Predation risk and reduced foraging activity in fish: experiments with parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L.

After varying periods of food deprivation the foraging behaviour of parasitized and non-parasitized sticklebacks was measured in both undisturbed and recently frightened fish. Parasitized sticklebacks forage significantly more actively and recover more quickly after a frightening stimulus than do control fish. They also react more quickly to food deprivation than do uninfected control fish. Seventy-two hours without food is sufficient to suppress the fright response in parasitized fish, and causes them to forage at the same rate as when undisturbed. Non-infected controls failed to forage successfully after a frightening stimulus, even when they had been without food for 96 h. Frightening stimuli can affect profoundly the normal foraging behaviour of hungry fish.     

Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus.

The three-spined stickleback Gasterosteus aculeatus is an intermediate host of the tapeworm Schistocephalus solidus. Changes in predator avoidance, foraging and shoaling behaviour have been reported in sticklebacks infested with S. solidus, but the mechanisms underlying parasite-induced behavioural changes are not understood. Monoamine neurotransmitters are involved in the control of behaviour and central monoaminergic systems are sensitive to various stressors. Thus, the behavioural effects of S. solidus infestation might be a reflection of changes in brain monoaminergic activity in the stickleback host. The concentrations of 5-hydroxytryptamine (5-HT), dopamine (DA), norepinephrine (NE) and their metabolites 5-hydroxy-indoleacetic acid (5-HIAA), homovanilic acid (HVA) and 3-methoxy-4-hydroxyphenylglycol (MHPG) were measured in the telencephalons, hypothalami and brainstems of parasitized and non-parasitized female sticklebacks held in the laboratory. The ratios of 5-HIAA:5-HT were significantly elevated in both the hypothalami and brainstems of infected sticklebacks. The concentrations of 5-HT and NE were significantly reduced in the telencephalons of infected fish as compared with controls, but there was no elevation of metabolite concentrations. The results are consistent with chronic stress in infected fish, but may also reflect other alterations of neuroendocrine status resulting from parasite infection.     

Pathological and ecological host consequences of infection by an introduced fish parasite

The infection consequences of the introduced cestode fish parasite Bothriocephalus acheilognathi were studied in a cohort of wild, young-of-the-year common carp Cyprinus carpio that lacked co-evolution with the parasite. Within the cohort, parasite prevalence was 42% and parasite burdens were up to 12% body weight. Pathological changes within the intestinal tract of parasitized carp included distension of the gut wall, epithelial compression and degeneration, pressure necrosis and varied inflammatory changes. These were most pronounced in regions containing the largest proportion of mature proglottids. Although the body lengths of parasitized and non-parasitized fish were not significantly different, parasitized fish were of lower body condition and reduced weight compared to non-parasitized conspecifics. Stable isotope analysis (δ(15)N and δ(13)C) revealed trophic impacts associated with infection, particularly for δ(15)N where values for parasitized fish were significantly reduced as their parasite burden increased. In a controlled aquarium environment where the fish were fed ad libitum on an identical food source, there was no significant difference in values of δ(15)N and δ(13)C between parasitized and non-parasitized fish. The growth consequences remained, however, with parasitized fish growing significantly slower than non-parasitized fish, with their feeding rate (items s(-1)) also significantly lower. Thus, infection by an introduced parasite had multiple pathological, ecological and trophic impacts on a host with no experience of the parasite.     

Diel vertical movements,and effects of infection by the cestode <Emphasis Type="Italic">Schistocephalus solidus</Emphasis> on daytime proximity of three-spined sticklebacks <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis> to the surface of a large Alaskan lake

We conducted a field study in Iliamna Lake, Alaska, to test the hypothesis that proximity of three-spined sticklebacks Gasterosteus aculeatus to the lake’s surface during the daytime varies with macroparasitic cestode parasite Schistocephalus solidus infection in a manner consistent with enhanced vulnerability to avian predators. Extensive sampling in the lake and likelihood-based modeling revealed that sticklebacks displayed a diel vertical migration, being closer to the surface at night than during the evening and early morning. Additional sampling, also coupled with a likelihood-based modeling approach, showed that fish caught at the surface of the lake during the day were more often parasitized (76 vs. 65%), more heavily parasitized (26.8 vs. 22.7% of their body mass), and had larger individual parasites (0.24 vs. 0.20 g) than those caught at night. Parasite infection was related, non-linearly, to fish size, which also differed between day and night sampling at the surface. We performed statistical competitions among nested hierarchies of models that accounted for this effect of length. The most likely models indicated that fish captured during the day had greater parasite prevalence, higher parasite burdens, and larger parasites than did fish captured at night. Proximity to the surface during the day in this very clear lake would likely increase the vulnerability of sticklebacks to predation from birds, enabling completion of the parasite’s lifecycle.     

