Insularity affects head morphology,bite force and diet in a Mediterranean lizard

Island environments differ with regard to numerous features from the mainland and may induce large‐scale changes in most aspects of the biology of an organism. In this study, we explore the effect of insularity on the morphology and performance of the feeding apparatus, a system crucial for the survival of organisms. To this end, we examined the head morphology and feeding ecology of island and mainland populations of the Balkan green lizard, Lacerta trilineata. We predicted that head morphology, performance and diet composition would differ between sexes and habitats as a result of varying sexual and natural selection pressures. We employed geometric morphometrics to test for differences in head morphology, measured bite forces and analysed the diet of 154 adult lizards. Morphological analyses revealed significant differences between sexes and also between mainland and island populations. Relative to females, males had larger heads, a stronger bite and consumed harder prey than females. Moreover, island lizards differed in head shape, but not in head size, and, in the case of males, demonstrated a higher bite force. Islanders had a wider food niche breadth and included more plant material in their diet. Our findings suggest that insularity influences feeding ecology and, through selection on bite force, head morphology. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 469–484.     

Gyro-scope: an individual-based computer model to forecast gyrodactylid infections on fish hosts

Individual-based computer models (IBM) feature prominently in current theoretical ecology but have only been applied in a small number of parasitological studies. Here we designed an IBM to simulate the infection dynamics of gyrodactylid parasites and immune defence of na?ve hosts (i.e. fish previously not exposed to these parasites). We compared the results of the model with empirical data from guppies (Poecilia reticulata) infected with Gyrodactylus parasites. The laboratory experiments on guppies showed that larger fish acquired a heavier parasite load at the peak of the infection. The survival probability declined with increased body size and no fish survived a parasite load of 80 or more worms in this experiment (i.e. lethal load). The model was a good predictor of the Gyrodactylus infection dynamics of guppies and the model output was congruent with previously published data on Gyrodactylus salaris infections of salmon (Salmo salar). Computer simulations indicated that the infections persisted longer on larger hosts and that the parasite load increased exponentially with the body size of the host. Simulations furthermore predicted that the parasite load of fish with a standard length in excess of 17mm (i.e. the size of adult guppies) reached a lethal load. This suggests that in the conditions of the experiment, the immune defence of na?ve guppies can offer moderate protection against gyrodactylid infections to juveniles, but not to na?ve adult guppies. The model is a useful tool to forecast the development of gyrodactylid infections on single hosts and make predictions about optimal life history strategies of parasites.     

Ecological consequences of ontogenetic changes in head shape and bite performance in the Jamaican lizard Anolis lineatopus

It has been documented extensively that body size affects the physiology and musculoskeletal function of organisms. However, less well understood is how body size affects the ecology of organisms through its effects on physiology and performance. We explored the effects of body size on morphology and performance in different ontogenetic classes and sexes of a common Anolis lizard ( A. lineatopus ). Next, we tested whether these morphological and performance differences may affect functional aspects of the diet such as prey size and prey hardness. Our data showed that males, females and juveniles differ significantly in head size, head shape and bite force. Multiple regression models indicated that head shape and bite force are significantly correlated to prey size and hardness. Yet juveniles had relatively large heads and bit disproportionately hard for their size, allowing them to eat prey as large as those of females. However, for a given prey size, males and females ate more robust prey than did juveniles. Additionally, males ate relatively harder prey than did juveniles. These data suggest that: (1) body size affects the dietary ecology of animals through its effect on head size and bite force; (2) changes in head morphology independent of changes in overall size also have important effects on performance and diet.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 443–454.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence

There is large spatial and temporal variation in the Gyrodactylus parasite fauna across natural guppy (Poecilia reticulata) populations in Trinidad. The life history evolution of these fish could be affected differently in the various habitats depending on the local parasite selection pressure. Here, we experimentally infected three guppy populations with three gyrodactylid strains in the laboratory and monitored the infection by recording the number of parasites and host mortality in a full factorial design. The origin of the guppy population and parasite strain, and the size of the hosts explained significant variation in the survival of hosts. Larger fish carried the highest parasite loads and experienced the highest mortality rates, which suggests that parasite-mediated selection may favour smaller phenotypes, possibly counter-balancing selection pressures by gape-limited predators, mate choice and female fecundity. We observed significant variation in virulence between parasite strains with the captive-bred experimental strain (Gt3) causing the highest mortality of hosts whilst reaching only relatively low maximum burdens. This suggests that adaptations to the captive environment and/or inbreeding depression may alter the virulence of such captive-bred parasites. There were significant differences in survival rate between guppy populations, with infected guppies from the large population of the Lower Aripo River showing a higher survival rate than the fish from the small and genetically less diverse Upper Aripo River population.     

