Abstract
The capacity to predict changes in the distribution and abundance of sessile marine invertebrates depends on quantifying factors that affect spatial and temporal variation in propagule production. This is particularly important for invasive species, since both the timing and abundance of introduced propagules can determine invasion success. This study examines the role of reproductive dynamics in contributing to the invasion success of the highly invasive bryozoan Membranipora membranacea by quantifying temporal patterns in the sexual stage and potential fecundity of colonies and examining the effects of intrinsic (colony size) and extrinsic (temperature, host substrate) factors on the reproductive potential of invasive populations. Colonies were collected on the 4 most abundant algal substrates in Nova Scotia at 2–3 sites approximately monthly from 2012 to 2015. Individual zooids within each collected colony were classified by sexual stage (immature, producing sperm only, producing sperm and oocytes, producing oocytes only), and the number of oocytes per colony was counted as a measure of potential colony fecundity (reproductive potential). There were significant seasonal patterns in colony fecundity; however, temperature and colony size accounted for only 12 and 7% of the observed variation, respectively. Instead, consistent differences in reproductive potential were observed among colonies on different algal substrates. Our results indicate how critical demographic processes can differ for invasive species outside of their native range. Our study underscores the need to quantify population dynamics of non-indigenous species within the invaded community to more accurately predict the long-term consequences for invaded ecosystems.
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Change history
02 December 2017
Fig. 2 was published with incorrect values for June 2012 and May 2014. The corrected Figure 2 is provided here.
References
Berman J, Harris L, Lambert WJ, Buttrick M, Dufresne M (1992) Recent invasions of the gulf of maine: three contrasting ecological histories. Conserv Biol 6:435–441
Caines S, Gagnon P (2012) Population dynamics of the invasive bryozoan Membranipora membranacea along a 450-km latitudinal range in the subarctic northwestern Atlantic. Mar Biol 159:1817–1832
Cancino JM, Hughes RN (1987) The effect of water flow on growth and reproduciton of Celleporella hyalina (L.) (Bryozoa: Cheilostomata). J Exp Mar Biol Ecol 112:109–130
Carlton JT (1996) Patterns, processes, and prediction in marine invasion ecology. Biol Conserv 78:97–106
Chapman AS, Scheibling RE, Chapman ARO (2002) Species introductions and changes in the marine vegetation of Atlantic Canada. In: Claudi R, Nantel P, Muckle-Jeffs E (eds) Alien invaders in Canada’s waters, wetlands, and forests. Natural Resources Canada, Canadian Forest Service, Science Branch, Ottawa
Denley D, Metaxas A, Short J (2014) Selective settlement by larvae of Membranipora membranacea and Electra pilosa (Ectoprocta) along kelp blades in Nova Scotia, Canada. Aquat Biol 21:47–56
Edwards KF, Stachowicz JJ (2010) Multivariate trade-offs, succession, and phenological differentiation in a guild of colonial invertebrates. Ecology 91:3146–3152
Eggleston D (1972) Patterns of reproduction in the marine Ectoprocta of the Isle of Man. J Nat Hist 6:31–38
Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963
Harvell DC (1985) Partial predation, inducible defenses, and the population biology of a marine bryozoan. Dissertation, University of Washington, Seattle
Harvell DC (1992) Inducible defenses and allocation shifts in a marine bryozoan. Ecology 73:1567–1576
Harvell DC, Grosberg RK (1988) The timing of sexual maturity in clonal animals. Ecology 69:1855–1864
Harvell DC, Helling R (1993) Experimental induction of localized reproduction in a marine bryozoan. Biol Bull 184:286–295
Harvell DC, Caswell H, Simpson P (1990) Density effects in a colonial monoculture: experimental studies with a marine bryozoan (Membranipora membranacea L.). Oecologia 82:227–237
Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2000) Suppy-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249
Hunter E, Hughes RN (1995) Environmental and genetic components of variation in sexual allocation by an epialgal bryozoan. Mar Ecol Prog Ser 120:193–202
Krumhansl KA, Scheibling RE (2011) Detrital production in Nova Scotian kelp beds: patterns and processes. Mar Ecol Prog Ser 421:67–82
Lambert WJ, Levin PS, Berman J (1992) Changes in the structure of a New England (USA) kelp bed: the effects of an introduced species? Mar Ecol Prog Ser 88:303–307
Lord JP (2016) Impact of seawater temperature on growth and recruitment of invasive fouling species at the global scale. Mar Ecol. doi:10.1111/maec.12404
Norton TA (1973) Orientated growth of Membranipora membranacea (L.) on the thallus of Saccorhiza polyschides (Lightf.) Batt. JEMBE 13:91–95
O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications from marine ecology, evolution, and conservation. PNAS 104:1266–1271
