Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations

Species may compete indirectly by altering the traits of a shared resource. For example, herbivore-induced responses in plants may make plants more resistant or susceptible to additional herbivorous insect species. Herbivore-induced plant responses can significantly affect interspecific competition and herbivore population dynamics. These herbivore-herbivore indirect interactions have been overlooked in aquatic ecosystems where previous studies used the same herbivore species to induce changes and to assess the effects of these changes. We asked whether seaweed grazing by one of two herbivorous, congeneric snail species (Littorina obtusata or Littorina littorea) with different feeding strategies and preferences would affect subsequent feeding preferences of three herbivore species (both snails and the isopod Idotea baltica) and population densities of three herbivore species (both snails and a third periwinkle snail, Lacuna vincta). In addition, we measured phlorotannin concentrations to test the hypothesis that these metabolites function as induced defenses in the Phaeophyceae. Snail herbivory induced cue-specific responses in apical tissues of the seaweed Fucus vesiculosus that affected the three herbivore species similarly. When compared to ungrazed controls, direct grazing by Littorina obtusata reduced seaweed palatability by at least 52% for both snail species and the isopod species. In contrast, direct grazing by L. littorea did not decrease seaweed palatability for any herbivore, indicating herbivore-specific responses. Previous grazing by L. obtusata reduced populations of L. littorea on outplanted seaweeds by 46% but had no effect on L. obtusata populations. Phlorotannins, a potential class of inducible chemicals in brown algae, were not more concentrated in grazed seaweed tissues, suggesting that some other trait was responsible for the induced resistance. Our results indicate that marine herbivores may compete via inducible responses in shared seaweeds. These plant-mediated interactions were asymmetric with a specialist (L. obtusata) competitively superior to a generalist (L. littorea).     

Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail

Geographic variability in abundance can be driven by multiple physical and biological factors operating at multiple scales. To understand the determinants of larval trematode prevalence within populations of the marine snail host Littorina littorea, we quantified many physical and biological variables at 28 New England intertidal sites. A hierarchical, mixed-effects model identified the abundance of gulls (the final hosts and dispersive agents of infective trematode stages) and snail size (a proxy for time of exposure) as the primary factors associated with trematode prevalence. The predominant influence of these variables coupled with routinely low infection rates (21 of the 28 populations exhibited prevalence <12%) suggest broad-scale recruitment limitation of trematodes. Although infection rates were spatially variable, formal analyses detected no regional spatial gradients in either trematode prevalence or independent environmental variables. Trematode prevalence appears to be predominantly determined by local site characteristics favoring high gull abundance.     

Anthropogenic influences on the infestation of intertidal gastropods by seabird trematode larvae on the southern Barents Sea coast

In this study we examined how the variation in the distribution of six species of seabird trematodes was influenced by human activities along the subarctic Barents Sea coast of northern Norway. This was done by comparing the prevalence of the parasites in two species of intermediate host (Littorinasaxatilis and Littorina obtusata) on seashores near fishing industry complexes, fish farms and at control sites. In L. saxatilis there were higher prevalences at sites influenced by human activities for three out of five trematode species (Microphallus piriformes,  M. similis, Cryptocotyle lingua) which have gulls (Larus spp.) as their predominant final hosts, while in L. obtusata, only  M. similis was more common at sites with human activity. For  M. pygmaeus, a trematode which has the common eider (Somateria mollissima) as its most predominant final host, the prevalence in L.␣saxatilis tended to be higher at sites with fishing industry, but differences were not significant. No such tendency was found in L. obtusata for this trematode. The overall prevalence in L. obtusata was lower than in L.␣saxatilis. This indicates that the vulnerability to trematode infection differs between the two snail species depending on the variation in the distribution patterns in the intertidal zone. Gulls tend to concentrate in areas near fishing industry and fish farms to feed on fish offal, which leads to an increase in the transmission between hosts, and to a higher level of parasite infection, locally. Received: 4 May 1998 / Accepted: 18 October 1998     

