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International Journal for Parasitology: Parasites and Wildlife logoLink to International Journal for Parasitology: Parasites and Wildlife
. 2025 Jun 16;27:101102. doi: 10.1016/j.ijppaw.2025.101102

First report of three different parasite species in two dolphin species stranded on the coast of Portugal

João T Cruz a,b,1, David W Ramilo c,d,e,1,⁎, Jorge Correia a,b, Fernando Afonso a,b, Isabel Pereira da Fonseca a,b, Luís Cardoso b,e,f, Alfonso Marzal g,h, Marina Sequeira i, Ana Falcão i, Luís Madeira de Carvalho a,b
PMCID: PMC12219366  PMID: 40606264

Abstract

Understanding the dynamics of the interaction of marine parasites with their hosts, especially in terms of diversity, distribution and pathogenicity can be of great importance in a Global Change era. Monitoring the parasite diversity of marine mammals holds not only ecological importance but also can be of significance for public health. However, there is a scarcity of parasitological research on cetaceans in the eastern Atlantic Ocean, namely in Portugal. Here we explore the morphology, diversity and pathogenicity of parasites in two different cetaceans, Delphinus delphis (common dolphin) and Stenella coeruleoalba (striped dolphin), stranded near the coast of Lisbon, Portugal. During their necropsy, three parasite species were collected and preserved in 70 % ethanol. In the laboratory, nematodes were identified as Halocercus delphini, and tetraphyllidean merocercoids as Clistobothrium delphini and Clistobothrium grimaldii. Additionally, C. delphini specimens were classified as belonging to morphotypes B and C. To the authors' knowledge, this is the first reference of these three parasites species in Portugal. This information is critical for understanding the impact of these organisms on the health of dolphins and adds information to the parasitological fauna of these hosts.

Keywords: Cetaceans, Halocercus delphini, Clistobothrium grimaldii, Clistobothrium delphini, Portugal

Graphical abstract

Image 1

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Highlights

  • •

    First report of three parasite species in dolphins along Portuguese coast.

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    High prevalence of Clistobothrium spp. in two dolphin species.

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    Lungworm Halocercus delphini linked to severe respiratory lesions.

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    Documented morphotypes of C. delphini cysts in subcutaneous blubber.

1. Introduction

Oceanic dolphins (family Delphinidae) are cetaceans widely distributed in the tropical and temperate oceans around the world (Natoli et al., 2006; Cunha et al., 2015). Common dolphins (Delphinus delphis) are one of the most abundant dolphin species in Atlantic Iberian waters, presenting the highest stranding occurrence in Portugal (Santos et al., 2012; Hammond et al., 2013; Ferreira et al., 2012; Monteiro et al., 2016). The world range of striped dolphins (Stenella coeruleoalba) extends from warm-temperate to tropical waters, and these cetaceans are the most frequent dolphins in the Mediterranean Sea (Archer and Perrin, 1994).

In Portugal, the striped dolphin primarily preys on mesopelagic and demersal fish, with sardine (Sardina pilchardus) and blue whiting (Micromesistius poutassou) as key species, along with cephalopods (Pinheiro, 2017; Marçalo et al., 2021). Although also classified as Least Concern in Portugal (Braulik, 2019), this species faces multiple threats, including bycatch, particularly in northern and central regions (Ferreira, 2007; Ferreira et al., 2012, 2016; Marçalo et al., 2021), high morbillivirus prevalence in Portugal and Galicia (Bento et al., 2016), and the ingestion of microplastics (Novillo et al., 2020) and marine litter (Puig-Lozano et al., 2018; Ferreira et al., 2023a).

The common dolphin has a more varied diet, primarily consisting of epipelagic and mesopelagic fish, with a smaller proportion of squid. Its prey includes gadids, small scombroids, clupeoids, and both loliginid and ommastrephid squids (Perrin, 2018; Saavedra et al., 2025, in press). The species is susceptible to infections by morbillivirus, herpesvirus, and Toxoplasma sp., which can significantly impact individual health (Bento et al., 2016, 2019). Additionally, it faces severe bycatch pressure; in mainland Portugal the bycatch rate is alarmingly high relative to population estimates (Vingada et al., 2015), with 44–61 % of stranded individuals showing evidence of entanglement (Sequeira and Ferreira, 1994; Marçalo et al., 2015; Ângelo, 2020). Due to population decline mainly driven by bycatch mortality, this species has been reclassified from Least Concern to Near Threatened (Ferreira et al., 2023b).

