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Gall-Forming Protistan Parasites Infect Southern Bull Kelp Across the Southern Ocean, with Prevalence Increasing to the South

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Gall-Forming Protistan Parasites Infect Southern Bull Kelp Across the Southern Ocean, with Prevalence Increasing to the South Vol. 583: 95–106, 2017 MARINE ECOLOGY PROGRESS SERIES Published November 16 https://doi.org/10.3354/meps12346 Mar Ecol Prog Ser OPEN ACCESS Gall-forming protistan parasites infect southern bull kelp across the Southern Ocean, with prevalence increasing to the south Callum Blake1, Martin Thiel2,3,4, Boris A. López2,5, Ceridwen I. Fraser1,* 1Fenner School of Environment and Society, Australian National University, Building 141 Linnaeus Way, Acton, ACT 2601, Australia 2Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile 3Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile 4Centro de Estudios Avanzados en Zonas Áridas, CEAZA, Coquimbo, Chile 5Departamento de Acuicultura y Recursos Agroalimentarios, Universidad de Los Lagos, Av. Fuchslocher 1305, Osorno, Chile ABSTRACT: Protistan pathogens can have devastating effects on marine plants, yet the processes that affect their distributions and infection intensities are poorly understood. Species within the brown algal genus Durvillaea are major ecosystem engineers throughout the sub-Antarctic and cold-temperate Southern Hemisphere, and a newly described genus of protistan parasite, Maullinia, was recently found infecting D. antarctica in Chile. We set out to address 3 key ques- tions. (1) Is there evidence for trans-oceanic dispersal of Maullinia? (2) Does Maullinia infect other Durvillaea species? (3) Does infection prevalence vary throughout the hosts’ ranges? We sampled Maullinia on Durvillaea populations along coasts in Chile (D. antarctica, from 32° to 42° S: 8 sites), Australia (D. potatorum and D. amatheiae, from 36° to 38° S: 5 sites) and sub-Antarctic Marion Island (46° 53’ 47’’ S, 37° 43’ 32’’ E). We used a genetic marker (18S rRNA) to verify the presence of Maullinia on Durvillaea at all sites and visual surveys of Maullinia galls to assess infection preva- lence in Chile and Australia. We confirm that Maullinia infects Australian Durvillaea species, but our results indicate that each host species is parasitised by a different Maullinia lineage. Maullinia infection prevalence increased with latitude. Long- and short-distance dispersal events are inferred to have occurred based on genetic patterns. We conclude that Maullinia protists are broadly distributed and affect multiple host species, including at least 3 Durvillaea species (2 in Australia, and 1 in both Chile and Marion Island), and that environmental factors influence host susceptibility to infection. KEY WORDS: Pathogen · Macroalgae · Host-specificity · Intertidal · Dispersal · Durvillaea · Maullinia INTRODUCTION potentially leading to ecosystem collapse (see Mou - ritsen et al. 2005, Collinge et al. 2008). As such, The infection intensities and geographic ranges of understanding the factors shaping parasite biogeog- many parasitic organisms are expected to increase raphy and patterns of infection is an important part of under forecast scenarios of environmental change predicting how ecosystems will respond to global (Eggert et al. 2010, Gleason et al. 2013). These in - environmental change. creases may prove devastating where infections Large algae (e.g. kelps) are critical components of affect keystone species at low trophic levels, even many shallow marine ecosystems as both food and © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 96 Mar Ecol Prog Ser 583: 95–106, 2017 habitat for diverse organisms (Jones et al. 1997). The virulence in natural populations are not. The only susceptibility of marine algae to pathogen infection Maullinia recorded on Durvillaea appears likely to can be influenced by factors including population be a newly recognised species (‘Maullinia sp.’ in density, tissue damage and life stage (Andrews Goecke et al. 2012; now M. braseltonii: Murúa et al. 1976). Analyses of kelp pathosystems have also re - 2017). Although Australian Durvillaea populations vealed evidence for a molecular basis to host resist- have not yet been confirmed to host Maullinia, galls ance, whereby some species or genetic lineages of resembling those of the parasite were observed at marine algae are more prone to infection than others Sorrento in southern Australia several decades ago (Carius et al. 2001, Gachon et al. 2009, 2010). Marine (Jahnke 1978), and samples of M. ectocarpii were pathogen and parasite infections may in crease along confirmed by Maier et al. (2000) on local populations environmental gradients (e.g. depth, longitude and of Ectocarpus siliculosus. latitude), and their distributions and intensities can D. antarctica is able to raft long distances and has indicate dispersal routes and barriers, and biogeo- even been known to wash up on Australian shores, graphical regions (Rohde 2002). 