Reference: Biol. Bull. 226: 203–210. (June 2014) © 2014 Marine Biological Laboratory
Growth and Calcification of Marine Bryozoans in a Changing Ocean ABIGAIL M. SMITH* Department of Marine Science, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand
ogists are more familiar with them than are biologists. In the southern hemisphere, however, this colonial invertebrate phylum has been gaining attention. Here they are common components of habitats deep-sea to shelf, sometimes forming large and spectacular complex habitats in shelf-depths (Wood et al., 2012). Bryozoans are colonial organisms, formed from repeated identical modules called zooids, and they can adopt forms ranging from encrusting to erect to massive (Hageman et al., 1998). Many marine bryozoans are heavily calcified, utilizing a wide range of biominerals (Smith et al., 2006). Large erect bryozoans may become ecosystem engineers and create framework habitat that enhances biodiversity (Lombardi et al., 2014; Wood et al., 2012). Bryozoans are important sediment-formers on southern temperate shelves (Taylor and James, 2013); skeletons may form up to 95% of extensive cool-water carbonate deposits on southern shelves (e.g., Nelson et al., 1988). Of the about 20,000 known species of bryozoans (sometimes known as moss animals or lace corals), about 5869 remain extant (Bock and Gordon, 2013). They fall into three classes, of which the Phylactolaemata are uncalcified and found in freshwater, and are not further considered here. The oldest class, Stenolaemata, has only one extant order: the marine calcified Cyclostomatida with characteristic tube-shaped zooids forming colonies that vary from encrusting to branched to massive. Class Gymnolaemata includes the uncalcified order Ctenostomata and the youngest order, Cheilostomatida, with typically box-shaped zooids; it is this speciose (4921 extant species) order that provides most mineralogical variability (Bock and Gordon, 2013; Smith et al., 2006). A colonial organism is hard to age. While one may be able to characterize the rate of calcification of an individual zooid, how does that relate to the growth of a whole colony? Growth studies of bryozoans have been hampered by their cryptic habits, deep-water distribution, slow growth rates,
Abstract. Bryozoans are colonial benthic marine invertebrate calcifiers, important and especially abundant and diverse in southern hemisphere shelf environments. Large heavily calcified colonies can be up to 50 years old, but most longer-lived bryozoans are limited to 10 –20 y. Many smaller species are annual. Radial extension in flat encrusting bryozoans is generally on the order of 1–5 mm/y. Erect calcified species generally grow vertically 2–15 mm/y, though articulated species such as Cellaria may reach rates of 40 mm/y. Corresponding calcification rates are generally 101–102 mg/y, but there can be an order of magnitude variation in rate among years in high-latitude bryozoans. Multi-branched bryozoans produce up to 24 g of CaCO3/y. The carbonate produced by bryozoans varies from calcite to aragonite and mixtures of both. Skeletal carbonate mineralogy of bryozoans is complex and appears to be strongly genetically controlled. Global climate change, leading to increasing water temperatures, will generally increase marine bryozoan metabolic rates, and may increase Mg in calcite. On the other hand, decreasing pH (ocean acidification) causes corrosion, changes in mineralogy, and decreased survival. This review of bryozoan growth and calcification allows a general perspective, but also reveals gaps in our knowledge which need to be addressed. Introduction Bryozoans have been described as a minor phylum, and it is true that the combination of being inedible, small, difficult to identify, and currently found mainly in cryptic habitats has resulted in a low profile for this taxon in invertebrate textbooks (and indeed among the wider public). The fossil record of the Bryozoa is extensive, so that paleontolReceived 24 October 2013; accepted 17 March 2014. * To whom correspondence should be addressed. E-mail: abby. [email protected] 203
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small sizes, difficulty of culture, and paucity of workers. And yet, understanding growth and calcification rates in bryozoans may be a critical part of understanding carbonate sediment budgets and the complex interactions of mineralogy, morphology, and dissolution (Smith, 2009), particularly over geologic time (Taylor and James, 2013). This paper reviews what is known about age, growth, and calcification in bryozoans and how they may be affected by changing ocean climate, particularly rising temperatures and increasing acidity. Skeletal carbonate mineralogy in this phylum is reasonably well-known, so only a summary is provided, after which the information is collated in order to make some general predictions about the likely effects of a changing ocean climate on bryozoans, and the likely utility of bryozoans in the study of changing oceans. Growth and Age in Bryozoan Colonies Growth and longevity information about bryozoans is scarce. While some studies do report growth as increases in branch length, colony diameter, colony area, or number of zooids over time (e.g., Stebbing, 1971; Ryland, 1976; Vail and Wass, 1981;Winston and Jackson, 1984; Pätzold et al., 1987; Stanwell-Smith and Barnes, 1997), they are mainly about weakly calcified or encrusting species that have low biomass and do not produce much sediment. Growth and age in large erect bryozoan colonies have been quantified using direct methods, including studies of morphological features by in situ measurements and photographs (Jackson and Winston, 1981; Barnes, 1995; Brey et al., 1998; Cocito et al., 1998, 2003; Barnes et al., 2006); mark and recapture techniques (Smith et al., 2001); and laboratory cultures (Kahle et al., 2003; Amui-Vedel et al., 2007). While direct methods of age determination are generally reliable, especially in situ, they are often of limited duration (usually no more than months). Indirect methods of studying growth, such as stable isotope analysis (Pätzold et al., 1987; Brey et al., 1998; Smith et al., 2001; Smith and Key, 2004; Bader and Schäfer, 2005) or growth-check lines (Stebbing, 1971; Brey et al., 1998; Bader and Schäfer, 2004; Barnes et al., 2006, 2007; Smith, 2007) provide tools for quantifying growth over longer periods of time, as well as in extinct species. Morphological growth-check analyses have the benefit of being non-destructive, and therefore specimens can be used for additional analyses (Smith et al., 2001; Smith and Lawton, 2010). Isotope studies, on the other hand, have the highest resolution because sample volume can be smaller. We have searched the literature and found measured and estimated growth rates and maximum ages for 44 bryozoan species (Supplementary Data Table 1 http://www.biolbull. org/content/supplemental), about 0.7% of described extant species. Different studies report different measurements and units, so the published data have been recalculated to stan-