Despite Portugal's extensive coastline, two major archipelagos (Madeira and Azores), a long-standing tradition of marine resource exploitation, and the regular consumption of fish and seafood, research in marine parasitology remains less developed than in other European countries such as France, the UK, and Norway (Costa, 2008). Within cetacean parasitology, studies in Portugal are even scarcer. The few existing works include an analysis of whale faecal samples in the Azores Islands (Hermosilla et al., 2016) and two reports on helminths in dolphins: the acanthocephalan Bolbosoma vasculosum in Delphinus delphis (Costa et al., 2000) and the nematode Anisakis spp., detected in a study on Delphinus delphis, Phocoena phocoena, and Stenella coeruleoalba, though the specific host species was not identified (Lino et al., 2021).

Because the intensity and pathologies of marine parasites are expected to increase due to Global Climate Change (Byers, 2021), monitoring of parasite diversity in marine environments is important for both ecological and public health points of view (Selbach et al., 2022). In this sense, the parasites of marine mammals can provide vital information on their dynamics in the marine ecosystems and the ecology of their hosts' populations, particularly by assisting in the identification of foraging locations, diets, and distribution (Castro et al., 2014). In addition, they have been used as sentinel species for biomonitoring purposes of pollutants (Nachev and Sures, 2016). However, the biodiversity of parasites in cetaceans is a neglected area of research in marine ecosystems, namely in Portugal (Agustí et al., 2005; Guimarães et al., 2015; Cipriani et al., 2022; Saldaña et al., 2022).

Lungworms of cetaceans belong to the family Pseudaliidae, which includes the genus Halocercus Baylis and Daubney, 1925 (Gibson et al., 1998). The life cycle of these parasites in marine mammals is not completely understood, although there is evidence of intermediate hosts which are prey for cetaceans (Dailey, 1970; Houde et al., 2003; Lehnert et al., 2010; Reckendorf et al., 2018). There are reports of Halocercus spp. in the lower respiratory system of cetaceans, causing emphysema, atelectasis, mineralization of bronchiolar cartilages, focal inflammatory processes and bronchointerstitial pneumonia (Demarque et al., 2020; Fischbach and Seguel, 2023; Balseiro et al., 2023).

Tetraphyllidean merocercoids (terminology of larval cestodes followed by Chervy, 2002) are commonly reported in most cetacean species and some pinnipeds worldwide, including S. coeruleoalba and D. delphis (Agustí et al., 2005; Oliveira et al., 2011; Quiñones et al., 2013). These parasitic cysts, typically measuring 0.5–4 cm in diameter, are fluid-filled and represent the intermediate stages of adult tapeworms (Gibson et al., 1998; Lehnert et al., 2017).

Two types of merocercoids have been widely recognized: Phyllobothrium delphini (Bosc, 1802) Gervais, 1885, encysted in the subcutaneous blubber, usually in the abdominal area; and Monorygma grimaldii (Moniez, 1889) Baylis, 1919, encysted mainly in the peritoneum of the abdominal cavity, being bigger than the previous one (Gibson et al., 1998; Agustí et al., 2005; Lehnert et al., 2017). A recent molecular study transferred these parasites to the Clistobothrium genus. Phyllobothrium delphini is now Clistobothrium delphini, and Monorygma grimaldii was changed to Clistobothrium grimaldii, preserving the same identification characteristics (Caira et al., 2020).

C. grimaldii cysts are morphologically identical to each other. Regarding C. delphini, different morphotypes (categories A, B and C) have been identified (Agustí et al., 2005). According to Dailey, 1985), these morphotypes belong to different species; however, Siquier and Le Basargued propose that the morphotypes represent different phases of evolution of the same parasite species (Agustí et al., 2005).