Relationships among three species of littorina and their larval digenea

The sympatric species Littorina saxatilis (Olivi), L. obtusata (L.), and L. littorea (L.) from the northeast coast of the USA were examined seasonally for larval trematodes. Snails were collected from two sites in Maine and one in Rhode Island. Eight species of Digenea were found: Microphallus pygmaeus (Levinsen, 1881), Microphallus similis (Jagerskiold, 1900), Microphallus sp., Cryptocotyle lingua (Creplin, 1825), Himasthla sp., Renicola roscovita (Stunkard, 1932), Podocotyle atomon (Rudolphi, 1809), and Cercaria lebouri (Stunkard, 1932). All 8 species were found to infect L. obtusata. Only Cercaria lebouri was absent from L. saxatilis. L. littorea was only infected with three species, M. pygmaeus, Cryptocotyle lingua, and R. roscovita. L. littorea does not appear to be a normal host for M. pygmaeus. Variation in occurrence and incidence of larval trematodes in snails from the three sites was related to the occurrence of the definitive hosts. Different seasonal variations in incidence of C. lingua and M. pygmaeus in L. obtusata and L. saxatilis were probably due to mortality of the snail hosts and the habits of the intermediate and definitive hosts. The incidence of C. lingua increased with increasing host size, but the incidence of M. pygmaeus reached a peak in smaller size classes. Although females were more abundant, significantly more male L. obtusata were infected at one Maine site.     

Morphologie,Entwicklung und Ökologie digener Trematoden-Larven der StrandschneckeLittorina littorea

More than 6000 individuals of the snailLittorina littorea L., from 6 different localities on the coast of the German Bay (North Sea), were examined for larval trematodes by crushing their shells, an additional 6000 by isolation in small quantities of sea water. Six species of larval trematodes were found inL. littorea and described: Notocotylid larva —Cercaria lebouri Stunkard, 1932; Cercaria ofHimasthla elongata (Mehlis, 1831); Cercaria ofPodocotyle atomon (Rudolphi, 1802); Cercaria ofRenicola roscovita (Stunkard, 1932) n. comb.; Metacercaria ofMicrophallus pygmaeus (Levinsen, 1881); Cercaria ofCryptocotyle lingua (Creplin, 1825). Considering the large number of investigated snails, the trematode fauna ofL. littorea in this area is assumed to be completely known. The life cycles ofHimasthla elongata andRenicola roscovita are described. Larvae of the different trematode species show differential preferences for distinct size groups of snail hosts. Juvenile snails are not infected. No correlation exists between infection rates and sex of the hosts. Quantitative aspects of multiple infections are calculated and discussed. The incidence of larval trematodes in the investigated localities differs. Information is presented on seasonal variations of infestations and their possible causes.     

Genetic evidence for the occurrence of a cryptic species with the littoral nemerteans Lineus ruber and L. viridis (Nemertea: Anopla)

Lineus ruber and L. viridis are common intertidal heteronemerteans found on the coasts of northern Europe and the east coast of North America. The two species resemble each other morphologically and were synonymised for many years prior to being separated on the basis of larval development. In this study, specimens of L. ruber and L. viridis were collected from sites along the west and southwest coast of Britain, northern France and the east coast of North America. The external morphology and allele frequencies of isozymes of the two species were compared from all sites. The external morphology of L. ruber and L. viridis was similar but they could generally be separated by colour. Allele frequencies for up to 13 enzyme loci between sympatric populations of L. ruber and L. viridis indicated that these two species are genetically very different (Nei's genetic identity=0.090 to 0.083). Allele-frequency data also indicated the presence of a third genetic type occurring sympatrically with populations of both L. ruber and L. viridis on the coasts of Britain and France but not on the coast of North America. Fixed differences in allele frequencies between populations of the third genetic type and sympatric populations of L. ruber and L. viridis were observed across multiple loci. Genetic identity between the third genetic type and sympatric populations of L. ruber and L. viridis were extremely low (Nei's genetic identity =<0.078). Such large genetic differences between populations indicate a barrier to gene flow and reproductive isolation. The aberrant type, which exhibits sufficient morphological variation to prevent individuals being distinguished from those of both L. ruber and L. viridis, therefore represents a separate species. The low genetic identities found in intrageneric comparisons of species found in this study have been found in other studies on nemerteans. They may indicate systematic problems within these groups or other phenomena such as morphological stasis.     

