Skip to main content
SpringerLink
Log in

Cold temperature stress and predation effects on corals: their possible roles in structuring a nonreefal coral community

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The incidence of Drupella corallivory in Hong Kong was observed to be higher following colder winters. A correlation between colder winter and increased corallivory could therefore be suggested, and a hypothesis that corals stressed by low temperature are preferred by corallivores was proposed. This study tested this hypothesis by investigating the effects of both low (14 °C) and elevated (32 °C) temperatures on the coral Acropora valida and the consequences of these exposures on corallivory by the gastropod Drupella rugosa using a prey-choice experimental strategy. The low temperature (14 °C) tested represents the mean lowest sea surface temperature (SST) recorded in winter in Hong Kong, and the elevated temperature (32 °C) tested represents the mean highest SST in summer. These temperatures do not occur every year. Experimental results showed that A. valida was sensitive to low, but not to elevated, temperature stress. Only the cold stressed corals showed paler tissue and coral decay after the one-week temperature treatment. The results of the prey-choice experiment also showed that cold stressed corals were preferentially attacked by the gastropods. Low-temperature stress also exerted effects on D. rugosa as the cold stressed gastropods were less responsive and sensitive than the normal gastropods in detecting prey. However, when both A. valida and D. rugosa were exposed to the same level of low-temperature stress, the impact was more detrimental to the coral than to the gastropod. Given that nonreefal coral communities like those in Hong Kong are periodically experiencing winter low temperatures, these differences in the response to low-temperature stress and the subsequent selective predation effect may prevent such fast-growing coral species such as A. valida from dominating and thereby contribute to the shaping of the coral community structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Ang PO Jr, Choi LS, Choi MM, Cornish A, Fung HL, Lee MW, Lin TP, Ma WC, Tam MC, Wong SY (2005) Hong Kong. In: Japan Wildlife Research Center, Ministry of the Environment, Government of Japan, (ed) Status of coral reefs of the East Asian Seas Region: 2004. Global Coral Reef Monitoring Network. Ministry of Environment, Tokyo, pp 121–152

  • Ayling AM, Ayling AL (1987) Ningaloo Marine Park: Preliminary fish density assessment and habitat survey, with information on coral damage due to Drupella cornus grazing: a report prepared for the Department of Conservation and Land Management Western Australia. Department of Conservation and Land Management

  • Berkelmans R, Oliver JK (1999) Large-scare bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60

    Article  Google Scholar 

  • Birkeland C (1989) The influence of echinoderms on coral-reef communities. In: Janhoux M, Lawrence JM (eds) Echinoderm studies 3. Balkema, Rotterdam, pp 1–19

    Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreak. PLoS Biol 5(6):e124

    Article  PubMed Central  PubMed  Google Scholar 

  • Buddemeier RW, Kleypas JA, Aronson RB (2004) Coral reefs and global climate change: potential contributions of climate change to stresses on coral reef ecosystems. Pew Center on Global, Climate Change p 44

    Google Scholar 

  • Carpenter RC (1997) Invertebrate predators and grazers. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 198–229

    Chapter  Google Scholar 

  • Choi LS (2003) Algal-Coral interactions in Tung Ping Chau, Hong Kong. M.Phil. thesis, The Chinese University of Hong Kong, p 168 [http://easysearch.lib.cuhk.edu.hk/cgi-bin/record?id=b2418162]

  • Choi MM (2002) Coral bleaching in Porites lobata and predation on Acropora tumida by corallivorous gastropods in Tung Ping Chau, Hong Kong. M.Phil. thesis, The Chinese University of Hong Kong, p 236 [http://easysearch.lib.cuhk.edu.hk/cgi-bin/record?id=b2418396]

  • Chow MH (2012) Effects of heterotrophy on the physiological responses of the scleractinian coral Goniopora lobata in Hong Kong. M.Phil. thesis, The Chinese University of Hong Kong, p 251

  • Colella MA, Ruzicka RR, Kidney JA (2012) Cold-water event of January 2010 results in catastrophic benthic mortality on patch reefs in the Florida Keys. Coral reefs 31:621–632

    Article  Google Scholar 

  • Cumming RL (2009a) Case study: impact of Drupella spp. on reef-building corals of the Great Barrier Reef. Great Barrier Reef Marine Park Authority. Townsville, QLD, Australia, p 44

  • Cumming RL (2009b) Population outbreaks and large aggregations of Drupella on the Great Barrier Reef. Great Barrier Reef Marine Park Authority, Townsville, QLD, Australia, p 26

    Google Scholar 

  • Cumming RL, McCorry D (1998) Corallivorous gastropods in Hong Kong. Coral Reefs 17:178

    Article  Google Scholar 

  • EPD-HKSAR Hong Kong Environmental Protection Department (1986–2012) Marine water quality data. http://epic.epd.gov.hk/EPICRIVER/marine/

  • Field A (2009) Mixed design ANOVA (GLM 5). In: Field A (ed) Discovering Statistics Using SPSS, 3rd edn. SAGE Publications Ltd, London, pp 506–538

    Google Scholar 

  • Forde M (1992) Populations, behavior and effects of Drupella cornus on the Ningaloo Reef, Western Australia. In: Turner S (ed) Drupella cornus: a synopsis. Department of Conservation and Land Management, pp 45–50

  • Hoegh-Guldberg O, Fine M, Skirving W, Johnstone R, Dove S, Strong A (2005) Cold bleaching following wintery weather. Limnol Oceanogr 50:265–271

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hsieh HJ, Chen KS, Lin YI, Huang YA, Baird AH, Tsai WS, Su WC, Chen CA (2011) Establishment of a no-take area (NTA) could not guarantee the preservation of coral communities in Chinwan Inner Bay, Penghu, Taiwan. Zool Stud 50:443–453