Adult worms were traditionally believed to inhabit the spiral valves of elasmobranch and holocephalan fishes (Euzet, 1994; Gibson et al., 1998; Lehnert et al., 2017), although a recent molecular study show that the adult forms of C. delphini and C. grimaldii are still unknown and those adult forms previously found don't correlate genetically with the larval forms (Caira et al., 2020).

Several negative effects on cetacean health of lungworm infections have previously been described (Siebert et al., 2001; Vlasman and Campbell, 2004; Lehnert et al., 2010; Reckendorf et al., 2018), as well as lesions caused by tetraphyllidean merocercoids (Alonso-Farré et al., 2013; Jerdy et al., 2022).

The authors here report recent parasitological findings regarding the hosts S. coeruleoalba and D. delphis and the parasites Halocercus delphini, C. grimaldii (syn. Monorygma grimaldii) and C. delphini (syn. Phyllobothrium delphini) in Portugal, providing macroscopic, microscopic and histopathologic descriptions of these parasites and the lesions they cause.

2. Material and methods

Two adult female dolphins, one D. delphis and one S. coeruleoalba, stranded along the Lisbon coast (Fig. 1) between 2018 and 2019, were stored frozen immediately after recovery and necropsied later at the Anatomic Pathology Laboratory of the Faculty of Veterinary Medicine, University of Lisbon (FMV-ULisboa). Both specimens were in a moderate nutritional status after recovery. Necropsies were performed following standardized pathological examination and sampling protocols (Pugliares et al., 2007), with only abnormal findings reported. Additionally, a full parasitological examination was conducted on both dolphins by the Parasitology and Parasitic Diseases Laboratory at FMV-ULisboa.

Fig. 1.

Fig. 1

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Map of Portugal showing the stranding locations of the studied dolphins. Red marker: Alcochete (Tagus River estuary), where the Stenella coeruleoalba specimen was found. Blue marker: Sado River estuary, where the Delphinus delphis specimen was found.

The D. delphis specimen stranded in the river Sado estuary and was received and necropsied on the October 1, 2018. The body was with moderate decomposition (Ijsseldijk et al., 2019), weighed prior to careful inspection for external lesions and was laid right flank down. A transverse incision was made cranial to the first rib, followed by two longitudinal incisions, one dorsal and one ventral, along the length of the carcass. The left thoracic and abdominal walls were removed to provide optimal exposure of both cavities. Internal organs and structures, including ribs, pleura, heart, lungs, peritoneum, stomach, gut, liver, pancreas, spleen, kidneys and ovaries were examined systematically for lesions superficially, on cross-section and palpated. Liver and lung lesions were collected for histopathology by fixing the tissue in 10 % buffered formalin. Parasitic cysts were counted and collected from the subcutaneous blubber of the inguinal region, peritoneum, and abdominal wall. Lung parasites and parasitic cysts were isolated, rinsed in tap water, and preserved in 70 % ethanol for further analysis. The lung nematodes were counted, and some specimens were mounted on slides using Hoyer's medium, examined under a compound microscope, and identified morphologically following Baylis and Daubney (1925) and Delyamure (1968).

The S. coeruleoalba specimen was found stranded in Alcochete (left bank of the Tagus River) and necropsied on the April 4, 2019. The same necropsy protocol as described before was performed, although the body, which was in moderate decomposition (Ijsseldijk et al., 2019), was not weighed. Lung lesions were collected for histopathology. Several cystic structures were collected from the subcutaneous blubber of the inguinal area (Fig. 2).

Fig. 2.

Fig. 2

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Parasitic cysts collected from subcutaneous blubber of Stenella coeruleoalba (black arrows).

Parasitic cysts were counted and analysed under a stereoscope, prepared for histology using H&E staining and were categorized according to Failla Siquier and Le Bas (2003).