dard measures as far as possible. As might be expected, the vast majority of the species studied are conspicuous and large. There are 18 (41% of 44) encrusting species, mostly unilaminar. Among the erect species, six (14% of 44) species are rigid branching and one is foliose. The remaining 19 species (43% of 44) are either flexible branching, articulated branching, or erect with a flexible base. The notion of age in a colonial organism is complex, as individuals (zooids) may live less than a year, whereas the colony may persist for decades. The longest-living bryozoan colony known is a specimen of Melicerita obliqua from Antarctica that was 200 mm tall and calculated to have an age of 50 y (Brey et al., 1998; Bader and Schäfer, 2004). In general, long-lived bryozoan colonies reach a maximum age of 10 –20 y. There are many species not represented here, however, that are probably annual, for whom maximum age is a single growing season. Linear growth in encrusting bryozoans (that is, the extension of radius in a year) generally varies from 1 to over 10 mm/y (approx. mean of those in Supplementary Data Table 1 ⫽ 3.2 mm/y with outliers removed, n ⫽ 14), which, assuming it is a circular colony, equates to an increase in surface area of about 20 to 50 mm2 in one year. An unusually fast-growing opportunistic Arctic bryozoan, Einhornia crustulenta, reportedly grew a colony covering 8290 mm2 in 8 months (Kuklinski et al., 2013), equivalent to a 77-mm radial extension per year and 12,400 mm2/y. Erect branching or blade-shaped colonies with a flexible, rooted base grow more rapidly than their encrusting counterparts, from 2 to 15 mm/y extension in overall colony height (mean ⫽ 5.4 mm/y with outliers removed, n ⫽ 15). Erect rigid branching or foliose colonies may grow even faster, at 7 to 20 mm/y (mean ⫽ 11.0 mm/y with outliers removed; n ⫽ 6). Bryozoans appear to reach their greatest linear extension rate in erect flexible articulated species (e.g., Cellaria sp.), where linear growth rate ranges from 10 to 40 mm/y, if the assumption that internodes are annual is correct (e.g., Bader and Schäfer, 2005). In all these cases there is probably a bias based on species selected for study. Researchers are more likely to study those species that are conspicuous and ecologically relevant. A significant number of species studied form part of investigations of polar ecology (28 of the 44 species listed in Supplementary Data Table 1 are from the Arctic or Antarctic regions), places where longevity is often coupled with slow annual growth (Smith and Lawton, 2010). And, some of the results reported form part of experiments designed to determine controls on growth rate, rather than reporting natural growth rates. Membranipora membranacea grows on kelp fronds at rates varying from 0.01 to 12.0 mm/day (linear extension) (Saunders and Metaxas, 2009). The major determinant of growth rate is colony size; larger colonies grow faster
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(Saunders and Metaxas, 2009). Temperature is also positively correlated with growth rate, at least when colonies are not competing for space, but food availability is not. Other factors proposed but not investigated include flow rates, competition, and reproductive status (those with many reproductive zooids may grow more slowly). Bryozoans generally grow more slowly at higher latitudes, presumably reflecting lower water temperatures, which reduce metabolic rate (Barnes et al., 2006). Slower polar growth may also reflect food availability and light limitation in winter (Kuklinski et al., 2013). Many polar bryozoans show “growth-check lines,” which indicate cessation of growth during winter (Barnes, 1995; Barnes et al., 2006; Smith, 2007). Competition levels can also be important in determining growth rate. Kuklinski et al. (2013) found extremely high growth rates in a brackish-water opportunist bryozoan with few competitors in the Baltic Sea. Bryozoans that experience spatial competition, on the other hand, may find their capacity for growth limited (Barnes et al., 2006). Calcification Mechanisms in Bryozoans Skeletal material in many marine invertebrates is not entirely mineral; it is often bound up with organic material. The majority of this organic tissue is made up of hydrophobic, cross-linked framework macromolecules, which provide a structure for the action of the less-common control macromolecules, a diverse group of large biomolecules related to proteins and polysaccharides, with charged groups that enable interaction with mineral ions (Weiner and Addadi, 1997). It is these macromolecules that control the process of calcification. In the case of molluscs, for example, crystallization is induced on a pre-constructed epithelial matrix (Simkiss and Wilbur, 1989), whereas in corals, crystals are formed in an extracellular fluid containing the necessary ions (Allemand et al., 2004). Mode of calcification in bryozoans is very little studied, and essentially unknown. One early study of calcification in a simple cheilostome bryozoan (Membranipora) suggests that calcification begins after differentiation of the cells is achieved (Lutaud, 1987). Calcium ions are released into intracellular spaces, with subsequent impregnation of organic matrix with calcium salts (Lutaud, 1987). This build-up of calcium in the cuticular matrix occurs before any crystallization takes place (Ryland, 1976). Aragonite or calcite crystals are precipitated on the matrix, with the choice of mineralogy possibly determined by amino acid composition of the cuticle itself, or by ions present in the intercellular fluids. These crystals are incorporated into the zooid walls as spheres, which may coalesce and develop into threads (Ryland, 1976) and eventually many other ultrastructural forms (see, e.g., Sandberg, 1977). At the colony scale, basal walls are generally formed
Figure 1. Astogenetic change along bryozoan colonies from southern New Zealand: (A) Melicerita chathamensis; (B) Odontionella cyclops. The youngest zooids (toward the left) show the basal wall forming first, then development of marginal walls, and finally the frontal shield. Further calcification with age shows development of ovicells, avicularia, and secondary thickening (toward the right). Scale bar is 1 mm.