Parasites grow larger in faster growing fish hosts

Parasites depend on host-derived energy for growth and development, and so are potentially affected by the host's ability to acquire nutrients under competitive foraging scenarios. Although parasites might be expected to grow faster in hosts that are better at acquiring nutrients from natural ecosystems, it is also possible that the most competitive hosts are better at countering infections, if they have an improved immune response or are able to limit the availability of nutrients to parasites. I first quantified the ability of uninfected three-spined sticklebacks Gasterosteus aculeatus to compete in groups for sequentially-presented food items, and then exposed either the best or worst competitors to infective stages of the cestode Schistocephalus solidus. Fish were subsequently raised in their original groups, under competitive feeding regimes, for 96 days, after which fish and parasite growth was determined. Unexpectedly, pre-exposure host competitive ability had no effect on susceptibility to infection, or on post-infection growth rate. Furthermore, despite a 120-fold variation in parasite mass at the end of the study, pre-infection competitive ability was not related to parasite growth. The closest predictor of parasite mass was body size-corrected host growth rate, indicating that the fastest growing fish developed the largest parasites. Faster growing hosts therefore apparently provide ideal environments for growing parasites. This finding has important implications for ecology and aquaculture.     

Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae)

This is the first study to demonstrate significant differences between two natural Trinidadian guppy populations in susceptibility to a pathogenic monogenean parasite, Gyrodactylus turnbulli . Following experimental infection with an isogenic laboratory culture of G. turnbulli , fish from the Upper Aripo (UA) lost parasites more slowly and carried up to three times as many parasites at peak infection than did those from the Lower Aripo (LA). The UA population appeared to be more susceptible than the LA fish, even though fish of both populations were naïve to this particular laboratory strain of G. turnbulli and had not encountered any gyrodactylid infection for at least 65 days. The parasite infection reduced the feeding response and feeding activity of UA and LA fish to a similar extent. Our findings suggest that this ectoparasite may have an important impact on the evolutionary biology of guppies (and possibly of other teleosts), particularly as the prevalence of Gyrodactylus infection in natural populations may be as high as 50%. We discuss the role of parasite infections on natural and sexual selection, the good genes model and the implications for immunogenetics in small genetically isolated host populations.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 645–651.     

Changes in ventral head width, a discriminating shape factor among African cichlids, can be induced by chronic hypoxia

A massive enlargement of the gill surface proved to be an important factor in the hypoxia survival of young cichlids. Because the heads of cichlids are densely packed with structures related to both feeding and breathing, we hypothesized that the extra space needed for gill enlargement requires such large structural reorganizations that outer head shape is affected. We used a three-dimensional model to describe changes in the outer head shape of cichlids. Broods of cichlids of different phylogenetic lineages, habitats, and trophic specialization were split and raised at either 10% or 80–90% air saturation. Despite the above-mentioned differences between the species that were used, all hypoxia raised groups showed similar volume enlargements. Volume increases were most prominent in the ventral suspensorial and ventral opercular subcompartments. A relation with the enlarged gills of hypoxia raised fish is likely because the gills are mainly located in these compartments. The differences in ventral width correspond to those found in other studies comprising a wide variety of genotypic and phenotypic variations. The present study shows that such variation in the ventral width is conceivable by phenotypic plasticity alone.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 608–619.     

Infection dynamics of Cichlidogyrus tilapiae and C. sclerosus (Monogenea, Ancyrocephalinae) in Nile tilapia (Oreochromis niloticus L.) from Uganda

