Parasite-parasite Interactions Research Articles

Warming alters life-history traits and competition in a phage community.

Host-parasite interactions are highly susceptible to changes in temperature due to mismatches in species thermal responses. In nature, parasites often exist in communities, and responses to temperature are expected to vary between host-parasite pairs. Temperature change thus has consequences for both host-parasite dynamics and parasite-parasite interactions. Here, we investigate the impact of warming (37°C, 40°C, and 42°C) on parasite life-history traits and competition using the opportunistic bacterial pathogen Pseudomonas aeruginosa (host) and a panel of three genetically diverse lytic bacteriophages (parasites). We show that phages vary in their responses to temperature. While 37°C and 40°C did not have a major effect on phage infectivity, infection by two phages was restricted at 42°C. This outcome was attributed to disruption of different phage life-history traits including host attachment and replication inside hosts. Furthermore, we show that temperature mediates competition between phages by altering their competitiveness. These results highlight phage trait variation across thermal regimes with the potential to drive community dynamics. Our results have important implications for eukaryotic viromes and the design of phage cocktail therapies.IMPORTANCEMammalian hosts often elevate their body temperatures through fevers to restrict the growth of bacterial infections. However, the extent to which fever temperatures affect the communities of phages with the ability to parasitize those bacteria remains unclear. In this study, we investigate the impact of warming across a fever temperature range (37°C, 40°C, and 42°C) on phage life-history traits and competition using a bacterium (host) and bacteriophage (parasite) system. We show that phages vary in their responses to temperature due to disruption of different phage life-history traits. Furthermore, we show that temperature can alter phage competitiveness and shape phage-phage competition outcomes. These results suggest that fever temperatures have the potential to restrict phage infectivity and drive phage community dynamics. We discuss implications for the role of temperature in shaping host-parasite interactions more widely.

The determination and relationship of four coexisting paramphistomes in perspective of integrative taxonomic investigation.

Co-infections with Orthocoelium species and other paramphistomes were found in different ruminant hosts from two provinces of Thailand. Whilst O. parvipapillatum coexisted with Paramphistomum epiclitum in the same cattle (Bos taurus) from Pathum Thani Province, Thailand, O. dicranocoelium and Fischoederius elongatus were found in water buffalo (Bubalus bubalis) from Chiang Mai Province. Morphological, histological, and tegumental surface features of both Orthocoelium species were intensively investigated for species differentiation. Statistical analysis of eight morphometric ratios presented morphological differences for three paramphistomes in the Paramphistomidae family and some relationships among paramphistomes in different definitive hosts. The genetic relationships of the co-infecting paramphistomes were investigated using p-distance and phylogenetic tree analyses. Genetic variations in the Orthocoelium co-infecting paramphistomes, P. epiclitum and F. elongatus, were calculated and compared to DNA sequence alignments based on internal transcribed spacer 2 (ITS2) and cytochrome c oxidase subunit I (COI) DNA markers. In addition, the phylogenetic tree constructions from both DNA markers and their concatenated sequence (ITS2+COI) were used for species confirmation and the presentation of genetic relationships between co-infecting paramphistomes and other paramphistomes. This study improves the basic taxonomical description and understanding of parasite-parasite and host-parasite interactions from the perspectives of morpho-histological, morphometric, and genetic variation in co-infecting paramphistomes and Orthocoelium species in different hosts.

Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing.

Several methodological issues currently hamper the study of entire trematode communities within populations of their intermediate snail hosts. Here we develop a new workflow using high-throughput amplicon sequencing to simultaneously genotype snail hosts and their infecting trematode parasites. We designed primers to amplify four snail and five trematode markers in a single multiplex PCR. While also applicable to other genera, we focused on medically and economically important snail genera within the superorder Hygrophila and targeted a broad taxonomic range of parasites within the class Trematoda. We tested the workflow using 417 Biomphalaria glabrata specimens experimentally infected with Schistosoma rodhaini, two strains of Schistosoma mansoni and combinations thereof. We evaluated the reliability of infection diagnostics, the robustness of the workflow, its specificity related to host and parasite identification, and the sensitivity to detect co-infections, immature infections and changes of parasite biomass during the infection process. Finally, we investigated its applicability in wild-caught snails of other genera naturally infected with a diverse range of trematodes. After stringent quality control the workflow allows the identification of snails to species level, and of trematodes to taxonomic levels ranging from family to strain. It is sensitive to detect immature infections and changes in parasite biomass described in previous experimental studies. Co-infections were successfully identified, opening the possibility to examine parasite-parasite interactions such as interspecific competition. Together, these results demonstrate that our workflow provides a powerful tool to analyse the processes shaping trematode communities within natural snail populations.