first from the proximal part of the zooid, with marginal walls following and the frontal shield last (Fig. 1). Detailed studies of the calcification mechanisms in bryozoans are long overdue. Recent developments in understanding of calcification in corals should allow similar progress in bryozoans over the coming decade. While it will be natural to begin with lightly calcified very well known bryozoans (e.g., Celleporella hyalina), we will eventually have to turn our attention to well-calcified slow-growing temperate taxa such as Pentapora. Evaluating the effects of
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environment on calcification requires this basic level of understanding. Calcification Rates in Bryozoans Biologists do not ordinarily weigh bleached colonies, and thus do not usually report on production of calcium carbonate. When carbonate production is calculated, it is usually on the basis of colonies of known age or turnover rate (Smith and Nelson, 1994; Cocito and Ferdeghini, 2001), so that the carbonate production rate reported is a mean over the age of the colony. For short-lived bryozoans (of less than 10-y maximum age), this figure is probably accurate (see, e.g., Smith and Haderlie, 1969), and generally lies in the range of 101–102 of mg CaCO3/y. In colder waters, however, bryozoans may live several decades (Barnes, 1995; Brey et al., 1998; Bader and Schäfer, 2004). Mean annual carbonate production is a more useful measure in these longer-lived bryozoans, if accompanied by some understanding of annual variation. The size and weight of annual production, however, is difficult to ascertain. Longer-lived colonies are not readily cultured. Oxygen isotopes have been shown to provide age-markers (e.g., Pätzold et al., 1987), but destructive sampling methods render this approach incompatible with carbonate production measurement. What is needed is a well-marked morphological signal (such as an annual growth band), and these are available in some polar (Barnes, 1995; Barnes et al., 2007; Smith, 2007) and temperate (Smith and Lawton, 2010) species. Growth in polar bryozoans varies considerably from year to year (Smith, 2007). Calcification in Cellarinella nutti, for example, ranges from 3 to 57 mg/y (mean ⫽ 22 mg/y, std dev ⫽ 11 mg/y, n ⫽ 59), C. nodulata from 5 to 33 mg (mean ⫽ 18 mg/y, std dev ⫽ 8 mg/y, n ⫽ 27), and Swanomia belgica from 1 to 22 mg/y (mean ⫽ 8 mg/y, std dev ⫽ 2 mg/y, n ⫽ 50) (see Supplementary Data Table 1). These species are all either unbranched or very seldom branching. Cellarinella watersi, in contrast, produces an order of magnitude more carbonate per year due to its more highly branched habit, between 100 and 200 mg/y (Barnes, 1995). Temperate bryozoans are generally missing the conspicuous growth-checks that allow for inter-annual comparison, but there are exceptions. The poorly calcified Flustra foliacea has recognizable annual growth bands (Stebbing, 1971), as does the rather more robust blade-shaped Melicerita chathamensis (Smith and Lawton, 2010). Segments from 41 colonies of M. chathamensis collected off southern New Zealand ranged from 1 to 37 mg (mean ⫽ 9 mg, std dev ⫽ 7 mg, n ⫽ 236): annual production by individuals of 1–37 mg/y. Carbonate production in the New Zealand fiords by Adeonellopsis sp. is many orders of magnitude larger— 23,700 mg/y—again partly because of its many-branched growth habit (Smith et al., 2001). Such multi-branched
bryozoans have the capacity to produce more carbonate over their longer lives. Variability among years that spans an order of magnitude means that average estimates over the full age of the colony have minimal ecological meaning (Wejnert and Smith, 2008). Longer-lived bryozoans appear to be able to calcify faster and more robustly when food supply and temperatures are sufficient, and to slow their growth under poorer conditions (Smith 2007). Skeletal Carbonate Mineralogy of Bryozoans Bryozoans may be the most mineralogically well-characterized invertebrate phylum. Certainly details of mineralogical complexity are better known in this taxon than in others of a similar biodiversity. Supplementary Data Table 2 (http://www.biolbull.org/content/supplemental) delineates what is known about skeletal carbonate mineralogy in 606 species of bryozoans, almost 10% of extant species. Regional studies (particularly Schopf and Manheim, 1967; Rucker and Carver, 1969; Schopf and Allan, 1970; Siesser, 1972; Poluzzi and Sartori, 1973, 1974; Smith et al., 1998) revealed a complex mineralogical suite in the marine bryozoan classes Gymnolaemata and Stenolaemata. Later workers tried to summarize bryozoan mineralogy, noting the dominance of calcite (e.g., Lowenstam and Weiner, 1989); the addition of aragonite in secondary calcification (Sandberg, 1983); the presence of entirely aragonitic bryozoans (Sandberg, 1983); and the presence of bimineralic forms, some with highly organized biominerals and others with fairly amorphous mixtures (Bone and James, 1993). More recently, the presence of two distinct calcites (dominant low-Mg calcite and subdominant high-Mg calcite) has been documented in a few anascan cheilostomes (Smith et al., 1998; Bader and Schäfer, 2005). The notion of biomineral space has been used to characterize the mineralogical variability in taxa, with the phylum Bryozoa as a whole occupying 63% of the space available for biomineralization (Smith et al., 2006). The phylum is thus highly variable and repays detailed investigation. The majority (about 2/3) of bryozoans are entirely calcitic, including essentially all of the extant stenolaemates (Smith et al., 2006). Of the remainder, about half are entirely aragonitic (Smith et al., 2006), and half are bimineralic. Three groups of bimineralic skeletons have been described: (A) mainly aragonite with small areas formed from calcite (e.g., Adeonellopsis sp.; Wejnert and Smith, 2008), (B) mainly low-Mg calcite with increasing amounts of high-Mg calcite with age (e.g., Melicerita chathamensis; Smith and Lawton, 2010), and (C) mainly calcite with secondary thickening by aragonite over time (e.g., Odontionella cyclops; Smith and Girvan, 2010). Mg in bryozoan calcite ranges from zero to 14 wt%
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MgCO3 (0 to 16 mol% MgCO3). When two calcites co-exist in a single skeleton (as occurs in a few anascan cheilostomes), the low-Mg mineral is about 2– 4 wt% MgCO3, and the high-Mg mineral ranges from 7 to 11 wt% MgCO3 (Smith et al., 2006). Phylogenetic influence on skeletal carbonate mineralogy in marine bryozoans is considerable. Stenolaemates, including the cyclostomes, form their skeletons almost entirely of low-Mg calcite; mineralogical complexity is provided by the gymnolaemate cheilostomes (Smith et al., 2006). Some cheilostome families are more consistent in their mineralogy (e.g., Cupuladriidae). Others, such as the Cellariidae, have a wider range of Mg content but are always calcitic. In contrast, there are a few families in which Mg content varies less but the calcite/aragonite ratio is more highly variable, such as the Margarettidae. The most mineralogically variable families are the Phidoloporidae and Membraniporidae, both of which occupy over 50% of available biomineral space (Smith et al., 2006). Polar bryozoans from both the Arctic (Kuklinski and Taylor, 2008, 2009) and Antarctic (Borisenko and Gontar, 1991) are dominated by calcite, with lower Mg content than is the norm in warmer waters. Many studies have commented on an apparent decrease in aragonite and Mg in calcite with increasing latitude, but detailed temperature- or latitude-related trends in mineralogy, such as those reported by Rucker and Carver (1969), have very likely been confounded by phylogenetic factors and cannot be considered anything other than vaguely indicative until phylogenetically independent statistical analysis has been carried out (e.g., Smith et al., 2013) to tease apart the environmental and phylogenetic signals. Cheilostome bryozoans mineralogically precipitate their skeletons out of equilibrium with seawater, sometimes precipitating more than one mineral, usually with organized and consistent ultrastructure (Taylor et al., 2008). They can thus be considered “active” or “controlling” biomineralizers (sensu Lowenstam and Weiner, 1989), as are molluscs and echinoderms, and in contrast to most “passive” biomineralizers such as algae and corals, which are more limited in their control of biomineralization (Ries, 2010). Suggestions that secular changes in seawater chemistry have driven the evolution of cheilostome bryozoans (e.g., Stanley and Hardie, 1998) are unsupported by fossil data or by the timing of major changes in mineralogy (Taylor et al., 2009), though it is possible that skeletal mineralogy at first appearance was affected by seawater chemistry at the time (Kiessling et al., 2008; Taylor, 2008). Cheilostome bryozoans are unlike the passive mineralizers that reflect seawater chemistry in their skeletons (see, e.g., Ries, 2004); it appears that they control the mineralogy of their skeletons despite the composition of seawater.
