Helminth Load in Feces of Free-Ranging Blue and Fin Whales from the Gulf of California.

INTRODUCTION: This is the first worldwide systematic and quantitative study to count and identify helminth parasites from 100 blue and 44 fin whale fecal samples collected in the Gulf of California during winter (1993-2014). RESULTS: Blue and fin whale feces had similar prevalence of adult acanthocephalans (Bolbosoma sp.) in feces (18.2% and 14.6%, respectively), but blue whales had significantly higher helminth egg prevalence in feces (100%) and mean intensity (443 ± 318 eggs/g) compared to fin whales (61%, 252 ± 327 eggs/g). Diphyllobothrium sp. eggs were identified in blue whale feces and Diphyllobothridae, Ogmogaster sp. and Crassicauda sp. eggs were identified in fin whale feces. We tested the hypothesis that egg intensity in blue whale's feces varies as a function of age class, reproductive status, sex, preservation and sampling years using a Generalized Linear Model. This model explained 61% of the variance in the helminth egg intensity, but it was not significant. Eighteen blue whale individuals were resampled over time without significant difference between consecutive samples. CONCLUSIONS: Thus, all individual blue whales that migrate to the Gulf of California during winter are permanently parasitized with helminths, while the resident fin whales showed lower prevalence and intensity. This helminth load difference is likely due to their different diets duringsummer-fall, when blue whales feed on other krill species in the California Current System and fin whales shift to school fish prey types in the Gulf of California.

Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system.

Sex-biased parasitism highlights potentially divergent approaches to parasite resistance resulting in differing energetic trade-offs for males and females; however, trade-offs between immunity and self-maintenance could also depend on host body condition. We investigated these relationships in the big brown bat, Eptesicus fuscus, to determine if host sex or body condition better predicted parasite resistance, if testosterone levels predicted male parasite burdens, and if immune parameters could predict male testosterone levels. We found that male and female hosts had similar parasite burdens and female bats scored higher than males in only one immunological measure. Top models of helminth burden revealed interactions between body condition index and agglutination score as well as between agglutination score and host sex. Additionally, the strength of the relationships between sex, agglutination, and helminth burden is affected by body condition. Models of male parasite burden provided no support for testosterone predicting helminthiasis. Models that best predicted testosterone levels did not include parasite burden but instead consistently included month of capture and agglutination score. Thus, in our system, body condition was a more important predictor of immunity and worm burden than host sex.

Effects of parasites and antigenic challenge on metabolic rates and thermoregulation in northern red-backed voles (Myodes rutilus).

Perturbations in host energetics are considered to be an essential pathway for parasite impact on host fitness. However, direct estimations of parasite-induced variations in basal metabolic rates of vertebrate hosts have so far provided contradictory results. The energy requirements of immunity and other vital functions may be compromised in energy-demanding conditions in comparison to comfortable conditions; therefore, in our study performed on the wild red-backed vole, Myodes rutilus, we compared the values of indices that reflect metabolic and thermoregulatory responses to acute cooling in individuals that had been naturally infected by gut helminths or Ixodes persulcatus taiga ticks to individuals with no signs of infestation. To consider the possible effects of an acquired immune response on host energetics, we also injected some of the tested individuals with sheep red blood cells (SRBC). Red-backed voles infected by the nematode Heligmosomum mixtum injected with SRBC showed significantly lower cold-induced maximum oxygen consumption than the saline control. Additionally, individuals infected with H. mixtum showed significantly lower oxygen consumption during the final minute of the 15-min acute cooling period and a significantly greater decline in body temperature than individuals free from helminths. In individuals concurrently infected by H. mixtum and the cestodes Arostrilepis horrida, these indices did not differ from helminth-free individuals. The number of ticks simultaneously parasitizing the voles at the moment of capture correlated positively with their SMR. Our results suggest that even natural parasites produce deleterious effects on host aerobic capacity and thermoregulatory abilities, although the effects of different parasites might not be additive.

Social status and helminth infections in female forest guenons (Cercopithecus mitis).

OBJECTIVE: When resource competition within primate social groups is effective, high-ranking individuals generally gain fitness benefits. Contrary to expectations, female Cercopithecus mitis form linear dominance hierarchies without evidence for rank-related variation in fitness-relevant measures, raising questions about the evolution of guenon social structure. Here, we test whether social status predicts gastrointestinal helminth infections, known to influence health and morbidity in other mammalian hosts. In addition, we assess whether infections contribute to stress responses as indicated by fecal glucocorticoid (fGC) levels. METHODS: We quantified infections and hormone levels in 382 fecal samples from 11 adult female Sykes' monkeys (C. m. albogularis) over four months in one wild study group at Gede Ruins, Kenya. Using a generalized estimating equations technique, we modeled the odds of infection, relative infection intensity, and fGC variation. RESULTS: High-ranking females were less likely infected with Trichuris and Trichostrongylus, had lower fecal egg counts for both taxa, and overall lower helminth richness than low-ranking females. An inverse relationship between rank and Trichuris egg counts existed also in a study population of blue monkeys (C. m. stuhlmanni), where we collected comparable data over a shorter period. Regardless of rank, lactating females were more likely than non-lactating females to be infected with Trichuris, and had higher fecal egg counts for both Trichuris and Oesophagostomum. Lastly, we report evidence that Trichuris infections exacerbated energetic stress and that food supplementation by tourists increased infection levels. CONCLUSION: Our findings suggest that high-rank may provide long-term health and energetic benefits for female C. mitis, with potential fitness implications.

