metamorphosis, parasite, reproduction, testicular ovarian follicles, vitellogenin.

 

 

Raffel, T.R.†, Sheingold, J.L.§, Rohr, J.R. 2009. Lack of pesticide toxicity to Echinostoma trivolvis eggs and miracidia. Journal of Parasitology. 95: 1548-1551

Pesticides can elevate trematode infections in amphibians. However, direct adverse effects of pesticides on embryos and free-living stages of trematodes have not been thoroughly explored, despite the potential for these effects to reduce amphibian trematode infections. We measured the effects of atrazine, glyphosate, carbaryl, and malathion on embryo and miracidium (free-living stage) survival of Echinostoma trivolvis, a common trematode of amphibians. We found no evidence of biologically relevant effects of these pesticides at ecologically relevant concentrations.

 

 

Clements, W.H., Rohr, J.R. 2009. Community responses to contaminants: Using basic ecological principles to predict ecotoxicological effects. Environmental Toxicology and Chemistry. 28: 1789-1800

Community ecotoxicology is defined as the study of the effects of contaminants on patterns of species abundance, diversity, community composition, and species interactions. Recent discoveries that species diversity is positively associated with ecosystem stability, recovery, and services have made a community-level perspective on ecotoxicology more important than ever. Community ecotoxicology must explicitly consider both present and impending global change and shift from a purely descriptive to a more predictive science. Greater consideration of the ecological factors and threshold responses that determine community resistance and resilience should improve our ability to predict how and when communities will respond to, and recover from, xenobiotics. A better understanding of pollution-induced community tolerance, and of the costs of this tolerance, should facilitate identifying contaminantimpacted communities, thus forecasting the ecological consequences of contaminant exposure and determining the restoration effectiveness. Given the vast complexity of community ecotoxicology, simplifying assumptions, such as the possibility that the approximately 100,000 registered chemicals could be reduced to a more manageable number of contaminant classes with similar modes of action, must be identified and validated. In addition to providing a framework for predicting contaminant fate and effects, food-web ecology can help to identify communities that are sensitive to contaminants, contaminants that are particularly insidious to communities, and species that are crucial for transmitting adverse effects across trophic levels. Integration of basic ecological principles into the design and implementation of ecotoxicological research is essential for predicting contaminant effects within the context of rapidly changing, global environmental conditions.

Keywords: community ecotoxicology; contaminant transport; global change; indirect effects; resistance/resilience.

 

 

Rohr, J.R., Mahan, C.G., Kim, K. 2009. Response of arthropod biodiversity to foundation species declines: the case of the eastern hemlock. Forest Ecology and Management. 258: 1503-1510

Widespread declines of foundation species, such as many corals, kelps, and overstory trees, are of grave concern because, by definition, these species create and maintain habitat that supports other species. Nevertheless, past responses to their declines, many of which were caused by invasive species, have been
late and ineffective, underscoring the need to predict changes in biodiversity and ecosystem function associated with species invasions and foundation species losses. One predictive, but under-used, approach is to compare the species and functions associated with the afflicted foundation species to its
projected replacement communities. The taxa associated with the foundation species and subsequent successional stages would be expected to decline and increase, respectively. We used this approach to generate hypotheses for how arthropod diversitymight change in response to extensive losses of eastern
hemlock trees caused by the invasive, hemlock woolly adelgid (insect: Hemiptera, Adelgidae). Our allstrata survey of the arthropods in an eastern hemlock forest and its expected replacement climax community in themid-Atlantic region of the United States,mixed hardwood forest, suggests that eastern hemlock losses might initiate increases in arthropod abundance, alpha diversity, and 23 arthropod taxa, might produce no change in evenness or composition of arthropod functional groups, but might trigger decreases in beta diversity and seven hemlock indicator taxa. These predictions are consistent with observed trends in arthropod responses to hemlock losses in other studies, and thus might be useful for targeting early monitoring, management, and conservation efforts. This research is exploratory, however, and tests of these predictions across larger spatial scales will be necessary to determine the generality of the findings.

Keywords: disease; forest; insect pests; invasive and introduced species; secondary species declines; succession.

 

 

Rohr, J.R., Swan, A.§, Raffel, T.R.†, Hudson, P.J. 2009. Parasites, info-disruption, and the ecology of fear. Oecologia. 159: 447-454

There is growing interest in the ecological consequences of fear, as evidenced by the numerous studies on the nonconsumptive, trait-mediated effects of predators. Parasitism, however, has yet to be fully integrated into research on the ecology of fear, despite it having direct negative and often lethal effects on hosts and being the most common life history strategy on the planet. This might at least be partly due to the traditional, but untested, assumption that anti-parasite responses are weak relative to antipredator responses. To test this hypothesis, we quantified the activity and location responses of Bufo americanus tadpoles to one of six chemical cues: water; cercariae of Echinostoma trivolvis, a trematode which infects and can kill amphibians; a snail releasing E. trivolvis cercariae; an uninfected snail; food; or conspecific alarm chemicals signaling predation. There is also literature encouraging research on the context dependency and pollution-induced disruption of fear responses. Consequently, before quantifying responses to the chemical cues, half of the B. americanus were exposed to the herbicide atrazine (201 g/l for 4 days), a reported inhibitor of fear responses in fish. Tadpoles were attracted to food, were indiVerent to an uninfected snail,
avoided alarm chemicals, and exhibited avoidance and elevated activity in response to a snail shedding cercariae and cercariae alone. Atrazine had no detectable effects on B. americanus’ responses to the tested cues despite the use of a higher concentration and longer exposure duration than has been repeatedly shown to inhibit chemical cue detection in fish. The magnitude of anti-parasite and anti-predator responses were qualitatively similar, suggesting that the fear of disease and its ecological consequences could be comparable to that of predation. Consequently, we call for a greater integration of parasites into research on the ecology
of fear and trait-mediated indirect effects.


Keywords: alarm chemical; atrazine; Bufo americanus; trait-mediated indirect effects; trematode.

 

 

Raffel, T.R.†, Le Gros, R.J.§, Love, B.C., Rohr, J.R., Hudson, P.J. 2009. Parasite age-intensity relationships in red-spotted newts: does immune memory influence salamander disease dynamics? International Journal for Parasitology. 39: 231-241

Acquired immune memory in vertebrates influences transmission and persistence of infections, with consequences for parasite dynamics at both the individual and population levels. The potential impact of acquired immunity is of particular interest for salamanders, whose acquired immune systems are thought to be less effective than those of frogs and other tetrapods. One way to examine the importance of acquired immunity to parasite dynamics at the population level is by examining the relationship between host age and parasite infection intensity. Acquired immunity reduces infection rates in older animals, causing decreased parasite intensity in older age classes and leading to curvilinear age-intensity relationships for persistent parasites and convex age-intensity relationships for transient parasites. We used age-intensity relationships to look for the signature of acquired immunity for 12 parasite taxa of red-spotted newts (Notophthalmus viridescens), using data from a 2-year parasitological survey of six newt populations. We estimated ages from snout-vent length (SVL) based on the relationship between SVL and skeletochronologically-derived ages in a subset of newts. We found evidence of acquired immunity to two parasite taxa, bacterial pathogens and the protist Amphibiocystidium viridescens, whose convex age-intensity relationships could not be easily explained by alternative mechanisms. Our results suggest that the acquired immune response of newts is sufficient to influence the dynamics of at least some parasites.

Keywords: Acanthocephalan; Amphibiocapillaria;Clinostomum;Ichthyophonus; nematode; Plagitura; trematode; trypanosome.