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Effects of the Changing Ocean Water temperature affects zooid size and growth rate in bryozoans over a range of scales. Zooid size within and among colonies appears to be generally correlated with seasonal changes in mean water temperature (Okamura and Bishop, 1988; O’Dea and Okamura, 1999; O’Dea et al., 2007). Within species, growth is enhanced by increasing temperature (e.g., Lombardi et al., 2006, 2008; Saunders and Mataxas, 2009). Overall, higher latitude bryozoans tend to grow relatively more slowly, presumably due to slower metabolic rates in cold waters (Smith and Lawton, 2010). Initial studies are showing that growth rates in some polar invertebrates have increased over the last few decades as the water warms and the winter period becomes shorter (e.g., Barnes et al., 2011). Ocean warming and lowered pH interacted to affect growth rate in the Australian cheilostome bryozoan Celleporaria nodulosa (Durrant et al., 2013). Growth was significantly decreased in lower-pH winter tests, whereas in summer it was higher temperatures that reduced growth rate. Saderne and Wahl (2013), on the other hand, found that present-day up-welling CO2 concentrations (about 1200 atm) enhanced the growth of kelp-encrusting bryozoans Alcyonidium hirsutum and Electra pilosa, and even higher projected CO2 levels (3150 atm) showed no effect on growth, except to remove the skeleton of E. pilosa. More heavily calcified bryozoans, however, do not fare well in lower-pH waters: Schizoporella errata showed skeletal corrosion and less investment in defensive heteromorphs (Lombardi et al., 2011a), and the larger Mediterranean bryozoan Myriapora truncata showed dissolution and lowered Mg in skeletal calcite under elevated pCO2 (Lombardi et al., 2011b). It might be expected that mineral composition would affect dissolution rate of bryozoan carbonates. Crystalline inorganic aragonite is more soluble than calcite and in a strict chemical experiment will dissolve sooner and faster (Weiner and Addadi, 1997). Biominerals in the real ocean are, however, very different. Laboratory dissolution experiments have shown that it is reactive surface area that determines dissolution rate in biogenic carbonates, with composition making little or no difference (Smith et al., 1992; Smith and Garden, 2013). Reactions of invertebrates to a changing marine environment are complex and problematic. Even though bryozoans have been very little studied in this regard, there is reason to suppose that the increasing temperatures and decreasing pH of the global ocean will have mainly negative effects on the calcification and growth of these invertebrates. Bryozoans offer considerable advantages to the study of the effects of a changing ocean. They occur naturally in a wide range of skeletal morphologies and mineralogies.
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Within a bryozoan colony, mineralogical and morphological responses to changing seawater can be traced in a series of genetically identical clones (e.g., Pistevos et al., 2011). It is possible to study seawater-driven changes in calcite/ aragonite ratio, in Mg content in calcite, or in ratios between low- and high-Mg calcite in bryozoans. Recommendations It is essential to the understanding of bryozoan calcification to discern the mechanisms and underlying biochemistry that enables calcification. Recent methodological advances in understanding coral calcification may be relevant and helpful here, as corals too are small and colonial. Growing calcifying bryozoans in water with different Mg/Ca ratios, following the experiments of Ries (e.g., 2004, 2010), would allow for a greater understanding of the degree to which skeletal mineralogy is “hard-wired” in cheilostomes, and thus how much flexibility they may be able to bring to changes in seawater chemistry. Not one study has measured the effect of temperature or seawater chemistry on early life stages in bryozoans (as suggested by Byrne, 2011). Larval development, survival, and recruitment in changing environmental conditions are an obvious area for fruitful study. Acknowledgments The author’s long-term commitment to bryozoan skeletal studies began in the laboratory of Prof. C.S. Nelson, Earth Sciences, University of Waikato, whose support is gratefully acknowledged. Colleagues and students who have collaborated over the years are also thanked: D.P. Gordon; M.M. Key, Jr.; H.G. Spencer; P.D. Taylor; K.E. Wejnert; E.I. Lawton; E. Girvan; C.J. Garden; D.I. Winter. This manuscript was improved greatly by comments from M.M. Key, Jr. and A.C.L. Wood. Literature Cited Allemand, D., C. Ferrier-Pages, P. Furla, F. Houlbreque, S. Puverel, S. Reynaud, E. Tambutte, S. Tambutte, and D. Zoccola. 2004. Biomineralisation of reef-building corals: from molecular mechanisms to environmental control. C. R. Palevol. 3: 453– 467. Amui-Vedel, A., P. J. Hayward, and J. S. Porter. 2007. Zooid size and growth rate of the bryozoan Cryptosula pallasiana Moll in relation to temperature, in culture and in its natural environment. J. Exp. Mar. Biol. Ecol. 353: 1–12. Bader, B. 2000. Life cycle, growth rate and carbonate production of Cellaria sinuosa. Pp. 136 –144 in Proceedings of the 11th International Bryozoology Association Conference, A. Herrera Cubilla and J. B. C. Jackson, eds. Smithsonian Tropical Research Institute, Balboa, Panama. Bader, B., and P. Schäfer. 2004. Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. J. Nat. Hist. 38: 2901–2922. Bader, B., and P. Schäfer. 2005. Impact of environmental seasonality on stable isotope composition of skeletons of the temperate bryozoan
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Growth and Calcification of Marine Bryozoans in a Changing Ocean ABIGAIL M. SMITH* Department of Marine Science, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand
ogists are more familiar with them than are biologists. In the southern hemisphere, however, this colonial invertebrate phylum has been gaining attention. Here they are common components of habitats deep-sea to shelf, sometimes forming large and spectacular complex habitats in shelf-depths (Wood et al., 2012). Bryozoans are colonial organisms, formed from repeated identical modules called zooids, and they can adopt forms ranging from encrusting to erect to massive (Hageman et al., 1998). Many marine bryozoans are heavily calcified, utilizing a wide range of biominerals (Smith et al., 2006). Large erect bryozoans may become ecosystem engineers and create framework habitat that enhances biodiversity (Lombardi et al., 2014; Wood et al., 2012). Bryozoans are important sediment-formers on southern temperate shelves (Taylor and James, 2013); skeletons may form up to 95% of extensive cool-water carbonate deposits on southern shelves (e.g., Nelson et al., 1988). Of the about 20,000 known species of bryozoans (sometimes known as moss animals or lace corals), about 5869 remain extant (Bock and Gordon, 2013). They fall into three classes, of which the Phylactolaemata are uncalcified and found in freshwater, and are not further considered here. The oldest class, Stenolaemata, has only one extant order: the marine calcified Cyclostomatida with characteristic tube-shaped zooids forming colonies that vary from encrusting to branched to massive. Class Gymnolaemata includes the uncalcified order Ctenostomata and the youngest order, Cheilostomatida, with typically box-shaped zooids; it is this speciose (4921 extant species) order that provides most mineralogical variability (Bock and Gordon, 2013; Smith et al., 2006). A colonial organism is hard to age. While one may be able to characterize the rate of calcification of an individual zooid, how does that relate to the growth of a whole colony? Growth studies of bryozoans have been hampered by their cryptic habits, deep-water distribution, slow growth rates,
Abstract. Bryozoans are colonial benthic marine invertebrate calcifiers, important and especially abundant and diverse in southern hemisphere shelf environments. Large heavily calcified colonies can be up to 50 years old, but most longer-lived bryozoans are limited to 10 –20 y. Many smaller species are annual. Radial extension in flat encrusting bryozoans is generally on the order of 1–5 mm/y. Erect calcified species generally grow vertically 2–15 mm/y, though articulated species such as Cellaria may reach rates of 40 mm/y. Corresponding calcification rates are generally 101–102 mg/y, but there can be an order of magnitude variation in rate among years in high-latitude bryozoans. Multi-branched bryozoans produce up to 24 g of CaCO3/y. The carbonate produced by bryozoans varies from calcite to aragonite and mixtures of both. Skeletal carbonate mineralogy of bryozoans is complex and appears to be strongly genetically controlled. Global climate change, leading to increasing water temperatures, will generally increase marine bryozoan metabolic rates, and may increase Mg in calcite. On the other hand, decreasing pH (ocean acidification) causes corrosion, changes in mineralogy, and decreased survival. This review of bryozoan growth and calcification allows a general perspective, but also reveals gaps in our knowledge which need to be addressed. Introduction Bryozoans have been described as a minor phylum, and it is true that the combination of being inedible, small, difficult to identify, and currently found mainly in cryptic habitats has resulted in a low profile for this taxon in invertebrate textbooks (and indeed among the wider public). The fossil record of the Bryozoa is extensive, so that paleontolReceived 24 October 2013; accepted 17 March 2014. * To whom correspondence should be addressed. E-mail: abby. [email protected] 203
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small sizes, difficulty of culture, and paucity of workers. And yet, understanding growth and calcification rates in bryozoans may be a critical part of understanding carbonate sediment budgets and the complex interactions of mineralogy, morphology, and dissolution (Smith, 2009), particularly over geologic time (Taylor and James, 2013). This paper reviews what is known about age, growth, and calcification in bryozoans and how they may be affected by changing ocean climate, particularly rising temperatures and increasing acidity. Skeletal carbonate mineralogy in this phylum is reasonably well-known, so only a summary is provided, after which the information is collated in order to make some general predictions about the likely effects of a changing ocean climate on bryozoans, and the likely utility of bryozoans in the study of changing oceans. Growth and Age in Bryozoan Colonies Growth and longevity information about bryozoans is scarce. While some studies do report growth as increases in branch length, colony diameter, colony area, or number of zooids over time (e.g., Stebbing, 1971; Ryland, 1976; Vail and Wass, 1981;Winston and Jackson, 1984; Pätzold et al., 1987; Stanwell-Smith and Barnes, 1997), they are mainly about weakly calcified or encrusting species that have low biomass and do not produce much sediment. Growth and age in large erect bryozoan colonies have been quantified using direct methods, including studies of morphological features by in situ measurements and photographs (Jackson and Winston, 1981; Barnes, 1995; Brey et al., 1998; Cocito et al., 1998, 2003; Barnes et al., 2006); mark and recapture techniques (Smith et al., 2001); and laboratory cultures (Kahle et al., 2003; Amui-Vedel et al., 2007). While direct methods of age determination are generally reliable, especially in situ, they are often of limited duration (usually no more than months). Indirect methods of studying growth, such as stable isotope analysis (Pätzold et al., 1987; Brey et al., 1998; Smith et al., 2001; Smith and Key, 2004; Bader and Schäfer, 2005) or growth-check lines (Stebbing, 1971; Brey et al., 1998; Bader and Schäfer, 2004; Barnes et al., 2006, 2007; Smith, 2007) provide tools for quantifying growth over longer periods of time, as well as in extinct species. Morphological growth-check analyses have the benefit of being non-destructive, and therefore specimens can be used for additional analyses (Smith et al., 2001; Smith and Lawton, 2010). Isotope studies, on the other hand, have the highest resolution because sample volume can be smaller. We have searched the literature and found measured and estimated growth rates and maximum ages for 44 bryozoan species (Supplementary Data Table 1 http://www.biolbull. org/content/supplemental), about 0.7% of described extant species. Different studies report different measurements and units, so the published data have been recalculated to stan-
