Cetaceans have developed a number of symbiotic associations (sensu Leung and Poulin, 2008) with other organisms, including endo-, meso- and ectoparasitism, commensalism, and mutualism (e.g., Arvy, 1982; Raga, 1994). Some of these organisms, the epibionts (also known as episymbionts or ectosymbionts), are associated to the external surface of cetaceans and can be classified into two basic types. On the one hand, ectoparasites live in/on the skin and cause a variable degree of harm by feeding on hosts’ integument (e.g., Smyth, 1962; Geraci and St. Aubin, 1987; Hopla et al., 1994). On the other hand, commensals or phoronts do not trophically depend on the tissues of cetaceans (also named basibionts in this case), thus they are generally harmless but benefit from epibiosis in multiple ways, e.g., via an improved feeding performance, reduction of predation, favored intraspecific contacts for reproduction, or offspring dispersion (Anderson, 1994; Seilacher, 2005; Carrillo et al., 2015). Not surprisingly, though, the limits of each type of interaction are not always clear-cut. For instance, whale-lice (fam. Cyamidae) are considered ectoparasites that primarily feed on hosts’ skin, but it has been speculated that they may opportunistically feed on plankton, even helping whales to detect plankton blooms, leading to a potentially mutualistic relationship (Rowntree, 1996). Or, high loads of commensal epibionts could increase the swimming drag or damage the skin on the site of settlement, thus producing indirect harm to cetaceans (Tomilin, 1957).

Given the high variety of life cycles of the epibionts of cetaceans, it is perhaps not surprising that their specific interactions are similarly diverse. Some epibionts depend strictly on cetaceans during their whole life (e.g., whale lice; Leung, 1976), whereas others use them only at some stages (e.g., barnacles; Nogata and Matsumura, 2006). Among commensals, many species are obligate epibionts, settling exclusively on cetaceans (e.g., coronulid barnacles; Hayashi et al., 2013), but others can colonize also inanimate substrata such as vessels or floating debris (e.g., Conchoderma spp. and Lepas spp.; Frick and Pfaller, 2013). The degree of host/basibiont specificity is also variable. For instance, many whale lice are known only from single, or a few, host species (Iwasa-Arai and Serejo, 2018), but other epibionts have a very broad host spectrum (e.g., Xenobalanus globicitipitis Steenstrup, 1852 or Pennella balaenoptera Koren & Danielssen, 1877; Kane et al., 2008; Fraija-Fernández et al., 2018). Finally, there are examples of hyperepibiosis in which some epibionts, e.g., barnacles, can act as basibionts for other epibionts, e.g., Conchoderma spp. or cyamids (Cornwall, 1927; Matthews, 1937; Leung, 1970a).

As many other symbionts, epibionts must succeed twice to live their associative life. This two-step process is mediated by the so-called encounter and compatibility filters (Combes, 2001). First, spatial and temporal overlap must take place for initial settlement. Second, whether the host is a suitable substratum will determine survival and/or reproduction on it. Epidermis renewal and hydrolytic substances of cetacean skin may prevent fouling, at least to some extent (Hicks 1985; Baum et al., 2000; Baum et al., 2001), but skin regeneration and immune functions are seemingly lower in debilitated dolphins (J. R. Geraci and S. H. Ridgway pers comm. in Aznar et al., 1994). Poor health can also result in slower swimming (Aznar et al., 1994; Lehnert et al., 2021), fostering better conditions for epibiotic settlement (e.g., providing more time for contact with blooms of free-living infective stages, or mild water flow over the host’s body, thus reducing drag and facilitating initial colonization). For instance, striped dolphins, Stenella coeruleoalba (Meyen, 1833), infected by morbillivirus and in poor nutritional condition harbored high loads of parasitic and commensal epizoites (Aguilar and Raga, 1993; Aznar et al., 1994; Aznar et al., 2005). Also, higher prevalence of cyamids in porpoises could hint a higher incidence of disease-related skin injuries, where they attach (Lehnert et al., 2021). Another example is the massive infestation of cyamids on a stranded humpback whale, Megaptera novaeangliae (Borowski, 1781), that suffered from severe discospondylitis and, as a result, reduced mobility (Groch et al., 2018).

Once settled, the impact of epibionts on cetacean health varies among taxa (especially between ectoparasites and commensals; see above). For instance, the mesoparasite Pennella balaenoptera penetrates the skin and blubber of its hosts; this process has been related to both macro- and microscopic lesions such as abscesses, inflammation, and dermatitis (Cornaglia et al., 2000; Gomerčić et al., 2006; IJsseldijk et al., 2018). In contrast, no direct damage has been related to whale lice infections (e.g., Migaki, 1987; Lehnert et al., 2021), although it has been speculated that their occurrence may hinder skin healing processes (Lehnert et al., 2021). On the other hand, the possibility that some cetacean epibionts can act as viral or bacterial vectors is an open question, as it has been observed for ectoparasitic crustaceans parasitizing fish (Smit et al., 2019) or lice infecting seals (La Linn et al., 2001). Climate changes have shifted the geographical distribution of arthropod-borne viruses (Gould and Higgs, 2008) and whether these may emerge in cetaceans and even be transmitted by their epibonts (e.g., ectoparasitic lice, see Van Bressem et al., 2009) remains unknown.

Due to temporal or permanent association with their hosts/basibionts, both endoparasites and epibionts represent a cost-effective tool to study multiple facets of cetacean biology (e.g., Dailey and Vogelbein, 1991; Balbuena et al., 1995; Gomes et al., 2021). However, epibionts are advantageous over endoparasites in that many of them are detectable in the field (e.g., using boat-based photography; see Hermosilla et al., 2015; Siciliano et al., 2020; Flach et al., 2021), and can often be easily found and counted on stranded hosts, be alive or dead, with minimum dissection, if at all (Balbuena et al., 1995). Most studies using epibionts as markers only require basic data to be gathered, i.e. genus- or, preferably, species-level identification, and quantification of population size at host individual or population scales. More elaborated research may require additional information on (1) degree of host specificity, (2) size measurements as an estimate of time since attachment, (3) distribution patterns on hosts’ body, (4) geographic range, and/or (5) selected molecular markers (e.g., Bushuev, 1990; Kaliszewska et al., 2005; Ten et al., 2019; Moreno-Colom et al., 2020; Lehnert et al., 2021).

At present, cetacean epibionts have been used, inter alia, as ‘tags’ to trace past (e.g., Collareta et al., 2018a; Taylor et al., 2019) or present-day (e.g., Pearson et al., 2020; Visser et al., 2020) migratory routes and habitat use; shed light on phylogeography, population structure, and ecological stock delimitation (e.g., Bushuev, 1990; Kaliszewska et al., 2005; Iwasa-Arai et al., 2018); give insight into hydrodynamics (e.g., Kasuya and Rice, 1970; Briggs and Morejohn, 1972; Fish and Battle, 1995; Carrillo et al., 2015; Moreno-Colom et al., 2020), assist in individual recognition (e.g., Visser et al., 2020); and act as sentinels of health status (Mackintosh and Wheeler, 1929; Van Waerebeek et al., 1993; Aznar et al., 1994; Aznar et al., 2005; Lehnert et al., 2007; Vecchione and Aznar, 2014; Lehnert et al., 2021; for more references see Results). Nonetheless, there is plently of further opportunities to exploit the full potential of these organisms as biological indicators.

Studies including information on cetacean epibionts have usually focused on particular geographical areas (e.g., Kane et al., 2008; Lehnert et al., 2019), host species (e.g., Rice, 1978; Stimmelmayr and Gulland, 2020) or epibiotic taxa (e.g., Kane et al., 2008; Iwasa-Arai and Serejo, 2018). Furthermore, in the last decades a number of nomenclatural changes, new associations, and geographical records have been accumulating, thus we think that the available comprehensive reviews and checklists on this subject (Beneden, 1870; Dailey and Brownell, 1972; Arvy, 1977; Arvy, 1982; Raga, 1994) should be updated. On the other hand, few articles have reviewed the use of marine mammal parasites as biological tags (Balbuena et al., 1995; Mackenzie, 2002), and none gathered information about the whole epibiotic fauna of cetaceans.

The present systematic review aims to compile and update all records of cetacean epibiotic fauna (= epizoites) to date as a thorough, handy catalogue for researchers. Other organisms, i.e. diatoms and cookie-cutter shark, Isistius brasiliensis (Quoy & Gaimard, 1824) are also included in a specific section of this review to provide a complete picture of other externally-associated organisms that have been proven to be valuable biological indicators for cetaceans. Finally, we identify information gaps and future research directions and highlight the value of cetacean epibionts as indicator tools, encouraging their application in cetacean research.

A systematic literature review was performed following PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines (Moher et al., 2015; Figure 1). We conducted a thorough bibliographic search in the following databases: Google Scholar (https://scholar.google.com), Scopus (https://www.scopus.com), ScienceDirect (https://www.sciencedirect.com), Web of Science (https://www.webofscience.com), and Sage (https://journals.sagepub.com). The following search string was used for Scopus, ScienceDirect, Web of Science, and Sage: (epibiont OR epibiotic OR epibiosis OR epizoite OR epizoic OR barnacle OR ectoparasite OR mesoparasite) AND (balaena OR eubalaena OR balaenoptera OR megaptera OR eschrichtius OR caperea OR cephalorhynchus OR delphinus OR feresa OR globicephala OR grampus OR lagenodelphis OR lagenorhynchus OR lissodelphis OR orcaella OR orcinus OR peponocephala OR pseudorca OR sotalia OR “Sousa chinensis” OR “Sousa plumbea” OR “Sousa sahulensis” OR “Sousa teuszii” OR stenella OR “Steno bredanensis” OR tursiops OR “Inia geoffrensis” OR kogia OR delphinapterus OR “Monodon monoceros” OR neophocaena OR phocoena OR phocoenoides OR physeter OR platanista OR pontoporia OR berardius OR hyperoodon OR mesoplodon OR tasmacetus OR ziphius OR indopacetus)

Note that the use of genus name in some cetacean genera, i.e., Monodon Linnaeus, 1758, Sousa Gray, 1866, and Steno Gray, 1846 yielded many records of unrelated taxa, thus full species name was included in these cases. The output was exported and checked for duplicates and non-relevant papers with the open-source reference management software Zotero.

In the case of Google Scholar, only the first 100 result pages are available, thus we used the search strings “(epibiont OR epibiotic OR epibiosis OR epizoite OR epizoic OR barnacle OR ectoparasite OR mesoparasite) AND i”, where i stands for a cetacean genus, to maximize the number of obtainable records. The output of each search was checked manually. In addition, we searched each epibiotic species in GBIF.org and included those associations and geographic locations that had not been reported in scientific publications. For all publications obtained, we looked up their references to search for potential missing records.

The final list includes the literature published until December 2021 that provides information on cetacean-epibiont(s) associations (Figure 1). These results are listed according to the epibiotic (see the Results) and the cetacean taxa (Supplementary Table 1). For each selected record, we extracted the following information, when available: cetacean species, epibiotic species, geographic area(s), prevalence (i.e., percent occurrence of the epibiont in each cetacean species of the sample), location on the cetacean, and any information related to indicator potential. Current species nomenclature and synonyms were checked in WoRMS (https://www.marinespecies.org/) and recent literature. Geographical locations were also classified at the scale of Large Marine Ecosystem (LME) (see e.g., Brotz et al., 2012).

For comparative purposes, we investigated research effort on each cetacean species using the number of results in Google Scholar as a proxy. For each species, we used the scientific name in quotation marks as search string. For the 6 species that previously constituted the Lagenorynchus genus (see Vollmer et al., 2019), we used the former nomenclature for the search to avoid understimation (i.e., "Lagenorynchus" followed by species name).

A total of 492 published documents, including 7 unpublished manuscripts, and 9 GBIF records were found. Three additional reliable records were serendipitously found in internet photo-catalogues and were also included in the final list (Supplementary Table 1). A roughly exponential trend in the number of publications was found throughout the period covered (1655-2021), with a peak in the 2010s decade (Figure 2); 2020 was the most productive year with 21 publications.

