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1.
Pathogens ; 11(6)2022 Jun 03.
Article in English | MEDLINE | ID: mdl-35745501

ABSTRACT

The emergence of cercariae from infected mollusks is considered one of the most important adaptive strategies for maintaining the trematode life cycle. Short transmission opportunities of cercariae are often compensated by periodic daily rhythms in the cercarial release. However, there are virtually no data on the cercarial emergence of bird schistosomes from freshwater ecosystems in northern latitudes. We investigated the daily cercarial emergence rhythms of the bird schistosome Trichobilharzia sp. "peregra" from the snail host Radix balthica in a subarctic lake under both natural and laboratory seasonal conditions. We demonstrated a circadian rhythm with the highest emergence during the morning hours, being seasonally independent of the photo- and thermo-period regimes of subarctic summer and autumn, as well as relatively high production of cercariae at low temperatures typical of northern environments. These patterns were consistent under both field and laboratory conditions. While light intensity triggered and prolonged cercarial emergence, the temperature had little effect on cercarial rhythms but regulated seasonal output rates. This suggests an adaptive strategy of bird schistosomes to compensate for the narrow transmission window. Our results fill a gap in our knowledge of the transmission dynamics and success of bird schistosomes under high latitude conditions that may serve as a basis for elucidating future potential risks and implementing control measures related to the spread of cercarial dermatitis due to global warming.

2.
Parasitology ; 149(4): 457-468, 2022 04.
Article in English | MEDLINE | ID: mdl-35331353

ABSTRACT

Cercarial activity and survival are crucial traits for the transmission of trematodes. Temperature is particularly important, as faster depletion of limited cercarial energy reserves occurs at high temperatures. Seasonal climate conditions in high latitude regions may be challenging to complete trematode life cycle during the 6-month ice-free period, but temperature effects on the activity and survival of freshwater cercariae have not been previously identified. After experimentally simulating natural subarctic conditions during warmer and colder months (13 and 6°C), a statistical approach identifying changes in the tendency of cercarial activity loss and mortality data was used to detect differences in three trematode genera, represented by four taxa (Diplostomum spp., Apatemon spp., small- and large-sized Plagiorchis spp.). A strong temperature-dependent response was identified in both activity loss and mortality in all taxa, with Diplostomum spp. cercariae showing the most gradual changes compared to other taxa. Furthermore, whilst activity loss and mortality dynamics could not be divided into 'fish- vs invertebrate-infecting cercariae' groups, the detected taxa-specific responses in relation to life-history traits indicate the swimming behaviour of cercariae and energy allocation among larvae individuals as the main drivers. Cercariae exploit the short transmission window that allows a stable continuance of trematodes' life cycles in high-latitude freshwater ecosystems.


Subject(s)
Ecosystem , Trematoda , Animals , Cercaria/physiology , Fresh Water , Temperature , Trematoda/physiology
3.
Pathogens ; 11(3)2022 Feb 24.
Article in English | MEDLINE | ID: mdl-35335614

ABSTRACT

Phenotypic polymorphism is a commonly observed phenomenon in nature, but extremely rare in free-living stages of parasites. We describe a unique case of somatic polymorphism in conspecific cercariae of the bird schistosome Trichobilharzia sp. "peregra", in which two morphs, conspicuously different in their size, were released from a single Radix balthica snail. A detailed morphometric analysis that included multiple morphological parameters taken from 105 live and formalin-fixed cercariae isolated from several naturally infected snails provided reliable evidence for a division of all cercariae into two size groups that contained either large or small individuals. Large morph (total body length of 1368 and 1339 µm for live and formalin-fixed samples, respectively) differed significantly nearly in all morphological characteristics compared to small cercariae (total body length of 976 and 898 µm for live and formalin samples, respectively), regardless of the fixation method. Furthermore, we observed that small individuals represent the normal/commonly occurring phenotype in snail populations. The probable causes and consequences of generating an alternative, much larger phenotype in the parasite infrapopulation are discussed in the context of transmission ecology as possible benefits and disadvantages facilitating or preventing the successful completion of the life cycle.