 

 

Delphia, C.M.*, Rohr, J.R., Stephenson, A.G., De Moraes, C.M., Mescher, M.C. 2009. Effects of genetic variation and inbreeding on volatile production in a field population of horsenettle. International Journal of Plant Sciences. 170: 12-20

Plant volatiles mediate numerous interactions between plants and insects, yet few studies have examined variation in volatile production within plant populations or the genetic and environmental causes of this variation. Here we document the effects of inbreeding and maternal family on volatile production by horsenettle
Solanum carolinense L. (Solanaceae).We collected volatiles from ramets (clones) of each of 12 genets (genotypes) of horsenettle grown in four agricultural fields with natural levels of herbivory. The 12 genets included self- and cross-pollinated progeny from six maternal plants. We found that inbreeding reduced total volatile production relative to that of outcrossed plants. We also found a breeding-by-family interaction for the total amount and blend of volatiles, indicating genetic variation among families for inbreeding depression. Analysis of outcrossed plants alone (a random sample from the population) revealed a genet effect on the total amount and blend of volatiles released, indicating broad-sense heritability of volatile traits. Our findings offer insight into the consequences of inbreeding on volatile production and the variation in volatile cues available to foraging insects in a wild plant system. Moreover, we believe this to be the first study demonstrating genetic variation for plant volatiles in a noncultivated species under field conditions.


Keywords: inbreeding; plant volatiles; genetic variation; Solanum carolinense; horsenettle; Solanaceae.

 

 

Rohr, J.R., Raffel, T.R.†, Romansic, J.†, McCallum, H., Hudson, P.J. 2008. Evaluating the links between climate, disease spread, and amphibian declines. PNAS. 45: 17436-17441

Human alteration of the environment has arguably propelled the Earth into its sixth mass extinction event and amphibians, the most threatened of all vertebrate taxa, are at the forefront. Many of the worldwide amphibian declines have been caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd), and two contrasting hypotheses have been proposed to explain these declines. Positive correlations between global warming and Bd-related declines sparked the chytrid-thermal-optimum hypothesis, which proposes that global warming increased cloud cover in warm years that drove the convergence of daytime and nighttime temperatures toward the thermal optimum for Bd growth. In contrast, the spatiotemporalspread hypothesis states that Bd-related declines are caused by the
introduction and spread of Bd, independent of climate change. We provide a rigorous test of these hypotheses by evaluating (i) whether cloud cover, temperature convergence, and predicted temperaturedependent Bd growth are significant positive predictors of amphibian extinctions in the genus Atelopus and (ii) whether spatial structure in the timing of these extinctions can be detected without making assumptions about the location, timing, or number of Bd emergences. We show that there is spatial structure to the timing of Atelopus spp. extinctions but that the cause of this structure remains equivocal, emphasizing the need for further molecular characterization of Bd. We also show that the reported positive multi-decade correlation between Atelopus spp. extinctions and mean tropical air temperature in the previous year is indeed robust, but the evidence that it is causal is weak because numerous other variables, including regional banana and beer production, were better predictors of these extinctions. Finally, almost all of our findings were opposite to the predictions of the chytrid-thermal-optimum hypothesis. Although climate change is likely to play an important role in worldwide amphibian declines, more convincing evidence is needed of a causal link.

 

Keywords: chytridiomycosis; climate change; emerging infectious disease; extinction; global warming.

 

 

Rohr, J.R., Schoetthofer, A.M., Raffel, T.R.†, Carrick, H.J., Halstead, N., Hoverman, J.T.†, Johnson, C.M., Johnson, L.B., Lieske, C., Piwoni, M.D., Schoff, P.K., Beasley, V.R. 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature. 455: 1235-1239

Global amphibian declines have often been attributed to disease, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than
240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) in the declining northern leopard frog Rana pipiens. The effects of atrazine were consistent across trematode taxa. The combination of atrazine and phosphate—principal agrochemicals in global corn and sorghum production—accounted for
74% of the variation in the abundance of these often debilitating larval trematodes (atrazine alone accounted for 51%). Analysis of field data supported a causal mechanism whereby both agrochemicals increase exposure and susceptibility to larval trematodes by augmenting snail intermediate hosts and suppressing amphibian immunity. A mesocosm experiment demonstrated that, relative to control tanks, atrazine tanks had immunosuppressed tadpoles, had significantly more attached algae and snails, and had tadpoles with elevated trematode loads, further supporting a causal relationship between atrazine and elevated trematode infections in amphibians. These results raise concerns about the role of atrazine and phosphate in amphibian declines, and illustrate the value of quantifying the relative importance of several possible drivers of disease risk while determining the mechanisms by which they facilitate disease emergence.

 

 

Raffel, T.R.†, Martin, L.B., Rohr, J.R. 2008. Parasites as predators: unifying natural enemy ecology. Trends in Ecology and Evolution. 23: 610-618

Parasitism and predation have long been considered analogous interactions. Yet by and large, ecologists continue to study parasite–host and predator–prey
ecology separately. Here we discuss strengths and shortcomings of the parasite-as-predator analogy and its potential to provide new insights into both fields.
Developments in predator–prey ecology, such as temporal risk allocation and associational resistance, can drive new hypotheses for parasite–host systems.
Concepts developed in parasite–host ecology, such as threshold host densities and phylodynamics, might provide new ideas for predator–prey ecology. Topics such as trait-mediated indirect effects and enemy-mediated facilitation provide opportunities for the two fields to work together. We suggest that greater unification of predator–prey and parasite–host ecology would foster advances in both fields.

 

 

Rohr, J.R., Raffel, T.R.†, Sessions, S.K., Hudson, P.J. 2008. Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications. 18: 1743-1753

Anthropogenic factors can have simultaneous positive and negative effects on parasite transmission, and thus it is important to quantify their net effects on disease risk. Net effects will be a product of changes in the survival and traits (e.g., susceptibility, infectivity) of both hosts and parasites. In separate laboratory experiments, we exposed cercariae of the trematode Echinostoma trivolvis, and its first and second intermediate hosts, snails (Planorbella trivolvis) and green frog tadpoles (Rana clamitans), respectively, to one of four common pesticides (atrazine, glyphosate, carbaryl, and malathion) at standardized, ecologically relevant
concentrations (201.0, 3700.0, 33.5, and 9.6 lg/L, respectively). We measured effects of pesticide exposure on six mechanisms important to this host–parasite interaction: (1) survival of E. trivolvis cercariae over 26 hours, (2) tadpole survival over two weeks, (3) snail survival over four weeks, (4) snail growth and fecundity, (5) cercarial infectivity, and (6) tadpole susceptibility to a fixed number of cercariae. Pesticides, in general, caused significantly greater mortality of E. trivolvis cercariae than did control treatments, but atrazine was the lone chemical to significantly reduce cercarial survival (LC50 value ¼ 267 mg/L) and then only at concentrations greater than commonly found in aquatic ecosystems (200 lg/L). None of the pesticides significantly enhanced E. trivolvis virulence, decreased tadpole survival, or reduced snail survival, growth, or fecundity. Sublethal exposure of the cercariae to the pesticides (4 h) did not significantly affect trematode encystment in R. clamitans. In contrast, sublethal exposure of R. clamitans to each of the four pesticides increased their susceptibility as measured by the percentage of cercariae that encysted. The reduction in exposure to trematodes due to pesticide-induced cercarial mortality (a density-mediated effect) was smaller than the pesticideinduced increase in amphibian susceptibility (a trait-mediated effect), suggesting that the net effect of exposure to environmentally realistic levels of pesticides will be to elevate amphibian trematode infections. These findings highlight the importance of elucidating the lethal and sublethal effects of anthropogenic factors on both hosts and parasites to understand the mechanisms underlying changes in parasite transmission and virulence, an approach that is
especially needed for amphibians, a taxon experiencing global disease-related declines.


