Large-scale patterns in trematode richness and infection levels in marine crustacean hosts

Little is known about the patterns of variation in parasitism in marine hosts. Trematodes, the dominant parasites in intertidal systems, are transmitted from their first intermediate hosts (snails) to a range of second intermediate hosts, including crustaceans. Using published studies of trematode infections in crustacean hosts, we investigated general patterns of variation in trematode species richness and infection levels (i.e. percentage of hosts infected and mean number of individual parasites per host). Since the production and release of infective stages in snails is strongly temperature dependent, we also investigated a potential decrease in trematode infection levels with increasing latitude (as a proxy for decreasing temperature). Trematode species richness in the crustacean hosts was generally low (mostly 1 or 2), and infection levels were moderate. However, there were differences among taxa in some groups, particularly among brachyuran crabs, which showed significantly higher values than in other groups. For amphipods, which were the only well-studied group across a large range of latitudes, we found negative correlations between latitude and the trematode species richness or measures of infection level considered here. These relationships persisted after correction of the potentially confounding effects of sampling effort, host body size and host generic identity (as a control for phylogenetic influences). We discuss these findings in light of environmental mediation of parasite transmission, in particular with respect to the probably fundamental role of temperature in driving the output of trematode infective stages in marine systems

Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems

Parasites, in particular trematodes, are unseen but ubiquitous components of marine intertidal ecosystems. Although parasites are known to affect population dynamics and food web structure, their potential function as an unrecognized path of energy flow in these ecosystems is yet to be quantified. We use published data on rates at which trematodes produce free-swimming infective larvae (cercariae) that are released from their gastropod intermediate hosts to investigate patterns in cercarial output as a function of different variables, and to calculate the annual production of cercariae in different marine benthic systems. Across 18 trematode species, cercarial output (no. cercariae shed snail–1 d–1) ranged over 4 orders of magnitude and was positively correlated with snail host species size. While cercarial output did not correlate with latitude, it did correlate negatively with the size of cercariae, and was influenced by the type of downstream host sought by cercariae, being highest when this host was a vertebrate. Our estimates of annual cercarial production (kJ m–2 yr–1), which take into account the density of infected snails in the habitat, were within the range of production values reported for free-living invertebrates inhabiting benthic ecosystems. These estimates would be much higher if they included all trematode species in an ecosystem, and not just single-species values. Overall, results suggest that trematode cercariae represent potentially important paths of energy flow in benthic systems as well as a potentially important food supply to benthic organisms

Efficacy of condensed tannins against larval Hymenolepis diminuta (Cestoda) in vitro and in the intermediate host Tenebrio molitor (Coleoptera) in vivo

Natural anti-parasitic compounds in plants such as condensed tannins (CT) have anthelmintic properties against a range of gastrointestinal nematodes, but for other helminths such effects are unexplored. The aim of this study was to assess the effects of CT from three different plant extracts in a model system employing the rat tapeworm, Hymenolepis diminuta, in its intermediate host, Tenebrio molitor. An in vitro study examined infectivity of H. diminuta cysticercoids (excystation success) isolated from infected beetles exposed to different concentrations of CT extracts from pine bark (PB) (Pinus sps), hazelnut pericarp (HN) (Corylus avellana) or white clover flowers (WC) (Trifolium repens), in comparison with the anthelmintic drug praziquantel (positive control). In the in vitro study, praziquantel and CT from all three plant extracts had dose-dependent inhibitory effects on cysticercoid excystation. The HN extract was most effective at inhibiting excystation, followed by PB and WC. An in vivo study was carried out on infected beetles (measured as cysticercoid establishment) fed different doses of PB, HN and praziquantel. There was a highly significant inhibitory effect of HN on cysticercoid development (p = 0.0002). Overall, CT showed a promising anti-cestodal effect against the metacestode stage of H. diminuta

Four trematode cercariae from the New Zealand intertidal snail 'Zeacumantus subcarinatus' (Batillariidae)

