Diversity in skeletal architecture influences biological heterogeneity and Symbiodinium habitat in corals

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  • Zoology 116 (2013) 262 269

    Contents lists available at ScienceDirect

    Zoology

    jou r n al hom epa ge: www . els ev ie r .com/ locate / zool

    Diversi oloand Sym

    Denise M ShiaRaymonda Hawaii Institu HawaUSAb National Mus OCc Institute of M Cd Institute of Marine Biotechnology, National Dong Hwa University, Pingtung, Taiwan, ROCe Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung, Taiwan, ROCf School of Biological Sciences, Washington State University, PO Box 644236, Pullman, WA 99164-4236, USA

    a r t i c l e i n f o

    Article history:Received 10 DReceived in reAccepted 28 JuAvailable onlin

    Keywords:Scleractinian cCoral architectPerforate coraSymbiodiniumHostsymbion

    a b s t r a c t

    1. Introdu

    Scleractiecosystem million yearapid changand local hdramaticall(Berkelmanthe commumany to q

    CorresponE-mail add

    0944-2006/$ http://dx.doi.oecember 2012vised form 24 June 2013ne 2013e 3 August 2013

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    habitatt dynamics

    Scleractinian corals vary in response to rapid shifts in the marine environment and changes in reefcommunity structure post-disturbance reveal a clear relationship between coral performance and mor-phology. With exceptions, massive corals are thought to be more tolerant and branching corals morevulnerable to changing environmental conditions, notably thermal stress. The typical responses of mas-sive and branching coral taxa, respectively, are well documented; however, the biological and functionalcharacteristics that underpin this variation are not well understood. We address this gap by compar-ing multiple biological attributes that are correlated with skeletal architecture in two perforate (havingporous skeletal matrices with intercalating tissues) and two imperforate coral species (Montipora aequitu-berculata, Porites lobata, Pocillopora damicornis, and Seriatopora hystrix) representing three morphotypes.Our results reveal inherent biological heterogeneity among corals and the potential for perforate skele-tons to create complex, three-dimensional internal habitats that impact the dynamics of the symbiosis.Patterns of tissue thickness are correlated with the concentration of symbionts within narrow regionsof tissue in imperforate corals versus broad distribution throughout the larger tissue area in perforatecorals. Attributes of the perforate and environmentally tolerant P. lobata were notable, with tissues 5times thicker than in the sensitive, imperforate species P. damicornis and S. hystrix. Additionally, P. lobatahad the lowest baseline levels of superoxide and Symbiodinium that provisioned high levels of energy.Given our observations, we hypothesize that the complexity of the visually obscured internal environ-ment has an impact on hostsymbiont dynamics and ultimately on survival, warranting further scienticinvestigation.

    2013 Elsevier GmbH. All rights reserved.

    ction

    nian corals create reef habitats that provide criticalservices worldwide. Corals have persisted over 500rs, but have become increasingly threatened by thees in the marine environment linked to climate changeuman activities (Glynn, 1996). Corals have respondedy to environmental disturbances within recent decadess et al., 2004) resulting in large-scale global changes innity structure of reefs. These changes have prompteduestion whether corals have the capacity to buffer,

    ding author. Tel.: +1 808 236 7420; fax: +1 808 236 7443.ress: rgates@hawaii.edu (R.D. Gates).

    acclimatize and/or adapt to the dynamic environmental conditionspredicted to occur as a result of climate change and to survive intothe next century.

    Observed ecological variation in the responses of corals andreef communities provides insight into which corals are likely topersist under challenging environmental conditions (Baker et al.,2004; van Woesik et al., 2011). Corals with massive morphologiesare among the most stress-tolerant corals, exhibiting much lowermortality rates following environmental disturbances (e.g., ther-mal stress) compared to branching and plating corals (Gates andEdmunds, 1999; McClanahan, 2004; Schloder and DCroz, 2004).Even within the same genus (e.g., Porites), massive coral mor-photypes appear to be less vulnerable to bleaching than theirbranching counterparts (McClanahan et al., 2001; but see also Guestet al. (2012)). Distinctive qualities of branching corals such as

    see front matter 2013 Elsevier GmbH. All rights reserved.rg/10.1016/j.zool.2013.06.001ty in skeletal architecture inuences bibiodinium habitat in corals