Keywords: atrazine; carbaryl; Echinostoma trivolvis trematode; indirect effect, density-mediated or trait-mediated; glyphosate; herbicide; insecticide; malathion; parasite; Planorbella trivolvis snail; Rana clamitans; amphibian decline.

 

 

Tooker, J.F. †, Rohr, J.R., Abrahamson, W.G., De Moraes, C.M. 2008. Gall insects can avoid and alter indirect plant defenses. New Phytologist. 178: 657-671

• Parasitic species can dramatically alter host traits. Some of these parasite-induced changes can be considered adaptive manipulations that benefit the parasites.
Gall-inducing insects are parasites well known for their ability to alter host-plant morphology and physiology, including the distribution of plant defensive compounds. Here it was investigated whether gall-inducing species alter indirect plant defenses, involving the release of volatile compounds that are attractive to foraging natural enemies.
• Using field and factorial laboratory experiments, volatile production by goldenrod (Solidago altissima) plants was examined in response to attack by two gall-inducing species, the tephritid fly Eurosta solidaginis and the gelechiid moth Gnorimoschema gallaesolidaginis, as well as the meadow spittlebug, Philaenus spumarius, and the generalist caterpillar Heliothis virescens.
Heliothis virescens elicited strong indirect defensive responses from S. altissima, but the gall-inducing species and spittlebugs did not. More significantly, infestation by E. solidaginis appeared to suppress volatile responses to subsequent attack by the generalist caterpillar.
• The extensive control that E. solidaginis apparently exerts over host-plant defense responses may reduce the predation risk for the gall inducer and the subsequent herbivore, and could influence community-level dynamics, including the distribution of herbivorous insect species associated with S. altissima parasitized by E. solidaginis.


Keywords: Eurosta; gall; Gnorimoschema; herbivory; induced responses; Solidago altissima; volatile response.

 

 

Rohr, J.R., Kim, K., Mahan, C. 2007. Developing a monitoring program for invertebrates: guidelines and a case study. Conservation Biology. 21: 422-433

Invertebrates provide the majority of ecosystem services; thus, it is important that they be inventoried, monitored, and protected. Nevertheless, inventories, monitoring, and management generally focus on vertebrates and flowering plants. Consequently, there are few guidelines or case studies for invertebrates. We present a procedure for developing a monitoring program for species-rich invertebrates that entails (1) characterizing the community; (2) identifying surrogates for biodiversity; and (3) establishing efficient methods to monitor surrogates and any ecologically important or sensitive taxa. We used these procedures, biodiversity-based statistical advances, and a survey of arthropods to develop a monitoring plan for the forests of Shenandoah National Park, Virginia (U.S.A.). Our case study revealed that mixed hardwood and hemlock forests had significantly different compositions of arthropods in their soil and understory strata. Of the 10 orders tested Coleoptera and Hymenoptera were the only two to pass most of the five surrogate tests, and their combination improved predictions of overall arthropod diversity. Because arthropods represent the majority of macroscopic species in most ecosystems, the ability of this assemblage to predict overall arthropod diversity makes it a powerful surrogate. Of the 11 collecting methods used, the beat-sheet method was the most efficient for monitoring this surrogate assemblage. To complement this coarse-filter approach to monitoring at-risk, invasive, or other important taxa (fine filter), we used ordination analyses to match 66 taxa with the methods that most effectively sampled them. Our methods serve as a model for developing an invertebrate monitoring plan and should facilitate linking such monitoring with ecosystem functions and management.

Keywords: arthropods; biodiversity surrogates; complementarity; Convention on Biological Diversity; higher taxa; morphospecies; ordination; rarefaction curves.

 

 

Leslie, T.W., Hoheisel, G.A., Biddinger, D.J., Rohr, J.R., Fleischer, S.J. 2007. Transgenes sustain epigeal biodiversity in diversified vegetable farm systems. Environmental Entomology. 36: 234-244

Many ecological studies have focused on the effects of transgenes in Þeld crops, but few have considered multiple transgenes in diversified vegetable systems. We compared the epigeal, or soil surface-dwelling, communities of Coleoptera and Formicidae between transgenic and isoline vegetable systems consisting of sweet corn, potato, and acorn squash, with transgenic cultivars expressing Cry1(A)b, Cry3, or viral coat proteins. Vegetables were grown in replicated split plots over 2 yr with integrated pest management (IPM) standards defining insecticide use patterns. More than 77.6% of 11,925 insects from 1,512 pitfall traps were identified to species, and activity density was used to compare dominance distribution, species richness, and community composition. Measures of epigeal biodiversity were always equal in transgenic vegetables, which required fewer insecticide applications than their near isolines. There were no differences in species richness between transgenic and isoline treatments at the farm system and individual crop level. Dominance distributions were also similar between transgenic and isoline farming systems. Crop type, and not genotype, had a significant infuence on Carabidae and Staphylinidae community composition in the Þrst year, but there were no treatment effects in the second year, possibly because of homogenizing effects of crop rotations. Communities were more infuenced by crop type, and possibly crop rotation, than by genotype. The heterogeneity of crops and rotations in diversiffed vegetable farms seems to aid in preserving epigeal biodiversity, which may be supplemented by reductions in insecticide use associated with transgenic cultivars.

Keywords: biodiversity; Carabidae; genetically modified crops; nontarget effects; Staphylinidae.

 

 

Lekberg, Y., Koide, R.T., Rohr, J.R., Aldrich-Wolfe, L., & Morton, J.B. 2007. Role of niche theory and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology. 95: 95-105

1. Metacommunity and neutral theory have reinvigorated the study of ‘niches’ and have emphasized the importance of understanding the influences of competition, abiotic factors and regional spatial processes in shaping communities.
2. We conducted a field survey to examine the effects of soil characteristics and distance on arbuscular mycorrhizal (AM) fungal communities of maize (Zea mays) in sand and clay soils. To address whether the field distributions of AM fungal species represented their fundamental or realized niches, we grew representative species of the two dominant genera, Glomus and Gigaspora, alone or together on Sorghum bicolor plants in sand,clay or a sand/clay mixture in the glasshouse.
3. In the field, soil characteristics and spatial structure accounted for significant proportions of the variation in community composition among sites, suggesting that both environmental variables and dispersal were important factors shaping AM fungal communities.
4. AM fungi in the family Glomeraceae occurred predominately in clay soils, whereas AM fungi in the family Gigasporaceae dominated in sand soils. Niche space of Glomeraceae was further partitioned by levels of soil organic carbon and nitrogen.
5. In the glasshouse, root colonization by Glomus was high in all three soils when grown in the absence of Gigaspora, indicating a broad fundamental niche. Root colonization by Gigaspora was negatively correlated with percentage clay when grown in the absence of Glomus, consistent with the low abundance of this family in clay soils in the field. When grown together, spore production of both Glomus and Gigaspora was significantly reduced only in the sand soil, indicating that competition could limit niches of both families in certain soil environments.
6. Our results suggest that AM fungal distributions are the product of environment, interspecific competition and regional spatial dynamics, emphasizing the importance of using a metacommunity perspective in community ecology.

Keywords: arbuscular mycorrhizal fungi; community composition; dispersal; fundamentaland realized niche; internal transcribed spacer; metacommunity; soil characteristics; competition; T-RFLP; Zea mays.

