ARTICLE in PRESS + MODEL SEARES-00562; No of Pages 11

ARTICLE IN PRESS + MODEL SEARES-00562; No of Pages 11

Journal of Sea Research xx (2007) xxx–xxx 1 www.elsevier.com/locate/seares

2 The cost of metamorphosis in flatfishes ⁎ 3 A.J. Geffen a, , H.W. van der Veer b, R.D.M. Nash c

4 a Department of Biology, University of Bergen, PO Box 7800, 5020 Bergen, Norway 5 b Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg Texel, The Netherlands 6 c Institute of Marine Research, PO Box 1870, Nordnes, 5817 Bergen, Norway 7 Received 14 July 2006; accepted 16 February 2007

8 Abstract

9 Flatfish development includes a unique physical metamorphosis with morphological andPROOF physiological changes associated with 10 eye migration, a 90° rotation in posture and asymmetrical pigmentation. Flatfish larvae also undergo settlement, a behavioural and 11 ecological change associated with a transition from a pelagic to a benthic existence. These processes are often assumed to be 12 critical in determining recruitment in flatfish, through their impact on feeding, growth and survival. The timing of metamorphosis 13 in relation to settlement varies between different flatfish species and this suggests that growth and development are not closely 14 coupled. Existing information on feeding, growth and survival during metamorphosis and settlement is reviewed. Growth during 15 metamorphosis is reduced in some but not all species. Despite the profound internal and external changes, there are no indications 16 that the process of metamorphosis results in an increased mortality or that it might affect recruitment in flatfishes. 17 © 2007 Elsevier B.V. All rights reserved. 18 19 Keywords: Metamorphosis; Settlement; Feeding; Growth; Survival; Flatfish

21 1. Introduction Pleuronectidae and Soleidae have more variation in 33 larval types. The unique characteristics of flatfish appear 34 22 Flatfishes (Pleuronectiformes) are widespread glob- during metamorphosis, at the end of the larval period. 35 23 ally and occur in a wide range of habitats: in fresh- The profound morphological changes have attracted 36 24 waters, estuarine habitats and all major oceans out to the considerable research interest, and many aspects of the 37 25 edge of the continental slopes (Munroe, 2005b). Flatfish developmental changes have been reviewed (Chambers 38 26 juveniles and adults are readily identified by their and Leggett, 1987, 1992; Fuiman, 1997; Gibson, 1997). 39 27 unique anatomy. However, as larvae they have a similar Information about distributions in time and space, 40 28 range in shapes, sizes and anatomical variability as the diet, and growth of flatfish larvae is abundant, reaching 41 29 rest of the teleosts (see e.g. Russell, 1976). In fact there back to the early 1900s. However, because these are 42 30 are few fundamental differences between the early life field studies, they offer only a low level of resolution in 43 31 stages of flatfish and other teleosts with pelagic larvae. space, time, and over individual variations. In addition, 44 32 UNCORRECTED 45 There are clear familial traits within flatfish, although the coverage of species is mostly restricted to commercially exploited species in the North Atlantic and North 46 ⁎ Corresponding author. Pacific, leaving the bulk of flatfishes with little data 47 E-mail address: [email protected] (A.J. Geffen). about their biology in the wild (Munroe, 2005a). In 48

