# Diversity of helminths parasitising North-East Atlantic and Antarctic seabirds

M Musiol, D Grabner, D Díaz-Morales, M Nachev, S Descamps, Frederic

Fonteneau, Bernd Sures, A Carravieri

► To cite this version:

M Musiol, D Grabner, D Díaz-Morales, M Nachev, S Descamps, et al. Diversity of helminths par-asitising North-East Atlantic and Antarctic seabirds. Journal of Helminthology, 2026, 100, pp.e22. 10.1017/s0022149x26101163. hal-05535259

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Research Paper

**Cite this article:** Musiol M, Grabner D, Diaz-Morales D, Nachev M, Descamps S, Fonteneau F, Sures B and Carravier A (2026). Diversity of helminths parasitising North-East Atlantic and Antarctic seabirds. *Journal of Helminthology*, **100**, e22, 1–10

https://doi.org/10.1017/S0022149X26101163

Received: 19 November 2025

Revised: 09 January 2026

Accepted: 11 January 2026

**Keywords:**

Parasites; feeding ecology; life strategy; life cycle; transmission

**Corresponding author:**

Bernd Sures;

Email: bernd.sures@uni-due.de

# Diversity of helminths parasitising North-East Atlantic and Antarctic seabirds

M. Musiol<fnref n="1" />,²,§ ID, D. Grabner<fnref n="1" />,²,§ ID, D. Díaz-Morales<fnref n="1" />,³ ID, M. Nachev<fnref n="1" />,²,

S. Descamps⁴ ID, Frederic Fonteneau⁵, B. Sures<fnref n="1" />,²,<fnref n="6" /> ID and A. Carravier⁷,⁸ ID

**Abstract**

Seabirds are largely used as indicators of Ocean health and are final hosts of several helminth parasites. However, the helminth fauna of seabirds is still poorly studied. Here, we quantified the diversity of gastrointestinal parasites in 52 individuals belonging to 10 seabird species with different habitat preferences and feeding strategies from the North-East Atlantic and Antarctica. Fresh carcasses were collected in Northern France and at Svarthamaren (Dronning Maud Land, Antarctica), helminth parasites were extracted from the gastrointestinal tract, and were identified by morphological inspection and DNA barcoding. In total, we identified 13 helminth taxa. North-East Atlantic seabirds hosted parasites from four helminth groups (Acanthocephala, Cestoda, Nematoda, Trematoda), while Antarctic seabirds hosted Acanthocephala and Cestoda only. The largest parasite diversity was found in northern fulmars *Fulmarus glacialis* (9 species), European shags *Gulosus aristotelis* (5 species), razorbills *Alca torda* (4 species), and black-legged Kittiwakes *Rissa tridactyla* (4 species). Co-infections with multiple parasite species in single hosts were common. Oceanic diving species were found to be the most parasite-poor, with common guillemots *Uria aalge* and Atlantic puffins *Fratercula arctica* hosting no parasites. In contrast, oceanic surface-feeding seabirds had a large parasite diversity, which notably included trematodes, and was comparable to that of coastal species. To the best of our knowledge, this study identified 9 new host-parasite associations: *Andracantha* sp. in northern fulmars and south polar skuas *Stercorarius maccormicki*, *C. septentrionale* in northern fulmars and black-legged Kittiwakes, a species of Microphallidae in black-legged Kittiwakes, *Cardiocephaloides longicollis* in European shags, *Cryptocotyle lingua* in Sandwich terns *Thalasseus sandvicensis*, and a clophyl-lidean species in south polar skuas and Antarctic petrels *Thalassioica antarctica*.

**Introduction**

Seabirds rely extensively on the marine environment for their life cycle and play an important role in marine food webs (Piatt and Sydeman 2007; Votier and Sherley 2017). Seabirds integrate processes occurring at lower trophic levels and are easy to observe when compared to other marine organisms. As such, seabirds are broadly used as indicators of ocean functioning and ocean health, notably in ecotoxicology, food web ecology, and conservation and fisheries sciences (Furness and Camphuysen 1997; Piatt and Sydeman 2007). As meso- to top predators with diverse diets, and the ability to migrate over distances ranging from short to intercontinental, seabirds are likely to encounter and disperse a wide range of trophically transmitted parasites from a variety of geographic regions (Gutiérrez *et al.* 2017; Mendes *et al.* 2013). However, there is a major knowledge gap on the parasite fauna of seabirds, notably for endoparasites such as helminths, which are mainly trophically transmitted and can disrupt host metabolism, fertility, and survival (Khan *et al.* 2019). These parasites are difficult to sample or observe with non-invasive techniques, thereby limiting their investigation in seabirds, which are one of the most endangered groups of birds globally (Dias *et al.* 2019). Moreover, the scarcity of available DNA sequences of seabird helminths (non-economically or medically relevant parasites are generally poorly represented in GenBank, Hupalo *et al.* (2025)), as well as the intermittent excretion of helminth eggs or debris in faeces (Granroth-Wilding *et al.* 2017), limits our capacity to rely solely on molecular non-invasive techniques to identify them. As such, necropsies of birds that died naturally are an essential step in the direct sampling and description of seabird helminth communities (e.g., Granroth-Wilding *et al.* 2017; Mallory *et al.* 2007; Provencher *et al.* 2014).