Susceptibility of Prussian carp infected by metacercariae of Posthodiplostomum cuticola (v. Nordmann, 1832) to fish predation

The susceptibility of prey fish infected by metacercariae of Posthodiplostomum cuticola (Digenea: Diplostomatidae) to the predation of non-host predators under experimental conditions was investigated. Parasitized young-of-the-year Prussian carp Carassius auratus were consumed significantly more often by perch Perca fluviatilis compared to non-parasitized individuals, independent of Prussian carp density. The proportion of parasitized and non-parasitized fish consumed by the predator remained stable at four different prey densities. The probability of predation did not increase with the intensity of parasite infection. The effect of P. cuticola on the host seems to result mostly from pathological changes (poor condition, black spots). However, our results provide evidence of higher probability of parasitized Prussian carp being consumed by fish predators under experimental conditions.     

丽蝇蛹集金小蜂寄生对寄主蛹可溶性蛋白与芳基蛋白组成与含量的影响

为了探讨蛹期寄生蜂对寄主蛋白代谢的寄生生理效应,利用Bradford蛋白含量测定法、Western免疫印迹法及酶联免疫吸附检测法研究了棕尾别麻蝇Boettcherisca peregrina蛹被丽蝇蛹集金小蜂Nasonia vitripennis寄生后其脂肪体和血淋巴中可溶性蛋白及芳基蛋白组成与含量的变化。结果表明：寄生蛹脂肪体和血淋巴中可溶性蛋白的组成与未寄生相比基本无明显差异; 不论寄生与否寄主蛹脂肪体和血淋巴中芳基蛋白亚基分子量均为80 kDa,该亚基在脂肪体中未出现降解现象,而在血淋巴中仅于寄生后12 h的寄主蛹中呈现2条分子量相近的Western免疫印迹带,说明其降解可能先于未寄生对照。就含量而言,寄生蛹脂肪体中可溶性蛋白含量除寄生后24 h外均显著低于未寄生对照,芳基蛋白含量除寄生后48 h外也均显著低于未寄生对照,其中寄生后12 h的含量仅为未寄生的32.0%。寄生蛹血淋巴中可溶性蛋白含量多低于未寄生蛹,且寄生后2,12,24 h的差异达显著水平;芳基蛋白的含量均有低于未寄生的趋势,其中寄生后12 h的含量为未寄生的17.0%。综合认为,丽蝇蛹集金小蜂的寄生可导致寄主脂肪体和血淋巴中可溶性蛋白及芳基蛋白含量下降。     

Two tachinid species discriminate between parasitized and non-parasitized hosts

The abilities ofMyiopharus doryphorae (Riley) andM. aberrans (Townsend) (Diptera: Tachinidae) to discriminate between parasitized and non-parasitized Colorado potato beetle (host)Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) larvae, were investigated under laboratory and field conditions. Laboratory experiments showed that bothMyiopharus species have a significantly greater frequency for larvipositing in non-parasitized hosts over parasitized ones. Direct field observations of larvipositional behavior of bothMyiopharus species over three growing seasons showed effective restraint from larviposition into parasitized hosts, while larviposition into nonparasitized ones occurred readily. Avoidance of previously-parasitized hosts occurred after the larvipositing flies briefly landed on host larvae without attempting to insert the larvipositor. The low levels of superparasitism which occurred in the caged experiments and in the field appeared to be due to a breakdown of the larvipositing parasitoids' restraint when they met only parasitized hosts or when many parasitoids competed for reduced numbers of hosts late in the season.     

