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Helminth parasites of L. dominicanus from the northern coast of Patagonia. 1 T. cylindraceus, scolex. 2 A. dominicana, scolex. 3 Lyperosomum sp., in toto. 4 S. podicipei, anterior end showing head collar. 5 H. escamosa, anterior end showing head collar. 6 Parorchis sp., in toto. 7 M. madrynensis, in toto. 8 Maritrema sp., in toto. 9 O.
Source publication
The helminth community of Larus dominicanus (Charadriiformes) is reported from Península Valdés, on the Patagonian coast, Argentina. From March 2000 to April 2004, 29 kelp gulls were collected and dissected. All the birds were parasitized by at least 2 of 18 parasite species: 2 cestodes (1 Tetrabothriidae, 1 Dilepididae), 10 trematodes (2 Echinosto...
Contexts in source publication
Context 1
... cylindraceus (Rudolphi, 1819) ( Fig. 1) Site of infection: intestine, mainly the first section. P, 38%; MI, ...
Context 4
... Spirurida (Diesing, 1861); Acuariidae (Seurat, 1913); Acuariinae Raillet, Henry and Sisoff, 1912 Cosmocephalus obvelatus (Creplin, 1825) (Fig. 12) Site of infection: oesophagus. P, 41%; MI, 8.5. ...
Context 5
... Spirurida (Diesing, 1861); Acuariidae (Seurat, 1913); Acuariinae Raillet, Henry and Sisoff, 1912 Cosmocephalus obvelatus (Creplin, 1825) (Fig. 12) Site of infection: oesophagus. P, 41%; MI, ...
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... adunca (Creplin, 1846) (Fig. 13) Site of infection: oesophagus. P, 62%; MI, 6. Deposited specimens: MLP no. 5282 and CNP-Par ...
Citations
... Between 2000 and 2018, 164 waterbirds were examined for helminths in Patagonia (Fig. 1) Diaz et al. 2011;Capasso et al 2022). We have also examined for digenean infections 100 specimens of T. geversianus collected from 2007 to 2010 in the estuary of Península Valdés, Chubut Province, Argentina (see Gilardoni et al. 2011). ...
The coastline of Argentine Patagonia in the Southwest Atlantic provides highly productive habitats for a variety of aquatic birds. Both resident birds and migratory birds coming for wintering from the high arctic tundra, converge in these wetlands for resting and feeding, which favours parasite transmission. In the course of helminth diversity survey in Patagonian birds, we found a new digenean species belonging to the genus Parorchis (Philophthalmidae). Herein, we describe its complete life cycle and provide the morphological description accompanied by DNA sequence data. Adult specimens were obtained from the resident Kelp Gull Larus dominicanus (Laridae), and Nearctic migratory shorebirds, the Baird’s Sandpiper Calidris bairdii and the White-rumped Sandpiper Calidris fuscicollis (Scolopacidae). Rediae of the new species were found in the muricid gastropod Trophon geversianus (Muricidae), whose distribution is restricted to the intertidal and subtidal marine south coasts of Argentina and Chile. Sequences of complete ITS and partial 28S regions confirmed the conspecificity of the rediae from T. geversianus and adults specimens recovered from L. dominicanus and C. fuscicollis. Cercariae emerge from these molluscs and quickly encyst on the substrate including surfaces of the mollusc itself; shorebirds become infected by eating snails. We examine phylogenetic affinities of the new species using partial 28S sequences. Our analysis placed the new species in a clade with other Parorchis spp., which also use muricid gastropods as intermediate hosts. This study contributes to the knowledge of the diversity of marine trematodes in the subpolar region of South America.
... Dentro de dicha familia, las especies del género Maritrema Nicoll, 1907 son componentes comunes en las comunidades de parásitos de aves en ambientes marinos, mixohalinos y de agua dulce (e.g. Cremonte y Martorelli, 1998;Martorelli et al., 2004;Diaz et al., 2011;Rauque et al., 2013;Capasso et al., 2019). ...