In the present study, we document the infection of ten seabird species from the North-East Atlantic and Antarctica with gastrointestinal helminths. Our aim was to assess the helminth

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CAMBRIDGE
UNIVERSITY PRESS

<footnote n="6">⁶Shared first author</footnote>

<footnote n="1">¹Department of Aquatic Ecology and Centre of Water and Environmental Research (ZWU), University Duisburg-Essen, Essen, Germany; ²Research Center One Health Ruhr, Research Alliance Ruhr, University Duisburg-Essen, Essen, Germany; ³Biological Sciences Department, DePaul University, Chicago, USA; ⁴Norwegian Polar Institute, Fram Centre, Tromsø, Norway; ⁵² Les Bertais, 35490 Sens-de-Bretagne, France; ⁶Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa; ⁷Centre d'Etudes Biologiques de Chizé (CEBC) UMR 7372 CNRS-La Rochelle Université, Villiers-en-bois, France and ⁸Littoral, Environnement et Sociétés (LIENSs) UMR 7266 CNRS-La Rochelle Université, La Rochelle, France</footnote>

<footnote>© The Author(s), 2026. Published by Cambridge University Press. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.</footnote>
diversity in different seabird host species and the association with host ecological characteristics (habitat preference, feeding strategies, and condition). We expected a higher diversity of helminths in coastal- than in oceanic-feeding seabirds, because several helminths rely on terrestrial, shoreline, and shallow water intermediate hosts to complete their life-cycle (Hoberg 1996). We also expected potentially different infection levels in bycatch birds in good condition compared to stranded individuals that died due to a variety of causes. Given the heterogeneous nature of our opportunistic sampling and the partly low sample sizes, the results are interpreted with regard to the study's limitations. Nevertheless, despite its exploratory character, this study provides valuable baseline information on the largely understudied helminth fauna of seabirds. The data presented here can serve as a reference point for future investigations, particularly in the context of ongoing environmental change. As shifting climatic and ecological conditions are likely to affect parasite distribution, transmission dynamics, and infection levels, establishing such baseline knowledge is crucial for tracking temporal trends and assessing future impacts on seabird populations and marine ecosystems.

## Material and methods

### Sample collection

Two sets of fresh carcasses were used in this study. The first set ('stranded birds') included 38 individual North-East Atlantic seabirds belonging to eight species (Atlantic puffins *Fratercula arctica*, common guillemots *Uria aalge*, razorbills *Alca torda*, European shags *Gulosus aristotelis*, black-legged Kittiwakes *Rissa tridactyla*,

common gulls *Larus canus*, sandwich terns *Thalasseus sandvicensis*, and northern fulmars *Fulmarus glacialis*) that were collected by wildlife rescue centres between 2010 and 2018 in coastal areas of north-western France, and three individuals belonging to 2 Antarctic species (south polar skua *Stercorarius maccormicki* and Antarctic petrel *Thalassioica antarctica*) collected at Svarthamaren, Dronning Maud Land (Antarctica) in 2022. The cause of death of the first set of carcasses was unknown in several cases (52%), while known causes included starvation due to winter storms (18%), oil pollution (15%), and others (collisions with objects, bycatch, 15%). Most North-East Atlantic birds were adults and were found during the nonbreeding period from September to March (boreal autumn-winter). All European shags were juveniles (post-fledging chicks), and a few individuals of other species were juveniles or immatures (3/5 Atlantic puffins, 1/4 common gulls, 1/11 razorbills, 1/5 sandwich terns). The Antarctic birds were all adults and were collected during the breeding period in January (austral summer). The second set of carcasses ('bycatch birds') included five adult common guillemots and five adult razorbills from a single bycatch event. These birds were entangled in a single fishing net that ended up on a beach in northern France in December 2018. These wintering individuals were in very good condition and presumably healthy. The 'bycatch' common guillemots and razorbills were compared to 'stranded birds' of the same species to test potential differences in infection levels between birds in good and bad condition, respectively. The total number of sampled individuals was 52 and all species and their feeding ecology are presented in Table 1. Carcasses from North-East Atlantic seabirds were stored at -20°C until dissections at the Centre d'Etudes Biologiques de Chizé (CEBC), France (stranded

<table><caption>**Table 1.** Bird species investigated including preferred habitat and feeding strategy, food source, and intensities of parasite infections. Intensity was quantified only for higher-level taxonomic groups of helminths (Acanthocephala, Cestoda, Nematoda, Trematoda). When possible, the number of cestode scolices was quantified</caption><thead><tr><th rowspan="2">Species</th><th rowspan="2">Habitat</th><th rowspan="2">Primary (secondary) prey</th><th colspan="4">Infection intensity</th></tr><tr><th>Acanthocephala</th><th>Cestoda</th><th>Nematoda</th><th>Trematoda</th></tr></thead><tbody><tr><td>Atlantic puffin<br>(n = 5)<br><i>Fratercula arctica</i></td><td>Oceanic diving</td><td>Fish (crustaceans)<sup>1,2,3</sup></td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Common<br>guillemot<br>(n = 5<br>stranded birds)<br><i>Uria aalge</i></td><td>Oceanic diving</td><td>Fish (crustaceans)<sup>2,4</sup></td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Common<br>guillemot<br>(n = 5<br>bycatch birds)<br><i>Uria aalge</i></td><td>Oceanic diving</td><td>Fish (crustaceans)<sup>2,4</sup></td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Razorbill<br>(n = 6<br>stranded birds)<br><i>Alca torda</i></td><td>Oceanic diving</td><td>Fish (crustaceans)<sup>2,3</sup></td><td>0</td><td>0</td><td>3-17 nematodes<br>S; 2<br>nematodes,<br>L.i.</td><td>0</td></tr><tr><td>Razorbill<br>(n = 5<br>bycatch birds)<br><i>Alca torda</i></td><td>Oceanic diving</td><td>Fish (crustaceans)<sup>2,3</sup></td><td>0</td><td>0</td><td>3 nematodes S;</td><td>0</td></tr><tr><td>Black-legged<br>kittiwake<br>(n = 4)<br><i>Rissa tridactyla</i></td><td>Oceanic surface-<br>feeding</td><td>Fish (polychaete worms,<br>crustaceans)<sup>5,6,7</sup></td><td>0</td><td>2-3 scolices,<br>S.i.</td><td>1 nematode, S.i.</td><td>15 <i>Cryptocotyle</i>, S.<br>i.; 4<br>Microphallidae,<br>S.i.</td></tr><tr><td>Northern fulmar<br>(n = 5)<br><i>Fulmarus glacialis</i></td><td>Oceanic surface-<br>feeding</td><td>Fish, fishery discards<br>(crustaceans,<br>cephalopods)<sup>8,9</sup></td><td>1 acanth., S.i.</td><td>1-20 scolices,<br>S.i.</td><td>1-60<br>nematodes,<br>S.i.</td><td>3-5 <i>Cryptocotyle</i>,<br>S.i.; 1<br><i>Cryptocotyle</i>, L.i.</td></tr><tr><td>Common gull<br>(n = 4)<br><i>Larus canus</i></td><td>Coastal generalist</td><td>Bivalves, polychaetes, fish,<br>fishery discards (insects,<br>earthworms)<sup>10,11</sup></td><td>0</td><td>Only<br>fragments,<br>S.i.</td><td>0</td><td>2-65 Himastlidae,<br>S.i.; 16<br>Himastlidae, L.i.</td></tr></tbody></table>

