Low Parasite Richness Research Articles

Non‐native freshwater snails: a global synthesis of invasion status, mechanisms of introduction, and interactions with natural enemies

Abstract Non‐native freshwater snails can play important roles as consumers, hosts, and prey. Despite their potential ecological importance, global patterns in non‐native snail taxonomy, geography, and ecology have not been documented. Our objectives were to use a semi‐quantitative systematic review to describe non‐native freshwater snail global diversity, distribution, mechanisms of introduction, and interactions with natural enemies, including parasites and predators. Based on 506 relevant publications, we recorded 95 non‐native freshwater snail species from 16 families. Six taxonomic families, and pulmonate snails as a group, were over‐represented relative to the number of species expected by chance. Eight snail species represented 63% of the research records. A few snail taxa (15%) were widespread global invaders, reported from four or more continents, while most invasions were limited to a single continent. Australia and the Pacific Islands were the largest ‘sink’ for non‐native snails, with the greatest difference in the number of non‐native taxa relative to native taxa that had spread to other continents. Aquarium hobby sales were implicated as the most common mechanism of introduction (41% of species), followed by “hitchhiking” on aquatic vegetation, human consumption, use for biocontrol, transportation in canals, commercial shipping, and outdoor recreation. A search of internet sales posts indicated that four of the six over‐represented snail families were readily available for purchase online. Non‐native snails hosted parasites of wildlife, livestock, and human health importance, yet on average had 80% lower parasite richness in their non‐native compared to native range. At least 65 taxa were documented as consumers of non‐native snails, including native predators of conservation concern. These findings suggest that non‐native snails often are released from parasitism, but may commonly experience biotic resistance from predators. Our synthesis emphasizes the relatively high diversity of non‐native snails, but the disproportionate role of a few taxonomic groups in driving ecological, economic, and public health challenges. Moving forward, it will be important to limit new snail introductions through policy, education, and monitoring, particularly as the effective control of established snail invasions remains challenging in most ecosystems.

Louse flies in Azorean and mainland populations of four Passeriformes species: A new perspective to parasite Island syndromes

Hippoboscid flies, also known as louse flies, are obligate blood-feeders ectoparasites of birds and mammals. By studying louse fly parasites of four Passeriformes species, Eurasian blackbird (Turdus merula), Eurasian blackcap (Sylvia atricapilla), common chaffinch (Fringilla coelebs) and European robin (Erithacus rubecula), with dissimilar time of colonization of Azores islands, we tested whether: (i) island host populations have lower parasite richness than the mainland one; (ii) island host populations undergo higher parasite prevalence, mean intensities and mean abundance than the mainland one; (iii) island parasite diversity are composed exclusively by specific parasites and (iv) parasite richness is positively correlated with the island area and proximity to the continent. For these purposes, 775 birds were sampled for presence of louse flies, by modified fumigation chamber method, from Azores Islands (São Miguel, Terceira and Flores) and Portugal mainland. Insular and mainland parasite assemblages were statistically compared. We record for the first time to Azores, Ornithomya fringillina and Icosta minor from Portugal mainland. Louse flies had highest prevalence and abundance from Azores Islands compared to those observed in mainland birds, especially blackbirds. The insular parasite diversity of Azores blackbirds, blackcaps and chaffinches was richer than the one observed in mainland population. None of the hippoboscid flies observed on the islands and mainland were host-specific. Thus, our findings provide an upgrade of parasite island syndromes knowledge, in the context of the ectoparasites, namely to the hippoboscid flies case.

Ecological release in lizard endoparasites from the Atlantic Forest, northeast of the Neotropical Region.

We compared lizard endoparasite assemblages between the Atlantic Forest and naturally isolated forest enclaves to test the ecological release hypothesis, which predicts that host specificity should be lower (large niche breadth) and parasite abundance should be greater for parasites from isolated forest enclaves (poor assemblages) than for parasites from the coastal Atlantic Forest (rich assemblages). Parasite richness per specimen showed no difference between the isolated and non-isolated areas. Parasite abundance did not differ between the isolated and non-isolated areas but showed a positive relationship with parasite richness considering all areas (isolated and non-isolated). Furthermore, host specificity was positively related to parasite richness. Considering that host specificity is inversely proportional to the host range infected by a parasite, our results indicate that in assemblages with greater parasite richness, parasites tend to infect a smaller range of hosts than do those in simple assemblages. In summary, our study partially supports the ecological release hypothesis: in assemblages with greater parasite richness, lizard parasites from Atlantic Forest are able to increase their parasite abundance (per host), possibly through facilitated infection; however, the amplitude of infected hosts only expands in poor assemblages (lower parasite richness).