dard measures as far as possible. As might be expected, the vast majority of the species studied are conspicuous and large. There are 18 (41% of 44) encrusting species, mostly unilaminar. Among the erect species, six (14% of 44) species are rigid branching and one is foliose. The remaining 19 species (43% of 44) are either flexible branching, articulated branching, or erect with a flexible base. The notion of age in a colonial organism is complex, as individuals (zooids) may live less than a year, whereas the colony may persist for decades. The longest-living bryozoan colony known is a specimen of Melicerita obliqua from Antarctica that was 200 mm tall and calculated to have an age of 50 y (Brey et al., 1998; Bader and Schäfer, 2004). In general, long-lived bryozoan colonies reach a maximum age of 10 –20 y. There are many species not represented here, however, that are probably annual, for whom maximum age is a single growing season. Linear growth in encrusting bryozoans (that is, the extension of radius in a year) generally varies from 1 to over 10 mm/y (approx. mean of those in Supplementary Data Table 1 ⫽ 3.2 mm/y with outliers removed, n ⫽ 14), which, assuming it is a circular colony, equates to an increase in surface area of about 20 to 50 mm2 in one year. An unusually fast-growing opportunistic Arctic bryozoan, Einhornia crustulenta, reportedly grew a colony covering 8290 mm2 in 8 months (Kuklinski et al., 2013), equivalent to a 77-mm radial extension per year and 12,400 mm2/y. Erect branching or blade-shaped colonies with a flexible, rooted base grow more rapidly than their encrusting counterparts, from 2 to 15 mm/y extension in overall colony height (mean ⫽ 5.4 mm/y with outliers removed, n ⫽ 15). Erect rigid branching or foliose colonies may grow even faster, at 7 to 20 mm/y (mean ⫽ 11.0 mm/y with outliers removed; n ⫽ 6). Bryozoans appear to reach their greatest linear extension rate in erect flexible articulated species (e.g., Cellaria sp.), where linear growth rate ranges from 10 to 40 mm/y, if the assumption that internodes are annual is correct (e.g., Bader and Schäfer, 2005). In all these cases there is probably a bias based on species selected for study. Researchers are more likely to study those species that are conspicuous and ecologically relevant. A significant number of species studied form part of investigations of polar ecology (28 of the 44 species listed in Supplementary Data Table 1 are from the Arctic or Antarctic regions), places where longevity is often coupled with slow annual growth (Smith and Lawton, 2010). And, some of the results reported form part of experiments designed to determine controls on growth rate, rather than reporting natural growth rates. Membranipora membranacea grows on kelp fronds at rates varying from 0.01 to 12.0 mm/day (linear extension) (Saunders and Metaxas, 2009). The major determinant of growth rate is colony size; larger colonies grow faster
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(Saunders and Metaxas, 2009). Temperature is also positively correlated with growth rate, at least when colonies are not competing for space, but food availability is not. Other factors proposed but not investigated include flow rates, competition, and reproductive status (those with many reproductive zooids may grow more slowly). Bryozoans generally grow more slowly at higher latitudes, presumably reflecting lower water temperatures, which reduce metabolic rate (Barnes et al., 2006). Slower polar growth may also reflect food availability and light limitation in winter (Kuklinski et al., 2013). Many polar bryozoans show “growth-check lines,” which indicate cessation of growth during winter (Barnes, 1995; Barnes et al., 2006; Smith, 2007). Competition levels can also be important in determining growth rate. Kuklinski et al. (2013) found extremely high growth rates in a brackish-water opportunist bryozoan with few competitors in the Baltic Sea. Bryozoans that experience spatial competition, on the other hand, may find their capacity for growth limited (Barnes et al., 2006). Calcification Mechanisms in Bryozoans Skeletal material in many marine invertebrates is not entirely mineral; it is often bound up with organic material. The majority of this organic tissue is made up of hydrophobic, cross-linked framework macromolecules, which provide a structure for the action of the less-common control macromolecules, a diverse group of large biomolecules related to proteins and polysaccharides, with charged groups that enable interaction with mineral ions (Weiner and Addadi, 1997). It is these macromolecules that control the process of calcification. In the case of molluscs, for example, crystallization is induced on a pre-constructed epithelial matrix (Simkiss and Wilbur, 1989), whereas in corals, crystals are formed in an extracellular fluid containing the necessary ions (Allemand et al., 2004). Mode of calcification in bryozoans is very little studied, and essentially unknown. One early study of calcification in a simple cheilostome bryozoan (Membranipora) suggests that calcification begins after differentiation of the cells is achieved (Lutaud, 1987). Calcium ions are released into intracellular spaces, with subsequent impregnation of organic matrix with calcium salts (Lutaud, 1987). This build-up of calcium in the cuticular matrix occurs before any crystallization takes place (Ryland, 1976). Aragonite or calcite crystals are precipitated on the matrix, with the choice of mineralogy possibly determined by amino acid composition of the cuticle itself, or by ions present in the intercellular fluids. These crystals are incorporated into the zooid walls as spheres, which may coalesce and develop into threads (Ryland, 1976) and eventually many other ultrastructural forms (see, e.g., Sandberg, 1977). At the colony scale, basal walls are generally formed
Figure 1. Astogenetic change along bryozoan colonies from southern New Zealand: (A) Melicerita chathamensis; (B) Odontionella cyclops. The youngest zooids (toward the left) show the basal wall forming first, then development of marginal walls, and finally the frontal shield. Further calcification with age shows development of ovicells, avicularia, and secondary thickening (toward the right). Scale bar is 1 mm.