Social wasp parasites affect the nestmate recognition abilities of their hosts (<Emphasis Type="Italic">Polistes atrimandibularis</Emphasis> and <Emphasis Type="Italic">P. biglumis</Emphasis>, Hymenoptera,Vespidae)

Summary. Queens of the parasitic social wasp, Polistes atrimandibularis, temporarily mimic the odor of their host species, Polistes biglumis, but their offspring have parasite-specific odors. As a consequence, in parasitized colonies individuals with different odors co-inhabit the colony and host workers, who are responsible for colony defense, accept wasps with different odors. In order to verify whether this particular condition causes a change in recognition abilities of hosts, we tested nestmate/non-nestmate discrimination in field colonies invaded by social parasites (and in non-parasitized colonies as controls). Results show that parasitized colonies distinguish between nestmates and non-nestmates, distinguish their parasite queen from those that usurped alien colonies, and accept their parasite's non-mimetic offspring but make more recognition errors than non-parasitized colonies. The optimal acceptance threshold model predicts that when the frequency of encountering non-kin increases, residents become less permissive towards intruders. However, my data show that parasitized colonies are more permissive towards non-nestmates with respect to non-parasitized colonies but they are also more aggressive towards nestmates, suggesting that host workers' learning abilities are impaired.     

Juvenile three-spined sticklebacks avoid parasitized conspecifics

Synopsis Juvenile three-spined sticklebacks,Gasterosteus aculeatus, were given a series of four choice tests to determine whether they avoided schools of conspecifics in which individuals were parasitized with the ectoparasiteArgulus canadensis. Results from these tests indicate that juvenile sticklebacks can avoid schools of parasitized conspecifics. Furthermore, parasites alone did not elicit an avoidance response, suggesting that it is both the presence of the parasite and its effect on stickleback behavior that causes avoidance of parasitized individuals.     

Potential interactions between metazoan parasites of the Mayan catfish Ariopsis assimilis and chemical pollution in Chetumal Bay,Mexico

The effect of pollutants on the intensity of infection of metazoan parasites in the Mayan catfish, Ariopsis assimilis was investigated. Data were collected on pollutants and metazoan parasites from 76 catfish from five localities in Chetumal Bay in October, 1996. Nineteen pollutants (pesticides, polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs)) were found in the catfish livers. Heavy metal content was not determined. Nineteen metazoan parasite species were recovered. After controlling for fish length and sampling station, there was a significant negative linear relationship between the intensity of the larval digenean Mesostephanus appendiculatoides and 1,1,1,-trichloro-2,2-bis (4-chlorophenyl) ethane (DDT) concentrations. This negative relationship may be explained either by the effect of the pesticide on the mortality of (i) free-living larval forms, (ii) metacercariae in the fish, (iii) infected fish or (iv) intermediate host snails. There were significant differences between fish parasitized and not parasitized with M. appendiculatoides with respect to their DDT concentrations. There were also significant differences between the variances of the mean Clark's coefficient of condition values between catfish parasitized and not parasitized by M. appendiculatoides, with the variance of non-parasitized catfish being significantly larger. The results provided statistical evidence that DDT has a detrimental effect on M. appendiculatoides infection intensity. Furthermore, the significantly larger variance value of Clark's coefficient for non-parasitized fish suggested that DDT affects both the parasite and general host condition.     

Group Choice as a Function of Group Size Differences and Assessment Time in Fish: The Influence of Species Vulnerability to Predation

The shoal-choice behaviour of two species of fish that differ in their vulnerability to predation was compared. Individuals of threespine stickleback, Gasterosteus aculeatus, and creek chub, Semotilus atromaculatus, were presented with a simultaneous choice of two equidistant stimulus shoals of conspecifics that differed in membership size (5 vs. 6 fish, 5 vs. 7, 5 vs. 8, 5 vs. 9 and 5 vs. 10). Test fish were allowed to view the stimulus shoals from a standard distance for either 10–20 or 120–150s before being frightened with a stimulus from an overhead light and released to join either shoal. We observed which shoal (the smaller or the larger one) the test fish approached. Preference for the larger stimulus shoal generally increased with increasing shoal size difference and with the duration of the assessment period, and was more pronounced in chub (the more vulnerable of the two species). For the short assessment period, chub showed a significantly stronger preference for the larger stimulus shoal than sticklebacks, whereas there was no significant difference between species for the long assessment period. Furthermore, chub responded more readily to small differences in shoal size (of 1–3 fish) than sticklebacks, for both short and long assessment periods. The above results are consistent with the hypothesis that chub, as the more vulnerable of the two species (in terms of predation), should be able to identify the larger of two shoals more quickly and should be more sensitive to small differences in shoal size than sticklebacks.     