Allozymes and morphometric characters of three species ofMytilus in the Northern and Southern Hemispheres

Many authors have considered the common mussels in temperate waters of the Northern and Southern Hemispheres to be a single cosmopolitan species,Mytilus edulis Linnaeus, 1758. Others have divided these mussels into several subspecies or species. Samples of mussels were collected from 36 locations in the Northern Hemisphere and nine locations in the Southern Hemisphere. Electrophoretic evidence from eight loci indicates that the Northern Hemisphere samples consist of three electrophoretically distinguishable species:M. edulis from eastern North America and western Europe;M. galloprovincialis Lamarck, 1819 from the Mediterranean Sea, western Europe, California, and eastern Asia; andM. trossulus Gould, 1850 from the Baltic Sea, eastern Canada, western North America and the Pacific coast of Siberia. Mussels from Chile, Argentina, the Falkland Islands and the Kerguelen Islands contain alleles characteristic of all three Northern Hemisphere species, but because they are most similar toM. edulis from the Northern Hemisphere, we suggest that they tentatively be included inM. edulis. These South American samples are morphologically intermediate between Northern HemisphereM. edulis andM. trossulus. Mussels from Australia and New Zealand are similar in allele frequency and morphometric characters toM. galloprovincialis from the Northern Hemisphere. FossilMytilus sp. are present in Australia, New Zealand and South America, which suggests that the Southern Hemisphere populations may be native, rather than introduced by humans. Morphometric characters were measured on samples which the allozyme data indicated contained a single species. Canonical variates analysis of the morphometric characters yields functions which distinguish among our samples of the species in the Northern Hemisphere.     

Feeding preferences of periwinkles among four species ofFucus

A widely accepted view of intertidal community organizatiton in the NW Atlantic proposes that fucoid vegetation is maintained by the actions of predators which remove species competitively superior toFucus species. Herbivory is an important component of these predatory interactions, but has been studied largely with reference to the interaction betweenF. vesiculosus andLittorina littorea. There are many species of fucoids and herbivorous invertebrates on the shores of the NW Atlantic and this paper reports field and laboratory experiments performed in 1987 (in or near Halifax, Canada) on the effects of grazing by three species ofLittorina on adults and juveniles of four species ofFucus. In laboratory experiments, portions ofFucus species were presented singly (no choice) or together (multiple choice) to single species ofLittorina. AdultF. distichus was grazed to only a small extent.F. evanescens andF. vesiculosus adult tissues were heavily grazed in most laboratory experiments.F. spiralis adults were heavily grazed in no choice experiments, but were grazed only slightly in multiple choice tests. When adult fucoid tissues were exposed to a mixed suite of grazers in the field, onlyF. vesiculosus was grazed heavily. Tests done on adult tissues showed clearly thatFucus species are highly variable in their vunerability to grazers. Moreover, we found variability among periwinkle species in grazing rates on adultFucus. We also found a great disparity in the feeding rates of different periwinkle species on juveniles ofFucus. Therefore, it is not possible to extrapolate from a single periwinkle species/single fucoid species interaction when attempting to identify vegetation structuring processes.     

Parasites of the chaetognath Sagitta setosa in the western English Channel

The temporal occurrence of parasites in Sagitta setosa J. Müller, caught one to three times a month during 1982 and 1983 off Plymouth, England, was investigated. S. setosa was infected by eight parasitic species: one nematode, five trematodes, one cestode and, possibly, one protozoon. Infection by a single parasite, normally found in the body coelom, was the rule. The nematode Hysterothylacium aduncum, as III-stage larva, was by far the most common parasite (56% of all parasites found), followed by the metacercariae of three non-encysted trematodes: Derogenes varicus, a didymozoid species and a Lecithochirium species. Two trematode species new to Chaetognatha were found. The percentage of infected S. setosa specimens ranged from 0 to 7%. Absence or low numbers of parasites from June to November were correlated to the disappearance of large S. setosa and the appearance of a new S. setosa generation. Trematodes may show great annual and seasonal differences in occurrence in S. setosa. No injuries due to parasites were seen. The reproduction of the S. setosa populations off Plymouth did not seem to be affected by parasite infections during 1982–1983.     

