Histopathology in Leuciscus cephalus (Pisces: Cyprinidae) resulting from infection with Pomphorhynchus laevis (Acanthocephala).

The histopathology present in Leuciscus cephalus Risso 1826 from the River Po, naturally infected with the acanthocephalan Pomphorhynchus laevis Müller 1776, was studied and described. The parasite was only found within the host's digestive tract, and a density of 10 P. laevis per square centimeter was common. On histological examination it was noticed that both male and female parasites penetrated deeply through all the layers of the host digestive tract by means of their slender neck, bulb and proboscis; thus the bulb and proboscis become encapsulated beneath the serosa and mesentery. As a result, the presence of a capsule was noticed on the external surface of the host digestive tract. P. laevis caused local damage to the intestinal wall, and the parasite elicited an intense host reaction. The response of L. cephalus at the attachment site of the acanthocephalan was hyperplasia of host connective tissue, with cellular infiltration. In a few hosts, the presence of a fibrous nodule on the outer surface of the alimentary canal was observed.     

The Mode of Attachment of Trypanosoma vivax in the Proboscis of the Tsetse Fly Glossina fuscipes: an Ultrastructural Study of the Epimastigote Stage of the Trypanosome*

SYNOPSIS. The ultrastructure of attached Trypanosoma vivax epimastigote clusters in the proboscis of the tsetse fly Glossina fuscipes is described from electron micrographs of thin sections. Some flagellates are attached directly to the lining of the insect's labrum by their flagella, most of which are aligned along the long axis of the proboscis. Other trypanosomes are attached indirectly, their flagella adhering to those of flagellates which are directly attached. Junctional complexes similar to those described from metazoan epithelia are found on the flagellar membrane. A long zonular hemidesmosome attaches the flagellum to the proboscis wall and a series of closely set macular desmosomes link the flagellar membranes of adjacent flagellates. Unlike the trypomastigote stages of T. vivax, more than one row of macular desmosomes may be present along the flagellum-body junction of the trypanosome. It is suggested that all these Junctional complexes serve to buttress the flagellate's attachment to its insect host and so maintain anchorage of the parasite during the fly's blood meals. The ability of the flagellum of trypanosomatids to form Junctional complexes may be a factor contributing to their success as parasites, this adaptation enabling them to multiply while attached to host surfaces.     

Differential precocious sexual development of Proctoeces lintoni (Digenea: Fellodistomidae) in three sympatric species of keyhole limpets Fissurella spp. may affect transmission to the final host.

The prevalence, abundance, and developmental status of the digenetic trematode Proctoeces lintoni Siddiqui et Cable 1960 were compared in 3 species of keyhole limpets Fissurella. A total of 197 limpets was collected at Caleta Chome, south-central Chile. Fissurella picta and F. costata had the highest prevalence of infection, whereas F. picta showed the greatest abundance of parasites, which increased with host shell length. However, the frequency of P. lintoni specimens with eggs in the uterus was greatest in F. costata. These results suggest that an increased rate of development of a parasite in the intermediate host may shorten the residence time necessary for maturation in the final host. Thus, faster development of the parasite in F. costata suggests the possibility that the parasites transmitted through this host species have shorter maturation times in clingfishes than individuals transmitted via other limpet species.     

Investing in attachment: evolution of anchoring structures in acanthocephalan parasites