In myxohaline environments, the digenean Maritrema bonaerense shares intermediate host species (crustaceans) and a definitive host species (bird) with another member of the family Microphallidae: Microphallus szidati. However, only M. szidati has been recorded parasitizing intermediate hosts in freshwater environments. Given that both species of microphallids would have affinity for the same host species in marine or mixohaline environments, it is possible that the absence of M. bonaerense in freshwater environments is mainly due to an environmental barrier that may affect the transmission of the free-swimming stages of the digenean (cercariae). Based on these considerations, the objective of this study was to analyze the effect of salinity on the survival of cercariae of M. bonaerense. For this, cercariae emitted by Heleobia australis from myxohaline environments were exposed to salinities of 16 ppm and 1 ppm in culture plates with 48 wells of 16 ml capacity. For 10 hours plates were observed every hour under a stereomicroscope and the number of live cercariae in each compartment was recorded. 24 hours after the experiment began, plates were observed, recording the total number of live cercariae, which were classified as active cercariae, lethargic cercariae, and lethargic cercariae that lost their tails. The effect of salinity on the survival of cercariae was analyzed by applying Generalized Linear Models (GLM). The results of the study revealed a marked influence of salinity levels on the survival and mobility of cercariae, and allow us to assume that M. bonaerense is a species better adapted to marine and mixohaline environments.
... Thick-billed murre Common loon, red-throated loon, common eider (Kinsella and Forrester, 1999;Haukisalmi, 2015;Skirnisson, 2015) -Black-throated loon, yellow-billed loon ----Fimbriarioides intermedia (Fuhrmann, 1913) Common eider, king eider Common eider (Bishop and Threlfall, 1974;Skirnisson, 2015) -C o m m o n e i d e r , k i n g eider; cysticercoids in barnacles Semibalanus balanoides (Schiller, 1955 (Pemberton, 1963;Pomeroy and Burt, 1964;Williams and Harris, 1965;Threlfall, 1967Threlfall, , 1968aBakke, 1985 (Baer, 1956(Baer, , 1962Pomeroy and Burt, 1964;Williams and Harris, 1965;Threlfall, 1967Threlfall, , 1968Threlfall, , 1971Haukisalmi, 2015;Parejo et al., 2015) Kelp gull (Diaz et al., 2011) European herring gull, glaucous-winged gull, black-legged kittiwake, western gull, black-tailed gull (Belogurov et al., 1968;Bondarenko and Kontrimavicius, 1999;Uchida et al., 1991;Hoberg et al., 1995) Kelp gull (Gonzales- (Baer, 1956(Baer, , 1962Pemberton, 1963;Pomeroy and Burt, 1964;Williams and Harris, 1965;Threlfall, 1967Threlfall, , 1968Threlfall, a, 1971Sanmartin et al., 2005) -Slaty-backed gull, common gull, black-tailed gull, common tern (Belogurov et al, 1968;Uchida et al., 1991) -G re a t e r crested tern (Shipley, 1903) --Tetrabothrius immerinus (Abilgaard, 1790) European herring gull, black-legged kittiwake Common murre, black guillemot, common loon, red-throated loon (Baer, 1962;Kinsella and Forrester, 1999;Haukisalmi, 2015) -Red-throated loon, western grebe, red-necked grebe (Belogurov, 1965;Stock and Holmes, 1988) ----Tetrabothrius jaegerskioeldi (Nybelin, 1916) Common murre, thick-billed murre, black guillemot Black guillemot (Nybelin, 1916;Baer, 1956) -C o m m o n m u r r e , black guillemot, spectacled guillemot, pigeon guillemot, marbled murrelet, rhinoceros auklet, glaucous-winged gull, pelagic cormorant (Hoberg, 1992(Hoberg, , 1979 Northern fulmar Northern fulmar, great shearwater, Scopoli's shearwater (Baer, 1956(Baer, , 1962Riley and Owen, 1975;Foster et al., 1996;Hervias et al., 2013) -N o r t h e r n f u l m a r , fork-tailed storm petrel (Temirova and Scriabin, 1978) Waved albatross, Antarctic petrel (Temirova and Scriabin, 1978 ...
