Development and evaluation of real‐time PCR assays for bloodmeal identification in Culicoides midges

Culicoides (Diptera: Ceratopogonidae) midges are the biological vectors of a number of arboviruses of veterinary importance. However, knowledge relating to the basic biology of some species, including their host‐feeding preferences, is limited. Identification of host‐feeding preferences in haematophagous insects can help to elucidate the transmission dynamics of the arboviruses they may transmit. In this study, a series of semi‐quantitative real‐time polymerase chain reaction (qPCR) assays to identify the vertebrate host sources of bloodmeals of Culicoides midges was developed. Two pan‐reactive species group and seven species‐specific qPCR assays were developed and evaluated. The assays are quick to perform and less expensive than nucleic acid sequencing of bloodmeals. Using these assays, it was possible to rapidly test nearly 700 blood‐fed midges of various species from several geographic locations in Australia.     

Foraging Ecology of Fall-Migrating Shorebirds in the Illinois River Valley

Populations of many shorebird species appear to be declining in North America, and food resources at stopover habitats may limit migratory bird populations. We investigated body condition of, and foraging habitat and diet selection by 4 species of shorebirds in the central Illinois River valley during fall migrations 2007 and 2008 (Killdeer [Charadrius vociferus], Least Sandpiper [Calidris minutilla], Pectoral Sandpiper [Calidris melanotos], and Lesser Yellowlegs [Tringa flavipes]). All species except Killdeer were in good to excellent condition, based on size-corrected body mass and fat scores. Shorebird diets were dominated by invertebrate taxa from Orders Diptera and Coleoptera. Additionally, Isopoda, Hemiptera, Hirudinea, Nematoda, and Cyprinodontiformes contribution to diets varied by shorebird species and year. We evaluated diet and foraging habitat selection by comparing aggregate percent dry mass of food items in shorebird diets and core samples from foraging substrates. Invertebrate abundances at shorebird collection sites and random sites were generally similar, indicating that birds did not select foraging patches within wetlands based on invertebrate abundance. Conversely, we found considerable evidence for selection of some diet items within particular foraging sites, and consistent avoidance of Oligochaeta. We suspect the diet selectivity we observed was a function of overall invertebrate biomass (51.2±4.4 [SE] kg/ha; dry mass) at our study sites, which was greater than estimates reported in most other food selection studies. Diet selectivity in shorebirds may follow tenants of optimal foraging theory; that is, at low food abundances shorebirds forage opportunistically, with the likelihood of selectivity increasing as food availability increases. Nonetheless, relationships between the abundance, availability, and consumption of Oligochaetes for and by waterbirds should be the focus of future research, because estimates of foraging carrying capacity would need to be revised downward if Oligochaetes are truly avoided or unavailable for consumption.     

Foraging Ranges of Immature African White-Backed Vultures (Gyps africanus) and Their Use of Protected Areas in Southern Africa

Vultures in the Gyps genus are declining globally. Multiple threats related to human activity have caused widespread declines of vulture populations in Africa, especially outside protected areas. Addressing such threats requires the estimation of foraging ranges yet such estimates are lacking, even for widespread (but declining) species such as the African white-backed vulture (Gyps africanus). We tracked six immature African white-backed vultures in South Africa using GPS-GSM units to study their movement patterns, their use of protected areas and the time they spent in the vicinity of supplementary feeding sites. All individuals foraged widely; their combined foraging ranges extended into six countries in southern Africa (mean (± SE) minimum convex polygon area  = 269,103±197,187 km²) and three of the vultures travelled more than 900 km from the capture site. All six vultures spent the majority of their tracking periods outside protected areas. South African protected areas were very rarely visited whereas protected areas in northern Botswana and Zimbabwe were used more frequently. Two of the vultures visited supplementary feeding sites regularly, with consequent reduced ranging behaviour, suggesting that individuals could alter their foraging behaviour in response to such sites. We show that immature African white-backed vultures are capable of travelling throughout southern Africa, yet use protected areas to only a limited extent, making them susceptible to the full range of threats in the region. The standard approach of designating protected areas to conserve species is unlikely to ensure the protection of such wide-ranging species against threats in the wider landscape.     

