Unique life history strategy in a successful Arctic bryozoan, Harmeria scutulata

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1 J. Mar. Biol. Ass. U.K. (2006), 86,1305^1314 Printed in the United Kingdom doi: /S Unique life history strategy in a successful Arctic bryozoan, Harmeria scutulata Piotr Kuklinski* OP and Paul D. Taylor* *Department of Palaeontology, Natural History Museum, Cromwell Road, London, SW7 5BD, UK. O Institute of Oceanology, Polish Academy of Sciences, ul. Powstancow Warszawy 55, Sopot , Poland. P Corresponding author, p.kuklinski@nhm.ac.uk Harmeria scutulata, a cheilostome bryozoan with a circum-arctic distribution, is an important component of intertidal and shallow subtidal rock communities. In terms of numerical abundance, H. scutulata can reach over 50% of total individuals within Arctic bryozoan assemblages. It is an annual, fast-growing species that loses over 70% of interactions for space with other organisms. Uniquely for a bryozoan, the subcircular colonies have large zooids at the centre ringed by a marginal zone of up to six generations of small zooids. This pattern is shown here to be due to polymorphism, re ecting a functional di erentiation between large, feeding zooids (autozooids) and small, non-feeding zooids that brood embryos (gonozooids). The switch from the budding of autozooids to gonozooids occurs more or less simultaneously around the circumferential growing edge of the colony and is irreversible. Colonies apparently produce embryos only near the end of the growing season. Strong wave action and/or ice scour during the winter months destroys most of the colony but it is inferred that some of the gonozooids, which are more thickly calci ed than the autozooids, overwinter, surviving into the spring and releasing their larvae to found a new generation of colonies. A formal systematic redescription of H. scutulata is given. INTRODUCTION Relative resource allocation between growth by zooidal budding and sexual reproduction varies through colony life among species of colonial animals (Hughes, 1989). In bryozoans di erent species exhibit substantial variations in life history investment strategies (McKinney & Jackson, 1989). Some species (e.g. Flustra foliacea) are long-lived perennials that, after a period of early growth, allocate resources jointly to sexual reproduction and continued colony growth. Such colonies typically grow to a large size and may have numerous annual cycles of sexual reproduction (iteropary). At the other end of the spectrum are short-lived, so-called solitary colonies (e.g. Disporella mbriata) with semideterminate growth and a single phase of sexual reproduction (semelpary) which is followed by death of the colony at a small size. Female sexual reproductive investment in most bryozoans culminates in the brooding of embryos that mature into larvae, the usual propagules of dispersal in bryozoans. Structures for brooding may be clearly expressed in bryozoan skeletons, and include the ovicells found in most species of cheilostomes and the specialized gonozooids present in cyclostomes. Therefore information on relative resource allocation to sexual reproduction can be obtained from dead and fossil skeletons. For example, McKinney & Taylor (1997) were able to interpret life history patterns in Jurassic and Cretaceous cyclostome bryozoans from the distribution of gonozooids. A knowledge of the functional morphology of bryozoan skeletons is a rst step towards understanding life history strategies, particularly in view of the di culties of culturing species or of making repeated observations of colonies in their natural habitats. Although it is not unusual to nd co-occurring species having di erent life history strategies, certain environments should favour particular strategies. Here we focus on the unusual life history strategy of the cheilostome bryozoan Harmeria scutulata Busk, a species that inhabits highly disturbed Arctic environments impacted by ice scour and storms. This species is an important component of intertidal and shallow subtidal Arctic communities where it can account for over 50% of individuals within bryozoan assemblages, despite being a poor competitor for substrate space and losing some 70% of interactions with other organisms (Barnes & Kuklinski, 2003; Kuklinski & Barnes, 2005a,b). The rst description of Harmeria scutulata by Busk (1855), based on material fromwest Greenland, noted the unusual organization of the small, subcircular colonies, with large zooids in the centre surrounded by an outer zone of small zooids (Figure 1A). This organization contrasts with the usual bryozoan pattern of zooid size increase through early colony development (zone of astogenetic change), followed by a levelling-o (zone of astogenetic repetition). The signi cance of the two sizes of zooids in H. scutulata has not been previously appreciated. Morphological variations between zooids in colonial animals can be ascribed to four principal sources: microenvironment, ontogeny, astogeny and polymorphism (Boardman & Cheetham, 1973). In Harmeria neither microenvironment (localized ecophenotypy) nor ontogeny (zooid age) can account for the consistent pattern of variation that is independent of the age of individual zooids. Astogeny refers to the

