Nearly all marine animals harbor epibionts, organisms living on their body surfaces. The positive or negative effects that epibionts have on their hosts depend on many factors, including the size and location of the epibionts on their host. The present study examined the effects of epibionts on gas exchange, locomotion, and drag of three species of Antarctic sea spiders (pycnogonids). Sea spiders are a cosmopolitan group of marine arthropods that lack gills and rely instead on the diffusion of oxygen directly across their cuticle. Encrusting epibionts, such as bryozoans and algae, had only minor effects on surface oxygen levels, but they reduced the functional diffusion coefficient of oxygen through the cuticle by about half. Although these effects are significant locally and may be severe in individuals with high coverage by epibionts, the total coverage on most individuals was not high enough to significantly alter oxygen fluxes into the animal. Macroepibionts, such as barnacles, had no effect on host walking speeds, but they increased by two-to-threefold the drag experienced by host sea spiders. This likely increases the energetic costs of walking and increases the chance of being dislodged by high currents. These results suggest that epibionts can impose diverse costs to their hosts but only in subtle ways that depend on total epibiont coverage of the host and rates of water flow.
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Arnaud F, Bamber RN (1987) The biology of Pycnogonida. Adv Mar Biol 24:1–96
Avolio C, Shine R, Pile AJ (2006) The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am Nat 167:728–738
Botton ML (2009) The ecological importance of horseshoe crabs in estuarine and coastal horseshoe crabs in estuarine and coastal communities: a review and speculative summary. In: Tanacredi JT, Botton ML, Smith D (eds) Biology and conservation of horseshoe crabs. Springer, USA, pp 45–63
Burnett LE, Holman JD, Jorgensen DD, Ikerd JL, Burnett KG (2006) Immune defense reduces respiratory fitness in Callinectes sapidus, the Atlantic blue crab. Biol Bull 211:50–57
Buschbaum C, Reise K (1999) Effects of barnacle epibionts on the periwinkle Littorina littorea (L.). Helgol Mar Res 53:56–61
Christie AO, Dalley R (1987) Barnacle fouling and its prevention. In: Southward AJ (ed) Barnacle biology. A. A. Balkema, Rotterdam, pp 419–433
Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (Online)
Davenport J, Blackstock N, Davies DA, Yarrington M (1987) Observations on the physiology and integumentary structure of the Antarctic pycnogonid Decolopoda australis. J Zool 211:451–465
Dejours P (1981) Principles of comparative respiratory physiology. Elsevier/North-Holland Biomedical Press, Amsterdam, p 265
Denny MW (1993) Air and water: the biology and physics of life’s media. Princeton University Press, Princeton, p 341
Eschweiler N, Buschbaum C (2011) Alien epibiont (Crassostrea gigas) impacts on native periwinkles (Littorina littorea). Aquat Inv 6(3):281–290
Gannon AT, Wheatly MG (1992) Physiological effects of an ectocommensal gill barnacle, Octolasmis muelleri, on gas exchange in the blue crab Callinectes sapidus. J Crustacean Biol 12:11–18
Garner YL, Litvaitis MK (2017) Effects of artificial epibionts on byssogenesis, attachment strength, and movement in two size classes of the blue mussel, Mytilus edulis. Invertebr Biol 136(1):15–21
Gordon I (1932) Pycnogonida. Discov Rep 6:1–138
Hedrick TL (2008) Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 3:1–6
Jackson BE, Evangelista DJ, Ray DD, Hedrick TL (2016) 3D for the people: multi-camera motion capture in the field with consumer-grade cameras and open source software. Biol Open 5:1334–1342
Jeffries WB, Voris HK, Yang CM (1982) Diversity and distribution of the pedunculate barnacle Octolasmis in the seas adjacent to Singapore. J Crustacean Biol 2:562
Key MM Jr, Jeffries WB, Voris HK, Yang CM (1996) Epizoic bryozoans, horseshoe crabs, and other mobile benthic substrates. Bull Mar Sci 58:368–384
