Dissepiments, Density Bands and Signatures of Thermal Stress in Porites Skeletons
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Coral Reefs DOI 10.1007/s00338-017-1566-9 REPORT Dissepiments, density bands and signatures of thermal stress in Porites skeletons 1,3 2 Thomas M. DeCarlo • Anne L. Cohen Received: 26 October 2016 / Accepted: 5 March 2017 Ó Springer-Verlag Berlin Heidelberg 2017 Abstract The skeletons of many reef-building corals are dissepiment spacing to reconstruct multiple years of accreted with rhythmic structural patterns that serve as monthly skeletal extension rates in two Porites colonies valuable sclerochronometers. Annual high- and low-den- from Palmyra Atoll and in another from Palau that sity band couplets, visible in X-radiographs or computed bleached in 1998 under anomalously high sea tempera- tomography scans, are used to construct age models for tures. Spacing between successive dissepiments exhibited paleoclimate reconstructions and to track variability in strong seasonality in corals containing annual density coral growth over time. In some corals, discrete, anoma- bands, with narrow (wide) spacing associated with high lously high-density bands, called ‘‘stress bands,’’ preserve (low) density, respectively. A high-density ‘‘stress band’’ information about coral bleaching. However, the mecha- accreted during the 1998 bleaching event was associated nisms underlying the formation of coral skeletal density with anomalously low dissepiment spacing and missed banding remain unclear. Dissepiments—thin, horizontal dissepiments, implying that thermal stress disrupts skeletal sheets of calcium carbonate accreted by the coral to support extension. Further, uranium/calcium ratios increased within the living polyp—play a key role in the upward growth of stress bands, indicating a reduction in the carbonate ion the colony. Here, we first conducted a vital staining concentration of the coral’s calcifying fluid under stress. experiment to test whether dissepiments were accreted with Our study verifies the lunar periodicity of dissepiments, lunar periodicity in Porites coral skeleton, as previously provides a mechanistic basis for the formation of annual hypothesized. Over 6, 15, and 21 months, dissepiments density bands in Porites, and reveals the underlying cause consistently formed in a 1:1 ratio to the number of full of high-density stress bands. moons elapsed over each study period. We measured Keywords Coral Á Calcification Á Density banding Á Sclerochronology Á Stress bands Á Bleaching Communicated by Biology Editor Dr. Mark R. Patterson Electronic supplementary material The online version of this article (doi:10.1007/s00338-017-1566-9) contains supplementary Introduction material, which is available to authorized users. & Thomas M. DeCarlo The history of the tropical oceans is archived in the cal- [email protected] cium carbonate (CaCO3) skeletons of reef-building corals. 1 Some corals live for a millennium and build massive 10-m- Massachusetts Institute of Technology/Woods Hole tall colonies (Soong et al. 1999) but, despite their size, only Oceanographic Institution Joint Program in Oceanography and Applied Ocean Science and Engineering, Woods Hole, thin layers (2 cm or less) of living polyps envelop them. MA 02543, USA Below this veneer of life, buried within the interior of the 2 Woods Hole Oceanographic Institution, Woods Hole, colony, is the skeleton constructed over the lifespan of the MA 02543, USA coral. Rhythmic patterns in the skeleton correspond to 3 Present Address: School of Earth and Environment, The specific periods of time, making corals valuable ‘‘scle- University of Western Australia, Crawley, Australia rochronometers,’’ analogous to tree rings used in 123 Coral Reefs dendrochronology (Buddemeier 1974; Hudson et al. 1976). climatic history. For example, Wells (1963) combined -1 -1 Scleractinian corals accrete skeleton with different CaCO3 circadian (*d ) and annual (*yr ) growth ridges in crystal morphologies between day and night (Barnes 1970; fossil solitary corals to track changes in day length over Gladfelter 1983; Cohen et al. 2001; Cohen and McCon- millions of years. Annual density bands are commonly naughey 2003; Shirai et al. 2012) and with different den- used to assign calendar dates to geochemical climate sities between summer and winter (Fig. 1) (Knutson 1972; proxies measured in the skeleton, such as Sr/Ca or d18O Buddemeier et al. 1974; Highsmith 1979; Barnes and (Weber and Woodhead 1972; Smith et al. 1979). In some Lough 1993; Dodge et al. 1993). Skeletal growth patterns cases, the accuracy of these dates—called ‘‘age models’’— have been exploited to reconstruct Earth’s astronomic and has been independently verified based on the presence of radioactive isotopes in bands corresponding to mid-twen- Fig. 1 Density bands visible