Intestinal helminths induce haematological changes in dogs from Jabalpur, India.

The effect of canine intestinal helminths on the haematological profile of 200 dogs, of both sexes and variable age, visiting university veterinary clinics for routine examination was investigated. The dogs were assigned to parasitized (n = 39) and non-parasitized (n = 161) groups of animals. Coprological examination revealed a 19.5% prevalence of different species of the helminths. Of these animals, 10.25% had mixed infections with Ancylostoma caninum, Toxascaris spp. and Dipylidium caninum. The intensity of A. caninum infection was the highest, with mean egg counts of 951.43 (standard error 88.66), followed by Toxascaris 283.33 (standard error 116.81) and D. caninum. The parasitized animals had significantly lower levels of haemoglobin, packed cell volume and total erythrocyte counts than non-parasitized animals (P < 0.01). Values of other parameters, except for lymphocytes and eosinophils, were not different between the two groups. Analyses of the haematological profile revealed normocytic hypochromic anaemia in the parasitized group of animals.

Neuroimmunoendocrine modulation in the host by helminth parasites: a novel form of host-parasite coevolution?

Helminth parasites have evolved diverse molecular mechanisms that facilitate their establishment, growth and reproduction inside an immunologically hostile environment. Thus, the physiological interactions during the course of the immune response to helminths are complex. Infection induces antigen-specific recognition by the immune system, which is consequently charged with the responsibility of marshalling the appropriate effector responses necessary to destroy the parasite, or at the very least inhibit its progression. Obviously, the immune system should accomplish this task while minimizing collateral damage to the host. As our understanding of the neuroendocrine system grows, it has become increasingly clear that this complex network of neurotransmitters, hormones, and cytokines plays an important role in mediating immunity. Helminths present an especially complex relationship between pathogen and these physiological systems, with hormonally dependent host factors such as sex and age correlated with parasite success. On top of the effect that this particular type of parasites may have on the invaded host, recent experimental evidence suggests that helminth parasites not only actively evade immune response, but are also able to exploit the hormonal microenvironment within their host to favor their establishment, growth and reproduction. This complex strategy of host-parasite relationship is much better exemplified by two helminth parasites: the trematode Schistosoma mansoni and the cestode Taenia crassiceps that respond to adrenal steroids and sexual steroids, respectively. Understanding how the host endocrine system can under certain circumstances favor the establishment of a parasitic infection opens interesting perspectives into the host-parasite relationship field.

The pathogenic helminth parasites of eels.

Although 63 and 55 species of helminths have been reported from each species of Atlantic eel and from 29 to 19 for each species of Pacific eel only the monogeneans Pseudodactylogyrus bini and P. anguillae and the nematode Anguillicola crassus, originally specific to species of Pacific eels, can be considered serious pathogens. None of the three are normally pathogenic to their preferred natural eel host species in the wild. Pseudodactylogyrus spp. only cause serious local gill damage when present on a host in large numbers under optimal conditions that facilitate transmission. This is the case in eel aquaculture, where infections can be controlled by drugs. Anguillicola crassus is only pathogenic to Anguilla anguilla and A. rostrata when Atlantic eels are introduced to the far east or when the parasites have been introduced to Europe. Here the parasite life cycle differs in that A. crassus can infect a wide range of intermediate hosts, employ paratenic hosts and survive as larvae for months in the swimbladder wall. This makes it an excellent colonizer. Its major pathogenic effects on eels result from haemorrhaging in, and thickening of, the swimbladder wall. It reduces the oxygen concentration in the swimbladder, reducing its ability to function as a hydrostatic organ, and increases the stress response of eels. In shallow lakes at warm temperatures this can result in mass mortalities. It is also feared that the parasite affects the ability of eels to migrate to the Sargasso Sea and so contributes to the decline in eel populations. Control by drug treatment is possible in culture, but not in the wild.

Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours.

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host's appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.

Effects of the gill monogenean Zeuxapta seriolae (Meserve, 1938) and treatment with hydrogen peroxide on pathophysiology of kingfish, Seriola lalandi Valenciennes, 1833.