Gastrointestinal helminths of Emperor Penguin (Aptenodytes forsteri) from Antarctica

Although research on parasitic diseases in Antarctic birds is scarce and the information largely fragmented, an increasing number of studies are currently in progress in this area. The host/parasite relationship is very important for understanding the impact of parasitism on the seabirds’ feeding ecology, especially in those isolated regions where the host is extremely sensitive to new diseases. Penguins are a big favorite for these studies because of their importance as indicators of change in the Antarctic ecosystem. This study aims at adding information on gastrointestinal parasites of the Emperor Penguin Aptenodytes forsteri from Snow Hill colony. Based on a sample of 43 individuals found freshly dead (3 adults and 40 chicks) from predation or starvation, the gastrointestinal helminth community in Emperor penguins was composed of two species of cestodes (Parorchites zederi and Tetrabothrius sp.) and three species of nematodes (Stegophorus macronectes, Tetrameres sp. and Contracaecum osculatum). This is the first record of S. macronectes in the Emperor Penguin. The low parasite richness observed might be related to the stenophagic and pelagic diet of this host.

Helminth Parasites of the Lizard Nothobachia ablephara (Gymnophthalmidae) in Caatinga Areas from the Sertão of Brazil.

The lizard Nothobachia ablephara is endemic to dune areas and sandy soils adjacent to the São Francisco River in semiarid northeastern Brazil. Forty-nine lizard specimens were collected in 2 Caatinga areas in the municipality of Petrolina in Pernambuco state. Three gastrointestinal helminth taxa were identified, the nematodes Parapharyngodon alvarengai and Physaloptera sp. and the cestode Oochoristica sp. Nothobachia ablephara showed low parasite richness, but high levels of infection by P. alvarengai. There were no significant differences between the parasitism rates of the 2 study areas or between male and female lizards. This is the first study on parasitism in N. ablephara, thereby increasing knowledge of parasite fauna that infect gymnophthalmid lizards in the Sertão of Brazil.

Gastrointestinal helminths of Adélie penguins (Pygoscelis adeliae) from Antarctica

Knowledge about parasitic organisms in Antarctica is scarce and fragmentary. The study reported here adds to the knowledge of gastrointestinal parasites of the Adelie penguin ( Pygoscelis adeliae ) (Sphenisciformes), from 25 de Mayo/King George Island (South Shetlands), Bahia Esperanza (Hope Bay) and Avian Island (Antarctica). Thirty-five freshly dead specimens (20 chicks and 15 adults) were collected from December 2007 to December 2014 and examined for internal macroparasites. Three adult parasite species were found: one Cestoda, Parorchites zederi , and two Nematoda, Stegophorus macronectes and Tetrameres sp. Immature Tetrabothrius sp. were found in hosts from Avian Island. Helminth communities are known to be related to host feeding behaviours. Low parasite richness observed in Adelie penguins could be related to the stenophagic and pelagic diet of this host species, which feeds almost exclusively on krill. Keywords: Parorchites zederi ; Stegophorus macronectes ; Tetrameres sp.; parasites; ecosystem health. (Published: 16 June 2016) Citation: Polar Research 2016, 35 , 28516,http://dx.doi.org/10.3402/polar.v35.28516

Annual variation of parasite communities of deep-sea macrourid fishes from the western Mediterranean Sea and their relationship with fish diet and histopathological alterations

Parasite communities of three abundant benthopelagic macrourid species (Hymenocephalus italicus, Nezumia aequalis and Trachyrincus scabrus) of the upper slope from the western Mediterranean were analysed seasonally. Histopathological, dietary and environmental information (temperature, salinity, O2 and turbidity) were also obtained. The three fish hosts shared only three parasite species (the nematodes Raphidascaris macrouri and Hysterothylacium aduncum and the acanthocephalan Echinorhynchus trachyrinci). H. italicus, the most benthopelagic fish, showed low parasite richness and diversity. The highest total mean abundance of parasites was found in spring for H. italicus and T. scabrus, coinciding with the highest prevalence/abundance of the majority of parasites whereas parasites of N. aequalis exhibited the highest richness, mean abundance and diversity in winter. Parasites related with benthic or infaunal preys were linked to autumn and summer samples off Besós (Barcelona). Some parasites were also linked to high turbidity, which may be due to higher abundances of the intermediate hosts, such as near-bottom zooplaktonic or suprabenthic preys. Few histopathological alterations (e.g. cysts of unknown aetiology) were observed restricted to the two most benthic-feeding fish species inhabiting more closely the near-bottom/sediment level, especially in autumn.

