Bryozoan Studies 2019

Growth geometry and measurement of growth rates in marine bryozoans: a review

Abigail M. Smith1* and Marcus M. Key, Jr.2

1 Department of Marine Science, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand [*corresponding author: email: [email protected]] 2 Department of Earth Sciences, Dickinson College, P.O. Box 1773, Carlisle, PA 17013-2896, USA

ABSTRACT measuring and reporting growth rate in bryozoans The relationship between age and size in colonial will ensure they are robust and comparable. marine organisms is problematic. While growth of individual units may be measured fairly easily, the growth of colonies can be variable, complex, and INTRODUCTION difficult to measure. We need this information in Bryozoans are lophophorate aquatic invertebrates order to manage and protect ecosystems, acquire which typically form colonies by iterative addition bioactive compounds, and understand the history of of modular clones (zooids). Freshwater species environmental change. Bryozoan colonial growth are uncalcified; the majority of marine species are forms, determined by the pattern of sequential calcified, so that there is an extensive fossil record of addition of zooids or modules, enhance feeding, marine bryozoan colonies. When calcified colonies colony integration, strength, and/or gamete/larval grow large, they can provide benthic structures dispersal. Colony age varies from three months to which enhance biodiversity by provision of sheltered 86 years. Growth and development, including both habitat. Agencies who wish to manage or protect addition of zooids and extrazooidal calcification, these productive habitats need to understand the can be linear, two-dimensional across an area, or longevity and stability of these structures. But how three-dimensional. In waters with seasonal variation are size and age related in colonial organisms? in physico-chemical parameters, bryozoans may We do not automatically know the age of a large exhibit a growth-check, like an annual “tree-ring”, bryozoan colony. While growth rate of zooids may showing interannual variation. Growth in other be relatively easily measured, the growth rates of bryozoans are measured using chemical markers colonies can be highly variable, difficult to measure, (stable isotopes), direct observation, or by inference. and complex. Yet without this information, it is Growth rates appear to be dependent on the method of difficult to manage or protect ecosystems based on measurement. Calcification rate (in g CaCO3/y) offers bryozoan colonies, or to grow them for bioactive a way to compare growth among different growth compounds, or to understand the carbonate record forms. If the weight of carbonate per zooid is fairly held in them. After several decades of struggling with consistent, it can be directly related to the number of growth rates in bryozoans, the authors here review zooids/time. Careful consideration of methods for and discuss the following issues in bryozoans: zoarial

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growth form, maximum size, age, growth (increase Early on, bryozoan colonial growth forms were in size), and measurements of growth rate (increase often given names that referred to an exemplar taxon, in size over time). usually a genus (e.g., Stach 1936; Lagaiij and Gautier 1965). So, a bryozoan that grew an erect flexible leafy colony like that of the genus Flustra was referred to as SHAPE OF A BRYOZOAN flustriform. This archetypal system was summarised The individual zooids that make up bryozoan colonies by Schopf (1969). As noted by Hageman et al. are fairly simple boxes or tubes, with more or less (1998), each category was made up of a combination ornamentation. Normal feeding zooids (autozooids) of characteristics, with no systemic recognition of are sometimes aided by zooids who specialise in shared or common characters. It was cumbersome, support, cleaning, or reproduction (heterozooids). difficult for non-specialists, and although there were Together with extrazooidal carbonate, they make up a great number of categories (with different systems the colony. Bryozoan colony growth form is thus for cheilostomes and cyclostomes), they failed in determined by the pattern of addition of zooids, aggregate to describe all the variety in bryozoan the same way that the shape of a knitted garment is colonial forms. determined by the addition of stitches. In the 1980s and 1990s, carbonate sedimentologists Most bryozoan colonies start out as a spot (sexually- who wanted to categorise bryozoans without excessive produced ancestrula). Then the first zooid buds from investment in species identification developed the ancestrula, but it is the one after the first budding a hierarchical classification system, where a few that makes the pattern (Fig. 1). In simple iterative characteristics were combined to make a simple code growth, new modules are added sequentially, often in to describe overall colonial shape (Nelson et al. 1988, some regular arrangement (Hageman 2003). Zooids revised and expanded by Bone and James 1993; Smith can be added in a line, or at the tips of branches, or 1995). Colonies were described as erect, encrusting, along an edge, on the substrate or lifting erect off or free-living; then subdivided into various shapes it. This kind of growth results in a small number (e.g., branching, articulated, rooted). These categories of simple growth forms, from runners and trees to were rather broad-brush and took no account of sheets and mounds (Nelson et al. 1988; Smith 1995). “rampant convergent evolution” (Taylor and James Combinations of these simple primary modules can 2013, p. 1186), or of the different ecological roles form more complex colonies with secondary structural played by different shapes. An alternative, using design units (composed of the primary modules) a classification based on the ecological function of (Hageman et al. 1998; Hageman 2003). growth forms (e.g., McKinney and Jackson 1989) Theoretically, a modular colony could take almost was inadequately supported by genuine ecological any form, but, in reality, bryozoan colonies tend to understanding of bryozoan ecology on different scales occur in a few basic forms, some of which have (Hageman et al. 1998). evolved repeatedly in different clades (McKinney Hageman et al. (1998) reviewed all this and and Jackson 1989). They achieve: access to food developed an “Analytical Bryozoan Growth Habit particles in the water, integration of the colony Classification”, in which they characterised bryozoan (connections between zooids), strength and resistance colonial forms using eco-morphological categories: to water flow/predation, reduction of interaction with orientation, attachment to substrate, construction, other species, competitive advantage, and capacity arrangement of zooecial series, arrangement of frontal to distribute larvae into the water (McKinney and surfaces, secondary skeletal thickening, structural units Jackson 1989). Bryozoan colonial growth form and their dimensions, frequency and dimensions of nomenclature tries to capture this variation, with bifurcation, and connections between structural units, varying degrees of success. along with substrate type. These twelve fundamental

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characters provided a complex but comprehensive and have often failed to show robust correlations with systematic method of describing the great diversity depth, water speed, or temperature (e.g., Liuzzi of bryozoan colony forms. Hageman revisited this et al. 2018). Certain broad general trends can be classification in his 2003 review of colonial growth observed, for example: that fragile small colonies in diverse bryozoan taxa. are probably not representative of strong hydraulic It is relevant to note that cyclostomes zooids are energy. That is not to say that bryozoans do not have tubes, where cheilostome zooids (usually) make potential as environmental indicators; there are, for more-or-less rectangular boxes. These modules example, assemblages that are strongly related to combine differently, but often make remarkably habitat (e.g., Wood and Probert 2013), as well as similar growth forms (Fig. 2). useful environmental geochemical signals in their Since Stach (1936), researchers have been skeletal carbonate (e.g., Key et al. 2018). enthusiastic about using colonial growth form as an indicator of (paleo)environment (reviewed by Smith 1995; Hageman et al. 1997). Despite the appealing SIZE OF A BRYOZOAN notion that different growth forms must be adapted Individual zooids in marine bryozoans are tiny, to different environments, and the development usually 0.1 to 1 mm across. In a given species, zooid of a standardized and statistically robust method size range is characteristic and sometimes diagnostic. (Hageman et al. 1997), rigorous investigations However, at least some species of bryozoans grow

Figure 1. Iterative growth in bryozoans: many ways to combine individual zooids. Multi-laminar and other complex forms are made by iterating these multi-zooid modules.