(Continued)
<table><caption>**Table 1.** (Continued)</caption><thead><tr><th rowspan="2">Species</th><th rowspan="2">Habitat</th><th rowspan="2">Primary (secondary) prey</th><th colspan="4">Infection intensity</th></tr><tr><th>Acanthocephala</th><th>Cestoda</th><th>Nematoda</th><th>Trematoda</th></tr></thead><tbody><tr><td>Sandwich tern<br>(n = 5)<br><i>Thalasseus sandvicensis</i></td><td>Coastal surface-<br>feeding</td><td>Fish (annelids, invertebrates)<sup>12</sup></td><td>0</td><td>0</td><td>0</td><td>12 <i>Cryptocotyle</i>,<br>S.i.</td></tr><tr><td>European shag<br>(n = 5)<br><i>Gulosus aristotelis</i></td><td>Coastal diving</td><td>Fish (crustaceans, annelids)<sup>13,14</sup></td><td>3–60 acanth., S.<br>i.; 1–52<br>acanth., L.i.</td><td>0</td><td>50–154<br>nematodes,<br>S.; 2 L.i.</td><td>0</td></tr><tr><td>South polar skua<br>(n = 2)<br><i>Stercorarius maccormicki</i></td><td>Oceanic<br>(nonbreeding),<br>terrestrial<br>(breeding)</td><td>Other birds and eggs<br>(breeding)<sup>15,16</sup>; Fish,<br>crustaceans (nonbreeding)<sup>17</sup></td><td>&gt;20 acanth., S.i.</td><td>1 scolex, S.i.</td><td>0</td><td>0</td></tr><tr><td>Antarctic petrel<br>(n = 1)<br><i>Thalassioica antarctica</i></td><td>Oceanic surface-<br>feeding</td><td>Crustaceans (fish,<br>cephalopods)<sup>18,19</sup></td><td>0</td><td>35 scolices,<br>S.i.</td><td>0</td><td>0</td></tr></tbody></table>

Abbreviations: L.i., Large intestine; S, stomach; S.i., small intestine.

References for diet (for Northern Hemisphere species, studies in the North-East Atlantic were prioritised): ¹Fayet et al. (2021); ²St. John Glew et al. (2018); ³St. John Glew et al. (2019); ⁴Anderson et al. (2014); ⁵Lewis et al. (2001); ⁶Markones et al. (2009); ⁷Lemesle et al. (2024); ⁸Ojowski et al. (2001); ⁹Darby et al. (2021, 2023); ¹⁰Kubetzki et al. (1999); ¹¹Kubetzki and Garthe (2003); ¹²Courtens et al. (2017); ¹³Michelot et al. (2017); ¹⁴Howells et al. (2018); ¹⁵Alfaro Garcia et al. (2022); ¹⁶Brooke et al. (1999); ¹⁷Weimerskirch et al. (2015); ¹⁸Descamps et al. (2016); ¹⁹Lorensen et al. (1998).

birds), or at the Littoral Environnement et Sociétés (LIENSs), France (bycatch birds), in 2022. Carcasses from stranded Antarctic individuals were dissected on site in 2022, with digestive tracts being isolated and stored at -20°C until extraction of parasites at the CEBC or at the University of Duisburg-Essen, Germany, in 2022.

## Extraction and identification of parasites from the gastrointestinal tract

Dissections were carried out using ethanol-sterilised instruments, beginning while the carcasses were still partially frozen. The digestive tract was separated from the carcass by ligaturing and transversally cutting the ends of the oesophagus and cloaca. Thereafter, different sections of the digestive tract were obtained: stomach, small intestine, and large intestine. The small and large intestines were then subdivided into three to 5 sections, with the number of sections varying depending on the species and the length of the intestine. The stomach and intestinal sections were cut open longitudinally and searched for parasites under a stereo-microscope (Leica MS5). Subsequently, the intestinal sections were washed in a beaker with a 400–500 mL physiological solution (0.9% NaCl). The contents of the beaker were then successively filtered using two filters (630 µm, 63 µm). The sieve residue of both filters was washed further with the physiological solution and then examined under the stereo-microscope. The parasites were extracted with tweezers and transferred to Petri dishes containing physiological solutions. For each bird host, the parasites were sorted according to the following taxonomic groups: acanthocephalans, cestodes, nematodes, and trematodes. Residual host digestive content was removed from the parasites by rinsing them several times with physiological solution. For molecular identification, parasites were washed twice in Milli-Q water to remove excess debris and salt residues. Thereafter, the parasites were transferred to a dish containing 70% ethanol, followed by full fixation in 99% ethanol.