 

 

Rohr, J.R., Kerby, J., Sih, A. 2006. Community ecology theory as a framework for predicting contaminant effects. Trends in Ecology and Evolution. 21: 606-613

Most ecosystems receive an assortment of anthropogenic chemicals from the thousands possible, making it important to identify a predictive theory for their direct and indirect effects. Here, we propose that the impacts of contaminants can be simplified and unified under the framework of community ecology. This approach offers predictions of the strength and direction of indirect effects, which species are crucial for propagating these effects, which communities will be sensitive to contaminants, and which contaminants will be most insidious to communities. We discuss insights offered by this approach, potential limitations and extensions, outstanding questions, and its value for integrated pest management, ecological risk assessment, and the development of remediation and ecosystem management strategies.

 

 

Raffel, T.R., Rohr, J.R., Kiesecker, J.M., Hudson, P.J. 2006. Negative effects of changing temperature on amphibian immunity under field conditions.Functional Ecology. 20: 819-828

1. Recent evidence of the important role of emerging diseases in amphibian population declines makes it increasingly important to understand how environmental changes affect amphibian immune systems.
2. Temperature-dependent immunity may be particularly important to amphibian disease dynamics, especially in temperate regions. Changes in temperature are expected to cause deviations away from optimal levels of immunity until the immune system can respond.
3. To test whether temperature changes cause deviations from optimal immunity under natural conditions, we conducted a seasonal survey of adult Red-Spotted Newts and measured basal levels of several immunological variables.
4. We then examined these findings in relation to: (1) the lag hypothesis, which predicts that changes in temperature-dependent immune parameters lag behind short-term temperature changes, and (2) the seasonal acclimation hypothesis, which predicts that immune cell production declines during long-term temperature decreases until amphibians can fully acclimate to winter conditions.
5. Our results supported both hypotheses, showing a spring lag effect on lymphocyte levels and an even stronger seasonal acclimation effect on lymphocytes, neutrophils and eosinophils in the autumn. Our findings suggest that temperature variability causes increased susceptibility of amphibians to infection, and they have implications for the emergence of disease and the potential for climate change to exacerbate amphibian decline.

Keywords: amphibian decline; climate change; immune; newt; Notophthalmus viridescens

 

 

Rohr, J.R., Sager, T. Sesterhenn, T., Palmer, B.D. 2006. Exposure, post-exposure, and density-mediated effects of atrazine on amphibians: Breaking down net effects into their parts. Environmental Health Perspectives. 114: 46-50

Most toxicology studies focus on effects of contaminants during exposure. This is disconcerting because subsequent survival may be affected. For instance, contaminant-induced mortality can be later ameliorated by reduced competition among the survivors, a concept we refer to as “density-mediated compensation.” Alternatively, it can be exacerbated by toxicant effects that persist or appear after exposure, a phenomenon we term “carryover effects.” We developed a laboratory framework for testing the contribution of exposure, density-mediated, and carryover effects to net survival, by exposing embryos and larvae of the streamside salamander (Ambystoma barbouri) to atrazine (0, 4, 40, 400 ppb; 3 ppb is the U.S. drinking water maximum) and quantifying survival during and 14 months after exposure. Atrazine is the most commonly used herbicide in the United States and a documented endocrine disruptor. We show that atrazine-induced mortality during exposure was ameliorated by density-dependent survival after exposure, but complete density-mediated compensation was precluded by significant carryover effects of atrazine. Consequently, salamanders exposed to ≥ 4 ppb of atrazine had significantly lower survival than did control animals 14 months postexposure. The greatest change in survival occurred at low exposure concentrations. These nonlinear, long-term, postexposure effects of atrazine have similarities to effects of early development exposure to other endocrine disruptors. Together with evidence of low levels of atrazine impairing amphibian gonadal development, the results here raise concerns about the role of atrazine in amphibian declines and highlight the importance of considering persistent, postexposure effects when evaluating the impact of xenobiotics on environmental health.

Keywords: amphibian declines; atrazine; density dependence; development; endocrine disruption; nonlinear dose response; pesticide; postexposure effects; salamander. Environ Health Perspect 114:46–50 (2006). PDF Available at: http://www.ehponline.org/members/2005/8405/8405.pdf

 

 

Raffel, T.R.†, Dillard, J.R., Hudson, P.J. 2006. Field evidence for leech-borne transmission of amphibian Ichthyphonus sp. Journal of Parasitology. 92: 1256-1264.

Parasites have been implicated in mass mortality events and population declines of amphibians around the world. One pathogen associated with mortality events in North America is an Ichthyophonus sp.-like organism that affects red-spotted newts (Notophthalmus viridescens) and several frog species, yet little is known about the distribution of this pathogen in wild populations or the mechanism of transmission. In an effort to identify factors influencing the distribution and abundance of this pathogen, we measured Ichthyophonus sp. prevalence and a series of factors that could contribute to transmission in 16 newt
populations during spring 2004. In contrast to our initial hypotheses of trophic transmission, several lines of evidence suggested a role for the amphibian leech (Placobdella picta) in Ichthyophonus sp. transmission. We propose the mechanistic hypothesis that a leech acquires Ichthyophonus sp. infection when inserting its proboscis into the muscles beneath the skin of infected newts and transmits the infection to other newts in subsequent feeding bouts. We also found effects of host sex, body mass, and breeding condition on Ichthyophonus sp. prevalence and the number of attached leeches. The number of leeches attached to newts was
strongly related to the proportion of newt habitat containing emergent vegetation, suggesting that anthropogenic eutrophication might lead to more frequent or severe outbreaks of Ichthyophonus sp. infection in amphibians.

 

 

Rohr, J.R., Crumrine, P. 2005. Effects of an herbicide and an insecticide on pond community structure and processes. Ecological Applications. 15:1135-1147

Virtually all species live within complex food webs, and many of these organisms are exposed to contaminants. However, we know little about how community processes, such as competition and predation, influence susceptibility to contaminants or how different types of contaminants shape communities. The objective of our study was to determine how realistic concentrations of the herbicide atrazine and the insecticide endosulfan influence the structure of a pond community when the presence of common community members was manipulated. We employed a factorial design in mesocosms to evaluate the effects of pesticide treatments (25 mg/L of atrazine, 10 mg/L of endosulfan, solvent control; two pulses separated by two weeks) and the presence or absence of wood frog tadpoles (Rana sylvatica), adult snails (Planorbella trivolvis), and caged dragonfly larvae (Anax junius) on a freshwater community. Tadpoles, snails, and chironomid larvae, Polypedilum sp. (Dipterans), all competed for periphyton. As a result, tadpoles reduced the survival, mass, and reproduction of snails; snails reduced the growth, development, inactivity, and dragonfly avoidance of tadpoles; snails and tadpoles reduced the abundance of chironomid larvae; and chironomid larvae reduced snail mass. The adverse effect of snails on tadpole growth and behavior was greater in the presence of the caged tadpole predator, A. junius. Neither pesticide affected dragonfly survival, but endosulfan directly reduced zooplankton (Daphnia), and atrazine indirectly reduced chironomid abundance. Atrazine also directly decreased periphyton, and endosulfan decimated chironomid larvae, resulting in indirect increases and decreases in competition for both snails and tadpoles, respectively. Consequently, relative to endosulfan, atrazine tended to decrease snail mass and reproduction and reduce tadpole mass, development, inactivity, refuge use, and dragonfly avoidance. However, the indirect effects of pesticides depended upon the presence of heterospecifics. The indirect benefit of endosulfan on snail mass was greater in the presence of caged dragonfly larvae, and endosulfan’s indirect benefit on tadpole mass was greater in the absence of snails. The effect of pesticides on tadpole activity depended on both caged dragonflies and snails. Thus, environmentally realistic concentrations of pesticides directly and indirectly shaped species responses and community composition, but the initial composition of the community influenced these pesticide effects. These results emphasize the importance of quantifying the effects of contaminants within complex natural communities.