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larger zooids in cooler waters/seasons (see review 2013). Large erect bryozoans today are generally 10- in Amui-Vedel et al. 2007), which has been used as 30 cm tall but Cocito et al. (2006) reported modern an environmental indicator (e.g., McClelland et al. Pentapora colonies in the Adriatic that reached 1 m 2014). Zooid size and arrangement are generally in height; there are fossil bryozoans that appear to held to be optimal for feeding currents (see, reach a similar size (Cuffey and Fine 2006). e.g., Ryland and Warner 1986). Colony size has been measured in many ways: Size of bryozoan colonies within a species, linear extent (height, width, thickness, diameter), unlike that of its zooids, varies greatly. A colony area, volume, and number of zooids. The most becomes mature (sexually reproductive) once it natural measurement depends on the colony form. has enough zooids to support embryo production In fact, each main colony form has an obvious (Nekliudova et al. 2019), usually 30-130 zooids, method of measuring it (Table 1). Thus, size in but embryos have been reported in species ranging one-dimensional colonies is measured in length, from 3 to 2700 zooids (Jackson and Wertheimer whereas sheet-like colonies are sometimes measured 1985). A bryozoan “spot” colony can be viable at in area (or in extension of diameter for flat nearly- only a few mm2, but equally, at the other end of circular colonies). Lumpier multilaminar three- the spectrum, one encrusting bryozoan (Einhornia dimensional colonies could be measured in volume, crustulenta) can cover 8290 mm2 (Kuklinski et al. but in fact generally are not measured at all, due

Figure 2. Convergent growth forms from different clades of bryozoans. (A) Diaperoecia sp. (stenolaemate cyclostome); (B) Galeopsis porcellanicus (gymnolaemate cheilostome); (C) Hippellozoon novaezelandiae (gymnolaemate cheilostome); (D) Hornera foliacea (stenolaemate cyclostome).

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to the challenges presented by their shape (but see not necessarily related to size if fission and/or partial Sokolover et al. 2018). mortality have occurred (Jackson and Winston 1981). Sometimes researchers add to their measurements Most large erect species, on the other hand, appear to the spatial density of zooids (i.e., number of zooids/ have a “normal maximum size,” possibly mediated mm2). In general, this measurement appears to by the mechanics of water flow and skeletal support. limit counts to autozooids, and it is worthwhile Age in the context of a bryozoan colony is considering whether or not heterozooids deserve thus how long the colony has been functioning, counting in this context. There is also a lack of specifically, time from metamorphosis of the larva comparability between cheilostome box-like zooids into the ancestrula to time of death/collection. There and stenolaemate tube-like zooids. are annuals and perennials among bryozoan colonies. Because of these different measurement schemes, An adult colony can die of old age after three months comparisons of size among growth forms has been (e.g., as winter arrives) or last as much as 50 years problematic and has required researchers to make unit (Melicerita obliqua in the Weddell Sea, Antarctica; conversions. For example, one could assume constant Brey et al. 1998); Celleporaria fusca in the Gulf of branch thickness in order to convert branch length Aqaba (Sobich, 1996) holds the longevity record of to volume. Smith and Nelson (1994) managed this 86 years. A range of about 90 to over 30,000 days issue by measuring size in terms of weight of skeletal means that age of bryozoan colonies, of different carbonate– which is independent of growth form. species and in different environments, can vary over four orders of magnitude. Having said that, most large erect heavily-calcified marine specimens that have AGE OF A BRYOZOAN been studied are about 10-30 years old (Smith 2014). What are life and death to a bryozoan? New individual zooids begin budded at the edge of a colony (often at the “growing edge” or “growth tip” but sometimes BRYOZOAN COLONY GROWTH frontally on top of old zooids). As the growing edge Growth is the increase in occupation of space. In moves away, the zooids mature, sometimes reproduce bryozoans, there are different kinds of growth: 1. sexually, and grow old. They can produce a brown body growth and development of the individual zooid and then regenerate, they can produce extrazooidal (ontogeny), generally a short-lived and small-scale thickening, they can die, and the chamber become process; 2. growth and development of the colony by empty, or they can bud frontally and essentially addition of zooids (which we call primary astogeny) overgrow themselves (Ryland 1976). Life history is which can be on the order of months or years or complex in bryozoans; age of a single bryozoan zooid decades (Lidgard and Jackson 1989); and 3. growth is not well constrained. It could be important, though, of the colony by extrazooidal calcification (which we for example, in studies where measuring zooids of the could call secondary astogeny) adding strengthening same generation is necessary, such as in age-growth- material that is not part of a zooid, also over the life climate correlations (e.g., Key et al. 2018). of the colony. On a different scale, the colony’s lifespan is In terms of measuring colony growth, there are the time from metamorphosis of the larva into the only a few categories (Table 1). In general, growth ancestrula to the time the last zooid dies, and the can occur around the edges of a colony (radial colony ceases to function. Some colonies die from growth) or be limited to one or two directions an event, like being eaten or crushed or buried. (linear growth), including, in frontal budding, up Theoretically, of course, a bryozoan colony is into the water column. The dimensionality of growth potentially immortal (McKinney and Jackson 1989). determines the dimensions that must be measured Even in a simple encrusting colony, however, age is to encapsulate growth. Units of growth rate vary

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Table 1. Three categories of geometry in bryozoan colonies, with relevant ways to measure size and growth.

Dimensions New Illustration Colonial Comment Growth increment zooids (ancestrula empty, growth form measured over time added new growth in black) nomenclature

1 dimension In a line Encrusting Length (length) at the tip Uniserial Number of zooids of the colony Runners (1 zooid in illustration)

At the Encrusting Each branch can be one Additive length growing multiserial zooid wide, or bilaminar, increase tip of each Branching or a circle of zooids around (= sum of all the new branch runners a central core or even more branch lengths) Erect branching complex Number of zooids (all kinds) Bifurcation angle and (3 zooids in Erect flexible rotation around the branch illustration) articulated axis allow branches to grow without running into each other

2 dimensions All along Encrusting Sheets are usually circular Increase in area, (area) the edge, unilaminar unless they run into calculated for a circle but flat on Spots, circles something or growth is not of radius R the substrate Free-Living consistent around the edge Increase in area, Caps (e.g. “belt” shaped colonies) calculated as length Caps are curved versions x width if roughly rectangular Number of zooids (17 zooids in illustration)

Along Erect foliose Can be unilaminar or Height the growing Erect fenestrate bilaminar Area = width of edge, Rooted sabres Fenestrate is really just growing edge x height away from Conescharallinids a sheet with holes in it Number of zooids substrate Sabres are leaves that aren’t (5 zooids in very wide illustration)

3 dimensions Along Encrusting Highly variable Volume of a sphere: (volume) the edge multilaminar This is difficult to generalise 4/3πr3 and on Mounds Self-overgrowth is typical in Or a disc/cylinder: the surface and nodules this group, and can be very H πr2 Spheres irregular Or a prism: H x W x L Number of zooids (6 zooids in illustration)

across the range of size and time, and possibly over in winter (Brey et al. 1998; Smith 2007), temperate the development of the colony. The most commonly species can also slow their growth in the cold months, used are: zooids added, linear increase (height, length, leaving a thickened layer as an annual marker (e.g., radius), and increase in area over time. Melicerita chathamensis, Smith and Lawton 2010, Key Bryozoans in cold waters sometimes stop growing, et al. 2018), or just a gap in the record (Adeonellopsis or slow down, during winter (Smith & Key, 2004). If sp., Smith et al. 2001, Smith and Key 2004). calcification continues while linear extension does not, A few colonial growth forms appear to have a thickened skeletal band, or growth check appears determinate growth, that is, they stop growing when in the skeleton. While most growth checks occur in they reach an optimal size (as some free-living forms polar colonies, reflecting a lack of food availability do; Winston and Håkansson 1989), or they may shed