2 1306 P. Kuklinski and P.D. Taylor Unique life history strategy brooding zooids, is unique among bryozoans as far as we are aware. We also include a taxonomic redescription of H. scutulata based on our new ndings as well as a scanning electron microscopy study of type and other material in the Natural History Museum, London (NHM) collections. MATERIALS AND METHODS Material Greenland: NHM , holotype, HMS Sophia, (73820 N W), 6^20 fathoms, on alga, Busk Collection; NHM , , MY Rosaura Expedition 1937^1938, Julianehaab Harbour (60843 N W), collected 4 November 1937, depth 20 m, on algae; NHM ^12 (on alga), MY Rosaura Expedition 1937^ 1938, Julianehaab Harbour (60843 N W); NHM , Dundee Collection; NHM , on alga, Levinsen Collection Canadian Arctic: NHM (on Fucus), (on alga), (15 fathoms, on alga), (15 fathoms, on alga), Assistance Bay, Barrow Strait (74840 N W], collected by Sutherland, Busk Collection. Spitsbergen: NHM , Smeerenburg Bay, 0^1 fathoms, on alga, Norman Collection, from E.A. Smitt; NHM , from E.A. Smitt; NHM , Billefjorden, on alga; NHM , , Advent Fjorden, on alga; NHM , Oxford University Expedition, Billefjorden, on alga; Kuklinski Collection, Isfjorden (788N 158E), NHM , Hornsund (778N 168E), Kuklinski Collection. Norway: NHM , Vadso«, East Finmark, Norman Collection; NHM ^15, near TromsÖ (708N 188E), Kuklinski Collection; NHM , Barents Sea, on Balanus, Hincks Collection; Alaska: NHM , Spruce Island, near Kodiak, intertidal, collected by M. Dick, 6 October Figure 1. (A) Mature colony of Harmeria scutulata (Busk) showing large zooids (autozooids) at the centre surrounded by a ring of small zooids (gonozooids); Julianehaab Harbour, Greenland, NHM ; and (B) gonozooids containing structures believed to be eggs or embryos; Greenland, NHM Scale bars: A, 1 mm; B, 0.3 mm. development of the colony, astogenetic variations being expressed as continuous clines in zooid morphology correlating with the time of formation (budding) of each zooid during the life history of the colony. Polymorphism refers to discontinuous variation (cf. astogeny) in zooidal morphology typically correlating with zooids ful lling di erent functional roles. We show here that zooidal variation in Harmeria is accounted for by polymorphism, the large, central zooids being feeding zooids (autozooids) and the small peripheral zooids non-feeding gonozooids used to brood embryos. No further autozooids are budded once the peripheral zone of gonozooids has been formed. The life history strategy of Harmeria, entailing a complete and irreversible switchover from the budding of feeding zooids to non-feeding Polymorphism In order to prove the presence of polymorphism among zooids within colonies of Harmeria scutulata, seven colonies were used for measurement of zooid dimensions (NHM ^7). Colonies were photographed digitally using a stereomicroscope set-up (NHM Paleovision Axiocam System). Lengths and widths of all zooids within each colony were measured from prints. To determine zooid surface areas, digital images were analysed using the program NIH Image J. It was important to relate zooid size measurements to the positions of the zooids within colonies in order to demonstrate the astogenetic component of intracolonial variation. This was accomplished in three ways, by allocating each zooid to: (1) a generation; (2) a concentric ring; or (3) a series within a ray. Generation number was inferred according to the method developed by Harmer (1931), which entails reconstructing the likely sequence of budding outwards from the ancestrula (primary zooid) based on inferred parent ^ daughter bud relationships. The concentric ring method divided the colony into bands of zooids centred on the ancestrula (primary zooid). The ray method was applied only to those zooids belonging to the