Keywords: amphibian declines; anurans; behavior; Daphnia; food web; metamorphosis; periphyton; trematode; trophic cascade.

 


Rohr, J.R., Palmer, B.D. 2005. Aquatic herbicide exposure increases salamander desiccation risk eight months later in a terrestrial environment. Environmental Toxicology and Chemistry. 24:1253-1258

Contaminants and climate change may be factors in amphibian declines. However, few studies have explored their joint impacts on postmetamorphic amphibians, a life stage of great importance to amphibian population dynamics. Here, we examine the effects of premetamorphic exposure (mean exposure of 64 d) to ecologically relevant concentrations of the globally common herbicide atrazine (0, 4, 40, 400 mg/L) on the behavior and water retention of lone and grouped postmetamorphic, streamside salamanders, Ambystoma barbouri. Salamanders exposed to $40 mg/L of atrazine exhibited greater activity, fewer water-conserving behaviors, and accelerated water loss four and eight months after exposure compared to controls. No recovery from atrazine exposure
was detected and its effects were independent of the presence of conspecifics. These results are consistent with the hypothesis that adverse climatic conditions and contaminants can interact to harm post-metamorphic amphibians; however, they suggest that these two stressors need not be experienced simultaneously to do so. These results emphasize the importance of considering both latent and cumulative effects of temporally linked stressors in ecotoxicology.

Keywords: amphibian declines; climate; ontogeny; pesticide; post-exposure effects.

 

 

Rohr, J.R., Palmer, B.D. 2005. Aquatic herbicide exposure increases salamander desiccation risk eight months later in a terrestrial environment. Environmental Toxicology and Chemistry. 24:1253-1258

Contaminants and climate change may be factors in amphibian declines. However, few studies have explored their joint impacts on postmetamorphic amphibians, a life stage of great importance to amphibian population dynamics. Here, we examine the effects of premetamorphic exposure (mean exposure of 64 d) to ecologically relevant concentrations of the globally common herbicide atrazine (0, 4, 40, 400 mg/L) on the behavior and water retention of lone and grouped postmetamorphic, streamside salamanders, Ambystoma barbouri. Salamanders exposed to $40 mg/L of atrazine exhibited greater activity, fewer water-conserving behaviors, and accelerated water loss four and eight months after exposure compared to controls. No recovery from atrazine exposure was detected and its effects were independent of the presence of conspecifics. These results are consistent with the hypothesis that adverse climatic conditions and contaminants can interact to harm post-metamorphic amphibians; however, they suggest that these two stressors need not be experienced simultaneously to do so. These results emphasize the importance of considering both latent and cumulative effects of temporally linked stressors in ecotoxicology.

Keywords: amphibian declines; climate; ontogeny; pesticide; post-exposure effects.

 

 

Rohr, J.R., Park, D., Sullivan, A.M., McKenna, M., Propper, C.R., Madison D.M. 2005. Operational sex ratio in newts: field responses
and characterization of a constituent chemical cue. Behavioral Ecology. 16:286-293

Operational sex ratio (OSR) has been traditionally thought of as a force imposing competition for mates rather than also a cue used to regulate the intrasexual competition individuals encounter. To assess whether eastern red-spotted newts, Notophthalmus viridescens, could appropriately compare OSRs, we quantified field responses to traps containing four males, a sexually receptive female, four males plus a female, or nothing as a control. Early in the breeding season, males from two populations chose competitive mating opportunities over no mating opportunity at all, but generally preferred less competitive mating prospects. Later in the breeding season, as the OSR of newt populations becomes more male biased, males accordingly increased their acceptance of intrasexual competition. Females avoided groups of four males, and for both sexes, avoidance of male-biased courting groups increased their probability of amplexus courtship. We then isolated an approximately 33-kD protein from male cloacal glands that was used by males to compare OSRs. To our knowledge, this protein represents the first isolated and characterized component of an olfactory cue used to evaluate OSR. These results support two important principles regarding mating systems: (1) OSR can somewhat paradoxically be both the source imposing competition for mates and the source used to reduce it, and (2) analogous to the sex in short supply often being ‘‘choosy’’ selecting mates, the sex in excess (here, males) appears to be choosy about its acceptance of intrasexual competition.

Key words: chemical cues; mating competition; mating system; Notophthalmus viridescens; olfaction; operational sex ratio; pheromone; salamander; sexual selection; spatiotemporal variation.

 

 

Rohr, J.R., Elskus, A.A., Shepherd, B.S., Crowley, P.H., McCarthy, T.M., Niedzwiecki, J.H., Sager, T., Sih, A., Palmer, B.D. 2004. Multiple stressors and salamanders: Effects of an herbicide, food limitation, and hydroperiod. Ecological Applications. 14:1028-1040

Amphibian populations can be affected adversely by multiple biotic and abiotic stressors that together can contribute to their local and global decline. We focused on the combined effects of food limitation, drying conditions, and exposure to possibly the most abundant and widely used herbicide in the world, atrazine. We used a factorial design to evaluate the effects of exposure to four ecologically relevant doses of atrazine (approximate measured doses: 0, 4, 40, and 400 mg/L), two food levels (limited and unlimited food), and two hydroperiods (presence or absence of a dry down) on the survival, life history, and behavior of the streamside salamander, Ambystoma barbouri, from the embryo stage through metamorphosis. In general, food and atrazine levels did not interact statistically, and atrazine affected dependent variables in a standard, dose-dependent manner. Exposure to 400 mg/L of atrazine decreased embryo survival and increased time to hatching. Drying conditions and food limitation decreased larval survival, while 400 mg/L of atrazine only reduced larval survival in one of the two years tested, suggesting that the lethality of atrazine may be condition dependent. Sublethal effects included elevated activity and reduced shelter use associated with increasing concentrations of atrazine and food limitation. The larval period was lengthened by food limitation and shortened by 400 mg/L of atrazine. Drying conditions accelerated metamorphosis for larvae exposed to 0 and 4 mg/L of atrazine but did not affect timing of metamorphosis for larvae exposed to 40 or 400 mg/L of atrazine. Food limitation, drying conditions, and 400 mg/L of atrazine reduced size at metamorphosis without affecting body condition (relationship between mass and length), even though feeding rates did not differ significantly among atrazine concentrations at any time during development. This suggests that high atrazine levels may have increased larval energy expenditures. Because smaller size at metamorphosis can lower terrestrial survival and lifetime reproduction, resource limitations, drying conditions, and environmentally realistic concentrations of atrazine have the potential to contribute to amphibian declines in impacted systems.

Key words: Ambystoma barbouri; amphibian decline; atrazine; behavior; embryos; larvae; life history; metamorphosis; ontogeny; survival.