3. Results and discussion

Delphinus delphis specimen: Body weight was 65.7 kg. At external examination, excoriation lesions on the caudal fin and the lateral wall were observed. No evidence of decomposition or autolysis was observed. Lesions of purulent bronchopneumonia were recorded, together with a heavy nematode infection in the bronchial lumen. A complete dissection of both lungs was conducted, and all lungworms were recovered and enumerated, yielding a total count of 198 individuals (Fig. 3A and B). Specimens measured between 5.5 and 7 cm in length, and after microscopic evaluation they were identified as H. delphini (Fig. 3C). Details of the male posterior region of H. delphini such as spicules, papillary terminations and bursal rays, and a female anterior region is shown in Fig. 4A–C. On the lung microscopic examination, acute lesions of purulent bronchopneumonia, lesions of chronic obliterating bronchitis with partially calcified exudate, pulmonary sclerosis and cross sections of several H. delphini parasites were identified (Fig. 5A−C). In the abdominal cavity, there was a moderate volume of serosanguinous fluid. A total of two nodular lesions were observed in peritoneum and abdominal wall, formed by yellowish, spherical-like parasites, with approximately 20 mm in length (Fig. 6A and C), agreeing with plerocercoid forms of C. grimaldii. Altogether, other seven parasitic cysts with an average length of 5 mm were also observed in the subcutaneous blubber of the inguinal area and identified as intermediate stages of C. delphini (Fig. 6B and C). Two morphotypes, B (external wall round and curved necks, n = 5) and C (characteristic external U-shape, n = 2), were identified.

Fig. 3.

Fig. 3

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Halocercus delphini collected from the lungs of Delphinus delphis. A – Adult lungworms in bronchial lumen; B – Specimens collected from only one bronchus; C – Female specimen with approximately 6.5 cm in length.

Fig. 4.

Fig. 4

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Morphological aspects of Halocercus delphini. A – Male posterior region with spicules (blue arrow) and papillary terminations (black arrow); B – Male posterior region, showing bursal rays (black arrows); C – Female anterior region.

Fig. 5.

Fig. 5

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Histological preparations of lungs of Delphinus delphis stained with H&E. A – Lung with lesions of purulent exudative bronchopneumonia, congestion and presence of fibrin-leukocyte exudate in the alveoli lumen; B – Lung with bronchus presenting innumerable adult forms of Halocercus delphini in the lumen; C – Lung with chronic obliterating bronchitis lesions in which the lumen of the bronchi was filled with catarrhal exudate partially calcified. We also identify lesions of chronic pneumonia with the presence of extensive areas of sclerosis.

Fig. 6.

Fig. 6

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Parasitic cysts collected from peritoneum (A) and subcutaneous blubber (B) of Delphinus delphis. C – While peritoneal cysts measured 20 mm in length (black arrows – Clistobothrium grimalldi), those from inguinal area had an average length of 5 mm (blue arrows – Clistobothrium delphini).

After complete liver dissection, a brownish nodular lesion with 2 cm in the major axis was observed. The microscopical examination of the hepatic nodule revealed the presence of parasitic granuloma rich in operculated eggs and delimited by a fibrous capsule (Fig. 7A and B).

Fig. 7.

Fig. 7

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Histological preparations of liver of Delphinus delphis stained with H&E. A – Hepatic nodule, with lesion of parasitic granuloma, encapsulated, in which numerous operculated eggs are observed. B - Higher magnification of the parasite eggs.

An osteomyelitis lesion was observed on the ventral side of the 7th left sided rib. The stomach contained a large quantity of small fish bones but no parasites. No other significant findings were noted.

Stenella coeruleoalba specimen: Post-mortem lesions were evident externally, more patently on the cranial and lateral regions of the dorsal fin and on the right side of the abdominal area, possibly due to the joint action of autolysis and predation. Internally, only minor signs of decomposition were observed. An abundant amount of blood was present in the mouth, while the stomach and intestines were empty and showed no evidence of parasitic infection. Macroscopically, hepatization areas and pus foci were present in the lungs, but no parasites were detected. On the lungs’ histopathological examination, acute lesions of purulent bronchopneumonia with neutrophils in pyknosis, karyorrhexis and karyolysis were identified. Several necrotic cells, including neutrophils in the bronchi and bronchioles were also observed. A total of six parasitic cysts were collected from the subcutaneous blubber of the inguinal area, measuring between 4 and 8 mm in length, and were identified as intermediate stages of C. delphini. Two morphotypes, B (external wall round and curved necks, n = 5) and C (characteristic external U-shape, n = 1), were identified (Fig. 8). No additional parasitic cysts were detected upon through necropsy of the entire body.

