The host-parasite association formed by anisakid parasites and their fish hosts: a model to investigate temporal changes in marine Arctic biodiversity and trophic webs

Motivation of the proposed research:
To detect "Changes in the marine Arctic ecosystem" is essential in responding to climate changes. 

This project proposes a comparative analysis of the genetic and infection data of anisakid parasites  through time, to detect temporal changes in marine Arctic biodiversity and trophic webs.
The transmission pathways of anisakid parasites are fully included in marine food webs, since their indirect life cycles involve crustaceans, fish, squids and marine mammals and require both stable marine trophic webs and constant host population size to be completed. Thus, ecosystem changes may have a big impact on the infection and genetic diversity fluctuations of the host-parasite system (Mattiucci & Nascetti, 2008; Zarlenga et al., 2014). Indeed, the genetic diversity of marine species is known to be a sensitive target of disturbance (i.e., genetic erosion; Pinsky and Palumbi, 2014; Pauls et al., 2013).
According to this rationale, we here proposed a multi-level approach to investigate the biodiversity of marine Arctic biota, based on the analysis of anisakid parasites. The availability of 25 years of previous data already hold by the Proposer is a way to detect temporal changes in the infection and the genetic diversity of the parasites and their hosts. Merging the different data obtained along time series will provide an indirect insight on Arctic food web stability.

The overall goal of the Project is to use the association anisakid parasites - fish host as an indicator of the "changes in the Arctic marine ecosystem".
Previous studies on a nisakid nematodes have shown that both their infection levels and genetic variability may be strongly affected by the population size of the hosts involved in parasites’ life cycle. The main objective of this project roots in this finding is investigate through time the variation of both the infection levels and the genetic variability inanisakids from the Arctic Region. This goal will be achievable by comparing parasites samples, genetic and parasitological data collected for over 25 years by the Responsible from the Arctic region, with new samples from this project.
The main impact of this research will be to test an  approach to ecosystem changes, by using anisakid parasites and their hosts as indicators of the state of Arctic trophic webs.
Since the time-series of data available for this area are among the most abundant, the results obtained would constitute a base for long-term ecological studies on Arctic biodiversity changes.

Abstract Publication no1. Global changes in the marine Arctic ecosystem affecting the demography of fish and seal populations may alter anisakid population sizes, potentially leading to genetic erosion in parasite gene pools. Contracaecum osculatum sp. B is a sibling species within the C. osculatum (s.l.) complex, parasitizing Arctic and sub-Arctic seals and fish. This study aimed to compare parasite genetic diversity across the Nordic Seas over a 35-year time scale. Historical specimens (1985–1986) from seals were compared with contemporary specimens (2021–2022) from fish in the same regions. Parasites were first identified through sequence analysis of mtDNA cox2 and ITS rDNA, followed by genotyping at seven newly developed SSRs nDNA loci. The population genetic structure of C. osculatum sp. B revealed the existence of two parasite subpopulations. This finding appears to be mostly influenced by the population structure of the seal hosts in the study area. High genetic variability was observed at both nuclear and mitochondrial levels. In the gene pool of the contemporary parasite population, some rare haplotypes in mtDNA cox2 and rare alleles at SSRs-DNA loci have been lost compared to the historical population, while novel unique alleles and haplotypes have simultaneously emerged. Overall, these findings seem suggest the occurrence of an initial decline in parasite population size, followed by a period of demographic stability and, more recently, a population increase. Similar demographic patterns have been documented in the host populations over the same time scale. Genetic polymorphisms in anisakids across temporal scales may help unravel and monitor trophic web dynamics in the Arctic marine ecosystem under global change.