in tieth century nuclear tests (Knutson et al. 1972) and computed tomography scan of a recently based on U–Th dating (Thompson et al. 2003; Porites skeleton collected on Cobb et al. 2003). Dongsha Atoll, Taiwan. Dark/light shading represents In addition to their chronometric value, density bands relatively low/high density. The provide insight into the sensitivity of corals to climate image contrast was adjusted for change. As anthropogenic CO2 emissions drive warming clarity using the histogram and acidification of the oceans, decreases in calcification equalization function in ImageJ rates and increases in the frequency of bleaching events are among the impacts projected for corals (Hoegh-Guldberg et al. 2007). Yet direct observations of these impacts are limited due to the difficulty of regularly monitoring reefs, especially those in remote locations. In lieu of direct observations, studies of the response of corals to climate change often rely on retrospective analyses of coral growth rates and bleaching histories, both of which have been interpreted from skeletal banding patterns (Dodge and Vaisnys 1975; Lough and Barnes 1992; Carilli et al. 2009a,b; Cantin et al. 2010; Castillo et al. 2012; Barkley and Cohen 2016). Coral growth histories are based on variations in the distance between successive annual den- sity bands (Knutson et al. 1972), and observations of the sensitivity of growth to temperature have been exploited in the reconstruction of paleotemperature records (Saenger et al. 2009). Anomalously high-density bands have been linked to known coral reef bleaching events (Hudson 1981a, b; Dodge et al. 1993; Smithers and Woodroffe 2001; Mendes and Woodley 2002; Carilli et al. 2009a, b; Cantin and Lough 2014; Mallela et al. 2015; Barkley and Cohen 2016), prompting the term ‘‘stress bands’’ and their use as proxies for past bleaching (Carilli et al. 2009a, b; Barkley and Cohen 2016). Despite the widespread application of annual density bands, and recently of stress bands, it is not entirely understood why, or how, corals accrete bands of varying density (Helmle and Dodge 2011). Published studies on the origins of coral banding generally agree that the rates of upward skeletal extension and/or the accretion of skeletal elements with variable thickness are sensitive to some environmental forcing(s) and this ultimately produces bands of variable density (e.g., Highsmith 1979; Barnes and Lough 1993; Dodge et al. 1993; reviewed in Helmle and Dodge 2011). Temperature and light are often cited as potential environmental drivers of calcification, yet they do 123 Coral Reefs not explain all the variability in density-banding patterns periods of time and then use dissepiments to investigate the (Helmle and Dodge 2011). Barnes and Lough (1993) and formation of skeletal density bands. Like Buddemeier and Taylor et al. (1993), investigating Porites, and Dodge et al. Kinzie (1975), we tracked skeletal accretion with vital (1993), investigating Orbicella, suggested that annual staining of the skeletons of living Porites spp. colonies, but density banding could arise from seasonal changes in cal- we followed Barnes and Lough (1993) in recording dis- cification rate, whereby skeletal elements of variable sepiments over [1 yr, rather than successive months. thickness are deposited over the course of a year in Within the framework of our dissepiment frequency response to annual temperature or light cycles. Comparing results, we examine the role of monthly changes in skeletal growth rates to density-banding patterns on sub-annual extension rate in the formation of both annual density timescales is one way to test these hypotheses (Barnes and bands and anomalously high-density ‘‘stress’’ bands. Lough 1993). However, without a proven sub-annual sclerochronometer, one that is independent of density bands, it has been difficult to measure seasonal variations Materials and methods in growth for comparison to skeletal density. Additional chronometers, recording frequencies Lunar rhythm between circadian and annual, may be preserved within coral skeletons. Buddemeier (1974) observed fine density Study design to test dissepiment frequency bands superposed on the more conspicuous annual bands and speculated that these fine bands may form with lunar To test for lunar periodicity of dissepiment formation, we rhythm (every *29.5 d, or *12.4 yr-1). Barnes and placed time markers in the skeletons of living Porites Lough (1989, 1993) suggested that the fine sub-annual colonies using vital stain. Critically, however, the stain is bands are related to dissepiments, thin (tens of microme- incorporated mainly at the outermost growing tip of the ters) sheets of skeleton oriented perpendicular to the main skeleton (Barnes and Lough 1993), whereas dissepiments axis of upward growth. Living coral polyps rest atop