Climate changes influence free‐living stages of soil‐transmitted parasites of European rabbits

Climate warming has been suggested to augment the risk of infectious disease outbreaks by extending the seasonal window for parasite growth and by increasing the rate of transmission. Understanding how this occurs in parasite‐host systems is important for appreciating long‐term and seasonal changes in host exposure to infection and to reduce species extinction caused by diseases. We investigated how free‐living stages of two soil‐transmitted helminths of the European rabbit (Oryctolagus cuniculus) responded to experimental changes in temperature by performing laboratory experiments with environmental chambers and field manipulations using open‐top‐chambers. This study was motivated by our previous observations that air temperature has increased over the last 30 years in our field site and that during this period intensity of infection of Graphidium strigosum but not Trichostrongylus retortaeformis was positively associated with this temperature increase. Laboratory and field experiments showed that both parasites accelerated egg development and increased hatching rate and larval survival in response to accumulating thermal energy. Both parasites behaved similarly when exposed to diverse temperature regimes, decadal trends, and monthly fluctuations, however, T. retortaeformis was more successful than G. strigosum by showing higher rates of egg hatching and larval survival. Across the months, the first day of hatching occurred earlier in warmer conditions suggesting that climate warming can lengthen the period of parasite growth and host exposure to infective stages. Also, T. retortaeformis hatched earlier than G. strigosum. These findings showed that seasonal changes in intensity, frequency, and duration of daily temperature are important causes of variability in egg hatching and larva survival. Overall, this study emphasizes the important role of climate warming and seasonality on the dynamics of free‐living stages in soil‐transmitted helminths and their contribution to enhance host exposure to parasitic infections. Yet, the ability to infect might ultimately depend on how hosts interact with parasites.     

The role of the European bitterling (<Emphasis Type="Italic">Rhodeus amarus,</Emphasis> Cyprinidae) in parasite accumulation and transmission in riverine ecosystems

In aquatic ecosystems, fish play a key role in parasite accumulation and transmission to predacious animals. In the present study, realized on seven populations of a small cyprinid fish species, the European bitterling Rhodeus amarus, we investigated (1) the role of the European bitterling as a potential intermediate or paratenic host, (2) the ability of the fish to accumulate parasites with similar final host group, and (3) its significance as a potential source of parasite infection in the ecosystem in respect to habitat characteristics. A total of 36 parasite species were recorded; 31 species (90% of all parasite specimens) were classified as endoparasites. Most of the endoparasites were found in the larval life stage, using bitterling as an intermediate or paratenic host. In particular, parasite community structure showed significantly higher proportions of allogenic parasites in comparison with autogenic. The supposed co-occurrence of parasite species with identical final host groups showed only a weak association. The adjacent reservoir areas were a significant determinant of both the total and infracommunity parasite species richness and for the mean parasite abundance. No relationship between the distance of sampling site from the adjacent reservoir and parasite community characteristics was found. As a small-sized fish with a wide distribution range and high local abundances, the European bitterling can represent a natural prey for a wide range of piscivorous predators. Due to its susceptibility to the number of larval endoparasites, this fish species may therefore fulfill the role as important transmitter of parasites to their final hosts.     

Larval mortality of pine sawflies [Hymenoptera: Diprionidae] in relation to pollution level: A field experiment

Larval mortality ofNeodiprion sertifer (Geoffroy),Diprion pini (L.) andGilpinia pallida (Klug) were studied in field experiments around a factory complex in southwestern Finland. Larval colonies were transferred on the shoots of Scots pines growing at different distances from the emission source. Larval mortality was highest near the factories. InN. sertifer, larval mortality caused by the nuclear polyhedrosis virus was higher and cocoon mortality caused by parasitoids was lower near the pollutant source. The most abundant parasitoid species wereSynomelix scutulata (Hartig) andLamachus eques (Hartig). 16–67% of theN. sertifer, 0–5% of theD. pini and the 73–100% ofG. pallida cocoons contained parasitoids oviposited during the larval period of the sawflies.      