Baleen whales, and particularly Megaptera novaeangliae (Borowski, 1781), show the highest diversity of epibionts, followed by Tursiops spp. (Figure 3). However, it is difficult to ascertain the extent to which this pattern is affected by sampling effort (Figure 3). Likewise, 26 cetacean species from four genera have no published records of epibiotic fauna to date (Supplementary Table 1), but these hosts have also been generally little studied (< 4,000 publications in Google Scholar, Figure 3). Research effort varies also among geographic regions (Figure 4). The Mediterranean Sea and Antarctica are, by far, the geographic areas with the highest number of publications of cetacean epizoites, and some areas still lack such studies.

A systematic list of the 58 epizoic taxa (53 at species level) found to date on cetaceans follows. For each one, we provide information on (i) taxonomic synonyms; (ii) a subset of selected references that provide a complete overview of the species morphology; (iii) molecular sequences available on GenBank (https://www.ncbi.nlm.nih.gov/genbank/), with references or with Accession Number whenever no published manuscript was available; (iv) primary type of association, including parasitic (34 spp.), obligate commensal (8-9 spp.), facultative commensal (8 spp.), mutualistic (possibly 1 sp.), or unknown (2 spp.); (v) a list of cetacean hosts/basibionts; (vi) geographic range; (vii) life-cycle; and (viii) microhabitat, i.e., the location(s) on the cetacean body, with references; and (ix) indicator use or potential, with references. Any other relevant data are reported in the ‘Remarks’ section, and all records of association between epizoites and cetaceans are cited in the ‘References’ section.

The Cyamidae (‘whale lice’) comprises a group of amphipods that are found exclusively on marine cetaceans (see, e.g., Iwasa-Arai and Serejo, 2018). These 3-30 mm creatures use their pereopods to cling to areas of reduced water flow (e.g., ventral grooves, blowhole, genital slit), where they spend their whole life feeding primarily on cetacean skin (Rowntree, 1983; Rowntree, 1996; Schell et al., 2000); thus, they are all considered ectoparasites. However, evidence that they cause any harm is rather scarce, so some authors support the use of the term ‘ectocommensals’ for them (Leung, 1976; Kenney, 2009). Rowntree (1996) discussed the possibility that some cyamids from whales may also feed on plankton, having perhaps developed mutualistic associations with their hosts. In particular, the cyamid species covering the sensory hairs of whales could increase their activity during plankton blooms, amplifying the signal for prey detection by whales. In addition, it has also been suggested that cyamids could feed on cetaceans’ dead skin and epibiotic algae, thus cleaning up wounds and speeding up healing (Williams and Bunkley-Williams, 2019). Lehnert et al. (2021), on the contrary, hypothesized that cyamids’ feeding activity could actually hinder the healing of skin injuries, and some authors have suggested that heavy cyamid infections may contribute to the death of their hosts (Mignucci-Giannoni et al., 1998).

Since cyamids lack swimming stages, transmission must occur through bodily contacts (Fransen and Smeenk, 1991; Pfeiffer, 2009). Males are typically larger than females (but see Fraija-Fernández et al., 2017) and, at least in some species, have been observed to perfom pre-copulatory mate guarding (Rowntree, 1996; Oliver and Trilles, 2000). Females mate after molting (Conlan, 1991) and incubate eggs and protect the hatchling in a ventral brood pouch (Leung, 1976; Williams and Bunkley-Williams, 2019).

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Aurivillius, 1879; Vervoort and Tranter, 1961; Bannister and Grindley, 1966

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Obligate commensal

Balaenoptera borealis Lesson, 1828, B. edeni Anderson, 1878, B. musculus, B. physalus

Arctic, Atlantic, eastern Pacific, Indian Ocean, Antarctica

Aurivillius (1879) describes a nauplius and five copepodite stages preceding the adult phase. In the allied species B. manatorum nauplii and early copepodite stages are unable to swim, and copepodite V and adults can perform only short swimming excursions (Domènech et al., 2017). Thus, host bodily contact or closeness is likely necessary for transmission in both species.

Baleen plates (Aurivillius, 1879; Cocks, 1885; Lillie, 1910; Scharff, 1913; Matthews, 1938b; Vervoort and Tranter, 1961; Rice, 1963; Gambell, 1964; Bannister and Grindley, 1966; Ichihara, 1966; Ichihara, 1978; Collet, 1986; Raga and Sanpera, 1986; Dalla Rosa and Secchi, 1997; Esteves et al., 2020), corner of the mouth (Raga and Sanpera, 1986)

-

The presence of this species is likely underestimated since it can be easily overlooked without exhaustive inspection of baleen plates (Aurivillius, 1879; Vervoort and Tranter, 1961). It can sometimes be colonized by chonotrichous ciliates, acting as basibiont (Fernandez-Leborans, 2001).

Cocks, 1885; Aurivillius, 1879; Lillie, 1910; Collet, 1912; Scharff, 1913; Allen, 1916; Cornwall, 1927; Cornwall, 1928; Matthews, 1938b; Vervoort and Tranter, 1961; Rice, 1963; Gambell, 1964; Bannister and Grindley, 1966; Ichihara, 1966; Kawamura, 1969; Rice, 1977; Ichihara, 1978; Collet, 1986; Raga and Sanpera, 1986; Dalla Rosa and Secchi, 1997; Esteves et al., 2020

Family Harpacticidae Dana, 1846

Members of this family are mostly marine or brackishwater macroalgal associates, with a few freshwater species (Joon and Young, 1993).

-

Humes, 1964

-

Unknown

Tursiops truncatus

-

Unknown for this species, but naupliar and copepodite stages have been described for other Harpacticus spp. (e.g., Itô, 1976; Walker, 1981; Choi and Kim, 1994). Harpacticoids generally lack planktonic larval stages, but adults are active swimmers (e.g., Hicks, 1985; Palmer, 1988). It is thus plausible that transmission to bottlenose dolphin occurred during the adult phase.

On ulcerated and sloughed skin (Humes, 1964)

-

This species was described by Humes (1964) on captive marine mammals and has never been reported again. Species of Harpacticus Milne Edwards H., 1840 typically colonize seagrass, algal clumps or sandy and muddy bottoms (Ólafsson, 2001 and references therein), thus the occurrence of H. pulex on cetaceans is intriguing and perhaps forced by confinement conditions (Humes, 1964). Future re-examination of the taxonomic status of H. pulex is advisable.

Humes, 1964

Order Siphonostomatoida Burmeister, 1835

Family Caligidae Burmeister, 1835

The family Caligidae (“sea lice”) contains 30 genera (Walter and Boxshall, 2020); species of Caligus Müller O. F., 1785 and Lepeophtheirus Nordmann, 1832 have great economic relevance due to their impact on salmonid fish mariculture (Costello, 2006; Hemmingsen et al., 2020). Caligids use their siphon and a pair of mandibles to feed on fish skin (Kabata, 1974), causing ulcerations and even death to their hosts (Tørud and Håstein, 2008), but their impact on cetaceans has not yet been reported.

Caligus arcticus Brandes, 1956, C. kroyeri Milne Edwards, 1840, C. latifrons Wilson C.B., 1905, C. leptochilus Leuckart in Frey & Leuckart, 1847, C. lumpi Krøyer, 1863, C. rabidus Leigh-Sharpe, 1936, C. rissoanus Milne Edwards, 1840, C. trachypteri Krøyer, 1863

Hemmingsen et al., 2020 and references therein

COI (Øines and Heuch, 2005; Raupach et al., 2015; GenBank AY386272; AY386273; EF452647), 16S rRNA (Øines and Schram, 2008; GenBank AY660020), 18S rRNA (Huys et al., 2006; Øines and Schram, 2008; Mohrbeck et al., 2015; Khodami et al., 2017; GenBank JX845119-JX845131), 28S rRNA (Khodami et al., 2017; GenBank DQ180336; DQ180337; EU118301; EU118302)

Ectoparasite

Balaenoptera acutorostrata, Hyperodoon ampullatus

North Atlantic (Hemmingsen et al., 2020)

Two free-living planktonic nauplius stages, one free-swimming infective copepodid stage, and four chalimus stages and one adult stage attached to the host (Maran et al., 2013).

Skin (O’Reilly, 1998; Ólafsdóttir and Shinn, 2013)

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This is a typical fish ectoparasite that has been reported on more than 80 species (Kabata, 1979; Agusti-Ridaura et al., 2019). Infections in cetaceans are exceptional and likely related to their occurrence close to cage farms (Ólafsdóttir and Shinn, 2013). The hyperparasitic monogenean Udonella caligorum Johnston, 1835, which typically attaches to fish copepods (Freeman and Ogawa, 2010), has been found on C. elongatus infecting common minke whales (Ólafsdóttir and Shinn, 2013).

O’Reilly, 1998; Ólafsdóttir and Shinn, 2013

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Wilson, 1905; Takemoto and Luque, 2002; Kim et al., 2019

-

Ectoparasite

Tursiops truncatus

Western Atlantic (Benz et al., 2011)

See C. elongatus (above).

Skin (Benz et al., 2011)

-

This species typically infects fish, but there is an exceptional record of adult individuals, including ovigerous females, on a carcass of bottlenose dolphin (Benz et al., 2011).

Benz et al., 2011

Gloiopotes crassus Wilson & Bere, 1936

Lewis, 1967

-

Ectoparasite

Delphinus delphis

Western Atlantic, North Pacific, Indian Ocean (Lewis, 1967)

Species of Lepeophtheirus have 2-4 chalimus stages and two preadult stages. The latter can be distinguished by their ability to detach and move over the surface of the host (Krøyer, 1834; see Hamre et al., 2013).

Hyperparasitic on Remora australis (Bennett, 1840; Radford and Klawe, 1965)

-

-

Radford and Klawe, 1965

Family Pennellidae Burmeister, 1835

Unlike other families of the order Siphonostomatoida, members of the family Pennellidae do have intermediate hosts, usually a fish or invertebrate (Kabata, 1979; Nagasawa et al., 1985; Suyama et al., 2021a and references therein). Mating seemingly occurs in the intermediate host and fertilized females attach to the final host in which they produce and release the eggs (Arroyo et al., 2002).

Pennella antarctica Quidor, 1913, P. anthonyi Quidor, 1913, P. balaenopterae Koren & Danielssen, 1877, P. cettei Quidor, 1913, P. charcoti Quidor, 1913

Koren and Danielssen, 1877; Turner, 1905; Hogans, 1987, Hogans, 2017; Abaunza et al., 2001; Vecchione and Aznar, 2014; Suyama et al., 2021b

COI (Fraija-Fernández et al., 2018)

Mesoparasite. The head penetrates the blubber and musculature to feed on blood and expands as 2-3 cephalic horns in host’s tissue to enable attachment, whereas the trunk, genital complex, and abdominal plumes protrude and hang on the host body (Hogans, 1987; Abaunza et al., 2001; Schmidt and Roberts, 2009; Hogans, 2017).

Balaenoptera acutorostrata, B. bonaerensis, B. borealis, B. edeni, B. musculus, B. physalus, Delphinus delphis, Eubalaena australis, Feresa attenuata Gray, 1874, Globicephala melas, Grampus griseus, Hyperoodon ampullatus, Kogia breviceps, Lissodelphis borealis (Peale, 1848), Megaptera novaeangliae, Mesoplodon bidens (Sowerby, 1804), M. carlhubbsi Moore, 1963, M. mirus, Orcinus orca, Phocoena phocoena, Physeter macrocephalus, Stenella coeruleoalba, Tursiops truncatus, Ziphius cavirostris

Atlantic, Pacific, Mediterranean, Indian Ocean, Antarctica

Based on information from other penellids, its life cycle is believed to include a pelagic naupliar stage and several copepodid and chalimus instars on the intermediate (squid) hosts; females are fertilized as late chalimi and undergo a pelagic phase to search out the definitive host, where they metamorphose into the adult stage (Schmidt and Roberts, 2009). In the case of P. balaenoptera, only adult females and the first naupliar stage are known (Arroyo et al., 2002). However, the copepodid and chalimus stages have been described for P. filosa (Linnaeus, 1758) collected from squids (Rose and Hamon, 1953; see also Arroyo et al., 2002), and P. filosa is now considered conspecific with P. balaenoptera (Fraija-Fernández et al., 2018; see also the Discussion). The life cycle of P. balaenoptera could be primarily oceanic because this species is more prevalent on pelagic versus coastal cetaceans (Fraija-Fernández et al., 2018).