Varying responses of northeastern North American amphibians to the chytrid pathogen Batrachochytrium dendrobatidis

Chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), is widespread among amphibians in northeastern North America. It is unknown, however, whether Bd has the potential to cause extensive amphibian mortalities in northeastern North America as have occurred elsewhere. In the laboratory, we exposed seven common northeastern North American amphibian species to Bd to assess the likelihood of population-level effects from the disease. We exposed larval wood frogs (Lithobates sylvaticus) and postmetamorphic frogs of six other species to two different strains of Bd, a northeastern strain (JEL404) and a strain that caused die-offs of amphibians in Panama (JEL423), under ideal in vitro growth conditions for Bd. Exposed American toads (Anaxyrus americanus) all died; thus, this species may be the most likely to die from Bd-caused disease in the wild. Both Bd strains were associated with mortalities of wood frogs, although half the metamorphs survived. The Bd strain from Panama killed metamorphic green frogs (L. clamitans), whereas the northeastern strain did not, which means novel strains of Bd may lead to death even when local strains may not. No mortality was observed in four species (bullfrogs [L. catesbeianus], northern leopard frogs [L. pipiens], spring peepers [Pseudacris crucifer], and blue-spotted salamanders [Ambystoma laterale]) and in some individuals of green frogs and wood frogs that we exposed. This finding suggests these six species may be Bd vectors. Our results show that systematic exposures of amphibian species to Bd in the laboratory may be a good first step in the identification of species susceptible to Bd-caused declines and in directing regional conservation efforts aimed at susceptible species.     

Effects of salinity on multiplication and transmission of an intertidal trematode parasite

Salinity levels vary spatially in coastal areas, depending on proximity to freshwater sources, and may also be slowly decreasing as a result of anthropogenic climatic changes. The impact of salinity on host–parasite interactions is potentially a key regulator of transmission processes in intertidal areas, where trematodes are extremely common parasites of invertebrates and vertebrates. We investigated experimentally the effects of long-term exposure to decreased salinity levels on output of infective stages (cercariae) and their transmission success in the trematode Philophthalmus sp. This parasite uses the snail Zeacumantus subcarinatus as intermediate host, in which it asexually produces cercariae. After leaving the snail, cercariae encyst externally on hard substrates to await accidental ingestion by shorebirds, which serve as definitive hosts. We found that at reduced salinities (25 or 30 psu), the cercarial output of the parasite was lower, the time taken by cercariae to encyst was longer, fewer cercariae successfully encysted and encysted parasites had lower long-term survival than at normal seawater salinity (35 psu). The strong effect of salinity on the replication and transmission of this parasite suggests that there may be sources and sinks of transmission to birds along coastal areas, depending on local salinity conditions. Also, unless it evolves to adapt to changing conditions, the predicted reduction in salinity as a consequence of climate change may have negative impact on the parasite’s abundance.     

Utilization of partially predated snail shells by the hermit crab Pagurus longicarpus Say, 1817

The hermit crab Pagurus longicarpus was shown to inhabit shells that were partially predated from intertidal areas of Long Island, New York. Among field collections of P. longicarpus, 2.13% of the hermit crabs (46 of 2155) were found with shells with snail tissue present. Over 90% of these partially predated snail shells were occupied by male hermit crabs. Although hermit crabs were in 8 species of snail shells, only Littorina littorea and Nassarius obsoletus were found occupied by hermit crabs and containing snail tissue. In the laboratory, we found that specimens of the spider crab Libinia emarginata were able to pull off the operculum of snails, leaving damage as found in field collections. In contrast, specimens of P. longicarpus were not able to prey on live, healthy snails. When specimens of P. longicarpus were placed in communal tanks, hermit crabs preferred partially predated snail shells to empty and original shells. However, original shells and empty shells were occupied with more frequency than partially predated shells when crabs were isolated. These findings indicate P. longicarpus actively seeks shells soon after attack and abandonment by snail predators, especially in the presence of competitors.     

Biochemical composition and energy reserves in the larvae and adults of the four british periwinkles Littorina littorea,L. littoralis,L. saxatilis and L. neritoides

The biochemical composition of the adult body tissue is similar in Littorina littorea, L. littoralis, L. saxatilis and L. neritoides. In the newly crawling metamorphosed young of L. littoralis and L. saxatilis, the biochemical composition is similar to that of the mature adults. The newly released planktonic veliger larvae of L. littorea and L. neritoides, which represent and earlier stage of development than the newly crawling young, have a neutral lipid level (mean, 16.5% of ash-free dry flesh weight) approximately three times the level (5.4%) in the newly crawling young of L. littoralis and L. saxatilis. Otherwise the biochemical composition of free-swimming larvae is similar to that of newly crawling young and adults. Neutral lipid is apparently utilised by L. littoralis and L. saxatilis larvae during larval development and metamorphosis. It is suggested that neutral lipid is the major energy reserve of Littorina veliger larvae whereas in the adults, as exemplified by L. littorea, both lipid and carbohydrate are important as energy reserves.     

