Carbonate Mineralogy of a Tropical Bryozoan Biota and Its Vulnerability to Ocean Acidification

Marine Biology Research

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Carbonate mineralogy of a tropical bryozoan biota and its vulnerability to ocean acidification

Paul D. Taylor, Aileen Tan Shau-Hwai, Anatoliy B. Kudryavstev & J. William Schopf

To cite this article: Paul D. Taylor, Aileen Tan Shau-Hwai, Anatoliy B. Kudryavstev & J. William Schopf (2016) Carbonate mineralogy of a tropical bryozoan biota and its vulnerability to ocean acidification, Marine Biology Research, 12:7, 776-780, DOI: 10.1080/17451000.2016.1203951

To link to this article: http://dx.doi.org/10.1080/17451000.2016.1203951

Published online: 23 Aug 2016.

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Download by: [University of Wisconsin - Madison] Date: 14 December 2016, At: 14:04 MARINE BIOLOGY RESEARCH, 2016 VOL. 12, NO. 7, 776–780 http://dx.doi.org/10.1080/17451000.2016.1203951

SHORT REPORT Carbonate mineralogy of a tropical bryozoan biota and its vulnerability to ocean acidiﬁcation Paul D. Taylora, Aileen Tan Shau-Hwaib, Anatoliy B. Kudryavstevc,d and J. William Schopfc,d,e,f aDepartment of Earth Sciences, Natural History Museum, London, UK; bMarine Science Laboratory, School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia; cCenter for the Study of Evolution and the Origin of Life, University of California, Los Angeles, USA; dUniversity of Wisconsin Astrobiology Research Consortium, Department of Geosciences, University of Wisconsin, Madison, USA; eDepartment of Earth, Planetary, and Space Sciences, University of California, Los Angeles, USA; fMolecular Biology Institute, University of California, Los Angeles, USA

ABSTRACT ARTICLE HISTORY Decreasing pH levels in the world’s oceans are widely recognized as a threat to marine life. Received 7 December 2015 Bryozoans are among several phyla that produce calcium carbonate skeletons potentially Accepted 14 June 2016 affected by ocean acidification (OA). Depending on species, bryozoan skeletons can consist Published online 23 August of calcite, aragonite or have a bimineralic combination of these two minerals. Aragonite is 2016 generally more soluble in seawater than calcite, making aragonitic species more vulnerable RESPONSIBLE EDITOR fi to OA. Here, for the rst time we use Raman spectroscopy to determine the mineral Tom Fenchel composition of a tropical bryozoan biota. Compared with bryozoan biotas from higher latitudes in which calcite predominates, aragonite was found to occur in a much higher KEYWORDS proportion of the 22 cheilostome bryozoan species collected from the shorelines of Penang Bryozoa; Cheilostomata; and Langkawi in Malaysia, where 46% of species are calcitic, 41% aragonitic and 13% Malaysia; mineralogy; ocean fi bimineralic. All but one of the aragonitic or bimineralic species belong to the ascophorans, acidi cation whereas calcitic skeletons characterized most of the anascans, many of which are primitive ‘weedy’ malacostegines. These results suggest a relatively high vulnerability of tropical bryozoan faunas to OA, with the weedier taxa likely to be least impacted.

Introduction Aragonite is relatively more soluble than calcite (except Ocean acidiﬁcation (OA) is one of the results of anthro- for calcite that contains appreciable substitution of Ca pogenic CO2 emissions that is causing widespread by Mg; Ries 2011), and species having aragonite in concern because of its expected deleterious effects their skeletons may therefore be more vulnerable to on marine organisms and ecosystems. A drop in OA than calcitic species. ocean surface water pH of 0.3–0.4 units has been pre- Bryozoans are a diverse phylum of colonial metazo- dicted by the year 2100 (Caldeira & Wickett 2005). ans in which the great majority of species biomineralize

Organisms secreting skeletons composed of CaCO3 skeletons of calcium carbonate, including all species may be especially vulnerable to OA (e.g. Orr et al. belonging to the Cheilostomata, the dominant order 2005; Fabry et al. 2008), requiring more energy both of living bryozoans. Cheilostome skeletons may be to biomineralize their skeletons and also to maintain made of aragonite or calcite, or be bimineralic in them after formation as the oceans move towards which a framework of calcite is later covered by arago- being undersaturated with respect to CaCO3 minerals. nite. The mineralogy of the bryozoan skeleton is under Responses of marine organisms with calcareous a high degree of organismal control (Smith 2014; Taylor skeletons to low pH conditions are varied, although et al. 2015), although bimineralic species may exhibit in experimental studies the majority show reduced apparent ecophenotypic variability in the proportions levels of calciﬁcation (e.g. Ries et al. 2009). A range of of calcite and aragonite in their skeletons (e.g. Lom- factors may determine the extent of the burden of bardi et al. 2008; Loxton et al. 2014). decreasing pH on marine organisms having calcareous Acid-bath immersion experiments on bryozoans of skeletons, one of which is the mineralogy of the skel- differing mineralogies failed to show the expected eton. Two skeletal minerals – aragonite and calcite – greater dissolution of the skeletons of bryozoan characterize most organisms with calcareous skeletons. species containing high contents of aragonite (Smith &