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layers that are heavily fouled (Winston and Håkansson time; conversely, measured calcification rates can be 1989). Some colonies, such as Membranipora, grow allocated to zooid number in order to determine mg along with their macro-algal substrate (Winston and CaCO3 per zooid (Reid 2014). Although technically Hayward 2012). Others, such as Pentapora, seem bryozoans should be bleached or ashed to remove as if they could grow forever (Cocito et al. 2004). organic material (ash-free dry weight) in order to

Growth has consequences – some biological calculate calcimass, in reality CaCO3 is much heavier activities do not happen until a colony reaches than dried organics and, at least among robustly a critical size. For example, the onset and frequency calcified bryozoans, dry weight is not much different of reproductive ovicells and degenerative brown bodies (Barnes et al. 2011) can be related to the overall size of the colony (or Less intuitive growth measures (per Amui-Vedel not, see Hayward and Ryland 1975). Some colonies et al. 2007) have been trialled, including: Specific may exert control over their shape as they grow, for Growth Rate r = ln(N/N0)/t where N0 = initial zooid example, by dropping unnecessary branches. number; N = final zooid number, t = time (days) elapsed, which ranges from 0.1 to 0.3; and doubling

time t2 = 0.693/r in days, where r = radius. BRYOZOAN COLONIAL GROWTH RATES Smith (2014) collated measured growth rates for As with the measurement of size, growth rates in 44 bryozoan species from the literature, and we have various forms are also measured in different ways. updated that table (by including additional references), A radial encrusting colony is generally measured in resulting in measured growth rates for 84 bryozoan terms of increase in diameter or area. A branching species (Appendix Table). The most commonly used colony, on the other hand, might be measured in measure of growth rate was linear extension, either as terms of increased height, or the sum of branch colony height or radius. We standardised these measures lengths or even the number of branches. Smith’s to mm/y (even though many species do not grow all year (2014) summary of growth rate measurements of long); rates ranged from 0.1 to 1400 mm/y (mean 87 bryozoan colonies (updated in Appendix Table) mm/y; standard deviation 245 mm/y; N = 54). Another shows a range of units and approaches in reporting common growth rate measure was increase in area; growth rates, including cm/y, mm2/y, zooids per again, we standardised to annual growth in mm2/y. month, specific growth rate, and doubling rate. These Colonial growth rate by area ranged from 44 to 193, various measurements are difficult to compare against 235 mm2/y (mean 20,998 mm2/y; SD 43, each other and make it nearly impossible to reach 897 mm2/y; N = 19). Calcification rate ranged any conclusions about the range of normal growth from 9 to 23,700 mg CaCO3/y (mean 1499 mg CaCO3/y; rates in bryozoans. SD 5247 mg CaCO3/y; N = 20). All three measures of Growth rate can translate, in most marine growth rate (Table 2) suggest either that growth rate bryozoans, into calcification rate. Specimens can varies among species by four orders of magnitude, or be weighed before and after, or the newly-added that growth rates measured by different researchers skeletal material can be separated and weighed (e.g., using different methods cannot be compared. In either Smith et al. 2001), or the proportion of volume that is case, the data do not lead to any useful generalisation calcified (% calcimass) can be applied to the volume about bryozoan colonial growth rates. of the newly added colony. Calcification rate (in mg

CaCO3/y) offers a way to compare growth rate among different colonial forms which expand in different INFLUENCE OF METHODS ON RESULTS ways. If the carbonate per zooid is fairly constant It may be that there is so much variation in measured (and it might be in a clonal organism, see Smith bryozoan colony growth rates because of the variety of et al. 2001), it can be directly calculated from zooids/ methods that are used. To consider this possibility, we

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Table 2. Summary of data comprising 88 measurements of colony growth from 81 species of bryozoan (based on Appendix Table).

Maximum Maximum Maximum Growth Increase Calcimass Calcification Calcification observed height observed known rate in (% that rate per zooid or radius area age extension area is skeleton) (mg CaCO /y) (mg CaCO /zz) (mm) (mm2) (y) (mm/y) (mm2/y) (wt%) 3 3

Min 2 97 0.1 0.1 44 0.4 9 0.1

Mean 114 4229 13 87 20988 85 1499 0.5

Max 1000 23400 86 1400 193235 230 23700 1.0

Range 998 23303 86 1400 193191 230 23691 1

StdDev 196 6288 16 245 43897 92 5247 0.4

N 28 20 42 54 19 4 20 3

have separated methods into seven categories (Table is known, it still measures the earliest, most rapid 3). Growth rate in bryozoan colonies can be measured growth of a colony, as it first spreads out. by direct observation (in the laboratory or in the field), Culturing bryozoans in the laboratory provides mark-and-recapture (both chemical and physical marks more environmental control, but it is notoriously can be used) or by inference/proxy. Each of these difficult, particularly for large robustly-calcified methods has its strengths and weaknesses. species. Environmental variations, such as temperature (Amui-Vedel et al. 2007) or current Direct Observation speeds (Sokolover et al. 2018), can promote or retard Direct observation of growth rate can occur either growth. It appears that genetic variation in growth in the sea (usually using settling plates) or in the rates may also be considerable (Bayer and Todd lab. Settling plates that are simply empty substrate 1996). Diet and feeding regime also affect growth placed in the sea (e.g., Skerman 1958) provide only rate (Winston 1976; Jebram and Rummert 1978). a minimum growth rate (as researchers don’t know Lab culture of bryozoans is often over short time when each colony settled). On the other hand, early periods (e.g., 42 days in Winston 1976), possibly growth when colonies are just starting out can be because bryozoans do not grow well in captivity. the most rapid growth of the colony’s life (Ryland If conditions are suboptimal, growing bryozoans 1976). Different substrates, flow rates, orientations, in culture may underestimate growth rate (see e.g., light regimes, and water depths may affect growth Smith et al. 2019). rate (e.g., Edmondson and Ingram 1939). And, of course, there is an element of random chance: Mark and Recapture researchers only catch the species that settle, which Mark-and-recapture techniques are well known in may be random or skewed towards first-colonising biology and have been applied to bryozoans as well as weedy r-selected species. whales (e.g., Urian et al. 2015). Here an adult bryozoan To overcome some of those difficulties, some colony is marked mechanically or chemically, and its researchers have settled larvae on glass slides, then size recorded. Then it is left in its natural habitat to grown them in the sea or in the laboratory (e.g., grow. After time elapses, researchers revisit the colony Jebram and Rummert 1978; Kitamura and Hirayama and re-record its size. The bryozoan is photographed 1984). Others have mounted a piece of adult colony before and after marking (e.g., Okamura and Partridge on a substrate (e.g., Sokolover et al. 2018). While 1999), or the bryozoan is immersed in a chemical this strategy ensures that the exact time of growth marker dye such as calcein (Smith et al. 2019) and

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Table 3. Methods used for the measurement of bryozoan colony growth.

