Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds

An important pattern in host-parasite assemblages is a higher intensity of parasites in juveniles than in adults, but the reasons for these differences remain obscure. Three non-mutually exclusive hypotheses have been proposed: (1) heavily parasitized juveniles die before being recruited into the adult population ('selection' hypothesis); (2) the development of an acquired immunity by the host in front of the parasite reduces the intensity of the parasite in adult hosts ('immunity' hypothesis); and (3) differences in behavior makes adults less exposed to the parasite than juveniles ('vector exposure' hypothesis). Having rejected the 'vector exposure' hypothesis in a previous study, here we tested the 'selection' and 'immunity' hypotheses in feral pigeons (Columba livia) infected by the blood parasite Haemoproteus columbae. In agreement with the 'selection' hypothesis, young (but not adult) pigeons that were highly parasitized had a lower probability of surviving until adulthood, independent of their body condition. However, selection was not strong enough to account for the observed differences in parasite intensity between age-classes, and after selection parasite intensity of survivors still remained 85% higher in juveniles than in adults. In contrast, the 'immunity' hypothesis offered a greater explanatory power. The intensity of blood parasites in young pigeons, but not in adults, decreased over time so dramatically that by the time they had become adults their intensities were indistinguishable from that typically seen in adults. Therefore, while selection against highly parasitized juveniles can contribute to some extent to a reduction in parasitism seen in the adult population, age-specific blood parasitism in feral pigeons is best explained as a transitory phase just before the host develops an effective immune response.     

Endoparasites of black-bellied whistling ducks in southern Texas.

Endoparasites detected in the black-bellied whistling duck (Dendrocygnaautumnalis) include one nasal mite, four nematodes, three trematodes, five cestodes, and two acanthocephalans. Each of these represents a new host record. Overall, 47% of the birds were parasitized with an average of 12 helminths per infected bird. Helminths were significantly more common in juveniles than in adults; more females than males were parasitized, but the difference was not statistically significant. No correlation existed between the parasite load and the physical condition of the host. Tissue damage in infected birds was minimal and limited to nematode cysts in the proventriculi. Parasite loads were light, apparently reflecting the food habits of the host.     

Interactions between year classes in the benthic amphipod Monoporeia affinis: effects on juvenile survival and growth

Summary The effect of 1-year-old Monoporeia (=Pontoporeia) affinis on the survival and growth of young of the year was studied in laboratory experiments. Amphipods were kept in jars with sediment and a continuous supply of cooled water for 3 months. Adults or juveniles were added to a control density of juveniles. Juvenile mortality increased at higher total densities, and was greater when adults were present. The mean length and dry weight of juveniles decreased at higher densities, but adults did not have a greater effect than juveniles. These density-dependent effects are probably caused by competition for food within and between year classes. Thus, a high abundance of juveniles or adults could reduce the recruitment of juveniles into the adult year-class the following year, and the suppression of juvenile growth could lower fecundity. The results of this experiment support the hypothesis, inferred from field data from the Baltic Sea and Swedish lakes, that intraspecific interactions contribute to fluctuations in the abundance of populations of M. affinis.     

Recruitment in the swash zone – temporal variations in juvenile recruitment of an exposed sand beach surf clam

This study examined factors affecting juvenile recruitment in the tuatua Paphies donacinaon an exposed surf beach in Pegasus Bay, South Island New Zealand between October 1994 and April 1997. Tuatua recruitment followed female gonad maturation with a delay of approximately 2 months. Juveniles (1–10 mm shell length) occurred throughout the study except during June and July 1995 (winter). Average densities (m^–2 ) were 28 in winter, 230 in spring, 174 in summer and 108 in autumn. There was high juvenile mortality and/or emigration and the maximum average density of (741m^–2 ) was recorded in November 1996. Recruit densities were similar between years except during winter. Adult tuatua populations were dominated by modal shell lengths greater than 70 mm.There was no significant relationship between adult and juvenile recruit length. Recruit length decreased with recruit density suggesting density dependent competition for space or food resources. Juvenile density increased following increases in food availability (chlorophyll a concentration) but average length of juveniles did not correlate directly with any of the environmental variables. Recruit density decreased as the modal adult length increased and recruit length reduced when adult populations had a high condition index. Because larvae, juveniles and adult are mobile the beach population is characteristic of an open system with adults and juveniles from the resident population affecting post-settlement density- dependent processes.     

