Vermetid Gastropods Mediate Within-Colony Variation in Coral
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Mar Biol (2015) 162:1523–1530 DOI 10.1007/s00227-015-2688-7 ORIGINAL PAPER Vermetid gastropods mediate within-colony variation in coral growth to reduce rugosity Jeffrey S. Shima1 · Daniel McNaughtan1 · Amanda T. Strong1,2 Received: 17 April 2015 / Accepted: 19 June 2015 / Published online: 7 July 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract Intraspecific variation in coral colony growth colony morphology. Given that structural complexity of forms is common and often attributed to phenotypic plas- coral colonies is an important determinant of “habitat qual- ticity. The ability of other organisms to induce variation in ity” for many other species (fishes and invertebrates), these coral colony growth forms has received less attention, but results suggest that the vermetid gastropod, C. maximum has implications for both taxonomy and the fates of corals (with a widespread distribution and reported increases in and associated species (e.g. fishes and invertebrates). Varia- density in some portions of its range), may have important tion in growth forms and photochemical efficiency of mas- indirect effects on many coral-associated organisms. sive Porites spp. in lagoons of Moorea, French Polynesia (17.48°S, 149.85°W), were quantified in 2012. The pres- ence of a vermetid gastropod (Ceraesignum maximum) was Introduction correlated with (1) reduced rugosity of coral colonies and (2) reduced photochemical efficiency (Fv/Fm) on terminal Reef-building corals exhibit a diversity of growth forms “hummocks” (coral tissue in contact with vermetid mucus that vary markedly among and within species (Chappell nets) relative to adjacent “interstitial” locations (tissue not 1980; Veron 2000; Todd 2008). Particular growth forms in contact vermetid mucus nets). A manipulative field exper- may be used to classify putative species and can be a iment confirmed that the relative growth rate of coral tissue source of taxonomic confusion (Fukami et al. 2004; Fors- was greater in interstices than hummocks when vermetids man et al. 2009). More importantly, structurally complex were present and similar (but with a trend for faster growth growth forms may be used by coral-dwelling organisms for on hummocks) when vermetids were absent. Collectively, shelter and/or refuges from predators (Rogers 1990; Hol- these results indicate that vermetid gastropods interact (pre- brook and Schmitt 2002; Bergsma 2012). sumably via their mucus nets) with coral colony architecture Intraspecific variation in coral growth forms is often to impair photochemical efficiency, reduce growth rates of attributed to phenotypic plasticity that may be adaptive (i.e. specific portions of a coral tissue, and induce a smoothed enabling long-lived colonies to maximise their fitness under changeable environmental conditions; Bruno and Edmunds 1997; Muko et al. 2000; Todd 2008; Padilla-Gamino et al. Communicated by L Mydlarz. 2012). Morphological variation may result from interactions with other corals (Lang 1973; Connell 1976; Rinkevich and Reviewed by undisclosed experts. Loya 1985), putative disease agents (Aeby et al. 2011; Stim- * Jeffrey S. Shima son 2011), or other coral-associated organisms (e.g. Abel- [email protected] son et al. 1991; Wielgus et al. 2002; Bergsma 2009), though the latter has received comparatively little attention (perhaps 1 School of Biological Sciences, and the Coastal Ecology Lab, University of Wellington, PO Box 600, Victoria, New because it is perceived as rare or anomalous). Zealand Previous experiments (Colgan 1985; Shima et al. 2010, 2 Present Address: Environmental Protection Authority, Level 2013) indicate that the vermetid gastropod, Ceraesignum 10, 215 Lambton Quay, Wellington, New Zealand maximum (formerly Dendropoma maximum; see Golding 1 3 1524 Mar Biol (2015) 162:1523–1530 Fig. 1 a Vermetid gastropod, Ceraesignum maximum (formerly listed are commonly associated with the presence of vermetids on Moorea. in the genus Dendropoma), with a mucus net draped over a portion c Experimental unit (concrete block affixed to reef) used to evaluate of a colony of massive Porites spp. Mucus nets used by vermetids the effects of vermetids on growth of massive Porites on hummocks for capture of food particles often come into direct contact with (small coral attached to top of block) or in interstitial positions (small polyps on hummocks of massive Porites colonies but not with pol- coral recessed within central portion of block). Vermetids embedded yps in interstitial spaces. The portion of the Porites colony in back- in rubble (treatment) or pieces of rubble without vermetids (control) ground lacks vermetids and is noticeably more rugose. b Locally were attached to periphery of block