    Google Scholar 

  • Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: a long-term perspective. Limnol Oceanogr 44:932–940

    Article  Google Scholar 

  • Kita M, Kitamura M, Koyama T, Teruya T, Matsumoto H, Nakano Y, Uemura D (2005) Feeding attractants for the muricid gastropod Drupella cornus, a coral predator. Tetrahedron Lett 46:8583–8585

    Article  CAS  Google Scholar 

  • Kleypas JA, McManus JW, Menus LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 159:146–159

    Google Scholar 

  • Knowlton N, Lang JC, Keller BD (1990) Case study of natural population collapse: post-hurricane predation on Jamaican staghorn corals. Smithson Contrib Mar Sci 31:1–25

    Article  Google Scholar 

  • Lam K, Shin PKS, Hodgson P (2007) Severe bioerosion caused by an outbreak of corallivorous Drupella and Diadema at Hoi Ha Wan Marine Park, Hong Kong. Coral Reefs 26:893

    Article  Google Scholar 

  • Lirman D, Schopmeyer S, Manzello D, Gramer LJ, Precht WF, Muller-Karger F, Banks K, Barnes B, Bartels E, Bourque A, Byrne J, Donahue S, Duquesnel J, Fisher L, Gilliam D, Hendee J, Johnson MS, Maxwell K, McDevitt E, Monty J, Rueda D, Ruzicka R, Thanner S (2011) Severe 2010 cold-water event caused unprecedented mortality to corals of the Florida reef tract and reversed previous survivorship patterns. PLoS One 6:e23047

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  • Mayor AG (1914) The effects of temperature on tropical marine animals. Year B Carnegie Inst Wash 6:1–24

    Google Scholar 

  • Mayor AG (1915) The lower temperature at which reef-corals lose their ability to capture food. Year B Carnegie Inst Wash 14:212

    Google Scholar 

  • McIlwain JL, Jones GP (1997) Prey selection by an obligate coral-feeding wrasse and its response to small-scale disturbance. Mar Ecol Prog Ser 155:189–198

    Article  Google Scholar 

  • Morton B, Blackmore G (2000) The impacts of an outbreak of corallivorous gastropods, Drupella rugosa and Cronia margariticola (Muricidae), on Hong Kong’s scleractinian corals. Final report submitted to the Government of the Hong Kong Special Administrative Region, China

  • Morton B, Blackmore G (2009) Seasonal variation in the density of and corallivory by Drupella rugosa and Cronia margariticola (Caenogastropoda: Muricidae) from the coastal waters of Hong Kong: (‘plagues’ or ‘aggregations’)? J Mar Biol Assoc U.K. 89:147–159

  • Morton B, Blackmore G, Kwok CT (2002) Corallivory and prey choice by Drupella rugosa (Gastropoda: Muricidae) in Hong Kong. J Molluscan Stud 68:217–223

    Article  Google Scholar 

  • Robertson R (1970) Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pac Sci 24:43–54

    Google Scholar 

  • Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91

    Article  Google Scholar 

  • Rotjan RD, Dimond JL, Thornhill DJ, Leichter JJ, Helmuth B, Kemp DW, Lewis SM (2006) Chronic parrotfish grazing impedes coral recovery after bleaching. Coral Reefs 25:361–368

    Article  Google Scholar 

  • Saxby T, Dennison WC, Hoegh-Guldberg O (2003) Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Mar Ecol Prog Ser 248:85–97

    Article  Google Scholar 

  • Selig ER, Harvell CD, Bruno JF, Willis BL, Page CA, Casey KS, Sweatman H (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreak at broad spatial scales. In: Phimmey JT, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: Science and management. American Geophysical Union, Washington D. C., USA, pp 111–128

  • Siebeck UE, Marshall NJ, Kluter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

    Article  Google Scholar 

  • Taylor JD (1980) Diets and habitats of shallow water predatory gastropods around Tolo Channel, Hong Kong. In: Morton B (ed) The Malacofauna of Hong Kong and Southern China. Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1997. University of Hong Kong Press, Hong Kong, pp 163–180

  • Turner SJ (1994) The biology and population outbreaks of the corallivorous gastropod Drupella on the Indo-Pacific reefs. Oceanography and Marine Biology: an Annual Review 32:461–530

    Google Scholar 

  • Zhang Y, Sperber KR, Boyle JS (1997) Climatology and interannual variation of the East Asian winter monsoon: results from the 1979-95 NCEP/NCAR reanalysis. Monthly Weather Reviw 125:2605–2619

    Article  Google Scholar 

Download references

Acknowledgments

This study was partly supported by Hong Kong SAR University Grant Council GRF Grant 460013. We thank MH Chow, PY Chui, YL Kam, KY Lam, TY Ng and KT Wong for their assistance in the experiments. Special thanks are given to YH Yung and HB Yeung for their logistic and technical supports.

Author information

Authors and Affiliations

  1. Marine Science Laboratory, Chinese University of Hong Kong, Shatin, NT, Hong Kong SAR, China

    Ryan Ho Leung Tsang & Put Ang Jr.

Authors
  1. Ryan Ho Leung Tsang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Put Ang Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Put Ang Jr..

Additional information

Communicated by Biology Editor Prof. Brian Helmuth

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsang, R.H.L., Ang, P. Cold temperature stress and predation effects on corals: their possible roles in structuring a nonreefal coral community. Coral Reefs 34, 97–108 (2015). https://doi.org/10.1007/s00338-014-1210-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-014-1210-x

Keywords

Search

Navigation