Are Bogs Reservoirs for Emerging Disease Vectors? Evaluation of Culicoides Populations in the Hautes Fagnes Nature Reserve (Belgium)

Several species of Culicoides (Diptera: Ceratopogonidae) biting midges serve as biological vectors for the bluetongue virus (BTV) and the recently described Schmallenberg virus (SBV) in northern Europe. Since their recent emergence in this part of the continent, these diseases have caused considerable economic losses to the sheep and cattle industries. Much data is now available that describe the distribution, population dynamics, and feeding habits of these insects. However, little is known regarding the presence of Culicoides in unusual habitats such as peaty marshes, nor their potential vector capacity. This study evaluated Culicoides biting midges present in the bogs of a Belgian nature reserve compared to those residing at a nearby cattle farm. Culicoides were trapped in 2011 at four different sites (broadleaved and coniferous forested areas, open environments, and at a scientific station) located in the Hautes Fagnes Nature Reserve (Belgium). An additional light trap was operated on a nearby cattle farm. Very high numbers of biting midges were captured in the marshy area and most of them (70 to 95%) were Culicoides impunctatus, a potential vector of BTV and other pathogens. In addition, fewer numbers of C. obsoletus/C. scoticus species, C. chiopterus, and C. dewulfi were observed in the bogs compared to the farm. The wet environment and oligotrophic nature of the soil were probably responsible for these changes in the respective populations. A total of 297,808 Culicoides midges belonging to 27 species were identified during this study and 3 of these species (C. sphagnumensis, C. clintoni and C. comosioculatus) were described in Belgium for the first time.     

The sound of a blood meal: Acoustic ecology of frog‐biting midges (Corethrella) in lowland Pacific Costa Rica

Animal communication systems are often exploited by eavesdropping antagonists, especially predators and ectoparasites. Female frog‐biting midges (Diptera: Corethrellidae) are known to use male anuran advertisement calls to locate their blood hosts, frogs. Here, we use acoustic midge traps broadcasting synthetic and recorded calls to identify those frog call parameters that affect midge attraction. At our study site in Pacific lowland Costa Rica, we found that overall midge attraction was influenced by both spectral and temporal acoustic parameters. Low dominant frequencies (below 1 kHz) and short pulse durations (between 125 and 500 ms) attracted the highest numbers of midges in tests with synthetic sinusoidal pure tones. These preferences partially explained the relative attractiveness of the advertisement calls of ten local frog species. The advertisement calls of the common and widespread Giant Bullfrog, Leptodactylus savagei (Anura: Leptodactylidae), attracted by far the largest number of midges, suggesting that this frog species might be a key resource for frog‐biting midges in Costa Rica. Although we found that calls of different frog species attracted different midge species/morphospecies in statistically different proportions, acoustic niche differentiation among midge species appeared to be moderate, suggesting either a limited degree of host specialization or the use of additional short‐range, that is, chemical, host recognition cues.     

Defects in Host Immune Function in Tree Frogs with Chronic Chytridiomycosis

The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has caused mass mortality leading to population declines and extinctions in many frog species worldwide. The lack of host resistance may be due to fungal immunosuppressive effects that have been observed when Bd is incubated with cultured lymphocytes, but whether in vivo host immunosuppression occurs is unknown. We used a broad range of hematologic and protein electrophoresis biomarkers, along with various functional tests, to assess immune competence in common green (Litoria caerulea) and white-lipped (L. infrafrenata) tree frogs experimentally infected with Bd. Compared with uninfected frogs, Bd infection in L. caerulea caused a reduction in immunoglobulin and splenic lymphocyte responses to antigenic stimulation with sheep red blood cells, along with decreased white blood cell and serum protein concentrations, indicating possible impaired immune response capability of Bd-infected frogs. This is the first in vivo study suggesting that infection with Bd causes multiple defects in systemic host immune function, and this may contribute to disease development in susceptible host species. Although L. infrafrenata failed to maintain Bd infection after exposure, white blood cell and serum globulin concentrations were lower in recovered frogs compared with unexposed frogs, but antigen-specific serum and splenic antibody, and splenic cellular, responses were similar in both recovered and unexposed frogs. This may indicate potential systemic costs associated with infection clearance and/or redirection of host resources towards more effective mechanisms to overcome infection. No clear mechanism for resistance was identified in L. infrafrenata, suggesting that localized and/or innate immune defense mechanisms may be important factors involved in disease resistance in this species.     