 

 

Sullivan, A.M.*, Madison, D.M., Rohr, J.R. 2004. Variation in the antipredator responses of three sympatric Plethodontid salamanders to predator-diet cues Herpetologica. 60:401-408

Organisms may reduce the risk of predation by responding to chemical cues from predators. Recent research shows that many species vary their antipredator response depending on the diet of the predator.We examined the responses of three plethodontid species of salamander (Plethodon cinereus, Eurycea
bislineata
, and Desmognathus ochrophaeus) to chemical cues from a shared snake predator (Thamnophis sirtalis). At the time of the study, Eurycea bislineata showed overlap in habitat with Plethodon cinereus and Desmognathus ochrophaeus, but Plethodon cinereus and Desmognathus ochrophaeus showed no overlap with one another. Each salamander species was presented with chemical cues from snakes fed Desmognathus ochrophaeus (TSDo), Eurycea bislineata (TSEb), and Plethodon cinereus (TSPc). Plethodon cinereus avoided both TSPc and TSEb, whereas Eurycea bislineata avoided only TSEb. Conversely, Desmognathus ochrophaeus did not avoid any cues from the predator, regardless of the diet of the snake. When we analyzed activity data, we discovered that Plethodon cinereus showed higher activity levels when exposed to TSPc than to the other cues. Individual Eurycea bislineata did not vary their activity to the three treatments. Lastly, Desmognathus ochrophaeus, which did not avoid any of the cues from the predator, were more active in response to TSDo and TSEb than to TSPc. These results show that phylogenetically related prey species may employ a variety of antipredator behaviors and suggest that discrimination of predator diet-cues may be linked to the degree of microhabitat overlap among the different prey species at the time of our study. Our study also highlights the importance of using multiple response variables when examining antipredator behavior.

Keywords: chemical cues; Desmognathus ochrophaeus; Eurycea bislineata; Plethodon cinereus; predator diet; predator-prey.

 

 

Sullivan, A.M., Madison, D.M., Rohr, J.R. 2004. The response of three Plethodontid salamander species to a common predator: Diet-related predator cues and community interactions. Herpetologica. 60:401-408

Organisms may reduce the risk of predation by responding to chemical cues from predators. Recent research shows that many species vary their antipredator response depending on the diet of the predator.We examined the responses of three plethodontid species of salamander (Plethodon cinereus, Eurycea bislineata, and Desmognathus ochrophaeus) to chemical cues from a shared snake predator (Thamnophis sirtalis). At the time of the study, Eurycea bislineata showed overlap in habitat with Plethodon cinereus and Desmognathus ochrophaeus, but Plethodon cinereus and Desmognathus ochrophaeus showed no overlap with one another. Each salamander species was presented with chemical cues from snakes fed Desmognathus ochrophaeus (TSDo), Eurycea bislineata (TSEb), and Plethodon cinereus (TSPc). Plethodon cinereus avoided both TSPc and TSEb, whereas Eurycea bislineata avoided only TSEb. Conversely, Desmognathus ochrophaeus did not avoid any cues from the predator, regardless of the diet of the snake. When we analyzed activity data, we discovered that Plethodon cinereus showed higher activity levels when exposed to TSPc than to the other cues. Individual Eurycea bislineata did not vary their activity to the three treatments. Lastly, Desmognathus ochrophaeus, which did not avoid any of the cues from the predator, were more active in response to TSDo and TSEb than to TSPc. These results show that phylogenetically related prey species may employ a variety of antipredator behaviors and suggest that discrimination of predator diet-cues may be linked to the degree of microhabitat overlap among the different prey species at the time of our study. Our study also highlights the importance of using multiple response variables when examining antipredator behavior.

Keywords: chemical cues; Desmognathus ochrophaeus; Eurycea bislineata; Plethodon cinereus; predator diet; predator-prey.

 

 

Rohr, J.R., Elskus, A.A., Shepherd, B.S., Crowley, P.H., McCarthy, T.M., Niedzwiecki, J.H., Sager, T., Sih, A., Palmer, B.D. 2003. The lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander, Ambystoma barbouri. Environmental Toxicology and Chemistry. 22:2385-2392

Agricultural contaminants may be contributing to worldwide amphibian declines, but little is known about which agrichemicals pose the greatest threat to particular species. One reason for this is that tests of multiple contaminants under ecologically relevant conditions are rarely conducted concurrently. In this study, we examined the effects of 37-d exposure to the agrichemicals atrazine (4, 40, and 400 mg/L), carbaryl (0.5, 5, and 50 mg/L), endosulfan (0.1, 1, and 10 mg/L for 31 d and 0.1, 10, and 100 mg/ L for the last 6 d), and octylphenol (5, 50, and 500 mg/L) and to a solvent control on streamside salamanders (Ambystoma barbouri) in the presence and absence of food. We found that none of the agrichemicals significantly affected embryo survival, but that hatching was delayed by the highest concentration of octylphenol. In contrast to embryos, larval survival was reduced by the highest concentrations of carbaryl, endosulfan, and octylphenol. Growth rates were lower in the highest concentrations of endosulfan and octylphenol than in all other treatments, and the highest concentration of endosulfan caused respiratory distress. Significantly more carbaryl, endosulfan, and octylphenol tanks had larvae with limb deformities than did control tanks. Refuge use was independent of chemical exposure, but 10 mg/L of endosulfan and 500 mg/L of octylphenol decreased larval activity. Systematically tapping tanks caused a greater activity increase in larvae exposed to 400 mg/L of atrazine and 10 mg/L of endosulfan relative to solvent controls, suggesting underlying nervous system malfunction. Hunger stimulated a decrease in refuge use and an increase in activity, but this response was least pronounced in larvae exposed to the highest concentration of any of the four agrichemicals, possibly because these larvae were the most lethargic. More studies are needed that concurrently examine the effect of multiple contaminants on amphibians so we can better identify effective mitigating measures.

Keywords: pesticide; amphibian survival; growth; behavior.

 

 

Rohr, J.R., Madison, D.M., Sullivan, A.M. 2003. On temporal variation and conflicting selection pressures: A test of theory using newts. Ecology. 84:1816-1826

Most studies that examine conflicting selection pressures hold resources and risks constant, despite their ubiquitous fluctuation. Since little is known about the consequences of neglecting this variation, we examined the temporal response of male red-spotted newts, Notophthalmus viridescens, to conflicting female pheromones and damage-release alarm chemicals signaling predation. After a single exposure in both the laboratory and field, males were attracted to female odor and avoided conspecific alarm chemicals. Response to these combined cues depended on time after exposure, with males initially avoiding, and then being attracted to, the cue combination. This response shift was due to the resource and risk declining at different rates, and female odor accelerating male recovery from antipredator behavior. In the laboratory, males suppressed activity when exposed to alarm chemicals alone but increased their activity when female odor was added. Iterative exposures through the breeding season revealed that, as male mate search activity declined, male avoidance of alarm chemicals increased, but alarm chemical production appeared unchanged. Thawing dates differed between ponds of the same and different populations, which offset levels of mate search activity and consequently alarm chemical avoidance. As a result, simultaneous pond surveys made it appear as though there was geographic variation in reproductive and predator-avoidance behaviors. However, when thawing dates were aligned, the time courses of reproductive and predator-avoidance behaviors for the ponds coincided, demonstrating that observed site differences were predominantly due to different behavioral onsets, which would have gone overlooked had the larger temporal scale not been considered. These results indicate that temporal variation can be easily mistaken for geographic variation in behavior, increasing the potential for data interpretation errors. These studies underscore the importance of considering temporal variation when examining conflicting selection pressures.

Keywords: amphibians; antipredator behavior; balancing conflicting demands; chemical cues; geographic variation; mating behavior; newts; Notophthalmus; recovery rate.