Morphological and molecular identification of parasites was carried out at the laboratory of the Aquatic Ecology department at the University of Duisburg-Essen, Germany. For the morphological identification, parasites were first photographed under a stereo-

microscope (Olympus SZ51) equipped with a Moticam 2300, and with a light microscope (Olympus BX51), and then identified to the lowest taxonomic level possible based on the relevant literature (Hoberg & Soudachanh 2020; Munro et al. 1995; Nagasawa et al. 1998; Rocka 2019). As the examined bird carcasses varied in their degree of preservation due to extended storage at -20°C, morphological identification at high taxonomic resolution was not always possible. For example, parasites in poor condition (e.g., small fragments or heavily degraded specimens) were excluded from morphological identification. Therefore, molecular identification using DNA barcoding was considered a more reliable approach for taxonomic identification. As amplification success as well as representation in GenBank can differ for the parasite taxa investigated, different primer pairs were used to amplify partial sequences of the internal transcribed spacer (ITS), cytochrome oxidase I (COI), and the 18S rRNA and 28S rRNA gene, via polymerase chain reaction (PCR) (for primer sequences and references as well as the respective PCR conditions see Supplementary Table S1). The parasite samples were homogenized in 1.5-mL reaction tubes with 600 µL TNES buffer (Tris, NaCl, EDTA, SDS) using a micropestle (Eppendorf), and the DNA extraction was performed with a salt precipitation according to Grabner et al. (2015). Amplification with the primer pairs was carried out in a 20 µL reaction volume containing 10 µL Accustart II PCR ToughMix with 0.35 µL loading dye (Quantabio), 0.5 µmol of each primer, and 1 µL DNA. The mixture was then brought to a volume of 20 µL with distilled water. The PCR protocols for each primer pair are listed in Supplementary Table S1. The positive PCR products were combined with 10 µL ultra-pure water, and 12 µL of each sample was sent for Sanger sequencing using the respective forward and reverse primers (Microsynth Seqlab, Germany). The obtained sequences were assigned to the lowest possible taxonomic level using BLAST search (https://blast.ncbi.nlm.nih.gov/Blast.cgi). The sequences were edited, and alignments were created in GENEIOUS (version 2022.0.2, Biomatters Ltd., Auckland, New Zealand).

## Data analysis

Parasite prevalence was calculated for each parasite taxon according to Bush et al. (1997). In order to evaluate the similarity in
parasite species composition between host species, the Sørensen
similarity index was considered, with bird species grouped accord-
ing to their habitat and feeding strategy as follows: oceanic/diving:
Atlantic puffin, Common guillemot, Razorbill; oceanic/surface:
Black-legged Kittiwake, Northern fulmar; Coastal: Common gull,
Sandwich tern, European shag. Antarctic species were excluded
from this analysis because of the small sample size and different
ecological context.

**Results**

Molecular data in combination with morphological features were
used to confirm the assignment to a particular parasite taxon. While
non-economically or medically important parasites are generally
underrepresented in GenBank (Hupało *et al.* 2025), there is also a
big difference among the gene regions that are used for barcoding.
While 18S and 28S rRNA sequences are comparatively well repre-
sented, they mostly allow distinction of isolates only at higher
taxonomic levels. In turn, ITS or COI allow distinction down to
the species level (e.g., *Contracaecum* sp.), but hardly any parasite
sequences are available. The primer pair/gene region that provided
the best classification, as well as the related GenBank accession
numbers, is shown in *Supplementary Table S2*. Only in a few cases,
no sequence result was obtained, and identification in these cases
was based purely on morphology (*Supplementary Table S2*).

A total of 52 individual seabirds belonging to 10 species were
examined. Parasite load of acanthocephalans was highest in
European shags, and most cestode scolices were retrieved from
northern fulmars (Table 1). European shags and northern fulmars
were also most heavily infected with nematodes, while trematode
loads were highest in common gulls (Table 1). Overall parasite
prevalence ranged from zero in Atlantic puffins and common
guillemots up to 80% in European shags (Table 2; prevalence
reached 100% in Antarctic petrels but this was based on a single
individual host). In total, we identified 13 helminth taxa including
1 acanthocephalan of the genus *Andracantha* (likely two species
due to sequence divergence of 2.8% for 28S rRNA in a sequence of
911 bp and 15.2% for COI in a sequence of 424 bp), 2 cestodes
(Cyclophyllidea, and potentially 5 *Tetrabothrius* spp. based on
divergence of 2.3–5.1% in a 1,037 bp 18S rRNA sequence), 6 nema-
todes (*Anisakis* sp., *Contracaecum* *rudolphii* and *C. septentrionale*,
*Cosmocephalus* sp., *Stegophorus* sp., and three isolates of Spirurina
based on divergence of 11.9–22.2% for COI in a sequence of
433 bp), and 4 trematode isolates (*Cardiocephaloides longicollis*,
*Cryptocotyle lingua*, Himasthliidae, and Microphallidae) (Table 2).
The largest diversity of parasite species was identified in northern
fulmars (9 species), European shags (5 species), razorbills
(4 species), and black-legged Kittiwakes (4 species) (Table 2). *Tetra-
bothrius* sp. and *C. septentrionale* were found in most host species
(n = 4), and no parasite taxon was present in all infected birds
(Table 2). Co-infections with multiple parasite species in one host
individual were common. The largest number of 5 parasite species
was found in 1 northern fulmar, while co-infections with 2 parasite
species were the most common overall (7 cases). Single infections
were found in 5 birds, 2 parasite species in 8, 3 parasite species in 4,
and 4 parasite species in 2 (Table 2). Only *Anisakis* sp. nematodes
and microphallid trematodes were found in single host species, the
northern fulmar and the black-legged Kittiwake, respectively.
Among North-East Atlantic seabirds, all four parasite groups were
found in both coastal and oceanic surface-feeding birds (Table 3).
Razorbills were infected exclusively by nematodes, while Sandwich

terns were infected with a single trematode species (*Cryptocotyle lingua*). Antarctic species were dominated by acanthocephalans and cestodes (Table 2).