The cercariae and sporocysts (or rediae) of four trematode species are described from the intertidal snail 'Zeacumantus subcarinatus': a distome xiphidiocercaria assigned to the genus 'Renicola' (family Renicolidae); a monostome xiphidiocercaria belonging either to the genus 'Microphallus' or 'Megalophallus' (family Microphallidae); a magnacercous cercaria of the genus 'Galactosomum' (family Heterophyidae); and a cercaria of the genus 'Philophthalmus' (family Philophthalmidae). The morphological features of these cercariae are compared to previously described cercariae of the same genera. In addition, since the philophthalmid cercaria encysts readily on artificial substrates in the laboratory, the metacercaria of this species is also described. These cercariae are part of a diverse community of at least six digenean species parasitising the snail 'Z. subcarinatus' that, together, have a major impact on the ecology and evolution of this snail

The true cost of host manipulation by parasites

If there is one thing that the past three decades of research in behavioural and evolutionary ecology have taught us, it is that there are no free lunches. Adaptive traits provide net fitness benefits to the animals bearing them, but the gains would be even greater if there were no concurrent costs associated with the expression of those traits. The ability of many parasites to enhance their transmission success by manipulating the behaviour of their hosts is one such trait (see Moore, 2002). In their excellent synthesis of past and current research on this phenomenon, Thomas et al. (2005) cast a doubt on the importance of the cost incurred by manipulating parasites. They argue that the existence and magnitude of such costs are dependent upon the type of mechanism used by a parasite to alter host behaviour. Thomas et al. (2005) focus exclusively on physiological, or proximate, costs such as the energetic costs necessary for the production of neuroactive substances in parasite species that use them to modify host behaviour. In a broader evolutionary context, however, one must consider costs at the ultimate level, in terms of fitness. Fitness is usually defined as the average number of surviving offspring produced by individuals with a certain genotype relative to that produced by other genotypes, or as an individual's relative contribution of genes to future generations (Ridley, 1996; Freeman and Herron, 2001), Energy is not the best currency to measure loss of fitness, because other fitness components, such as mortality risk, cannot readily be quantified in units of energy. Elsewhere in their review, in their discussion of mafia-like strategies, Thomas et al. (2005) consider fitness costs, but a similar perspective is needed to assess the cost of manipulation itself. Here, we wish to re-visit the issue of costs associated with manipulation

Parasites modulate the gut-microbiome in insects: A proof-of-concept study.

Host-parasite interactions may be modulated by host- or parasite-associated microbes, but the role of these are often overlooked. Particularly for parasites with intestinal stages (either larval or adult), the host gut microbiome may play a key role for parasite establishment; moreover, the microbiome may change in response to invading parasites. Hypothesis testing at the organismal level may be hampered, particularly in mammalian definitive hosts, by ethical, logistical, and economical restrictions. Thus, invertebrates naturally serving as intermediate hosts to parasites with complex life cycles may inform the development of mammalian models as an early-stage host-parasite model. In addition, several important pathogens are vectored by insects, and insect gut microbiome-pathogen interactions may provide essential base-line knowledge, which may be used to control vectorborne pathogens. Here, we used the grain beetle, Tenebrio molitor, a host of the tapeworm Hymenolepis diminuta, to explore interactions between infection status and resident gut microbiota at two pre-determined time points (day two and seven) post infection. Using 16S/18S microbial profiling, we measured key parameters of the composition, relative abundance, and diversity of the host gut bacteriome and mycobiome. In addition, we quantified the systemic beetle immune response to infection by Phenoloxidase activity and hemocyte abundance. We found significant changes in the gut bacteriome and mycobiome in relation to infection status and beetle age. Thus, the relative abundance of Proteobacteria was significantly higher in the gut of infected beetles and driven mostly by an increased abundance of Acinetobacter. In addition, the mycobiome was less abundant in infected beetles but maintained higher Shannon diversity in infected compared with non-infected beetles. Beetles treated with a broad-spectrum antibiotic (Tetracycline) exhibited significantly reduced parasite establishment compared with the untreated control group, indicating that the host microbiome may greatly influence hatching of eggs and subsequent establishment of H. diminuta larvae. Our results suggest that experimental work using invertebrates may provide a platform for explorative studies of host-parasite-microbe interactions and their underlying mechanisms