Commonly on the flanks (Raga and Sanpera, 1986; Aznar et al., 1994; Gomerčić et al., 2006; Souza et al., 2005; Ciçek et al., 2007; Foskolos et al., 2017), but occasionally reported on the head (Pouchet and Beauregard, 1889; Foskolos et al., 2017) and flukes (Foskolos et al., 2017). A single record on a whale sucker, Remora australis (Bennett, 1840) attached to a dolphin (Radford and Klawe, 1965).

It may be an indicator of compromised health in cetacean hosts (Mackintosh and Wheeler, 1929; Aznar et al., 2005; Vecchione and Aznar, 2014).

Since P. balaenoptera is the only recognized species of Pennella Oken, 1815 parasitizing cetaceans, we consider that the published records of Pennella sp. in cetaceans could be assigned to this species, unless proven otherwise. Dailey et al. (2002) reported P. balaenoptera in one northern elephant seal, Mirounga angustirostris (Gill, 1866). Recently, molecular analyses revealed that specimens of P. balaenoptera collected from several cetaceans in western Mediterranean could be conspecific with P. filosa from swordfish, Xiphias gladius Linnaeus, 1758, collected in the same area (Fraija-Fernández et al., 2018). This finding begs further attention (see the Discussion).

Steenstrup and Lütken, 1861; Sars, 1866; Pouchet and Beauregard, 1889; Anthony and Calvet, 1905; Turner, 1905; Bouvier, 1910; Japha, 1910; Mörch, 1911; Collet, 1912; Quidor, 1912; Liouville, 1913; Olsen, 1913; Scharff, 1913; Cornwall, 1927; Cornwall, 1928; Mackintosh and Wheeler, 1929; Van Oorde-de Lint and Schuurmans-Stekhoven, 1936; Matthews, 1938b; Allen, 1941; Stephensen, 1942; Mizue, 1950; Nishiwaki and Hayashi, 1950; Mizue and Murata, 1951; Nishiwaki and Oye, 1951; Ohno and Fujino, 1952; Kakuwa et al., 1953; Barnard, 1955; Chapman and Santler, 1955; Clarke, 1956; Zenkovich, 1956; Tomilin, 1957; Rice, 1963; Radford and Klawe, 1965; Kawamura, 1969; Berzin, 1972; Rice, 1977; Rice, 1978; Dailey and Stroud, 1978; Dailey and Walker, 1978; Ivashin and Golubovsky, 1978; Greenwood et al., 1979; Best, 1982; Raga and Carbonell, 1985; Raga and Sanpera, 1986; Smiddy, 1986; Mead, 1989; Bushuev, 1990; Dorsey et al., 1990; Sedlak-Weinstein, 1990 (unpubl.); Dailey and Vogelbein, 1991; Raga and Balbuena, 1993; Aznar et al., 1994; Aznar et al., 2005, unpubl.; Raga, 1994; Vecchione, 1994; Cerioni and Mariniello, 1996; Kuramochi et al., 1996; Araki et al., 1997; Kuramochi et al., 2000; McAlpine et al., 1997; Terasawa et al., 1997; Uchida, 1998; Walker and Hanson, 1999; Cornaglia et al., 2000; Uchida and Araki, 2000; Abaunza et al., 2001; Arroyo et al., 2002; Brzica, 2004; Gomerčić et al., 2006; Souza et al., 2005; Ciçek et al., 2007; Kautek et al., 2008; Martín et al., 2011; Rosso et al., 2011; Bertulli et al., 2012; Ólafsdóttir and Shinn, 2013; Tonay and Dede, 2013; Danyer et al., 2014; Öztürk et al., 2015; Delaney et al., 2016; Birincioğlu et al., 2017; Foskolos et al., 2017; Hogans, 2017; Fraija-Fernández et al., 2018; IJsseldijk et al., 2018; Marcer et al., 2019; Methion and Díaz López, 2019; Herr et al., 2020; Orrell, 2020; Ten et al., unpubl.

Subclass Cirripedia Burmeister, 1834

Order Balanomorpha Pilsbry, 1916

Family Balanidae Leach, 1817

Thoracic barnacles (Infraclass Thoracica) are sessile, hermaphroditic crustaceans that attach to diverse substrata and have specialized cirri to filter organic particles from water for feeding (Anderson, 1994). The life cycle typically includes a free-swimming nauplius larva that undergoes several (usually 6) moults, and a non-feeding cypris larva that searchs out, and attaches to, an appropriate substratum. Subsequent metamorphosis leads to a juvenile filter-feeding version of the adult (Darwin, 1854; Cornwall, 1955; Maruzzo et al., 2012). The cyprid stage is unique to barnacles and shows little morphological variability across species, even though they can attach to strikingly different substrata (Maruzzo et al., 2012; Dreyer et al., 2020).

This family originally encompassed all sessile barnacles (Leach, 1817), but whale barnacles and most sea turtles were later re-classified (Pitombo, 2004; see below). Most members of Balanidae are intertidal, although some species are facultative epibionts, e.g., those found on sea turtles, such as Balanus trigonus (Ten et al., 2019).

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Darwin, 1854

COI (Chen et al., 2013; Ashton et al., 2016; GenBank JQ035523; JQ035524; MF974362; MK308152; MK308163; MK308322; MK496572; MT258956; MW277718; MW277822), EF1a (Chan et al., 2017), RPII (Chan et al., 2017), 12S rRNA (Endo et al., 2010; Kamiya et al., 2012; Pérez-Losada et al., 2014; Chan et al., 2017; GenBank GU983669; GU983670), 16S rRNA (Chan et al., 2017; GenBank JQ035491; JQ035492), 18S rRNA (Pérez-Losada et al., 2014; Chan et al., 2017), 28S rRNA (Pérez-Losada et al., 2014), and the complete mitochondrial genome (GenBank MW646099; MZ049958; NC_056392)

Facultative commensal

Megaptera novaeangliae

Cosmopolitan (Werner, 1967)

Metamorphosis from nauplius to cyprid stage is speeded up at higher water temperature, i.e., 4-11 days (Thiyagarajan et al., 2003). Recruitment is seasonal and takes place at approximately 24°C (Lam, 2000).

As a hyperepibiont on the barnacle Coronula diadema (Cornwall, 1928)

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Cornwall, 1928

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A general account of Balanus spp. can be found in Darwin (1854); Newman and Ross (1976), and Pitombo (2004).

> 5,000 results in GenBank

Presumably facultative commensal

Megaptera novaeangliae

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Information for Balanus spp. is available from Brown and Roughgarden (1985) and Maruzzo et al. (2012).

As a hyperepibiont on the barnacle Coronula spp. (Rice, 1963)

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Balanus spp., as in Rice (1963), may correspond to a single or several species.

Rice, 1963

Balanus tintinnabulum (Linnaeus, 1758), Lepas tintinnabulum Linnaeus, 1758

Darwin, 1854; Barnard, 1924

COI (Chen et al., 2013; Ashton et al., 2016; GenBank JQ035525-JQ035527), H3 (Pérez-Losada et al., 2004), 12S rRNA (Pérez-Losada et al., 2004), 16S rRNA (Pérez-Losada et al., 2004; GenBank JQ035505-JQ035508), 18S rRNA, 28S rRNA (Pérez-Losada et al., 2004), and the complete mitochondrial genome (Che et al., 2019; GenBank MW281857; NC_056162)

Facultative commensal

Unidentified whale

Tropical or sub-tropical to warm temperate waters (Otani et al., 2007)

In the Arabian Sea, barnacles breed at lower temperatures, i.e., less than 24 °C in winter vs. > 28 °C in summer; and grow at a rate of 0.44-0.63 mm/year (Ali and Ayub, 2021).

As a hyperepibiont on the barnacle Coronula diadema (Barnard, 1924)

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Barnard, 1924

Family Coronulidae Leach, 1817

Coronulids are typically obligate epibionts of sea turtles, sirenians or cetaceans (Marlow, 1962; Hayashi et al., 2013). One species, Chelonibia testudinaria (Linnaeus, 1758), can also be found on crustaceans and sea snakes, and even on inanimate substrata (Frazier and Margaritoulis, 1990; Cheang et al., 2013).

Coronula balaenaris (Gmelin, 1791), C. complanata (Mörch, 1852)

Darwin, 1854; Pilsbry, 1916; Scarff, 1986; Pastorino and Griffin, 1996; Seilacher, 2005

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Obligate commensal

Eubalaena australis, E. glacialis

Arctic, Atlantic, eastern North Pacific, Antarctica

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Lips, fins (Guiler, 1956; Best, 1991)

Shell plate remains of C. complanatus in Nerja Cave (Málaga, southern Spain) were used as indirect evidence of whale consumption by humans in the Upper Magdalenian (Álvarez-Fernández et al., 2013) and of the presence and migration of right whales (Balaenidae) in the Mediterranean during the Early Pleistocene (Collareta et al., 2016; Bosselaers et al., 2017).

There is a single record on Megaptera novaeangliae (Guiler, 1956), but it was probably confused with Coronula reginae (Holthuis et al., 1998).

Chemnitz, 1785; Chemnitz and Martini, 1790; Darwin, 1854; Gruvel, 1903; Pilsbry, 1916; Nilsson-Cantell, 1931; Best, 1991

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Darwin, 1854; Dall, 1872; Cornwall, 1955; Scarff, 1986; Anderson, 1994

H3, 12S rRNA, 16S rRNA, 18S rRNA, 28S rRNA (Hayashi et al., 2013)

Obligate commensal

Typical from Megaptera novaeangliae but some records on Balaenoptera bonaerensis, B. borealis, B. musculus, B. physalus, Eubalaena glacialis, Hyperoodon ampullatus and Physeter macrocephalus

Atlantic, Pacific, Indian Ocean, Antarctica

A one-year life cycle has been proposed (Angot, 1951; Newman and Abbott, 1980). Larval release and settlement seem to occur in warm waters (20-25°C in September-October off Madagascar), whereas adult development may take place during whale migration to the poles (Angot, 1951). Details of development from the embryo to the juvenile stage have been studied in vitro (Nogata and Matsumura, 2006). Larval settlement is likely induced by chemical cues from whale skin, such as alpha-2-macroglobulin (Nogata and Matsumura, 2006).

Rostrum, lips, lower jaw, fins (Dall, 1872; Pilsbry, 1916; Nilsson-Cantell, 1930a, Nilsson-Cantell, 1930c; Stephensen, 1938; Scheffer, 1939; Tomilin, 1957; Scarff, 1986)

Isotope analyses (δ¹⁸O) of shells of C. diadema and its direct ancestor C. bifida (Dominici et al., 2011) accurately trace current and Pleistocene-Miocene whale migration routes (Buckeridge et al., 2018; Collareta et al., 2018a; Collareta et al., 2018b; Buckeridge et al., 2019; Taylor et al., 2019). Fossil remains have also been used to infer humpback whale migration routes and breeding areas in the Late Pliocene-Pleistocene (Bianucci et al., 2006a; Bianucci et al., 2006b). Present-day observations of Coronula sp. (Olsen, 1913; Angot, 1951) helped to elucidate right whales’ migration from warmer waters (Best, 1991). The co-occurrence of C. bifida with Cetopirus complanatus may indicate that whales belonging to Balaenopteridae and Balaenidae shared breeding grounds during the Early Pleistocene (Collareta et al., 2016). Interestingly, the presence of C. diadema on cetaceans other than humpback whales could also indicate some geographical overlap between species (see the Discussion). Coronula spp. have been suggested as natural marks for individual photo-identification (Franklin et al., 2020). The pattern of attachment of barnacles (presumably C. diadema) indicates non-uniform water flow over humpback whale flippers and has shed light on the function of leading-edge tubercles (Fish and Battle, 1995). Rubbing against rocks and the sea bottom has been observed in humpback whales, which may be an attempt to remove these barnacles (Tomilin, 1957) and could limit its application as an indicator.