Secure attachment to host tissues is essential for survival and reproduction in parasitic organisms. The production of elaborate attachment structures must be costly, however, and investments in attachment should be approximately proportional to the likelihood that a parasite will be dislodged. In the present study, relative investments in attachment as a function of body size and the type of host used were examined across 138 species of acanthocephalans. These worms live anchored to the intestinal wall of a vertebrate host by inserting their hooked proboscis into host tissues. Taking proboscis volume into account, there is a negative interspecific relationship between the number of hooks borne on the proboscis and their mean length, reflecting a trade‐off between hook number and hook length. This supports the assumption that hooks are costly to produce, because any given species cannot simultaneously maximize both the relative number and relative length of the hooks it produces. There is a positive relationship between total worm size and total hook length, but it is weak, with a slope indicating that, as total body volume increases, total hook length also increases but at a slower rate. Indeed, relative investments in attachment, measured as hook length per unit body volume, decrease as worm size increases. Independently of total body size, investments in hook production are higher in species exploiting endothermic hosts, especially birds, than in those living in ectothermic hosts. Given the greater amounts of food passing through the gut of endotherms, and the richer and denser communities of intestinal parasites that they harbour, they are likely to select for greater investments in attachment. These results support the prediction that investments in attachment are influenced by the probability of being dislodged, and allow comparisons with other groups of intestinal parasites such as cestodes or trematodes. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 637–645.     

Echinostoma caproni in mice: ultrastructural studies on the formation of immune complexes on the surface of an intestinal trematode

The binding of mouse antibodies to the surface antigens of juvenile and 7 and 28 day old Echinostoma caproni was examined by transmission electron microscopy of thin sections of parasites, which were treated with antibodies in a double sandwich technique with ferritin-conjugated antibody. The surface of freshly recovered mature adult parasites was covered with an irregular but often rather intensive mouse antibody containing matrix, which probably represents a layer of mouse antibody/parasite antigen complexes. The complexes were lost after in vitro culturing of the parasites for 24 h, but incubation of the in vitro-maintained antibody-negative adult parasites with immune mouse serum led to reformation of a similar but less intensive cover with immune complexes. Juvenile and young stages of E. caproni, which had never been exposed to host antibodies, obtained a layer of immune complexes on their surface after incubation with immune mouse serum in vitro. In both young and mature parasites, the antibody-antigen complexes were observed to be rather loosely attached to the outer surface of the parasites, where the antigens probably constitute a part of the irregular glycocalyx of the organisms. It may also be that the antigens are present as isolated excretion along the surface of the parasites. Several sections indicated that the parasite surface antigens may be present in the tegument in vesicles which fuse with the outer membrane of the parasite whereby their contents are released to the exterior.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

Ultrastructural study of the host-parasite interface of Moniliformis moniliformis (Archiacanthocephala) in laboratory-infected rats

The fine structure of the host-parasite interface of Moniliformis moniliformis in rats is described, comprising investigations on the ontogenic development of the presomal tegument, on the lesions caused by the worms, and on the host cellular reactions at the points of attachment of the worm. The presomal tegument of the worm contained more fibrous elements than the metasomal tegument. The sclerotization increased with the ages of the worms and toward the tip of the proboscis. The presomal surface coat was more coarsely structured and osmiophilic than that of the metasoma and was neither continuous with the contents of the tegumental crypts nor supported by lipids from necrotic host tissue. The surface coat occasionally detached from the proboscis, probably due to the activity of the surrounding granulocytes of the host. The proboscis hooks lost their tegumental covering during their larval development. Hooks of all worms from rats were invested with a semiliquid lipid coat, apparently derived from tegumental excretions at the base of the hooks. The invaginated area of excretion around the base of the hooks was rich in endoplasmic reticulum. The hooks seemed to renew their lipid coats at certain intervals by dipping into the excreted lipid. In rats all worms, irrespective of their age, attached superficially, penetrating only the intestinal mucosa and the tunica propria. No fibrous connective tissue was found in the lesions caused by the worms, indicating that they frequently changed their site of attachment. At 3-10 days postinfection the host's defense cells observed in the lesions consisted mainly of granulocytes, whereas plasma cells were the predominant leukocytes in lesions of older infections.     

