Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda)

Acanthocephalan parasites are known to alter the reproductive biology and physiology of their hosts in various ways. In this study we investigated the influence of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on the fecundity and pairing success of female Gammarus pulex. The results show that P. laevis and P. minutus affect female intermediate host reproduction in different ways. Females infected with P. minutus were totally castrated, whereas those infected with P. laevis only showed reduced fecundity. The oocytes of P. laevis-infected females showed a similar structure to those of uninfected females, although infected females had a higher proportion of oocytes that had failed to reach complete maturity. In comparison, the oocytes of P. minutus-infected females demonstrate a clearly altered structure that suggests a major disruption to the process of vitellogenesis. In the field, males paired more frequently with uninfected females than with infected ones, and is a stronger effect for P. minutus-infected females than P. laevis-infected females. We suggest that the difference in pairing success of P. minutus-infected and P. laevis-infected females is a direct result of the different effects that the two parasites have on female fecundity.     

The helminth parasites of the bullhead Cottus gobio (L.) and the stone loach Noemacheilus barbatulus (L.) from the River Avon, Hampshire

Specimens of Cottus gobio and Noemacheilus barbatulus from the River Avon, Hampshire, were examined between July 1970 and July 1971. Both fish were found to act as hosts for Nicolla gallica (adult), Pomphorhynchus laevis (adult) and Triaenophorus nodulosus (plerocercoid). The incidence and intensity of infection were lower in N. barbatulus than in C. gobio , and this was related to differences in host diet. A small number of N. barbatulus were also found to harbour Proteocephalus torulosus . Seasonal cycles of incidence and intensity were evident in N. gallica , with a peak occurring in the winter. P. laevis and T. nodulosus showed no such cycles. Increasing host size was associated with a higher infection of both N. gallica and P. laevis , but not T. nodulosus . The diet of the host was considered to be important in influencing this increase. Differences in host reproductive condition affected the population levels of N. gallica only, where an increased parasite burden was evident in gravid female fish. This was considered to influence the observed increase in incidence and intensity of this parasite during the winter. None of the parasites showed any seasonal maturation cycles. There was no evidence of any interactions between the parasite populations. Host diet and the availability of infective larvae were considered to be the most important features influencing the number of parasites which became established, and the rate at which this occurred. Temperature probably acted indirectly on the establishment of N. gallica , by controlling the availability of the larval stages, and also, by influencing the host reproductive condition, on the length of time for which the parasite was retained by the host.     

Patterns of intermediate host use and levels of association between two conflicting manipulative parasites.

For many parasites with complex life cycles, manipulation of intermediate host phenotypes is often regarded as an adaptation to increase the probability of successful transmission. This phenomenon creates opportunities for either synergistic or conflicting interests between different parasite species sharing the same intermediate host. When more than one manipulative parasite infect the same intermediate host, but differ in their definitive host, selection should favour the establishment of a negative association between these manipulators. Both Polymorphus minutus and Pomphorhynchus laevis exploit the amphipod Gammarus pulex as intermediate host but differ markedly in their final host, a fish for P. laevis and a bird for P. minutus. The pattern of host use by these two conflicting manipulative parasites was studied. Their incidence and intensity of infection and their distribution among G. pulex were first examined by analysing three large samples of gammarids collected from the river Tille, Eastern France. Both parasites had low prevalence in the host population. However, temporal fluctuation in the level of parasitic infection was observed. Overall, prevalence of both parasite species was higher in male than in female G. pulex. We then assessed the degree of association between the two parasites among their intermediate hosts, using two different methods: a host-centred measure and a parasite-centred measure. Both measures gave similar results; showing random association between the two acanthocephalan species in their intermediate hosts. We discuss our results in relation to the selective forces and ecological constraints that may determine the pattern of association between conflicting manipulative parasites.     

Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae)

Because of their effects on host reproductive behaviour, parasites are theoretically expected to create sometimes assortative mating among hosts, with heavily parasitized individuals pairing together and lightly parasitized ones pairing among themselves. We investigated the influence of protozoan gut parasites on the pairing pattern of the chrysomelid beetle Timarcha maritima. In the field, fecundity was negatively correlated with the parasite load of females, unpaired males were significantly more heavily infected than paired ones and, among pairs, males and females were matched for parasite load. Mate choice experiments in the laboratory showed that males have some ability to avoid heavily infected partners when given the choice between two females. Male competitiveness, measured as their mobility, was also negatively correlated with parasite load. These results indicate that parasite-related assortative pairing in this beetle could result from parasitized females being less fecund and parasitized males less competitive.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.     

艾美耳球虫对高原鼠兔繁殖的影响

寄生物对宿主繁殖的影响取决于宿主对当前繁殖值和剩余繁殖值的权衡。球虫为微型寄生物,而微型寄生物对宿主当前繁殖值的影响较剩余繁殖值要大。因此,本研究检验了寄生在高原鼠兔肠道内的艾美耳球虫可影响其当前繁殖的假设。在繁殖早、中、晚期,野外共观测高原鼠兔170只。结果表明,不同繁殖期感染率有显著差异。在繁殖中期,未感染雌性的妊娠率显著高于感染雌性。且未妊娠雌性较妊娠雌性有更高的感染强度,但在另外两个繁殖期没有发现此效应。在雄性中,任何繁殖期的感染强度和感染率与睾丸和附睾指数均无显著相关性,且感染和未感染球虫雄性睾丸及附睾指数无显著差异。此外,野外观测实验结果表明,感染雌性的胚胎重较未感染雌性显著降低,与野外感染对胚胎重量影响的实验结果相一致。说明艾美耳球虫感染可影响胚胎的发育。上述结果说明,艾美耳球虫对高原鼠兔繁殖的影响随繁殖期而有不同效应,且存在性别间差异,这种效应可能与不同性别间的繁殖对策有关。     

Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage

Many trophically transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host's antipredatory defenses when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when noninfective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by noninfective stage of P. laevis (acanthella) hid significantly more under refuges than uninfected ones. In addition, acanthella-infected gammarids were less predated upon by trout than uninfected ones. As predicted, a switch toward decreased antipredatory behavior of G. pulex and enhanced vulnerability to predation was found when P. laevis reached the stage infective to its final host. The parasites appear to be able to exploit plasticity in host antipredatory responses, and shift the host optimal response toward their own optimal balance.     

Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation,host adaptation,or side effect?

Parasitic infections may cause alterations in host life history, including changes in reproductive investment (absolute amount of energy allocated to reproduction) and reproductive effort (proportion of available energy allocated to reproduction). Such changes in host life history may reflect: 1) a parasite tactic: the parasite adaptively manipulates energy flow within the host so that the host is induced to make a reduction in reproductive effort and reproductive investment, making more energy available to the parasite; 2) no tactic: there is no change in host reproductive effort and reproductive investment simply decreases as a side effect of the parasite depleting host energy stores; 3) a host tactic: the host adaptively increases reproductive effort in the face of infection and loss of body condition, reproductive investment possibly being reduced despite the increased reproductive effort. Females in Alaskan lake populations of threespine sticklebacks ( Gasterosteus aculeatus ) are capable of clutch production when parasitized by the cestode Schistocephalus solidus despite large relative parasite masses. We analyzed the somatic energy reserves, maturation stage and ovarian mass of female sticklebacks collected from an Alaska lake during a single reproductive season. We found that parasitized females were less likely to carry fully-matured gametes, had smaller ovarian masses, and had lower somatic energy stores than unparasitized females. The relationship between reproductive investment and energy storage did not differ between parasitized and unparasitized females. Thus, reproductive effort did not change in response to parasitic infection. We conclude there was no indication of either a parasite tactic or a host tactic. Simple nutrient theft is involved in the parasite's influence on host reproduction, consistent with an earlier hypothesis that reproductive curtailment in threespine sticklebacks is a side effect.     

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasite's reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.     

Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition

1. Seasonality of rainfall can exert a strong influence on animal condition and on host-parasite interactions. The body condition of ruminants fluctuates seasonally in response to changes in energy requirements, foraging patterns and resource availability, and seasonal variation in parasite infections may further alter ruminant body condition. 2. This study disentangles the effects of rainfall and gastrointestinal parasite infections on springbok (Antidorcas marsupialis) body condition and determines how these factors vary among demographic groups. 3. Using data from four years and three study areas, we investigated (i) the influence of rainfall variation, demographic factors and parasite interactions on parasite prevalence or infection intensity, (ii) whether parasitism or rainfall is a more important predictor of springbok body condition and (iii) how parasitism and condition vary among study areas along a rainfall gradient. 4. We found that increased parasite intensity is associated with reduced body condition only for adult females. For all other demographic groups, body condition was significantly related to prior rainfall and not to parasitism. Rainfall lagged by two months had a positive effect on body condition. 5. Adult females showed evidence of a 'periparturient rise' in parasite intensity and had higher parasite intensity and lower body condition than adult males after parturition and during early lactation. After juveniles were weaned, adult females had lower parasite intensity than adult males. Sex differences in parasitism and condition may be due to differences between adult females and males in the seasonal timing of reproductive effort and its effects on host immunity, as well as documented sex differences in vulnerability to predation. 6. Our results highlight that parasites and the environment can synergistically affect host populations, but that these interactions might be masked by their interwoven relationships, their differential impacts on demographic groups, and the different time-scales at which they operate.     

Recognition of social parasites as nest-mates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer.

Colonies of the polistine wasp Polistes dominulus are parasitized by the permanent worker-less social parasite Polistes sulcifer. After usurpation of the host colony, parasite females are characterized by a change in the relative proportions of their cuticular hydrocarbons to match those of the host species. In this paper we present evidence from field data and laboratory experiments that P. sulcifer females adopt a colony-specific host odour that facilitates their acceptance by host females of the usurped colony. Presentation experiments demonstrate that parasite females are recognized as foreign individuals by workers of other parasitized nests. We show that the modification of parasite cuticular compounds is sufficient for this recognition. This provides evidence that, after invasion, P. sulcifer queens do not require appeasement or propaganda substances for their acceptance by host colonies. Furthermore, multivariate discriminant analysis of the cuticular hydrocarbon proportions of the parasites after usurpation assigns the parasites together with P. dominulus females of their own host colony. To the authors' knowledge, this is the first confirmation that social parasites adopt colony-specific host odours.     

Ectoparasite Raymondia lobulata infestation in relation to the reproductive cycle of its host--the greater false vampire bat Megaderma lyra

To study variation of infestations by the bat fly Raymondia lobulata (Diptera: Streblidae) on the greater false vampire bat Megaderma lyra (Chiroptera: Megadermatidae), we captured individual bats at their day roost in the south of India and recorded their rate of infestation continuously for a year. All examined bats (n = 72 individuals, 202 captures) were infested with parasites (n = 3,008). However, the recorded intensity of infestation (range 1-33) was gender-related and statistically higher in females than in males (F(1, 200) = 304.45, P < 0.001). Furthermore, pregnant and lactating females had greater parasite loads than non-reproductive females and males (F(1, 63) = 23.34, P < 0.001 and F(1, 37) = 78.07, P < 0.001, respectively). No significant differences were observed between males either during mating and non-mating periods or breeding and non-breeding seasons. Analysis of the relationship between parasite infestation and the reproductive status of bats revealed that pregnant and lactating females with pups were more vulnerable hosts for parasites. Our results also suggest a well-developed coevolutionary strategy for synchronized reproduction within the host-parasite relationship and add to our understanding of how host sex and reproductive status shape the dynamics of parasitism.     

The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis

We investigated the role of host sex in parasite transmission and questioned: ‘Is host sex important in influencing the dynamics of infection in free living animal populations?’ We experimentally reduced the helminth community of either males or females in a yellow‐necked mice (Apodemus flavicollis) population using an anthelmintic, in replicated trapping areas, and subsequently monitored the prevalence and intensity of macroparasites in the untreated sex. We focussed on the dominant parasite Heligmosomoides polygyrus and found that reducing parasites in males caused a consistent reduction of parasitic intensity in females, estimated through faecal egg counts, but the removal of parasites in females had no significant influence on the parasites in males. This finding suggests that males are responsible for driving the parasite infection in the host population and females may play a relatively trivial role. The possible mechanisms promoting such patterns are discussed.     

Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators

Phenotypic alterations induced by parasites in their intermediate hosts often result in enhanced trophic transmission to appropriate final hosts. However, such alterations may also increase the vulnerability of intermediate hosts to predation by non-host species. We studied the influence of both infection with 3 different acanthocephalan parasites (Pomphorhynchus laevis, P. tereticollis, and Polymorphus minutus) and the availability of refuges on the susceptibility of the amphipod Gammarus pulex to predation by 2 non-host predators in microcosms. Only infection with P. laevis increased the vulnerability of amphipods to predation by crayfish, Orconectes limosus. In contrast, in the absence of refuges, the selectivity of water scorpions, Nepa cinerea, for infected prey was significant and did not differ according to parasite species. When a refuge was available for infected prey, however, water scorpion selectivity for infected prey differed between parasite species. Both P. tereticollis- and P. laevis-infected gammarids were more vulnerable than uninfected ones, whereas the reverse was true of P. minutus-infected gammarids. These results suggest that the true consequences of phenotypic changes associated with parasitic infection in terms of increased trophic transmission of parasites deserve further assessment.     

Sex discriminatory effect of the acanthocephalan Acanthocephaloides propinquus on a gobiid fish Gobius bucchichii

Most studies which aim at detecting effects of parasites on fish show that intermediate stages of parasites affect their host while adult parasites are usually less virulent in the final host. We studied the effect of the acanthocephalan Acanthocephaloides propinquus on one of its final hosts, the fish Gobius bucchichii. This study showed that the adult parasites affect host fitness. Moreover, our results showed that at the same level of infection in male and female gobiids, the female's reproductive success was negatively correlated to parasite abundance while the male's reproductive success was not. The negative effects on females includes reductions in gonado-somatic index and egg production. We hypothesized that it might be more difficult for females to compensate the cost of parasitism because of the very high cost of egg production. We discussed these results in terms of host population regulation.     

Increased parasite abundance associated with reproductive maturity of the clam Anodonta piscinalis.

Several studies on vertebrates have demonstrated that reproductive activities may increase the parasite load, but this has not been shown in invertebrate hosts. We studied abundance of a potentially harmful gill parasite, the ergasilid copepod Paraergasilus rylovi, from the freshwater bivalve host Anodonta piscinalis in relation to reproductive maturity of the host in the field. Prevalence of this previously unstudied parasite varied from 90 to 100%, and the mean parasite abundance from 16.3 to 28.8 among 3 study populations. Abundance of P. rylovi increased with host size. In the maturating age groups (3-5 yr) the length-adjusted mean parasite abundance among mature, reproducing female clams that brooded glochidia larvae was 2 times higher than in nonreproducing females, the observed pattern being consistent among the 3 study lakes. Alternative, mutually nonexclusive explanations may be found for the result. For example, changes in clam behavior or filtration activity accompanying maturation can increase host exposure to parasites, or reproduction may decrease energy available to host immunologic defense. However, the present result indicates that maturation, and reproduction, is associated with increased parasite abundance in A. piscinalis, an invertebrate host.     

Parasite infectivity to hybridising host species: a link between hybrid resistance and allopolyploid speciation?

Variation in host-specific infectivity was studied in monogenean polystome parasites (Protopolystoma spp.) of the interfertile, parapatric anurans Xenopus laevis laevis and Xenopus muelleri. Laboratory-raised host F1 hybrids were resistant to parasites respectively specific to each parent taxon in nature. This resistance occurred against parasite isolates from both inside and outside a host hybrid/sympatric zone (and no isolate was compatible with the foreign host species under experimental conditions). Geographical Protopolystoma xenopodis isolates showed variable infectivity to a single full-sib group of their usual host, X. l. laevis, and strains with high or low infectivity to these sibs co-occurred in spatially distant local areas (separated by 1,700 km). The host compatibility of P. xenopodis was also subject to host genotypexparasite genotype interactions. Refractoriness to some parasites or pathogens, as a consequence of hybridisation, may have conferred a selective advantage on the allopolyploid pathway by which most Xenopus spp. are believed to have evolved.     