Overwinter body condition,mortality and parasite infection in two size classes of 0+ year juvenile European bitterling Rhodeus amarus

Body condition and parasite abundance were examined in two size classes of European bitterling Rhodeus amarus during the first overwintering period in two seasons (2007–2008 and 2009–2010). Body condition of large fish did not change during winter, and increased significantly in March. From November to February, small fish showed a decreasing trend in condition. Despite a significant increase in March condition of small fish only reached the same level as before winter. Total parasite abundance increased significantly in winter in both fish size classes, reflecting a seasonal increase in monogenean infection. Large fish were parasitized significantly more than small fish during winter, but only in small fish was a negative correlation between parasite infection and condition found and a significant decrease in parasite abundance recorded after wintering, indicating mortality of heavily infected individuals with low condition during the winter. A trend for higher overwinter mortality in small fish was found under semi‐experimental conditions. The decrease in condition during the winter period in small fish may reflect faster energy depletion generally expected in smaller individuals. The results indicate that parasite infection may contribute to the overwinter mortality of 0+ year R. amarus, with a stronger effect in smaller individuals.     

Ectoparasites and age-dependent survival in a desert rodent

Host age is one of the key factors in host–parasite relationships as it possibly affects infestation levels, parasite-induced mortality of a host, and parasite distribution among host individuals. We tested two alternative hypotheses about infestation pattern and survival under parasitism in relation to host age. The first hypothesis assumes that parasites are recruited faster than they die and, thus, suggests that adult hosts will show higher infestation levels than juveniles because the former have more time to accumulate parasites. The second hypothesis assumes that parasites die faster than they are recruited and, thus, suggests that adults will show lower infestation levels because of acquired immune response and/or the mortality of heavily infested juveniles and, thus, selection for less infested adults. As the negative effects of parasites on host are often intensity-dependent, we expected that the age-related differences in infestation may be translated to lower or higher survival under parasitism of adults, in the cases of the first and the second hypotheses, respectively. We manipulated ectoparasite numbers using insecticide and assessed the infestation pattern in adult and juvenile gerbils (Gerbillus andersoni) in the Negev Desert. We found only a partial support for age-dependent parasitism. No age-related differences in infestation and distribution among host individuals were found after adjusting the ectoparasite numbers to the host’s surface area. However, age-related differences in survival under parasitism were revealed. The survival probability of parasitized juveniles decreased in about 48% compared to unparasitized hosts while the survival probability of adults was not affected by ectoparasites. Our results suggest that the effect of host age on host–parasite dynamics may not explicitly be determined by age-dependent differences in ectoparasite recruitment or mortality processes but may also be affected by other host-related and parasite-related traits.     

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.     

Population variables and causes of mortality in a hedgehog (Erinaceous europaeus) population in southern Sweden

A hedgehog population in southern Sweden was studied by capture-mark-recapture during 1972–1979. Each animal was weighed, sexed and marked with one numbered clip in each ear.
The number of subadult and adult hedgehogs was about 20 in the first two years, 1972–1973. Numbers then increased and approximately doubled and the population peaked in 1978. A decrease came in 1979.
The estimated number of juveniles produced varied between years with the lowest figure (15 juv.) in 1974 when the population was low and the highest in 1977 (39 juv.) when the population was high. As no captured subadult female had suckled young, estimates of recruitment rate assumed that females did not reproduce until they were adult. The average number of juveniles per adult female was 2.8. Recruitment rate did not show any correlation with non-juvenile population densities.
For both juveniles and non-juveniles the annual mortality varied greatly between years. Average yearly mortality was 47% for non-juveniles and 34% for juveniles.
For non-juveniles, most of the total mortality occurred during winter, ranging between 26% and 43% (average 33%), and increased with increasing densities of non juveniles. Juvenile winter mortality varied between 6% and 94%, averaging 33%.
Summer mortality of non-juveniles averaged 15%, ranging between 3% and 22%. Traffic kills were the predominant cause of death. Only a few juveniles were found dead during summer and autumn.
There were no statistical differences in age-specific survival rate between males and females and, generally, no differences in survival rate between the age categories within each sex. It is argued that the population size appears to be more influenced by environmental factors, such as food availability, winter nest sites and winter climate, than by density-dependent factors.     