Infections by the gill fluke Zeuxapta seriolae are a serious concern for sea cage aquaculture of kingfish, Seriola lalandi. The present study aimed to determine the pathophysiological effects of a progressive infection with Z. seriolae and the effects of treatment with hydrogen peroxide. For the progression of infection study, infected fish were taken from a sea cage farm, treated to remove parasites and then infected by cohabitation with heavily infected fish. Samples were taken at 2-week intervals for 8 weeks. Infection intensity peaked at 4 weeks post-infection (mean intensity 565.9) and the number of mature worms (2 mm fixed length or larger) peaked at 6 weeks post-infection. Attachment of Z. seriolae appeared to cause little localized pathology; however, the occurrence of hyperplastic lamellae increased as the infection progressed. Haemoglobin concentrations were negatively correlated with Z. seriolae intensity and were lower than controls at 4 weeks (35.8% decrease) and 6 weeks (57.4% decrease) post-infection. Blood lactate concentration and plasma osmolality increased throughout the course of infection. For the effect of treatment experiment, groups of infected and non-infected fish were sampled either before or after treatment with hydrogen peroxide. Treated fish from both infected and uninfected groups had increased plasma lactate, osmolality and pH compared with pre-treatment groups. Treatment with hydrogen peroxide appeared to have acute effects on fish health but the magnitude (e.g. lactate, osmolality) and extent of the effects (e.g. haemoglobin) was much less than that caused by chronic infection with Z. seriolae.

Associations between fish reproductive cycle and the dynamics of metazoan parasite infection.

The parasite fauna of the stone loach (Barbatula barbatula) was investigated monthly from May to December 2001. Four parasite species were recorded: Gyrodactylus spp. (Monogenea), Tylodelphys clavata (Digenea), Proteocephalus sagittus (Cestoda), and Raphidascaris acus (Nematoda). The changes in the seasonal dynamics of parasite infection were investigated throughout the 8 months. The potential effect of the reproductive investment of the host, measured by gonad mass and gonado-somatic index (GSI), on the parasite infection was tested against the prediction that, during periods of high reproductive investment (beginning of the breeding period or forming gonads after breeding), the fish are more susceptible to parasite infection. Differences between parasite loads between genders were also hypothesized. Seasonal differences in infection were observed for all parasite species studied. The values of GSI showed a pattern of energy accumulation in the pre-reproductive period and at the beginning of breeding, a decrease during breeding, and an increase in the post-breeding period. A similar pattern was observed for parasite abundance, a strong or weak increase in spring and/or autumn and a decrease during summer (July and August). Positive correlations between the abundance of Gyrodactylus spp. and R. acus and both gonad mass and GSI were found in females after eliminating the effect of fish weight. Our results suggest that stone loach females are more susceptible to parasite infection in periods of higher reproductive investment. The main factor determining the infection of T. clavata was fish size. The abundance of P. sagittus was positively correlated with GSI in the total fish sample with no detectable effect of sex or fish weight. The increase in cestode infection in spring supports the hypothesis that the parasite life cycle could by synchronized with the beginning of host reproduction, probably induced by increasing fish hormone levels in the spring.

Do helminths increase the vulnerability of released pheasants to fox predation?

The success of ring-necked pheasant (Phasianus colchicus) restocking in Asturias, northern Spain was assessed, and the role of parasites and predators in the mortality of released birds was studied. The experimental release of 56 radio-tagged pheasants showed that 98% of birds died within 12 days. As soon as 72 h after release, 67.5% of males and 55.0% of females were found dead. Foxes (Vulpes vulpes) killed 63% of the birds. The survival of those birds killed by foxes was lower than for birds which died due to other causes, and pheasants depositing eggs of the nematode Eucoleus contortus (Creplin, 1839) survived less than those apparently non-parasitized. No impact of the parasite on the pheasants' condition was found, but foxes preyed upon parasitized birds more than expected by random. The results suggest that: (i) the current pheasant releases in this area are unsuccessful and need to be improved; (ii) this is mainly due to intense predation by red foxes; and (iii) parasites could have some influence on the predation of released birds by foxes. However, the way parasites affect pheasant vulnerability remains unclear.

Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta.

