Can a Terrestrial Ectoparasite Disperse with Its Marine Host?

Abstract

One of the most extreme examples of parasite adaptation comes from terrestrial ectoparasites exploiting marine hosts. Despite the ubiquity of such ectoparasitism and its ecological and evolutionary importance, investigations of the responses of ectoparasites to conditions encountered on their hosts are rare. In the case of penguins and their ticks, current understanding suggests that ticks freely parasitize their hosts on land but are incapable of surviving extended oceanic journeys. We examined this conjecture by assessing the physiological capacity of little penguin ticks to endure at-sea foraging and dispersal events of their hosts. Survival in penguins ticks was not significantly compromised by exposure to depths commonly associated with host dives (40 and 60 m), repeated seawater exposure relevant to the most common (30 s) and longest (120 s) recorded host dives, or extended (48 h) exposure to seawater. Mean (5SD) closed-phase durations in adult and nymphal ticks exhibiting discontinuous gas exchange (339 5 237 and 240 5 295 s, respectively) exceeded that of the maximum recorded host dive duration (120 s). Normoxic-anoxicnormoxic respirometry also confirmed spiracle closure. Mean metabolic rates (0:354 5 0:220 and 4:853 5 4:930 mL/h at 257C for unfed and fed adult females, respectively) were significantly influenced by temperature; optimal and LT 50 temperatures for adult ticks and fed nymphal ticks were typically higher than swimming penguin body temperatures. These findings suggest that marine host dispersal is unlikely to present an insurmountable barrier to long-distance tick dispersal. Such dispersal has important implications for evolutionary theory, conservation, and epidemiology.

Tandem host‐parasite dispersal inferred from similarities in phylogeographical patterns among Little Penguins and their ‘terrestrial’ ectoparasites

“…Our results support our hypotheses that Little Penguin ticks are host-species specific, and that they are capable of considerable aquatic dispersal in association with their hosts. These results are consistent with previous fine-scale genetic studies (McCoy et al, 2012;McCoy, Chapuis, et al, 2005;Moon et al, 2015), and a recent study of Little Penguin tick physiological tolerances (Moon et al, 2019), but are the first to indicate penguin-associated tick movement between landmasses separated by thousands of kilometres of open ocean. Although the ticks showed greater phylogeographical structure than their hosts-which may be due, in part, to the higherresolution markers used in this study, or as a result of the tendency of parasites to show higher levels of genetic structure than hosts (e.g.…”

“…For example, Kangaroo and Troubridge Islands in South Australia are only separated by ~60 km of open ocean, and were found to share a single, panmictic tick population. Movement between these colonies is well‐supported by the physiological capabilities of Little Penguin ticks, and, based on average swimming speeds of Little Penguins (1.8 m/sec: Bethge, Nicol, Culik, & Wilson, ), dispersal between them could be achieved by a swimming penguin in under an hour (Moon et al, ). Likewise, population assignments and phylogenetic analyses of the ticks at Oamaru (New Zealand), Wedge Island (Tasmania) and Phillip Island (Victoria) colonies also provide evidence for immigration.…”

“…Penguin ticks might be transported by other means, too, such as oceanic rafting (Thiel & Gutow, 2005). Such a mechanism seems considerably less plausible than transport with penguins, however, especially given evidence that these ticks can survive conditions encountered during penguin dives (Moon et al, 2019) and because the ticks do not, to our knowledge, usually occupy littoral habitats independently of their hosts.…”

“…We here carried out a broad-scale phylogenomic assessment of Little Penguin ticks from throughout their range. Based on physiological analyses suggesting Little Penguin ticks can survive some time at sea (Moon et al, 2019), which would facilitate co-diversification, we hypothesised that they would show similar phylogeographic structure to their hosts, supporting their capacity to survive lengthy ocean trips. Based on previous research (as outlined above), we also hypothesised that Little Penguin ticks would be distinct from ticks on sympatric flighted seabirds.…”

Local, but not long-distance dispersal of penguin ticks between two sub-Antarctic islands

“…Dispersal of penguins among colonies, however, necessarily involves aquatic movement, which may restrict tick dispersal (Pugh 1997, Dietrich et al 2011; ticks are generally not found on penguins returning from foraging trips (Pugh 1997). A recent physiological study has found that little penguin ticks I. eudyptidis and I. kohlsi around Australasia can tolerate some conditions faced at sea (e.g., immersion in seawater for a few days and to penguin dive depths; Moon et al 2019a), and phylogeographic work suggests at-sea movement is occurring occasionally at the scale of 10s to 100s of kilometers (Moon et al 2019b). The capacity of the more generalist and widespread Ixodes uriae ticks to disperse with penguin hosts over short or long distances remains, however, largely unknown.…”