Cues used in host‐seeking behavior by frog‐biting midges (Corethrella spp. Coquillet)

We investigated the role of carbon dioxide and host temperature in host attraction in frog‐biting midges (Corethrella spp). In these midges, females are known to use frog calls to localize their host, but the role of other host‐emitted cues has yet not been investigated. We hypothesized that carbon dioxide acts as a supplemental cue to frog calls. To test this hypothesis, we determined the responses of the midges to carbon dioxide, frog calls, and both cues. A significantly lower number of midges are attracted to carbon dioxide and silent traps than to traps broadcasting frog calls. Adding carbon dioxide to the calls does not increase the attractiveness to the midges. Instead, carbon dioxide can have deterrent effects on frog‐biting midges. Temperature of calling frogs is not a cue potentially available to the midges. Contrary to our hypothesis, there was no supplemental effect of carbon dioxide when presented in conjunction to calls. Midge host‐seeking behavior strongly depends on the mating calls emitted by their anuran host. Overall, non‐acoustic cues such as host body temperature and carbon dioxide are not important in long‐distance host location by frog‐biting midges.     

Behavioural tactics used by invasive cane toads (Rhinella marina) to exploit apiaries in Australia

Behavioural flexibility plays a key role in facilitating the ability of invasive species to exploit anthropogenically‐created resources. In Australia, invasive cane toads (Rhinella marina) often gather around commercial beehives (apiaries), whereas native frogs do not. To document how toads use this resource, we spool‐tracked cane toads in areas containing beehives and in adjacent natural habitat without beehives, conducted standardized observations of toad feeding behaviour, and ran prey‐manipulation trials to compare the responses of cane toads versus native frogs to honeybees as potential prey. Toads feeding around beehives travelled shorter distances per night, and hence used different microhabitats, than did toads from nearby control sites without beehives. The toads consumed live bees from the hive entrance (rather than dead bees from the ground), often climbing on top of one another to gain access to the hive entrance. Prey manipulation trials confirm that bee movement is the critical stimulus that elicits the toads’ feeding response; and in standardized trials, native frogs consumed bees less frequently than did toads. In summary, cane toads flexibly modify their movements, foraging behaviour and dietary composition to exploit the nutritional opportunities created by commercial beehives, whereas native anurans do not.     

Distribution Patterns Predict Individual Specialization in the Diet of Dolphin Gulls

Many animals show some degree of individual specialization in foraging strategies and diet. This has profound ecological and evolutionary implications. For example, populations containing diverse individual foraging strategies will respond in different ways to changes in the environment, thus affecting the capacity of the populations to adapt to environmental changes and to diversify. However, patterns of individual specialization have been examined in few species. Likewise it is usually unknown whether specialization is maintained over time, because examining the temporal scale at which specialization occurs can prove difficult in the field. In the present study, we analyzed individual specialization in foraging in Dolphin Gulls Leucophaeus scoresbii, a scavenger endemic to the southernmost coasts of South America. We used GPS position logging and stable isotope analyses (SIA) to investigate individual specialization in feeding strategies and their persistence over time. The analysis of GPS data indicated two major foraging strategies in Dolphin Gulls from New I. (Falkland Is./Islas Malvinas). Tagged individuals repeatedly attended either a site with mussel beds or seabird and seal colonies during 5 to 7 days of tracking. Females foraging at mussel beds were heavier than those foraging at seabird colonies. Nitrogen isotope ratios (δ¹⁵N) of Dolphin Gull blood cells clustered in two groups, showing that individuals were consistent in their preferred foraging strategies over a period of at least several weeks. The results of the SIA as well as the foraging patterns recorded revealed a high degree of specialization for particular feeding sites and diets by individual Dolphin Gulls. Individual differences in foraging behavior were not related to sex. Specialization in Dolphin Gulls may be favored by the advantages of learning and memorizing optimal feeding locations and behaviors. Specialized individuals may reduce search and handling time and thus, optimize their energy gain and/or minimize time spent foraging.     