To date, 53 helminth species have been discovered in the gastrointestinal tracts and other internal organs of Barents Sea birds. These parasites circulate in pelagic and coastal biocenoses. This paper analyzes their spatial distribution and host preferences in other geographical regions based on data collected by the author in the course of long-term studies and literature data. It is established that the only Barents Sea endemic is the cestode Tetrabothrius morschtini. Fifty-two species were recorded in the North Atlantic, 48 species in the North Pacific, six species in the South Atlantic, six in the Australia-New Zealand region, five in the Antarctic, four in the South Pacific, and three in the Indian Ocean basin. Analysis showed that these parasites feature two main distribution types. The amphiboreal distribution typical for the majority of species is determined by the existence of a single transarctic range of many intermediate and definitive hel-minth hosts in the Pliocene and the dispersion of their eggs by birds during interglacial periods of the Pleis-tocene. The bipolar distribution typical for 12 species is likely determined by the transfer of parasites from the Holarctic realm by their definitive hosts in the course of species divergence or during seasonal migrations. It cannot be ruled out that some helminth species have migrated from the Antarctic region to the Holarctic realm with their definitive hosts. The roles of key evolutionary-environmental factors (e.g., mobility of definitive hosts, presence of intermediate hosts, and life spans of sexually mature helminth stages) determining the biogeographical patterns of various host-parasite complexes were examined.
... Gymnophallid adult digeneans infect marine charadriiform (shorebirds) or anseriform (ducks) [19,24,54] and typically have a three-host life cycle with bivalves as first intermediate hosts and bivalves or, more rarely, gastropods [13] or polychaetes [35,51] as second intermediate hosts [54]. There are also known examples of unusual cycles that involve parthenogenetic metacercariae [26,27] or no free-living stage [31]. ...
The coquina, Donax variabilis , is a known intermediate host of monorchiid and gymnophallid digeneans. Limited morphological criteria for the host and the digeneans’ larval stages have caused confusion in records. Herein, identities of coquinas from the United States (US) Atlantic coast were verified molecularly. We demonstrate that the current GenBank sequences for D. variabilis are erroneous, with the US sequence referring to D. fossor . Two cercariae and three metacercariae previously described in the Gulf of Mexico and one new cercaria were identified morphologically and molecularly, with only metacercariae occurring in both hosts. On the Southeast Atlantic coast, D. variabilis ’ role is limited to being a facultative second intermediate host, and D. fossor, an older species, acts as both first and second intermediate hosts. Sequencing demonstrated 100% similarities between larval stages for each of the three digeneans. Sporocysts, single tail cercariae, and metacercariae in the incurrent siphon had sequences identical to those of monorchiid Lasiotocus trachinoti , for which we provide the complete life cycle. Adults are not known for the other two digeneans, and sequences from their larval stages were not identical to any in GenBank. Large sporocysts, cercariae ( Cercaria choanura ) , and metacercariae in the coquinas’ foot were identified as Lasiotocus choanura (Hopkins, 1958) n. comb. Small sporocysts, furcocercous cercariae, and metacercariae in the mantle were identified as gymnophallid Parvatrema cf. donacis . We clarify records wherein authors recognized the three digenean species but confused their life stages, and probably the hosts, as D. variabilis is sympatric with cryptic D. texasianus in the Gulf of Mexico.
... Profilicollis chasmagnathi (Holcman-Spector, Mañé-Garzón & Dei-Cas, 1977) is the only representative of the genus so far reported at adult stage along the southwestern Atlantic coast (Lorenti et al. 2018). This species has been recorded at the estuaries of Buenos Aires Province and Patagonian coasts, infecting the gut of several bird species (Martorelli 1989;Vizcaíno 1989;Diaz et al. 2011;La Sala et al. 2013;Lorenti et al. 2018). Cystacanths of this species are common parasites of different crab species inhabiting estuarine and rocky intertidal marine habitats in Uruguay and Argentina (Holcman-Spector et al. 1977;Martorelli 1989;Alda et al. 2011;La Sala et al. 2012;Méndez Casariego et al. 2016;Rodríguez et al. 2017). ...
... Such facts are relevant, especially considering the low specificity of this parasite for its definitive hosts. Indeed, P. chasmagnathi has been reported in six families of birds, belonging to five orders (Martorelli 1989;Vizcaíno 1989;Torres et al. 1993;Diaz et al. 2011;La Sala et al. 2013;Lorenti et al. 2018), including podicipedids and phalacrocoracids, which are primarily piscivorous (Petracci et al. 2009;Josens et al. 2010) and abundant in Mar Chiquita basin (Favero et al. 2001;Ferrero and Iribarne 2001). ...