The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex)

SUMMARY 1. The drift of Gammarus pulex in a population in which approximately 20% of adults are infected with the acanthocephalan parasite Pomphorhynchus laevis was monitored at margin and mid-river sites in the River Teme, England over a 24-h period in mid-summer.
2. Drift densities showed a diurnal pattern with a large increase at night, independent of parasite burden.
3. There was no significant effect of site (margin or mid-river) on the proportion of parasitized and unparasitized G. pulex found in the drift or the benthos.
4. The drift of parasitized G. pulex was significantly greater than unparasitized animals. Gammarids harbouring only one parasite were found in significantly higher proportions in the drift than those with two or more parasites.
5. At both sites (margin and mid-river) the proportion of unparasitized adult G. pulex in the drift was significantly lower than that in the benthos. However, there was a significantly higher proportion of parasitized animals in the drift than in the benthos.     

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.     

Ontogeny of microhabitat use and two-step recruitment in a specialist reef fish, the Browncheek Blenny (Chaenopsidae)

Ecological specialization is common on coral reefs and almost certainly contributes to the high diversity of fishes and invertebrates associated with reefs. Here, the recruitment pathway of an endemic Gulf of California fish, the Browncheek Blenny, Acanthemblemaria crockeri (Teleostei: Chaenopsidae), which specializes as an adult on vacant invertebrate tests or tubes, is reported. Like most reef fishes, Browncheek Blennies have a planktonic larval stage that leaves the reef and later settles on suitable habitat as a fully developed juvenile. These blennies follow a clear, “two-step” recruitment pathway, however, and do not reside in invertebrate tests until reaching an adult body size. Individual juveniles and adults were observed for 3 min intervals in order to develop average time budgets for this species. Members of both sexes and all post-settlement life-history stages were included in the analysis. The difference in habitat use by post-settlement juveniles and adults is striking; the average juvenile spends none of its time inside a test, and the average large adult spends all of its time inside a test. Using data on intermediate-sized individuals, the behavioral change associated with invading a test was determined to be size-cued, and it occurs between 20 and 30 mm standard length. Changes in feeding and predator avoidance behaviors are also associated with the ontogenetic shift from life in the open to life in a shelter. Addition of artificial shelters demonstrated the essential role of access to this specialized resource in the population regulation of adults but not juveniles of these blennies.     

Influence of Parasitism on Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae)

Banded killifish, Fundulus diaphanus, were presented individually with a choice of ‘shoaling’ with either of two conspecific stimulus shoals, one consisting of fish with externally visible black spots (indicating the presence of a parasitic trematode worm, Crassiphiala bulboglossa), the other consisting of fish without such spots. Both parasitized and unparasitized test fish significantly preferred to shoal with unparasitized stimulus shoals over parasitized ones. The relative preference of unparasitized killifish for unparasitized shoals increased with increasing degree of parasite load in parasitized stimulus fish. However, no significant preference by unparasitized fish for unparasitized shoals was observed if unparasitized shoals were presented versus mixed shoals consisting of parasitized and unparasitized fish. We conclude that killifish preferred unparasitized shoals over parasitized shoals only if all fish in the respective stimulus shoals were phenotypically uniform (either with or without black spots). A final experiment showed that killifish used black spots as an indicator of parasite presence to make their shoal choice. The significance of these results for the formation of parasite-assorted shoals is discussed.     

Seasonal distribution of juvenile Atlantic cod in the southern Gulf of St Lawrence

Seasonal changes in the geographic distribution of juvenile (ages 1–4) Atlantic cod Gadus morhua were determined from research surveys conducted in the southern Gulf of St Lawrence during 1986–87, 1990–91, and 1994. From late June to early October, juvenile cod were most abundant in shallow water (<50 m deep). By early November, all age groups (adults and juveniles) had migrated to deep (>100 m) offshore waters for the winter. For most juveniles, this represented a minimum migration of >225 km (each way). Age 3 and 4 cod migrated greater distances than age 1 and 2 fish. Some age 3 and 4 cod migrated as far as 650 km from their summer and early autumn areas. Although there was partial geographic segregation of juvenile and adult fish during summer and winter, all age groups were found together during the migration. No cod were present in the shallow waters (<80 m deep) of the south-western Gulf during April due, in part, to later than average ice-melt. Large numbers of all age-classes were present in most of the south-eastern Gulf by mid-May.     