Influence of Resource Availability on the Foraging Strategies of the Triangle Butterflyfish Chaetodon triangulum in the Maldives

Obligate coral feeders such as many members of the Chaetodontidae family (also known as butterflyfish) often show strong preferences for particular coral species. This is thought to have evolved through natural selection as an energy-maximising strategy. Although some species remain as highly specialised feeders throughout their lifetime, many corallivores show a degree of dietary versatility when food abundance is limited; a strategy described by the optimal foraging theory. This study aimed to examine if, within-reef differences in the feeding regime and territory size of the Triangle Butterflyfish Chaetodon triangulum occurred, as a function of resource availability. Results showed that the dietary specialisation of C. triangulum was significant in both areas of low and high coral cover (χL2² = 2.52 x 102, P<0.001 and χL2² = 3.78 x 102, P<0.001 respectively). Resource selection functions (RSFs), calculated for the two main sites of contrasting coral assemblage, showed that in the resource-rich environments, only two Genera (Acropora and Pocillopora) were preferentially selected for, with the majority of other corals being actively ‘avoided’. Conversely, in territories of lower coral coverage, C. triangulum was being less selective in its prey choice and consuming corals in a more even distribution with respect to their availability. Interestingly, coral cover appeared to show no significant effect on feeding rate, however it was a primary determinant of territory size. The findings of the study agree with the predictions of the optimal foraging theory, in that where food supply is scarce, dietary specialisation is minimised and territory size increased. This results in maximising energy intake. This study represents the first scientific evidence that C. triangulum is an obligate corallivore and, as with many other butterflyfish, is therefore dependent on healthy scleractinian corals for survival.     

Sensilla coeloconica ringed by microtrichia in host‐seeking biting midges

The distribution and morphology of antennal sensilla coeloconica in parasitic and predaceous biting midges were studied in females of Forcipomyia (feeding on the blood of frogs), Atrichopogon (feeding on haemolymph), Austroconops, Culicoides (feeding on the blood of birds and mammals) and Brachypogon (feeding on haemolymph and dissolved tissues of insects) (all: Diptera: Ceratopogonidae). A Lower Cretaceous female of Archiculicoides (Diptera: Ceratopogonidae) from Lebanese amber, which fed on the blood of unknown vertebrates, was also examined. In sensilla coeloconica ringed by microtrichia, the peg is grooved longitudinally and protrudes distinctly from the pit. We suggest that the microtrichia encircling the protruding peg form a structure resembling a picket fence in order to maintain a higher level of humidity, which facilitates the capture and transport of odour molecules through the channels in the peg wall. Sensilla coeloconica ringed by microtrichia function as very effective chemoreceptors in host‐ and prey‐seeking activity. During the evolution of Ceratopogonidae, sensilla coeloconica with a fence of microtrichia have evolved twice in groups feeding on the blood of vertebrates (i.e. in the basal lineage: Lower Cretaceous or earlier) and in the subgenus Lasiohelea of Forcipomyia (Palaeogene). Sensilla coeloconica ringed by microtrichia are described for the first time in the relict genus Austroconops.     