Immunohistochemical and pathological studies were carried out on the digestive tract of parasitized and uninfected specimens of Salmo trutta (L.). A total of 124 brown trout were collected on several occasions from 3 tributaries of the Brenta River, northern Italy. Twenty-eight individuals of S. trutta (22.6%) were parasitized with Pomphorhynchus laevis (Miller, 1776). The occurrence of P. laevis in the trout gut significantly increased the number of endocrine cells immunoreactive to calcitonin gene-related peptide (CGRP), beta-endorphin, met-enkephalin, neuropeptide Y (NPY) and Substance P (SP) antisera. Moreover, bombesin-, cholecistokinin-8- (CCK-8), leu-enkephalin- and serotonin- (5-HT)-like immunoreactive cells were less numerous in the intestine of the parasitized brown trout. A strong positive immunoreactivity was observed in nerve fibres and neurones of the myenteric plexus of the parasitized fish; the antisera involved in this positive reactivity were bombesin, met-enkephalin, SP and vasoactive intestinal peptide (VIP). More neurones immunoreactive to anti-CGRP and anti-5-HT sera were noted in the myenteric plexus and in the inner layer of the tunica muscularis of the infected fish. Most of the above-mentioned neuromodulators are known to control gut motility, digestive/absorptive processes, as well as the immune response. The changes induced by parasites in the neuroendocrine system of the brown trout are discussed.

Increase in milk yield following eprinomectin treatment at calving in pastured dairy cattle.

Gastrointestinal nematodes rarely cause signs of clinical disease in adult cattle. However, they have been shown to exert a negative impact on production in lactating animals, as seen by improved production following elimination of the worms using anthelmintics. A double blind, randomized clinical trial was performed in 28 dairy herds in Canada. The objective of the study was to evaluate the effect of treatment with eprinomectin pour-on solution (IVOMEC EPRINEX) at calving on production, in cattle that have had some exposure to pasture. Cows were randomly allocated to treatment or placebo in blocks of 10, based on calving date, and treated with eprinomectin or placebo on the day of calving. Information on milk production was obtained from all animals, as well as recorded cases of selected diseases. Milk production results from the Canadian dairy herd management system database were analysed using a mixed model with herd as a random effect and test within-cow as a repeated measurement. Test day milk yields from the first six tests after treatment were included in the model, representing a period of between 180 and 200 days in milk (dim). Treated cows produced an additional 0.94 kg of milk per day when compared to the controls over this period. The production effect was independent of calving season, age of the animal and geographical location. No effect of treatment was seen on milk composition, somatic cell count (scc) or on the selected health parameters that were recorded for all included animals. Monthly fecal egg counts (FEC) were performed for eight randomly selected animals in each herd. The observed FEC were low in this study, with a range from 0 to 419 trichostrongyle type eggs per 5g (ep5g) of feces in animals not yet treated with the anthelmintic. The average count was 9.8 and the median was 1.0. FECs dropped immediately after calving and stayed lower for at least 100 days in treated animals when compared to controls. In conclusion, gastrointestinal nematodes appear to have an effect on milk production in Canadian dairy cows that have had some degree of pasture exposure. Eliminating the present subclinical parasite burdens produced a consistent increase in milk production that can yield economic benefits for the dairy producer.

Economics of prophylaxis against peste des petits ruminants and gastrointestinal helminthosis in small ruminants in north Cameroon.

Data on reproduction and mortality were collected over one year from 5100 sheep and 13,300 goats in treated and control flocks. The treated animals received vaccination against peste des petits ruminants (PPR) and anthelmintics twice a year. Productivity parameters (fecundity and mortality rates) obtained with and without prophylaxis were fitted into a benefit-cost economic analysis model and run for project lifespans varying from one to five years. At a 7% discount rate, the overall benefits for a project lifespan of five years were estimated as over 15 million FCFA and 11 million FCFA for sheep and goats, respectively. The benefit-cost ratio ranged from 2.26 to 3.27 in goats and 3.01 to 4.23 in sheep, depending on the project lifespan. It was concluded that PPR and gastrointestinal helminthosis are important causes of economic losses in small ruminants in Cameroon. A national or even a regional vaccination campaign against PPR and strategic anthelmintic treatment of small ruminants are recommended.

Impact of abomasal nematodes on roe deer and chamois body condition in an alpine environment.

Abomasal helminths were examined from 101 roe deer and 43 chamois, shot or found-dead, in the period July-November 1993-95, in the Parco Naturale Paneveggio Pale di San Martino (Italian Eastern Alps). Twelve helminth species were observed in both roe deer and chamois. For both host species, discriminant analysis, using the abundance of each parasite species in the hosts, failed to distinguish between subjects from each of the three study years. For 44 roe deer and 27 chamois data on body weight, body length, foot length, withers height, thoracic circumference and kidney fat index were also available. Principal Component Analysis was performed on the biometrical data in order to group related variables into a few compound variables. In both host species it was possible to identify two principal components, with an explained variance > 80%: the first component, led by body length, was an expression of skeletal development and the second, led by kidney fat index, of nutritional status. Parasite abundance and richness appeared to be negatively correlated with the scores of both skeletal and nutritional Components in the two host species, although only the correlation between parasite abundance and the scores of the nutritional component in roe deer was statistically significant (Spearman r = -0.411; p < 0.05). These results support the susceptibility of roe deer to abomasal helminths, which could be important considering the spatial and nutritional interspecific competition between domestic and wild ruminants often recorded in alpine environments.