Metazoan parasites of African annual killifish (Nothobranchiidae): abundance,diversity, and their environmental correlates

Estimates of biodiversity and its global patterns are affected by parasite richness and specificity. Despite this, parasite communities are largely neglected in biodiversity estimates, especially in the tropics. We studied the parasites of annual killifish of the genus Nothobranchius that inhabit annually desiccating pools across the African savannah and survive the dry period as developmentally arrested embryos. Their discontinuous, non‐overlapping generations make them a unique organism in which to study natural parasite fauna. We investigated the relationship between global (climate and altitude) and local (pool size, vegetation, host density and diversity, and diversity of potential intermediate hosts) environmental factors and the community structure of killifish parasites. We examined metazoan parasites from 21 populations of four host species (Nothobranchius orthonotus, N. furzeri, N. kadleci, and N. pienaari) across a gradient of aridity in Mozambique. Seventeen parasite taxa were recorded, with trematode larval stages (metacercariae) being the most abundant taxa. The parasites recorded were both allogenic (life cycle includes non‐aquatic host; predominantly trematodes) and autogenic (cycling only in aquatic hosts; nematodes). The parasite abundance was highest in climatic regions with intermediate aridity, while parasite diversity was associated with local environmental characteristics and positively correlated with fish species diversity and the amount of aquatic vegetation. Our results suggest that parasite communities of sympatric Nothobranchius species are similar and dominated by the larval stages of generalist parasites. Therefore, Nothobranchius serve as important intermediate or paratenic hosts of parasites, with piscivorous birds and predatory fish being their most likely definitive hosts.     

Influence of initial egg density and host size on the development of the gregarious parasitoid <Emphasis Type="Italic">Bracon hebetor</Emphasis> on three different host species

Bracon hebetor (Say) (Hymenoptera : Braconidae) is a gregarious parasitoid that attacks a variety of important lepidopterous pests of stored product and in the field. In this study the effect of host species, size and larval competition on parasitoid size, survival and development were investigated. In laboratory studies, wasp eggs at a range of densities, were placed on larvae of different weight of three Lepidoptera host species namely Adoxophyes orana (Fischer von Röslerstamm, Tortricidae), Plodia interpunctella (Hubner, Pyralidae) and, Lobesia botrana(Dennis & Schiffermueller, Tortricidae). On A. orana survival of immature parasitoids was very low at all densities and different host weights. On L. botrana survival progressively reduced as egg density increased at both host weights examined for this host. Survival on P. interpunctella was significantly affected by egg density but not by host weight. Initial egg density had a significant effect on the size of emerging adults from each rearing host. Smaller adult parasitoids emerged as egg density per larva increased. Larval host weight of P. interpunctella and A. orana had a significant effect on the size of emerging adult parasitoids mainly at the higher egg densities used in these experiments. The above results of host quality on fitness of parasitoid are discussed.     

Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK

Many crayfish species have been introduced to novel habitats worldwide, often threatening extinction of native species. Here we investigate competitive interactions and parasite infections in the native Austropotamobius pallipes and the invasive Pacifastacus leniusculus from single and mixed species populations in the UK. We found A. pallipes individuals to be significantly smaller in mixed compared to single species populations; conversely P. leniusculus individuals were larger in mixed than in single species populations. Our data provide no support for reproductive interference as a mechanism of competitive displacement and instead suggest competitive exclusion of A. pallipes from refuges by P. leniusculus leading to differential predation. We screened 52 P. leniusculus and 12 A. pallipes for microsporidian infection using PCR. We present the first molecular confirmation of Thelohania contejeani in the native A. pallipes; in addition, we provide the first evidence for T. contejeani in the invasive P. leniusculus. Three novel parasite sequences were also isolated from P. leniusculus with an overall prevalence of microsporidian infection of 38% within this species; we discuss the identity of and the similarity between these three novel sequences. We also screened a subset of fifteen P. leniusculus and three A. pallipes for Aphanomyces astaci, the causative agent of crayfish plague and for the protistan crayfish parasite Psorospermium haeckeli. We found no evidence for infection by either agent in any of the crayfish screened. The high prevalence of microsporidian parasites and occurrence of shared T. contejeani infection lead us to propose that future studies should consider the impact of these parasites on native and invasive host fitness and their potential effects upon the dynamics of native-invader systems.     