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49 contrast, there is abundant information from laboratory organ system’. Though many authors likewise use a 101 50 studies about larval development, growth, physiology, very general definition of metamorphosis, more practi- 102 51 behaviour and responses to environmental conditions cal definitions restrict the process to the visible changes 103 52 (see Gibson, 2005a). Larval nutrition, digestive physi- in morphology that begin with eye migration and end 104 53 ology and morphological development have been stud- with the completion of squamation and full pigmenta- 105 54 ied in detail for aquaculture purposes (Pittman et al., tion. Other authors have defined metamorphosis only by 106 55 1990; Bisbal and Bengtson, 1995; Rønnestad et al., stages of eye migration with the completion of 107 56 2000; Morais et al., 2004). These studies provide metamorphosis coinciding with the completion of eye 108 57 information with a high level of resolution in time and migration (Hotta et al., 2001 cited in Wada et al., 2004). 109 58 over individuals. Laboratory studies also focus on a In this review we consider metamorphosis as both the 110 59 limited number of commercially important species, and process and the time period between the first morpho- 111 60 in many cases the experimental conditions preclude logical asymmetry to the completion of juvenile 112 61 insight into larvae in their natural environment. features. We use the term metamorphosis to define 113 62 Synthesis of the existing information about the early morphological and physiological development, and the 114 63 life history of flatfish for generalisation of the ecological term settlement to define behavioural and ecological 115 64 significance of metamorphosis is difficult. Fuiman changes associated with the transition of larvae from the 116 65 (1997) discussed the morphological characteristics, 3-dimentional planktonic environment to the 2-dimen- 117 66 development, behaviour and performance of flatfish tional demersal way of life. 118 67 larvae and suggested that the ontogenetic patterns held During metamorphosis and settlement flatfish larvae 119 68 important clues about the adaptations of flatfish to spend varying amounts of time in the water column and 120 69 PROOF 121 benthic life. Larval development patterns differed on the bottom (Fig. 1). Metamorphosing larvae that are 70 somewhat between flatfish and pelagic species, espe- pelagic (Fig. 1b) are ecologically part of the planktonic 122 71 cially in later stages approaching settlement. Flatfish 72 larval development is characterised by the transition to 73 benthic habits, but these larvae must pass successfully 74 through pelagic life in order to reach that point. The ED 75 evolutionary aspects and functional demands of size at 76 transformation were discussed by Osse and Van den 77 Boogaart (1997), who linked species-specific size 78 ranges to juvenile habitats and feeding. 79 Metamorphosis might be a key process in overall 80 population dynamics since it occurs in the early stages 81 of recruitment (Leggett and DeBlois, 1994; Van der Veer 82 et al., 2000). Here we consider the physiological and 83 anatomical changes associated with metamorphosis in 84 relation to the behavioural and ecological changes 85 involved in settlement. We ask to what extent these 86 two processes may be temporally or spatially un- 87 coupled, and examine their ecological consequences 88 through their impact on feeding, growth and mortality. 89 Numerous terms have been used for the developmental 90 stages and the process of development from flatfish larvae 91 to juveniles. Since many of the processes are different in 92 mechanism (being physiological, behavioural, or ana- 93 tomical in basis), it is critical to define the terms for each 94 application. UNCORRECT 95 The process of metamorphosis may begin with 96 physiological changes well before any outward sign of 97 morphological change (Schreiber, 2001). Sæle et al. Fig. 1. Flatfish (Pleuronectes platessa) during metamorphosis, 98 ‘ illustrating the definitions adopted in this review: (a) Larva at the (2004) defined metamorphosis as the post-embryonic beginning of metamorphosis, (b) pelagic larva, during metamorphosis 99 morphological change from the larval to the sexually and start of settlement, (c) demersal larva at end of metamorphosis and 100 immature juvenile’, encompassing ‘changes in every settlement. Scale bar=1 mm.