3 Unique life history strategy P. Kuklinski and P.D. Taylor 1307 Figure 2. Frequency distribution of surface areas of zooids within a single colony of Harmeria scutulata showing the distinction between small zooids (gonozooids) and large zooids (autozooids); Julianehaab Harbour, Greenland, NHM ^6 rays traceable directly to the 5^6 periancestrular zooids. For each method (generation, ring, ray) we calculated the mean and standard deviations of zooid size according to position within the colony. We subjected all comparative data to analysis of variance (ANOVA). Colony astogeny data were obtained from panels deployed at 6 m depth for a year (July 2004 to July 2005) in Isfjorden, Spitsbergen (788N 158E). The total diameter of colonies and the diameter of the central zone of autozooids was measured for all colonies on one of these settlement panels, and also from all colonies encrusting a 132 cm 2 rock collected during July 2005 from the intertidal near TromsÖ in northern Norway (708N198E). A low vacuum scanning electron microscope (Leo 1455-VP) was used to study and image the skeletal morphology of bleached, uncoated specimens. Observations of living colonies In order to make observations of living colonies, rocks encrusted by H. scutulata were obtained from 3 m depth in Spitsbergen (788N 158E) during July 2005, transferred to the laboratory and placed in a refrigerator in darkness at a constant temperature of 28C. Only colonies with a peripheral zone of small zooids were selected for observation using a stereomicroscope. Tentacle activity was recorded and counts were made of tentacle numbers. In an attempt to stimulate larval release, colonies kept in darkness were exposed to the light (see Ryland, 1960). RESULTS All measurements of zooid size and surface area showed similar bimodal patterns, supporting the existence of two Table 1. Analaysis of variance results for di erences between measurements of two zooid groups. Source df SS MS F P Total Length SL Width SL Surface area SL E E Generations Length Width Surface area Rings Length Width Surface area Rays Length Width Surface area df, degree of freedom; SS, sum of squares; MS, mean square; F, ratio of within group variation to between group variation; P, probability value; S, small polymorphs; L, large polymorphs in total, and when classi ed according to rays, rings, or generations (as explained in text) for a colony of Harmeria scutulata from Julianehaab Harbour, South Greenland (NHM ).

4 1308 P. Kuklinski and P.D. Taylor Unique life history strategy Figure 3. Mean and standard deviations of surface areas of zooids within a single colony of Harmeria scutulata according to location within colony classi ed by (A) generation; (B) ring; or (C) ray as explained in the text; Julianehaab Harbour, Greenland, NHM

5 Unique life history strategy P. Kuklinski and P.D. Taylor 1309 zooid polymorphs within colonies of Harmeria scutulata (Figures 1^4). The two size-categories of zooids are the central zooids, ranging in length from to mm (mean mm) and surface area from to mm 2 (mean mm), and the smaller peripheral zooids, ranging in length from to mm (mean mm) and surface area from to 0.037mm 2 (mean mm 2 ). Zooid width in the small zooids showed the greatest level of variability of any measured parameter, ranging from to mm (mean mm). This re ects the general increase in small-zooid width outwards resulting from the fact that no new rows of zooids are intercalated to accommodate colony expansion within the zone of small zooids, in contrast to the central zone of large zooids where row intercalations are frequent. There were signi cant di erences between the lengths, widths and surface areas of the two groups of zooids within all colonies (Table 1). The relationship between zooid size (length and width) and astogeny showed the same general pattern regardless of which method (generation, ring or ray) was used to guage the position of the zooid within the colony (Figure 3). A gradual increase in zooid size occurs outwards from the ancestrula to a maximum average value, after which size at rst decreases slightly before diminishing rapidly and abruptly at the transition to the peripheral zone of small zooids. Signi cant di erences were found between generations using all methods (Table 1). Scanning electron microscopy of the transition between the large and small zooids supports the quantitative distinction between the two polymorph types (Figure 4). The large zooids are not only bigger but have more extensive proximal gymnocysts, smaller cryptocystal pseudopores and bell-shaped ori ces as opposed to the oval ori ces found in the small zooids. Although it is sometimes possible to nd a large zooid in one row budded in a more distal location (and therefore seemingly later) than a small zooid in a di erent row of the same colony, once an individual row had commenced budding small zooids it never reverted to large zooids. Therefore, switchover from large to small zooids is