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Determinants of Lungworm Specificity in Five Cetacean Species in The Pool et al. Parasites Vectors (2021) 14:196 https://doi.org/10.1186/s13071-021-04629-1 Parasites & Vectors RESEARCH Open Access Determinants of lungworm specifcity in fve cetacean species in the western Mediterranean Rachel Pool* , Clara Romero‑Rubira, Juan Antonio Raga, Mercedes Fernández and Francisco Javier Aznar Abstract Background: Current data about Pseudaliidae show contrasting patterns of host specifcity between congeneric species. We investigated how both contact and compatibility between hosts and parasites contributed to the pat‑ terns of lungworm infection observed in a community of fve species of cetaceans in the western Mediterranean. Methods: The lungs of 119 striped dolphins Stenella coeruleoalba, 18 bottlenose dolphins Tursiops truncatus, 7 Risso’s dolphins Grampus griseus, 7 long‑fnned pilot whales Globicephala melas, and 6 common dolphins Delphinus delphis were analysed for lungworms. Parasites were identifed by morphology and analysis of ITS2 sequences using both maximum likelihood and Bayesian inference methods. Body length was used as a proxy for lungworm species ftness in diferent hosts and compared with Kruskal‑Wallis tests. Infection parameters were compared between cetacean species using Fisher’s exact tests and Kruskal‑Wallis tests. Phylogenetic specifcity was explored by collating the overall lungworm species prevalence values in hosts from previous surveys in various localities. To explore the relative impor‑ tance of vertical and horizontal transmission, Spearman’s rank correlation was used to look for an association between host size and lungworm burden. A Mantel test was used to explore the association between lungworm species simi‑ larity and prey overlap using dietary data. Results: Halocercus delphini had higher infection levels in striped dolphins and common dolphins; Stenurus ovatus had higher infection levels in bottlenose dolphins; and Stenurus globicephalae had higher infection levels in long‑ fnned pilot whales. These results are congruent with fndings on a global scale. Morphometric comparison showed that the larger nematodes were found in the same host species that had the highest parasite burden. Lungworms were found in neonatal striped dolphins and a Risso’s dolphin, and there was a weak but signifcant correlation between host size and parasite burden in striped dolphins and bottlenose dolphins. There was also a weak but signif‑ cant association between prey overlap and lungworm species similarity. Conclusions: Data indicate that phylogenetic specifcity has an important role in governing host–parasite associa‑ tions, as indicated by the higher infection levels and larger nematode size in certain hosts. However, diet can also infuence infection patterns in these preferred hosts and contribute to less severe infections in other hosts. Keywords: Lungworms, Pseudaliidae, Cetaceans, Mediterranean Sea, Host specifcity, Parasites Background Adults of all but one of the 29 currently valid species of lungworms of the family Pseudaliidae typically infect the lungs, middle ear and air sinuses of odontocetes world- wide [1, 2]. In heavy infections, lungworms can cause *Correspondence: [email protected] Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary severe health problems such as osseous lesions in the cra- Biology, Science Park, University of Valencia, PO Box 22085, nial sinuses, blocked airways, verminous pneumonia and Valencia 46071, Spain © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Pool et al. Parasites Vectors (2021) 14:196 Page 2 of 14 secondary bacterial infections, all of which can lead to the analysis obviously assumes that parasites are reliably stranding or even death of their hosts [1]. identifed. Little is known about the life cycles of pseudaliids. In this study we investigate, for the frst time, patterns Other metastrongyloid nematodes infecting terrestrial or of host specifcity of the Pseudaliidae in a local commu- marine mammals have heteroxenous cycles and, depend- nity of fve cetacean species following the above scheme. ing on the habitat, can use gastropods or oligochaetes as First, we combined morphological and molecular meth- intermediate hosts, or fsh as paratenic hosts [1, 3]. In ods to verify whether putative nematode species infect- pseudaliids, however, direct evidence on the use of inter- ing diferent hosts are indeed conspecifc. Second, we mediate or paratenic hosts is limited to a single species. looked for evidence of vertical and/or trophic transmis- Lehnert et al. [4] detected larvae of Pseudalius infexus sion for each lungworm species. Since direct detection in dabs Limanda limanda, which are common prey of of intermediate or paratenic hosts has proven unsuc- harbour porpoises Phocoena phocoena (defnitive hosts) cessful to date (see, e.g., [16]), we investigated the prob- in North Sea waters. In other pseudaliids, evidence for ability of parasite exchange among host species through trophic transmission is only implied by the absence of dietary overlap analysis, assuming that the greater the infection in unweaned hosts, coupled with the increase overlap in the consumption of infected prey species, the in prevalence with host age [1]. However, there is also higher the probability that the hosts share the same para- evidence for vertical transmission from mother to calf at sites [12–14]. Tird, we used proxies to compare ftness least for three species of Halocercus infecting bottlenose of lungworms between host species. Finally, we explored dolphins Tursiops truncatus, orcas Orcinus orca, and the consistency of host choice in other cetacean commu- striped dolphins Stenella coeruleoalba [5–7]. nities and estimated the global phylogenetic specifcity of Data about the specifcity of pseudaliids are similarly the lungworm species based on overall records. scarce, in part because host sampling is problematic and experimental work virtually impossible. Based on host– parasite records, it would seem that patterns of specifc- Methods ity are contrasting even between congeneric species. For Sample collection example, Stenurus minor seems to be widespread among Pseudaliid lungworms were collected from the car- members of the families Phocoenidae, Delphinapteridae casses of 119 striped dolphins Stenella coeruleoalba, and Delphinidae, whereas Stenurus arctomarinus has 18 bottlenose dolphins Tursiops truncatus, 7 Risso’s only been reported in the beluga whale Delphinapterus dolphins Grampus griseus, 7 long-fnned pilot whales leucas [2, 8]. In addition, the same odontocete species Globicephala melas, and 6 short-beaked common dol- can have strikingly diferent levels of infection for the phins Delphinus delphis that were found stranded along same pseudaliid species depending on geographic loca- the Mediterranean coast of Spain (Valencian Commu- tion. For example, the prevalence of Halocercus lageno- nity, between 40°31′00″N, 0°31′00″E and 37°50′00″N, rhynchi in striped dolphins in Italy, the UK and Costa 0°45′42″W) between 1982 and 2019. In the case of the Rica was 6.67%, 14.3% and 54.2%, respectively [9–11], striped dolphins, we excluded individuals from 1990 and and this species has never been detected in striped dol- 2007 because they had sufered a Morbillivirus outbreak, phins from the western Mediterranean Sea despite the which could produce a confounding efect on parasite high sampling efort [7]. abundance. Only carcasses in preserved states 1–3 [17] Generally speaking, patterns of specifcity can be were selected for analysis. understood as the result of two sequential flters, i.e., During the necropsy, the animals were measured and contact and compatibility [12–14], which operate at sexed; their cranium was disarticulated from the spine the local community of relevant hosts. Investigating and cranial sinuses were examined for parasites, and the the action of these flters obviously requires data on life lungs were removed and stored at −20 °C. Only one lung cycles (to shed light on patterns of contact) and data on per individual, randomly selected, was used in this study; ftness in each host (to shed light on patterns of compat- the other was saved for a future study on microhabitat ibility). Furthermore, the analysis of specifcity must be selection. After thawing, the airways of each lung were addressed considering diferent facets [15], i.e., (1) struc- cut from the trachea to the caudal apex and rinsed over tural specifcity (how parasite populations are distrib- a 0.2 mm sieve. uted among the host species of the
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