 

 

Sullivan, A.M., Madison, D.M., Rohr, J.R. 2003. Behavioural responses by red-backed salamanders to conspecific and heterospecific cues. Behaviour. 140:553-564

Chemical cues released from injured prey are thought to indicate the proximity of a predator or predation event, and therefore, an area of elevated predation risk. Prey often avoid chemical cues released from injured heterospecifics, but there is little evidence to determine whether this is due to homologous cues among phylogenetically related species, or avoidance of injured syntopic species that experience predation from the same predators. The purpose of this study was to examine the response of terrestrial red-backed salamanders (Plethodon cinereus) to chemical cues from non-injured and injured members of their prey guild that vary in their relatedness to P. cinereus. In the laboratory, P. cinereus avoided chemical cues from injured conspecifics, injured and non-injured slimy salamanders (P. glutinosus), and injured confamilial dusky salamanders (Desmognathus ochrophaeus). Red-backed salamanders did not avoid rinses from non-injured conspecifics and dusky salamanders, or cues from injured and non-injured earthworms (Lumbricus sp.), a more distantly related prey guild member. These results cannot be fully explained by either phylogenetic relatedness (among plethodontid salamanders) or prey guild membership alone. We suggest that a combination of these factors, and perhaps others, likely influenced the evolution of heterospecific alarm cue avoidance in the red-backed salamander.

 

 

Rohr, J.R., Madison, D.M. 2003. Dryness increases predation risk in efts: Support for an amphibian decline hypothesis. Oecologia. 135: 657-664

One hypothesis for amphibian declines is that increased dryness attributed to global climate change exposes amphibians to greater biotic threat and, consequently, greater mortality. But, little is known about behavioral responses of terrestrial amphibians to dry conditions alone or in combination with biotic threats. We used field observations and laboratory experiments to test the response of efts (terrestrial juveniles) of the eastern red-spotted newt, Notophthalmus viridescens, to separate and combined desiccation and predation risks. When only at risk of desiccation, efts moved into shade, traveled down slope, decreased activity, and adopted water conserving postures. Efts also significantly reduced the rate of water loss by huddling and were attracted to chemical cues from conspecific efts but not from conspecific adults. Thus, efts have a variety of behaviors that reduce the risk of dehydration associated with climate change. When faced only with a predation risk, represented by adult and eft newt tissue extracts (alarm chemicals), efts reduced their activity and avoided alarm cues from both sources. When exposed to combined desiccation and predation risks, efts were less active than when exposed to either risk separately and avoided adult tissue extracts, but not eft extracts. These results suggest that under dry conditions, conspecific tissue extracts contain both attractive (huddling) and repulsive (predator- related) chemical components that induce offsetting behavioral responses. This is the first study to demonstrate moisture-dependent responses to conspecific rinses and alarm substances, underscoring the importance of considering environmental moisture and animal hydration in studies examining responses to conspecific odors and/or alarm chemicals. These results support the hypothesis that elevated dehydration risk may compromise anti-predator behavior and exacerbate amphibian population declines.

Keywords: chemical cues; huddling; conflicting demands; individual variation and consistency; salamander.

 

 

Rohr, J.R. 2002. Temporal and spatial variation in newt (Notophthalmus viridescens) response to non-injured and injured conspecifics. Dissertation, Binghamton University

I examined red-spotted newt, Notophthalmus viridescens, responses to chemicals from injured conspecifics (alarm chemicals thought to signal foraging predators) and non-injured conspecifics at various temporal scales. During the breeding season, female odor accelerated male recovery from antipredator responses induced by alarm chemicals, such that male response depended on time after treatment exposure. As mate search activity and male attraction to females increased during the breeding season, male avoidance of conspecific alarm chemicals declined, but alarm chemical production appeared unchanged. Thawing dates differed between bordering subpopulations and between populations, which offset levels of mate search activity and consequently alarm chemical avoidance. As a result, simultaneously examining these sites made it appear as though there was significant geographic variation in newt activity and response to alarm chemical. However, upon aligning site thawing dates, activity and behavior across sites became strikingly similar, indicating that temporal variation can easily be mistaken for spatial variation.
            While males during the breeding season were attracted to both sexes, and on average did not avoid alarm chemical, females during the breeding season were indifferent to conspecifics of both sexes, and only avoided injured females. During the non-breeding season, both males and females were indifferent to conspecifics and avoided injured conspecifics, but the magnitude of male avoidance was almost significantly greater than female avoidance, suggesting sex differences in both the breeding and non-breeding seasons.
            When examining responses across ontogeny, recently-hatched predator-naïve and predator-experienced larvae decreased activity in response to odor from adults (frequent cannibals of larvae), but these larvae did not possess alarm chemicals. Adults and efts (terrestrial juveniles) were indifferent to non-injured, but avoided injured adults and efts in moist environments. Under dry conditions, efts were attracted to conspecific odors, which facilitated huddling and reduced evaporative water loss, but did not avoid injured conspecifics. Attraction to conspecifics in dry conditions likely compromised alarm chemical avoidance. Time in ontogeny, in a year, in a season, and after exposure to a predation stimulus all affected newt antipredator behavior emphasizing their extreme plasticity, but more importantly, the risks of misinterpreting biological systems if various temporal scales are not considered.

 

 

Rohr, J.R., Madison, D.M. 2002. Notophthalmus viridescens (Eastern Red-Spotted Newt) Predation. Herpetological Review. 33:122-123

NOTOPHTHALMUS VIRIDESCENS (Eastern Red-Spotted Newt). PREDATION. No significant predation on adult eastern red-spotted newts, Notophthalmus viridescens, has been documented in the wild. Natural predation on the toxic adult newts may help explain their cryptic dorsal coloration.
During late September 1998, two female newts were placed in a minnow trap over night in Binghamton University’s Nature Preserve pond (Broome County, NY), and one experienced limb and tail predation that provided the impetus for further investigation of newt predation. At 1700 h, on 25 September 2000 and 2 and 9 October 2000 at the same site, three newts were placed in each of nine minnow traps set 30-60 cm deep, and ca. 1.0 m from shore and 7 m apart. Trap checks at 1000 h the following mornings revealed no newt captures. On 26 September, two of the 27 newts had disappeared and 11 had serious or fatal injuries: all lost limbs (Fig. 1), four had partial or total tail loss, and one had only the spine, head, and dorsal skin remaining (Fig. 2). On 3 October, one of the 27 newts was missing and one had lost a limb. No newts were injured or missing on 10 October. The first frost of the year occurred between the first and second trapping sessions, and two frosts occurred between the second and third. Injuries appeared to have been inflicted from outside the traps since many newts were found with their bodies partially pulled through the trap mesh. The predation appears to be crepuscular or nocturnal, since we have over 1500 newt captures in 3000 hours of diurnal trapping (1000-1700 h) at the same population from March until June of 1999 and 2000 without an incident of predation (unpublished).
            These are the first observations of natural and significant predation on adult eastern red-spotted newts. Many predator species can be ruled out because they either are not found at our site (crayfish), were concurrently captured in traps with newts during the day without predation (fish, dragonfly larvae), repeatedly reject newts as food (fish, water snakes, garter snakes: Hurlbert 1970. J. Herpetol. 4:47-55), are diurnal foragers (painted turtles: Johnson 1997. The Amphibians and Reptiles of Missouri. Missouri Dept. Conserv., Jefferson City, Missouri. 163 pp.), or are incapable of removing newt limbs (water beetles and bugs have piercing mouthparts: Peckarsky et al. 1990. Freshwater Macroinvertebrates of Northeastern North America. Cornell University Press, Ithaca, New York.138 pp.). However, snapping turtles, Chelydra serpentina, have consumed adult newts and newt limbs in the laboratory (Hurlbert, op. cit.), and use a combination of sucking and rapid head movements to bite off sections of prey (Lagler 1943. Am. Midl. Nat. 29:257-312), which would be necessary to draw newt limbs through the trap mesh for seizing. Additionally, at a similar latitude (ca. 3º N, Ontario, Canada), they were crepuscular and entered winter dormancy as temperatures dropped during October, matching the timing of our predation declines (Obbard and Brooks 1981. Copeia 1981:630-637). Future studies will confirm whether snapping turtles consume newts in the wild.