The effect of a species-specific avoidance response to predatory starfish on the intertidal distribution of two gastropods

Summary The gastropodsAcmaea (Collisella) limatula andAcmaea (Notoacmea) scutum respond to water flowing over certain predatory starfish (i.e. to the scent of the starfish) by moving rapidly up a submerged, vertical surface. These limpets respond with upward movement to the scent ofPisaster ochraceus, Pisaster giganteus, Pycnopodia helianthoides, andLeptasterias aequalis. All of these starfish are predators on molluscs and at least occasionally inhabit the intertidal. In contrast, the limpets respond weakly or not at all to the scent ofPatiria miniata andPisaster brevispinus. Patiria is an omnivorous scavenger, andP. brevispinus is predaceous but strictly subtidal when it occurs on rocky shores. For the starfish tested, then, the limpets only give avoidance responses to starfish species naturally encountered as predators.The avoidance response ofA. limatula andA. scutum to predatory stafish can also be demonstrated in the field. When onePisaster ochraceus is placed beneath a population of limpets in the intertidal and confined so that contacts between the starfish and limpets are impossible, the limpet population is displaced significantly upward after one tidal cycle. In addition, the closer the limpets are to the starfish, the greater is their upward displacement.     

A trematode infection with no effect on reproductive success of a sand-bubbler crab

The infection effects of the parasitic digenean trematode on the body weight and reproductive success of the sand-bubbler crab were examined. Gynaecotyla squatarolae (Trematoda: Microphallidae) infects the body cavity of Scopimera globosa (Decapoda: Scopimeridae) and uses the crab as its second intermediate host. The parasites infected all reproductive crabs examined to varying degrees. Larger crabs of both sexes had more parasites than smaller ones, probably because body size reflects age, and older crabs had a longer period of exposure to infection. Males had more parasites than females, probably because of sexual difference in acting time on the surface. Ovigerous females stay in closed burrows and do not act on the surface during incubation, and so have less chance of infection than males. The quantity of infecting parasites did not explain variations in either body weight or reproductive success of individual crabs in a field experiment. The life history of this parasite, relative body size of the crabs, and cost and the possible benefit of manipulation for the parasite may explain these results.     

Male parasitism and intrasexual competition in a burrowing barnacle

Summary In sexually dimorphic animals, large male body size is often associated with direct interference competition among males for access to females or resources used in reproduction. In constrast, small male body size may be associated with indirect scramble competition among males for temporal or spatial access to females. Minute, “parasitic” males of the acrothoracican barnacleTrypetesa lampas (Hancock) appear to compete with one another for permanent attachment sites on the external body of the female. Several spatial patterns suggest indirect male-male competition: 1) males were consistently aggregated on the anterior surface of the female ovarian disc; 2) the average distance from attached males to the site of insemination correlated positively with local male density; 3) average male body size on a female decreased as a function of male density; 4) the distribution of males on the left and right hand sides of the female ovarian disc was more even than expected, suggesting that males avoided crowded settlement sites. The number of males attached to a female increased with female body size and matched a null model in which males colonized female “targets” of differing areas. These results suggest that competition between males primarily affected settlement sites and male body sizes within, rather than among, females. Male parasitism may have evolved through both sexual selection for efficient access to females (Ghiselin 1974) and natural selection for reduced burrow density in a space-limited habitat (Turner and Yakovlev 1983).     

Fluorescence-activated cell-sorting analysis of fibronectin peptides binding to Trypanosoma cruzi trypomastigotes

The binding of synthetic peptides modeled from the sequence of the cell attachment site of fibronectin to T. cruzi trypomastigote surface receptors was investigated by fluorescence-activated cell-sorting analysis using fluorescein-labeled peptides. Peptides with the sequence Arg-Gly-Asp-Ser bound to the parasite surface. A low percentage of fresh parasites recently liberated from infected fibroblasts had the capacity to bind the peptide. In contrast, these parasites showed a time-dependent several-fold increase in their ability to bind the Arg-Gly-Asp-Ser-containing peptides during extracellular incubation. From these observations, it appears that the expression of surface receptors on a particular, mature stage of the parasite parallels its ability to adhere to and infect host cells.     

Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.     