Parasites of European hedgehogs (<Emphasis Type="BoldItalic">Erinaceus europaeus</Emphasis>) in Britain: epidemiological study and coprological test evaluation

Seventy-four European hedgehogs (Erinaceus europaeus) that had died in wildlife rehabilitation centres were dissected and their parasite burdens documented. Overall parasite prevalence was 91%, and a total of six helminth species were isolated: five nematodes (Crenosoma striatum, Eucoleus aerophilus, Capillaria erinacei, Capillaria ovoreticulata and Capillaria spp.), one trematode (Brachylaemus erinacei) and one acanthocephalan (Oliganthorhynchus erinacei). The tick Ixodes hexagonus and flea Archeopsylla erinacei were also collected. The effect of parasite infection on body condition was assessed by correlation of burdens with the residuals of weight–skeletal length regression. Tick presence was positively related to body condition; for other parasites, no significant relationship was found. Faecal egg or larval count was closely correlated with adult parasite burden for C. striatum and Capillaria/Eucoleus spp., but not for other species. Coprological analysis should therefore be useful for in vivo studies of nematode parasite infection in hedgehogs. The epidemiology of parasites in hedgehogs and their possible role in recent population declines are discussed.     

Effects of Asobara japonica venom on larval survival of host and nonhost Drosophila species

Abstract Ovipositing Asobara japonica females inject venom (containing paralysis‐inducing factors) immediately after the insertion of their ovipositors into Drosophila larvae, and lay eggs a little later. Interruption of their oviposition behaviour before egg laying causes high larval mortality in host Drosophila species, whereas normal oviposition does not. This suggests that venom of this parasitoid is toxic to larvae of these host species but its toxicity is suppressed by factor(s) provided by parasitoid females at the time of laying egg or by parasitoid embryos developing in the hosts. On the other hand, venom does not show toxicity to larvae of nonhost Drosophia species. Possible functions of venom are discussed.     

Parasitoid assemblages of soybean defoliator Lepidoptera in north-western Buenos Aires province, Argentina

1 The objective of this study was to examine the structure of parasitoid assemblages attacking soybean defoliator Lepidoptera in north-western Buenos Aires province, Argentina. 2 Through larvae sampling from 1992 to 1996, and laboratory data plus the known biology of the species recorded during the study, parasitoid species composition, richness, number of guilds per host species, and levels of parasitism, were determined. 3 Total species richness was 23, all species were primary endoparasitoids, and categorized as koinobionts. They belonged to Hymenoptera (11 species) and Diptera (12 species). Rachiplusia nu (Noctuidae) hosted the highest number of parasitoid species. 4 Four parasitoid guilds were recorded for R. nu (egg–prepupal endoparasitoid, early larval endoparasitoid, late larval endoparasitoid, and larval–pupal endoparasitoid); two for Spilosoma virginica (Arctiidae) (late larval endoparasitoid and larval–pupal endoparasitoid) and Colias lesbia (Pieridae) (early larval endoparasitoid and larval–pupal endoparasitoid); and one for Anticarsia gemmatalis (Noctuidae) and Loxostege biffidalis (Pyralidae) (early larval endoparasitoid). 5 Only four out of seven potential parasitoid guilds defined for Lepidoptera were recorded in a soybean agroecosystem located in north-western Buenos Aires province, suggesting that potential host niches were not totally utilized. 6 Soybean lepidopteran defoliators supported a mean species richness of 4.8 parasitoids, a result that is similar to that reported for exophytic hosts in the Neotropics. 7 Parasitoid assemblages from each host differed in species composition, richness, number of guilds, and levels of parasitism.     

