Experimental evidence for a hierarchy of mate- and host-induced cues in a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura)

Argulus coregoni is an ectoparasite primarily infesting freshwater salmonids. Sexually reproducing parasites such as A. coregoni are confronted with a dilemma between finding a mate and the costs involved in doing so; if mating partners are unavailable on a host, by leaving to search for a mate on a new host, the parasite is exposed to risks such as predation and energy loss. The utilization of chemical cues could enhance the probability of finding a host and/or a suitable mating partner and thus decrease the level of costs associated with detachment from the host. In this study we constructed a Y-maze arena to determine if adult A. coregoni respond to mate- and host-related chemical cues. We also tested the directional response towards light, since it has been suggested that photic cues are the most important cues for juvenile A. coregoni locating a host. Our results showed that both sexes were attracted to light and fish odour. Free-swimming A. coregoni males responded to chemical cues produced by adult females but not vice versa. The hierarchy of these stimuli was analyzed by pitting the cues against one another in the Y-maze, showing that light was the most salient stimulus for both male and female parasites. Moreover, male parasites were more strongly attracted towards light and fish odour than female odour. In another experiment in a semi-natural environment, we examined whether the ability of A. coregoni males to detect female odour influences their host choice. Free-swimming males did not preferentially infest fish infected with female parasites over parasite-free fish. We suggest that a hierarchy of stimulus responses exists, whereby free-swimming parasites first respond to host-related signals and most dominantly to visual cues. However, cues connected to mate finding may become a priority for late adult stages and/or once the parasite has attached to the host.     

How do fish ectoparasites Argulus spp. (Crustacea: Branchiura) match with their hosts at the behavioural and ecological scales?

Features of the Argulus foliaceus and A. coregoni life cycles including spatial distribution and hatching patterns of the resting eggs as well as their host searching behaviour were analyzed on the basis of field and experimental data obtained in lakes and a fish farm in the Central Finland. Published data on behaviour and ecology of these parasites were also used. The main point of this analysis was an ecological adjustment of the life cycles of parasites to that of their fish hosts at different spatial and temporal scales. Due to different spatial distribution of overwintering eggs, the newly hatched larvae of A. coregoni are more likely to attach to salmonids, which are their main hosts, while A. foliaceus to percids and cyprinids. The main peak of argulid hatching occurs in late spring-early summer and coincides with the period when most of freshwater fishes concentrate close to the shore, either for spawning, or, foraging. Nevertheless, despite the general coincidence, the parasite-host encounter rate could still be very low. The main peak of hatching is followed by a long "tail". We suggest that under fluctuating and uncertain environmental conditions characterised by both abiotic stochasticity and poor predictability of the hosts, an optimal recruitment strategy is to hedge a bet, with a proportion of eggs synchronously hatching and a proportion remaining dormant and hatching at much lower rate during an extended period. One of the main behavioural adaptations to match with the hosts is all-over-the-day searching activity of argulids. The boreal A. coregoni relies primarily on vision, which is most effective in transparent waters during long polar days in summer. Vision is also important in the behavioural repertoire of the temperate A. foliaceus in the light, but olfaction and mechanoreception in the dark provide the highest host searching rate. The two generally sympatric species of argulids segregated on the finer habitat scale. Partially overlapping on salmonid hosts, they prefer ecologically distinct categories of fish, and use different microhabitats for egg laying and searching for hosts.     

Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency

Disease-mediated impacts of exotic species on their native counterparts are often ignored when parasite-free individuals are translocated. However, native parasites are frequently acquired by exotic species, thus providing a mechanism through which native host-parasite dynamics may be altered. In Argentina, multiple exotic salmonids are host to the native fish acanthocephalan parasite Acanthocephalus tumescens. Field evidence suggests that rainbow trout, Oncorhynchus mykiss, may be a major contributor to the native parasite’s population. We used a combination of experimental infections (cystacanth—juvenile worm transmission from amphipod to fish; post-cyclic—adult worm transmission between definitive fish hosts) and dynamic population modelling to determine the extent to which exotic salmonid hosts may alter A. tumescens infections in native freshwater fish. Experimental cystacanth infections demonstrated that although A. tumescens establishes equally well in native and exotic hosts, parasite growth and maturity is superior in exotic O. mykiss. Experimental post-cyclic infections also showed greater establishment success of A. tumescens in O. mykiss, though post-cyclic transmission did not result in greater parasite size or maturity. Dynamic population modelling, however, suggested that exotic salmonids may have a very limited influence on the A. tumescens population overall, due to the majority of A. tumescens individuals being maintained by more abundant native hosts. This research highlights the importance of considering both a host’s relative density and its competency for parasites when evaluating whether exotic species can modify native host-parasite dynamics.     