Abundance data applied to a novel model invertebrate host shed new light on parasite community assembly in nature.

Understanding how environmental drivers influence the assembly of parasite communities, in addition to how parasites may interact at an infracommunity level, are fundamental requirements for the study of parasite ecology. Knowledge of how parasite communities are assembled will help to predict the risk of parasitism for hosts, and model how parasite communities may change under variable conditions. However, studies frequently rely on presence-absence data and examine multiple host species or sites, metrics which may be too coarse to characterise nuanced within-host patterns. We utilised a novel host system, the freshwater mussel Anodonta anatina, to investigate the drivers of community structure and explore parasite interactions. In addition, we aimed to highlight consistencies and inconsistencies between PA and abundance data. Our analysis incorporated 14 parasite taxa and 720 replicate infracommunities. Using Redundancy Analysis, a joint species distribution model and a Markov random field approach, we modelled the impact of both host-level and environment-level characteristics on parasite structure, as well as parasite-parasite correlations after accounting for all other factors. This approach was repeated for both the presence and abundance of all parasites. We demonstrated that the regional species pool, individual host characteristics (mussel length and gravidity) and predicted parasite-parasite interactions are all important but to varying degrees across parasite species, suggesting that applying generalities to parasite community construction is too simplistic. Furthermore, we showed that PA data fail to capture important density-dependent effects of parasite load for parasites with high abundance, and in general performs poorly for high-intensity parasites. Host and parasite traits, as well as broader environmental factors, all contribute to parasite community structure, emphasising that an integrated approach is required to study community assembly. However, care must be taken with the data used to infer patterns, as presence-absence data may lead to incorrect ecological inference.

The socially parasitic ant Polyergus mexicanus has host-associated genetic population structure and related neighbouring colonies.

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka "slave-making") ant (Polyergus mexicanus), which is known for its host-specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite-parasite interactions in social parasites via inclusive fitness.

Multi-driver and multi-scale assessment of vine community structure and composition across a complex tropical environmental matrix.

Ecological communities are structured by multiple processes operating at multiple scales yet understanding the scale-dependency of these processes remains an open challenge. This might be particularly true for parasites, for which biotic rather than abiotic processes may play a primary role in structuring communities. Focusing on vines, a group of structural parasites that gain access to the canopy using different climbing mechanisms, we examined the influence of abiotic factors in tandem with host-parasite and parasite-parasite interactions in the assembly of tropical vine communities. Two synthetic variables, namely Climate1 and landscape Variety, were consistently important in explaining variation in species richness and diversity, as well as species composition, but their importance varied with scale. Whereas Climate1 summarizes the largest variability among climatic variables, landscape Variety expresses landscape heterogeneity within a neighborhood. Significant patterns of species co-occurrences suggest that vine-vine interactions also contribute to vine community assembly. Our results may be critical to understand vine proliferation and help design management strategies for their control.

Parasite community dynamics in an invasive vole – From focal introduction to wave front

Multiple parasite species simultaneously infecting a host can interact with one another, which has the potential to influence host-parasite interactions. Invasive species typically lose members of their parasite community during the invasion process. Not only do the founding population escape their parasites, but the rapid range expansion of invaders once in the invaded range can lead to additional stochastic loss of parasites. As such, parasite community dynamics may change along an invasion gradient, with consequences for host invasion success. Here, we use the bank vole, Myodes glareolus, introduced as a small founding population at a point source in the Republic of Ireland in c.1920's and its ecto- and endoparasites to ask: i) how does the parasite community vary across an invasion gradient, and ii) are parasite community associations driven by host traits and/or distance from the point of host introduction? We sampled the parasite community of M. glareolus at the proposed focal site of introduction, at mid-wave and the invasion front, and used a parasite interactivity index and statistical models to determine the potential for the parasite community to interact. Bank voles harboured up to six different parasite taxa, with a significantly higher parasite interactivity index at the foci of introduction (z = 2.33, p = 0.02) than elsewhere, suggesting the most established parasite community has greater opportunities to interact. All but one of four synergistic parasite community associations were driven by host traits; sex and body mass. The remaining parasite-parasite associations occurred at the mid-point of the invasion wave, suggesting that specific parasite-parasite interactions are not mediated by distance from a focal point of host introduction. We propose that host traits rather than location along an invasion gradient are more likely to determine parasite-parasite interactions in the invasive bank vole.