Among North-East Atlantic seabirds, the oceanic diving species were found to be the most parasite-poor in our study, both in terms of diversity (only nematodes) and number of infected bird species, i.e., only one (razorbills), while Atlantic puffins and common guillemots did not have any parasites (Table 3). Although the number of samples was limited, a pattern emerged with respect to habitat-related feeding preferences of bird species. The highest faunistic similarity in parasite species composition (Sørensen's index = 0.66) was observed between the oceanic surface-feeding and coastal birds. In contrast, both groups showed markedly lower similarity to bird species feeding in the water column (oceanic divers), with Sørensen's index values of 0.42 for the oceanic surface-feeding group and 0.33 for the coastal group. Due to the limited sample size of Antarctic bird species, they were excluded from the analysis.

A comparison of the parasites found in stranded and bycatch
birds revealed a similar diversity. Specifically, no parasites were
observed in either the stranded or bycatch individuals of the
common guillemot. Among razorbills, two stranded birds (ID4
and ID6) and two bycatch birds (ID7 and ID9) hosted parasites
of the species *Contracaecum septentrionale* (Table 2). One of the
stranded razorbills (ID4) was also infected with three other species
of nematodes (Table 2).

**Discussion**

The present study is one of the few to examine helminth occurrence
in seabird hosts, especially in such a large number of seabird species
simultaneously (n = 10), with different habitat preferences and
feeding strategies, from both the North-East Atlantic and Antarc-
tica. A total of 13 parasite taxa were identified, which most likely
comprise more species, as genetic determination was not always
possible down to the species level. To the best of our knowledge, this
study is the first record of *Andracantha* sp. in northern fulmars and
south polar skuas, of *C. septentrionale* in northern fulmars and
black-legged Kittiwakes, of a species of Microphallidae in black-
legged Kittiwakes, of *Cardiocephaloides longicollis* in European
shags, of *Cryptocotyle lingua* in Sandwich terns, and of a cyclophyl-
lidean species in south polar skuas and Antarctic petrels. Given the
limited number of individuals examined for each seabird species
(n between 1 and 6), we focus on the comparison of the parasite
diversity between the studied species and the literature, without
considering infection intensities, and provide a qualitative assess-
ment of parasite diversity variation depending on host feeding
strategy and habitat. Table 4 gives an overview of the available life
cycle parameters of the parasites detected in the present study.

Helminth diversity

Acanthocephala

Acanthocephalans of the genus *Andracantha* could be identified,
with divergence of 28S rRNA and COI indicating the presence of at
least two species. Due to a lack of matching sequences, these isolates
could not be compared to existing molecular phylogenies (e.g.,
Garcia-Varela *et al.* 2023). The genus *Andracantha* is common in
species of the family Phalacrocoracidae (cormorant and shag spe-
cies), Gaviidae (loon species), and in some penguins (Spheniscidae),
but several species have also been described in other aquatic birds
<table><caption>**Table 2.** Parasites detected and their prevalence in ten seabird species from the North-East Atlantic and Antarctica. The identity (ID) of the infected individuals is shown to illustrate co-infections. 'Types' for *Andracantha*, *Tetrabothrius*, and *Spirurina* denote different sequence isolates that are likely indicating different species. Cyclophyllidea were also likely 5–6 different species according to sequences, but as isolates were obtained from different primer pairs, direct comparison was not possible (see Supplementary Table S2). Individuals underlined were identified based on morphology only, as no usable sequence was retrieved</caption><thead><tr><th rowspan="2">Host species</th><th colspan="2">Acantho-cephala</th><th colspan="3">Cestoda</th><th colspan="3">Nematoda</th><th colspan="4">Trematoda</th></tr><tr><th>Andra-cantha sp. (Types A, B)*</th><th>Cyclo-phyllidea</th><th>Tetra-bothrius spp. (Types A, B, C, D, E)*</th><th>Anisakis sp.</th><th>Contra-caecum rudolphii</th><th>Contra-caecum septentrionale</th><th>Cosmo-cephalus sp.</th><th>Spirurina (Types A, B, C)*</th><th>Stego-phorus sp.</th><th>Cardio-cephaloides longicollis</th><th>Crypto-cotyle lingua</th><th>Himasth-lidae</th><th>Micro-phallidae</th></tr></thead><tbody><tr><td>Atlantic puffin (n = 5)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Common guillemot (n = 5 stranded birds)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Common guillemot (n = 5 bycatch birds)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Razorbill (n = 6 stranded birds)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>ID4, ID6, (33%)</td><td>ID4 (16%)</td><td>ID4 (16%) Type B</td><td>ID4 (16%)</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Razorbill (n = 5 bycatch birds)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>ID7, ID9 (40%)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Black-legged Kittiwake (n = 4)</td><td>0</td><td>0</td><td>ID1, ID4 (50%) Type C</td><td>0</td><td>0</td><td>ID2 (25%)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>ID4 (25%)</td><td>0</td><td>ID1 (25%);</td></tr><tr><td>Northern fulmar (n = 5)</td><td>ID1 (20%) Type A</td><td>ID1, ID3 (40%)</td><td>ID1, ID3, (40%) Type A, B</td><td>ID2, ID4 (40%)</td><td>0</td><td>ID4 (20%)</td><td>0</td><td>ID2, ID4 (40%) Type C</td><td>ID2, ID4 (40%)</td><td>0</td><td>ID1, ID2 (40%)</td><td>ID2 (20%)</td><td>0</td></tr><tr><td>Common gull (n = 4)</td><td>0</td><td>ID3, ID4 (50%)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>ID3, ID4 (50%)</td><td>0</td></tr><tr><td>Sandwich tern (n = 5)</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>ID5 (20%)</td><td>0</td><td>0</td></tr><tr><td>European shag (n = 5)</td><td>ID2, ID3, ID4, ID5 (80%) Type A</td><td>0</td><td>0</td><td>0</td><td>ID2, ID3, ID4, ID5 (80%)</td><td>ID2 (20%)</td><td>0</td><td>ID3 (20%) Type A</td><td>0</td><td>ID5 (20%)</td><td>0</td><td>0</td><td>0</td></tr><tr><td>South polar skua (n = 2)</td><td>ID1 (50%) Type B</td><td>ID2 (50%)</td><td>ID2 (50%) Type D</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr><tr><td>Antarctic petrel (n = 1)</td><td>0</td><td>ID1 (100%) Type E</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td><td>0</td></tr></tbody></table>
<table><caption>**Table 3.** Number of seabird species infected with the respective parasite group according to habitat preference for North-East Atlantic seabirds</caption><thead><tr><th></th><th>Acanthocephala</th><th>Cestoda</th><th>Nematoda</th><th>Trematoda</th></tr></thead><tbody><tr><td>Oceanic diving (3 spp.)</td><td>0</td><td>0</td><td>1</td><td>0</td></tr><tr><td>Oceanic surface (2 spp.)</td><td>1</td><td>2</td><td>2</td><td>2</td></tr><tr><td>Coastal (3 spp.)</td><td>1</td><td>1</td><td>1</td><td>2</td></tr></tbody></table>

