1 Introduction.- 2 Spatial Distribution.- 3 Structure and Function.- 4 Feeding.- 5 Environmental Factors, Metabolism and Energetics.- 6 Growth and Production.- 7 Reproduction.- 8 Inter-specific Interactions.- 9 Population Dynamics.- 10 Ecological Genetics.- 11 Life-history Strategy in Sticklebacks.- References.

A functional biology of sticklebacks

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of these parasites are passed directly between ultimate hosts, others need to navigate through a series of intermediate hosts before reaching a host in (or on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten by specific predators to ensure transmission, has renewed interest in the evolutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and parasitic infections have been demonstrated to have consequences for almost every aspect of fish behaviour. Despite a scarcity of knowledge regarding the mechanistic basis of such behaviour changes in most cases, and an even lower understanding of their ecological consequences, there can be little doubt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency, time budget, habitat selection, competitive ability, predator-prey relationships, swimming performance and sexual behaviour and mate choice have all been associated with – and in some cases been shown to be a result of – parasite infections, and are reviewed here in some detail. Since the behavioural consequences of infections are exposed to evolutionary selection pressures in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found little conclusive evidence for the Parasite Increased Trophic Transmission (PITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of the many behavioural changes described have rarely been quantified, their evolutionary and ecological significance is effectively unknown. Potential hosts may also change their behaviour in the presence of infective parasite stages, if they adopt tactics to reduce exposure risk. Such `behavioural resistance', which may take the form of habitat avoidance, prey selectivity or avoidance of infected individuals, can be viewed as behavioural change associated with the threat of being parasitised, and so is included here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, although the efficacy of the latter as a parasite removal strategy is currently subject to a good deal of debate. The effects parasites have on shoaling behaviour of host fish have attracted a good deal of attention from researchers, and we have provided a case study to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individual's foraging ability. It therefore seems unsurprising that, in a number of species avoidance of parasitised individuals has evolved which may explain the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tendency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for parasitised hosts and their parasites are not always easy to predict, yet an understanding of these is important before we can make predictions regarding the ecological impact of infections on host fish populations. Clearly, there remain many gaps in our knowledge regarding the effects of parasites on the behaviour of host fish. We believe that a much greater understanding of the importance of infection-associated behaviour changes in fish could be gained from high quality research in comparatively few areas. We have completed our review by highlighting the key research topics that we believe should attract new research in this field.

http://web.mnstate.edu/wisenden/AqBiol/Barber%20et%20al%202000.pdf

Effects of parasites on fish behaviour: a review and evolutionary perspective

Multiparasite communities in animals and humans: frequency, structure and pathogenic significance.

A primary difference between predators and parasites is the number of victims that an individual attacks throughout a life-history stage. A key division within natural enemies is whether a successful attack eliminates the fitness of the prey or the host. A third distinctive axis for parasites is whether the host must die to further parasite development. The presence or absence of intensity-dependent pathology is a fourth factor that separates macroparasites from microparasites; this also distinguishes between social and solitary predators. Combining these four dichotomies defines seven types of parasitism, seven corresponding parasites, three forms of predation and, when one considers obligate and facultative combinations of these forms, four types of predator. Here, we argue that the energetics underlying the relative and absolute sizes of natural enemies and their victims is the primary selective factor responsible for the evolution of these different trophic strategies.

Trophic strategies, animal diversity and body size

Interactions between monogenean parasites and their fish hosts.