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123 community as is illustrated by the fact that they consume a small volume aids survival due to its lower main- 173 124 primarily pelagic prey. Metamorphosing larvae that are tenance costs. Fluctuating food densities at high lati- 174 125 demersal (or benthic, Fig. 1c) are associated with the tudes select for larger larvae, because a large volume 175 126 epi-benthic or benthic community and their diet is com- gives better survival over patchy prey availability 176 127 posed of benthic or epi-benthic prey items. (Gross et al., 1988). 177 Towards the end of the pelagic stage, larvae which 178 128 2. Pre-metamorphosis stage are smaller at the start of metamorphosis will have a 179 lower food demand than larger larvae, but contain 180 129 Size and timing of metamorphosis may logically be relatively lower energy reserves (Kooijman, 2000). The 181 130 considered to be adaptations to juvenile habitats. How- general latitudinal gradient in size at metamorphosis fits 182 131 ever, there may be some influence of larval character- the pattern of more constant food densities at lower 183 132 istics and pelagic conditions. latitudes and more fluctuating food densities at high 184 133 Body size scaling relationships and a general theory latitudes. However, because temperature in tropical and 185 134 of energy allocation (Kooijman, 2000) accurately subtropical waters is higher, small larvae in these waters 186 135 predict that maximum adult body size increases with will have a much higher energy turn-over rate. 187 136 latitude both within and among flatfish species (Van der During metamorphosis there are changes in swim- 188 137 Veer et al., 2003). This latitudinal trend also influences ming posture that may serve to maintain binocular 189 138 other correlates of maximum body size, such as egg vision while late stage larvae are still pelagic (Schreiber, 190 139 sizes, incubation times, larval size at hatching and size at 2006). Demersal larvae continue to consume pelagic 191 140 metamorphosis (Miller et al., 1991; Van der Veer et al., plankton prey until settlement is complete (Jenkins, 192 141 2003). 1987; Fernandez-DiazPROOF et al., 2001). In this way the early 193 142 Egg size in flatfishes ranges between 0.50 and larval feeding patterns may continue to influence 194 143 4.25 mm, and does not seem to differ from that in other feeding during metamorphosis. However, most teleost 195 144 teleosts (Rijnsdorp and Witthames, 2005). Between larvae exhibit ontogenic shifts in prey, and learn new 196 145 species, larger eggs result in a larger larva at hatching feeding patterns during metamorphosis. 197 146 and, because it takes more time to ‘build’ a larva that is 147 bigger at hatching, larger eggs have a longer develop- 3. Metamorphosis 198 148 ment time. This relationship is confirmed by analysis of 149 hatching time in marine fish eggs in relationship to It is clear that flatfish species are extremely variable in 199 150 temperature and size (Pauly and Pullin, 1988). They the patterns of metamorphosis that they exhibit. Size at 200 151 concluded that larger eggs develop more slowly than metamorphosis, duration of metamorphosis and syn- 201 152 small eggs, all other factors being equal. Within a chrony of metamorphosis with settlement vary between 202 153 species, there is a complex relationship between egg and sometimes within species. The order of ontogenic 203 154 size, temperature, and development rate, as demonstrat- events may also differ. For example, jaw elements ossifiy 204 155 ed for plaice (Fox et al., 2003). There is some variability early in metamorphosis in halibut (Sæle et al., 2004), but 205 156 in the relationship between individual egg size and at the end of metamorphosis in winter flounder (Hunt 206 157 individual larval size at hatching, although on average, von Herbing, 2001). Osse and Van den Boogaart (1997) 207 158 larger eggs produce larger larvae (Chambers and constructed two general patterns of metamorphosis 208 159 Leggett, 1996). which they termed ‘plaice-like’ and ‘sole-like’. Plaice- 209 160 Prey abundance for the developing flatfish larvae is like metamorphosis occurred at larger sizes whereas the 210 161 positively correlated with latitude (Petersen and Curtis, sole-like pattern occurred at smaller sizes and was of 211 162 1980; Gross et al., 1988). At high latitudes, seasonal shorter duration. These generalisations echo the earlier 212 163 temperature oscillations divide the year into times of flatfish groupings based on adult feeding patterns (De 213 164 very high and very low production. The consequence is Groot, 1969; Gibson, 2005b): visual feeding piscivores 214 165 that during periods of high food production the energy (Bothids), mainly visual feeders (flounders) and mainly 215 166 available per individualUNCORRECTED is high. In the tropics, temper- olfactory feeders (soles). Metamorphosis must reflect 216 167 ature oscillations are much reduced, as are seasonal adaptations to juvenile and adult habitats but these 217 168 variations in production. Food availability per individ- generalisations are too broad to explain the extensive 218 169 ual is therefore more constant year round and culling species-specific variations. If metamorphosis is a critical 219 170 effects are likely to be gradual rather than episodic as in period in flatfish recruitment, then these diverse patterns 220 171 temperate or polar regions. The more constant food may reveal the ecological consequences in terms of 221 172 densities at lower latitudes select for small larvae, since feeding, growth and survival (Yamashita et al., 2001). 222