This species serves as a basibiont of the facultative epibionts Balanus spp., Conchoderma auritum (Linnaeus, 1767), and Megabalanus tintinnabulum, and of the hydroid Obelia dichotoma (Linnaeus, 1758) (Liouville, 1913; Barnard, 1924; Cornwall, 1928; Stephensen, 1938; Rice, 1963; Kim et al., 2020).

Dall, 1872; Scammon, 1874; Fischer, 1884; Sars, 1890-1895; Borradaile, 1903; Liouville, 1913; Pilsbry, 1916; Cornwall, 1924; Cornwall, 1927; Cornwall, 1928; Nilsson-Cantell, 1930a; Nilsson-Cantell, 1930c, Hiro, 1935; Hiro, 1938; Stephensen, 1938; Nilsson-Cantell, 1939; Scheffer, 1939; Mizue and Murata, 1951; Rees, 1953; Tomilin, 1957; Nishiwaki, 1959; Cockrill, 1960; Wolff, 1960; Rice, 1963; Nilsson-Cantell, 1978; O’Riordan, 1979; Scarff, 1986; Paterson and Van Dyck, 1991; Young, 1991; Holthuis and Fransen, 2004; Félix et al., 2006; Nogata and Matsumura, 2006; Wirtz et al., 2006; Jones, 2010; Ávila et al., 2011; Jiménez et al., 2011; Hayashi, 2012; Angeletti et al., 2014; Kim et al., 2020; Minton et al., 2020 (in press.); Tasmanian Museum and Art Gallery, 2020; Ueda, 2020; Ten et al., unpubl.

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Darwin, 1854; Scarff, 1986

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Obligate commensal

Balaenoptera bonaerensis, B. borealis, B. musculus, B. physalus, Eubalaena glacialis, Megaptera novaeangliae; single report on Delphinapterus leucas and Physeter macrocephalus

Arctic, Atlantic, North Pacific, Indian Ocean, Antarctica

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Lower jaw, flukes (Cockrill, 1960; Scarff, 1986)

See Coronula diadema (above).

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Collet, 1912; Pilsbry, 1916; Cornwall, 1927; Cornwall, 1928; Mackintosh and Wheeler, 1929; Nilsson-Cantell, 1930a; Nilsson-Cantell, 1930b; Hiro, 1938; Stephensen, 1938; Scheffer, 1939; Rees, 1953; Guiler, 1956; Tomilin, 1957; Cockrill, 1960; Rice, 1963; Klinkhart, 1966; Kawamura, 1969; Rice, 1977; Nilsson-Cantell, 1978; Silva-Brum, 1985; Scarff, 1986; Bushuev, 1990; Smiddy and Berrow, 1992; Holthuis and Fransen, 2004; Ten et al., unpubl.

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Dall, 1872; Cornwall, 1955; Achituv, 1998; Seilacher, 2005

H3, 12S rRNA, 16S rRNA, 18S rRNA, 28S rRNA (Hayashi et al., 2013)

Obligate commensal, although Tomilin (1957) considered this species to be potentially harmful because it can impede whales’ movement and damage their skin.

Eschrichtius robustus; once reported on Delphinapterus leucas and Orcinus orca

North Pacific; one record in the Gulf of Mexico (eastern North Atlantic)

Gray whales wintering in waters off California and Mexico bear large and small specimens of C. rhachianecti when migrating northward, but only large barnacles when sighted during the southbound migration (Rice and Wolman, 1971). This would suggest that larval settlement occurs in wintering areas. This interpretation is supported by the observation that belugas held captive in San Diego Bay have C. rhachianecti in synchrony with gray whale northward migration (Rice and Wolman, 1971; Ridgway et al., 1997). Vertical shell growth is 0.12 mm/day (Killingley, 1980).

Rostrum, lips, throat, peduncle, fins (Kasuya and Rice, 1970; Briggs and Morejohn, 1972)

Isotope analysis (δ¹⁸O) and geographical patterns of occurrence of fossilized remains have helped to reveal gray whale migration routes (Killingley, 1980; Bosselaers and Collareta, 2016; Taylor et al., 2019). Small size of barnacles and other features (appearance and associated scarring) have been used to identify calves of gray whale in photo-identification studies (Bradford et al., 2011). Barnacle orientation reflects waterflow patterns on gray whales (Kasuya and Rice, 1970; Briggs and Morejohn, 1972). Greater abundance of C. rachianecti on the left side of the head of gray whales may indicate that the right side is used predominantly for benthic feeding (Kasuya and Rice, 1970). In fact, right-sided feeding bias has been observed in some cetaceans (e.g., Clapham et al., 1995; Marino and Stowe, 1997; Karenina et al., 2016), including gray whales (e.g., Woodward and Winn, 2006).

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Dall, 1872; Pilsbry, 1916; Rice, 1963; Roest, 1970; Rice and Wolman, 1971; Briggs and Morejohn, 1972; Leung, 1976; Wellington and Anderson, 1978; Sullivan and Houck, 1979; Achituv, 1998; Weller et al., 1999; Takeda and Ogino, 2005; Sokolov and Arsen'ev, 2006; Murase et al., 2014; Scordino et al., 2017; Kasuya and Rice, 1970; Killingley, 1980; Swartz, 1981; Samaras, 1989; Ridgway et al., 1997; Findley and Vidal, 2002

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Darwin, 1854; Seilacher, 2005

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Obligate commensal, although Tomilin (1957) considered this species to be potentially harmful because it can impede whales’ movement and damage their skin.

Eubalaena australis; once reported on Balaenoptera borealis and E. glacialis

Atlantic, western South Pacific, Antarctica

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Upper jaw, callosities, forehead, over the eye (Pilsbry, 1916; Scarff, 1986)

Shell plate remains of T. major found in Nerja Cave (Málaga, southern Spain) were used as indirect evidence of whale consumption by humans in the Upper Magdalenian (Álvarez-Fernández et al., 2013).

Reported as a basibiont of facultative epibionts of the genus Conchoderma (Liouville, 1913).

Worm, 1655; Marloth, 1900; Gruvel, 1903; Liouville, 1913; Pilsbry, 1916; Reeb et al., 2007

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Darwin, 1854; Cornwall, 1955; Rajaguru and Shantha, 1992; Anderson, 1994; Seilacher, 2005

COI (Pérez-Losada et al., 2014), H3, 12S rRNA, 16S rRNA, 18S rRNA, 28S rRNA (Hayashi et al., 2013)

Obligate commensal

Balaenoptera acutorostrata, B. bonaerensis, B. borealis, B. edeni, B. musculus, B. physalus, Delphinus delphis, Feresa attenuata, Globicephala macrorhynchus, G. melas, Grampus griseus, Kogia sp., Lagenodelphis hosei Fraser, 1956, Lissodelphis borealis, Megaptera novaeangliae, Mesoplodon bidens, M. mirus, Neophocaena asiaeorientalis Pilleri & Gihr, 1972, N. phocaenoides (Cuvier, 1829), Orcinus orca, Peponocephala electra, Phocoena phocoena, P. sinus Norris & McFarland, 1958, P. spinnipinnis (Burmeister, 1865), Physeter macrocephalus, Pontoporia blainvillei, Pseudorca crassidens, Sagmatias obliquidens (Gill, 1865), S. obscurus, Sotalia fluviatilis (Gervais & Deville in Gervais, 1853), S. guianensis (Van Beneden, 1864), Sousa plumbea (G. Cuvier, 1829), Stenella attenuata, S. clymene, S. coeruleoalba, S. frontalis (Cuvier, 1829), S. longirostris, Steno bredanensis, Tursiops aduncus, T. truncatus, Ziphius cavirostris

Cosmopolitan (Arctic, Atlantic, Pacific, Mediterranean, South China Sea, Indian Ocean, Antarctica)

Under experimental conditions at 28°C, the nauplii develop into cyprids in c. 8 days of hatching (Dreyer et al., 2020). Cyprids are similar to those of other barnacles but show variation in the structures that contact the substratum (Dreyer et al., 2020). In Guiana dolphins, Sotalia fluviatilis, off southern Brazil, field observations suggest that barnacle growth rate is initially fast and slows down after c. 30 days; sexual maturity seems to be reached in 40-45 days, and life span does not exceed one year (Flach et al., 2021).

Trailing edge of dorsal fin, pectoral flippers, and mostly tail flukes (Calman, 1920; Barnard, 1924; Cornwall, 1927; Cornwall, 1928; Pope, 1958; Caldwell et al., 1971; Devaraj and Bennet, 1974; Bryden, 1976; Rice, 1978; Greenwood et al., 1979; Bane and Zullo, 1980; Spivey, 1980; Raga et al., 1983b; Ross, 1984; Raga and Sanpera, 1986; Brownell et al., 1987; Mead and Potter, 1990; Rajaguru and Shantha, 1992; Van Waerebeek et al., 1993; Watson et al., 1994; Jefferson et al., 1995; Reyes and Van Waerebeek, 1995; Araki et al., 1997; Orams and Schuetze, 1998; Rittmaster et al., 1999; Vidal et al., 1999; Barros and Stolen, 2001; Parsons et al., 2001; Resendes et al., 2002; Berland et al., 2003; Di Beneditto and Ramos, 2004; Palacios et al., 2004; Kane et al., 2008; Bearzi and Patonai, 2010; Best and Meÿer, 2010; Carvalho et al., 2010; Ribeiro et al., 2010; Foote et al., 2011; Karaa et al., 2011; Martín et al., 2011; Oliveira et al., 2011; Rosso et al., 2011; Díaz-Aguirre et al., 2012; González et al., 2012; Ólafsdóttir and Shinn, 2013; Towers et al., 2013; Whitehead et al., 2014; Díaz-Gamboa, 2015; Kim and Sohn, 2016; Methion and Díaz López, 2019; Pacheco et al., 2019; Herr et al., 2020; Matthews et al., 2020; Siciliano et al., 2020; Visser et al., 2020; Flach et al., 2021); also reported on the head (Samaras, 1989; Engel, 1994) and on a facial lesion (Alves-Motta et al., 2020).

The high detectability of X. globicipitis from visual surveys makes it applicable for individual marking of cetaceans (Visser et al., 2020) and as a multifaceted indicator. First, differences in its prevalence have been used to trace cetacean long-distance migrations (Best, 1982; Bushuev, 1990; Matthews et al., 2020; Ten et al., unpubl.) and to discriminate ecological stocks (Kawamura, 1969; Bushuev, 1990; Toth et al., 2012; Towers et al., 2013; Urian et al., 2019; Silva et al., 2020) and climate change-derived shifts in cetacean distribution (Visser et al., 2020). Second, its settlement patterns on hosts, which seem mainly driven by water flow, have been used to investigate cetacean swimming and hydrodynamics (Carrillo et al., 2015; Moreno-Colom et al., 2020). Lastly, the higher prevalence on immunosuppressed hosts highlights its potential as an indicator of health status in cetacean populations (Aznar et al., 1994; Aznar et al., 2005).