Microhabitat distributions and species interactions of ectoparasites on the gills of cichlid fish in Lake Victoria,Tanzania

Heterogeneous exposure to parasites may contribute to host species differentiation. Hosts often harbour multiple parasite species which may interact and thus modify each other’s effects on host fitness. Antagonistic or synergistic interactions between parasites may be detectable as niche segregation within hosts. Consequently, the within-host distribution of different parasite taxa may constitute an important axis of infection variation among host populations and species. We investigated the microhabitat distributions and species interactions of gill parasites (four genera) infecting 14 sympatric cichlid species in Lake Victoria, Tanzania. We found that the two most abundant ectoparasite genera (the monogenean Cichlidogyrus spp. and the copepod Lamproglena monodi) were non-randomly distributed across the host gills and their spatial distribution differed between host species. This may indicate microhabitat selection by the parasites and cryptic differences in the host–parasite interaction among host species. Relationships among ectoparasite genera were synergistic: the abundances of Cichlidogyrus spp. and the copepods L. monodi and Ergasilus lamellifer tended to be positively correlated. In contrast, relationships among morphospecies of Cichlidogyrus were antagonistic: the abundances of morphospecies were negatively correlated. Together with niche overlap, this suggests competition among morphospecies of Cichlidogyrus. We also assessed the reproductive activity of the copepod species (the proportion of individuals carrying egg clutches), as it may be affected by the presence of other parasites and provide another indicator of the species specificity of the host–parasite relationship. Copepod reproductive activity did not differ between host species and was not associated with the presence or abundance of other parasites, suggesting that these are generalist parasites, thriving in all cichlid species examined from Lake Victoria.     

Differential responses to related hosts by nesting and non-nesting parasites in a brood-parasitic duck

Host-parasite relatedness may facilitate the evolution of conspecific brood parasitism, but empirical support for this contention remains inconclusive. One reason for this disparity may relate to the diversity of parasitic tactics, a key distinguishing feature being whether the parasite has a nest of her own. Previous work suggests that parasites without nests of their own may be of inferior phenotypic quality, but because of difficulties in identifying these parasitic individuals, little is known about their host selection criteria. We used high-resolution molecular maternity tests to assign parasitic offspring to known parasites with and without their own nests in a population of Barrow's goldeneyes (Bucephala islandica). We determined whether parasite nesting status, host-parasite relatedness and distance between host and parasite nests affected the probability of parasitizing a host and the number of eggs laid per host. We also investigated whether nesting parasites, conventionally nesting females and non-nesting parasites differed regarding their age, structural size, body condition, nesting phenology or total brood size. The probability of engaging in parasitism increased with host-parasite relatedness and spatial proximity to host nests for nesting and non-nesting females alike. However, nesting parasites increased the number of eggs donated with relatedness to the host, while non-nesting parasites did not do so. Non-nesting parasites laid fewer eggs in total, but did not differ by any of the other quality measures from conventional nesters or nesting parasites. Our study provides the first demonstration that nesting and non-nesting parasites from the same population may use different host selection criteria.     

Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer (Hymenoptera, Vespidae)

In multiple-foundress nests of the wasp Polistes dominulus, dominance hierarchies are established among foundresses, and only the dominant (=alpha) individual lays eggs. The alpha female can be distinguished from subordinate females and workers on the basis of the proportions of some hydrocarbons present on the cuticle, suggesting that chemical signaling of her reproductive status could occur. P. dominulus is also the host species of the obligate social parasite Polistes sulcifer. After aggressively usurping host colonies and behaviorally replacing the host alpha female, parasites are characterized by a change in the proportions of their cuticular hydrocarbons to match that of the host cuticular profile at both species and colony levels. In the current study, we demonstrate that P. sulcifer queens also modify their cuticular hydrocarbon proportions after usurpation to match that of the host alpha female. Parasite females, therefore, acquire the dominant rank in host colonies both reproductively and chemically by mimicking the typical alpha profile of the host. Parasite females were not able to fully inhibit ovary development in host foundresses, and 10 days after usurpation, parasites, alpha and beta foundresses show similar chemical profiles and ovarian development.