Abstract Publication no2

Anisakid nematodes are widespread marine parasites with complex life cycles involving invertebrates and fish as intermediate or transport hosts, and marine mammals as definitive hosts. Despite their ecological importance, and the zoonotic potential associated with the larval stages found in fish, recent data on anisakid species diversity in pinnipeds from Norwegian waters remain scarce. In this study, we investigated anisakid infections in two juvenile harbour seals (Phoca vitulina) stranded along the southern coast of Norway. Gastrointestinal nematodes were collected, morphologically classified to the genus level, and subsequently identified to species level through molecular analyses of mitochondrial (mtDNA cox2) and nuclear (rDNA ITS) markers. Five anisakid species were identified: Contracaecum osculatum sp. A (reported here for the first time in harbour seals), C.
osculatum (sensu stricto), Phocanema decipiens (s.s.), P. krabbei, and Anisakis simplex (s.s.). The latter species was found in unexpectedly high abundance and in fully developed adult stages in one of the seals. Notably, these adult A. simplex (s.s.) exhibited large body size, in contrast with previous studies reporting either absence or minimal presence of adults in harbour seals. The underlying mechanisms promoting growth and reproductive development of A. simplex (s.s.) in this host species remain unclear, but may involve a combination of host-specific physiological traits, environmental factors, and parasite phenotypic plasticity. Gross pathological examination revealed multiple gastric and intestinal ulcers in the same seal, including seven crateriform lesions consistent with ulcerative gastritis and enteritis, associated with nematode attachment and feeding.
These findings expand the current knowledge on anisakid diversity in P. vitulina and provide novel evidence of its role as a definitive host for A. simplex (s.s.) in Norwegian coastal waters. Furthermore, the results suggest that competitive interactions among anisakid species, combined with ecological and physiological host factors, may facilitate the development and maturation of A. simplex (s.s.) in harbour seals. Further studies are warranted to assess the frequency and health implications of such infections in wild pinniped populations.

• Tesi di Dottorato in Ecologia e Gestione Sostenibile delle risorse Ambientali (maggio 2025), Dottoranda Dr. Beatrice Belli;
• Presentazione con una comunicazione orale al XXXIII Congresso della Società Italiana di Parassitologia (SOIPA), Padova, Giugno 2024, dal titolo: Genetic variability in the anisakid Contracaecum osculatum B over a temporal scale: a tool for monitoring the food webs in sub-Arctic Sea
• Presentazione con una comunicazione orale al XIV European Multicolloquium of Parasitology (Congresso delle Federazioni Europee di Parassitologia) EMOP 2024 (Polonia, Agosto 2024), dal titolo: Genetic variability in the anisakid Contracaecum osculatum B over a temporal scale: a tool for monitoring the food webs in sub-Arctic Sea?
• Presentazione dei primi risultati durante la Conferenza  (Poster)  Roma, CNR;

• Presentazione orale dei risultati febbraio 2024 Roma, CNR;

  PUBBLICAZIONI IN EXTENSO:

1. Beatrice Belli, Marialetizia Palomba, Veronica Rodriguez-Fernandez, Paolo Cipriani, Roberta Andolfi_, Lucilla Giulietti, Miguel Bao, Giuseppe Nascetti, Simonetta Mattiucci (2025) Genetic structure of the anisakid nematode Contracaecum osculatum sp. B over a temporal scale: a tool for monitoring trophic-web dynamics in Arctic Sea? Parasitology Research 2025  https://doi.org/10.1007/s00436-025-08561-6
2. Paolo Cipriani· Lucilla Giulietti · Marialetizia Palomba · Veronica Rodriguez Fernandez · Simonetta Mattiucci, Arne Bjørge· Arne Levsen · Miguel Bao (2025). Anisakid biodiversity in two young harbour seals (Phoca vitulina L.) from coastal South‑West Norway. Parasitology Research, 124:110
   https://doi.org/10.1007/s00436-025-08559-0.
3. Veronica Rodriguez-Fernandez, Marialetizia Palomba, Beatrice Belli, Paolo Cipriani· Miguel Bao, Kurt Buchmann, Giuseppe Nascetti, Simonetta Mattiucci.  Cross-utility of microsatellite DNA-loci in  the species of the Contracaecum osculatum (s.l.) complex: estimating genetic variability in Arctic and Antarctic endoparasite species (In preparation, to be submitted)