(Bennett et al. 2023; Garcia-Varela et al. 2009; 2023; Presswell et al. 2018). To the best of our knowledge, we present the first record of *Andracatha* sp. in northern fulmars. The type found in northern fulmars was the same as the one infesting European shags in our sample ('type A'). European shags were previously found to be infected with *Andracantha tunitae* (Munro et al. 1995). This is also the first record of *Andracantha* sp. ('type B') in south polar skuas, or in any skua species, to the best of our knowledge. However, the molecular sequences obtained showed insufficient discriminatory power between the *Andracantha* species, so it cannot be determined with certainty whether type A represents *A. tunitae* or another *Andracantha* species.

### Cestoda

Both cestode groups found (the cyclophyllidean species and *Tetrabothrius* spp.) are common in seabirds with a number of known species (e.g., Barbosa & Palacios 2009; Hoberg 1996; Hoberg and Soudachanh 2020; Rocka 2019; Schwantes 2023). Again, divergence of the obtained 18S rRNA/COI sequence sections indicates the presence of different species of both groups, but the lack of reference sequences in GenBank prevented a more precise identification. *Tetrabothrius* sp. were found in four seabird species, including both Antarctic seabirds (each hosting a different species 'type'). Interestingly, two *Tetrabothrius* sp. individuals, each sampled from a different northern fulmar, had different morphological characteristics, indicating that at least 2 different species of *Tetrabothrius* infected northern fulmars. In a previous study, *Tetrabothrius minor* was the most prevalent species in northern fulmars (Kuklin et al. 2019), suggesting it as a potential candidate for the species recorded here. South polar skuas were previously found to be infected with *Tetrabothrius* (*Culmenamniculus*) *cylindraceus* at the South Shetlands Islands (Rocka 2019). Antarctic petrels were also already found to host four species of *Tetrabothrius*, although their identification is not available (Jones 1988). In contrast, Cyclophyllidae cestodes were not previously described in the 2 Antarctic species targeted, being more common in subarctic birds feeding in terrestrial/coastal environments (kelp gull *Larus dominicanus*, Snowy sheathbill *Chionis alba*, Barbosa and Palacios 2009).

### Nematoda

The most common nematode taxa found belonged to the genus *Contracaecum*, with *Contracaecum rudolphii* reaching the highest intensities in European shags. Both *C. rudolphii* and *C. septentrionale* have previously been recorded in European shags (Abollo et al. 2005). *C. septentrionale* was found to be less abundant than *C. rudolphii* both in the study of Abollo et al. (2005) and in the present study. Similar to our study, *C. septentrionale* was found previously in razorbills (Li et al. 2005), while it was, to our