Host range in solitary versus gregarious parasitoids: a laboratory experiment

Behavioural interactions among relatives may have consequences for many other traits. We tested the hypothesis that solitary parasitoids (displaying siblicidal behaviour in their larvae) have narrower host ranges than gregarious parasitoids (with tolerant larvae). In laboratory experiments, we compared parasitization success in two sister species of braconid wasp [Aphaereta genevensis (Fischer), solitary, and Aphaereta pallipes (Say), gregarious (Hymenoptera: Braconidae: Alysiini)] on eight Drosophila species or strains. Host species or strain was the most important factor affecting parasitization success, and some of this variation was accountable to host physiological defences. Although two hosts were more suitable for the solitary species, and one more suitable for the gregarious species, these differences were small, and there was no consistent difference across all hosts. Wasp body size was positively correlated with parasitization success in both wasp species. This may be because body size increases oviposition success, or the motivation to oviposit. In A. pallipes parasitization success peaked after 3–4 days, but later in A. genevensis. This is likely due to low life expectancy and high egg loads increasing oviposition tendency in young A. pallipes, and egg limitation decreasing oviposition tendency in old A. pallipes. These data suggest that interactions among wasp larvae do not greatly affect the size of the fundamental niche examined here. However, they show the potential for life history traits, which differ between the species as a likely consequence of larval interactions, to affect the extent of the realized niche.     

Herbivore egg deposition induces tea leaves to arrest the egg‐larval parasitoid Ascogaster reticulata

Plants are able to activate direct and indirect defences against egg deposition by herbivorous insects. A known indirect defence is the production of synomones to help egg‐ and egg‐larval parasitoids to locate their hosts. The wasp Ascogaster reticulata Watanabe (Hymenoptera: Braconidae) is a solitary egg‐larval parasitoid of the moth Adoxophyes honmai Yasuda (Lepidoptera: Tortricidae), which lays eggs and feeds as caterpillars on the leaves of the tea plant Camellia sinensis (L.) Kuntze (Theaceae). Here, we studied whether or not oviposition by A. honmai induces tea plants to produce synomones that help the parasitoid to locate its host. An olfactometer bioassay suggested that synomones produced by the infested plants did not attract the parasitoid over a short range. However, a contact bioassay showed that tea leaves were induced to arrest the parasitoid 24 h after egg deposition and remained induced until the host‐egg masses were no more attractive to the parasitoids. Wing scales and deposits of adult moths and the contents of the egg masses did not induce the tea leaves to arrest the parasitoid, but the contents of the female moth's reproductive system did. Synomone induction was systemic: uninfested leaves in the vicinity of egg‐laden leaves also arrested the parasitoid.     

Geographic variation in winter freezing susceptibility in the eggs of the European pine sawfly (Neodiprion sertifer)

Abstract 1 The European pine sawfly, Neodiprion sertifer (Geoffroy) (Hymenoptera, Diprionidae), frequently defoliates Scots pine (Pinus sylvestris L.) forests in northern Europe. It overwinters as an egg. It has been proposed that the high egg mortality caused by low winter temperatures limits the occurrence of outbreaks to the southern part of Fennoscandia. 2 In this study, variation in freezing avoidance by egg supercooling between four Finnish populations (originating between latitudes 60°N and 69°N) of N. sertifer was tested by differential thermal analysis. Offspring of 20 females within each population were selected for the study. The freezing avoidance of parasitized eggs was also examined. 3 The northernmost Inari population was found to be the cold hardiest, and the southernmost (Hanko) was the least hardy population. The within‐population variation between females was greatest in the population from Inari, and the next greatest in the one from Hanko. The inland populations in Eastern Finland had the smallest within‐population variation in freezing avoidance. 4 The high variation in freezing avoidance of eggs will enable N. sertifer to adapt to the predicted climate change and to spread its distribution northwards. This may also change the risk for outbreaks in this area. Parasitized eggs froze at higher temperature than healthy eggs. This observation indicates that N. sertifer may experience reduced egg parasitism in certain winter climate conditions.     