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Steenstrup, 1852; Darwin, 1854; Hoek, 1883; True, 1890; Richard and Neuville, 1897; Weltner, 1897; Gruvel, 1905; Gruvel, 1912; Collet, 1912; Liouville, 1913; Gruvel, 1920; Calman, 1920; Nilsson-Cantell, 1921; Barnard, 1924; Broch, 1924; Cornwall, 1927; Cornwall, 1928; Mackintosh and Wheeler, 1929; Nilsson-Cantell, 1930a; Richard, 1936; Matthews, 1938b; Heldt, 1950; Cornwall, 1955; Pope, 1958; Rice, 1963; Zullo, 1963; Stubbings, 1965; Pilleri, 1967; Dollfus, 1968; Kawamura, 1969; Pilleri and Gihr, 1969; Pilleri and Knuckey, 1969; Pilleri, 1970; Rice, 1977; Rice, 1978; Caldwell et al., 1971a; Devaraj and Bennet, 1974; Brownell, 1975; Mead, 1975; Bryden, 1976; Spivey, 1977; Dailey and Walker, 1978; Greenwood et al., 1979; Bane and Zullo, 1980; Spivey, 1980; Raga et al., 1982; Raga et al., 1983b; Ross, 1984; Raga and Carbonell, 1985; Gittings et al., 1986; Raga and Sanpera, 1986; Brownell et al., 1987; Rappé, 1988; Rappé and Van Waerebeek, 1988; Pinedo et al., 1989; Samaras, 1989; Bushuev, 1990; Mead and Potter, 1990; Van Waerebeek et al., 1990; Young, 1991; Duignan et al., 1992; Rajaguru and Shantha, 1992; Aguilar and Raga, 1993; Raga and Balbuena, 1993; Van Waerebeek et al., 1993; Aznar et al., 1994; Aznar et al., 2005; Aznar et al., 2016, unpubl.; Engel, 1994; Fertl, 1994; Watson et al., 1994; Jefferson et al., 1995; Reyes and Van Waerebeek, 1995; Azevedo et al., 1996; Fertl et al., 1996; Araki et al., 1997; Orams and Schuetze, 1998; Uchida, 1998; Rittmaster et al., 1999; Vidal et al., 1999; Di Beneditto and Ramos, 2001; Guerrero-Ruiz and Urbán, 2000; Kuramochi et al., 2000; Uchida and Araki, 2000; Addink and Smeenk, 2001; Barros and Stolen, 2001; Parsons et al., 2001; Danilewicz et al., 2002; Louella and Dolar, 2002; Resendes et al., 2002; Berland et al., 2003; Di Beneditto and Ramos, 2004; Karuppiah et al., 2004; Palacios et al., 2004; Watson and Gee, 2005; Bellido et al., 2006; Sakai et al., 2006; Best, 2007; Pitman et al., 2007; Toth-Brown and Hohn, 2007; Kane et al., 2008; Kautek et al., 2008; Rotstein et al., 2009; Sakai et al., 2009; Bearzi and Patonai, 2010; Best and Meÿer, 2010; Carvalho et al., 2010; Ribeiro et al., 2010; Weir, 2010; Foote et al., 2011; Karaa et al., 2011; Martín et al., 2011; Oliveira et al., 2011; Rosso et al., 2011; Bertulli et al., 2012; Díaz-Aguirre et al., 2012; González et al., 2012; Hayashi, 2012; Pugliese et al., 2012; Toth et al., 2012; Ólafsdóttir and Shinn, 2013; Towers et al., 2013; Lane et al., 2014; Whitehead et al., 2014; Díaz-Gamboa, 2015; Carrillo et al., 2015; Blum and Fong, 2016; Prestridge, 2016; Kim and Sohn, 2016; Denkinger and Alarcon, 2017; Donnelly et al., 2018; Ronje et al., 2018; Cortés-Peña, 2019; Methion and Díaz López, 2019; Pacheco et al., 2019; Urian et al., 2019; Alves-Motta et al., 2020; Gagnon and Torgersen, 2020; Gómez-Hernández et al., 2020; Herr et al., 2020; Matthews et al., 2020; Minton et al., 2020 (in press); Minussi, 2020; Moreno-Colom et al., 2020; Natural History Museum, 2020; Orrell, 2020; Siciliano et al., 2020; Silva et al., 2020; Ueda, 2020; Vargas-Bravo et al., 2020; Visser et al., 2020; CW Azores, 2021; Flach et al., 2021; iNaturalist, 2021; Ten et al., unpubl.

Order Scalpellomorpha Buckeridge & Newman, 2006

Family Lepadidae Darwin, 1852

Lepadids are oceanic fugitive species with relatively rapid growth and require a hard substratum to settle (e.g., Skerman, 1958; Patel, 1959; Southward, 1987; Harper, 1995; Hinojosa et al., 2006; Fraser et al., 2011; Wegner and Cartamil, 2012; Frick and Pfaller, 2013; Schiffer and Herbig, 2016). Overall, they are generalistic settlers on floating objects, be living or inanimate. This feature makes it often difficult to ascertain whether settlement on putative basibionts is pre- or postmortem (e.g., Magni et al., 2015; Ten et al., 2019). However, some degree of specialization for living cetaceans seems to be apparent especially for Conchoderma auritum (see below). Apart from cetaceans, other basibionts for species of Lepas and Conchoderma are, inter alia, bull kelps (Fraser et al., 2011; López et al., 2017), sea turtles (Ten et al., 2019), and even human corpses (Magni et al., 2015). Extensive description of the metamorphosis for species of this family is provided by Darwin (1854).

Conchoderma leporinum Olfers, 1814, Lepas aurita Linnaeus, 1767, Otion stimpsoni Dall, 1872

Darwin, 1854; Dall, 1872; Monod, 1938; Cornwall, 1955

COI (Ashton et al., 2016; GenBank MT563423; MT563438; MT563441), H3 (Pérez-Losada et al., 2008), 12S rRNA (Endo et al., 2010), 16S rRNA (Tomioka et al., 2020), 18S rRNA, 28S rRNA (Pérez-Losada et al., 2008)

Facultative commensal. However, Newman and Abbott (1980) considered that this species might actually be an obligate commensal on cetaceans because most records of this species involve, as substrata, the shells of coronulid barnacles and/or on exposed hard surfaces of these mammals, e.g., baleens or tusks of ziphids. Rasmussen (1980) postulated that C. auritum prefers hard substrates in motion, although this species has also been reported on animate objects (see below).

Balaenoptera acutorostrata, B. bonaerensis, B. borealis, B. musculus, B. physalus, Berardius bairdii, Eschrichtius robustus, Eubalaena glacialis, Feresa attenuata, Globicephala macrorhynchus, G. melas, Hiperoodon ampullatus, H. planifrons, Megaptera novaeangliae, Mesoplodon bidens, M. densirostris (de Blainville, 1817), M. europaeus, M. hectori (Gray, 1871), M. layardii (Gray, 1865), M. mirus, M. stejnegeri True, 1885, Neophocaena phocaenoides, Peponocephala electra, Physeter macrocephalus, Pontoporia blainvillei, Stenella attenuata, S. frontalis, S. longirostris, Tursiops aduncus, T. truncatus, Ziphius cavirostris

Cosmopolitan

Growth rate of metamorphosed individuals are available only from inanimate substrata (0.1-1.0 mm/day; Il'in et al., 1978; Rasmussen, 1980; Dalley and Crisp, 1981). At a mean temperature of 23°C, the capitulum of newly recruited individuals can reach 1 mm long in just two days, and 6 mm in 9 days; in older individuals, growth rate estabilizes at 0.55 mm/day (Dalley and Crisp, 1981). Cyprids of C. auritum sampled along the Atlantic Ocean were found in low concentration between 25° N and 34 °S (Dalley and Crisp, 1981).

On baleen plates (Nilsson-Cantell, 1930a; Nilsson-Cantell, 1939; Omura, 1950a; Christensen, 1985; Raga and Sanpera, 1986; Ólafsdóttir and Shinn, 2013); odontocete teeth (Beneden, 1870; Ohlin, 1893; Lillie, 1910; Hamilton, 1914; Broch, 1924; Nansen, 1925; Nilsson-Cantell, 1930a; Nilsson-Cantell, 1930c; Gauthier, 1938; Monod, 1938; Nilsson-Cantell, 1939; Scheffer, 1939; Fabian, 1950; Mizue, 1950; Omura, 1950a; Omura et al., 1955; Sergeant and Fisher, 1957; Tomilin, 1957; Wolff, 1960; Marlow, 1963; Rice, 1963; Morris and Mowbray, 1966; Pilleri, 1969a; Pilleri, 1969b; Caldwell et al., 1971b; Van Bree, 1971; Fordyce et al., 1979; Dixon, 1980; Baker, 1983; Pastene et al., 1990; Balbuena, 1991; Debrot, 1992; Rodríguez-López and Mignucci-Giannoni, 1999; Soto, 2001; O’Connor and Franco, 2003; Bermúdez-Villapol et al., 2006; Van Waerebeek et al., 2008; Holmes and Franco, 2010; Martín et al., 2011; Bachara and Gullan, 2016; Foskolos et al., 2017; Tomioka et al., 2020), and on the coronulid barnacles C. diadema (Beneden, 1870; Dall, 1872; Sars, 1880; Gruvel, 1911; Mörch, 1911; Liouville, 1913; Borradaile, 1916; Pilsbry, 1916; Broch, 1924; Cornwall, 1924; Cornwall, 1927; Cornwall, 1928; Nilsson-Cantell, 1930a; Nilsson-Cantell, 1930c; Hiro, 1935; Stephensen, 1938; Nilsson-Cantell, 1939; Scheffer, 1939; Tomilin, 1957; Rice, 1963; Clarke, 1966; Newman and Ross, 1971; Holthuis and Fransen, 2004; Kim et al., 2020), C. reginae (Nilsson-Cantell, 1930a; Nilsson-Cantell, 1939; Wolff, 1960; Rice, 1963; Clarke, 1966; Newman and Ross, 1971), and X. globicipitis (Ten et al., unpubl.). Also, on deformed or injured jaws that leave the teeth exposed (Davis, 1874; Mörch, 1911; Matthews, 1938c; Chapman and Santler, 1955; Clarke, 1956; Nasu, 1958; Cockrill, 1960; Wolff, 1960; Slijper, 1962; Spaul, 1964; Clarke, 1966; Pilleri, 1969b; Beach, 2015). Once recorded as an hyperepibiont on P. balaenoptera (Nilsson-Cantell, 1930a).

Holmes and Franco (2010) observed several individuals of C. auritum on the left tooth of Sowerby’s beaked whale, Mesoplodon bidens, but none on the right tooth. These authors speculated that the barnacles could indicate some type of chirality during feeding, which may hinder barnacle development on the right side (see Cryptolepas rachianecti above). On the other hand, the presence of C. auritum has been suggested as an indicator of previous interaction of cetaceans with fisheries since these barnacles can attach on scarred mouth injuries (Beach, 2015; Welch, 2017). Finally, knowledge of growth rates of C. auritum makes this species potentially suitable to make temporal calibrations of time since settlement. This could inform on basibiont movements or interaction with fisheries (see, e.g., Dalley and Crisp, 1981; Wegner and Cartamil, 2012; Zettler, 2021), although this application has not been used yet in cetaceans.

Also recorded on inanimate substrata (e.g., ship hulls, moorings, ropes; Foster and Willan, 1979; Rasmussen, 1980; Farrapeira et al., 2007) and elephant seals, Mirounga spp. (Best, 1971; Joseph et al., 1986).