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223 3.1. Impact on feeding in most species the stomach and gut development is 274 not complete until after metamorphosis. Turbot larvae 275 224 Metamorphosis is assumed to be an energy-demand- have same digestive efficiency throughout development 276 225 ing process (Brewster, 1987; Gwak et al., 2003), and (6 – 49 mm) when feeding on natural zooplankton, but 277 226 may interfere with growth in size if the developmental absorption of lipids is incomplete (Conway et al., 1993). 278 227 changes cause difficulties in feeding (Wyatt, 1972; Brewster (1987) suggested that flatfish larvae increase 279 228 Keefe and Able, 1993). The evidence from field and their storage of lipids obtained from planktonic prey 280 229 laboratory studies has not produced any systematic species and that these nutrients are utilised for 281 230 trends, and it is difficult to generalize about feeding metamorphosis. 282 231 during metamorphosis. It is usually assumed that flat- 232 fish suffer during metamorphosis due to changes in 3.2. Impact on growth 283 233 behaviour or to the inability to process visual informa- 234 tion and thus feed effectively (Neave, 1985). In the case Many studies of flatfish metamorphosis have as- 284 235 of turbot, visual acuity reaches its maximum after meta- sumed that the developmental changes resulting in 285 236 morphosis, whereas in plaice the eye is fully developed asymmetry take place at the cost of somatic growth, 286 237 before metamorphosis (Neave, 1984). especially growth in length (Osse and Van den 287 238 Metamorphosing summer flounder had the lowest Boogaart, 1997). There are species-specific differences 288 239 indication of food consumption in field studies (Grover, in feeding ability, and digestion and assimilation are not 289 240 1998), but this is not the case for all species, for example equally efficient in all groups. These differences could 290 241 sole which continue to feed throughout metamorphosis be reflected in changes in growth rate during metamor- 291 242 PROOF 292 and settlement (Lagardere et al., 1999). Early field phosis. Larvae of most teleosts go through develop- 243 studies indicated that Solea senegalensis did not feed mental changes and metamorphosis, and declines in 293 244 during metamorphosis, though more recently it has been growth rate are a general feature of this transition period. 294 245 shown that feeding continues, but not as effectively Both laboratory and field studies have observed changes 295 246 (Yufera et al., 1999) and prey ingestion and daily ration in growth during metamorphosis (Table 1), but only a 296 247 (food ingested by fish weight) decline at early meta- fewED have specifically considered the impact on nutri- 297 248 morphosis (Cañavate et al., 2006). S. solea continue tional condition or the energetic cost of metamorphosis. 298 249 feeding during metamorphosis (Amara et al., 1993) The actual energy budgets for metamorphosis are not 299 250 and begin to feed on epi-benthic prey while still con- known but it is likely that the process of metamorphosis 300 251 suming planktonic prey (Lagardere et al., 1999). In S. has an added energy cost that is higher in flatfish than in 301 252 senegalensis, the stomach and gut are not fully other groups. In plaice, for example, the metabolic costs 302 253 functional until after metamorphosis, and this is the are in the order of 20 J cm− 3 body wet mass d− 1 at 10 °C 303 254 case for many, but not all flatfish. Japanese flounder, (Van der Veer et al., 2001). For a plaice larva beginning 304 255 Paralichthys olevaceus, cease feeding at metamorphosis metamorphosis at 10 mm with a body mass of about 305 256 and settlement, and can remain on the bottom for up to 0.01 – 0.015 g wet body mass (Hovenkamp, 1991; Van 306 257 two days without feeding (Tanaka et al., 1989, 1996). der Veer et al., 2001), this means an energy demand in 307 258 Lack of feeding was also noted in marbled sole Pseu- the order of 0.2 – 0.3Jd− 1. This demand could be 308 259 dopleuronectes yokohamae (Fukuhara, 1988), English met by consumption of 30 – 60 harpacticoid co- 309 260 sole (Rosenberg and Laroche, 1982) and plaice (Lock- pepods (3811 J g− 1 wet wt, Boldt and Haldorson, 2002; 310 261 wood, 1984; Hamerlynck et al., 1989). 0.51 – 10 μg individual dry wt, Goodman, 1980). The 311 262 Osse and Van den Boogaart (1997) suggested that diet of newly settled plaice (15 mm) is comprised of 312 263 flatfish larvae should be inactive during metamorphosis harpacticoid copepods and polychaetes (Amara et al., 313 264 to allow recalibration of binocular vision after eye 2001), but without precise estimates of the energetic 314 265 migration. However, neuronal and behavioural changes demand during the period of metamorphosis (10 – 315 266 can occur very early in metamorphosis (Schreiber, 2001; 15 mm), it is difficult to evaluate whether consumption 316 267 Solbakken andUNCORRECT Pittman, 2004) so that the transition is rates meet the needs and sustain growth. 317 268 gradual, rather than an abrupt shift. In many flatfish Brewster (1987) refers to observations by Evseenko 318 269 species the larvae continue to feed on planktonic prey (1978), who suggested that flatfish larvae accumulate a 319 270 throughout metamorphosis (Jenkins, 1987; Fernandez- large food reserve in the liver which they utilised dur- 320 271 Diaz et al., 2001), which also suggests that feeding ing metamorphosis, when he assumed that they had 321 272 efficiency may be maintained in some species. Diges- reduced feeding abilities. Brewster (1987) then con- 322 273 tion and assimilation may be less efficient because cluded that significant energetic costs were associated 323