Coupled range dynamics of brood parasites and their hosts responding to climate and vegetation changes.

As populations shift their ranges in response to global change, local species assemblages can change, setting the stage for new ecological interactions, community equilibria and evolutionary responses. Here, we focus on the range dynamics of four avian brood parasite species and their hosts in southern Africa, in a context of bush encroachment (increase in woody vegetation density in places previously occupied by savanna-grassland mosaics) favouring some species at the expense of others. We first tested whether hosts and parasites constrained each other's ability to expand or maintain their ranges. Secondly, we investigated whether range shifts represented an opportunity for new host-parasite and parasite-parasite interactions. We used multispecies dynamic occupancy models with interactions, fitted to citizen science data, to estimate the contribution of interspecific interactions to range shifts and to quantify the change in species co-occurrence probability over a 25-year period. Parasites were able to track their hosts' range shifts. We detected no deleterious effect of the parasites' presence on either the local population viability of host species or the hosts' ability to colonize newly suitable areas. In the recently diversified indigobird radiation (Vidua spp.), following bush encroachment, the new assemblages presented more potential opportunities for speciation via host switch, but also more potential for hybridization between extant lineages, also via host switch. Multispecies dynamic occupancy models with interactions brought new insights into the feedbacks between range shifts, biotic interactions and local demography: brood parasitism had little detected impact on extinction or colonization processes, but inversely the latter processes affected biotic interactions via the modification of co-occurrence patterns.

Exploring the Gastrointestinal "Nemabiome": Deep Amplicon Sequencing to Quantify the Species Composition of Parasitic Nematode Communities.

Parasitic helminth infections have a considerable impact on global human health as well as animal welfare and production. Although co-infection with multiple parasite species within a host is common, there is a dearth of tools with which to study the composition of these complex parasite communities. Helminth species vary in their pathogenicity, epidemiology and drug sensitivity and the interactions that occur between co-infecting species and their hosts are poorly understood. We describe the first application of deep amplicon sequencing to study parasitic nematode communities as well as introduce the concept of the gastro-intestinal “nemabiome”. The approach is analogous to 16S rDNA deep sequencing used to explore microbial communities, but utilizes the nematode ITS-2 rDNA locus instead. Gastro-intestinal parasites of cattle were used to develop the concept, as this host has many well-defined gastro-intestinal nematode species that commonly occur as complex co-infections. Further, the availability of pure mono-parasite populations from experimentally infected cattle allowed us to prepare mock parasite communities to determine, and correct for, species representation biases in the sequence data. We demonstrate that, once these biases have been corrected, accurate relative quantitation of gastro-intestinal parasitic nematode communities in cattle fecal samples can be achieved. We have validated the accuracy of the method applied to field-samples by comparing the results of detailed morphological examination of L3 larvae populations with those of the sequencing assay. The results illustrate the insights that can be gained into the species composition of parasite communities, using grazing cattle in the mid-west USA as an example. However, both the technical approach and the concept of the ‘nemabiome’ have a wide range of potential applications in human and veterinary medicine. These include investigations of host-parasite and parasite-parasite interactions during co-infection, parasite epidemiology, parasite ecology and the response of parasite populations to both drug treatments and control programs.

Network-based gene prediction for Plasmodium falciparum malaria towards genetics-based drug discovery.