irreversible. Occasionally, examples of zooids were observed that appeared to start out as large polymorphs but changed to small polymorphs before their skeletons were completely formed (Figure 4I). There are some indications near the onset of the transition to small zooids of an overall decline in large zooid size, and there is a tendency for large zooids near the transition to develop umbonal structures resembling those normally associated with small zooids (Figure 4F). Actively feeding zooids with protruded lophophores were observed only in the large zooids at the centres of colonies. These autozooids possessed 15 tentacles in all counts. Protruded lophophores or other indications of a fully developed polypide were never observed in the small zooids. No feeding activity was observed in any of the ancestrulae. Preserved material (Figure 1) revealed the presence in the small peripheral zooids of yellowish spherical structures (Figure 1B) that, by comparison with other cheilostomes, can be inferred to be eggs or embryos. Egg/ embryo size decreased towards the growing edge, the largest examples lling almost all of the space available within the zooid. The presence of eggs or embryos in these zooids enables them to be categorized as gonozooids. Exposure to light after a period in the dark failed to stimulate larval release from the small zooids, perhaps because the eggs had not been fertilized or the embryos were insu ciently mature. One year-old colonization panels deployed in Svalbard supported colonies of various sizes, from small colonies comprising only a few autozooids, to large colonies with peripheral zones of gonozooids surrounding autozooids. Colonies from northern Norway were found to be larger than those collected from Svalbard at about the same time (Figure 5). The colonies from Norway also had more extensive central zones of autozooids. In both cases the di erence was statistically signi cant (ANOVA of F 1 ¼4.67, P¼0.032, and F 1 ¼7.16, P¼0.008 respectively). Among 117 measured colonies from northern Norway, 114 (97%) contained gonozooids, while at Svalbard among 88 measured colonies only 39 (44%) had gonozooids. When space was severely limited (e.g. on gastropod shells occupied by hermit crabs), the switchover from budding autozooids to gonozooids could commence as early as the fourth budded generation. Colonies with autozooids budded beyond (distally of ) the band of gonozooids were never encountered, either in the eld samples from Svalbard and northern Norway, or among museum material of H. scutulata. SYSTEMATICS Order CHEILOSTOMATA Busk, 1852 Suborder ASCOPHORA Levinsen, 1909 Superfamily SCHIZOPORELLOIDEA Jullien, 1903 Family CRYPTOSULIDAE Vigneaux, 1949 Genus Harmeria Norman, 1903 Harmeria scutulata (Busk, 1855) (Figures 1 & 4) Lepralia scutulata Busk, 1855, p. 255, pl. 2, gures 1^2. Discopora scutulata (Busk): Smitt, 1868, p. 165^166, pl. 27, gures 160^161. Cribrilina scutulata (Busk): Nordgaard, 1896, p. 20. Harmeria scutulata (Busk): Norman, 1903 p. 107; Levinsen, 1916, p. 447, pl. 19, gures 15^17; Osburn, 1952, p. 282; Kluge, 1962, p. 516^517, gure 360; Kluge, 1975, p. 627^628, gure 360; Gostilovskaya, 1978, p. 212, gure 134; Dick & Ross, 1986, p. 89; Dick & Ross, 1988, p. 55, pl. 9, gure D; Viskova, 1993, pl. 1, gure 8; Kuklinski & Barnes, 2005a, gure 3. Material See above. Description Colony encrusting, multiserial, unilaminar, subcircular, small, up to 5.1mm in diameter, an inner zone of large autozooids surrounded by an outer ring of up to six generations of small gonozooids. Zooids arranged in wellde ned, bifurcating rows. Ancestrula oval, about 0.31mm long by 0.23 mm wide, frontal surface entirely membranous, gymnocyst, cryptocyst and spines all lacking, budding two distolateral daughter zooids, later buds from post-ancestrular zooids encircling ancestrula. Autozooids in early astogeny resembling later autozooids but smaller,

6 1310 P. Kuklinski and P.D. Taylor Unique life history strategy Figure 4. Scanning electron micrographs of skeletal morphology in Harmeria scutulata (Busk, 1855). (A) Mature colony with large polymorphs (autozooids) in the centre and small polymorphs (gonozooids) at the periphery; Julianehaab Harbour, Greenland, NHM ; (B) early stage of astogeny showing ancestrula (bottom), two periancestrular buds and four further zooids; Isfjorden, Spitsbergen, Kuklinski Collection; (C) underside of colony edge with basal windows present in autozooids but lacking in gonozooids at top of image; Julianehaab Harbour, Greenland, NHM ; (D) young colony with only autozooids present; Isfjorden, Spitsbergen, Kuklinski Collection; (E) monster zooid resulting from incomplete bud fusion; Isfjorden, Spitsbergen, Kuklinski Collection; (F) umbonal structures of autozooids and gonozooids in transitional zone; Julianehaab Harbour, Greenland, NHM ; (G^I), Julianehaab Harbour, Greenland, NHM (G) Ori ce of an autozooid with pair of small pseudopores arrowed; (H) transition between zones of autozooids and small gonozooids; and (I) example of zooid (centre) in transition zone showing proximal morphology of an autozooid with a gymnocyst but the distal morphology of a gonozooid. Scale bars: A, 1 mm; B,F,H,I, 100 mm; C^E, 200 mm; G, 20 mm