4.
J Anim Ecol ; 90(4): 978-988, 2021 04.
Article in English | MEDLINE | ID: mdl-33481253

ABSTRACT

Free-living parasite life stages may contribute substantially to ecosystem biomass and thus represent a significant source of energy flow when consumed by non-host organisms. However, ambient temperature and the predator's own infection status may modulate consumption rates towards parasite prey. We investigated the combined effects of temperature and predator infection status on the consumer functional response of three-spined sticklebacks towards the free-living cercariae stages of two common freshwater trematode parasites (Plagiorchis spp., Trichobilharzia franki). Our results revealed genera-specific functional responses and consumption rates towards each parasite prey: Type II for Plagiorchis spp. and Type III for T. franki, with an overall higher consumption rate on T. franki. Elevated temperature (13°C) increased the consumption rate on Plagiorchis spp. prey for sticklebacks with mild cestode infections (<5% fish body weight) only. High consumption of cercarial prey by sticklebacks may impact parasite population dynamics by severely reducing or even functionally eliminating free-living parasite life stages from the environment. This supports the potential role of fish as biocontrol agents for cercariae with similar dispersion strategies, in instances where functional response relationships have been established. Our study demonstrates how parasite consumption by non-host organisms may be shaped by traits inherent to parasite transmission and dispersal, and emphasises the need to consider free-living parasite life stages as integral energy resources in aquatic food webs.


Subject(s)
Cestode Infections , Smegmamorpha , Trematoda , Animals , Cercaria , Ecosystem , Host-Parasite Interactions
5.
Parasitol Res ; 119(12): 4271-4276, 2020 Dec.
Article in English | MEDLINE | ID: mdl-32845358

ABSTRACT

Direct consumption on free-living cercariae stages of trematodes by non-host organisms interferes with trematode transmission and leads to reduced infections in the next suitable hosts. Consumer functional responses provide a useful tool to examine relationships between consumption rates and ecologically relevant prey densities, whilst also accounting for abiotic factors that likely influence consumption rates. We investigated how temperature influences the consumer functional response of the amphipod Gammarus lacustris towards the cercariae of three freshwater trematodes (Diplostomum, Apatemon and Trichobilharzia). Amphipods displayed different functional responses towards the parasites, with Type II responses for Diplostomum and Type I responses for Apatemon prey. Temperature did not alter the consumption rate of the amphipod predator. Trichobilharzia was likely consumed at similar proportions as Diplostomum; however, this could not be fully evaluated due to low replication. Whilst Type II responses of invertebrate predators are common to various invertebrate prey types, this is the first time a non-filter feeding predator has been shown to exhibit Type I response towards cercarial prey. The prey-specific consumption patterns of amphipods were related to cercarial distribution in the water column rather than to the size of cercariae or temperature influence. The substantial energy flow into food webs by non-host consumer organisms highlights the importance of understanding the mechanisms that modulate functional responses and direct predation in the context of parasitic organisms.


Subject(s)
Amphipoda/physiology , Predatory Behavior/physiology , Trematoda/physiology , Animals , Cercaria/classification , Cercaria/growth & development , Cercaria/physiology , Food Chain , Predatory Behavior/classification , Species Specificity , Temperature , Trematoda/classification , Trematoda/growth & development , Trematode Infections/parasitology , Trematode Infections/transmission
6.
Parasitol Res ; 114(4): 1327-39, 2015 Apr.
Article in English | MEDLINE | ID: mdl-25630694

ABSTRACT

Co-introduction and colonization of parasites with the introduction of new host species into aquatic habitats may depend on the host specificity and dispersal capabilities of the parasites. We compared the metazoan parasite community of an introduced three-spined stickleback (Gasterosteus aculeatus) population with that of the nearby source population in subarctic Norway. As expected from a small spatial scale (5 km), the parasite component communities in the two lakes were highly similar. All identifiable allogenic parasite taxa (Diphyllobothrium dendriticum, Diphyllobothrium ditremum, Diphyllobothrium spp., Schistocephalus solidus, Apatemon sp. and Diplostomum spp.) were also observed in both lakes while inter-lake differences were driven by autogenic parasite taxa (Eubothrium spp., Crepidostomum spp., Nematoda spp., Proteocephalus sp. and Gyrodactylus arcuatus). Contrary to expectation, the total number of parasite taxa was higher in the introduced stickleback population (12) compared to that found in the source population (9) with three parasite taxa (Eubothrium spp., Crepidostomum spp., Nematoda spp.) only occurring in the introduced population. These parasites were uncommon however and normally restricted to salmonids. Sticklebacks from both populations were heavily infected, particularly with eye-infecting metacercariae. Sequences from the DNA barcode region of cytochrome oxidase 1 indicated that these include Diplostomum lineage 6, a member of the Diplostomum baeri complex and a member of the Strigeinae. Despite high similarity between the two component communities, quantitative inter-lake differences were found at the infracommunity level. At this scale, parasite intensity was significantly higher in the source population for the two autogenic stickleback specialists: G. arcuatus and Proteocephalus sp., assumed to be the autogenic stickleback specialist Proteocephalus filicollis. Parasite infracommunities within each lake also resembled each other significantly more than infracommunities between lakes, primarily driven by the allogenic cestode D. ditremum, as well as G. arcuatus and Proteocephalus sp. Overall, quantitative dissimilarities between the two parasite communities were possibly explained by inter-lake differences in the density of sticklebacks and intermediate hosts.