In the ocean (in vivo) In the lab (in vitro) In dead specimens (post-mortem)

A. Settling plate placed empty in the sea, Direct collecting whatever settles C. Seeding a substrate, Observation B. Seeding a substrate, then growing it in the lab then returning it to the sea to grow

D. Marking colonies either E. Marking colonies with with chemicals or tags, Mark and chemicals or tags, growing returning to the field, Recapture in the lab, then collecting re-collecting or or photographing them photographing after a time

F. Counting annual growth checks or generations of ovicells

Inference G. Using chemical signals (such as stable isotopes) to track seasonal variations in environment then recovered and the unmarked skeleton measured Growth checks can lead to underestimation of the (e.g., Smith et al. 2001). These techniques have the overall average growth rate (calculated as a simple advantage that growth is of adult colonies, beyond the size/time) (Key et al. 2018). Antarctic bryozoans initial flush of growth, and that growth is occurring in grow at the same approximate rate as their temperate the natural habitat. It is not uncommon, however, to counterparts, but only for the few months of summer. lose colonies or be unable to relocate them, not least So, a colony of the same size would be much older because tagging itself can increase colony vulnerability than its temperate or tropical cousin. to currents and waves. Comparison of Methodologies Inference/Proxy We collated measured growth rates collected using Direct observation and mark-and-recapture techniques all seven of these methods (see Table 4), grouped measure growth over a short period of time. A better them according to method of measurement, and way to determine age and growth over the life of calculated basic descriptive statistics on them, the whole colony is to utilize signals, physical and/ to see if measurement method influences growth or chemical, that indicate periods of time (like tree rate measured. In every case where there was rings). For example, cross-time colony samples of a range, we chose the maximum growth rate. oxygen isotope concentrations form a record of sea- While there are very unequal sample numbers water temperature and consequently document the among methods, and the data were not designed passing of seasons (e.g., Pätzold et al. 1987; Bader for this test, nevertheless Table 4 shows that and Schaefer 2005; Key et al. 2013, 2018). Colonies long-term measurements of growth over the life with measurable growth checks also allow annual of the colony (annual growth checks and chemical growth to be measured from the annual bands of proxies for growth) give much lower numbers than thicker skeleton that can be detected by x-rays or those which measure growth rate over periods of even just visually (e.g., Barnes 1995; Smith 2007). days to weeks. Settling plates de novo measure Using growth checks and isotopes simultaneously the fastest growth rates, which makes sense as allows validation of the annual nature of the signal they attract early settlers who grow fast to carve (Key et al. 2018). out space early.

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Table 4. The influence of measurement technique on measured growth rate.

Mean annual growth rate

Linear extension Increase in Area Calcification Rate Number Method of (mm/y) (mm2/y) (mg CaCO /y) of species 3 measuring growth measured Std Std Std rate Min Max Mean Min Max Mean Min Max Mean this way Dev Dev Dev

A Settling Plates 38 1 1400 136 331 665 193235 30203 53183 220 736 478 258 in vivo, de novo B Substrate seeded, 2 220 0 73 0 730 0 in vivo C Substrate seeded, 6 438 0 52 7300 3461 3327 48 0 in lab D Mark and Recapture 4 7 730 368 362 44 37595 18820 18776 23700 0 in vivo E Mark and Recapture 5 0 1 1 1 in lab F Annual growth checks 23 1 36 9 8 9 1593 270 451 (morphological) G Chemical proxies 4 8 40 19 13 222 0 160 230 195 35 for annual growth All Methods 81 0 1400 88 245 44 193235 20211 42853 9 23700 1467 5116

CONCLUSIONS only the first flush of rapid growth or rely on It is a little disappointing to have summarised data culture in the laboratory. Mark-and-recapture is from dozens of papers and species and not to be effective over a short time, but the best picture able to answer the question: “How fast do bryozoan of growth and growth rate in a bryozoan colony colonies grow?” Until we have a standardized is achieved by the interpretation of physical or methodology, we will be unable to do more than chemical annual markers, when present. In addition, cite whichever paper is most relevant to our we recommend that characterisations of growth in own species and growth form. Furthermore, it well-calcifieid bryozoans (whether linear, areal, or is currently impossible to compare growth rates in number of zooids) include also the weight of the among bryozoans, especially among those with skeleton, so that calcification rate can be calculated. different growth forms. Calcification rate has real potential, among well- A study should be designed in which bryozoans of calcified bryozoans, to be a unit comparable among both encrusting and erect branching growth forms are growth forms. cultured in the laboratory, grown at sea, and observed in the wild. Post-mortem analysis of oxygen isotopes or growth checks should also be carried out. The use ACKNOWLEDGEMENTS of different techniques over the same season(s) in We gratefully acknowledge support from the Division the same species should reduce variability and allow of Science at University of Otago and the Centre for selection of the best methods for ascertaining for Global Study and Engagement at Dickinson bryozoan growth rates. College. The manuscript was much improved by In the meantime, we suggest that growth rate comments from Prof. Steve Hageman, Appalachian studies in bryozoans avoid methods that measure State University.