The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncovhynchus mykiss (Walbaum) under experimental conditions

An experimental epidemiological approach was chosen to study the survival and infection dynamics of Gyrodactylus salaris on juvenile rainbow trout, Oncorhynchus mykiss , in the laboratory. A marked heterogeneity in the host stock was apparent. The rainbow trout could be divided into three groups on the basis of parasite survival and infection pattern on individually isolated fish: (1) hosts receptive to initial parasite attachment, but unreceptive to parasite establishment and reproduction; (2) hosts moderately susceptible to parasite establishment and reproduction, but which, after a period of restricted parasite population growth, responded, recovered and eliminated the parasites; and (3) hosts very susceptible to parasite infection and reproduction, but which, after a period of significant parasite population growth, responded, recovered and eliminated the parasites. These different patterns are considered to reflect genetic differences between host individuals. Parasite aggregation was also shown to be an important factor in the outcome of the host-parasite association. The parasites were finally eliminated on the individually isolated hosts, but not on hosts maintained in batches and so host population size and immigration of fresh. previously unexposed, hosts appeared to be important for growth and maintenance of the parasite population. The parasite was not found to cause host mortality. Rainbow trout was a suitable host for G. salaris , capable of transmitting the parasite to new localities as a consequence of stocking programmes or migratory behaviour.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

A comparative study of the host-parasite relationship of Pomphorhynchus patagonicus (Acanthocephala) in two species of fish from Lake Rosario (Chubut, Argentina).

Some aspects of the host-parasite relationships of Pomphorhynchus patagonicus (Acanthocephala) in 2 fish species from Lake Rosario (Chubut, Argentina) were studied. The fish species Patagonina hatcheri (Atherinidae) is autochthonous, and Oncorhynchus mykiss (Salmonidae) is introduced. The host species appears to influence attachment, size, sexual maturity, and distribution of parasites along the digestive tract. In P. hatcheri, an effective major host, parasites are attached firmly to the wall of the gut, well developed, attain a greater size, and a large proportion of females is gravid with ripe eggs. In O. mykiss, an unsuccessful host, there were many unattached parasites that were small and not well developed; gravid females were rare and never had ripe eggs.     

Induced resistance to infection of lobsters Homarus americanus by Aerococcus viridans (var.) homari, the bacterium causing gaffkemia

Efficacy of in-feed treatment with emamectin benzoate (Slice) for the control of ectoparasitic Argulus coregoni on rainbow trout Oncorhynchus mykiss was tested under laboratory and field conditions. In both experiments fish were fed with fish feed to deliver a therapeutic dose of 0 (control) or 50 microg emamectin benzoate kg(-1) d(-1) (treatment) for a period of 7 d. After 3 d of challenge with A. coregoni in the laboratory, the infestation level in treated fish was lower than that observed in the controls (p < 0.001). Efficacy of 100% against newly hatched A. coregoni metanauplii and adults and 80% against juveniles was observed. In the field, trial medication was undertaken at 2 sections on a flow-through canal with 1 wk between treatments. Mean infestations of 100 to 200 A. coregoni per fish with 100% prevalence was recorded prior to medication. Following the treatment, the mean infestation of A. coregoni on fish declined to 31 lice per fish at Section A and 2.5 lice per fish at Section B. Then, after 28 d of treatment, the number of lice per fish was < 1 at Section A; in contrast the mean number of A. coregoni per fish at the control section was > 20. The prevalence of A. coregoni remained < 50% over a period of 72 d of treatment, but started to increase again thereafter. This suggests that emamectin benzoate concentration in fish remained at a level high enough to kill A. coregoni over a period of 9 wk. Emamectin benzoate was very effective in the control of A. coregoni infesting trout.     