Polymorphid acanthocephalans are parasites of marine mammals, waterfowl and ichthyophagous birds. Among these, the genus Profilicollis is known to use exclusively decapods as intermediate hosts. Here, we report the first record of living cystacanths of Profilicollis parasitizing the body cavity of a fish host, Oligosarcus jenynsii, inhabiting the freshwater section of an estuarial system, Mar Chiquita coastal lagoon, in southeast Buenos Aires Province, Argentina. In this environment, cystacanths of Profilicollis chasmagnathi have been previously recorded infecting decapod crabs and as transient accidental infections in the gut of some carcinophagous fishes. In the present study, larvae from the crab Neohelice granulata, from the intestine of the estuarine fish Odontesthes argentinensis and from the body cavity of O. jenynsii were morphologically and genetically compared , confirming their identity as P. chasmagnathi, a species characteristic of estuaries and marine coasts along Argentina, Uruguay and Chile. These findings can be interpreted as a possible case of incipient paratenicity for Profilicollis, and a coloni-zation event of freshwater habitats, probably promoted by the highly variable conditions, typical of ecotonal environments. In addition, cystacanths of the genus Polymorphus were also found in O. jenynsii, representing the first record of this genus in Oligosarcus from Argentina.
... Both groups act as definitive hosts, while crustaceans, fishes, and cephalopods are intermediate hosts (Hoberg, 1989). This parasite has been recorded in various birds of the order Charadriiformes (Alcidae, Stercorariidae, Laridae) from Europe (Roca et al., 2001;Santoro et al., 2011;Haukisalmi, 2015;Parejo et al., 2015), Asia (Uchida et al., 2005;Kuklin, 2011), North America (Threlfall, 1968;Muzaffar, 2009), South America (Argentina and Chile) (González-Acuña et al., 2009;Diaz et al., 2011), and Antarctica (Barbosa & Palacios, 2009;Rocka, 2019). In Latin America, it has been isolated from the gull L. dominicanus in Chile (Torres et al., 1991(Torres et al., , 1992(Torres et al., , 1993González-Acuña et al., 2009) and later from the same host in Argentina (Diaz et al., 2011). ...
... This parasite has been recorded in various birds of the order Charadriiformes (Alcidae, Stercorariidae, Laridae) from Europe (Roca et al., 2001;Santoro et al., 2011;Haukisalmi, 2015;Parejo et al., 2015), Asia (Uchida et al., 2005;Kuklin, 2011), North America (Threlfall, 1968;Muzaffar, 2009), South America (Argentina and Chile) (González-Acuña et al., 2009;Diaz et al., 2011), and Antarctica (Barbosa & Palacios, 2009;Rocka, 2019). In Latin America, it has been isolated from the gull L. dominicanus in Chile (Torres et al., 1991(Torres et al., , 1992(Torres et al., , 1993González-Acuña et al., 2009) and later from the same host in Argentina (Diaz et al., 2011). Despite being a common parasite in seagulls, this study presents the first record of T. cylindraceus in L. pipixcan worldwide. ...
... Furthermore, other genera of family Dilepididae (e.g. Alcataenia and Anomotaenia) have been recorded in other gulls such L. dominicanus and brown-hooded gull Chroicocephalus maculipennis from Chile (Torres et al., 1991(Torres et al., , 1992(Torres et al., , 1993González-Acuña et al., 2009) and other South American (Diaz et al., 2011) and European countries (Sanmartín et al., 2005;Álvarez et al., 2006;Sagerup et al., 2009;Santoro et al., 2011). Also, other cyclophyllidean genera such Aploparaksis (Aploparaksidae), Nadejdolepis, Microsomacanthus and Wardium (Hymenolepididae) have been recorded in gulls around the world (Khalil et al., 1994;González-Acuña et al., 2009;Sagerup et al., 2009;Bondarenko & Kontrimavichus, 2018). ...