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Journal of Experimental Edmondson, C.H. and Ingram, W.M. 1939. Fouling Marine Biology and Ecology. 188, 181–198. organisms in Hawaii. Occasional Papers of Bernice P Barnes, D.K.A., Webb, K.E. and Linse, K. 2007. Bishop Museum, Honolulu Hawaii XIV, 251–300. Growth rate and its variability in erect Antarctic bryozoans. Fortunato, H., Schäfer, P. and Blaschek, H. Polar Biology 30, 1069–1081. 2013. Growth rates, age determination, and calcification Barnes, D.K.A., Kuklinski, P., Jackson, J.A., levels in Flustra foliacea (L.) (: Cheilostomata): Keel, G.W., Morley, S.A. and Winston, J.A. preliminary assessment. In: A. Ernst, P. Schäfer and J. 2011. Scott’s collections help reveal accelerating marine Scholz (eds) Bryozoan Studies 2010, Lecture Notes in life growth in Antarctica. Current Biology 21, R147–R148. Earth System Sciences 143, 59–74. Bayer, M.M. and Todd, C.D. 1996. Effect of polypide Geraci, S. and Relini, G. 1970. Osservazioni regression and other parameters on colony growth in sistematico-ecologiche sui briozoi del fouling Portuale the cheilostomate Electra pilosa (L.). In: D.P. Gordon, di Genova. Bollettino dei Musei e degli Istituti Biologici A.M. Smith and J.A. Grant-Mackie (eds), Bryozoans in del’Universitadi Genova 38, 103–139. Space and Time. Proceedings of the 10th International Hageman, S.J. 2003. Complexity generated by iteration Bryozoology Conference. Wellington, Wilson and Horton, of hierarchical modules in Bryozoa. Integrative and pp. 29–45. Comparative Biology 43, 87–98. Bayer, M.M., Cormack, R.M., and Todd, C.D. Hageman, S.J., Bock, P.E., Bone, Y., and 1994. Influence of food concentration on polypide McGowran, B. 1998. Bryozoan Growth Habits: regression in the marine bryozoan Electra pilosa (L.) Classification and Analysis. Journal of Paleontology (Bryozoa: Cheilostomata). Journal of Experimental Marine 72, 418–436. Biology and Ecology 178, 35–50. Hageman, S.J., Bone, Y., McGowran, B. and Bone, Y. 1991. Population explosion of the bryozoan James, N.P. 1997. Bryozoan colonial growth forms as Membranipora aciculata in the Coorong Lagoon in paleoenvironmental indicators: Evaluation of methodology. late 1989. Australian Journal of Earth Sciences 38, Palaios 12, 406–419. 121–123. Hayward P.J. and Harvey, P.H. 1974. Growth and Bone Y. and James N.P. 1993. Bryozoans as carbonate mortality of the bryozoan Alcyonidium hirsutum (Fleming) sediment producers on the cool-water Lacepede shelf, on Fucus serratus L. Journal of the Marine Biological southern Australia. Sedimentary Geology 86, 247–271. Association of the UK 54, 677–684. Brey, T., Gutt, J., Mackensen, A. and Starmans, Hayward, P.J. and Ryland, J.S. 1975. Growth, A. 1998. Growth and productivity of the high Antractic reproduction and larval dispersal in Alcyonidium hirsutum bryozoan Melicerita obliqua. Marine Biology 132, 327–333. (Fleming) and some other Bryozoa. 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Nielsen and G.P. Larwood Taylor, P.D. 2008. Influence of seawater temperature (eds), Bryozoa: to Recent. Fredensborg, Olsen on growth bands, mineralogy and carbonate production and Olsen, pp. 161–168. in a bioconstructional bryozoan. Facies 54, 333–342. Jackson, J.B.C. and J.E. Winston. 1981. Modular McClelland, H.L.O., Taylor, P.D., O’Dea, A. growth and longevity in bryozoans. In: G.P. Larwood and and Okamura, B. 2014. Revising and refining the C. Nielson (eds), Recent and Fossil Bryozoa. Fredensborg, bryozoan zs-MART seasonality proxy. Palaeogeography, Olsen and Olsen, pp. 121–126. Palaeoclimatology, Palaeoecology 410, 412–420. Jebram, D. and Rummert, H.-D. 1978. Influences McKinney F.K. and Jackson, J.B.C. 1989. Bryozoan of different diets on growth and forms of Conopeum Evolution. Boston, Unwin-Hyman, Boston. seurati (CANU) (Bryozoa, Cheilostomata). Zoologische Menon, N.R. 1975. Observations on growth of Flustra Jahrbücher Abteilun für Systematik, Geographie, und foliacea (Bryozoa) from Helgoland waters. Helgoländer Biologie der Teire 105, 502–514. wiss Meeresunters 27, 263–267. Kahle, J., Liebezeit, G. and Gerdes, G. 2003. Menon, N.R. and Nair, N.B. 1972. The growth rates of Growth aspects of Flustra foliacea (Bryozoa, Cheilostomata) four species of intertidal bryozoans in Cochin backwaters. in laboratory culture. Hydrobiology 503, 237–244. Proceedings Indian National Science Academy 38, Key, M.M., Jr., Hollenbeck, P.M., O’Dea, A. and 397–402. Patterson, W.P. 2013. Stable isotope profiling in Nelson, C.S., Hyden, F.M., Keane, S.L., Leask, modern marine bryozoan colonies across the Isthmus of W.L. and Gordon, D.P. 1988. Application of bryozoan Panama. Bulletin of Marine Science 89, 837–856. zoarial growth form studies in facies analysis of non- Key, M.M., Jr., Rossi, R.K., Smith, A.M., Hageman, tropical carbonate deposits in New Zealand. Sedimentary S.J. and Patterson, W.P. 2018. Stable isotope Geology 60, 301–322. profiles of skeletal carbonate validate annually-produced Nekliudova U.A., Shunkina K.V., Grishankov growth checks in the bryozoan Melicerita chathamensis A.V., Varfolomeeva M.N., Granovitch A.I. from Snares Platform, New Zealand. Bulletin of Marine and Ostrovsky A.N. 2019. Colonies as dynamic Science 94, 1447–1464. systems: reconstructing the life history of Cribrilina Kitamura, H. and Hirayama, K. 1984. Growth of annulata (Bryozoa) on two algal substrates. Journal the bryozoan Bugula neritina in the sea at various water of the Marine Biological Association of the United temperatures. Bulletin of the Japanese Society of Scientific Kingdom 99, 1–15. Fisheries 50, 1–5. O’Dea, A. and Okamura, B. 2000. Cheilostome Kuklinski, P. and P.D. Taylor. 2006. Unique life bryozoans as indicators of seasonality in the Neogene history strategy in a successful Arctic bryozoan, Harmeria epicontinental seas of Western Europe. In: A. Herrera- scutulata. Journal of the Marine Biological Association Cubilla and J.B.C. Jackson (eds.), Proceedings of the 11th of the UK 86, 1305–1314. International Bryozoology Association Conference. Balboa, Kuklinski, P., Sokolowski, A., Ziolkowska, M., Smithsonian Tropical Research Institute, pp. 74–86. Balazy, P., Novosel, M. and Barnes, D.K.A. Okamura, B. and Partridge, J.C. 1999. Suspension 2013. Growth rate of selected sheet-encrusting bryozoan feeding adaptations to extreme flow environments in colonies along a latitudinal transect: preliminary results. a marine bryozoan. Biological Bulletin 196, 205–215. In: A. Ernst, P. Schäfer and J. Scholz (eds) Bryozoan Pätzold, J., Ristedt H, and Wefer G. 1987. Rate Studies 2010, A. Lecture Notes in Earth System Sciences of growth and longevity of a large colony of Pentapora 143, pp. 155–167 foliacea (Bryozoa) recorded in their oxygen isotope Lagaaij, R. and Gautier, Y.V. 1965. Bryozoan profiles. Marine Biology 96, 535–538. assemblages from marine sediments of the Rhone delta, Reid CM. 2014. Growth and calcification rates in polar France. Micropaleontology 11, 39–58. bryozoans from the of Tasmania, Australia. In:

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Effects of reproductive strategy, Marine Biology Research, DOI: temperature, size, and food on the growth of Membranipora 10.1080/17451000.2018.1526385 membranacea in laboratory and field studies. Marine Stach, L.W. 1935. Growth variation in Bryozoa Biology 156, 2267–2276. Cheilostomata. The Annals and Magazine of Natural Schopf, T.J.M. 1969. Paleoecology of ectoprocts History 16, ser 10, 645–647. (bryozoans). Journal of Paleontology 43, 234–244. Stebbing, A.R.D. 1971. Growth of Flustra foliacea Skerman, T.M. 1958. Marine fouling at the port of (Bryozoa). Marine Biology 9, 267–272. Lyttelton. New Zealand Journal of Science 1, 224–257. Taylor, P.D. and James, N.P. 2013. Secular changes in Smith, A.M. 1995. Palaeoenvironmental interpretation colony-forms and bryozoan carbonate sediments through using bryozoans: a review. In: D. Bosence and P. Allison geological history. Sedimentology 60, 1184–1212. (eds), Marine Palaeoenvironmental Analysis from Fossils. Taylor, P.D. and E. Voigt. 1999. 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Wass, R.E., Vail, L.L. and Boardman, R.S. 1981. Smith, A.M., Key, M.M., Jr. and Wood, A.C.L. Early growth of Bryozoa at Lizard Island, Great Barrier 2019. Culturing large erect shelf bryozoans: skeletal Reef. In: G.P. Larwood and C. Nielsen (eds), Recent and growth measured using calcein staining in culture. In: Fossil Bryozoa, Fredensborg, Olsen and Olsen, 299–303. R. Schmidt, C.M. Reid, D.P. Gordon, G. Walker‐Smith, Winston, J.E. 1976. Experimental culture of the estuarine S. Martin and I. Percival (eds), Bryozoan Studies 2016. ectoproct Conopeum tenuissimum from Chesapeake Bay. Proceedings of the Seventeenth International Bryozoology Biological Bulletin 150, 318–335. Association Conference, 10‐15 April 2016, Melbourne, Winston, J.E. 1983. Patterns of growth, reproduction and Australia. Memoirs of the Australasian Association of mortality in bryozoans from the Ross Sea, Antarctica. Palaeontologists 52, 131–138. Bulletin of Marine Science 33, 688–702. 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2001 2013 1972 2007 2007 2019 2007 2006 1995; Sources Bader & Hayward & Kitamura & Smith et al., Smith et al., Barnes et al., Barnes et al. Bader, 2000; Bader, Ingram 1939 Smith, 2007; Smith, 2007; Barnes et al., Barnes et al., Barnes, 1995 Ryland, 1976 Ryland, Ryland, 1975 Ryland, Bowden et al., Skerman 1958 Skerman 1958 Edmondson & Winston, 1983 Winston, Winston, 1983 Winston, Winston, 1983 Winston, Winston, 1983 Winston, Menon & Nair Schaefer, 2005 Schaefer, Winston, 1983; Winston, Winston, 1983; Winston, Winston, 1983; Winston, Hirayama 1984 Kuklinski et al., Brey et al., 1999 Barnes et al., 2011