 

 

Rohr, J.R., Madison, D.M., Sullivan, A.M. 2002. The ontogeny of chemically-mediated antipredator behaviours in newts (Notophthalmus viridescens): Responses to injured and non-injured conspecifics. Behaviour. 139:1043-1060

Responses to alarm chemicals from injured prey may influence predation risk and foraging success of receivers and senders, while learning can influence the strength of these responses. Thus, it is important to know when in ontogeny prey produce and detect alarm substances and how learning shapes their response, but surprisingly little is known about either of these topics. We assessed when in the life of red-spotted newts, Notophthalmus viridescens, alarm chemicals are produced and detected by comparing adult versus eft (terrestrial juveniles) and larval responses to rinses and tissue extracts from individuals in each life-history stage. To evaluate the influence of experience in larvae exposed to conspecific alarm substances and rinses from adults known to cannibalize larvae, we compared the response of naïve larvae, which had no prior experience with alarm chemicals or predators, to experienced larvae, which were likely to have experienced alarm chemicals and predators in their native pond. Larvae were indifferent to larval rinses and extracts, but reduced their activity in response to adult rinses and extracts. There was no difference between responses of recently hatched naïve and experienced larvae, indicating that larvae exhibit innate antipredator behaviors in response to adult odour. Adults were indifferent to all larval treatments and adult rinse, but avoided adult extract. Since neither adults nor larvae responded to larval extract, larvae did not appear to possess alarm chemicals, and consequently, we were unable to assess the influence of experience on alarm substance response in larvae. Adults and efts were indifferent to rinses, but avoided extracts from conspecifics of both life-history stages. Together, these results demonstrate that red-spotted newts do not produce alarm chemicals until late in larval development, but can respond to predation-related chemical cues soon after hatching.

 

 

Rohr, J.R., Madison, D.M., Sullivan, A.M. 2002. Sex differences and seasonal trade-offs in response to injured and non-injured conspecifics in red-spotted newts, Notophthalmus viridescens. Behavioral Ecology and Sociobiology. 52:385-393

Injured prey often release alarm chemicals that induce antipredator behaviors in conspecifics. Injured or killed prey most likely release a wide array of chemicals in addition to alarm substances, such as sexual pheromones, which could enhance or compromise antipredator responses. Thus, damage-release cues provide an excellent opportunity to examine the influence of seasonally fluctuating sexual pheromones on antipredator behaviors. We used a series of laboratory and field experiments and meta-analysis to examine seasonal changes and sex differences in the response of red-spotted newts, Notophthalmus viridescens, to the odor of non-injured conspecifics and conspecific tissue extracts, the latter of which presumably contain pheromones of non-injured conspecifics combined with alarm chemicals signaling predation. During the peak of the breeding season, males were attracted to females and multiple males, but did not avoid tissue extracts from either sex. As the breeding season waned, male attraction to females and males decreased, while avoidance of alarm extracts from both sexes concurrently increased. In contrast to male behavior, females were indifferent to both sexes during the breeding season, and showed significant avoidance only of female extract. As the breeding season progressed, females displayed no change in response to treatments. Male and female responses to female rinse and extract differed significantly, but their response to male treatments did not. During the nonbreeding season, both males and females were indifferent to the odor of conspecifics and avoided conspecific tissue extracts, with the magnitude of male avoidance greater than that of female avoidance, suggesting sex differences in response to alarm cues in both the breeding and non-breeding seasons. In general, both male and female response to conspecific odor and tissue extracts covaried positively, suggesting that social pheromones can be detected within conspecific macerates and compromise alarm-chemical avoidance. Many of the sex differences in both seasons are likely explained by selection pressures imposed on males to intensely mate search during the breeding season, suggesting that the mating system of newts directly influences predation threat during reproductive activity and may have significant indirect consequences on risk during the nonbreeding season.

Keywords: antipredator behavior; alarm chemical; seasonal variation; conflicting chemical cues; salamanders.

 

 

Madison, D.M., Sullivan, A.M., Maerz, J.C., McDarby, J.H., Rohr, J.R. 2002. A complex, cross-taxon, chemical releaser of anti-predator behavior in amphibians. Journal of Chemical Ecology. 28:2251-2262

Prey species show diverse antipredator responses to chemical cues signaling predation threat. Among terrestrial vertebrates, the red-backed salamander, Plethodon cinereus, is an important species in the study of these chemical defenses. During the day and early evening, this species avoids rinses from garter snakes, Thamnophis sirtalis, independent of snake diet, but late at night, avoids only those rinses from garter snakes that have recently eaten P. cinereus. We tested whether the selective, late-night response requires the ingestion or injury of salamanders. In three experiments, we tested P. cinereus for their responses to separate or combined rinses from salamanders (undisturbed, distressed, and injured P. cinereus) and snakes (unfed, earthworm fed, and salamander-fed T. sirtalis). When paired against a water control, only rinses from salamander-fed snakes were avoided. When salamander treatments (undisturbed or distressed) were combined with the snake treatments (unfed or earthworm-fed) and tested against a water control, the combinations elicited avoidance. When selected treatments were paired against the standard rinse from salamander-fed snakes, only the combined rinses from salamanders and snakes nullified the avoidance response to the standard rinse. These data reveal a prey defense mechanism involving chemical elements from both the predator and prey that does not require injury or ingestion of the prey in the formation of the cue.

Keywords: chemical cues; predation; scent; composition; alarm; synergism; defense; diet; salamander; Thamnophis sirtalis; Plethodon cinereus.

 

 

Rohr, J.R., Madison, D.M. 2001. A chemically-mediated trade-off between predation risk and mate search in newts. Animal Behaviour. 62:863-869

Previous studies have demonstrated that adult male red-spotted newts, Notophthalmus viridescens, are attracted to female sexual pheromones and avoid conspecific alarm substances that signal predation. In this study, we tested the response of red-spotted newts to different concentrations and combinations of macerated male newt extract (MNE) and gravid female odour in the laboratory and field. In the laboratory, males decreased their activity in response to MNE and showed an intermediate attraction (a trade-off) to female odour when paired with MNE. The intermediate attraction indicates that predators may inhibit mate search, and that male newts apparently take greater risks during the breeding season. Results from tests conducted at two sites within the same pond complex demonstrated plasticity in response to MNE. One site showed the laboratory trade-off between mate search and predator avoidance for males, while at the second site, no significant avoidance of MNE was detected for either sex. To explain the discrepancy in MNE avoidance between the sites we propose a trade-off that incorporates risk and resource sensitivity.

 

 

Rohr, J.R., Madison, D.M. 2001. Do newts avoid conspecific alarm substances: the predation hypothesis revisited. In: Chemical Signals in Vertebrates (Ed. by Marchlewska-Koj, L. & Müller- Schwarze, D.), NY: Kluwer Academic/Plenum Publishers, 295-304

Numerous amphibian species release and avoid alarm pheromones that signal predation. Recent laboratory and field experiments have demonstrated that adult male red-spotted newts, Notophthalmus viridescens, avoid extracts of the damaged skin of con-specifics, presumably to avoid predators. In this study, we tested the response of red-spotted newts to macerated conspecific male extract in the laboratory and at two locations within the same pond complex. Males avoided male newt extract in the laboratory, and for two successive years, avoidance was recorded in one pond but not in a contiguous side pond. Habitat features and newt and predator densities differed between the two sites. Lower predation risk was thought to compromise avoidance in the side pond.