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. |