The infection dynamics of the gill monogeneans Cichlidogyrus tilapiae and C. sclerosus on Oreochromis niloticus with respect to habitat type (reservoir, stream, ponds and cages), host sex, size and seasons was determined between January and November 2008. During the study period, 45.2% of the 650 fish examined were infected with Cichlidogyrus spp. The infected hosts harboured an average of 8.6 ± 3.4 parasites/fish. Across habitat types, the proportion of infected fish was not statistically different. In contrast, the number of parasites recorded on infected fish from different habitat types differed significantly. The highest parasite number was recorded in reservoir-dwelling fish and lowest in stream-dwelling hosts. Concerning sex, more female O. niloticus were infected and harboured a high number of parasites than male and sexually undifferentiated fish. A weak negative relationship was found between rainfall and monthly parasite infections. However, a higher number of parasites and proportion of infected hosts were found during dry than in wet seasons, except in ponds. Results of this study show that differential exposure due to changes in fish behaviour associated with habitat modification and sex may account for the infection difference across the sampled sites. Meanwhile, rainfall and the associated hydrological events are important factors regulating monogenean infections in tropical aquatic environments. The continuous presence of Cichlidogyrus spp. in fish provides evidence of possible parasite outbreaks, indicating the application of biosecurity measures as crucial for the success of intensive fish farming.     

Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea).

In European freshwater, cyprinid fish may be heavily infected by plerocercoids of the pseudophyllidea cestode Ligula intestinalis (L.). During their development, these parasites grow rapidly to a large size in the fish's body cavity, characteristically distending the abdomen. In this study, the influence of this tapeworm on roach (Rutilus rutilus L.) morphology was analyzed. Forty-five infected and 45 uninfected roach were collected from the Lavernose-Lacasse gravel pit in Toulouse, south western France and examined for 40 morphological measurements to study phenotypic modification of the body and 14 bilateral characters for an analysis of asymmetry. Results indicate that the degree of bilateral asymmetry does not change between infected and uninfected roach, despite the strong host-morphological modifications such as deformation of the abdomen, fin displacements at the level of the tail, and sagging of the vertebral column. The intensity of abdominal distension and fish morphology changes depends on the total parasite biomass present. Differences were observed in morphology at different levels of infection, which relate to established effects of L. intestinalis on the physiology and behavior of intermediate hosts. These morphological changes induced by the parasite could increase trophic transmission to the definitive avian hosts.     

Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata

Histological examinations were carried out on the stomach, pyloric caeca and 4 different parts of the intestine, as well as the rectum, hepatopancreas, gall bladder and spleen of 52 sea bream Sparus aurata spontaneously infected by Enteromyxum leei. Fifteen fish from a non-infected farm were included as a control. Clinical signs appeared only in extensively and severely infected fish. We observed Enteromyxum leei almost exclusively in the intestinal tract, and very rarely in the intrahepatic biliary ducts or gall bladder. We observed heavily infected intestinal villi adjacent to parasite-free villi. Histological changes indicated a parasite infection gradually extending from villus to villus, originating from an initial limited infected area probably located in the rectum. The parasite forms were exclusively pansporoblasts located along the epithelial basement membrane. Periodic acid-Schiff (PAS)-Alcian blue was the most useful histological stain for identifying the parasite and characterising the degree of intestinal infection. We observed severe enteritis in infected fish, with inflammatory cell infiltration and sclerosis of the lamina propria. The number of goblet cells was considerably and significantly decreased in heavily infected fish. The intestines of 4 of the 5 survivor fish were totally free of parasites and showed severe chronic enteritis with a regenerative epithelium, suggesting that an acquired immune process may spontaneously eliminate parasites.     

Functional basis for sexual differences in bite force in the lizard Anolis carolinensis

In many species of lizards, males attain greater body size and have larger heads than female lizards of the same size. Often, the dimorphism in head size is paralleled by a dimorphism in bite force. However, the underlying functional morphological basis for the dimorphism in bite force remains unclear. Here, we test whether males are larger, and have larger heads and bite forces than females for a given body size in a large sample of Anolis carolinensis . Next, we test if overall head shape differs between the sexes, or if instead specific aspects of skull shape can explain differences in bite force. Our results show that A. carolinensis is indeed dimorphic in body and head size and that males bite harder than females. Geometric morphometric analyses show distinct differences in skull shape between males and females, principally reflecting an enlargement of the jaw adductor muscle chamber. Jaw adductor muscle mass data confirm this result and show that males have larger jaw adductors (but not jaw openers) for a given body and head size. Thus, the observed dimorphism in bite force in A. carolinensis is not merely the result of an increase in head size, but involves distinct morphological changes in skull structure and the associated jaw adductor musculature.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 111–119.     