Parasite fauna of bream Abramis brama and roach Rutilus rutilus from a man-made waterway and a freshwater habitat in northern Germany

Fifty specimens each of bream Abramis brama and roach Rutilus rutilus were examined for metazoan parasite fauna and trichodinid ciliates; 25 specimens of each species were collected from the Kiel Canal, a man-made waterway, and a nearby freshwater lake, the Dieksee. This is the first detailed parasitological examination of A. brama and R. rutilus at these locations: 30 parasite species were found, comprising 4 protozoans, 4 myxozoans, 5 digeneans, 3 monogeneans, 2 cestodes, 6 nematodes, 2 acanthocephalans, 3 crustaceans and 1 hirudinean. The crustacean Caligus lacustris occurred in both habitats while 2 other crustacean species, 2 acanthocephalans and 1 hirudinean were recorded exclusively for the lake habitat. Larval as well as adult stages of the different parasite species were found, indicating that both fish species act as intermediate and final hosts in both habitats. The Kiel Canal (total of 17 parasite species) showed a lower parasite species richness for A. brama and R. rutilus (14 and 10 parasite species, respectively) than the lake (25 parasite species). A. brama had a higher parasite richness (22 species) than R. rutilus (16 species) in the lake habitat. Most parasites collected were of freshwater origin. Consequently, the observed infection pattern of both fish species in the waterway is mainly influenced by the limited salinity tolerance of freshwater parasites, which are negatively affected even by a salinity of 2.3 to 4.5. In the central Kiel Canal, neither fish species was infected with marine parasites of low host specifity. These parasites are either limited by the low salinity at this sampling site (<4.5 to 6.0) or they cannot enter the canal due to the environmental conditions prevailing in this artificial brackish water habitat. Thus, the canal may comprise a natural barrier preventing the distribution of North Sea parasites into the Baltic Sea. However, the brackish water Baltic Sea nematodes Paracuaria adunca and Cosmocephalus obvelatus were found in R. rutilus from the canal, demonstrating the ability of some parasite species to invade and extend their range of distribution through this man-made shipping route from the Baltic to the North Sea.     

Host immunization shapes interspecific associations in trematode parasites

1. Individuals of free-living organisms are commonly infected by multiple parasite species. Under such circumstances, positive or negative associations between the species are possible because of direct or indirect interactions, details in parasite transmission ecology and host-mediated factors. One possible mechanism underlying these processes is host immunity, but its role in shaping these associations has rarely been tackled experimentally.
2. In this study, we tested the effect of host immunization on associations between trematode parasites infecting eyes of fish. We first analysed the associations between three species ( Diplostomum spathaceum , Diplostomum gasterostei and Tylodelphys clavata ) in wild hosts, roach ( Rutilus rutilus ) and perch ( Perca fluviatilis ). Second, using rainbow trout ( Oncorhynchus mykiss ) as a model fish species, we experimentally investigated how sequential immunization of the host (i.e. one parasite species infects and immunizes the host first) could affect the associations between two of the species.
3. The results indicated that most of the associations were positive in wild hosts, which supports between-individual variation in host susceptibility, rather than competitive exclusion between the parasite species. However, positive associations were more common in roach than in perch, possibly reflecting differences in ecological conditions of exposure between the host species. The experimental data showed that positive associations between two of the species were eroded by host immunization against one of the parasite species.
4. We conclude that sequential immunization of hosts has a marked effect on interspecific parasite associations and basically can determine if positive associations are detected or not. This implies that correlative results suggesting non-interactive community structure in general may be obscured by the sequence of previous parasite exposure and corresponding dynamics of host immunization.     

A link between ectoparasite infection and susceptibility to bacterial disease in rainbow trout

Rainbow trout, Oncorhynchus mykiss, were infected concomitantly with Argulus coregoni and Flavobacterium columnare and their survival was compared with that of fish infected with either the parasite or the bacterium alone. The mortality of fish challenged with A. coregoni was negligible while infection with F. columnare alone led to significantly lower survival. However, compared with single infections, the mortality was significantly higher and the onset of disease condition was earlier among fish, which were concomitantly infected by A. coregoni and F. columnare. This data presents, for the first time, experimental support for the hypothesis that an ectoparasite infection increases susceptibility of fish to a bacterial pathogen.     