Parasitological studies of the Franklin’s gull, Leucophaeus pipixcan, are scarce, and knowledge about its endoparasites is quite limited. In order to describe its parasitic community, a total of 60 Franklin’s gulls were captured in the coastal area in central Chile, using modified Bal-chatri traps. Ectoparasites were collected from all 60 live individuals through inspection of their plumage, while 30 were examined for endoparasites by standard parasitological necropsy. The prevalence of ectoparasites was 78.3%, including the feather mite Zachvatkinia larica (43.3%) and four species of lice: Actornithophilus piceus lari (15.0%), Austromenopon transversum (6.7%), Quadraceps punctatus (10.0%) and Saemundssonia lari (46.7%). Some 25 of 30 (83.3%) of birds necropsied were parasitized with the following helminths: Aporchis sp. (6.7%), Tetrabothrius cylindraceus (56.7%), Cyclophyllidea gen. sp. (3.3%), Profilicollis altmani (56.7%), Eucoleus contortus (10.0%), Cosmocephalus obvelatus (13.3%), Paracuaria adunca (10.0%), Stegophorus sp. (3.3%) and Tetrameres skrjabini (3.3%). To our knowledge, with the exception of P. altmani, these helminths are reported for first time in the Franklin’s gull.
... This strong relationship between human past populations from Patagonia and the marine species imply a possible source of parasitic infections and zoonotic risk. This hypothesis is also sustained by the many evidences of marine parasites recorded by ecological and taxonomical research in current samples from Southern Atlantic Ocean (Cremonte et al., 2002(Cremonte et al., , 2005Diaz et al., 2011;Alarcos and Timi, 2012;Cantatore and Timi, 2015;Agüero et al., 2016;Lanfranchi et al., 2016;Luque et al., 2017;Poulin and Jorge, 2018;Hernández-Orts et al., 2019a, 2019b, which could also be present in the past. Thus, the aim of this paper is to propose the potential parasitic infections produced by the consumption of marine molluscs, fishes, seabirds and marine mammal species by human populations from Patagonia during the Holocene, considering the current parasitic species identified in the Southern Atlantic Ocean. ...
Several foodborne diseases have been described in coastal populations from the past, many of them including parasitic infections related to marine diets. Considering this background, the strong relationship between hunter-gatherers from Patagonia and the marine species implies a possible source of parasitic infections and zoonotic risk. However, marine parasitic species have not been identified in archaeological sites from Patagonia so far. The aim of this paper is to propose the potential parasitic infections produced by the consumption of marine molluscs, fishes, birds and sea mammals by human populations from Patagonia during the Holocene, considering the current parasitic species identified in the Southern Atlantic Ocean. We searched in journal articles and book chapters for references of archaeological remains of molluscs, fishes, seabirds and marine mammals recorded in archaeological sites from the Atlantic coast below the 42nd parallel South. Afterwards, we surveyed all the macroparasites of marine origin identified by current parasitological research in the same species found in the archaeological record. We found that most of the marine species in the zooarchaeological record of Patagonia are currently hosts of many parasites. Some species of molluscs, fishes and pinnipeds are highly infected by larvae that are potentially hazardous for human health. Some of them are responsible for acute or chronic zoonotic diseases, with severe consequences depending on how the food was cooked, the amount of consumed parasites and the immune response of the host, in this case, humans. Fishes are host of several parasites related to anisakidosis and corynosomiasis. Sea lions species were also a potential source of the same zoonosis but also diphyllobothriasis. Molluscs are hosts of several parasitic species, but with less severe consequences for human health. On the other hand, birds are infected by adult parasites, without direct zoonotic importance. These findings, although limited by temporal and environmental variability, can provide a speculative overview about the potential influence of marine diets in the health of past hunter-gatherers of Patagonia, particularly if fishes, molluscs or marine mammals were consumed inadequately cooked.
... L: Chubut Province: Fracaso Beach (42°25'S, 64°07'W), Puerto Madryn Beach (42°47'S, 65°02'S). R:,Diaz et al. (2011). Spheniscus magellanicus (Forster) (Sphenisciformes, Spheniscidae). ...
A detailed list of acanthocephalans from Argentina was generated based on 205 published records. The list includes 52 named and 35 undetermined species of Acanthocephala infecting 6 species of invertebrate (2 amphipods, 3 decapods and 1 insect) and 155 species of vertebrate (one cartilaginous fish, 95 bony fishes, 10 amphibians, 3 reptiles, 13 birds and 33 mammals) host species in the Argentinean territory. The present list contains information on the invertebrate and vertebrate host(s), site of infection, developmental stage and locality(ies) of the acanthocephalans listed and references. For some species of acanthocephalans, information about repositories of the type material, voucher specimens, and DNA sequences of individual taxa are also presented. Finally, a host-Acanthocephala list is also provided. The data compiled revealed considerable gaps in the knowledge of the diversity, taxonomy, distribution, and life cycles of the acanthocephalans from Argentina.