Seasonal population dynamics of Neoechinorhynchus qinghaiensis in the carp, Gymnocypris przewalskii przewalskii, from Qinghai Lake, China

Studies on the seasonal population dynamics of Neoechinorhynchus qinghaiensis (Acanthocephala: Neoechinorhynchidae) in its fish host Gymnocypris przewalskii przewalskii in the Qinghai Lake, China, were carried out with samples taken in May 1991, August 1992, November 1992 and February 1993. Prevalences were higher than 44% in all seasons. The mean intensity of infection was above 124 worms per fish. The maximum intensity of worms recovered from a single fish was 1402 in the autumn of 1992. Differences in the mean abundance, mean intensity and prevalence are not statistically significant relative to season and this is likely to be related to the stable temperatures recorded at the bottom of Qinghai Lake. Over-dispersed distributions of N. qinghaiensis in the host population, due to heterogeneity and feeding habits, were observed in all seasons. The size composition of both sexes of N. qinghaiensis showed males to be less than 3.5 mm and females between 0.5 and 4.25 mm, with the main recruitment phase in the worm populations occurring in the autumn, extending through winter and spring with the lowest recruitment occurring in the summer. The maturation and copulation of worms were mainly focused in the summer season. The sex ratio of female to male was both high in winter (1.51:1) and spring (1.48:1). The higher proportion of females and the change in the worm sex ratio in winter can be attributed to the reduced longevity of male worms. As immature male worms exhibit a higher proportion of the worm population than females in all seasons, further studies are needed to determine if such a situation compensates for the shorter life span of males.     

Factors affecting entomophilic activity of Neoaplectana feltiae in mushroom compost

The host-searching ability of Neoaplectana feltiae Filipjev (= S. bibionis Bovien) (Nematoda: Steinernematidae) in response to larvae of a mushroom fly, Lycoriella solani Winn. was examined in a mushroom substrate. Individuals of L. solani were less attractive for the parasite than larvae of Galleria mellonella L. The nematode juveniles penetrated a 22 cm layer of casing mixture within 2–4 days. In the casing alone nematode effectiveness was better than in mushroom compost or in compost and casing together. In the casing mixture parasite dosages of 20 and 100 juveniles per cm² led to 22% and 45% parasitization of L. solani respectively, while all G. mellonella larvae were parasitized at both dosages. The prevalence of nematode infection depended on the content of water in the mushroom substrate. The highest N. feltiae infectivity was observed, when the ratio of the dry casing weight to the weight of water content was 1: 2.5. The practical aspects of the observed phenomena, essential for the use of N. feltiae in the protection of commercial mushroom cultivation are discussed.     

Parasitism may enhance rather than reduce the predatory impact of an invader

Invasive species can have profound impacts on communities and it is increasingly recognized that such effects may be mediated by parasitism. The ‘enemy release’ hypothesis posits that invaders may be successful and have high impacts owing to escape from parasitism. Alternatively, we hypothesize that parasites may increase host feeding rates and hence parasitized invaders may have increased community impacts. Here, we investigate the influence of parasitism on the predatory impact of the invasive freshwater amphipod Gammarus pulex. Up to 70 per cent of individuals are infected with the acanthocephalan parasite Echinorhynchus truttae, but parasitized individuals were no different in body condition to those unparasitized. Parasitized individuals consumed significantly more prey (Asellus aquaticus; Isopoda) than did unparasitized individuals. Both parasitized and unparasitized individuals displayed Type-II functional responses (FRs), with the FR for parasitized individuals rising more steeply, with a higher asymptote, compared with unparasitized individuals. While the parasite reduced the fitness of individual females, we predict a minor effect on population recruitment because of low parasite prevalence in the peak reproductive period. The parasite thus has a large per capita effect on predatory rate but a low population fitness effect, and thus may enhance rather than reduce the impact of this invader.     