Intestinal pathology and site specificity of the acanthocephalan Neoechinorhynchus carpiodi Dechtiar, 1968, in quillback, Carpiodes cyprinus (Lesueur)

Intestinal pathology and site specificity of Neoechinorhynchus carpiodi Dechtiar, 1968, in quillback, Carpiodes cyprinus (Lesueur), from Dauphin Lake, Manitoba, was investigated. Neoechinorhynchus carpiodi elicits the formation of a nodule at the point of proboscis attachment. Over 98% of the worms were attached in sections 6-8 of the intestine. Fish had clusters of 1-8 nodules, cluster size increased with worm burden, and the volume of nodules increased with worm numbers. Nodule number, size, and pathology was related to intensity of infection and to depth of proboscis penetration. Three types of pathology were noted. Type I nodules had few worms and the proboscides were attached in the lamina propria; Type II nodules harbored more worms and the proboscides penetrated to, but not through, the stratum compactum; and Type III nodules had the greatest numbers of N. carpiodi and proboscides penetrated through the stratum compactum. Hyperplasia, vascularization, and collagen deposition were extensive, especially in Type III nodules. An epithelium-lined channel was present in most nodules. Type III nodules were most anterior (75% of the time), harbored the greatest proportion of immature worms regardless of cluster size, and had more gravid females. The largest nodules (Type III pathology) were well vascularized, long-lasting, and appeared to be the preferred microhabitat for the parasite.     

The attachment of Clinostomum sp. (Digenea,Clinostomidae) to the oesophagus of the bird Ardea cocoi (Aves,Ardeidae)

The attachment of Clinostomum sp. to the oesophagus of the bird definitive host Ardea cocoi is reported. The parasite attaches to the mucous layer of the oesophagus by the acetabulum, oral sucker, and oral collar. The mucous layer of the oesophagus engulfed by the oral sucker presents an intense liquefactive necrosis, and the engulfment is not likely to contribute significantly to the attachment of the parasite. The oral collar of the parasite, surrounding the oral sucker, is juxtaposed to the oesophagus mucous layer, showing a perfect fitting of both surfaces. It is concluded that the main attachment mechanism of the parasites to the oesophagus of the host is provided by the acetabulum and by the juxtaposition of the oral collar of the parasites to the oesophagus host surface.     

Fluorescence-Activated Cell-Sorting Analysis of Fibronectin Peptides Binding to Trypanosoma cruzi Trypomastigotes1

ABSTRACT. The binding of synthetic peptides modeled from the sequence of the cell attachment site of fibronectin to T. cruzi trypomastigote surface receptors was investigated by fluorescence-activated cell-sorting analysis using fluorescein-labeled peptides. Peptides with the sequence Arg-Gly-Asp-Ser bound to the parasite surface. A low percentage of fresh parasites recently liberated from infected fibroblasts had the capacity to bind the peptide. In contrast, these parasites showed a time-dependent several-fold increase in their ability to bind the Arg-Gly-Asp-Ser-containing peptides during extracellular incubation. From these observations, it appears that the expression of surface receptors on a particular, mature stage of the parasite parallels its ability to adhere to and infect host cells.     

Sexual size dimorphism in parasitic oxyurid nematodes

As in many invertebrates, female oxyurids are larger than male. Sexual size dimorphism (SSD) of oxyurid nematodes (the hosts of which are both invertebrate and vertebrate), is investigated regarding body size of both host and parasite. SSD of parasites appeared to be weakly, but not significandy, correlated with invertebrate and vertebrate host body size. However, this study reveals a different pattern for SSD with respect to either type of host. SSD does not increase in tandem with body size in vertebrate parasites either at the level of species or genus. SSD is much more pronounced in Syphaciidae than in Heteroxynematidae, two families of vertebrate parasites exhibiting different modes of transmission (members of the Syphaciidae are transmitted through perianal contamination). SSD is investigated in one monophyletic group of parasites of primates, for which a phylogeny is known. Independent comparisons method is used and we find that the body size of female parasite is strongly correlated with that of the male. The hypoallometry (slope<1) of the relationship suggests that the SSD is not linked to an increase of parasite body size. Moreover, there is no influence of host body size on parasite SSD. The pattern in parasites of invertebrates is different. First, SSD has been found to increase with parasite body size in two groups of invertebrate parasites: the oxyurids of Dictyoptera and Coleoptera. Second, female body size of invertebrate parasites is not correlated with male body size either at genus or species level. Finally, the evolution of SSD is discussed in relation to the demographic patterns of invertebrate parasites and the haplodiploid mode of reproduction of these parasitic nematodes.     