Bennet, 1837; Bennett, 1840; Hallas, 1868; Beneden, 1870; Dall, 1872; Davis, 1874; Sars, 1880; Ohlin, 1893; Lillie, 1910; Gruvel, 1911; Mörch, 1911; Collet, 1912; Liouville, 1913; Hamilton, 1914; Allen, 1916; Borradaile, 1916; Pilsbry, 1916; Broch, 1924; Cornwall, 1924; Hinton, 1925; Nansen, 1925; Cornwall, 1927; Cornwall, 1928; Mackintosh and Wheeler, 1929; Nilsson-Cantell, 1930a; Nilsson-Cantell, 1930c; Matthews, 1937; Matthews, 1938c; Gauthier, 1938; Hiro, 1938; Monod, 1938; Stephensen, 1938; Nilsson-Cantell, 1939; Scheffer, 1939; Fabian, 1950; Mizue, 1950; Omura, 1950a; Omura, et al., 1955; Angot, 1951; Ohno and Fujino, 1952; Kakuwa et al., 1953; Rees, 1953; Chapman and Santler, 1955; Clarke, 1956; Sergeant and Fisher, 1957; Tomilin, 1957; Nasu, 1958; Symons and Weston, 1958; Cockrill, 1960; Wolff, 1960; Sergeant, 1962; Slijper, 1962; Marlow, 1963; Rice, 1963; Spaul, 1964; Clarke, 1966; Morris and Mowbray, 1966; Perrin, 1969; Pilleri, 1969b; Newman and Ross, 1971; Van Bree, 1971; Monod and Serene, 1976; Fordyce et al., 1979; Dixon, 1980; Baker, 1983; Christensen, 1985; Raga and Sanpera, 1986; Mead, 1989; Bushuev, 1990; Pastene et al., 1990; Bordino and González, 1992; Debrot, 1992; García-Godos, 1992; Raga and Balbuena, 1993; Mignucci-Giannoni et al., 1998; Rodríguez-López and Mignucci-Giannoni, 1999; Huang et al., 2000; Soto, 2001; O’Connor and Franco, 2003; Holthuis and Fransen, 2004; Bermúdez-Villapol et al., 2006; Van Waerebeek et al., 2008; Holmes and Franco, 2010; Ávila et al., 2011; Martín et al., 2011; Ólafsdóttir and Shinn, 2013; Angeletti et al., 2014; Insacco et al., 2014; Beach, 2015; Elorriaga-Verplancken et al., 2015; Bachara and Gullan, 2016; Foskolos et al., 2017; Iwasa-Arai et al., 2017b; Wheeler and McIntosh, 2018; Kim et al., 2020; Natural History Museum, 2020; Tomioka et al., 2020; Ueda, 2020; Ten et al., unpubl.

Conchoderma virgata (Spengler, 1790), Lepas virgata Spengler, 1790

Darwin, 1854; Nilsson-Cantell, 1928

COI (Chen et al., 2013), H3 (Pérez-Losada et al., 2008), 12S rRNA (Endo et al., 2010), 18S rRNA (Pérez-Losada et al., 2008; Yusa et al., 2012), 28S rRNA (Pérez-Losada et al., 2008)

Facultative commensal

Balaenoptera acutorostrata, B. bonaerensis, B. borealis, B. musculus, B. physalus, Delphinus delphis, Feresa attenuata, Megaptera novaeangliae, Neophocaena phocaenoides, Physeter macrocephalus, Stenella coeruleoalba

Cosmopolitan

Most growth rate estimates of this species have been studied on inanimate substrata (0.1-1.5 mm/day; Darwin, 1851; Annandale, 1909; MacIntyre, 1966; Tsikhon-Lukanina et al., 1977; Il'in et al., 1978; Dalley and Crisp, 1981). For instance, at a mean temperature of 23°C and 14 days after metamorphosis, individuals grew 0.66 mm/day on an experimental torpedo (Dalley and Crisp, 1981). Eckert and Eckert (1987) provide a von Bertalanffy’s growth equation obtained from C. virgatum measurements on nesting sea turtles, which shows an asymptotic trend comparable to that of previous studies. Differences in growth rate estimates and maximum size between studies suggest an effect of the ecological conditions (Eckert and Eckert, 1987).

Mostly as a hyperepibiont of Pennella balaenoptera (Sars, 1866; Koren and Danielssen, 1877; Turner, 1905; Nilsson-Cantell, 1930a; Clarke, 1956; Clarke, 1966; Raga and Sanpera, 1986; Araki et al., 1997; Terasawa et al., 1997; Uchida, 1998; Ólafsdóttir and Shinn, 2013), but it can also attach directly to odontocete teeth (Lillie, 1910; Aznar et al., 1994). Once reported on C. auritum (Clarke, 1966), Neocyamus physeteris (Oliver and Trilles, 2000), and on the shell of Xenobalanus globicipitis (Ten et al., unpubl.).

Knowledge of growth rates of C. virgatum makes this species potentially suitable to make temporal calibrations of time since settlement (see C. auritum). Indeed, unusual attachment of C. virgatum and Lepas spp. on dolphin teeth may have occurred after dolphin death, when teeth remain exposed (Aznar et al., 1994). This provides the opportunity to infer the approximate time of death, as it has been done in sea turtles (Ten et al., 2019). The finding of Conchoderma sp. (presumably C. virgatum) attached to a marlin spear that was inserted into the jaw of an Antarctic minke whale suggested that spearing occurred a few months before the finding (Ohsumi, 1973). Lastly, its presence and size has been used as an indicator of oceanic habitat use by sea turtles (Casale et al., 2004; Casale et al., 2012; Ten et al., 2019) and of interaction with pelagic fisheries (Wegner and Cartamil, 2012; Ten et al., 2019).

It is typical settler of inanimate substrata, e.g., ship vessels, buoys (Foster and Willan, 1979; Farrapeira et al., 2007; González et al., 2012; Wegner and Cartamil, 2012), but also attaches to multiple marine animals, including fish (e.g., Crozier, 1916; Hastings, 1972; Ohsumi, 1973), sea turtles (e.g., Eckert and Eckert, 1987; Alonso et al., 2010), elephant seals (Joseph et al., 1986), sea snakes (Annandale, 1909; Yamato et al., 1996), and pelagic crabs (Jerde, 1967; Moazzam and Rizvi, 1979). It has also been reported as a hyperepibiont of fish copepods (e.g., Williams, 1978; Williams and Williams, 1986).

Sars, 1866; Koren and Danielssen, 1877; Turner, 1905; Lillie, 1910; Collet, 1912; Liouville, 1913; Mackintosh and Wheeler, 1929; Nilsson-Cantell, 1930a; Clarke, 1956; Clarke, 1966; Kawamura, 1969; Berzin, 1972; Rice, 1977; Greenwood et al., 1979; Raga and Carbonell, 1985; Raga and Sanpera, 1986; Bushuev, 1990; Aguilar and Raga, 1993; Aznar et al., 1994, unpubl.; Araki et al., 1997; Terasawa et al., 1997; Uchida, 1998; Huang et al., 2000; Kuramochi et al., 2000; Oliver and Trilles, 2000; Uchida and Araki, 2000; Ólafsdóttir and Shinn, 2013; Ten et al., unpubl.

Lepas hillii (Leach, 1818)

Darwin, 1854; Cornwall, 1955

-

Facultative commensal

Once reported on Stenella coeruleoalba

Pantropical (González et al., 2012)

At temperatures ca. 25 °C, individuals attached to a ship in central Atlantic Ocean reached maturity after 30-43 days for a capitulum 13-17 mm long (i.e., a growth rate of 0.5 mm/day; Evans, 1958). Similarly as in Conchoderma spp. (see above), growth was asymptotic and fell to 0.03 mm/day after maturity (Evans, 1958).

Teeth (Aznar et al., 1994)

Deeper knowledge of growth rates of L. hillii would refine estimates of time since settlement (see C. virgatum). Some applications include the estimation of the time of death of basibionts (Aznar et al., 1994; Ten et al., 2019), interaction with fisheries (Wegner and Cartamil, 2012; Ten et al., 2019), and oceanic habitat use (Casale et al., 2004; Casale et al., 2012; Ten et al., 2019).

On inanimate substrata, e.g., buoys, ship hulls, a rope (Il'in et al., 1978; Dalley and Crisp, 1981; Farrapeira et al., 2007; Wegner and Cartamil, 2012) and on marine vertebrates, including fish (Dulčić et al., 2015), sea turtles (Domènech et al., 2015; Ten et al., 2019), and elephant seals (Joseph et al., 1986).

Aznar et al., 1994

Lepas pectinata Spengler, 1793

Darwin, 1854; Cornwall, 1955

COI (Chen et al., 2013; Schiffer and Herbig, 2016; Aguilar et al., 2018; Rech et al., 2018; GenBank KY639421-KY639424; MF974366-MF974369), H3 (Pérez-Losada et al., 2008), 18S rRNA (Pérez-Losada et al., 2008; Schiffer and Herbig, 2016), 28S rRNA (Pérez-Losada et al., 2008)

Facultative commensal

Stenella coeruleoalba

Cosmopolitan (González et al., 2012)

This is the most abundant lepadid in the Northeast Atlantic, where its development has been studied (Ellis et al., 1983; Conway et al., 1990). Interestingly, L. pectinata presumably performs ontogenetic depth migrations, i.e., nauplii feed in the upper 150 m and the non-feeding cyprids distribute at 300-400 m (Conway et al., 1990). Nauplii show similar feeding and swimming features as other barnacle larvae (Moyse, 1984).

Teeth (Aznar et al., 1994)

See L. hillii (above).

Closely associated to Sargassum spp. weed (Fine, 1970; Conway et al., 1990); also found on inanimate substrata (e.g., floating crude oil, plastic debris; Horn et al., 1970; Minchin, 1996; Bergami et al., 2021) and on sea turtles (Domènech et al., 2015; Ten et al., 2019).

Aguilar and Raga, 1993; Aznar et al., 1994

Phylum Chordata Haeckel, 1874

Class Actinopteri Cope, 1871

Subclass Teleostei Müller, 1846

Order Carangiformes Jordan, 1963

Family Echeneidae Rafinesque, 1810

Remoras or diskfishes include 8 species of specialized teleosts that use their dorsal fin as an adhesive disc to attach to a great variety of marine vertebrates from which they benefit through, e.g., ventilation, protection from predators, and increased contact with conspecifics (Fertl and Landry, 1999a; Fertl and Landry, 1999b). The fact that remoras live in association with elasmobranchs, teleosts, sea turtles, and cetaceans (Cressey and Lachner, 1970) has hampered research on basic biological features such as growth and reproduction for most species (Battaglia et al., 2016).

Echeneis chiromacer Duméril, 1858, E. fasciata Gronow, 1854, E. fusca Gronow, 1854, E. guaican Poey, 1860, E. lunata Bancroft, 1831, E. metallica Poey, 1860, E. naucratus Linnaeus, 1758, E. neucrates Linnaeus, 1758, E. scaphecrates Duméril, 1858, E. vittate Rüppell, 1838, Echensis naucrates Linnaeus, 1758, Echneis naucrates Linnaeus, 1758, Leptecheneis flaviventris Seale, 1906, L. naucrates (Linnaeus, 1758)

Collette, 2003; Skaramuca et al., 2009

> 40,000 results in GenBank

Facultative commensal

Sotalia guianensis, Tursiops truncatus

Cosmopolitan (Collette et al., 2015)

In the eastern Gulf of Mexico females show slower growth but achieve larger size than males; spawning takes place in August (Bachman et al., 2018).

Flanks and both dorsal and ventral sides

-

It can free swim in the water column while feeding on small fishes and plankton (O’Toole, 2002), but also attach to a broad spectrum of basibionts, including reef teleosts, sharks, and sea turtles (O’Toole, 2002; Sazima and Grossman, 2006; Gray et al., 2009), nearshore dolphins (above), and even to conspecifics (Brunnschweiler and Sazima, 2006). It is considered a sister-species of E. neucratoides (O’Toole, 2002).

Fertl and Landry, 1999b; Fertl et al., 2002; Noke, 2004; Santos and Sazima, 2005

-

-

COI (GenBank KF461171), EGR1, EGR2B, EGR3 (Campbell et al., 2013), ITS1 (Gray et al., 2009), ND2 (Gray et al., 2009), RAG1, RH1 (Campbell et al., 2013), VCPIP, ZIC1 (Betancur et al., 2013), 5.8S rRNA, 12S rRNA, 16S rRNA, 18S rRNA (Gray et al., 2009)

Presumably facultative commensal

Two unidentified cetaceans

Western Atlantic Ocean (Fertl and Landry, 1999a; Fertl and Landry, 1999b)

-

-

-

Typical commensal of sharks and once observed on a West Indian manatee captured in Puerto Rico (Mignucci-Giannoni et al., 1999).

