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Vol. 430: 133–146, 2011 doi: 10.3354/meps08965 INTRODUCTION Patterns of growth in plants and animals have long been used to gain insights into past environments. Variable accretion of structural material in trees, fish otoliths and the shells of bivalve or gastropod molluscs, for example, can be used to retrospectively extract ambient environmental conditions such as rainfall, temperature or food availability (e.g. Falcon-Lang 2005, Zazzo et al. 2006, Hallmann et al. 2009). Organismal attributes that favour such analyses in clude a *Email: b.okamura@nhm.ac.uk MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser Contribution to the Theme Section ‘Evolution and ecology of marine biodiversity’ Bryozoan growth and environmental reconstruction by zooid size variation Beth Okamura 1, *, Aaron O’Dea 2, 3 , Tanya Knowles 4 1 Department of Zoology, Natural History Museum, London SW7 5BD, UK Published May 26 2Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Research Institute, Apartado 0843-03092 Panamá, República de Panamá 3Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada 4Department of Earth Science and Engineering, Imperial College London, London SW7 2BP, UK ABSTRACT: The modular growth of cheilostome bryozoans combined with temperature-induced variation in module (zooid) size has enabled the development of a unique proxy for deducing seasonal temperature regimes. The approach is based on measures of intracolonial variation in zooid size that can be used to infer the mean annual range of temperature (MART) experienced by a bryozoan colony as predicted by a model of this relationship that was developed primarily to infer palaeoseasonal regimes. Using the model predictions effectively requires a highly strategic approach to characterise the relative amount of within-colony zooid size variation (by adopting random or very systematic measurements of zooids that meet a stringent set of criteria) to gain insights on temperature variation. The method provides an indication of absolute temperature range but not the actual temperatures experienced. Here we review the development of, support for and applications of the zooid size MART approach. In particular, we consider the general issue of why body size may vary with temperature, studies that validate the zooid size–temperature relationship and insights that have been gained by application of the zooid size MART approach. We emphasise the potential limitations of the approach, including the influence of confounding factors, and highlight its advantages relative to other proxies for palaeotemperature inferences. Of prime importance is that it is relatively inexpensive and quick and allows a direct estimate of temperature variation experienced by an individual colony. Our review demonstrates a strong and growing body of evidence that the application of the zooid size MART approach enables robust interpretations for palaeoclimates and merits broad recognition by environmental and evolutionary biologists and climate modellers. KEY WORDS: Cheilostomes · Mean annual range of temperature · MART · Body size–temperature relationship · Palaeoclimates Resale or republication not permitted without written consent of the publisher continuous record of growth and the sequential development of discrete and measurable features that vary consistently with respect to a single environmental variable and remain fixed, thereby permitting the retrieval of environmental conditions relevant to particular time periods. Benthic colonial invertebrates can provide an especially appropriate system for such retrieval, since, with some exceptions (e.g. sponges), they comprise distinct, individual modules (zooids) that are produced iteratively throughout the lifetime of the colony. The sclerochronological analysis of modular © Inter-Research 2011 · www.int-res.com OPEN PEN ACCESS CCESS
134 growth can provide inferences for both intra- and interannual environmental variation, information that is not readily available from analyses of short-lived, unitary organisms that are commonly used as proxies, such as foraminifers or ostracodes. Furthermore, coloniality is often associated with polymorphism, with modules specialised for different functions within a colony. These attributes, viz. modular iteration, polymorphism and individual colony longevities ranging from months to many years, may enable joint insights into environmental conditions and associated life history variation (O’Dea & Okamura 2000a, O’Dea & Jackson 2002). Such insights are generally difficult to achieve through investigations of longer-lived unitary organisms, such as bivalves or brachiopods, since the morphologies of these organisms do not readily provide a record of functional allocation during their lifetime. Surprisingly, however, the unique contribution of colonial invertebrates for retrospectively deducing environmental and life history variation has not been widely recognised. Bryozoans are colonial, suspension-feeding invertebrates that are common members of benthic assemblages (McKinney & Jackson 1989). There are some 6000 described extant species of bryozoans (Gordon et al. 2009), most of which belong to the order Cheilostomata. Colonies of cheilostomes comprise asexually budded zooids that are reinforced by skeletal walls composed of calcitic and/or aragonitic car - bonate (Rucker & Carver 1969, Smith et al. 2004). Typically, cheilostomes display zooid polymorphism (McKinney & Jackson 1989). The majority of zooids are specialised for feeding (autozooids), whilst a smaller proportion function in reproduction (ovicells) and defense (avicularia). The carbonate skeleton (‘zooecium’) confers preservation of colony features, including zooid polymorphism, and bryozoans are well represented in the fossil record (McKinney & Jackson Mar Ecol Prog Ser 430: 133–146, 2011 1989). Once the skeletal walls of a new zooid are secreted, there is no further expansion of zooid surface area (O’Dea & Okamura 2000b). This gives the zooid a determinate size that has been shown to be controlled to a significant extent by the ambient water temperature at the time the zooid was produced. Bryozoan colonies therefore record