Selection of Bemisia nymphal stages for oviposition or feeding,and host-handling times of arrhenotokous and thelytokous <Emphasis Type="Italic">Eretmocerus mundus</Emphasis> and arrhenotokous <Emphasis Type="Italic">E. eremicus</Emphasis>

Host-handling behavior is an important aspect of parasitoid foraging behavior. When a parasitoid encounters a potential host, the handling behavior starts with the evaluation of the host and continues if the host has been judged acceptable. Host handling is usually terminated after egg laying or host feeding and host marking. Host-handling behavior of an arrhenotokous population of two Eretmocerus species, E. mundus Mercet and E. eremicus Rose and Zolnerowich, along with a thelytokous population of E. mundus were compared under laboratory conditions. Several elements of host-handling behavior, including encountering, ascending, turning on host, descending, preening, egg laying, and host feeding were recorded. There were no correlations among the durations of these phases across parasitoid populations/species or host nymphal instars. Duration of different phases of host-handling behavior showed only slight and sometimes significant differences between different Eretmoceruspopulations/species. The actual laying of the egg had the longest duration of all host-handling behaviors, and was longer on third nymphal instars than on younger ones. Females of the three populations/species accepted the first three nymphal stages either for egg laying or for host feeding. Females spent a lot of time to make wounds in the host when preparing for host feeding, and eventually killed the host. The implications of these findings for the use of the different Eretmoceruspopulations/species in biological control are discussed.     

Changes in abundance of native and introduced parasites (Hymenoptera: Braconidae), and of the target and non-target plant bug species (Hemiptera: Miridae), during two classical biological control programs in alfalfa.

High numbers of tarnished plant bugs [Lygus lineolaris (Palisot)], were once common in alfalfa, as was a low level of parasitism (9%) by the native Peristenus pallipes (Curtis). After the bivoltine European parasite Peristenus digoneutis Loan became well established, average parasitism of the first and second generations increased to 64%, and tarnished plant bug numbers dropped by 65%. This reduced host density eventually caused a decline in total parasitism by both parasite species to 22%. A few P. digoneutis also attacked the alfalfa plant bug, Adelphocoris lineolatus (Goeze), but did not reduce this pest or increase its parasitism rate. At another location, where P. digoneutis is not established, parasitism of first generation alfalfa plant bugs, an adventive (accidently introduced) pest, was increased to 21% by the introduced univoltine parasite, Peristenus conradi Marsh, and a slight reduction in the pest may have resulted. P. digoneutis did not parasitize the meadow plant bug, Leptopterna dolabrata (L.), an adventive pest of forage grasses, so did not affect this mirid or its parasite. Neither introduced parasite eliminated the native parasites of the tarnished or alfalfa plant bugs. The narrow host ranges of the braconid parasites of mirid nymphs are contrasted with the broad host range of the native tachinid parasite [Phasia robertsoni (Towns.)] of adult mirids. The major changes in mirid abundance and their mortality by parasites that slowly occurred during this 19-year study demonstrate the need for long-term field research, to adequately document and understand these complex interactions.     

The role of the rock cod Notothenia coriiceps Richardson, 1844 in the life-cycle of Antarctic parasites

Fifty specimens of Notothenia coriiceps caught in Potter Cove, King George Island, were examined for ecto- and endoparasites. Of the 22 parasite species found, 18 were helminths, 2 were hirudineans and 2 were crustaceans. The isopod Aega antarctica and an unidentified hirudinean are reported for the first time from this fish host. Dominant parasites were the adults of Aspersentis megarhynchus, the invasive stage of Corynosoma spp. (cystacanth) and the adults of Macvicaria pennelli, with respective prevalences of infestation of 94, 76 and 74%. The preferred sites of infestation were the pylorus and intestine, where five different larval (nematodes and cestodes) and eight adult (digeneans and acanthocephalans) parasite species were found. No adult nematodes and cestodes were found and no parasites could be isolated from the musculature. The results of the present study are related to previous findings on the parasite fauna of N. coriiceps. The comparison implies a high parasite diversity in this benthic Antarctic fish species. Most parasites found appear to have a wide range of distribution within Antarctic waters together with a low host specificity. Besides its role as final host for several species of trematodes and acanthocephalans, N. coriiceps serves as transmitter of parasite larvae to piscivorous birds and seals. It is concluded that the parasite fauna in Antarctic fish species provides important insights into the different habitat use and trophic relationship of their fish hosts. Received: 11 September 1997 / Accepted: 12 January 1998     