Histopathological and ultrastructural studies of the tapeworm Monobothrium wageneri (Caryophyllidea) in the intestinal tract of tench Tinca tinca

Monobothrium wageneri is a monozoic caryophyllidean tapeworm of tench Tinca tinca. The pathological changes caused by this parasite within the intestinal tract of wild tench are described for the first time. Parasites were found attached to the anterior third of the intestine in tight clusters comprising up to 109 tapeworms. Infection was associated with the formation of raised inflammatory swellings surrounding the parasites. This host response, combined with the deep penetration of the scolex into the gut wall, formed a very firm seat of parasite attachment. Histopathological changes were characterised by a pronounced fibrogranulomatous lesion that extended through all layers of the intestine. This was accompanied by haemorrhage, oedema, necrosis and degeneration of the muscularis. A marked eosinophilic interface layer between the scolex of the tapeworm and gut wall indicated intimate host-parasite contact. Ultrastructural examinations revealed coniform spinitriches covering the neck and lateral sides of the scolex and capilliform filitriches present on the apical end of the scolex. Numerous glandular cytons (tegumental glands) were recorded throughout the scolex tegument. Large numbers of secretory granules discharged from the glands through a network of processes onto the scolex surface were consistent with distancing the cellular responses of the host. Observations of severe inflammatory lesions, partial intestinal occlusion and the potential for intestinal perforation represent important pathological changes that are consistent with loss of normal gut function. The lesions associated with the attachment of M. wageneri are more severe than those recorded for any other tapeworm of British freshwater fish.     

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.     

The Giardia ventrolateral flange is a lamellar membrane protrusion that supports attachment

Attachment to the intestinal epithelium is critical to the lifestyle of the ubiquitous parasite Giardia lamblia. The ventrolateral flange is a sheet-like membrane protrusion at the interface between parasites and attached surfaces. This structure has been implicated in attachment, but its role has been poorly defined. Here, we identified a novel actin associated protein with putative WH2-like actin binding domains we named Flangin. Flangin complexes with Giardia actin (GlActin) and is enriched in the ventrolateral flange making it a valuable marker for studying the flanges’ role in Giardia biology. Live imaging revealed that the flange grows to around 1 μm in width after cytokinesis, then remains uniform in size during interphase, grows in mitosis, and is resorbed during cytokinesis. A flangin truncation mutant stabilizes the flange and blocks cytokinesis, indicating that flange disassembly is necessary for rapid myosin-independent cytokinesis in Giardia. Rho family GTPases are important regulators of membrane protrusions and GlRac, the sole Rho family GTPase in Giardia, was localized to the flange. Knockdown of Flangin, GlActin, and GlRac result in flange formation defects. This indicates a conserved role for GlRac and GlActin in forming membrane protrusions, despite the absence of canonical actin binding proteins that link Rho GTPase signaling to lamellipodia formation. Flangin-depleted parasites had reduced surface contact and when challenged with fluid shear force in flow chambers they had a reduced ability to remain attached, confirming a role for the flange in attachment. This secondary attachment mechanism complements the microtubule based adhesive ventral disc, a feature that may be particularly important during mitosis when the parental ventral disc disassembles in preparation for cytokinesis. This work supports the emerging view that Giardia’s unconventional actin cytoskeleton has an important role in supporting parasite attachment.