7 Unique life history strategy P. Kuklinski and P.D. Taylor 1311 Figure 5. Mean and standard deviation of total colony diameter (black) and central autozooid zone (grey) for populations of Harmeria scutulata encrusting a rock from TromsÖ, northern Norway (708N) and a settlement panel from Isfjorden, Spitsbergen (778N). having more extensive proximal gymnocysts, correspondingly smaller cryptocysts with fewer pseudopores, no di erentiated distolateral pseudopores and are never umbonate. Multiporous septula providing communication between zooids. Autozooids longer than wide, averaging 0.47 mm long by 0.23 mm wide, rhomboidal to ovoidal, separated from lateral neighbours by deep grooves; without spines. Frontal shield strongly convex, thinly calci ed, comprising marginal gymnocyst raised above central cryptocyst. Gymnocyst smooth, sometimes displaying planar spherulitic surface fabric, broad proximally, extending distally as narrow rim bordering lateral edges of zooid and encircling ori ce, continuous with proximal gymnocyst of next zooid in row. Cryptocyst non-granular, pseudopores numerous (25^43), distributed semi-regularly over surface, density and size decreasing towards ori ce, an apron of nonpseudoporous cryptocyst developed proximally of ori ce, a characteristic pair of small pseudopores present at distolateral corners of cryptocyst opposite proximal edge of ori ce. Frontal shield variably raised towards ori ce, sometimes forming subrounded umbo projecting over ori ce. Primary ori ce equidimensional or longer than wide, bell-shaped, with straight, or slightly concave proximal margin; no condyles. Basal wall incompletely calci ed, containing an irregular window. Polypide with 15 tentacles. Gonozooids less than half the length of autozooids, squat, approximately equidimensional, rhomboidal, distal and proximal edges straight, averaging 0.20 mm long by 0.16 mm wide, separated from lateral neighbours by deep grooves; without spines. Frontal shield convex, with gymnocyst forming narrow border, widest proximally, enclosing large area of cryptocyst. Cryptocyst pseudoporous except around ori ce, pseudopores numbering about 15, smaller than those of autozooids. Ori ce oval, wider than long, less than half the size of an autozooidal ori ce, closed by an operculum, variably umbonate, umbonal margins sometimes infolded to form a tube open along its upper edge. Basal wall usually fully calci ed, without a window. Row bifurcation infrequent within gonozooid zone, average gonozooid width increasing with successive generations. Avicularia unknown. Remarks Harmeria is a monospeci c genus introduced by Norman (1903) for Lepralia scutulata Busk, Busk s material of this species in the NHM collections consists of a single specimen (NHM ) from the only locality (West Greenland) mentioned in the original description. This specimen is therefore regarded as the holotype of the species. Recent taxonomic studies (e.g. Dick & Ross, 1988) have classi ed Harmeria in the family Cryptosulidae, H. scutulata being the only Arctic species belonging to this family. The nominotypical species of Cryptosulidae is Cryptosula pallasiana (Moll), a common intertidal and shallow subtidal fouling species widely distributed in temperate latitudes (e.g. Hayward & Ryland, 1999). Compared with H. scutulata, C. pallasiana has a similar bell-shaped ori ce, though with condyles, and a frontal shield that is porous

8 1312 P. Kuklinski and P.D. Taylor Unique life history strategy but entirely cryptocystal, much thicker and more rugose than that of H. scutulata. Suboral avicularia are occasionally present in C. pallasiana, and the ancestrula resembles later zooids, unlike the anascan-grade ancestrula of H. scutulata. Tentacle number is slightly di erent: 16^17 in C. pallasiana, compared with 15 in H. scutulata. So-called monster zooids, resulting from incomplete bud fusion, are common in C. pallasiana (Jebram, 1977) and have also been observed in H. scutulata (Figure 4E). The contrast is very striking between the life histories of H. scutulata and the closely-related C. pallasiana. Colonies of Cryptosula are perennials, often attaining a large size (450 