Polychlorinated dibenzo‐p‐dioxins and dibenzofurans (PCDD/Fs) in dated environmental samples,and their connection to known sources

This article investigates available environmental data from measurements of the everywhere present contaminants polychlorinated dibenzo‐p‐dioxins and dibenzofurans (PCDD/F) in dated trends in sediment, soil and herbage from locales in Europe and North America. The PCDD/F data are examined in relation to potential major PCDD/F sources based on volume: wood and coal, example of natural combustion; pentachlorophenol (PnCP), example of chlorinated aro‐matics; and polyvinyl chloride (PVC) pyrolysis, example of chlorinated aliphatic. Collected PCDD/F data of congener sums and 2, 3, 7, 8‐substituted congener (PCDD/F profiles) have been investigated with multivariate methods: principal component analysis (PCA) and partial least squares projection to latent structures model (PLS). The results show that PCDD/F data from 12 locales can be separated in one to three independent profiles. Normally one profile is related to the PCDD/F found in PnCP and another to combustion. A subtype of the ‘PnCP’ and ‘combustion’ profiles indicates PCDD/F contributions from PVC‐related combustions. The environmental profiles exhibit some differences from the suggested sources. The relatively unprotected PCDD/F related to PnCP is suggested to have passed photolytic and/or thermal dechlorinations. Lower‐chlorinated congeners in environmental profiles related to combustion appear to have been influenced by environmental distribution processes. PCDD/F data before industrial production of chlorinated organics have only limited similarity to PCDD/F in technical PnCP profiles; an average 4.6% of the PCDD/F is related to PnCP. This suggests that PnCP similarity in recent deposition profiles cannot be a result of environmental transformation. The average proportion of PnCP‐related PCDD/F profile in recent depositions is 35% with North America high (average 57%) and Europe low (average 24%).     

Terrestrial liming benefits birds in an acidified forest in the northeast

Studies in Europe have reported negative effects of acid deposition on forest birds, and research in North America has identified links between forest bird abundance and rates of acid deposition. We examined the bird community in an acidified forest in central Pennsylvania (USA) and evaluated the effects of terrestrial lime application on birds. We used a before-after control-impact (BACI) study design, with one year of observation before (2003) and three years after lime application (2004, 2005, and 2006). Between the 2003 and 2004 field seasons, 4500 kg/ha of dolomitic lime were applied to two of four 100-ha watersheds. Each year, we monitored bird abundance and Ovenbird (Seiurus aurocapilla) eggshell thickness and territory size. Soil and snail abundance data were also collected. The bird community and territory size results indicated that the study area may be providing low-quality habitat for forest birds, perhaps as a result of acid deposition. We found lower forest bird abundances than have been found in less acidified areas of Pennsylvania, and larger Ovenbird territory sizes than have been found in other studies. We found a significant positive relationship between soil calcium and bird abundance, indicating that soil calcium may affect bird abundance. Liming increased soil calcium and pH and led to increased snail and bird abundances. After liming, bird abundance was positively related to snail abundance. No significant changes occurred in Ovenbird territory size or eggshell thickness. Our results suggest that acid deposition could be responsible for reduced bird abundance, and that liming is a potential mitigation technique.     

Plant invasions, generalist herbivores, and novel defense weapons

One commonly accepted mechanism for biological invasions is that species, after introduction to a new region, leave behind their natural enemies and therefore increase in distribution and abundance. However, which enemies are escaped remains unclear. Escape from specialist invertebrate herbivores has been examined in detail, but despite the profound effects of generalist herbivores in natural communities their potential to control invasive species is poorly understood. We carried out parallel laboratory feeding bioassays with generalist invertebrate herbivores from the native (Europe) and from the introduced (North America) range using native and nonnative tetraploid populations of the invasive spotted knapweed, Centaurea stoebe. We found that the growth of North American generalist herbivores was far lower when feeding on C. stoebe than the growth of European generalists. In contrast, North American and European generalists grew equally well on European and North American tetraploid C. stoebe plants, lending no support for an evolutionary change in resistance of North American tetraploid C. stoebe populations against generalist herbivores. These results suggest that biogeographical differences in the response of generalist herbivores to novel plant species have the potential to affect plant invasions.     