<table><caption>**Table 4.** Information on life cycles of the parasites encountered in the present study in seabirds</caption><thead><tr><th>Parasite</th><th>Intermediate host(s)</th><th>Final host</th><th>References</th></tr></thead><tbody><tr><td colspan="4"><strong>Acanthocephala</strong></td></tr><tr><td>Andracantha sp.</td><td>Amphipods, transmitted by paratenic fish hosts</td><td>Seabirds</td><td>Garcia-Varela et al. (2009)</td></tr><tr><td colspan="4"><strong>Cestoda</strong></td></tr><tr><td>Tetrabothrius sp.</td><td>Poorly known, probably crustaceans, fish or cephalopods, pot. Arctic cod for Arctic species</td><td>Piscivorous birds, marine mammals</td><td>Kuklin and Kuklina (2022); Rocka (2019)</td></tr><tr><td>Cyclophyllidea (e.g., Dilepididae, Hymenolepididae in seabirds)</td><td>Mostly crustaceans as intermediate host</td><td>Variety of vertebrate hosts; commonly found in seabirds</td><td>Schwantes (2023)</td></tr><tr><td colspan="4"><strong>Trematoda</strong></td></tr><tr><td>Cardiocephaloides longicollis</td><td>2nd fish (often cultured gilthead seabream in the Mediterranean Sea)</td><td>Typically gulls, here only shags</td><td>Born-Torrijos et al. (2016)</td></tr><tr><td>Cryptocotyle lingua</td><td>1st intermediate host Littorina, 2nd fish</td><td>Piscivorous birds</td><td>Schwantes (2023)</td></tr><tr><td colspan="4"><strong>Nematoda</strong></td></tr><tr><td>Anisakis simplex</td><td>Various fish or cephalopods as intermediate host</td><td>Marine mammals</td><td>Schwantes (2023)</td></tr><tr><td>Contracaecum spp.</td><td>Fish as intermediate host</td><td>Piscivorous birds and marine mammals</td><td>Mattiucci and Nascetti (2008)</td></tr><tr><td>Cosmocephalus sp.</td><td>Amphipods as first intermediate host, fish as paratenic host</td><td>Aquatic birds</td><td>Mutafchiev et al. (2010)</td></tr><tr><td>Stegophorus sp.</td><td>Unknown</td><td>Piscivorous birds</td><td>Nagasawa et al. (1998)</td></tr></tbody></table>

knowledge, not reported from black-legged kittiwakes and northern fulmars. Larval *Anisakis* sp. were also found in northern fulmars, as previously shown (e.g., Kuklin et al. 2019; Mallory et al. 2007). *Stegophorus* sp. was found in northern fulmars and razorbills in the present study. The most commonly mentioned species of this genus in the literature occurring in the Northern Hemisphere is *S. stellaepolaris*, which was originally described from northern fulmars (Parona 1901), but also found in a number of other seabird hosts (Nagasawa et al. 1998; Threlfall 1971). 1998). This seemingly
generalist parasite might be a species complex, as slightly divergent morphological variants were found in individuals parasitising Brünnich's guillemots *Uria lomvia* (Nagasawa *et al.* 1998). The nematode *Cosmocephalus* sp. is also worldwide distributed and is found in various seabird hosts (e.g., Fusaro *et al.* 2024; Mutafchiev *et al.* 2010; Shutler *et al.* 2012; Threlfall 1971). Here, *Cosmocephalus* sp. was detected only in a single razorbill individual. Other species of nematodes were detected in razorbills, European shags, and northern fulmars, but could only be classified to a very general level (infraorder Spirurina), due to the lack of reference sequences in GenBank. Nevertheless, they seemed to be 3 different species based on the comparison of the sequences.

### Trematoda

The most common trematode was *Cryptocotyle lingua*, with 3 seabird species being infected, specifically sandwich terns (first record, and the only helminth found in this seabird species in the present study), black-legged Kittiwakes, and northern fulmars, as previously found (reviewed in Schwantes 2023). This is consistent with *C. lingua* metacercariae being common in North-East Atlantic fish (Duflot *et al.* 2021; 2023). *Cardiocephaloides longicollis* was the only trematode found in European shags and the first record for the species. Species of Himasthlimidae and Microphallidae are commonly found in coastal ecosystems of the North-East Atlantic (Lauckner 1984; Richard *et al.* 2022), having gastropods as first intermediate hosts and reaching maturity in seabirds, notably in species of Laridae.

### Qualitative differences in helminth diversity depending on host species feeding strategies

The targeted seabird species present contrasting feeding strategies and habitats. In the North-East Atlantic, all 3 species of auks (Atlantic puffins, common guillemots, and razorbills) are pursuit-diving, specialised piscivorous seabirds that feed primarily on small schooling fish, such as sandeels, clupeids, and sprat (Anderson *et al.* 2013; Fayet *et al.* 2021; St John Glew *et al.* 2018; 2019). Chick-rearing adults forage in both oceanic and neritic waters, minimising distance to the colonies (Fayet *et al.* 2021), while during the non-breeding period, all three species feed mainly in oceanic waters (Buckingham *et al.* 2023; Fayet *et al.* 2017). Black-legged Kittiwakes and northern fulmars feed at the surface in oceanic waters both during the breeding and nonbreeding periods, and have a more diverse diet, relying primarily on fish (Lemesle *et al.* 2024; Mar-kones *et al.* 2009; Ojowski *et al.* 2001). In particular, northern fulmars are highly mobile generalist surface feeders that exploit extensively and increasingly fisheries discards, both during and outside breeding (Darby *et al.* 2021; 2023). Sandwich terns and common gulls are restricted to coastal environments and feed at the surface, both during and outside the breeding period (Garthe and Flore 2007; Pedersen *et al.* 2000). Sandwich terns are fish-specialists (Courtens *et al.* 2017), while common gulls have a generalist diet, with prey captured in marine or terrestrial environments, including during the nonbreeding period (Kubetzki *et al.* 1999; Kubetzki and Garthe 2003). European shags are also restricted to coastal envir-onments and are piscivorous specialists feeding on benthic and demersal fish captured by pursuit-diving, both during and outside breeding (Howells *et al.* 2018; Michelot *et al.* 2017). The Antarctic seabird species targeted breed in an inland location in Dronning Maud Land, approximately 200 km from the open sea. During breeding, south polar skuas feed exclusively on eggs, chicks, and sometimes adults of the Antarctic petrel and snow petrel

*Pagodroma nivea*, and never forage at sea (Brooke *et al.* 1999; Busdieker *et al.* 2020), while they migrate to oceanic waters of the Indian and Atlantic oceans during the non-breeding season (Weimerskirch *et al.* 2015). The Antarctic petrel is a pagophilic species foraging in dense pack ice but also open Antarctic waters, feeding primarily on Antarctic krill *Euphasia superba* (Descamps *et al.* 2016; Lorentsen *et al.* 1998).