A delayed effect of the aquatic parasite <Emphasis Type="Italic">Margaritifera laevis</Emphasis> on the growth of the salmonid host fish <Emphasis Type="Italic">Oncorhynchus masou masou</Emphasis>

Parasitic species often have detrimental effects on host growth and survival. The larvae of the genus Margaritifera (Bivalvia), called glochidia, are specialist parasites of salmonid fishes. Previous studies have reported negligible influences of the parasite on their salmonid hosts at natural infection levels. However, those studies focused mainly on their instantaneous effects (i.e., during the parasitic period). Given the time lag between physiological and somatic responses to pathogen infections, the effect of glochidial infection may become clearer during the post-parasitic period. Here, we examined whether the effect of glochidial infections of Margaritifera laevis on its salmonid host Oncorhynchus masou masou would emerge during the post-parasitic period. We performed a controlled aquarium experiment and monitored fish growth at two time intervals (i.e., parasitic and post-parasitic periods) to test this hypothesis. Consistent with previous observations, the effects of glochidial infection were unclear in the middle of the experiment (day 50; parasitic period). However, even with a natural glochidial load (48 glochidia per fish), we found a significant reduction in growth rates of infected fish in the extended period of the experiment (day 70; post-parasitic period). Our results suggest that examining only instantaneous effects may provide misleading conclusions about mussel–host relationships.     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh,Northern Ireland

LIGULA (Cestoda: Pseudophyllidea) infections in gudgeon (Gobio gobio) and roach (Rutilus rutilus) differ markedly in the pathology that is observed in the host, particularly with respect to a tissue response and the extent of inhibition of gonadal development. The entire internal transcribed spacer (ITS) region (ITS-1, 5.8S and ITS-2) and the large subunit domains D1-D3 were sequenced and compared in parasites from these fish from Lough Neagh, Northern Ireland, together with a single specimen from minnow (Phoxinus phoxinus) from Wales. Sufficient differences were observed between parasites from R. rutilus and G. gobio to support the suggestion that they may represent different strains/species. In contrast, Ligula from P. phoxinus closely resembled those from R. rutilus. Ligula infections in G. gobio were recorded prior to the introduction of R. rutilus. The co-existence of separate strains or species of Ligula in Lough Neagh probably resulted from the introduction of R. rutilus to these waters, correlated with an increase in the number of great crested grebes (Podiceps cristatus).     

Accumulation of plerocercoids of Triaenophorus crassus in the second intermediate host Coregonus lavaretus and their effect on growth of the host

Patterns of accumulation of Triaenophorus crassus in its second intermediate host whitefish Coregonus lavaretus s.l. were studied between 1991 and 1996 from two host populations in two separate areas of Lake Saimaa, Finland. Whitefish were infected commonly with several T. crassus plerocercoids and the parasites were aggregated into the oldest hosts. In one host population the annual parasite accumulation was 0·9 parasites in all host age groups between 3 and 8 years. In the other host population the annual accumulation was 1·6 parasites in 3–5-year-old fish, but increased up to 3 to 4 parasites per year in fish over 5 years old. The increase did not coincide with the period of maturation or any increase in whitefish growth, both of which could alter the food intake of the fish. The sharp increase in the annual accumulation suggests a threshold intensity above which the probability of acquiring further parasites increases. In spite of a heavy aggregation of parasites there was no evidence of parasite-induced host mortality. The annual increase in mean abundance was not correlated with the mean annual weight increase in 2–4-year-old fish within cohorts. However, evidence of a negative effect of parasites on whitefish growth was revealed by back-calculation of lengths of uninfected and infected whitefish and correlations between length or weight of fish and intensity of infection with fish age. Both analyses suggested that larger young fish harboured more parasites than the smaller ones while in older fish the reverse was true, a pattern that has not been shown earlier for parasitized fish.     

Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout

The habitat and diet choice and the infection (prevalence and abundance) of trophically transmitted parasites were compared in Arctic charr and brown trout living sympatrically in two lakes in northern Norway. Arctic charr were found in all main lake habitats, whereas the brown trout were almost exclusively found in the littoral zone. In both lakes the parasite fauna reflected the niche segregation between trout and charr. Surface insects were most common in the diet of trout, but transmit few parasites, and accordingly the brown trout had a relatively low diversity and abundance of parasites. Parasites transmitted by benthic prey such as Gammarus and insect larva, were common in both salmonid host species. Copepod transmitted parasites were much more common in Arctic charr, as brown trout did not include zooplankton in their diets. Parasite species that may use small fish as transport hosts, were far more abundant in piscivorous fish, especially brown trout. The seasonal dynamics in parasite infection were also consistent with the developments in the diet throughout the year. The study demonstrates that the structure of parasite communities of charr and the trout is highly dependent on shifts in habitat and diet of their hosts both on an annual base and through the ontogeny, in addition to the observed niche segregation between the two salmonid species.     