Behavioral and ecological correlates of foureye butterflyfish, Chaetodon capistratus, (Perciformes: Chaetodontidae) infected with Anilocra chaetodontis (Isopoda: Cymothoidae)

We observed the behavior and ecology of Chaetodon capistratus infected and uninfected with the ectoparasitic isopod Anilocra chaetodontis to assess whether there may be parasite induced alterations in host biology, host defenses against infection, and/or pathology related to infection. We also examined habitat related differences in infection rates. Infected fish had higher rates of interaction with conspecifics and spent more time in low flow environments (which might improve transmission of juvenile parasites to new hosts). Butterfly fish without isopods were chased more frequently by damselfishes, fed more, and had larger territories. Time spent near conspecifics, and fish condition and gonadosomatic index did not vary between infected and uninfected fish. These results suggest that foureye butterfly fish behavior is altered by the isopod parasite in order for the isopods to more easily gain mates or transmit offspring to new hosts.     

How fish-helminth associations arise: an example from Arctic charr in Loch Rannoch

Three sympatric morphs of Arctic charr Salvelinus alpinus occur in Loch Rannoch, Scotland, and are identified by their differing head morphology and diet. These are small-headed benthic, large-headed benthic and pelagic morphs. Six species of endoparasitic helminth were found in the fish, but the morphs had different patterns of infection. Overall infections in pelagic charr were heavier than in large-headed benthics, which were in turn heavier than in small-headed benthics, even though benthic charr live longer than pelagics. Pelagic fish had high prevalences and intensities of pseudophyllidean tapeworms, the intermediate hosts of which are copepods. The prevalence and intensity of metacercariae of Diplostomum sp. (the intermediate hosts of which are snails) were high in the benthic morphs. The results are discussed in terms of the effects of ecological factors on transmission of helminth parasites to their hosts and the evolution of host-parasite associations.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Morphological and ecological convergence in two natricine snakes

Similar morphologies between species may be due to shared ancestry or convergent evolution . Understanding instances of morphological and ecological convergence is central to evolutionary ecology because they help us understand the fit between organism and environment. Two species of stream-dwelling natricine snakes, Thamnophis rufipunctatus and Nerodia harteri present a model system for studying ecological and morphological convergence and adaptation. The species are allopatric and both live in shallow riffles in streams and forage visually for fish. We studied morphological similarity, trait evolution and functional significance of ecologically relevant traits in these and related species, and used mitochondrial DNA sequences for the ND4 gene to estimate their phylogenetic relationships. Character mapping of head length and head width supported the hypothesis of independent evolution of head shape in T .  rufipunctatus and N .  harteri . The elongate snout is a derived trait in these two taxa that is associated with reduced hydrodynamic drag on the snakes' heads when in a swift current, compared to other species with the ancestral blunt snout. We hypothesize that lower hydrodynamic drag facilitates prey capture success in these species that are known to forage by holding their position in currents and striking at fish prey. The elongate snout morphology has also resulted in a diminished binocular vision field in these snakes, contrary to the hypothesis that visually orientated snakes should exhibit relatively greater binocular vision. Convergent evolution of the long snout and reduced hydrodynamic drag in T. rufipunctatus and N. harteri are consistent with the hypothesis that the long snout is an adaptation to foraging in a swift current.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 363–371.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater (= obesus)]

The Common Chuckwalla [ Sauromalus ater (=  obesus )] is a large, sexually dimorphic lizard with a flattened head that takes refuge from predators in rock crevices. Males use their relatively large heads to bite competing males during territorial fights and to restrain females during copulation. Flattened heads with an antipredator function (i.e. seeking refuge in crevices) and enlarged heads with intrasexual competition and reproductive functions suggest possible antagonism between selective pressures on head morphology in males. To examine this hypothesis, we performed a morphometric analysis and measured the bite-force performance of 49 adult chuckwallas. Males had disproportionately wider heads than females, but did not have deeper heads. Males bit with nearly four times the force of females, consistent with the notion of sexual selection for high bite force in males. Although constrained by crevice-wedging behaviour, head depth was a good predictor of bite force in both sexes. In males, however, osteological head width also was a good predictor of bite force. These results are consistent with the hypothesis that head shape in males is under antagonistic selective pressures, which may partly explain the pattern of head shape dimorphism. The disproportionately wide head of males may reflect anatomical modifications to enhance bite force in response to sexual selection in spite of presumed constraints on head shape for crevice-wedging behaviour  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 215–222.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.