The occurrence and life history of Asymphylodora kubanicum (Platyhelminthes: Digenea: Monorchidae) in the Worcester-Birmingham canal, with special reference to the feeding habits of the definitive host, Rutilus rutilus

Two hundred roach and over 400 molluscs were examined over a one year period to investigate the occurrence and life history of Asymphylodora kubanicum in the Worcester-Birmingham canal. Larval stages, infective to the fish definitive host, were present in molluscs throughout the year but did not show a seasonal fluctuation in numbers. Parasites in the intestine of the roach showed a marked annual cycle of occurrence and maturation: low winter infection levels preceded a dramatic increase in infection during the spring and summer. Maturation of the parasite population was rapid during the spring and summer and in late summer and early autumn the parasites laid their eggs and subsequently died. The death of parasites after egg-laying resulted in the low winter infection level during which time little recruitment occurred.
Roach became infected mainly in their third year when molluscs become a dominant component of their diet. Thereafter the older fishes (<2+) are all equally susceptible to infection, but the larger (older) fishes become more heavily infected because of the greater consumption of molluscs per fish. The sex of the fish made no difference to infection with the parasite.     

Factors affecting the distribution of juvenile estuarine and inshore fish

The differential distributions of juveniles and adults of 25 species of teleost were investigated and compared from four habitat types in sub-tropical Moreton Bay, Queensland. The aim of the study was to identify factors influencing the distribution of juveniles, particularly the species which enter estuaries. The following habitats were sampled: a shallow, sheltered tidal estuary (Caboolture); a shallow, exposed bay with muddy substrates (Deception Bay); an exposed area of sandy substrates and seagrass (Toorbol Point) and a sheltered oceanic site with sandy substrates and seagrass (Kooringal). Data on diet, spawning seasons and recruitment periods of fry are presented together with measurements of salinity, temperature and turbidity. Species entering estuaries recruited mainly in summer (rainy season). The possible preference of juveniles for calm water, the roles of food and predation pressure, the effects of salinity, temperature and turbidity are discussed in relation to the biology and distribution of the fish. Salinity and temperature were probably not important to most juvenile fish. The effects of calm water, suitable food and predators vary according to species. Although all juveniles studied preferred shallow water, in the case of those entering estuaries, turbidity was the single most important factor. Juveniles of the same species occurred in both the estuary and Deception Bay where abiotic and biotic factors other than turbidity were different. During summer, turbidity gradients extended from east to west in Moreton Bay with highest turbidities in Caboolture estuary and Deception Bay. In winter, turbidities throughout Moreton Bay were low and relatively uniform. At this time many of the ‘clear water’ species occurred in Deception Bay. The influence of high turbidity on fish may be linked to reduced predation pressure and perhaps food supply in shallow water. Turbidity gradients in summer may aid fry in locating estuarine nursery grounds. It is apparent however, that juveniles of many species are probably not attracted to estuaries per se but to shallow turbid areas.     

Infracommunity structure of parasites of Hemigymnus melapterus (Pisces: Labridae) from Lizard Island, Australia: the importance of habitat and parasite body size

This study describes the community of all metazoan parasites from 14 individuals of thicklip wrasse, Hemigymnus melapterus, from Lizard Island, Australia. All fish were parasitized, and 4,649 parasite individuals were found. Twenty-six parasite species were identified although only 6 species were abundant and prevalent: gnathiid isopods, the copepod Hatschekia hemigymni, the digenean Callohelmis pichelinae, and 3 morphotypes of tetraphyllidean cestode larvae. We analyzed whether the body size and microhabitat of the parasites and size of the host affected understanding of the structure of the parasite community. We related the abundance, biovolume, and density of parasites with the host body size and analyzed the abundances and volumetric densities of some parasite species within microhabitats. Although the 2 most abundant species comprised 75% of all parasite individuals, 4 species, each in similar proportion, comprised 85% of the total biovolume. Although larger host individuals had higher richness, abundance, and biovolume of parasites than smaller individuals, overall parasite volumetric density actually decreased with the host body size. Moreover, parasites exhibited abundances and densities significantly different among microhabitats; some parasite species depended on the area available, whereas others selected a specific microhabitat. Parasite and habitat size exhibited interesting relationships that should be considered more frequently. Considerations of these parameters improve understanding of parasite community structure and how the parasites use their habitats.