O’Toole, 2002

Echeneis australis Bennett, 1840, E. scutata Günther, 1860, Remilegia australis (Bennett, 1840), Remora australia (Bennett, 1840), R. scutata (Günther, 1860)

Rice and Caldwell, 1961

COI (GenBank GU440495; OK030822), CYTB (Sanciangco et al., 2016), ITS1, ND2 (Gray et al., 2009), RAG1 (GenBank EU167871), 5.8S rRNA, 12S rRNA, 16S rRNA, 18S rRNA (Gray et al., 2009)

Obligate commensal/mutualist. Although previously considered as an obligate commensal (Rice and Caldwell, 1961), later evidence has shown that this species can feed on host’s ectoparasites (O’Toole, 2002). However, remoras may potentially disrupt the flow over cetaceans’ body, increasing drag, and their sucking disk may produce irritation (Fish et al., 2006).

Balaenoptera borealis, B. edeni, B. musculus, Delphinus delphis, Orcinus orca, Physeter macrocephalus, Stenella attenuata, S. frontalis, S. longirostris, Tursiops truncatus

eastern Pacific, Atlantic, Indian Ocean, Indonesian Sea

Off Brazil, remoras of the smallest size class (i.e., < 10 cm) were the most abundant size class in May and their frequency fell until none were reported in October (Wingert et al., 2021).

Ubiquitous on skin (Wingert et al., 2021)

Remoras on blue whales preferentially attach to regions with reduced drag. Therefore, they could evince patterns of water flow over swimming whales, which could optimize tag deployment for extended ecological monitoring (Flammang et al., 2020).

The records from B. edeni, O. orca, S. attenuata, and T. truncatus above provide only identification to genus level, but are here assigned to R. australis since it is the only species of Remora associated to cetaceans (O’Toole, 2002). Individuals of R. australis appear to disengage from whales during whaling (Pike, 1951; Rice and Caldwell, 1961), which might result in gross underestimations of actual prevalence in nature. Prior to towing, the prevalence of R. australis on blue whales, Balaenoptera musculus, captured in California and Peru was close to 100 percent (Rice and Caldwell, 1961). Attachment marks of this species on the host’s epidermis are superficial, and scarring is not typically observed (Rice and Caldwell, 1961; Visser, pers. obs.). There is a single record of two copepod hyperparasites on R. australis, namely Pennella balaenoptera and Lepeophtheirus crassus (Radford and Klawe, 1965).

Carl and Wilby, 1945; Cadenat, 1953; Krefft, 1953; Follet and Dempster, 1960; Mahnken and Gilmore, 1960; Rice and Caldwell, 1961; Rice, 1963; Radford and Klawe, 1965; Rice, 1977; Rice, 1978; Notarbartolo di Sciara and Watkins, 1979; Fertl and Landry, 1999a; Fertl and Landry, 1999b; Wingert et al., 2021

Order Siluriformes -

Family Trichomycteridae Bleeker, 1858

Catfishes (Siluriformes) are widely distributed in freshwater, estuarine, and marine habitats of continental shelves (de Pinna, 1998). Members of the family Trichomycteridae, known as pencil or parasitic catfishes (de Pinna and Wosiacki, 2003), inhabit continental freshwaters from Costa Rica to Patagonia (de Pinna and Wosiacki, 2003; Eschmeyer et al., 2017).

-

Araújo-Wang et al., 2019

COI, CYTB, H3, ND4, MYH6, RAG1, RAG2, 12S rRNA, and 16S rRNA of three Ochmacanthus spp. (see GenBank)

Presumably obligate commensal

Inia geoffrensis (Blainville, 1817)

South American rivers (Koch, 2002)

-

On lateral and ventral surfaces (Araújo-Wang et al., 2019)

-

Candirus are generally commensal on various freshwater fishes (Adriaens et al., 2010), but Araújo-Wang et al. (2019) reported year-round observations on Inia geoffrensis.

Araújo-Wang et al., 2019

Entosphenus epihexodon Gill, 1862, E. tridentatus tridentatus (Richardson, 1836), Lampetra tridentatus (Richardson, 1836), Petromyzon astori Girard, 1858, P. ciliatus Ayres, 1855, P. epihexodon (Gill, 1862), P. lividus Girard, 1858, P. tridentatus Richardson, 1836

Creaser and Hubbs, 1922

COI (Yamazaki et al., 2006; April et al., 2011; Carim et al., 2017; GenBank GU440367; KF918874; KF918875; KF929845; KY570333), CR (GenBank AY205567), CYTB (Docker et al., 1999; Lorion et al., 2000; Yamazaki et al., 2006; Boguski et al., 2012; GenBank DW022992; GQ206157; KR422618; KR422619; KU672473-KU672485), ETR-1, ETR-2, ETR-3, ETR-4, ETR-5, ETR-6 (Spice et al., 2011), GnRH-III (Silver et al., 2004), ND1, ND2, ND4, ND5 (Docker et al., 2007), RT (GenBank AJ244558), 12S rRNA (GenBank LC091545; LC091546), 16S rRNA (GenBank KJ010762), and the whole genome (Hess et al., 2020)

Ectoparasite

Balaenoptera borealis, B. musculus, B. physalus, Berardius bairdii, Megaptera novaeangliae, Physeter macrocephalus

North Pacific, from Baja California north to the Bering and Chukchi seas and westward into Russia and Japan, showing the greatest latitudinal range of any lamprey (Renaud, 2011)

Laboratory observations hypothesized that the time of residence in the ocean is ≤ 3.5 years (Beamish, 1980). Movements in the ocean are poorly understood, but they are typically caught between the surface and 500 m (see Clemens et al., 2019).

-

Based on the degree of healing of the marks of Pacific lampreys on several species of whales, Pike (1951) inferred that lamprey attacks took place during the northward migration in the North Pacific. Therefore, marks could be used to trace whale’s migration.

Typically parasitizes fish (Clemens et al., 2019).

Carl, 1950; Pike, 1951; Nemoto, 1955; Rice, 1963; Rice, 1977; Rice, 1978

Ammocoetes bicolor Lesueur, 1818, Batymyzon bairdii (Gill, 1883), Lampetra marina (Linnaeus, 1758), Oceanomyzon wilsoni Fowler, 1908, Petromyzon adriaticus Nardo, 1847, P. americanus Lesueur, 1818, P. bairdii Gill, 1883, P. concolor Wright, 1892, P. lampetra Pallas, 1814, P. maculosus Gronow, 1854, P. marinus dorsatus Wilder, 1883, P. marinus unicolor Gage, 1928, P. maximus Cuvier, 1816, P. nigricans Lesueur, 1818, P. ruber Lacepède, 1800

Creaser and Hubbs, 1922

> 193,000 results in GenBank

Ectoparasite, inferred from resulting wounds and scars (Silva et al., 2014)

Balaenoptera acutorostrata, B. borealis, B. physalus, Eubalaena glacialis, Grampus griseus, Megaptera novaeangliae, Mesoplodon bidens, Orcinus orca, Physeter macrocephalus, Tursiops truncatus, Ziphius cavirostris

Atlantic coast of North America and Europe, including the central Mediterranean Sea (Holčík et al., 2004; Kottelat and Freyhof, 2007)

This hematophagous species grows to adult size in 1 year; the complete metamorphosis and reproduction takes 1.5 years (Silva et al., 2013).

Flanks of middle and posterior body areas (Bertulli et al., 2012; Ólafsdóttir and Shinn, 2013)

In some cases, the individuals are still attached to the host when found, being easier to detect (Nichols and Hamilton, 2004; Nichols and Tscherter, 2011; Samarra et al., 2012; Miočić-Stošić et al., 2020). In others, however, only the remaining marks are visible. The applicability of these marks is still to be determined. Samarra et al. (2012) stated that they apparently disappear within 1 year, whereas Miočić-Stošić et al. (2020) claim that they are seemingly short-lived, thus not being suitable markings in photo-identification. In the past years, it has been more commonly found in Icelandic waters, and this change in distribution seems to be due to a gradual increase in water temperatures around Iceland (Astthorsson and Palsson, 2006).

This species is often found on freshwater and marine fishes (Collette and Klein-MacPhee, 2002).

Japha, 1910; Collet, 1912; Nichols and Hamilton, 2004; Nichols and Tscherter, 2011; Rosso et al., 2011; Bertulli et al., 2012; Samarra et al., 2012; Ólafsdóttir and Shinn, 2013; Silva et al., 2014; Bertulli et al., 2016; Miočić-Stošić et al., 2020

Phylum Cnidaria Hatschek, 1888

Class Hydrozoa Owen, 1843

Subclass Hydroidolina Collins, 2000

Order Leptothecata Cornelius, 1992

Family Campanulariidae Johnston, 1836

Members of this family of thecate hydroids are ubiquitous in marine benthic communities. Given that the morphology of colonies and polips are highly variable within species, it is difficult to find diagnostic morphological characters to separate congeneric species (Cunha et al., 2015), which may hinder correct identification to species level.

Multiple; see Schuchert (2021).

Orejas et al., 2012

COI (Govindarajan et al., 2006; Cunha et al., 2015; Cunha et al., 2017; GenBank MG791815; MW277711; MW277730; MZ580517; MZ580890), calmodulin (Govindarajan et al., 2006), LSU rRNA (Pruski and Miglietta, 2019; Penney and Rawlings, 2021; GenBank MG786561; MG786562), SSU rRNA (MG792325), 5.8S rRNA (Cunha et al., 2015), 16S rRNA (Bridge et al., 1995; Govindarajan et al., 2006; Cunha et al., 2015; Cunha et al., 2017; Rech et al., 2018), 18S rRNA, 28S rRNA (Bridge et al., 1995; Govindarajan et al., 2006; Cunha et al., 2015; Maronna et al., 2016; Cunha et al., 2017)

Unknown, although a commensalist or even mutualistic association cannot be ruled out since newly released medusae of this species are bacteriophagous (Boero et al., 2007).

Once reported on Megaptera novaeangliae

Nearly cosmopolitan (Orejas et al., 2012)

Kubota (1999) reported the complete life cycle of O. dichotoma in Northern Japan.

As a hyperepibiont on the barnacle Coronula diadema (Cornwall, 1928)

-

It can be found on hard substrata, such as floats, pilings, rocks, and shells (Orejas et al., 2012).

Cornwall, 1928

-

Cornelius (1990) provides extensive descriptions of European Obelia spp.

> 400 results in GenBank

Unknown

Once reported on Megaptera novaeangliae

-

See Cornelius (1990).

As a hyperepibiont on Coronula spp. (Rice, 1963)

-

-

Phylum Nematoda Cobb, 1932

Class Chromadorea Inglis, 1983

Subclass Chromadoria Pearse, 1942

Order Monhysterida Filipjev, 1929

Family Monhysteridae de Man, 1876

This family is composed of terrestrial, freshwater, and marine forms. Some species are free-living in the sediment (e.g., Fonseca and Decraemer, 2008), bacterivorous on plants (Alkemade et al., 1992), associated to pack ice (Blome and Riemann, 1999) or living epibiotically on crustaceans in marine, limnetic, and terrestrial habitats (Lorenzen, 1986).

-

Roussel de Vauzème, 1834; Baylis, 1923; Lorenzen, 1986

-

Obligate commensal; it probably feeds primarily on organic particles from whales’ diet (Baylis, 1923).

Balaenoptera borealis, B. musculus, B. physalus, Eubalaena australis, Megaptera novaeangliae

Atlantic, North Pacific, Antarctica

Eggs are laid on the baleen plates but, since no larval stages have been found on cetaceans, further development may take place in the sea (Baylis, 1923).

Baleen plates (Roussel de Vauzème, 1834; Baylis, 1923; Skrjabin, 1959; Rice, 1963; Lorenzen, 1986), in association with the ciliated protozoon Haematophagus megaptere Woodcock & Lodge, 1921 (Baylis, 1923).