1000s of km from the nearest source population Durvillaea is a brown algal genus comprising large, (Moore & Cribb 1952). We hypothesised that Maul - keystone species inhabiting rocky intertidal and linia would thus have a broad distribution and that shallow subtidal shores in the Southern Hemisphere. distant populations — possibly even those affecting In Australia, 2 Durvillaea species occur: D. amatheiae other host species — would show evidence of connec- is found along the south-eastern coasts of New South tivity. We further hypothesised that infection preva- Wales, Victoria and Tasmania, and D. potatorum lence would vary along latitudinal gradients, with along the coasts of eastern South Australia, western the greatest infection prevalence toward the north- Victoria and Tasmania (Fraser et al. 2009, Weber et ern limits of the hosts’ ranges, where kelps are most al. 2017). D. antarctica is not found in Australia but physiologically stressed (e.g. Tala et al. 2016). We has a broad, circumpolar distribution that includes tested these hypotheses using ecological and genetic the sub-Antarctic islands, New Zealand and much of surveys of infected Durvillaea along the southern the coast of Chile (Fraser et al. 2010). The species is Australian and southern-central Chilean coasts. highly buoyant and dispersive, and has previously been inferred to have transported an endophytic algal parasite, Herpodiscus durvillaeae, across the MATERIALS AND METHODS Pacific Ocean (Fraser & Waters 2013). Maullinia is a recently identified genus of phyto- Sample collection myxean parasite that can infect several brown algal genera including Macrocystis, Ectocarpus and Aci - Sampling was conducted in Australia, Chile and neto spora (Maier et al. 2000, Goecke et al. 2012). The sub-Antarctic Marion Island (Fig. 1). Australian sam- microscopic organisms produce motile zoospores pling and surveys were carried out at 5 sites: Tathra, which disperse and infect new hosts, causing gall- City Rock, Mallacoota, Cape Conran and Cape like hypertrophies of host tissue (Neuhauser et al. Schanck. In Chile, intertidal sampling was carried 2011). The production of resting spores may enable out at 8 sites: Pichicuy, Quintay, Pichilemu, Cura- the parasite to disperse long distances and survive nipe, Queule, Chaihuin, Hua Huar and Pumillahue. adverse conditions (Neuhauser et al. 2011). While Infected tissue from Marion Island was collected some research has described phytomyxids, including opportunistically from 3 sites: Macaroni Bay, Trypot Maul linia, as parasites that infect hosts without Beach and Rockhopper Bay. All sampling occurred in directly leading to mortality (Neuhauser et al. 2014), late spring and summer 2015/16. For visual quantifi- on flexible species such as D. antarctica the forma- cation of infections in the field (Australia and Chile tion of galls has been suggested to reduce the host’s only), morphological identification of galls was based ability to survive in high-energy wave environments on descriptions in Aguilera et al. (1988), Jahnke (Eggert et al. 2010). In laboratory cultures, Maullinia (1978) and Goecke et al. (2012). Infection prevalence ectocarpii was also found to heavily infect the game- was quantified along a series of 10 m transects. Num- tophytes of algal species such as Macrocystis pyrifera bers of kelp transect−1 varied within and between (Maier et al. 2000), which could reduce the reproduc- sites, leading to differing sample sizes at each loca- tive potential of its host. The host range, life cycle tion (Table 1). Three transects site−1 were surveyed in and infection pathway of M. ectocarpii are relatively Australia, and 3 to 5 transects site−1 were surveyed in well characterised, but the factors shaping its Chile, depending on the extent and accessibility of Blake et al.: Protistan parasites of southern bull kelp 97 Fig. 1. (A) Global projection of Antarctica and sub-Antarctic areas, showing the main marine currents and the location of sub-Antarctic Marion Island. The study areas on (B) the Australian coast, (C) the Chilean coast and (D) Marion Island and their local marine currents are also indicated. Black dots indicate sampling and survey sites. The geographic distribution of Durvillaea antarctica along the Chilean coast is indicated Table 1. Sampling and sequencing information for intertidal sites visited Country Site Individuals Samples Samples Samples Number of surveyed collected amplified sequenced unique sequences Australia Tathra 63 8 4 4 2 City Rock 63 2 2 2 1 Mallacoota 79 9 9 9 1 Cape Conran 64 7 4 3 1 Cape Schanck 125 12 7 4 2 Chile Pichicuy 112 4 1 1 1 Quintay 133 17 8 4 2 Pichilemu 158 10 4 4 4 Curanipe 76 4 3 2 1 Queule 164 2 2 2 2 Chaihuin 144 24 14 5 3 Hua Huar 317 24 13 7 4 Pumillahue 145 32 18 7 4 kelp beds. Transect lines were laid on rocky plat- parallel to one another. Rather, they were laid on the forms partially or completely emergent at low tide. edges of such platforms, separated by at least 2 m if As Durvillaea species often inhabit fragmented rocky on the same platform, where kelp are likely to expe- platforms composed of a number of reefs separated rience similar exposure to environmental factors by water, it was not always possible to lay transects between sites.
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