Conspicuous behaviour of Fundulus heteroclitus associated with high digenean metacercariae gill abundances

Fundulus heteroclitus from six sites throughout the Hackensack Meadowlands District in northern NJ, U.S.A., were examined. Differences in behaviour (surfacing, conspicuousness and activity) were compared to gill infection intensity. Fish from populations infected with >1500 digenean metacercariae of Ascocotyle phagicola diminuta and Echinochasmus schwartzi , spent significantly more time at the water surface and exhibited significantly more conspicuous behaviour ( e.g. jerking) than fish from less parasitized populations. This more conspicuous behaviour has the potential to increase trophic transmission of the parasite to its definitive wading-bird host.     

Intraspecific nest parasitism and anti-parasite behavior in the grey starling,Sturnus cineraceus

I studied intraspecific nest parasitism in the grey starlingSturnus cineraceus in 1992 and 1993. The population in this study consisted of 290 nests (157 nests in 1992 and 133 nests in 1993) in which the clutches were completed before May 10 in the year studied. Twenty-nine nests in 1992 and 32 nests in 1993 contained at least 1 parasitic egg. Hatching success per nest of parasitized nests was slightly higher than that of non-parasitized nests. However, fledging success per nest of parasitized nests was significantly lower than that of non-parasitized nests. Thus parasitism appeared to reduce the reproductive success of hosts. Hosts exhibited a few behaviors that minimized the potential cost of brood parasitism. These behaviors included throwing out the parasitic egg and nest guarding. Hosts threw out parasitic eggs before the onset of laying, but they never did so to parasitic eggs laid after that period. The nest guarding level was low during the hosts’ laying periods, and one observed nest was parasitized during this time. Thus, nest-guarding behavior was not effective as an anti-parasite behavior. Grey starlings do not appear to adopt strategies effective in reducing parasitism.     

Oviposition Behavior and Conspecific Host Discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a Fruit Fly Parasitoid

We studied conspecific host discrimination and oviposition behavior of Diaschasmimorpha longicaudata (Ashmead), in third instar Anastrepha ludens (Loew) under laboratory conditions. The complete process of oviposition in D. longicaudata required an average of 29±11.7 s (Mean±SE), during which time the female remained completely immobile. This contrasts with attempts to oviposit for lesser durations (2-4 s), during which the female constantly moved her antennae and abdomen. In order to determine the host discrimination ability of this species (i.e., the capacity to distinguish between parasitized and non-parasitized hosts), third-instar A. ludens non-parasitized or parasitized 24 h earlier, were exposed simultaneously to individual female wasps with or without previous oviposition experience. An identical test was performed using larvae parasitized 48 h earlier. Both types of females showed a similar behavioral pattern of oviposition, but with significant differences in the number of eggs laid in parasitized and non-parasitized larvae. Experienced females showed reduced incidence of oviposition in parasitized larvae as well as a greater number of probes that did not lead to parasitism (rejection), although this difference was only significant in the 24-h test. This suggests that the host discrimination capacity of this parasitoid is innate and that previous oviposition experience increases the discrimination ability of females.     

Further evidence for size-assortative schooling in sticklebacks

Using brook ( Culaea inconstans ) and 10-spined ( Pungitius pungitius ) sticklebacks we examined body-size related schooling behaviour. Small and large sticklebacks were allowed to choose between two test schools, of small and of large individuals, with and without a piscivorous fish ( Oncorhynchus mykiss ) visible. Sticklebacks of both species preferred the company of fish of matching body size: small fish associating with a school of small fish, large fish with a school of large fish. While no interspecific differences were found in responses to school selection, body size and predator presence did affect selection of school-type. In both species, small fish tended to show a stronger preference for matching schools. The preference was enhanced in small fish with presence of a predator, but not in large fish. These observations are further evidence for assortative schooling in sticklebacks.     