with cable ties flattened appearance of hummocks on massive Porites colonies that et al. 2014 for recent taxonomic revision), reduces the degree of variation in tissue colour between hummocks and growth and survival of several species of corals and may interstices, or locally flattened growth forms. have the ability to dramatically alter coral growth forms These observations led us to hypothesise that the ver- (Colgan 1985; Zvuloni et al. 2008; Shima et al. 2010). metid gastropod, C. maximum, alters the growth form C. maximum produces pelagic larvae (Phillips and Shima of massive Porites spp. when its mucus nets come into 2010) that settle and permanently attach to bare substrate direct contact with exposed portions of the colony (i.e. (Phillips et al. 2014). Settled individuals grow by adding on hummocks). In the absence of vermetids, we predicted to uncoiled tubular shells and often become encased in a that coral tissue in a hummock position would grow faster matrix of live and dead coral. They capture food using a than coral tissue in interstices (because hummocks might mucus net (Fig. 1a), which is secreted and retracted at be exposed to increased light and/or water flow; e.g. intervals (Kappner et al. 2000). The mucus nets of ver- Dustan 1975) to yield colonies that become increasingly metids often come into direct contact with the terminal structurally complex with age. Conversely, we predicted branches or “hummocks” of corals including colonies of that the presence of vermetids might reverse this pat- massive Porites spp. that are prevalent within the lagoons tern of differential growth between coral tissue in hum- of Moorea, French Polynesia (Fig. 1a, b; a species com- mocks and interstitial positions (i.e. coral growth slows plex determined by Edmunds (2009) to be a mix of P. or ceases on hummocks where it is affected by vermetid lobata and P. lutea, though phylogenetic analysis by Fors- mucus nets, but continues within the interstices until the man et al. (2009) indicates taxonomic uncertainty within gaps fill in) to yield colonies that become increasingly this group; hence, we refer to the complex collectively as locally flattened with age. To test this hypothesis, we “massive Porites spp.”). Our preliminary observations sug- first quantified patterns and sources of spatial variation gest that tissue of massive Porites spp. (on both P. lutea- in the height of hummocks (to formally test our prelimi- like colonies and P. lobata-like colonies) that is in direct nary observations that hummock height appears greater contact with vermetid mucus nets (e.g. on hummocks) on colonies without vermetids). In addition, we char- appears lighter in colour, with a distinct corallite/coenos- acterised aspects of the photobiology of coral tissue on teum structure (Fig. 1a) relative to tissue of the same col- hummocks or interstitial positions for colonies of mas- ony that is not in direct contact with vermetid mucus nets sive Porites spp. that naturally had or lacked vermetids (i.e. recessed in the interstices between hummocks). In (to evaluate patterns and sources of variation in photo- addition, hummocks on massive Porites spp. colonies with physiological performance). Finally, we conducted a field vermetids often appear locally flattened (Fig. 1b; see also experiment to simulate hummocks and interstitial sites Shima et al. 2010). In contrast, massive Porites spp. colo- and quantified the growth rates of small coral colonies nies (both P. lutea-like colonies and P. lobata-like colo- deployed to these positions in the presence and absence nies) without vermetid populations do not show the same of transplanted vermetids. 1 3 Mar Biol (2015) 162:1523–1530 1525 Methods Experimental study Observational study We constructed a field experiment to quantify the effects of vermetids on growth of massive Porites spp. corals that Structural morphology were located in simulated hummock or interstitial posi- tions. We collected 44 small colonies ( 5 cm diameter) of ≤ We measured the heights of hummocks relative to adja- massive Porites spp from a site in the lagoon (2–3 m water cent interstices on massive Porites spp. colonies with depth) near to where we quantified structural morphol- and without the vermetid gastropod C. maximum. Spe- ogy and photochemical efficiency. We transported corals cifically, we quantified the heights of 3 randomly selected to the flow-through sea water facility at the UC Berkeley hummocks on each of 10 randomly selected colonies Gump Research Station, attached each coral to a small (~1–2 m diameter) of each type ( vermetids), sampled (~8 8 cm) plastic base using A-788 splash zone epoxy ± × from a site in Vaipahu Lagoon, Moorea, French Polyne- (Z-spar), and estimated the initial skeletal mass of each sia (17.48067°S, 149.84698°W). Hummock height was focal