Green Frogs Show Reduced Foraging Success in Habitats Invaded by Japanese knotweed

Habitat loss is causing amphibian population declines worldwide, so there is increased attention to forces that degrade remaining habitats. Terrestrial habitats surrounding wetlands are critical foraging areas for temperate anurans. We investigated plant community changes in two old fields invaded by Japanese knotweed (Fallopia japonica) and the foraging success of Green frogs (Rana clamitans) in invaded and non-invaded portions of those fields. Within each field, vegetation data were recorded in quadrats located along two transects bisecting the invasion fronts. We placed frogs in ‘foraging buckets’ along transects and measured their change in mass over a 38 h period. There were significant changes in vegetation structure and composition associated with Japanese knotweed invasion. Diverse assemblages of native plants that covered non-invaded plots were absent from areas invaded by Japanese knotweed. There was also a significant change in vegetation architecture between invaded and non-invaded habitats. Change in frog mass declined significantly along transects, with most frogs in non-invaded plots gaining mass and no frogs in invaded plots gaining mass. Most frogs from non-invaded plots but only two from invaded plots defecated shortly after removal from foraging buckets (verification of recent feeding). We hypothesize that Japanese knotweed invasions degrade terrestrial habitat quality for frogs by indirectly reducing arthropod abundance. Nonnative plant invasions may be another factor contributing to amphibian population declines.     

What you need is what you eat? Prey selection by the bat Myotis daubentonii

Optimal foraging theory predicts that predators are selective when faced with abundant prey, but become less picky when prey gets sparse. Insectivorous bats in temperate regions are faced with the challenge of building up fat reserves vital for hibernation during a period of decreasing arthropod abundances. According to optimal foraging theory, prehibernating bats should adopt a less selective feeding behaviour – yet empirical studies have revealed many apparently generalized species to be composed of specialist individuals. Targeting the diet of the bat Myotis daubentonii, we used a combination of molecular techniques to test for seasonal changes in prey selectivity and individual‐level variation in prey preferences. DNA metabarcoding was used to characterize both the prey contents of bat droppings and the insect community available as prey. To test for dietary differences among M. daubentonii individuals, we used ten microsatellite loci to assign droppings to individual bats. The comparison between consumed and available prey revealed a preference for certain prey items regardless of availability. Nonbiting midges (Chironomidae) remained the most highly consumed prey at all times, despite a significant increase in the availability of black flies (Simuliidae) towards the end of the season. The bats sampled showed no evidence of individual specialization in dietary preferences. Overall, our approach offers little support for optimal foraging theory. Thus, it shows how novel combinations of genetic markers can be used to test general theory, targeting patterns at both the level of prey communities and individual predators.     

Selective Defecation and Selective Foraging: Antiparasite Behavior in Wild Ungulates?

Selective defecation and selective foraging are two potential antiparasite behaviors used by grazing ungulates to reduce infection by fecal–oral transmitted parasites. While there is some evidence that domestic species use these strategies, less is known about the occurrence and efficacy of these behaviors in wild ungulates. In this study, I examined whether wild antelope use selective defecation and selective foraging strategies to reduce exposure to gastrointestinal nematode parasites. By quantifying parasite levels in the environment in relation to the defecation patterns of three species, dik‐dik (Madoqua kirkii), Grant's gazelle (Gazella granti), and impala (Aepyceros melampus), I found that nematode larval concentrations in pasture were higher in the vicinity of clusters of feces (dung middens) compared to single fecal pellet groups or dung‐free areas. In addition, experimental feeding trials in free‐ranging dik‐dik showed that individuals selectively avoided feeding near concentrations of feces. Given that increased parasite contamination was found in the immediate vicinity of fecal clusters, fecal avoidance could help reduce host consumption of parasites and may therefore be an effective antiparasite behavior for certain species. On the other hand, while the concentration of parasite larvae in the vicinity of middens coupled with host avoidance of these areas during grazing could reduce host contact with parasites, results showing a positive correlation between the number of middens in a habitat and larval abundance at control sites suggest that dung middens might increase and not decrease overall host exposure to parasites. If this is the case, dung midden formation may not be a viable antiparasite strategy.     