Fig. 8.

Fig. 8

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Histological preparations of the parasitic cysts of Clistobothrium delphini stained with H&E. A - (Left) Cyst 1, a morphotype category “B” because of the curved neck; (Right) Cyst 1 scolex detail. B - (Left) Cyst 2, a morphotype category “B” due to the presence of separate scolex and neck in the same transversal cut; (Right) Cyst 2 scolex detail. C - (Left) Cyst 3, a morphotype category “C” due to U-shape of the cyst wall (black arrow); (Right) Cyst 3 scolex detail.

The cause of death in both dolphins was attributed to pneumonia. In the S. coeruleoalba specimen, the pneumonia was classified as purulent bronchopneumonia, suspected to be of bacterial origin, with no evidence of parasitic involvement. In contrast, the D. delphis specimen died as a result of pneumonia caused by a severe H. delphini infection, accompanied by a secondary bacterial infection. These findings highlight the significant impact of H. delphini on dolphin health. The negative effect of this parasite on odontocete health has also been stated previously (Vlasman et al., 2004; Lehnert et al., 2010; Reckendorf et al., 2018). Severe lungworm infections, like the one reported in the present work, have been described previously as causes of general respiratory distress, bronchopneumonia and secondary bacterial infections (Siebert et al., 2001; Vlasman et al., 2004; Siebert et al., 2007; Reckendorf et al., 2018), and have also been implicated as a common and important contributing factor to the mortality of dolphins (Lehnert et al., 2010). A study analysing 300 cetaceans stranded along the coast of England and Wales between 1990 and 1994 found H. delphini exclusively in common dolphins (Delphinus delphis), with a prevalence of 43.5 % among the 101 individuals examined. Regarding other Halocercus species identified in the study, H. lagenorhynchi was detected in 14 % of the 14 Stenella coeruleoalba examined, while H. invaginatus and H. taurica were each found in two of the 173 Phocoena phocoena analysed (Gibson et al., 1998). Similarly, a study of five cetacean species stranded along the Spanish Mediterranean coast between 1987 and 2019 found that D. delphis and S. coeruleoalba had the highest prevalence of H. delphini, at 100 % (n = 6) and 61.3 % (n = 119), respectively (Pool et al., 2021). Notably, these two species, also analysed in the present study, exhibited significantly higher infection rates compared to bottlenose dolphins and pilot whales (Pool et al., 2021). Additionally, the molecular analysis of Pseudaliidae parasites was consistent with species identification based on morphological characteristics (Pool et al., 2021), confirming the reliability of morphological identification for this parasite. Later, Pool and colleagues (2024) further validated this approach by exclusively using morphological methods to identify and study the distribution of Halocercus delphini in the lungs of striped dolphins.

In the present study, operculated eggs were also observed in the liver. While it is possible that these eggs belong to a trematode species, this identification remains tentative, as no trematode parasites were detected during the comprehensive parasitological screening.

Tetraphyllidean merocercoid infections can also cause lesions in their hosts. In some cases, they can evolve into large purulent abscesses (Alonso-Farré et al., 2013) and have also been described as a cause of granulomatous dermatitis (Jerdy et al., 2022). Clistobothrium delphini and C. grimalldi are considered to be among the most common parasites of cetaceans. Despite that, the life cycles of these parasites have not been elucidated, and little is known about the biology of their larval forms (Abollo et al., 1998; Failla Siquier and Le Bas (2003); Caira et al., 2020). Considering the presence of C. delphini in the striped dolphin, published reports of this infection are only available from the United States of America, Costa Rica, Argentina, the United Kingdom, Italy and Spain (Oliveira et al., 2011; Castro et al., 2011). Previous studies in S. coeruleoalba and D. delphis in Spain showed a very high prevalence of C. delphini in both species, where 87.5 % of S. coeruleoalba (n = 8) and 70 % of D. delphis (n = 50) were infected with this parasite in the Atlantic coasts of Galicia (Abollo et al., 1998), and 100 % of sampled striped dolphins (n = 11) in Mediterranean coasts of Valencia and Murcia harbored C. delphini worms (Agustí C et al., 2005). These studies also reported that 75 % of striped dolphins (n = 8) and 42 % of common dolphins (n = 50) from Galicia were infected with C. grimaldii (Abollo et al., 1998), whereas all the striped dolphin (n = 11) from Valencia and Murcia harboured this parasite (Agustí C et al., 2005). Our outcomes reveal a high incidence of both tetraphyllidean merocercoids parasites in the two-dolphin species. However, because of the low sample size in our study (one specimen of each dolphin species), we should be cautious with the interpretation of our results regarding the incidence of these parasites. Further studies exploring parasite diversity, prevalence and intensity abundance are required for a complete understanding of the life cycle and distribution of parasites impacting the health of cetaceans.