first from the proximal part of the zooid, with marginal walls following and the frontal shield last (Fig. 1). Detailed studies of the calcification mechanisms in bryozoans are long overdue. Recent developments in understanding of calcification in corals should allow similar progress in bryozoans over the coming decade. While it will be natural to begin with lightly calcified very well known bryozoans (e.g., Celleporella hyalina), we will eventually have to turn our attention to well-calcified slow-growing temperate taxa such as Pentapora. Evaluating the effects of
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environment on calcification requires this basic level of understanding. Calcification Rates in Bryozoans Biologists do not ordinarily weigh bleached colonies, and thus do not usually report on production of calcium carbonate. When carbonate production is calculated, it is usually on the basis of colonies of known age or turnover rate (Smith and Nelson, 1994; Cocito and Ferdeghini, 2001), so that the carbonate production rate reported is a mean over the age of the colony. For short-lived bryozoans (of less than 10-y maximum age), this figure is probably accurate (see, e.g., Smith and Haderlie, 1969), and generally lies in the range of 101–102 of mg CaCO3/y. In colder waters, however, bryozoans may live several decades (Barnes, 1995; Brey et al., 1998; Bader and Schäfer, 2004). Mean annual carbonate production is a more useful measure in these longer-lived bryozoans, if accompanied by some understanding of annual variation. The size and weight of annual production, however, is difficult to ascertain. Longer-lived colonies are not readily cultured. Oxygen isotopes have been shown to provide age-markers (e.g., Pätzold et al., 1987), but destructive sampling methods render this approach incompatible with carbonate production measurement. What is needed is a well-marked morphological signal (such as an annual growth band), and these are available in some polar (Barnes, 1995; Barnes et al., 2007; Smith, 2007) and temperate (Smith and Lawton, 2010) species. Growth in polar bryozoans varies considerably from year to year (Smith, 2007). Calcification in Cellarinella nutti, for example, ranges from 3 to 57 mg/y (mean ⫽ 22 mg/y, std dev ⫽ 11 mg/y, n ⫽ 59), C. nodulata from 5 to 33 mg (mean ⫽ 18 mg/y, std dev ⫽ 8 mg/y, n ⫽ 27), and Swanomia belgica from 1 to 22 mg/y (mean ⫽ 8 mg/y, std dev ⫽ 2 mg/y, n ⫽ 50) (see Supplementary Data Table 1). These species are all either unbranched or very seldom branching. Cellarinella watersi, in contrast, produces an order of magnitude more carbonate per year due to its more highly branched habit, between 100 and 200 mg/y (Barnes, 1995). Temperate bryozoans are generally missing the conspicuous growth-checks that allow for inter-annual comparison, but there are exceptions. The poorly calcified Flustra foliacea has recognizable annual growth bands (Stebbing, 1971), as does the rather more robust blade-shaped Melicerita chathamensis (Smith and Lawton, 2010). Segments from 41 colonies of M. chathamensis collected off southern New Zealand ranged from 1 to 37 mg (mean ⫽ 9 mg, std dev ⫽ 7 mg, n ⫽ 236): annual production by individuals of 1–37 mg/y. Carbonate production in the New Zealand fiords by Adeonellopsis sp. is many orders of magnitude larger— 23,700 mg/y—again partly because of its many-branched growth habit (Smith et al., 2001). Such multi-branched
bryozoans have the capacity to produce more carbonate over their longer lives. Variability among years that spans an order of magnitude means that average estimates over the full age of the colony have minimal ecological meaning (Wejnert and Smith, 2008). Longer-lived bryozoans appear to be able to calcify faster and more robustly when food supply and temperatures are sufficient, and to slow their growth under poorer conditions (Smith 2007). Skeletal Carbonate Mineralogy of Bryozoans Bryozoans may be the most mineralogically well-characterized invertebrate phylum. Certainly details of mineralogical complexity are better known in this taxon than in others of a similar biodiversity. Supplementary Data Table 2 (http://www.biolbull.org/content/supplemental) delineates what is known about skeletal carbonate mineralogy in 606 species of bryozoans, almost 10% of extant species. Regional studies (particularly Schopf and Manheim, 1967; Rucker and Carver, 1969; Schopf and Allan, 1970; Siesser, 1972; Poluzzi and Sartori, 1973, 1974; Smith et al., 1998) revealed a complex mineralogical suite in the marine bryozoan classes Gymnolaemata and Stenolaemata. Later workers tried to summarize bryozoan mineralogy, noting the dominance of calcite (e.g., Lowenstam and Weiner, 1989); the addition of aragonite in secondary calcification (Sandberg, 1983); the presence of entirely aragonitic bryozoans (Sandberg, 1983); and the presence of bimineralic forms, some with highly organized biominerals and others with fairly amorphous mixtures (Bone and James, 1993). More recently, the presence of two distinct calcites (dominant low-Mg calcite and subdominant high-Mg calcite) has been documented in a few anascan cheilostomes (Smith et al., 1998; Bader and Schäfer, 2005). The notion of biomineral space has been used to characterize the mineralogical variability in taxa, with the phylum Bryozoa as a whole occupying 63% of the space available for biomineralization (Smith et al., 2006). The phylum is thus highly variable and repays detailed investigation. The majority (about 2/3) of bryozoans are entirely calcitic, including essentially all of the extant stenolaemates (Smith et al., 2006). Of the remainder, about half are entirely aragonitic (Smith et al., 2006), and half are bimineralic. Three groups of bimineralic skeletons have been described: (A) mainly aragonite with small areas formed from calcite (e.g., Adeonellopsis sp.; Wejnert and Smith, 2008), (B) mainly low-Mg calcite with increasing amounts of high-Mg calcite with age (e.g., Melicerita chathamensis; Smith and Lawton, 2010), and (C) mainly calcite with secondary thickening by aragonite over time (e.g., Odontionella cyclops; Smith and Girvan, 2010). Mg in bryozoan calcite ranges from zero to 14 wt%
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MgCO3 (0 to 16 mol% MgCO3). When two calcites co-exist in a single skeleton (as occurs in a few anascan cheilostomes), the low-Mg mineral is about 2– 4 wt% MgCO3, and the high-Mg mineral ranges from 7 to 11 wt% MgCO3 (Smith et al., 2006). Phylogenetic influence on skeletal carbonate mineralogy in marine bryozoans is considerable. Stenolaemates, including the cyclostomes, form their skeletons almost entirely of low-Mg calcite; mineralogical complexity is provided by the gymnolaemate cheilostomes (Smith et al., 2006). Some cheilostome families are more consistent in their mineralogy (e.g., Cupuladriidae). Others, such as the Cellariidae, have a wider range of Mg content but are always calcitic. In contrast, there are a few families in which Mg content varies less but the calcite/aragonite ratio is more highly variable, such as the Margarettidae. The most mineralogically variable families are the Phidoloporidae and Membraniporidae, both of which occupy over 50% of available biomineral space (Smith et al., 2006). Polar bryozoans from both the Arctic (Kuklinski and Taylor, 2008, 2009) and Antarctic (Borisenko and Gontar, 1991) are dominated by calcite, with lower Mg content than is the norm in warmer waters. Many studies have commented on an apparent decrease in aragonite and Mg in calcite with increasing latitude, but detailed temperature- or latitude-related trends in mineralogy, such as those reported by Rucker and Carver (1969), have very likely been confounded by phylogenetic factors and cannot be considered anything other than vaguely indicative until phylogenetically independent statistical analysis has been carried out (e.g., Smith et al., 2013) to tease apart the environmental and phylogenetic signals. Cheilostome bryozoans mineralogically precipitate their skeletons out of equilibrium with seawater, sometimes precipitating more than one mineral, usually with organized and consistent ultrastructure (Taylor et al., 2008). They can thus be considered “active” or “controlling” biomineralizers (sensu Lowenstam and Weiner, 1989), as are molluscs and echinoderms, and in contrast to most “passive” biomineralizers such as algae and corals, which are more limited in their control of biomineralization (Ries, 2010). Suggestions that secular changes in seawater chemistry have driven the evolution of cheilostome bryozoans (e.g., Stanley and Hardie, 1998) are unsupported by fossil data or by the timing of major changes in mineralogy (Taylor et al., 2009), though it is possible that skeletal mineralogy at first appearance was affected by seawater chemistry at the time (Kiessling et al., 2008; Taylor, 2008). Cheilostome bryozoans are unlike the passive mineralizers that reflect seawater chemistry in their skeletons (see, e.g., Ries, 2004); it appears that they control the mineralogy of their skeletons despite the composition of seawater.