BackgroundMalaria is the most deadly parasitic infectious disease. Existing drug treatments have limited efficacy in malaria elimination, and the complex pathogenesis of the disease is not fully understood. Detecting novel malaria-associated genes not only contributes in revealing the disease pathogenesis, but also facilitates discovering new targets for anti-malaria drugs.MethodsIn this study, we developed a network-based approach to predict malaria-associated genes. We constructed a cross-species network to integrate human-human, parasite-parasite and human-parasite protein interactions. Then we extended the random walk algorithm on this network, and used known malaria genes as the seeds to find novel candidate genes for malaria.ResultsWe validated our algorithms using 77 known malaria genes: 14 human genes and 63 parasite genes were ranked averagely within top 2% and top 4%, respectively among human and parasite genomes. We also evaluated our method for predicting novel malaria genes using a set of 27 genes with literature supporting evidence. Our approach ranked 12 genes within top 1% and 24 genes within top 5%. In addition, we demonstrated that top-ranked candied genes were enriched for drug targets, and identified commonalities underlying top-ranked malaria genes through pathway analysis. In summary, the candidate malaria-associated genes predicted by our data-driven approach have the potential to guide genetics-based anti-malaria drug discovery.

A Glycosylation Mutant of Trypanosoma brucei Links Social Motility Defects In Vitro to Impaired Colonization of Tsetse Flies In Vivo.

Transmission of African trypanosomes by tsetse flies requires that the parasites migrate out of the midgut lumen and colonize the ectoperitrophic space. Early procyclic culture forms correspond to trypanosomes in the lumen; on agarose plates they exhibit social motility, migrating en masse as radial projections from an inoculation site. We show that an Rft1(-/-) mutant needs to reach a greater threshold number before migration begins, and that it forms fewer projections than its wild-type parent. The mutant is also up to 4 times less efficient at establishing midgut infections. Ectopic expression of Rft1 rescues social motility defects and restores the ability to colonize the fly. These results are consistent with social motility reflecting movement to the ectoperitrophic space, implicate N-glycans in the signaling cascades for migration in vivo and in vitro, and provide the first evidence that parasite-parasite interactions determine the success of transmission by the insect host.

Microbiomes, plausible players or not in alteration of host behavior.

Many parasites can affect the physiology and behavior of their hosts in ways that seem to improve the parasites' chances of completing their life cycle (Biron and Loxdale, 2013; Lafferty and Shaw, 2013; Webster et al., 2013). These parasite species are so-called “manipulative parasites.” Common habitats of manipulative parasites are the host's body cavity, muscles and brain (Lafferty and Shaw, 2013). Typically the host's neural, endocrine, neuromodulatory, and immunomodulatory systems are targeted (Adamo, 2013; Lafferty and Shaw, 2013). In evolutionary biology, manipulation of host behavior by parasites is considered to be an example of the “extended phenotype” concept (Dawkins, 1982; Libersat et al., 2009). There are numerous fascinating cases of alteration of host behavior induced by a parasite; for instance, the suicidal behavior of crickets induced by hairworms (Thomas et al., 2002; Biron and Loxdale, 2013). Many studies on strategies used by manipulative parasites assume that only two organisms are involved in crosstalk based on Dawkins' assumption: the host and a manipulative parasite. However, hosts are frequently invaded by more than one species of parasite (Ferrari and Vavre, 2011; Cezilly et al., 2014). The interests of different parasitic species may conflict; for example, two parasites may share an intermediate host but require a different definitive host. Parasite-parasite interactions in the intermediate host can result in perturbation of the parasite infection process for each parasite species (Lafferty and Shaw, 2013; Cezilly et al., 2014). As far as we know, microbiomes are not considered to be taking part in crosstalk between an aquatic host and a manipulative parasite. Therefore, we first briefly present the background for microbiomes as plausible and underestimated players in the crosstalk in host-manipulative parasite associations in aquatic ecosystems, and secondly we discuss concepts and -omics methods to determine whether or not host microbiomes can influence host behavior in aquatic models. Finally, we discuss the importance of considering context-dependent changes in the analysis of -omics data to decode and understand the role of a host microbiome in the alteration of host behavior in aquatic ecosystems.