F F F F F F F F F F E B A A A A A A D D G G Code Method (Table 4) (Table checks checks checks checks checks checks checks checks checks checks in vivo in vivo profiles profiles Method in culture then in vivo Observation Stable isotope Stable isotope Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Larvae seeded Annual growth Annual growth Annual growth Annual growth Annual growth Annual growth Annual growth Annual growth Annual growth Annual growth Calcein marked Calcein marked /zz) 3

0.13 zooid (mg CaCO Calcification per Calcification per /y) 3

24 63 55 57 45 160 730 rate 23700 Calcification (mg CaCO

(wt% skeleton) Calcimass

/y) 2 44 36240 Growth rate (area in mm 1 8 5 60 40 5.5 6.9 4.4 5.4 4.4 5.6 7.1 4.6 5.6 4.3 420 152 mm/y) Growth rate Growth (extension in

7 2 20 15 20 18 26 14 18 14 15 12 14 (y) 0.4 0.2 0.5 age Max

) 2 100 area area 3020 (in mm Max observed 56 70 30 80 48 57 60 60 2.8 300 100 size (height or size (height or Max observed radius in mm)

/y /y /y

cm,

2 3 3

/y on /y 2 3 mm

/mo /y mg, 2 3 /y 3 cm, mg ash free cm, max in 160 days cm, max 14 2 mg CaCO mg CaCO mg CaCO cm, 12 internodes cm in 6 mo 1 mm/y dry wt/y in spring 7 yrs age cm in 2 mo in 14 days internodes in summer 7 max age 14 y 24 g CaCO max size 8 1-3 24 mg CaCO (assumed annual) height in 156 days max 18 internodes (mean = 131, n=2) 270 zooids, 28 max 11 internodes; max 11 1964-3020 mm max size 5.6 one branch/y, 8 mm/y, 8 mm/y, one branch/y, 52-210 mm2 in 18 mo mm/y, 30 mm/y, max 11 internodes, 3.9 max 11 Reported growth rate Reported growth max age 20 y, 5.4 mm/y max age 20 y, max age 1.5-2 y, growth max age 1.5-2 y, 3 inches in mo, 65 6.9 mm/y branch length, max size 6.0 10 internodes; 3.4 mm/y, 10 internodes; 3.4 mm/y, .0 to 7.1 mm/y, 3-57 mg/y, 3-57 mg/y, 1 .0 to 7.1 mm/y, 5.2 mm/y, 55 5.2 mm/y, 4.6 mm/y, 45 4.6 mm/y, 1.3 to 5.6. mm/y, 5-33 mg/y, 5-33 mg/y, 1.3 to 5.6. mm/y, 32-40 mm/y, 12-57 g/m 32-40 mm/y, artificial panels, n = 10; up up to 100 mm to 0.4 mm/d radial extension max size 6 max age 14 y, max size 5.7 max age 14 y, max age 26 y, 63 max age 26 y, mean increase 100 mm max age 18 y, max size 4.8 am, max age 18 y, branching branching branching branching branching articulated articulated articulated articulated Erect rigid Erect rigid Encrusting Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar flexible base flexible base flexible base flexible base flexible base flexible base flexible base flexible base flexible base Erect flexible Erect flexible Erect flexible Erect flexible Erect flexible Erect flexible Erect flexible Growth form Growth erect branching, erect branching, erect branching, erect branching, erect branching, erect branching, erect branching, erect branching, erect branching,

NZ NZ UK India Japan Hawaii English Cochin, Signy Is Channel Ross Sea Ross Sea Ross Sea Ross Sea Ross Sea Location Lyttleton, Lyttleton, Lyttleton, Lyttleton, Ross Sea, Ross Sea, Nagasaki, Antarctica Antarctica Ryder Bay, Bay, Ryder Otago shelf, Adriatic Sea Weddell Sea Weddell Weddell Sea Weddell Weddell Sea Weddell Weddell Sea Weddell South Wales, South Wales, New Zealand Kaneohe Bay, Kaneohe Bay, Otago Shelf NZ Doubtful Sound, ppendix Table: Summary of published literature on size, age, growth and calcification in 83 species of bryozoans. and calcification growth age, on size, Summary of published literature Table: ppendix Adeonellopsis sp. Adeonellopsis sp. Species Alcyonidium hirsutum Alderina arabianensis Alloeflustra tenuis Arachnopusia inchoata Bugula neritina Bugula neritina Bugula sp. (aff. neritina ) Caberea zelandica Caberea Callopora dumerilii Cellaria incula Cellaria sinuosa Cellarinella foveolata Cellarinella margueritae Cellarinella njegovanae Cellarinella nodulata Cellarinella nutti Cellarinella rogickae Cellarinella rossi Cellarinella roydsi Cellarinella sp. M A

152 Abigail M. Smith and Marcus M. Key, Jr.

2007 2019 1994 2007 1985 2013 2013 1972 1972 2013 2013 2006 Hunter & Jebram & Paul 1942 Jackson & reported in et al., 2001 Wertheimer, Wertheimer, Barnes et al., Sobich, 1996 Hughes 1993 Barnes, 1995; Winston 1976 Winston Bayer & Todd Bayer & Todd Bowden et al., Skerman 1958 Menon & Nair Menon & Nair Menon & Nair Rummert, 1978 Key et al., 2013 Kuklinski et al., Kuklinski et al., Kuklinski et al., Kuklinski et al., Smith et al 2019 and many others Amui-Vedel et al, Amui-Vedel Smith & Nelson, Nekliudova et al., 1996; Hermansen Bayer et al., 1994; F F F E C C C A A A A A C A A A A A A G checks Ovicell profiles Culture Culture Culture isotopes in culture generations Lab Culture Stable isotope Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Annual growth Growth checks, Calcein marked 230 176 736 230 260 222 2400 8484 33936 193 235 1102-6230 4 4.1 3.7 8.4 1.3 4.3 1.15 77.1 0.75 1 11 86 2.5 0.5 1.5 0.12 > 2y 222 140 707 1200 2828 18 000 3 2 65 50 8.4