Hypoxia and the antipredator behaviours of fishes

Hypoxia is a phenomenon occurring in marine coastal areas with increasing frequency. While hypoxia has been documented to affect fish activity and metabolism, recent evidence shows that hypoxia can also have a detrimental effect on various antipredator behaviours. Here, we review such evidence with a focus on the effect of hypoxia on fish escape responses, its modulation by aquatic surface respiration (ASR) and schooling behaviour. The main effect of hypoxia on escape behaviour was found in responsiveness and directionality. Locomotor performance in escapes was expected to be relatively independent of hypoxia, since escape responses are fuelled anaerobically. However, hypoxia decreased locomotor performance in some species (Mugilidae) although only in the absence of ASR in severe hypoxia. ASR allows fish to show higher escape performance than fish staying in the water column where hypoxia occurs. This situation provides a trade-off whereby fish may perform ASR in order to avoid the detrimental effects of hypoxia, although they would be subjected to higher exposure to aerial predation. As a result of this trade-off, fishes appear to minimize surfacing behaviour in the presence of aerial predators and to surface near shelters, where possible. For many fish species, schooling can be an effective antipredator behaviour. Severe hypoxia may lead to the disruption of the school unit. At moderate levels, hypoxia can increase school volume and can change the shuffling behaviour of individuals. By altering school structure and dynamics, hypoxia may affect the well functioning of schooling in terms of synchronization and execution of antipredator manoeuvres. School structure and volume appear to be the results of numerous trade-offs, where school shape may be dictated by the presence of predators, the need for energy saving via hydrodynamic advantages and oxygen level. The effects of hypoxia on aquatic organisms can be taxon specific. While hypoxia may not necessarily increase the vulnerability of fish subject to predation by other fish (since feeding in fish also decreases in hypoxia), predators from other taxa such as birds, jellyfish or aquatic mammals may take advantage of the detrimental effects of hypoxia on fish escape ability. Therefore, the effect of hypoxia on fish antipredator behaviours may have major consequences for the composition of aquatic communities.     

Host behaviour alteration by its parasite: from brain gene expression to functional test

Many parasites with complex life cycles modify their intermediate hosts'' behaviour, presumably to increase transmission to their final host. The threespine stickleback (Gasterosteus aculeatus) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S. solidus to determine the proximal causes of these behavioural alterations. We show that infected fish have altered expression levels in genes involved in the inositol pathway. We thus tested the functional implication of this pathway and successfully rescued normal behaviours in infected sticklebacks using lithium exposure. We also show that exposed but uninfected fish have a distinct gene expression profile from both infected fish and control individuals, allowing us to separate gene activity related to parasite exposure from consequences of a successful infection. Finally, we find that selective serotonin reuptake inhibitor-treated sticklebacks and infected fish do not have similarly altered gene expression, despite their comparable behaviours, suggesting that the serotonin pathway is probably not the main driver of phenotypic changes in infected sticklebacks. Taken together, our results allow us to predict that if S. solidus directly manipulates its host, it could target the inositol pathway.     

Intraspecific variation in behaviour: effects of evolutionary history, ontogenetic experience and sex

Geographical variation in behaviour within species is common. However, how behavioural plasticity varies between and within locally adapted populations is less studied. Here, we studied behavioural plasticity induced by perceived predation risk and food availability in pond (low predation - high competition) vs. coastal marine (high predation - low competition) nine-spined sticklebacks (Pungitius pungitius) reared in a common garden experiment. Pond sticklebacks were more active feeders, more risk-taking, aggressive and explorative than marine sticklebacks. Perceived predation risk decreased aggression and risk-taking of all fish. Food restriction increased feeding activity and risk-taking. Pond sticklebacks became more risk-taking than marine sticklebacks under food shortage, whereas well-fed fish behaved similarly. Among poorly fed fish, males showed higher drive to feed, whereas among well-fed fish, females did. Apart from showing how evolutionary history, ontogenetic experience and sex influence behaviour, the results provide evidence for habitat-dependent expression of adaptive phenotypic plasticity.     

Influence of Nematode Parasitism,Body Size,Temperature, and Diel Period on the Flight Capacity of <Emphasis Type="Italic">Sirex noctilio</Emphasis> F. (Hymenoptera: Siricidae)

Sirex noctilio F. (Hymenoptera: Siricidae) is a woodwasp of pine trees that has recently invaded and established in North American forests. Although S. noctilio has had a limited impact in North America to date, there is some concern that it could have a significant impact on pine plantations, especially in the southeastern U.S.A. Moreover, there are few data on the flight capacity of male S. noctilio. We found no association between parasitism by D. siricidicola and whether or not S. noctilio initiated flight on the flight mill. Male wasps that were parasitized by nematodes were heavier than non-parasitized males, but there was no significant difference in mass between parasitized and non-parasitized females. We also examined the flight capacity of male and female S. noctilio in relation to nematode parasitism, body mass, temperature (for only males), and diel period. Body mass, temperature, and diel period affected flight in S. noctilio such that wasps were generally observed to fly faster, farther, and more frequently if they were heavier, flying at warmer temperatures, and flying during the photoperiod. The fact that nematode-parasitized male wasps were found to fly farther than the non-parasitized males is consistent with the hypothesis that nematode parasitism does not negatively affect the flight capacity of S. noctilio.