Discovery of cryptic diversity in phytophagous gall midges (Diptera: Cecidomyiidae) associated with different ecotypes of the perennial herb Cimicifuga simplex

Studying the diversification patterns of species-rich phytophagous insect taxa can help us understand the factors that cause species diversification. We conducted a molecular phylogenetic analysis of the mitochondrial COI gene of larvae of gall midges (Diptera: Cecidomyiidae) using three genetically differentiated morphs of Cimicifuga simplex plants and found that the gall midges could be divided into five major clades. Gall midges collected from morph I of C. simplex belonged to four Schizomyia clades. Gall midges collected from morph II of C. simplex belonged to one of the four Schizomyia clades collected from morph I. Gall midges collected from morph III belonged one Contarinia clade. On morphs I and II of C. simplex, the Schizomyia species induced galls on the flower bud, whereas on morph III of C. simplex, the Contarinia species was collected from normal fruits (not gall inducer); thus, morph III plants were used differently by gall midges than plants of morphs I and II. These results indicate that the cryptic diversity of these phytophagous insects correspond to that of plant ecotypes, and suggests that the diversification of the host plant contributed to parallel diversification of the phytophagous gall midges.     

Relationships between environmental gradients and geographic variation in the intraspecific body size of three species of frogs (Anura)

The relationship between environmental gradients and patterns of geographic variation in body size has been a controversial topic for ectothermic organisms globally. To examine whether the patterns that generally hold in more temperate species also hold for tropical ones, we examined the intraspecific body size variation in three species of Neotropical frogs, Dendropsophus minutus, Hypsiboas faber and Physalaemus cuvieri, along different environmental gradients (e.g. temperature, precipitation and topography). We analysed four competing hypotheses: (i) the water availability hypothesis that predicts a negative relationship between body size and precipitation; (ii) the heat balance hypothesis that predicts a negative relationship between body size and temperature; (iii) the topography hypothesis that predicts a negative relationship between body size and altitude; and (iv) the mixed‐effect hypothesis that predicts that individuals occurring in wet and cold sites would be larger than individuals occurring in dry and warm sites. The spatial pattern of geographic variation in body size among populations of H. faber was associated with the mixed‐effect hypothesis. In localities with low precipitation seasonality and cold conditions, H. faber individuals were larger than in localities with high precipitation seasonality and warm conditions. Variation in the body size of D. minutus was the opposite of that predicted by the heat balance hypothesis. Individuals in localities with high temperatures were larger than in localities with low temperatures. On the other hand, variation in the body size of P. cuvieri was not associated with the variables used in this study. Our results suggest that intraspecific variation in anuran body size is more dependent on species‐specific response than on the region (i.e. temperate or tropical) where they occur.     

Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad)

Predictions from foraging theory suggest that the probability a native predator will incorporate a novel type of prey (such as an invasive species) into its diet depends upon the potential benefits (e.g., nutrient input) vs. costs (e.g., handling time) of ingesting it. Cane toads (Bufo marinus) were introduced to Australia in 1935 and are highly toxic to many frog-eating snakes, thus there was strong selection to delete toads from the diet of these species. What has happened, however, to the feeding responses of an Australian snake species that is able to consume toads without dying? Our field surveys in northeastern Queensland show that, despite their high tolerance to toad toxins (compared to other native snakes), keelbacks (Tropidonophis mairii) feed primarily on native frogs rather than cane toads. This pattern occurs because the snakes show active prey preferences; even under standardized conditions in the laboratory, snakes are more likely to consume frogs than toads. When they are force-fed, snakes frequently regurgitate toads but not frogs. Thus, despite the high availability of the abundant toads, these invasive anurans are largely avoided as prey. This probably occurs because consumption of toads, although not lethal to keelbacks, causes significant sublethal effects and confers little nutritional benefit. Hence, keelback populations are not threatened by toad invasion, but neither do the snakes benefit substantially from the availability of a new type of potential prey.     