,

2

/y

3

/14 2 cm, /y on 2

cm tall in 8 mo /56 days; 2 in 2 y 2 2 2 in 103 d, 2 in one year /mo in spring mg CaCO in 18 mo 3 2 2 in 4 y (n = 4) /mo (june-Jan) in 6 mo 2 2 2 mm diameter, mm diameter, mm diameter, mm diameter, mm diameter, g in 1.0 y g in 1.5 y g in 2.5 y mm in 34 days 1.4 cm , max colony area in summer in 4 weeks 1.15 mm/y 2 in 25-31 days 0.23 0.31 0.20 12 cm max age 17 mo (mean = 92, n 3) (depending on diet) 14°C: 100 zooids in 82-98 mm 81 to 234 mm (mean = 4951, n 4) up to 1629 zooids and up to about 800 zooids in July; radius of about 180x100 750µ/y, up to 6.5 750µ/y, days; 15-100 zz/14 days GP2: 16.6 GP3: 15.6 GP1: 16.8 311-1758 mm 311-1758 8 generations in 42 days mm (measured off photo), mean max of 155 zooids 0.1 cm max age 86 y, avg growth max age 86 y, 4 weeks; 18C: 300 zooids max age 9 y, max ht 5 max age 9 y, 736 mg CaCO 2376 to 8290 mm from 1 to 40 mm lifespan >2 y, 2-15 mm lifespan >2 y, 53 to 88 mm 4.1 mm/y, 176 4.1 mm/y, 3 mean increase 50 mm 314-707 mm 0.3 mm/day radial extension median colony area = 0.6 cm from 6 to 591 zooids/56 days artificial panels, n = 20; up to smallest reproductive colony = 2213-2828 mm braching branching Erect rigid Encrusting Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting Encrusting unilaminar flexible base multilaminar multilaminar Erect flexible erect branching,

NZ NZ UK UK USA India India Wales, Wales, Cochin, Cochin, Jamaica Harbour, Harbour, Signy Is, Germany Lyttleton, Lyttleton, Baltic Sea Antarctica Rio Bueno Ryder Bay, Bay, Ryder Kiel Canal, Spitsbergen Spitsbergen Otago shelf, Adriatic Sea Weddell Sea Weddell Kandalaksha Swansea UK New Zealand Hauraki Gulf, Gulf of Aqaba Gulf of Bay, White Sea Bay, Gulf of Panama Chesapeake Bay Scotland, Wales, Scotland, Wales, Cellarinella watersi Celleporaria fusca Celleporella hyalina Celleporella Chaperiopsis protecta Cinctipora elegans Conopeum seurati Conopeum tenuissimum Cribrilina annulata Cribrilina annulata Crisia sp. Cryptosula pallasiana Cryptosula pallasiana Cupuladria exfragminis Diploselen cf obelia Diplosolen arctica Disporella gordoni Disporella Drepanophora tuberculatum Einhornia crustulenta Electra bengalensis Electra crustulenta Electra pilosa

153 Bryozoan Studies 2019 1994 2007 2013 2013 2013 2006 2019 2019 Sources Smith & Stebbing, Eckman & Bone 1991 Brey et al., Saunders & Okamura & Smith et al., Smith et al., Kuklinski & Taylor, 2006 Taylor, Barnes et al., 1971; Menon Lawton, 2010 Duggins 1993 Metaxas 2009 Bowden et al., Skerman 1958 Partridge 1999 1998; Bader & Winston, 1983; Winston, 1975; O‘Dea & Schaefer, 2004; Schaefer, Okamura 2000; Fortunato et al., Kuklinski et al., Kuklinski et al., Smith & Nelson, Kahle et al, 2003 Smith et al, 2019

F F F E E E A C A C A C A A A D D Code Method (Table 4) (Table in situ checks checks checks in vivo Method in culture in culture in culture Mark and photograph Lab Culture Lab Culture Observation then in vitro Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Larvae seeded Annual growth Annual growth Annual growth Calcein marked Calcein marked Calcein marked /zz) 3

zooid (mg CaCO Calcification per Calcification per /y) 3

9 48 34 220 rate about 850 Calcification (mg CaCO

(wt% skeleton) Calcimass

/y) 2 52 665 7300 37595 Growth rate (area in mm 4 2.5 8.1 1.4 2.5 438 730 13.7 1.38 0.05 0.05 mm/y) 10 to 26 Growth rate Growth (extension in

1 3 9 50 12 (y) 1.7 age Max

) 2 97 400 area area (in mm Max observed 2 30 40 5.1 200 size (height or size (height or Max observed radius in mm)

2 mg /d 2 in

/y on mg 3 2 /day 2 mm, less cm in 8 y, cm, mg in 92 max, mean /y 2 3 in 3 y (n = 4) in 4 y 2 2 /y, max age 32 /y, 3 mg CaCO in 20 mo 6cm days cm, 9 segments, area of front 2 2 one year CaCO extension 2.65 cm/y in summer 1.38 mm/y 0.05 mm/y 0.05 mm/y 92 mm /y, ht of 7.93 /y, 4 cm 3 max size 6.6 than a year‘s growth 19 days in pipes with from 5 to 20 mm 1.3 to 13.7 mm/y, 9 1.3 to 13.7 mm/y, Reported growth rate Reported growth 25 to 220 annual growth rates up to 1-13 mm 0.1 to 1.2 mm/day linear in 92 days , 3-12 2 mm/day, max diameter 2 mm/day, growth rate 86-103 mm max size 4 mean increase 50 mm different flows: growth rates 34 mg CaCO CaCO 0.3 mm/day radial extension mean, 1400 mm max 22 segments, 4.9 mm/y; 12 y age, 15 mm/y, 25 – 220 12 y age, 15 mm/y, 137 to 175 mm 10 days, added 800-900 mm max diameter of 5.1 artificial panels, n = 50; up to branches in 92 days, 80-248 zz mostly fenestrate branching branching branching Erect rigid Erect rigid Encrusting Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Blade with Blade with Encrusting, flexible base flexible base Erect flexible Erect flexible Growth form Growth

NZ NZ USA State Arctic Ireland Lagoon, Scotland Coorong Ross Sea Location Lyttleton, Lyttleton, North Sea Antarctica Helgoland, S Australia Ryder Bay, Bay, Ryder Otago shelf, Otago shelf, Otago shelf, Nova Scotia Washington, Washington, Wales, North Wales, Weddell Sea, Weddell Lough Hyne, New Zealand New Zealand New Zealand Hauraki Gulf, & Washington & Washington Norwegian Sea Norwegian Sea S New Zealand Sea, Baltic Friday Harbour, Friday Harbour, Snares Platform, Flustra foliacea rugula Membranipora nitida Membranipora membranacea Escharella immersa Escharella Species Membranipora aciculata Membranipora membranacea Melicerita obliqua Encrusting bryozoans (18 spp.) Escharoides angela Escharoides Flustra foliacea Membranipora membranacea Harmeria scutulata Figularia sp. Hornera foliacea Hornera robusta Melicerita chathamensis Summary of published literature on size, age, growth and calcification in 83 species of bryozoans (continuation). in 83 species of bryozoans and calcification growth age, on size, Summary of published literature

154 Abigail M. Smith and Marcus M. Key, Jr. 1972 1985 1985 2013 1987 1972 1972 1985 2008 2013 2013 1999 Cocito & et al 2018 Paul 1942 et al. 2006 Jackson & Jackson & Jackson & reported in reported in Ferdeghini, Wertheimer, Wertheimer, Wertheimer, Wertheimer, Wertheimer, Wertheimer, Ingram 1939 Barnes, 1995 Friedle 1952, Pätzold et al., Ganapati et al Skerman 1958 Edmondson & Menon & Nair Menon & Nair Menon & Nair Menon & Nair Taylor & Voigt, & Voigt, Taylor Lombardi et al., Geraci & Relini Kuklinski et al., Kuklinski et al., Kuklinski et al., 2001; Lombardi 1958 reported in 1970; Sokolover Wass et al., 1981 Wass F F F F A A A A A A B A A A A G checks checks checks checks profiles Seeding Stable isotope Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Settling plates Annual growth Annual growth Annual growth Annual growth 97 73 3120 30415 17605 20 36 10 1.3 3.8 2.2 2.9 803 220 3 11 35 26 0.25 260 4600 2500 1640 3700 11400 23400 10 2.5 116 105 1000