... Species of the genus Maritrema Nicoll 1907 in the tribe Maritrematiini, are characterized by the presence of a small and linguiform body, uterine coils entirely postcaecal, vitellaria in two symmetrical ribbons surrounding uterus and testes, opened or closed posteriorly (Deblock, 2008). Species of Maritrema are very common components of the parasite communities in brackish, marine and to a lesser extent, freshwater birds (Cremonte and Martorelli, 1998;Diaz et al., 2011;Martorelli et al., 2004;Rauque et al., 2013). ...
Birds are hosts of a wide diversity of trematodes. Between them, the Microphallidae is a common family with a cosmopolitan distribution. Nevertheless, only 10 Maritrema species have been recorded previously in South America. The aim of the present paper is to describe a new species of Maritrema parasitizing the Nearctic Baird's sandpiper, Calidris bairdii in its wintering areas in Patagonia, Argentina. We also analyze and compare the microphallid diversity in two host species. We collected 44 C. bairdii and 50 C. fuscicollis in search of helminths. Trematodes were found only in C. bairdii. A total of 694 trematodes belonging to 4 microphallid species were found parasitizing the intestine and caeca. Four microphallid species were found: Maritrema formicae, Odhneria odhneri, Levinseniella cruzi and Maritrema pichi n. sp. M. formicae showed the highest prevalence, while M. pichi n. sp. was the species with the highest mean intensity and mean abundance. The new species M. pichi n. sp. differs from congeners by the position of the ventral sucker that is included within the vitellarium ring, the ovary is anterior to the ventral sucker, and the testes are lateral to it. We discuss the parasitological results in relation with the biological and ecological characteristics of both different host species.
... All members of the genus Profilicollis infect mainly waterfowl as adults and use decapods as intermediate hosts (Zdzitowiecki, 1985;Nickol et al., 1999;. Along the southwestern Atlantic coast, only adults of P. chasmagnathi have been reported, from the gut of several bird species in the estuaries of Buenos Aires Province (Martorelli, 1989;Vizcaíno, 1989;La Sala et al., 2013), and from that of the kelp gull Larus dominicanus (Lichtenstein) (Aves, Laridae) on the coast of Chubut Province (Diaz et al., 2011). In contrast, cystacanths of 2 species of Profilicollis have been reported on the southwestern Atlantic coast: P. chasmagnathi parasitizes different crab species from estuarine and rocky intertidal habitats in Uruguay and Argentina (Holcman-Spector et al., 1977a;Martorelli, 1989;La Sala et al., 2012;Rodríguez et al., 2017), while P. altmani parasitizes the mole crab Emerita brasiliensis (Schimitt) on sandy beaches along the Uruguayan coast . ...
... Mature acanthocephalan specimens were obtained from a total of 89 kelp gulls, L. dominicanus, out of which 29 were collected along the coast of Península Valdés and adjacent areas (42°05' to 42º53'S, 64°21' to 65º04'W), Chubut Province, Argentina (see Diaz et al., 2011). The remaining 60 gulls were obtained from the same area between 2012 and 2015 while conducting a project aimed to mitigate the interaction between kelp gulls and southern right whales developed by the Ministerio de Ambiente y Control del Desarrollo Sustentable, Chubut and the CCT CONICET-Centro Nacional Patagónico (Decree 1106/12). ...
... Prevalence (P), mean intensity (MI) and mean abundance (MA) were calculated following Bush et al. (1997). The seasonal distribution of adult acanthocephalans was based on counts of the kelp gulls made by Diaz et al (2011). For data analysis, Spearman's rankorder coefficient (rs) was used to establish the relationship between crab size and season vs. P and MI. ...
This study verifies the identity of adult specimens of the parasite Profilicollis chasmagnathi (Achantocephala, Polymorphidae) recovered from kelp gulls Larus dominicanus (Aves, Laridae), and cystacanths found in crabs Cyrtograpsus altimanus (Crustacea, Decapoda) from the southwestern Atlantic coast. The life cycle of this parasite is elucidated in the intertidal zone of Patagonia, Argentina, based on morphological and molecular data. Preferences by size and sex of the intermediate host and seasonal variation of this parasite are provided, contributing to the knowledge of this host-parasite association.