the range of temperatures experienced during their lifetime as intracolonial variation in zooid size (Fig. 1). Such temperature-induced variation in size is also observed in unitary animals and is generally known as the ‘temperature–size rule’ (Atkinson 1994). The above-mentioned features make cheilostome bryozoans unique amongst colonial taxa in offering opportunities for inferring environmental conditions and biotic responses in the present day as well as over geological time. Other colonial taxa such as corals, hydroids, ascidians and other non-cheilostome bryo - zoans either do not produce carbonate skeletons, show indeterminate growth of their polyps or zooids, or ex - hibit little to no polymorphism and therefore preclude gaining additional insights on how life histories may respond to environmental conditions. Recognition of the unique opportunities afforded by cheilostome bryozoans for the retrieval of environmental information led to the development of a method that allows the estimation of the mean annual range of temperature (MART) based on variation in zooid size within cheilostome colonies. The method is based on using model predictions for how zooid size varies with MART and thus requires that zooids meet a stringent set of criteria, in keeping with assumptions of the model, and that a strategic sampling protocol is adopted to target appropriate zooids randomly or very systematically. The method informs on absolute seasonal variation in temperature but does not indicate the actual temperatures. Thus polar and tropical bryozoans will converge on similar low MART values. Fig. 1. Cupuladria exfragminis. Seasonal variation in zooid size. Scanning electron micrographs of a recent col - ony from the Gulf of Panama. Size difference between zooids that developed during (A) upwelling (cold) and (B) non-upwelling (warm) conditions. Same magnification for the purpose of comparison. The skeletal walls of both autozooids (large orifices) and avicularia (small orifices) are evident. Scale bar = 150 µm. Photos by R. Dewel
Page 1 and 2: THEME SECTION CONTENTS Evolution an
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Page 8 and 9: Fig. 1. Littorina saxatilis. Shell
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182 tion ascent-adaptation may be m
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184 from the estuaries to the sea i
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186 1977 for the first release and
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188 Table 3. Platichthys flesus. Re
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190 were made at positions, in the
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192 Displacement of flounder to Poo
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194 successive spawning seasons. Pl
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196 Kerstan M (1991) The importance
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198 length-depth relationship on th
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200 tions were very similar in deep
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202 fish recaptured at the earliest
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204 LITERATURE CITED Allen RL, Balz
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Manríquez & Castilla: Behaviour of
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No. of larvae (- - swimming; - - ad
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224 into account when considering i
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226 cies that did not occur under a
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228 Mar Ecol Prog Ser 430: 223-234,
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230 Mar Ecol Prog Ser 430: 223-234,
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232 (Lubchenco 1983). Johnson et al
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234 succession. J Exp Mar Biol Ecol
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236 South America, SE Asia and Japa
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238 reported maximum sizes. In gene
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240 Acknowledgements. We thank the
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242 trawling disturbance in terms o
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244 among sites and with other stud
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246 Univariate measures of biotic d
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248 Infaunal indicator species The
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250 the 2 sites. The burrowing anem
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252 mud or sandy sediment environme
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254 terms of univariate indices and
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Most of the 68 000 extant species o
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transport are unclear, but estimate
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Whiteley 1989, Whiteley 1999). More
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araneus (Walther et al. 2010). In a
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selective survivorship associated w
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Burnett LE (1997) The challenges of
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in diadromous, freshwater palaemoni
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274 Fig. 1. Scottish west coast, sh
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276 Table 1. Summary for 3-factor n
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278 microscopy, a method employed s
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280 pulidae) reef communities from
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282 strate and develop the rudiment
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284 produce a straight line for all
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286 Fig. 3. Number of benthic and r
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288 and plateaus on the Pacific pla
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