Biogeography of haemo- and ectoparasites of an arid-land bird, the Trumpeter finch

The study of biogeographical patterns is basic to understand the processes that rule the distribution of parasites and to understand the influence that they have on host population dynamics. We tested (i) whether island dwelling host populations have lower parasite richness and higher prevalence than the mainland one; and, (ii) whether an expanding host population undergoes both lower parasite richness and prevalence than the source one. For these purposes, we studied the parasite fauna (haemo- and ectoparasites) of 398 Trumpeter finches (Bucanetes githagineus), an arid-adapted passerine, in three regions, the Canary Islands, south-eastern Iberian Peninsula (continental expanding) and Northwest Africa (mainland, source population). We searched for blood parasites microscopically. We studied feather lice and feather mites by scanning plumage of trapped birds. Whereas we found two haemoparasite species in the mainland/source population, one in the island and two in the expanding population, we found two ectoparasites species in the mainland/source and three both in the island and in the expanding populations. Average and total prevalence of haemoparasites were highest in the mainland/source population. Ectoparasites had the lowest prevalence in the mainland/source population. Thus, we found that blood parasites fit the biogeographical predictions whereas ectoparasites do not.

Macroparasite community of the Eurasian red squirrel (Sciurus vulgaris): poor species richness and diversity

The Eurasian red squirrel (Sciurus vulgaris) is the only naturally occurring tree squirrel throughout its range. We aim at improving current knowledge on its macroparasite fauna, expecting that it will have a poor parasite diversity because in species that have no sympatric congeners parasite richness should be lower than in hosts sharing their range with several closely related species, where host-switching events and lateral transmission are promoted. We examined gastro-intestinal helminth and ectoparasite communities (excluding mites) of, respectively, 147 and 311 red squirrel roadkills collected in four biogeographic regions in Italy and France. As expected, the macroparasite fauna was poor: we found five species of nematodes and some unidentified cestodes, three fleas, two sucking lice and two hard ticks. The helminth community was dominated by a single species, the oxyurid Trypanoxyuris (Rodentoxyuris) sciuri (prevalence, 87%; mean abundance, 373 ± 65 worms/host). Its abundance varied among seasons and biogeographic regions and increased with body mass in male hosts while decreased in females. The most prevalent ectoparasites were the flea Ceratophyllus (Monopsyllus) sciurorum (28%), whose presence was affected by season, and the generalist tick Ixodes (Ixodes) ricinus that was found only in France (34%). All the other helminths and arthropod species were rare, with prevalence below 10%. However, the first record of Strongyloides robustus, a common nematode of North American Eastern grey squirrels (S. carolinensis), in two red squirrels living in areas where this alien species co-inhabits, deserves further attention, since low parasite richness could result in native red squirrels being particularly vulnerable to parasite spillover.

Gastrointestinal helminths of Gentoo penguins (Pygoscelis papua) from Stranger Point, 25 de Mayo/King George Island, Antarctica

The aim of this work is to contribute to the knowledge of gastrointestinal parasites of the Gentoo penguin (Pygoscelis papua) from 25 de Mayo/King George Island (South Shetlands, Antarctica). Gastrointestinal tracts of 37 fresh dead individuals (21 chicks, 10 juveniles, and 6 adults) were collected from December 2006 to February 2012 and examined for macroparasites. Four adult parasite species were found: one Cestoda species (Parorchites zederi), two Nematoda species (Stegophorus macronectes and Tetrameres wetzeli), and one Acanthocephalan (Corynosoma shackletoni). Two species of immature acanthocephalans, Corynosoma hamanni and Corynosoma bullosum, were found in a single host. This is the first record of Tetrameres wetzeli in Gentoo penguins. The low parasite richness observed could be related to the stenophagic and pelagic diet of this host species which feeds almost exclusively on krill.

The parasites of the invasive Chinese sleeperPerccottus glenii(Fam. Odontobutidae), with the first report ofNippotaenia mogurndaein Ukraine

The parasites of the Asian invasive fish, Chinese sleeper Perccottus glenii , were studied in 6 localities in different parts of Ukraine. In total, 15 taxa of parasites were registered; among them were 1 species of Microsporidia, 5 species of ciliates, 2 species of cestodes, 2 species of trematodes, 2 species of nematodes, 1 species of acanthocephalan, 1 species of parasitic crustacean and 1 mollusk (glochidia). The invasive Chinese sleeper is included as a paratenic host in the life cycle of the parasites of indigenous reptiles in Europe. The non-indigenous cestode Nippotaenia mogurndae occurred in the intestine of the Chinese sleeper from the Ivachiv Reservoir (Dniester River basin). This cestode is recorded for Ukrainian fauna for the first time. In addition, 3 species of parasites were recorded in the Chinese sleeper for the first time: Nicolla skrjabini , Cosmocephalus obvelatus and Pomphorhynchus laevis . We note the low similarity among the different localities and the low parasite richness, that suggest that the parasite fauna of the Chinese sleeper in Ukraine is in transition.