To the best of our knowledge, this is the first published reference of C. delphini, C. grimaldii and H. delphini in Portugal, which can contribute to future studies on their prevalence and intensity in D. delphis and S. coeruleoalba hosts. The expected high prevalence in this country, at least regarding C. delphini and C. grimaldii, and the non-existence of previous studies reporting these parasite species in Portugal coasts point out the need of additional research in this field. Our outcomes reveal new parasite distribution on marine mammals and provide valuable information to understand the pathogenic impact of parasites on dolphin health. These results are of importance to future studies exploring changes in the distribution and pathogenicity of parasites in a Global Climate Change scenario.

CRediT authorship contribution statement

João T. Cruz: Writing – review & editing, Writing – original draft, Investigation, Conceptualization. David W. Ramilo: Writing – review & editing, Writing – original draft, Investigation, Conceptualization. Jorge Correia: Writing – review & editing, Resources, Investigation. Fernando Afonso: Writing – review & editing. Isabel Pereira da Fonseca: Writing – review & editing, Resources, Conceptualization. Luís Cardoso: Writing – review & editing. Alfonso Marzal: Writing – review & editing. Marina Sequeira: Writing – review & editing. Ana Falcão: Writing – review & editing. Luís Madeira de Carvalho: Writing – review & editing.

Institutional review board statement

Ethical review and approval were waived for the present study, due to the absence of interference with the normal life standard of free-living animal. This study was performed only after the animal’ stranding without any human interference before this happened.

Funding

The research developed by J.T.C., D.W.R., J.C., F.A., I.P.d.F. and L.M.d.C. is supported by national funds through FCT—Fundação para a Ciência e Tecnologia, under the scope of projects UIDB/00276/2020 (CIISA-FMV-ULisboa) and LA/P/0059/2020 (AL4AnimalS). J.T.C. holds a scientific initiation grant (ref. UIDB/00276/2020) and a master grant, MSC22Jul-04, both provided by CIISA-FMV-ULisboa. The research developed by A.M. was funded by the line of action LA4 (R + D + I program in the Biodiversity Area financed with the funds of the FEDER Extremadura, 2021–2027 Operational Program of the Recovery, Transformation and Resilience Plan).

Declaration of competing interest

None.

Acknowledgements

The authors would like to thank all anonymous people who helped the above-mentioned cetaceans while they were stranding and who also helped and made possible all the collected samples from these animals.

Contributor Information

João T. Cruz, Email: joaot99fmv@gmail.com.

David W. Ramilo, Email: david.ramilo@ulusofona.pt.

Jorge Correia, Email: jcorreia@fmv.ulisboa.pt.

Fernando Afonso, Email: fafonso@fmv.ulisboa.pt.

Isabel Pereira da Fonseca, Email: ifonseca@fmv.ulisboa.pt.

Luís Cardoso, Email: lcardoso@utad.pt.

Alfonso Marzal, Email: amarzal@unex.es.

Marina Sequeira, Email: marina.sequeira@icnf.pt.

Ana Falcão, Email: ana.falcao@icnf.pt.

Luís Madeira de Carvalho, Email: madeiradecarvalho@fmv.ulisboa.pt.

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