CONTACT Paul D. Taylor [email protected] Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK © Crown Copyright 2016. Reproduced with the permission of the Controller of Her Majesty’s Stationery Ofﬁce and The Trustees of the Natural History Museum MARINE BIOLOGY RESEARCH 777

Garden 2012), the relative surface area of the complex skeletons were analysed, which were probably skeletons being interpreted as a more important deter- formed no more than six months prior to collection. minant. Nevertheless, the importance of mineral solu- Environmental records for Langkawi and Penang bility is strongly suggested by the latitudinal pattern show water temperatures from April to October that is evident in bryozoan mineralogy: as in molluscs ranging from 29.7 to 32.3°C, and salinities from 27 to (Taylor & Reid 1990) and serpulids (Lowenstam 1954), 33 ppt. Specimens were washed and air-dried after col- the proportion of aragonitic bryozoan species declines lection. Scanning electron microscopy was employed significantly away from the equator into colder waters for imaging and to confirm species’ identities after where the solubility of CaCO3 is greater (Kuklinski & bleaching (see Taylor & Tan 2015). Taylor 2009; Taylor et al. 2009; Taylor & Di Martino 2014). Mineralogical determinations Skeletal mineralogy is known for only a small proportion of living cheilostome species, the great The mineralogy of 22 cheilostome species was deter- majority coming from temperate or polar regions. mined using Raman spectroscopy, a non-destructive, Very few tropical cheilostomes have been analysed non-invasive and confocal method that permits mineralogically (Taylor et al. 2009; Taylor & Di Martino precise analysis at submicron (0.8 μm) resolution 2014) and there are no publications dealing with the (Taylor et al. 2008). Duplicate analyses were made mineralogical composition of a bryozoan biota from from all specimens, and mineralogical constancy was the tropics (i.e. between 23.5°N and 23.5°S latitude). also checked by analysing more than one colony for This paper presents the first mineralogical survey of a some of the species. Unequivocal identification of tropical bryozoan biota, based on shore collections calcite and aragonite is possible because the Raman made in Penang and Langkawi, Malaysia during 2013 spectra for these two minerals are readily distinguish- (Taylor & Tan 2015). We employed Raman spec- able. These mineralogical analyses were undertaken troscopy, a precise and non-destructive method of using a T64000 triple-stage laser-Raman system analysis, to determine the mineralogies of 22 species equipped with a Coherent Innova 90 argon ion laser of cheilostomes. Our findings are discussed in the projected through an Olympus 154 BX41 microscope

context of the latitudinal increase in aragonitic bryozo- in the Schopf lab (UCLA). Point spectra were obtained ans towards the tropics and their enhanced vulner- from the frontal walls of the bryozoan zooids. When ability to OA, as well as the taxonomic correlation of these walls proved to be aragonitic, additional analyses cheilostome bryozoan mineralogy. were made of orificial rims, basal walls and/or avicular- ian crossbars to test for a bimineralic composition as one or more of these structures will be calcitic in bimi- Materials and methods neralic species (Taylor et al. 2008). Localities and collection Results The bryozoans used in this study were collected during a reconnaissance survey of the shorelines of Penang As is shown in Table I, 10 (46%) of the 22 species ana- and Langkawi during October 2013. Situated off the lysed were found to be calcitic, nine (41%) aragonitic west coast of the Malaysian Peninsula, Penang is an and three bimineralic (13%). The 11 anascan-grade island in the Strait of Malacca, at latitude 5°N. Langkawi cheilostomes were predominantly calcitic; only one is an archipelago of islands 80 km north of Penang in species – Cranosina coronata (Hincks, 1881) – was aragon- the Andaman Sea, at latitude 6°N. The four sites itic (Figure 1). In contrast, none of the 11 ascophoran- sampled at Penang and the eight sites at Langkawi grade cheilostomes had a calcite skeleton: eight were yielded a total of 23 species of cheilostome bryozoans entirely aragonitic and three species were bimineralic (site details, species descriptions and specimen reposi- (Hippopodina feegeensis (Busk, 1884), Schizoporella tory information can be found in Taylor & Tan 2015); japonica Ortmann, 1890 and Microporella sp.). one species, Antropora minor (Hincks, 1880), was rep- resented by a single colony deep within a gastropod Discussion shell and could not be analysed. Some of the bryozoans fouled man-made structures, such as pier wharves, Judging from the limited previously available data, the fishing floats and plastic objects, whereas others proportion (54%) of cheilostome species biomineraliz- encrusted mollusc shells or rocks. All occurrences are ing aragonite, either alone or in combination with from shallow water. Only relatively new parts of the calcite, matches expectations for a tropical bryozoan 778 P. D. TAYLOR ET AL.