Assessment of Survival and Body Size Variation of Culicoides imicola (Diptera: Ceratopogonidae) as Functions of “Candidatus Cardinium” (Bacteroidetes) Infection Status

“Candidatus Cardinium hertigii” (Bacteroidetes) is a maternally inherited endosymbiont known from several arthropods. Its mechanisms for persistence in host populations are mostly reproductive manipulation, though it has been occasionally reported to improve fitness parameters in several hosts. In Culicoides (Diptera: Ceratopogonidae) biting midges, the prevalence of “Candidatus Cardinium” infection was documented as moderate, with no detectable sex bias. We therefore investigated whether “Candidatus Cardinium” affects important fitness parameters, such as survival and body size, in Culicoides imicola, a dominant vector species. Field-collected midges were trapped and analyzed for survival under different environmental conditions and antibiotic treatment, taking into account “Candidatus Cardinium” infection status and parity status (i.e., parous or nulliparous). Additionally, wing lengths were measured as a proxy parameter for body size and analyzed together with “Candidatus Cardinium” infection data. The findings revealed no difference in survival of Culicoides infected with “Candidatus Cardinium” and that of uninfected midges in both parity states and under all tested conditions: optimal, starvation, heat, and antibiotic treatment. Beyond survival, no wing length difference was found for “Candidatus Cardinium”-infected versus uninfected midges. In aggregate, these findings support our conclusion that “Candidatus Cardinium” does not have an overt effect on the survival and size of adult C. imicola midges. “Candidatus Cardinium” may affect immature stages or may alter adult reproductive performance.     

Coexistence of helminth species in Lysapsus limellus (Anura: Pseudidae) from an Argentinean subtropical area: influence of biotic and abiotic factors

The need for studies on helminth communities of South American amphibians was addressed by examining changes in composition and population dynamics of the helminth component and infracommunities in the frog Lysapsus limellus Cope, 1862, from 1994 to 1996. Two pond types were considered, one permanent and one semipermanent. The main goals of this study were (1) to investigate the relationships between pond type, season, study time, frog body size, and frog sex and the presence-absence and counts of helminth parasite species in the frog host, L. limellus, and (2) to examine the co-occurrence of the different parasite species in the frog host in terms of the structure, assembly, and dynamics of the helminth infracommunity. Parasite presence and absence were analyzed using logistic regression and parasite counts were analyzed using log-linear modeling. To examine the association between parasite species, a principal components analysis was carried out on the correlation matrix for the counts. The pattern of co-occurrences was also examined through a randomization test. The main results were as follows: (1) five parasite species were found in the infracommunity; (2) the pond type and the host size class were the principal factors related to the presence and absence of parasites for the three dominant species, while the year of study and the host sex were only important for one of the species; (3) for the parasite counts, many more factors were significant, with body size class and pond type always important factors for the three core species of the infracommunity, with season, year of study, and sex also sometimes important, and (4) strong associations were observed between some helminth species of the host from the permanent pond, but the same species did not co-occur in frogs in the semipermanent pond. The life histories of the five species can be considered as opportunistic or "r strategists."     

Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan

Background

By definition, parasites harm their hosts. However, some forms of parasite-induced alterations increase parasite transmission between hosts, such that manipulated hosts can be considered extensions of the parasite''s phenotype. While well accepted in principle, surprisingly few studies have quantified how parasite manipulations alter host performance and survival under field and laboratory conditions.

Methodology/Principal Findings

By interfering with limb development, the trematode Ribeiroia ondatrae causes particularly severe morphological alterations within amphibian hosts that provide an ideal system to evaluate parasite-induced changes in phenotype. Here, we coupled laboratory performance trials with a capture-mark-recapture study of 1388 Pacific chorus frogs (Pseudacris regilla) to quantify the effects of parasite-induced malformations on host locomotion, foraging, and survival. Malformations, which affected ∼50% of metamorphosing frogs in nature, caused dramatic reductions in all measures of organismal function. Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations. Furthermore, while normal and malformed individuals had comparable survival within predator-free exclosures, deformed frogs in natural populations had 22% lower biweekly survival than normal frogs and rarely recruited to the adult population over a two-year period.

Conclusions/Significance

Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival. These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.