Quantification of Plasmodium falciparum malaria from complex infections in the Peruvian Amazon using quantitative PCR of the merozoite surface protein 1, block 2 (PfMSP1-B2): in vitro dynamics reveal density-dependent interactions

The majority of Plasmodium falciparum field isolates are defined as complex infections because they contain multiple genetically distinct clones. Studying interactions between clones in complex infections in vivo and in vitro could elucidate important phenomena in malaria infection, transmission and treatment. Using quantitative PCR (qPCR) of the P. falciparum merozoite surface protein 1, block 2 (PfMSP1-B2), we provide a sensitive and efficient genotyping method. This is important for epidemiological studies because it makes it possible to study genotype-specific growth dynamics. We compared 3 PfMSP1-B2 genotyping methods by analysing 79 field isolates from the Peruvian Amazon. In vivo observations from other studies using these techniques led to the hypothesis that clones within complex infections interact. By co-culturing clones with different PfMSP1-B2 genotypes, and measuring parasitaemia using qPCR, we found that suppression of clonal expansion was a factor of the collective density of all clones present in a culture. PfMSP1-B2 qPCR enabled us to find in vitro evidence for parasite-parasite interactions and could facilitate future investigations of growth trends in naturally occurring complex infections.

Cerebral malaria: insights from host-parasite protein-protein interactions

BackgroundCerebral malaria is a form of human malaria wherein Plasmodium falciparum-infected red blood cells adhere to the blood capillaries in the brain, potentially leading to coma and death. Interactions between parasite and host proteins are important in understanding the pathogenesis of this deadly form of malaria. It is, therefore, necessary to study available protein-protein interactions to identify lesser known interactions that could throw light on key events of cerebral malaria.MethodsSequestration, haemostasis dysfunction, systemic inflammation and neuronal damage are key processes of cerebral malaria. Key events were identified from literature as being crucial to these processes. An integrated interactome was created using available experimental and predicted datasets as well as from literature. Interactions from this interactome were filtered based on Gene Ontology and tissue-specific annotations, and further analysed for relevance to the key events.ResultsPfEMP1 presentation, platelet activation and astrocyte dysfunction were identified as the key events influencing the disease. 48896 host-parasite along with other host-parasite, host-host and parasite-parasite protein-protein interactions obtained from a disease-specific corpus were combined to form an integrated interactome. Filtering of the interactome resulted in five host-parasite PPI, six parasite-parasite and two host-host PPI. The analysis of these interactions revealed the potential significance of apolipoproteins and temperature/Hsp expression on efficient PfEMP1 presentation; role of MSP-1 in platelet activation; effect of parasite proteins in TGF-β regulation and the role of albumin in astrocyte dysfunction.ConclusionsThis work links key host-parasite, parasite-parasite and host-host protein-protein interactions to key processes of cerebral malaria and generates hypotheses for disease pathogenesis based on a filtered interaction dataset. These hypotheses provide novel and significant insights to cerebral malaria.

EXACERBATION OF PLASMODIUM YOELII MALARIA IN ECHINOSTOMA CAPRONI INFECTED MICE AND ABATEMENT THROUGH ANTHELMINTIC TREATMENT

The effect of chronic intestinal trematode infection on malaria was examined in a murine model of co-infection using Echinostoma caproni and Plasmodium yoelii. BALB/c mice (n = 32) infected with a low dose of E. caproni (approximately 10 cysts) 25-35 days before malaria infection displayed significantly increased malaria parasitemia (P = 0.01), extended patency of malaria (P = 0.03), and increased fatality (47%; P < 0.001) compared to mice infected only with P. yoelii (17X nonlethal strain) (n = 18). Further analysis revealed that differences in malaria parasitemia between fatal co-infections and infections with P. yoelii only were highly significant (P < 0.0001), whereas nonfatal co-infections were not statistically different. Exacerbation of malaria was demonstrated to be reversible through clearance of E. caproni worms by praziquantel treatment administered 10 days before malaria infection. No deaths were observed during malaria infection in mice cleared of their E. caproni infection (n = 10), and parasitemia was significantly reduced from that of untreated co-infected mice (P = 0.03) and was not different from that of mice infected with P. yoelii only. Further studies examining parasite-parasite interactions and host immune response in the echinostome model are warranted to understand the mechanisms affecting the course and outcome of malaria infection during concomitant helminth infection.

Density dependence of postlarval survivorship in primary infections of Protopolystoma xenopodis.