Genetic variability and components of fitness in hatchery strains of rainbow trout

Two fitness components, development rate and egg size, were examined in six hatchery strains of rainbow trout, Oncorhynchus mykiss (syn. Salmo gairdneri Richardson), with different amounts of enzyme heterozygosity. The average expected heterozygosities per strain ranged from 4 to 8%, based upon an electrophoretic analysis of the protein products of 42 loci. Strains with higher heterozygosities had faster development rates, as measured by hatching time, than strains with lower heterozygosity. Concordance between hatching time and another measure of development rate, degree of yolk-sac resorption, suggests that hatching time is a valid measure of embryonic development rate in salmonid fishes. Earlier-hatching embryos were longer and heavier at the time of yolk-sac resorption than later-hatching fish. Females from more-heterozygous strains also had a tendency to have larger eggs. These data suggest that genetic variation is an important biological resource to be conserved in hatchery stocks.     

Ecological determinants of parasite acquisition by exotic fish species

Disease‐mediated threats posed by exotic species to native counterparts are not limited to introduced parasites alone, since exotic hosts frequently acquire native parasites with possible consequences for infection patterns in native hosts. Several biological and geographical factors are thought to explain both the richness of parasites in native hosts, and the invasion success of free‐living exotic species. However, the determinants of native parasite acquisition by exotic hosts remain unknown. Here, we investigated native parasite communities of exotic freshwater fish to determine which traits influence acquisition of native parasites by exotic hosts. Model selection suggested that five factors (total body length, time since introduction, phylogenetic relatedness to the native fish fauna, trophic level and native fish species richness) may be linked to native parasite acquisition by exotic fish, but 95% confidence intervals of coefficient estimates indicated these explained little of the variance in parasite richness. Based on R²‐values, weak positive relationships may exist only between the number of parasites acquired and either host size or time since introduction. Whilst our results suggest that factors influencing parasite richness in native host communities may be less important for exotic species, it seems that analyses of general ecological factors currently fail to adequately incorporate the physiological and immunological complexity of whether a given animal species will become a host for a new parasite.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Whirling disease: host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and rainbow trout Oncorhynchus mykiss

Scanning electron microscopic studies were conducted on rainbow trout Oncorhynchus mykiss in the first 60 min after their exposure to the triactinomyxon spores of Myxobolus cerebralis. The results demonstrated that as early as 1 min post exposure the whole process, from the attachment of the triactinomyxon spores to the complete penetration of their sporoplasm germs, had occurred. The triactinomyxon spores sought out the secretory openings of mucous cells of the epidermis, the respiratory epithelium and the buccal cavity of trout and used them as portals of entry. Exposure experiments of the triactinomyxon spores of M. cerebralis to non-salmonid fish, such as goldfish Carassius auratus, carp Cyprinus carpio, nose Chondrostoma nasus, medaka Oryzias latipes, guppy Poecilia reticulata and also the amphibian tadpole Rana pipiens as well as to rainbow trout fry indicated a specificity for salmonids. Attempts to activate the triactinomyxon spores by exposure to mucus prepared from cyprinid and salmonid fish showed no significant differences from those conducted in tap water. The results suggest that the simultaneous presence of both mechano- and chemotactic stimuli was required for finding the salmonid fish host.     

Counter-intuitive developmental plasticity induced by host quality

Adaptation to different hosts plays a central role in the evolution of specialization and speciation in phytophagous insects and parasites, and our ability to experimentally rank hosts by their quality is critical to research to understand these processes. Here we provide a counter-intuitive example in which growth is faster on poor quality hosts. The leaf beetles Oreina elongata and Oreina cacaliae share their host plant with the rust Uromyces cacaliae. Larvae reared on infected Adenostyles alliariae show reduced growth rate, reduced maximum weight and longer development time. However, they normally respond adaptively to the rust's mid-season arrival. When switched during development from healthy to infected leaves, larvae accelerate growth and reduce development time, but pupate at lower body weight. In this novel plant-insect-fungus interaction, infection forms the cue to trade off life-history traits in order to complete development within the brief alpine summer. It represents a novel mode of developmental plasticity, which is likely to be found in other host-parasite systems whenever host quality deteriorates due to multiple infection or ageing. This phenotypic plasticity would modify competition after co-infection and the mutual selection imposed by hosts and parasites, and creates a paradoxical negative correlation between growth rate and environmental quality.