Subject(s)
Cestoda/physiology , Cestode Infections/veterinary , Fish Diseases/epidemiology , Smegmamorpha/parasitology , Trematoda/physiology , Trematode Infections/veterinary , Animals , Base Sequence , Cestoda/genetics , Cestode Infections/epidemiology , Cestode Infections/parasitology , Ecosystem , Female , Fish Diseases/parasitology , Lakes , Male , Molecular Sequence Data , Norway/epidemiology , Phylogeny , Population Dynamics , Sequence Analysis, DNA/veterinary , Species Specificity , Trematoda/genetics , Trematode Infections/epidemiology , Trematode Infections/parasitology
7.
Oecologia ; 171(4): 993-1002, 2013 Apr.
Article in English | MEDLINE | ID: mdl-23053223

ABSTRACT

Introduced species can alter the topology of food webs. For instance, an introduction can aid the arrival of free-living consumers using the new species as a resource, while new parasites may also arrive with the introduced species. Food-web responses to species additions can thus be far more complex than anticipated. In a subarctic pelagic food web with free-living and parasitic species, two fish species (arctic charr Salvelinus alpinus and three-spined stickleback Gasterosteus aculeatus) have known histories as deliberate introductions. The effects of these introductions on the food web were explored by comparing the current pelagic web with a heuristic reconstruction of the pre-introduction web. Extinctions caused by these introductions could not be evaluated by this approach. The introduced fish species have become important hubs in the trophic network, interacting with numerous parasites, predators and prey. In particular, five parasite species and four predatory bird species depend on the two introduced species as obligate trophic resources in the pelagic web and could therefore not have been present in the pre-introduction network. The presence of the two introduced fish species and the arrival of their associated parasites and predators increased biodiversity, mean trophic level, linkage density, and nestedness; altering both the network structure and functioning of the pelagic web. Parasites, in particular trophically transmitted species, had a prominent role in the network alterations that followed the introductions.


Subject(s)
Food Chain , Introduced Species , Models, Biological , Smegmamorpha/parasitology , Trout/parasitology , Animals , Birds/physiology , Body Weights and Measures , Lakes , Norway , Population Dynamics , Predatory Behavior/physiology , Smegmamorpha/physiology , Species Specificity , Trout/physiology
8.
J Parasitol ; 90(1): 1-7, 2004 Feb.
Article in English | MEDLINE | ID: mdl-15040660

ABSTRACT

Individual Arctic charr (Salvelinus alpinus) from Fjellfrøsvatn, northern Norway, could be categorized by their stomach contents as zooplanktivores or benthivores. Feeding specialization among these fish was evident from negative correlations between helminths transmitted by pelagic copepods (Diphyllobothrium dendriticum and D. ditremum) and those transmitted by the benthic amphipod Gammarus lacustris (Cystidicola farionis and Cyathocephalus truncatus). Occurrences of parasite species acquired from the same types of invertebrate were positively correlated in the fish. Strong relationships among habitat use, diet, and helminth infections among the Arctic charr indicated persistent foraging patterns involving long-term habitat use and feeding specialization. The distribution of all parasite species was highly aggregated in the fish samples, measured by the exponent k of the fitted negative binomial distributions (range: 0.5-7.5) and the variance-to-mean ratios (s2/mean, range: 5-85). Charr specializing on either copepods or Gammarus predominantly contributed to high-intensity class intervals within the overall frequency distributions of the corresponding parasite species. Such fish had low infection intensities of helminths transmitted by other prey organisms. The detailed analyses of the parasite frequency distributions for fish with different habitat or feeding preferences evidently show how heterogeneity in trophic behavior contributes strongly to the commonly observed aggregation of helminths among hosts under natural conditions.


Subject(s)
Disease Vectors/classification , Feeding Behavior/physiology , Fish Diseases/parasitology , Helminthiasis, Animal/transmission , Trout/parasitology , Amphipoda/parasitology , Animals , Copepoda/parasitology , Diphyllobothriasis/epidemiology , Diphyllobothriasis/transmission , Diphyllobothriasis/veterinary , Diphyllobothrium/isolation & purification , Fish Diseases/epidemiology , Fish Diseases/transmission , Fresh Water , Gastrointestinal Contents/parasitology , Helminthiasis, Animal/epidemiology , Helminthiasis, Animal/parasitology , Norway/epidemiology , Predatory Behavior , Spirurida Infections/epidemiology , Spirurida Infections/transmission , Spirurida Infections/veterinary , Spiruroidea/isolation & purification , Trout/physiology
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