Key MM Jr, Knauff JB, Barnes DKA (2013) Epizoic bryozoans on predatory pycnogonids from the South Orkney Islands, Antarctica: “If you can’t beat them, join them fouled pycnogonids from Antarctica”. In: Ernst A, Schäfer P, Scholz J (eds) Bryozoan studies 2010. Lecture notes in earth system sciences, vol 143. Springer, Heidelberg, pp 137–153
King PE (1973) Pycnogonids. Hutchinson, London, p 144
Lane SJ, Shishido CM, Moran AL, Tobalske BW, Woods HA (2016) No effects and no control of epibionts in two species of temperate pycnogonids. Biol Bull 230:165–173
Lane SJ, Shishido CM, Moran AL, Tobalske BW, Arango CP, Woods HA (2017) Upper limits to body size imposed by respiratory–structural trade-offs in Antarctic pycnogonids. Proc R Soc B 284:20171779
Lane SJ, Moran AL, Shishido CM, Tobalske BW, Woods HA (2018) Cuticular gas exchange by Antarctic sea spiders. J Exp Biol 221:177568. https://doi.org/10.1242/jeb.177568
Lau WWY, Martinez MM (2003) Getting a grip on the intertidal: flow microhabitat and substratum type determine the dislodgement of the crab Pachygrapsus crassipes (Randall) on rocky shores and in estuaries. J Exp Mar Biol Ecol 295:1–21
Martinez MM (1996) Issues for aquatic pedestrian locomotion. Am Zool 36:619–627
Moran AL, Woods HA, Shishido CM, Lane SJ, Tobalske BW (2018) Predatory behavior of giant Antarctic sea spiders (Colossendeis) in nearshore environments. Invertebr Biol 137:116–123
Pipe AR (1982) Epizoites on marine invertebrates: with particular reference to those associated with the pycnogonid Phoxichilidium tubulariae Lebour, the amphipod Caprella linearis (L.) and the decapod Corystes cassivelaunus (Pennant). Chem Ecol 1:61–74
Poulter R, Oliver PG, Hauton C, Sanders T, Ciotti BJ (2017) Infestation of shore crab gills by a free-living mussel species. Mar Biodiv 48:1241–1246
Rasband WS (2014) ImageJ. US National Institutes of Health, Bethesda (Online)
Scholnick DA, Burnett KG, Burnett LE (2006) Impact of exposure to bacteria on metabolism in the penaeid shrimp Litopenaeus vannamei. Biol Bull 211:44–49
Seaborn T (2014) Limpets and their algal epibionts: costs and benefits of Acrosiphonia spp and Ulva lactuca growth. J Mar Biol 2014:1–7
Shine R, Brischoux F, Pile AJ (2010) A seasnake’s colour affects its susceptibility to algal fouling. Proc R Soc Lond B Biol Sci 277:2459–2464
Thomas F, Poulin R, de Meeüs T, Guégan JF, Renaud F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84:167–171
Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189
Wahl M (1996) Fouled snails in flow: potential of epibionts on Littorina littorea to increase drag and reduce snail growth rates. Mar Ecol Prog Ser 138:157–168
Wahl M (1997) Increased drag reduces growth of snails: comparison of flume and in situ experiments. Mar Ecol Prog Ser 151:291–293
Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438
Wahl M, Lafargue F (1990) Marine epibiosis. II. Reduced fouling on Polysyncraton lacazei (Didemnidae, Tunicata) and proposal of an antifouling potential index. Oecologia 82:275–282
Watling L, Thiel M (2013) Functional morphology and diversity, vol 1. Oxford University Press, New York
Whitley E, Ball J (2002) Statistics review 6: nonparametric methods. Crit Care 6:509–513
Witman JD, Suchanek TH (1984) Mussels in flow: drag and dislodgement by epizoans. Mar Ecol Prog Ser 16:259–268
Woods HA, Moran AL (2008) Oxygen profiles in egg masses predicted from a diffusion-reaction model. J Exp Biol 211:790–797. https://doi.org/10.1242/jeb.014613
We thank the staff at McMurdo Station for technical support. Special thanks to Rob Robbins, Steve Rupp, and Timothy Dwyer for SCUBA support. In addition, we thank two anonymous reviewers for providing helpful comments on earlier drafts of the manuscript. Funding was provided by the National Science Foundation Grant PLR-1341485 to HAW and BWT and PLR-1341476 to ALM.
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
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Lane, S.J., Tobalske, B.W., Moran, A.L. et al. Costs of epibionts on Antarctic sea spiders. Mar Biol 165, 137 (2018). https://doi.org/10.1007/s00227-018-3389-9