, 2 , 2 2 2

, 2

mm

m mm

cm

2 2 cm diam in 4 y 2 in 2 y, in 2 y, 2 mm apart , max colony , max colony g. Up to 1 2 in 3 y (n = 4) ; 2 /mo in spring 2 in 18 mo 2 cm tall, 82 2 /y, largest branch largest /y, mm in 30 days 8-10 mm mm in 3 yrs 2 mm after 60 d after 3 mo tall, 3 cm/y 44.6 in 4 y area 114 cm area 114 area 234 cm /day; mean max 37 cm max age 26 y 60 length 232 mm 2 , max colony area 46 cm 2 132 in summer; 125 to 100 mm 8 to 89 mm /y, 3.6 cm/y, max skeletal 3.6 cm/y, /y, 41x40mm in 34 days 89 to 192 mm mm in winter; 12-21 smallest reproductive 50x50 smallest reproductive 30,000 zooids in 5 mo 2 dark bands 3 diameter, 358 to 1214 g/ diameter, in diameater after 3 mo; mm diameter in 3 months max size 42 mass 35-1098 median colony area = 5 cm 889 g/m m after 6 weeks; 5.5 122-260 mm 5 smallest reproductive colony = one large fossil colony with one large colony = 8 cm 6-7 1 mm/d in diameter; 50-70 1 09 to 139 mm colony = 22 cm median colony area = 27 cm 0.4 cm 0.73 cm median colony area = 55 cm branching branching branching branching articulated Erect rigid Erect rigid Erect rigid Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting Encrusting Encrusting unilaminar multilaminar multilaminar multilaminar Erect flexible Erect flexible Erect branching Upper Hawaii Europe, Jamaica Jamaica Jamaica Signy Is Harbour Irish Sea Harbour, Harbour, Harbour, Harbour, Harbour, Harbour, UK, NW UK, NW Australia Plymouth and Italian Rio Bueno Rio Bueno Rio Bueno Maastricht, Cretaceous, Netherlands Adriatic Sea Queensland, Ligurian Sea Lyttleton, NZ Lyttleton, Cochin, India Lizard Island, Kaneohe Bay, Kaneohe Bay, Mediterranean Mediterranean Israeli coast of Mediterranean, Norwegian Sea Norwegian Sea Visakhapatnam Visakhapatnam Pentapora foliacea Microporella arctica Microporella Menipea sp. Membranipora sp. Schizoporella Schizoporella sanguinensis unicornis Schizporella Patinella sp. Schizoporella Schizoporella cochinensis Pennipora anomalopora Pentapora spp. Schizoporella errata Schizoporella Membranipora sp. Peullina hincksi Steginoporella sp. nov. Steginoporella Repadeonella ‚plagiopora‘ Microporella sp. Microporella Nematoflustra flagellata Parasmittina sp. Pentapora fascialis

155 Bryozoan Studies 2019 2007 1985 1978 2013 Sources Jackson & Reid, 2019 Reid, 2014 Smith, 2007 Wertheimer, Wertheimer, Wass & Vail & Vail Wass Ingram 1939 Barnes et al., Edmondson & Kuklinski et al., Wass et al. 1981 Wass Wass et al., 1981 Wass

F F F F A A A A A Code Method (Table 4) (Table checks checks checks checks Method Settling plates Settling plates Settling plates Settling plates Settling plates Annual growth Annual growth Annual growth Annual growth

/zz) 3 3 0.9 0.19 1.03 0.45 0.13 1.03 0.41 per zooid per Calcification (mg CaCO /y) 3

9 46 27 20 528 rate 1593 1499 5247 23700 23691 Calcification (mg CaCO

4 12 38 85 92 230 0.38 (wt% 229.62 skeleton) Calcimass

/y) 2 44 19 2700 3435 20988 43897 193235 193191 Growth rate (area in mm 6 16 33 87 54 4.2 4.5 9.7 245 0.05 1400 1400 mm/y) 1399.95 Growth rate Growth (extension in

15 25 28 23 13 86 16 42 (y) age 0.25 0.17 0.25 0.12 Max 85.88

) 2 97 20 584 675 area area 9100 4229 6288 23400 23303 (in mm Max observed 2 28 350 350 114 998 196 1000 size (height or size (height or Max observed radius in mm)

2 , 2

2 mg /y, /y, 3 mg

cm tall in mm thick. cm wide , smallest 2 in 3 y (n = 5) 2 mg CaCO cm in 3 months 3 months /y, 0.19 mg/zooid /y, /y, 1.03 mg/zooid /y, 3 3 mm in 56 days after 9 weeks max age 23 y median colony 5 11-15 y max age 11-15 cm tall, 50 cm wide, 3.5 35 Reported growth rate Reported growth area = 16 cm 4.5x1.5 max colony area 91 cm CaCO CaCO 8.2 to 16 mm/y, max age 8.2 to 16 mm/y, 4 bilamellar, 12.5 bilamellar, 28 y old, 6mm/y, 1593 28 y old, 6mm/y, 4.5 mm/y, 46 4.5 mm/y, 0.6 to 9.7 mm/y, 1-27 mg/y, 1-27 mg/y, 0.6 to 9.7 mm/y, 25 y, 12% calcimass, 528 25 y, reproductive colony = 4 cm 276 to 495 mm Min Mean Six colonies, 148 to 584 mm Max Range StdDev N branching articulated Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar Encrusting unilaminar flexible base flexible base Erect foliose Erect flexible Erect flexible Growth form Growth Erect branching erect branching, erect branching, Hawaii Jamaica Harbour, Harbour, Ross Sea Australia Australia Australia Australia Location Tasmania, Tasmania, Tasmania, Tasmania, Rio Bueno Permian of Permian of Spitsbergen Queensland, Queensland, Weddell Sea Weddell Maria Island, Maria Island, Lizard Island, Lizard Island, Port Hacking, Kaneohe Bay, Kaneohe Bay, NSW, Australia NSW, duplicates = 5 List above = 89 So N species = 84 Stylopoma spongites Species Stenopora tasmaniensis Swanomia belgica Stomhypselosaria watersi Valdemunitella Valdemunitella vldemunita sp Vittaticella Stenopora spiculata sp. Thalamoporella Zoobotryon pellucidus Tegella arctica Tegella Summary of published literature on size, age, growth and calcification in 83 species of bryozoans (continuation). in 83 species of bryozoans and calcification growth age, on size, Summary of published literature

156 Bryozoan Studies 2019

Edited by Patrick Wyse Jackson & Kamil Zágoršek Cover illustration: Calloporina decorata (Reuss, 1847) from section Sedlec (South Moravia – Czech Republic)

Bryozoan studies 2019 – Proceedings of the eighteenth International Bryozoology Association Conference Liberec – Czech Republic, 16th to 21st June 2019

Editors: Patrick Wyse Jackson & Kamil Zágoršek Graphic design: Eva Šedinová Printing: Reprographic Centre of the Czech Geological Survey Published by the Czech Geological Survey, Prague 2020 Publisher is not responsible for the correct grammar of contributions

ISBN 978-80-70759-70-7