mm), becoming irregular in shape, multilayered and showing common evidence of reparative growth ( Jebram, 1977). By comparison, Harmeria colonies are annuals that are always small in size (56 mm), regular in shape and lack reparative structures. Larval brooding in Cryptosula occurs within feeding zooids (autozooids) which are not polymorphs (Calvet, 1900), whereas brooding occurs within polymorphic, non-feeding gonozooids in Harmeria. Distribution Harmeria scutulata is locally common in the intertidal and shallow subtidal of the Arctic. In Svalbard and northern Norway it occurs mostly on rocks but rarely on other substrates such as algae or shells (Kuklinski, 2005; Kuklinski & Barnes, 2005b; P.K., personal observations). Literature records and museum collection studies indicate that in other regions the species may be found more commonly on algae than in Svalbard. Global distribution is circumpolar, the most southerly record being the Kodiak Islands, Alaska (578N; Dick & Ross, 1988), and the most northerly Kongsfjorden, Spitsbergen (798N; Kuklinski & Barnes, 2005a). DISCUSSION Quantitative analysis of zooid length, width and surface area, as well as qualitative data obtained from scanning electron microscopy of skeletal morphology, proves the existence of two distinct types of zooidsöpolymorphsö in the endemic Arctic bryozoan Harmeria scutulata. Large zooids budded during early growth of the subcircular colonies are surrounded by a peripheral zone of signi cantly smaller zooids that also di er qualitatively. Thus, the pattern of astogenetic variation in zooid size contrasts with that found in other bryozoans where the smallest zooids are formed rst and zooid size increases towards a mature average value through astogeny (Boardman & Cheetham, 1969, 1973; Taylor & Furness, 1978; Taylor, 1988a). The observation of expanded tentacle crowns in the large zooids but not in the small zooids, and the discovery of probable eggs or embryos lling the small zooids in preserved material, suggests that the morphological di erences in Harmeria are because the large zooids are feeding zooids (autozooids) whereas the small zooids are brooding zooids (gonozooids) that do not feed. The origin of brooding in cheilostome bryozoans represents a major evolutionary innovation that undoubtedly contributed to their success in benthic marine communities (Taylor, 1988b). In most cheilostomes, embryos are brooded in ovicellsöglobular external structures situated at the distal end of the maternal zooidöprior to being released into the water column as coronate larvae that are non-planktotrophic. Notably, of the 258 cheilostome species described in Kluge s (1962) monograph of Arctic bryozoans, 227 species (88%) have ovicells for brooding. Specialized brooding zooidsögonozooidsöoccur in relatively few cheilostomes (cf. cyclostomes where they are ubiquitous). Cheilostome gonozooids may be enlarged and or dwarfed, and can retain or have lost the ability to feed. In the well-known Celleporella hyalina (L.), for example, gonozooids are dwarfed, do not feed, originate as frontal buds above the layer of autozooids, and have ovicells for brooding (Hughes, 1987). The non-ovicellular, internal brooding of embryos in dwarfed, non-feeding gonozooids at the outer margins of Harmeria scutulata colonies is apparently unique, not only for Arctic bryozoans but for cheilostomes worldwide. The related genus Cryptosula lacks ovicells and broods its embryos internally within autozooids (Calvet, 1900), but these are neither morphologically di erentiated nor con ned to the periphery of the colony. Internal brooding is regarded as an advanced trait in cheilostomes, derived from an ancestral condition in which ovicells are employed for brooding (Ostrovsky et al., 2006). This trend has apparently been taken several stages further in Harmeria through dwar ng and loss of feeding ability in the brooding zooids, as well as their formation only during late growth stages after all of the feeding zooids in the colony have been budded. One-year settlement panel investigations in Svalbard suggest that H. scutulata is among the fastest growing Arctic bryozoans. Colonies encrusting natural substrates further south in northern Norway were found to be larger and had more autozooids than those from Svalbard (Figure 5), possibly re ecting greater growth rates or early time of recruitment consequent upon the higher temperatures. Scanning electron microscopy investigations show that the gonozooids containing embryos are more heavily calci ed than the larger autozooids, lacking the basal windows seen in autozooids (Figure 4C). Older colonies on boulders very often have mechanically damaged