Table I. Results of the Raman spectroscopic mineralogical analyses of Malaysian cheilostome bryozoans. Species Family Locality Mineralogy Aetea ligulata Busk, 1852 Aeteidae Kampung Kuala Temoyong, Langkawi Calcitic Acanthodesia cf. falsitenuis (Liu, 1992) Membraniporidae Kampung Kuala Temoyong, Langkawi Calcitic Acanthodesia cf. irregulata (Liu, 1992) Membraniporidae Pulau Betong, Penang Calcitic Acanthodesia perambulata (Louis & Menon, 2009) Membraniporidae Pantai Pasir Hitam, Langkawi Calcitic Jellyella eburnea (Hincks, 1891) Membraniporidae Pantai Chenang, Langkawi Calcitic Arbopercula sp. Electridae Pulau Betong, Penang Calcitic Sinoﬂustra amoyensis (Robertson, 1921) Sinoﬂustridae Batu Muang, Penang Calcitic Cranosina coronata (Hincks, 1881) Calloporidae Pantai Pasir Hitam, Langkawi Aragonitic Nellia oculata Busk, 1852 Quadricellariidae Balik Pulau, Penang Calcitic Bugula neritina (Linnaeus, 1758) Bugulidae Batu Uban, Penang Calcitic Cradoscrupocellaria sp. Candidae Kuah Jetty, Langkawi Calcitic Adeonella lichenoides (Lamarck, 1816) Adeonidae Kampung Kuala Temoyong, Langkawi Aragonitic Celleporaria aperta (Hincks, 1882) Lepraliellidae Kampung Kuala Temoyong, Langkawi Aragonitic Parasmittina raigioidea Liu in Liu et al., 2001 Smittinidae Pulau Betong, Penang Aragonitic Parasmittina winstonae Liu, 2001 Smittinidae Kuah Jetty, Langkawi Aragonitic Parasmittina sp. 1 Smittinidae Kuah Jetty, Langkawi Aragonitic Parasmittina sp. 2 Smittinidae Kampung Kuala Temoyong, Langkawi Aragonitic Hippoporina indica Madhavan Pillai, 1978 Bitectiporidae Pulau Betong, Penang Aragonitic Schizoporella japonica Ortmann, 1890 Schizoporellidae Kuah Jetty, Langkawi Bimineralic Hippopodina feegeensis (Busk, 1884) Hippopodinidae Pantai Pasir Hitam, Langkawi Bimineralic Microporella sp. Microporellidae Kampung Kuala Temoyong, Langkawi Bimineralic Scorpiodinipora costulata (Canu & Bassler, 1929) Hippoporidridae Pulau Betong, Penang Aragonitic Note: The mid-table line divides anascan-grade species above from ascophoran-grade species below.

Figure 1. Mineralogical compositions of cheilostome bryozoan biotas from different latitudes. Note the increasing proportion from the poles to the tropics of species biomineralizing aragonite, either monomineralically (a, pale grey) or bimineralically with calcite (b, mid grey), and the corresponding decrease in calcitic species (c, dark grey). As noted by Kuklinski & Taylor (2009), the one record (Borisenko & Gontar 1991) of an aragonitic bryozoan species in the Antarctic is questionable (see also Krzeminska et al. 2016 who found no aragonitic bryozoans in their samples from King George Island, Antarctica). MARINE BIOLOGY RESEARCH 779 biota. Taylor et al. (2009) compiled published analyses more aragonite would be expected in bryozoans of the mineralogy of 37 cheilostome species between from deeper parts of the Malaysian shelf and the con- latitudes 30°N and 30°S and added new analyses, trast with regions of higher latitude would be even finding 24% of the species to be aragonitic, 38% to greater. be calcitic and 38% bimineralic. Taylor & Di Martino A relatively high proportion (26%) of the sampled (2014) used Raman spectroscopy to determine the bryozoan biota from Penang and Langkawi in Malaysia mineralogy of 23 cheilostome species encrusting the consists of malacostegines. Typically, malacostegines undersides of plate-like scleractinian corals from reefs account for less than 10% of cheilostomes in higher in Puerto Rico and Peninsular Malaysia, finding 10 latitude biotas; for example, of the 262 cheilostome (43%) of these species to be calcitic, six (27%) aragon- species listed from the Italian biota by Rosso et al. itic and seven (30%) bimineralic. (2010), only 12 (4.6%) are malacostegines. Malacoste- The new data presented here on the skeletal miner- gines are primitive cheilostomes characterized by alogy of the cheilostome biota from Penang and Lang- planktotrophic larvae that are not brooded. This con- kawi make it possible for the first time to contrast the trasts with the brooded lecithotrophic larvae of the mineralogy of a tropical biota with biotas from higher neocheilostomes occurring in the great majority of latitudes (summarized by Kuklinski & Taylor 2009, cheilostome bryozoan species. All of the Malaysian Figure 1). malacostegines were found to have calcitic skeletons. Figure 1 compares the mineralogical compositions Indeed, calcitic skeletons are almost ubiquitous of polar (Arctic and Antarctic), northern temperate among malacostegines (Taylor et al. 2009), a notable (Mediterranean), southern temperate (Chile and New exception being the algal epiphyte Membranipora. Zealand) and tropical (Malaysia) cheilostome bryozoan Smith & Clark (2010: 231) commented on the mineralo- biotas. There is a strong and consistent increase in the gical variability within putative Membranipora membra- proportion of aragonitic species towards the equator, nacea (Linnaeus, 1767) from several localities around with a corresponding decrease in calcitic species. This the globe, noting that some analyses found it to be ara- pattern is partly due to latitudinal changes in the gonitic, others calcitic, and yet others bimineralic. The mineralogies of widely distributed genera, and partly related M. isabelleana (d’Orbigny, 1847) from Chile