Gastrointestinal parasites in Chinstrap Penguins from Deception Island, South Shetlands, Antarctica

Knowledge about parasites of Antarctic birds is fragmented and scarce. The aim of this work is to contribute to the knowledge of gastrointestinal parasites of the Chinstrap Penguin (Pygoscelis antarctica) from Deception Island (South Shetlands, Antarctica). Gastrointestinal tracts of 64 fresh dead individuals (61 chicks and three adults) were collected from December 2006 to February 2009 and examined for macroparasites. Three adult parasite species were found: two Cestoda species (Parorchites zederi and Tetrabothrius pauliani) and one Nematoda species (Stegophorus macronectes). Also, immature acanthocephalans (Corynosoma sp.) were found in one penguin. The low parasite richness observed could be related to the stenophagic and pelagic diet of the host species. False negatives were found in coprological studies.

Species abundance and the distribution of specialization in host–parasite interaction networks

1 Recent studies have evaluated the distribution of specialization in species interaction networks. Species abundance patterns have been hypothesized to determine observed topological patterns. We evaluate this hypothesis in the context of host–parasite interaction networks. 2 We used two independent series of data sets, one consisting of data for seven sites describing interactions between freshwater fish and their metazoan parasites and another consisting of data for 25 localities describing interactions between fleas and their mammalian hosts. We evaluated the influence of species abundance patterns on the distribution of specialization in these host–parasite interaction networks with the aid of null models. 3 In parallel with recent studies of plant–animal mutualistic networks, our analyses suggest that host–parasite interactions in these systems are highly asymmetric: specialist parasites tend to interact with hosts with high parasite richness, whereas hosts with low parasite richness tend to interact mainly with generalist parasites. 4 The observed distribution of specialization was predicted by a null model that assumed that species-specific probabilities of being assigned a link during the randomization process were roughly proportional to their relative abundance. Thus, abundant hosts tend to harbour richer parasite faunas, with a high proportion of rare specialists.

Importance of lake characteristics in structuring parasite communities of salmonids from insular Newfoundland

Metazoan parasites of Salmo salar and Salvelinus fontinalis were studied at eight sites in insular Newfoundland. The locations included water bodies of various sizes (<1, 1–100, and >100 ha) and depths (<1, 1–5, and >5 m). Nine of 14 parasite species were salmonid specialists and generally had wider geographic distributions than the remaining generalists, with one exception (Echinorhynchus lateralis). The distributions of Crepidostomum farionis, Sterliadochona ephemeridarum, and E. lateralis appeared to be facilitated by the widespread distribution of intermediate hosts. Larval digeneans (Apophallus imperator, Diplostomum sp., and Tetracotyle sp.) were typically associated with shallow medium-sized lakes. Species using limnetic copepods as intermediate hosts (Philonema agubernaculum, Eubothrium salvelini, and Diphyllobothrium sp.) were most often found in fishes inhabiting the deeper lakes. Small ponds had low parasite richness (R = 5); medium and large lakes had similar richness (R = 9–11). Jaccard's index and cluster analysis revealed that fishes in the small ponds and deep lakes had inherently different parasites from fishes of the shallow medium-sized lakes, the latter containing fishes parasitized by larval digeneans. Based on the study it was concluded that lake depth is a fundamental factor determining the structure of parasite communities in salmonids in insular Newfoundland.

Do birds use biological control against nest parasites?

Hippoboscid flies, also known as louse flies, are obligate blood-feeders ectoparasites of birds and mammals. By studying louse fly parasites of four Passeriformes species, Eurasian blackbird (Turdus merula), Eurasian blackcap (Sylvia atricapilla), common chaffinch (Fringilla coelebs) and European robin (Erithacus rubecula), with dissimilar time of colonization of Azores islands, we tested whether: (i) island host populations have lower parasite richness than the mainland one; (ii) island host populations undergo higher parasite prevalence, mean intensities and mean abundance than the mainland one; (iii) island parasite diversity are composed exclusively by specific parasites and (iv) parasite richness is positively correlated with the island area and proximity to the continent. For these purposes, 775 birds were sampled for presence of louse flies, by modified fumigation chamber method, from Azores Islands (São Miguel, Terceira and Flores) and Portugal mainland. Insular and mainland parasite assemblages were statistically compared. We record for the first time to Azores, Ornithomya fringillina and Icosta minor from Portugal mainland. Louse flies had highest prevalence and abundance from Azores Islands compared to those observed in mainland birds, especially blackbirds. The insular parasite diversity of Azores blackbirds, blackcaps and chaffinches was richer than the one observed in mainland population. None of the hippoboscid flies observed on the islands and mainland were host-specific. Thus, our findings provide an upgrade of parasite island syndromes knowledge, in the context of the ectoparasites, namely to the hippoboscid flies case.