-

Considered a taxon inquirendum (WoRMS, 2021).

Roussel de Vauzème, 1834; Baylis, 1923; Skrjabin, 1959; Rice, 1963; Lorenzen, 1986

The present review includes records covering over three and a half centuries, a fact that attests to the curiosity that cetacean epibionts have sparked among naturalists, probably due to their often bizarre appearance and conspicuousness. As a result, a reasonable account of the associations between cetaceans and their metazoan epibionts has been achieved. However, important biases and gaps still remain. First of all, the vast majority of studies has not primarily focused on epibiosis and thus provides little quantitative information on these associations. For instance, less than a quarter (110 out of 493) of the publications in this review include data on prevalence. This ‘quantitative gap’ problem is worsened by the selective ‘picking’ of positive records, i.e., there is a tendency to report on the occurrence, but not on the absence, of epibionts in descriptive surveys on cetaceans. Consequently, it can be difficult to draw accurate pictures of the degree of specificity and, especially, geographic distribution of epizoic taxa. Another source of bias concerns epibiont size. Studies on large, visible barnacles such as Xenobalanus globicipitis are far more numerous than those focusing on minute creatures such as Balaenophilus unisetus (Badillo et al., 2007) or species of Cyamidae infecting dolphins (Fraija-Fernández et al., 2017). The genetic information available also varies among epibiotic taxa: 28 out of 54 species lack sequenced genetic material. Among these, some are poorly known species, but others have a long study history and numerous records (e.g., Odontobius ceti vs. Coronula reginae).

There is also an uneven coverage and research effort on cetaceans as basibionts, which can result in somewhat biased impressions on epibiont diversity among cetaceans. For instance, baleen whales as a group exhibit the greatest epibiont diversity most likely because they are large, slow-swimming hosts with a number of skin folds and callosities that provide suitable microhabitats for epibiont settlement (Berzin and Vlasova, 1982; see Fraija-Fernández et al., 2017). Moreover, the occurrence of certain epibionts on whales (e.g., coronulids) promotes the settlement and/or population growth of others (e.g., lepadids, cyamids), acting as pioneers (e.g., Matthews, 1937; Rice, 1963). However, mysticetes also are a well-studied cetacean group and, not surprinsingly, only the pygmy right whale, Caperea marginata (Gray, 1846), and Omura’s whale, Balaenoptera omurai Wada et al., 2003, described in 2003 (Wada et al., 2003), still lack records of epibiotic fauna. Conversely, odontocetes may exhibit relatively poor epizoic fauna because many of them (e.g., delphinids) are fast-swimming hosts with small, smooth surfaces. Moreover, there are riverine dolphins, i.e. species of Inia, Neophocaena, Orcaella, Platanista, and Sotalia that can seldom, if at all, be exposed to epibiotic taxa of marine origin. Research effort is also low for many odontocetes, and no studies are indeed available from species of Orcaella Gray, 1866, Platanista Wagler, 1830, and Tasmacetus Oliver, 1937. The overall point is, therefore, that epibiotic richness in the less studied cetaceans likely has an unassessed degree of underestimation.

The spatial distribution of data is also heterogeneous. First, records from oceanic waters are far less common than those from coastal areas. Second, most geographic records concentrate in the Southern Ocean, Mediterranean Sea, off South Africa, and California, followed by other Northern Pacific regions (Eastern waters and Japan) and the North Sea. However, other vast areas have few surveys, or even none, including the Arctic, Black Sea, Red Sea, Indian Ocean (except South African waters), and the Southwestern Pacific and adjacent seas (e.g., Sulu-Celebes Sea). In this context, it is worth noting that the higher number of records in particular regions does not necessarily result from higher epizoite diversity or abundance, but rather from higher sampling effort. Whaling was a fundamental source of data but focused mainly on areas and seasons where the target species occurred at higher densities, e.g., Antarctic whaling during the austral summer or Saldanha and Durban whaling stations in South Africa (see Findlay and Best, 2016; IWC, 2021). Also, the Mediterranean and U.S. stranding networks have been working for several decades (Becker et al., 1994), while other areas have recently started to gather data on cetaceans (e.g., the Western Indian Ocean region; Plön et al., 2020) or lack active stranding or research programs (i.e., eastern Russian Arctic).

Finally, we still know very little about biology of the epibiotic fauna of cetaceans; a problem which results, at least in part, from the difficulties of dealing with organisms that depend on marine hosts whose accessibility is often limited due to economical, logistic, and legal constraints for sampling. We call this the ‘association gap’; we often do not know basic aspects of many epibiont taxa, such as the complete life cycle or the actual nature of the interactions (commensal, parasitic or mutualistic).

The origin of epibiotic associations of some animal groups with cetaceans is an exciting evolutionary issue since this epibiont fauna was acquired after the ancestors of these mammals colonized the sea (Aznar et al., 2001). Thus, there are instances of a simple use of cetaceans as additional substrata for facultative epibionts such as the Lepadidae (Newman and Abbott, 1980); host-switching events from prior obligate associations with other marine vertebrates, resulting in co-speciation, e.g., the Coronulidae (Frick et al., 2011; Hayashi et al., 2013; Buckeridge et al., 2019) and, perhaps, B. unisetus (Badillo et al., 2007); or putative colonization without speciation, e.g., in the case of Pennella balaenoptera (Fraija-Fernández et al., 2018). As far as we are aware, the Cyamidae could represent the only case of a potential primary adaptation to parasitism on cetaceans from a putative marine free-living ancestor (see Lowry and Myers, 2013). The nature of each type association brought about a variable degree of modifications in morphology, dependency of host/basibiont, and life history traits yet to be investigated in detail (see, e.g., Pugliese et al., 2012; Dreyer et al., 2020, for the case of X. globicipitis). These features define the potential of each epibiont as a tool to uncover aspects of cetaceans’ biology. In what follows, we condense the key biological data shown above for the main epibiotic groups, i.e., amphipods, cirripeds, and copepods; we also summarize their use as indicators. Other members of the epibiotic fauna of cetaceans are certainly interesting from ecological and evolutionary points of view, e.g., the roundworm Odontobius ceti or the whalesucker Remora australis. However, their usefulness as indicators are, in principle, more limited, and will not be further discussed here.

The level of host specificity varies greatly among whale lice species; some species have been reported only, or preferentially, on single cetacean species (e.g., Cyamus boopis, C. catodontis, C. ceti, C. eschrichtii, Neocyamus physeteris) or clades (e.g., Balaenocyamus balaenopterae, C. erraticus, C. gracilis), whereas others appear to be more generalist (e.g., Syncyamus aequus). The combination of bodily transmission and high specificity makes cyamids especially useful to shed light on phylogeography and social interactions of cetaceans (see references above). Moreover, cyamids can outlive their host for several days, thus providing a rough proxy of the time of death of cetaceans (Leung, 1976; Lehnert et al., 2007). However, when dealing with stranded cetaceans (a common scenario nowadays), these parasites can readily dislodge from hosts, which represents a potential drawback if quantitative infection data are to be used (Fraija-Fernández et al., 2017).

All epibiotic barnacles of cetaceans are filter-feeders whose life cycle includes a series of planktotrophic naupliar stages followed by a non-feeding cyprid, which permanently attaches to the basibiont (Darwin, 1851; Anderson, 1994; Høeg et al., 2003). Coronulids typical from whales tend to be selective and preferentially settle on single host species. For instance, Coronula diadema is associated to humpback whales (ca. 70% of records of C. diadema) and occurs on nearly all whales examined in surveys (Nishiwaki, 1959; Rice, 1963). In contrast, the basal representative of coronulids colonizing cetaceans, namely, Xenobalanus globicipitis, has been found on a total of 41 odontocete and mysticete species worldwide. The actual and potential indicator value of coronulids are thus defined by the commensal mode of feeding, the strict dependence on cetacean epidermis for attachment, and the variable degree of basibiont specificity. Species of this family have been used to unveil hydrodynamic features of cetaceans (Kasuya and Rice, 1970; Fish and Battle, 1995; Carrillo et al., 2015; Moreno-Colom et al., 2020) or systemic disease (Aznar et al., 1994; Aznar et al., 2005; Flach et al., 2021). However, their utility to inform on other aspects of cetacean biology, particularly movements and stock identification, are still far from full exploitation. For instance, Bushuev (1990) found significant differences of prevalence of X. globicipitis on Antartic minke whales from different Antarctic sectors, and interpreted them as evidence that whales used different wintering areas and did not mix in the Southern Ocean. However, this interpretation relies on the untested assumption that barnacle recruitment can only occur at low latitudes.

The second group of barnacles occurring on cetaceans, i.e., members of the Lepadidae, includes generalist dwellers on any type of hard substrata available in oceanic waters (e.g., Farrapeira et al., 2007; Wegner and Cartamil, 2012). Perhaps the most interesting species in this respect is Conchoderma auritum because, as noted above, it tends to be associated to cetaceans, either directly (on teeth) or indirectly (via the shell of coronulids, or the body of the mesoparasite P. balaenoptera). This raises the interesting question over the extent to which individuals of C. auritum recognize cetaceans as preferential substrata, and whether their populations depend on these basibionts for long-term stability. In any event, lepadids are fast-growing organisms that can be amenable for observational and experimental studies to determine their growth rate at different temperatures (Evans, 1958; Rasmussen, 1980; Dalley and Crisp, 1981; Eckert and Eckert, 1987; Inatsuchi et al., 2010). This makes them suitable as indicators of drifting time of their ‘living platforms’ (Fraser et al., 2011; Magni et al., 2015; López et al., 2017; Ten et al., 2019), and other aspects yet to be explored in cetaceans.

Two copepods have also developed intimate associations with cetaceans. Balaenophilus unisetus occurs on the baleen plates of four Balaenoptera spp. and is believed to feed on baleen’s keratin (or the associated microfilm) as an obligate commensal (Vervoort and Tranter, 1961; Ogawa et al., 1997; Fernandez-Leborans, 2001; Badillo et al., 2007). Interestingly, available evidence for the congeneric species B. manatorum suggests that direct contact is necessary for transmission of Balaenophilus spp. (Domènech et al., 2017). This feature has allowed to draw striking inferences on unexpected contacts between otherwise solitary juveniles of marine turtles (Domènech et al., 2017). However, the indicator value of B. unisetus seems much more limited because accessibility to whale samples is very restricted.

Females of the world-largest known copepod, Pennella balaenoptera, act as mesoparasite of at least 24 cetacean species, penetrating the blubber and musculature to feed on blood (Schmidt and Roberts, 2009; Hogans, 2017). Recent evidence has shown that there are not clear diagnostic morphological traits to differentiate this species from its congener P. filosa except for the use of different hosts (Abaunza et al., 2001; Hogans, 2017). Moreover, molecular data do not support segregation between specimens collected from cetaceans and the swordfish in the western Mediterranean (Fraija-Fernández et al., 2018). Pennella filosa parasitizes a broad spectrum of large marine fishes in the oceanic realm (Román-Reyes et al., 2019 and references herein). Apparently, then, the occurrence of P. balaenoptera (= filosa) in oceanic cetaceans could have resulted from and co-accommodation of the parasite on further hosts sharing the same habitat. However, this conclusion should be confirmed by analyzing more specimens of P. balaenoptera collected from other fish and cetaceans in other geographical regions. This is paramount because both P. balaenoptera and P. filosa exhibit low host specificity, contrary to other members of the family Pennellidae, which infect one or two hosts (Hogans, 2017). Thus, the possibility that cryptic speciation have occurred in P. balaenoptera (= filosa) cannot be ruled out. This taxonomic issue is also relevant to assess the usefulness of P. balaenoptera as an indicator species. So far, the species has been used as an indicator of host’s health status, i.e., heavy loads of this parasite could reflect poor health of the affected cetacean (Vecchione and Aznar, 2014). However, population inferences are more dependent on whether or not fishes should be included as part of the actual host community supporting the local population of P. balaenoptera (= filosa).