to the differences in genera present in the tropics com- has an aragonitic skeleton (Smith & Clark 2010). pared with higher latitudes. For example, the four These two species of Membranipora apart, malacoste- species of the cosmopolitan genus Parasmittina ana- gines have retained the calcitic skeleton that is lysed from Malaysia were found to have aragonitic skel- primitive for cheilostomes (Taylor et al. 2009). etons, whereas previous analyses of the skeletal Malacostegines seldom have defensive polymorphs composition of other species of this genus from (Taylor 1987) and may be characterized as ‘weedy’ higher latitudes showed them to be calcitic or bimi- bryozoans that grow particularly rapidly: in a recent neralic (see Taylor et al. 2009: supplementary material compilation of bryozoan growth rates (Smith 2014: S 3). On the other hand, the specimen of Cranosina ana- supplemental data table 1), the two malacostegine lysed in this study, a genus known to occur only in the species M. membranacea and Einhornia crustulenta tropics of the Indo-Pacific, Hawaii and Caribbean (Chi- (Pallas, 1766) showed the highest growth rates. monides & Cook 1994) and not at higher latitudes, Assessment of the relative vulnerabilities of bryozo- was found to be aragonitic. ans to ocean acidification is complicated (see Fortunato Sampling depth is a potential confounding factor in 2015 and references therein) and the skeletal mineralo- the latitudinal comparisons shown in Figure 1. All of the gies of different species must certainly be taken into bryozoans from Langkawi and Penang are shore account. The first analysis of a tropical cheilostome samples of colonies from very shallow water (<10 m), biota presented here show that it is particularly rich whereas many of the bryozoans reported in previous in species that biomineralize aragonite, the more publications came from mid- to outer shelf depths. soluble of the two polymorphs of CaCO3 occurring in Analyses of bryozoan assemblage mineralogy relative skeletonized marine organisms. All of the cheilostome to depth on the continental shelf are lacking, although species from Penang and Langkawi in Malaysia that Loxton et al. (2014) found a positive correlation have entirely calcitic skeletons are of anascan-grade between depth and the proportion of aragonite in skel- and include many primitive malacostegines known or etons of the bimineralic cheilostome Microporella inferred to possess planktotrophic larvae. On the ciliata (Pallas, 1766) in NE Scotland. The generality of basis of biomineralogy alone, ocean acidification can this trend within and among species is unknown but be expected to impact tropical bryozoan biotas to a if applied to the latitudinal comparisons made here greater extent than those of higher latitudes, affecting 780 P. D. TAYLOR ET AL. ascophoran-grade species most and ‘weedy’ malacos- Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, et al. tegine anascans least. 2005. Anthropogenic ocean acidification over the twenty- first century and its impact on calcifying organisms. Nature 437:681–86. doi:10.1038/nature04095 Acknowledgements Poluzzi A, Sartori R. 1975. Report on the carbonate mineralogy of Bryozoa. Documents des Laboratoires de We are grateful to Ivan Chinon Yaman, Woo Sau Pin and Poi Géologie de la Faculté des Sciences de Lyon, Hors Serie Khoy Yen for assistance during fieldwork. 3:193–210. Ries JB. 2011. Skeletal mineralogy in a high-CO2 world. 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