Naive, full-sibling juveniles of Xenopus laevis laevis were exposed to 10, 30, or 50 larvae of the monogenean Protopolystoma xenopodis from an isolate known to produce relatively low adult establishment (typically less than 25% prevalence) in hosts of the same pedigree. Postlarval survival (worms per host) 7 days postinfection (PI), timing from the end of a 10-day infection window, was significantly related and proportional (approximately 31%) to infection dose. Establishment of newly mature adults 90 days PI was low (0-3 worms/host) and unrelated to infection dose. Results confirm that postlarval mortality is severe in primary infections, and that surviving adult infrapopulations appear to be regulated to a very low level (most often 1 worm/ host), even at relatively high larval infection pressures. This density-dependent process could involve direct antagonistic parasite-parasite interactions or indirect interference mediated by parasite-induced host defenses.

Biotic and abiotic effects on endoparasites infecting Dipodomys and Perognathus species.

Between 1989 and 1998, 3,504 rodents of the genera Dipodomys and Perognathus were collected from 4 permanent collecting sites on the University of New Mexico's Long Term Ecological Research station, located on the Sevilleta National Wildlife Refuge (SNWR), Socorro County. New Mexico. All animals were killed and examined for endoparasites (acanthocephalans, cestodes, coccidia, and nematodes). The present report focuses on 3 endoparasite groups, cestodes, coccidia, and nematodes. Specific analyses address how prevalence changes were related to abiotic factors such as habitat, season, or precipitation, and how prevalence of each parasite species in each host species differed in relation to host age, host sex, host reproductive status, host body mass, host density, parasite-parasite interactions, and host specificity. A logistic regression was used to determine which host characters and which abiotic factors are correlated with a parasite infection. Significant variables for at least half of the parasites include season, site, and winter precipitation. However, no parasite prevalences were correlated, and significant variables were not identical between parasites, indicating that each parasite species varied independently and that no generalizations can be drawn. The parasite prevalences in these rodents on the SNWR vary in independent and complex ways.

Changing surface antigen and carbohydrate patterns during the development of Oesophagostomum dentatum.

Living and fixed specimen of Oesophagostomum dentatum were labelled in situ with serum antibodies or a panel of biotin-labelled lectins. Specific binding of antibodies was observed in all parasitic stages--freshly exsheathed 3rd-stage larvae (L3), 3rd- and 4th-stage (L4) larvae cultured in vitro and L3 and L4 and adults isolated from pig intestines. The shedding of the stained layer by motile larvae was inhibited by levamisole-induced paralysis. Larvae cultured in vitro exposed serum-derived proteins on their surface which could be labelled with secondary antibody directed against the respective serum donor species. While freshly exsheathed larvae were recognized by O. dentatum-positive serum only, older larvae and adults cross-reacted with serum from pigs infected with O. quadrispinulatum, a closely related species. Lectin binding varied considerably between stages. While binding was not observed in pre-parasitic stages, Concanavalin A, Soybean Agglutinin, Wheat Germ Agglutinin, Ricinus communis Agglutinin and Peanut Agglutinin bound to developing larvae in varying degrees. Dolichos biflorus Agglutinin only bound to advanced (luminal) larval stages, while adults generally displayed only weak or partial lectin binding (except with Concanavalin A and Wheat Germ Agglutinin). Ulex europaeus Agglutinin only labelled larvae derived from cultures containing 10% pig serum. Cleavage of the carbohydrate residues by sodium periodate treatment resulted in reduction of antibody binding to cultured larvae, but not to freshly exsheathed L3. Concanavalin A, Soybean Agglutinin, and Peanut Agglutinin binding was also reduced by periodate treatment, while binding of Wheat Germ Agglutinin and Ricinus communis Agglutinin was inhibited only in early L3, but not in older stages. The different lectin labelling patterns are related to the different stages of the nematode--infective, invasive, histotropic, and luminal--and may serve as a mode of adaptation for the parasite against the host's immune attack by surface glycoprotein variation, together with antigen shedding (as demonstrated by labelling of motile larvae) and a possible acquisition of host molecules at the parasite's surface. Furthermore, a possible role of this developmental variation in surface carbohydrates in parasite-parasite interactions is discussed.