Infections are described of Gasterosteus aculeatus in a pond at Leeds with the plerocercoid larvae of Schistocephalus solidus.Very heavy infections were found in the summer of 1962 and early 1963; many fish harboured over 50 worms and the maximum was 130.For each individual host the relative percentage parasite-weight to host-weight has been determined (parasitization index). In more than 50% of the fish the P.I. exceeded 25; the maximum value was 68·5. The relationship between P.I., numbers of worms and weight of worms is described.Some effects of parasitization on the host are described; they include gross distension of the body, reduction of liver weight, reduction of packed cell volume of erythrocytes and delay in oocyte maturation. In some heavily parasitized individuals spawning is apparently inhibited.Concurrent infections with the microsporidian Glugea anomala are described.Our thanks are due to Mr A. Rennie, B.Sc., of the Yorkshire Ouse and Hull River Authority for drawing our attention to the source of infected sticklebacks, to Mr A. O. Holliday for the preparation of photographs and to Mr G. R. Standley for assistance in the preparation of the slide shown in PI. 1, fig. 3. We also wish to thank Dr J. N. Ball, Department of Zoology, University of Sheffield, for his helpful comments on the gonads of infected fish, and Professor J. M. Dodd, Department of Zoology, University of Leeds, for providing facilities and much helpful discussion. One of us (C. A.) gratefully acknowledges the receipt of a Science Research Council Research Studentship and Fellowship.

Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects.

Protopolystoma xenopodis (Price, 1943) Bychowsky, 1957 is a parasite of the African clawed toads, species of Xenopus. Adult worms in the host's urinary bladder produce up to 15 eggs/24 h; these are voided with the urine and hatch after 20–24 days (at 26 °C). The swimming oncomiracidia enter the cloaca of the toad and travel via the urinary ducts to the kidneys. Larval development in the kidneys lasts 8–12 weeks (at 22 °C) and the juvenile parasites then migrate to the urinary bladder where maturity is reached after a further 3–4 weeks, i.e. 3–4 months after invasion. Egg production is continuous and parasite longevity has been found to exceed1½ years. Rarely, the adult worms may undertake a return migration from bladder to kidneys.The morphology of the oncomiracidium is described and compared with available accounts of other polystomatid genera. Consideration of data for the genus Polystoma suggests that the arrangement of the epidermal ciliary cells is relatively constant at the inter-specific level. Comparison of Protopolystoma with Polystoma, Diplorchis and Oculotrema reveals that whilst the ciliary cell patterns are clearly related there are important differences in both cell number and disposition at the inter-generic level. Differences are also evident in the distribution of epidermal sensillae in Protopolystoma and Polystoma. Protopolystoma is distinguished from all other polystomatids infecting anuran hosts by the presence of two pairs of haptoral hamuli.

Studies on the biology of Protopolystoma xenopodis (Monogenoidea): the oncomiracidium and life-cycle

Infection of certain species of cyprinid fish with the plerocercoid larva of the cestode Ligula intestinalis is accompanied by a host tissue response.



The tissue reaction is evident in roach Rutilus rutilus as young as three months. An initial cellular infiltration is followed by the laying down of sheets of connective tissue. A case of calcification is described in a single infected rudd Scardinius erythrophthalmus.

Observations on a tissue response within the body cavity of fish infected with the plerocercoid larvae of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea)

Although much information is available on the occurrence of helminth parasites, little is known concerning the composition, size and variability of parasite populations in a particular host species.



Comprehensive data have been compiled from the examination of 135 juvenile and 223 adult starlings from Northern England over a period of nineteen months. Only four of the fifteen species recorded are found in more than 25 per cent of juveniles or adults.



During the first quarter of the year the incidence of infection is low and the numbers of parasites are small, but in the second quarter the incidence and intensity of infection increase rapidly to their maximum levels. Newly fledged juveniles, when they first appear at the end of May, are also universally and heavily infected. The incidence and level of infection in both groups gradually decrease during the remaining six months of the year.



The numbers of parasite species and individuals appear to be related to the incidence of infection. When the incidence is low infected birds always harbour small numbers of parasites; when it is high a large proportion of birds carry heavy or very heavy infections.

R. Wynne Owen

Papers

Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects.

Studies on the biology of Protopolystoma xenopodis (Monogenoidea): the oncomiracidium and life-cycle

Observations on a tissue response within the body cavity of fish infected with the plerocercoid larvae of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea)

Helminth infection of the starling (sturnus vulgaris l.) in northern england

The morphology and biology of Xenopodistomum xenopodis from the gall bladder of the African clawed toad, Xenopus laevis