autozooids or consist only of gonozooids (Dick & Ross, 1988, personal observations). The ability of some gonozooids to survive through the harsh winter months suggests that the most likely mechanism for maintaining populations from one year to the next in Harmeria is by overwintering of embryos in gonozooids. These would then be released as larvae to found new colonies when conditions ameliorated the following summer. Our failure to stimulate larval release in the laboratory during July could be explained by a long gestation period before larvae become competent. An alternative possibility is that free larvae of Harmeria are able to overwinter but this is considered to be very unlikely in view of the fact that this genus belongs to a group of cheilostomes with non-planktotrophic larvae with lifespans seldom longer than a few hours. Skeletal investment in the defence of the embryos contrasts with the apparently small investment made by Harmeria in defending its colonies from overgrowthöas Barnes & Kuklinski (2003) have shown, H. scutulata is an inferior competitor, losing over 70% of its interactions with other organisms. Yet H. scutulata is very abundant and recruits onto hard and rm substrates in massive

9 Unique life history strategy P. Kuklinski and P.D. Taylor 1313 numbers each year. Large colonies of Harmeria scutulata (Figure 1A) may contain a greater number of gonozooids than autozooids, suggesting production of on average more than one larva per feeding zooid in each colony. These parameters typical of an opportunistic species make H. scutulata extremely successful in the seasonally disturbed habitats where it lives. A similarly successful and opportunistic life history pattern is seen in the cheilostome Drepanophora tuberculatum Osburn, the most common organism encrusting small coral rubble in shallow waters of Jamaica (Winston & Jackson, 1984). Its success has been attributed to fast growth and rapid maturity despite little investment in defence (McKinney & Jackson, 1989). Catastrophic mortality caused, for example, by frequent ice scour promotes life histories with increased fecundity and/or accelerated development and reproduction, rather than selecting for competitive ability in interactions with other species. Harmeria scutulata occurs in highly disturbed Arctic habitats which are impacted by strong wave action, ice scour and large annual uctuations in food supply. To succeed in such environments organisms need to have special adaptations. The present study of this numerically dominant (Barnes & Kuklinski, 2003; Kuklinski & Barnes, 2005)öand hence ecologically successfulö cheilostome bryozoan shows that it possesses some apparently unique life history adaptations. Even though it is an inferior competitior for substrate space (Barnes & Kuklinski, 2003, 2005; Kuklinski et al., 2005), both eld collections and colonization experiments con rm that H. scutulata is able to dominate on intertidal and shallow subtidal rocks, owing primarily to its ability to recruit massively, reach maturity during a short growing season and overwinter its embryos successfully in thickly calci ed gonozooids. Many aspects of the biology of Harmeria remain to be investigated. For example, the means of sustaining populations from one year to the next, inferred to be due to overwintering of embryos in gonozooids, needs to be rmly established. Nothing is yet known about the anatomy of embryonic brooding in Harmeria, or of fertilization. The developmental biology of polymorphism requires investigation not only in Harmeria but in bryozoans as a whole. How is the switchover from autozooids to gonozooids achieved in Harmeria and what triggers this transition? Movement of metabolites between zooids in cheilostome bryozoan colonies occurs via the funicular system (e.g. Best & Thorpe, 2002). Provisioning of embryos in nonfeeding gonozooids requires translocation of metabolites from the feeding zooids of the colony. There must be an e cient system of translocation in Harmeria because, unlike most cheilostomes, a high proportion of the gonozooids do not directly adjoin an autozooid but are separated from the nearest autozooid by up to ve generations of gonozooids. JÖrgen Berge (University Center, Svalbard) is thanked for help and providing laboratory space, Mary Spencer Jones (Department of Zoology, NHM) for assistance with literature and collections, and Alex Ayling (NHM volunteer) for measuring colony sizes. Financial support for this study was provided by the European Union Marie Curie programme BRYOARC. REFERENCES Busk, G., Zoophytology. Quarterly Journal of Microscopical Science, 3, 253^256. 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