Previous research has demonstrated that diet plays a crucial role in the parasite diversity of birds. Notably, dietary generalist feeding birds have a higher diversity of parasites than dietary specialist birds (Gutiérrez *et al.* 2017; Thieltges *et al.* 2013). Our results are partially in agreement with this. Fish-feeding specialists such as the auks were less parasitised than generalist species such as the northern fulmar. However, the generalist common gull was infected with only two parasite taxa. In contrast, European shags, which are fish specialists, had high parasite diversity and prevalence. Parasite diversity has also been shown to vary with habitat, being, for example, greater in coastal/neritic marine mammal hosts than in their oceanic counter-parts (Raga *et al.* 2009), because of higher availability and abundance of intermediate hosts at the interface between coastal and terrestrial environments, favouring complex parasite life cycles. Based on our dataset, feeding in coastal or oceanic waters did not seem to be a clear driver of variation in parasite diversity. Instead, oceanic surface-feeding seabirds had comparable parasite diversity to coastal surface-feeding seabirds, as shown by a relatively high Sørensen's similarity index between these 2 groups. In addition, both oceanic surface-feeders and coastal seabirds had higher para-site diversity than the oceanic diving species (the auks). This sug-gests that oceanic birds feeding at the surface are more prone to parasite infection than birds that feed deeper in the water column. One possible explanation for this could be the manipulation of intermediate hosts by the parasites themselves. While this behaviour has not been investigated in open-sea marine fish, studies on estu-arine and freshwater fish species infected with trematodes have revealed that parasitised fish spend more time at the surface of the water or display more conspicuously, making them more susceptible to predation by birds foraging at the surface (Lafferty & Morris 1996; Schwelm *et al.* 2021). The European shag was an exception, being parasite-rich and a diving species. The high parasite diversity of European shags could stem from feeding in coastal benthic envir-onments, which have been shown to be parasite-rich (Hoberg 1996). In addition, and in contrast to the other bird species, all European shags were juveniles, suggesting a potential age-class effect on parasite richness that should be confirmed by further studies.

Interestingly, several trematode parasites were present in the oceanic black-legged Kittiwakes and northern fulmars. This obser-vation is consistent with previous records of *Cryptocotyle lingua* in these seabird species (Kuklin *et al.* 2019; Schwantes 2023). Although trematode life cycles are typically associated with coastal environ-ments due to the shallow-water distribution of their molluscan intermediate hosts, infection of oceanic seabirds does not necessarily imply recent coastal feeding. Instead, these birds may have acquired infections through the consumption of infected fish acting as second intermediate hosts, many of which are known to migrate from coastal nursery habitats into offshore waters (Duflot *et al.* 2023). Such host movements likely facilitate the transport of metacercariae far from the coast and provide an effective mechanism for offshore transmission of coastal trematode parasites (Marcogliese 2007).

The only seabird species that were completely free from hel-minthic gastrointestinal parasites in the present study were common guillemots and Atlantic puffins, even though these species were previously found to harbour various helminths (Hoberg 1996;
Kuklin *et al.* 2025; Muzaffar and Jones 2004; Hoberg and Souda-chanh 2020; Schwantes 2023). This probably stems from the small sample size, the body condition of the birds, or other unknown factors. Stranded and bycatch razorbills and common guillemots harboured broadly comparable parasite communities, and no obvi- ous differences in infection patterns were detected between the two groups. This suggests that variation in parasite occurrence may be more strongly influenced by extrinsic factors, such as diet or sea- sonal effects, rather than intrinsic factors like body condition, although this cannot be conclusively assessed with the present data. Given the limited sample size, these observations should be inter- preted with caution. Nevertheless, the results indicate that stranded birds can provide useful material for the assessment of helminth diversity in seabirds.

Finally, it is noteworthy that parasite infection in south polar skuas during the breeding period could originate directly from their prey (Antarctic and snow petrels) through post-cyclic transmis- sion, or, more likely, from ingestion of the petrels' stomach contents (primarily krill). Snow petrel parasite diversity, and a larger sample size of south polar skuas and Antarctic petrels, should be analysed to unravel this.

## Conclusions

Several novel host-parasite associations (n = 9) were reported in the present study, contributing to the knowledge of seabird helminth fauna. The small size and heterogeneous nature of the sample prevented us from statistically testing differences in infection char- acteristics between groups. Our observation of a higher helminth diversity in oceanic surface-feeding *versus* diving seabirds merits further investigation, including a larger sample size. This could be achieved by using molecular, non-destructive techniques such as eDNA metabarcoding, and should account for potentially confound- ing factors such as host sex, age, migratory destinations, season, and geographic region. Nevertheless, this study provides an overview of the distribution of helminth parasites among a subset of understud- ied seabird species.

**Supplementary material.** The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X26101163.

**Acknowledgements.** The authors thank Ewan Wakefield, Joanna Sulich, and Ceslav Czyz for assistance in the field at Svarthamaren and at Troll Station, as well as Frédéric Angelier, Charles-André Bost, Paco Bustamante, Charline Parenteau, and Gauthier Poiriez for support during dissections at the CEBC and LIENSs. Further, the authors are grateful to the French wildlife rescue centres of the Nantes Veterinary School (CVFSE/ONIRIS), the Ille Grande Station (Ligue de Protection des Oiseaux), and the Association ‘Volée de Piafs’ for providing carcasses of birds.

**Financial support.** Excellence Chair ECOMM funded by the Region Nouvelle Aquitaine (France). The work at Svarthamaren in the 2021/2022 breeding season was funded by the Antarctic Programme of the Norwegian Polar Insti- tute.

**Competing interest.** The authors declare none.

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