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Effects of the Changing Ocean Water temperature affects zooid size and growth rate in bryozoans over a range of scales. Zooid size within and among colonies appears to be generally correlated with seasonal changes in mean water temperature (Okamura and Bishop, 1988; O’Dea and Okamura, 1999; O’Dea et al., 2007). Within species, growth is enhanced by increasing temperature (e.g., Lombardi et al., 2006, 2008; Saunders and Mataxas, 2009). Overall, higher latitude bryozoans tend to grow relatively more slowly, presumably due to slower metabolic rates in cold waters (Smith and Lawton, 2010). Initial studies are showing that growth rates in some polar invertebrates have increased over the last few decades as the water warms and the winter period becomes shorter (e.g., Barnes et al., 2011). Ocean warming and lowered pH interacted to affect growth rate in the Australian cheilostome bryozoan Celleporaria nodulosa (Durrant et al., 2013). Growth was significantly decreased in lower-pH winter tests, whereas in summer it was higher temperatures that reduced growth rate. Saderne and Wahl (2013), on the other hand, found that present-day up-welling CO2 concentrations (about 1200 atm) enhanced the growth of kelp-encrusting bryozoans Alcyonidium hirsutum and Electra pilosa, and even higher projected CO2 levels (3150 atm) showed no effect on growth, except to remove the skeleton of E. pilosa. More heavily calcified bryozoans, however, do not fare well in lower-pH waters: Schizoporella errata showed skeletal corrosion and less investment in defensive heteromorphs (Lombardi et al., 2011a), and the larger Mediterranean bryozoan Myriapora truncata showed dissolution and lowered Mg in skeletal calcite under elevated pCO2 (Lombardi et al., 2011b). It might be expected that mineral composition would affect dissolution rate of bryozoan carbonates. Crystalline inorganic aragonite is more soluble than calcite and in a strict chemical experiment will dissolve sooner and faster (Weiner and Addadi, 1997). Biominerals in the real ocean are, however, very different. Laboratory dissolution experiments have shown that it is reactive surface area that determines dissolution rate in biogenic carbonates, with composition making little or no difference (Smith et al., 1992; Smith and Garden, 2013). Reactions of invertebrates to a changing marine environment are complex and problematic. Even though bryozoans have been very little studied in this regard, there is reason to suppose that the increasing temperatures and decreasing pH of the global ocean will have mainly negative effects on the calcification and growth of these invertebrates. Bryozoans offer considerable advantages to the study of the effects of a changing ocean. They occur naturally in a wide range of skeletal morphologies and mineralogies.
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Within a bryozoan colony, mineralogical and morphological responses to changing seawater can be traced in a series of genetically identical clones (e.g., Pistevos et al., 2011). It is possible to study seawater-driven changes in calcite/ aragonite ratio, in Mg content in calcite, or in ratios between low- and high-Mg calcite in bryozoans. Recommendations It is essential to the understanding of bryozoan calcification to discern the mechanisms and underlying biochemistry that enables calcification. Recent methodological advances in understanding coral calcification may be relevant and helpful here, as corals too are small and colonial. Growing calcifying bryozoans in water with different Mg/Ca ratios, following the experiments of Ries (e.g., 2004, 2010), would allow for a greater understanding of the degree to which skeletal mineralogy is “hard-wired” in cheilostomes, and thus how much flexibility they may be able to bring to changes in seawater chemistry. Not one study has measured the effect of temperature or seawater chemistry on early life stages in bryozoans (as suggested by Byrne, 2011). Larval development, survival, and recruitment in changing environmental conditions are an obvious area for fruitful study. Acknowledgments The author’s long-term commitment to bryozoan skeletal studies began in the laboratory of Prof. C.S. Nelson, Earth Sciences, University of Waikato, whose support is gratefully acknowledged. Colleagues and students who have collaborated over the years are also thanked: D.P. Gordon; M.M. Key, Jr.; H.G. Spencer; P.D. Taylor; K.E. Wejnert; E.I. Lawton; E. Girvan; C.J. Garden; D.I. Winter. This manuscript was improved greatly by comments from M.M. Key, Jr. and A.C.L. Wood. Literature Cited Allemand, D., C. Ferrier-Pages, P. Furla, F. Houlbreque, S. Puverel, S. Reynaud, E. Tambutte, S. Tambutte, and D. Zoccola. 2004. Biomineralisation of reef-building corals: from molecular mechanisms to environmental control. C. R. Palevol. 3: 453– 467. Amui-Vedel, A., P. J. Hayward, and J. S. Porter. 2007. Zooid size and growth rate of the bryozoan Cryptosula pallasiana Moll in relation to temperature, in culture and in its natural environment. J. Exp. Mar. Biol. Ecol. 353: 1–12. Bader, B. 2000. Life cycle, growth rate and carbonate production of Cellaria sinuosa. Pp. 136 –144 in Proceedings of the 11th International Bryozoology Association Conference, A. Herrera Cubilla and J. B. C. Jackson, eds. Smithsonian Tropical Research Institute, Balboa, Panama. Bader, B., and P. Schäfer. 2004. Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. J. Nat. Hist. 38: 2901–2922. Bader, B., and P. Schäfer. 2005. Impact of environmental seasonality on stable isotope composition of skeletons of the temperate bryozoan
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