Pöckl M (2007) Strategies of a successful new invader in European fresh waters: fecundity and reproductive potential of the Ponto-Caspian amphipod Dikerogammarus villosus in the Austrian Danube, compared with the indigenous Gammarus fossarum and G. roeseli. Freshwater Biol 52:50–63
Pratt MC, Grason EW (2007) Invasive species as a new food source: does a nudibranch predator prefer eating an invasive bryozoan? Biol Invasions 9:645–655
Ramirez-Llodra E (2002) Fecundity and life-history strategies in marine invertebrates. Adv Mar Biol 43:87–170
Rinkevich B, Loya Y (1979) The reproduction of the red sea coral Stylophora pistillata. II. Sychronization in breeding and seasonality of planulae shedding. Mar Ecol Prog Ser 1:145–152
Ritzmann NF, da Rocha RM, Roper JJ (2009) Sexual and asexual reproduction in Didemnum rodriguesi (Ascidiacea, Didemnidea). Ser Zool Porto Alegre 99:106–110
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–663
Ryland JS (1976) Physiology and ecology of marine bryozoans. Adv Mar Biol 14:285–433
Ryland JS, Stebbing ARD (1971) Settlement and orientated growth in epiphytic and epizoic bryozoans. In: Crisp DJ (ed) Fourth European marine biology symposium. Cambridge University Press, Cambridge, pp 105–123
Sams MA, Keough MJ (2012a) Contrasting effects of variable species recruitment on marine sessile communities. Ecology 93:1153–1163
Sams MA, Keough MJ (2012b) Effects of pulse versus steady recruitment on sessile marine communities. Oecologia 170:209–219
Saunders MI, Metaxas A (2007) Temperature explains settlement patterns of the introduced bryozoan Membranipora membranacea in Nova Scotia, Canada. Mar Ecol Prog Ser 344:95–106
Saunders MI, Metaxas A (2008) High recruitment of the introduced bryozoan Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser 369:139–151
Saunders MI, Metaxas A (2009) Population dynamics of a nonindigenous epiphytic bryozoan Membranipora membranacea in the western North Atlantic: effects of kelp substrate. Aquat Biol 8:83–94
Saunders MI, Metaxas A (2010) Physical forcing of distributions of bryozoan cyphonautes larvae in a coastal embayment. Mar Ecol Prog Ser 418:131–145
Saunders MI, Metaxas A, Filgueira R (2010) Implications of warming temperatures for population outbreaks of a nonindigenous species (Membranipora membranacea, Bryozoa) in rocky subtidal ecosystems. Limnol Oceanogr 55:1627–1642
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. PNAS 99:15497–15500
Temkin MH (1994) Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biol Bull 187:143–155
Tuomi J, Vuorisalo T (1989) What are the units of selection in modular organisms? Oikos 54:227–233
Underwood AJ, Fairweather PG (1989) Supply-side ecology and benthic marine assembalges. Trends Ecol Evol 1:16–20
Van Veghel MLJ, Bak RPM (1994) Reproductive characteristics of the polymorphic caribbean reef building coral Montastrea annularis. III. Reproduction in damaged and regenerating colonies. Mar Ecol Prog Ser 109:229–233
Vizoso DB, Schärer L (2007) Resource-dependent sex-allocation in a simultaneous hermaphrodite. Eur Soc Evol Biol 1046–1055
Yorke AF, Metaxas A (2011) Interactions between an invasive and a native bryozoan (Membranipora membranacea and Electra pilosa) species on kelp and Fucus substrates in Nova Scotia, Canada. Mar Biol 158:2299–2311
Yorke AF, Metaxas A (2012) Realtive importance of kelps and fuciods as substrata of the invasive epiphytic bryozoan Membranipora membranacea in Nova Scotia, Canada. Aquat Biol 16:17–30
Yoshioka PM (1973) The population dynamics and ecology of the encrusting ectoproct Membranipora serrilamella. Dissertation, University of California, San Diego
Zar JH (1999) Biostatistical analysis. Prentice-Hall, NJ
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. In: Krickeberg K, Samet JM, Tsiatis A, Wong W (eds) Gail M. Spring Science and Business Media, New York
Acknowledgements
We thank J. Lindley, R.E. Scheibling, C. Feehan, K. Filbee-Dexter, J. O’Brien, E. Simonson, K. Sorochan, and C. Civelek for assistance with field work, and R.E. Scheibling for providing comments on an earlier version of the manuscript. This research was funded by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant to A.M., and a Dalhousie Faculty of Graduate Studies scholarship, Nova Scotia Scholarship, NSERC Canada Graduate Scholarship, and Dalhousie Killam Scholarship to D.D.
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This study was funded by a Natural Sciences and Engineering Research Council Discovery grant (NSERC RGPIN 2229322-2011) to AM.
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All applicable national and institutional guidelines for the care and use of animals were followed in accordance with the recommendations of the Canadian Council on Animal Care and the policies of Dalhousie University.
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A correction to this article is available online at https://doi.org/10.1007/s00227-017-3268-9.
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Denley, D., Metaxas, A. Effects of intrinsic and extrinsic factors on reproduction of an ecologically significant invasive bryozoan: implications for invasion success. Mar Biol 164, 145 (2017). https://doi.org/10.1007/s00227-017-3172-3
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DOI: https://doi.org/10.1007/s00227-017-3172-3