Methylmercury levels in a parasite (<Emphasis Type="Italic">Apophallus brevis</Emphasis> metacercariae) and its host,yellow perch (<Emphasis Type="Italic">Perca flavescens</Emphasis>)

The biomagnification of methylmercury (MeHg) amongst trophic levels results in high levels of this compound in many freshwater fish species. The role of parasites in MeHg cycling and trophic transfer in freshwater systems is largely unknown. This study examined the potential for metacercariae of Apophallus brevis to accumulate and biomagnify MeHg from their second intermediate host, yellow perch, Perca flavescens. Contrary to our prediction that MeHg levels would be higher in parasites than in the host muscle tissue in which they are embedded, we found that concentrations were similar. The lack of increase in MeHg levels from host to parasite may be due to limited assimilation of host muscle tissue or, in part, to low parasite metabolism. Parasite load did not reduce fish growth and subsequently alter MeHg concentrations. This study suggests that relationships between larval parasites and their hosts do not conform to typical patterns of MeHg biomagnification seen in aquatic systems.     

Tight insect–host phenological synchrony constrains the life‐history strategy of European pine sawfly

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Intrinsic, inter-specific competition between egg, egg–larval, and larval parasitoids of plusiine loopers

Abstract.  1. Intrinsic, inter-specific competition between parasitoid wasp species is a key factor in ecological community dynamics and is particularly important for application in biological control. Here three parasitoid wasp species with overlapping host ranges and differing life history strategies were chosen to examine parasitoid–parasitoid interactions: the egg parasitoid Trichogramma pretiosum, the egg–larval, polyembryonic parasitoid wasp Copidosoma floridanum, and the gregarious larval parasitoid Glyptapanteles pallipes , with the plusiine loopers Acanthoplusia agnata and Trichoplusia ni as hosts.
2.  Copidosoma floridanum has been shown to be an intrinsically superior competitor against larval parasitoids because of their production and increased investment in a soldier larval caste during development, but little is known of their interactions with egg parasitoid species. Trichogramma pretiosum completely dominated intrinsic competition with C. floridanum regardless of oviposition order or sex of the C. floridanum egg.
3. Competition between C. floridanum and G. pallipes , however, depended on the host stage at which parasitism occurred, the sex of the C. floridanum egg, and parasitoid development time. Copidosoma floridanum outcompeted G. pallipes overall, despite the fact that G. pallipes injects a polyDNA virus into the host.
4. The sex of the C. floridanum egg was a significant factor in its ability to shift caste ratios to produce more soldiers in response to G. pallipes competition.
5. Only developing female C. floridanum responded to competition with G. pallipes by increasing the ratio of soldier to reproductive larvae, and this happened only when multiparasitism occurred in the host's 1st and 2nd instar.     

Interactions between the egg and larval parasitoids of a gall-forming midge and their impact on the host

1. The gall‐forming midge Rhopalomyia californica was exposed experimentally to parasitism and predation during only the egg stage, during only the larval stage, during neither stage, or during both stages. 2. The combined action of natural enemies that attack during both the egg stage and the larval stage led to the lowest number of midges and total insects (midges + parasitoids) in the next generation, and the highest percentage parasitism. 3. The larval parasitoid killed a large fraction of hosts without producing new parasitoid offspring, while there is some indication that the egg parasitoid on its own tended to produce the most parasitoid offspring. The contrasting implications of host mortality versus parasitoid production for biological control are discussed. 4. Exposure to larval parasitoids resulted in a reduction in the number of egg parasitoid offspring produced, but exposure to the egg parasitoid did not affect the number of larval parasitoid offspring produced significantly.