    . Yosta, Li-Hsueh Wangb, Tung-Yung Fanb,c, Chii- W. Leef, Emilia Sogina, Ruth D. Gatesa,

    te of Marine Biology, School of Ocean and Earth Science and Technology, University of

    eum of Marine Biology and Aquarium, 2 Houwan Road, Checheng, Pingtung, Taiwan, Rarine Biodiversity and Evolution, National Dong Hwa University, Pingtung, Taiwan, ROgical heterogeneity

    rng Chenb,d,e,

    ii, 46-007 Lilipuna Road, Kaneohe, HI 96744,

  • D.M. Yost et al. / Zoology 116 (2013) 262 269 263

    the combination of shallow tissue depths and limited resources(Loya et al., 2001), along with high metabolic rates (Gates andEdmunds, 1999), have been implicated as key factors that increasethe thermal sensitivity of these corals. Branching corals also dis-play strongcorals (Antstrategies fing of end(sensu Bakeronmental cof the intimmately dictenvironmenteristics thahow they cbut such ancorals will rtion.

    Beneathan interior (micro-denture and vawithin a sinthrough peintercalatina veneer ointo the skskeletal manant reef-bAstreopora, environmenseveral obsments may dynamics orate skeleto1993) and stressful evtate the cal1971; Gladof Symbiodi(Santos et aand deep tstress throuphotodamaare known and high Sythese coralsas PocillopoSymbiodiniu

    In the punderstandthat are cospecies (Moicornis, and(foliose, mamation on afound in thhave very dTo comparwe evaluatphysiologiccomparisonand suggesin structuriplex Symbiomassive m

    architecture of P. lobata is simple, in fact it is not. As a result, inter-colating, deep tissues create a habitat within P. lobata that is uniqueamong the coral morphotypes investigated, a key biological featurethat in combination with other correlated attributes may explain

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    wer areon aniateler responses to ocean acidication compared to massivehony et al., 2008). In addition to tissue depth, otheror buffering environmental factors may include shuf-osymbiotic dinoagellate (Symbiodinium) communitiesr, 2003) to optimize performance in response to envi-hange. Indeed, the functional integrity and persistenceate associations between corals and Symbiodinium ulti-ates whether corals survive in the face of changingtal conditions or not. That said, the biological charac-t contribute to response variability among corals andompare among coral species is not well characterized,alyses serve as important context for predicting howespond to rising sea temperatures and ocean acidica-

    the commonly known gross morphology of corals liescalcium carbonate skeleton. Carbonate skeletal densitysity) and porosity are key features of coral architec-ry signicantly between species, colonies, and evengle colony (Bucher et al., 1998). Longitudinal sectionsrforate (porous) corals reveal skeletal matrices withg tissues, whereas imperforate species typically haver surface covering of tissue that does not penetrateeleton as is the case with perforate corals. Perforatetrices are characteristic of many species in the domi-uilding genera such as Acropora, Porites, Montipora andbut how skeletal porosity inuences the biology andtal range of corals is not well understood. There areervations that suggest perforate architectural arrange-have a positive impact on the survival and physiologicalf the symbiosis. Deep tissues that penetrate perfo-ns are thought to enable the survival (Jokiel et al.,

    rapid recovery (Krupp et al., 1993) of corals followingents (low salinity, tissue damage), as well as facili-cication process (Buchsbaum-Pearse and Muscatine,felter, 1983), by promoting within-colony transportnium cells and potentially maximizing photosynthesisl., 2009). Additionally, corals with perforate skeletonsissues appear more physiologically robust to thermalgh reduced sunlight exposure in tissues and reducedge to Symbiodinium (Santos et al., 2009). Deep tissuesto co-occur with high levels of tissue-soluble proteinsmbiodinium densities in Porites lobata, which may give

    a competitive advantage over branching species suchra damicornis that have lower protein levels and fewerm (Schloder and DCroz, 2004).resent study, we address a fundamental gap in ouring of coral biology by examining biological attributesrrelated with coral skeletal architecture. Four coralntipora aequituberculata, Porites lobata, Pocillopora dam-

    Seriatopora hystrix) representing three morphotypesssive, and branching) were selected to provide infor-

    wide range of the structural and biological complexitye scleractinians, as well as encompass corals known toifferent environmental thresholds (Loya et al., 2001).e the baseline biology of these four coral species,ed their skeletal and tissue architecture and multipleal traits, using a variety of analytical approaches. This