Regulation of intertidal food webs by avian predators on New England rocky shores

Although there is a large body of research on food webs in rocky intertidal communities, most of the emphasis has been on the marine benthic components. Effects of avian predation on highly mobile predators such as crabs, remains practically unstudied in rocky shore ecosystems. The crab, Cancer borealis, is an important component of the diet of gulls (Larus marinus, L. argentatus) at the Isles of Shoals, Maine, USA. C. borealis prey include the predatory gastropod Nucella lapillus L., the herbivore Littorina littorea, and mussels Mytilus edulis L. We hypothesized that gulls reduce abundance of C. borealis in the low intertidal and shallow subtidal, thereby allowing C. borealis prey to persist in high numbers. A study of crab tidal migration showed that C. borealis density nearly doubled at high tide compared to low tide; thus, crabs from a large subtidal source population migrate into the intertidal zone during high tides and either emigrate or are removed by gulls during low tides. Results from a small-scale (1 m2) predator caging experiment in the low intertidal zone indicated that enclosed crabs significantly reduced L. littorea abundance when protected from gull predation. In a much larger-scale gull exclusion experiment, densities of C. borealis increased significantly during low and high tides in exclosures relative to the controls. C. borealis density was inversely correlated with changes in the abundance of two mesopredators Carcinus maenas and Nucella lapillus, and with the space-occupier M. edulis. There was a similar negative correlation between abundance of C. borealis and the change in abundance of the herbivore L. littorea, but the trend was not significant. Mortality of tethered L. littorea was associated with C. borealis density across sites. However, preferred algae did not change in response to L. littorea density during the experiment. Thus, we found suggestive, but not conclusive, evidence for a three-level cascade involving gulls, crabs, and L. littorea. Our studies strongly suggest that gulls, as apex predators, generate three-level trophic cascades in rocky intertidal food webs by preventing the highly mobile subtidal predator, C. borealis, from establishing substantial populations in the low-mid intertidal zone thereby indirectly enhancing densities of two key mesopredators (N. lapillus, Carcinus) and blue mussels (M. edulis).     

Predicting Invasions of Woody Plants Introduced into North America

Plant species continue to be introduced in North America for various purposes. If the trend continues, it is probable that some will escape cultivation and become invasive in native ecosystems. We present a retrospective analysis of several structural, life history, and biogeographical attributes of woody plants introduced in North America to determine which traits characterize species that have and have not invaded. Predictive models derived from discriminant analysis correctly classified 86.2% of the species in cross-validation, whereas those derived from classification and regression trees classified 76% correctly. From these models we created a hierarchical predictive tree that allows the user to divide species into three categories: admit (low risk of invasiveness), deny admission (high risk of invasiveness), or delay admission for further analyses and/or monitor intensively (risk cannot adequately be assessed based on only the included attributes). We recommend that species that are highly invasive elsewhere not be allowed into the U.S. and that a more conservative introduction policy using a hierarchical predictive method be employed.     

Patterns of mtDNA diversity in North Atlantic populations of the mussel Mytilus edulis

Patterns of (female) mitochondrial DNA diversity were investigated in the blue mussel Mytilus edulis. Mytilus edulis is a ubiquitous member of contemporary North Atlantic hard-substrate communities and well represented in studies of this region. Mytilus edulis was surveyed in North America and Europe, as well as mid-Atlantic sites in Greenland, Iceland, and the Faroe Islands. Mitochondrial DNA sequences revealed considerable population structure but no monophyly of haplotypes between any major regions. Coalescent analyses suggest that migration across the Atlantic Ocean has prominently been from North American source populations and that Greenland was colonized recently and exclusively from North America. In North America, there was support for two regional groups along the North American coastline. Surprisingly, we also found evidence of recombination between some Mytilus edulis and Mytilus galloprovincialis female mtDNA sequences, particularly in northern Europe. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. An erratum to this article can be found at     

Understanding the net effects of pesticides on amphibian trematode infections

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 microg/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 = 267 mg/L) and then only at concentrations greater than commonly found in aquatic ecosystems (> or =200 microg/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 pesticide-induced 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.