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A.J. Geffen et al. / Journal of Sea Research xx (2007) xxx–xxx 5 t1:1 Table 1 t1:2 Examples of changes in feeding and growth associated with metamorphosis t1:3 Species Source Response Reference t1:4 Scophthalmus aquosus L, F Growth rate declines prior to settlement, Neuman et al. (2001) based on otolith analysis t1:5 Pleuronectes platessa F Growth rate reduced in newly settled fish Amara and Paul (2003) t1:6 P. platessa F No feeding during metamorphosis Hamerlynck et al. (1989) t1:7 P. platessa L Growth ceases during metamorphosis, Christensen and Korsgaard (1999) confirmed with protein metabolism, RNA/DNA t1:8 Pseudopleuronectes americanus L Feeding in the water column during Jearld et al. (1993) metamorphosis, activity and growth rates decline t1:9 P. americanus L Growth cessation, latency period defined Bertram et al. (1997) t1:10 Pseudopleuronectes yokohamae L Growth ceases during first half of Fukuhara (1988) metamorphosis, then resumes at end of metamorphosis t1:11 P. yokohamae F Growth ceases and growth rate becomes Joh et al. (2005) negative before and during metamorphosis t1:12 Pseudopleuronectes herzensteini L No cessation of growth or feeding Aritaki and Seikai (2004) t1:13 Verasper variegates L Growth and feeding continues through late Wada et al. (2004) metamorphosis t1:14 Glyptocephalus cynoglossus L Growth cessation during metamorphosis Bidwell and Howell (2001) t1:15 Parophrys vetulus F Reduced growth during metamorphosis PROOFRosenberg and Laroche (1982) t1:16 Microstomus pacificus L, F Growth rate declines prior to settlement, Butler et al. (1996) based on otolith analysis t1:17 M. pacificus F Growth cessation during metamorphosis, Markle et al. (1992) based on size-at-stage t1:18 Platichthys flesus M Growth and feeding continues through Engell-Sørensen et al. (2004) metamorphosis t1:19 Platichthys stellatus L Growth rate reduced at metamorphosis Campana (1984) t1:20 Platichthys olivaceus L Growth rate reduction through Gwak et al. (2003) metamorphosis, confirmed with RNA/DNA t1:21 Paralichthys dentatus L Feeding ceases in early metamorphosis Keefe and Able (1993) stages, (stage G), recommences at end of metamorphosis (stages H, H+) t1:22 Paralichthys olivaceus L Feeding ceases during metamorphosis Tanaka et al. (1996) and settlement t1:23 Solea senegalensis L Increase in energy content prior to Yufera et al. (1999) metamorphosis, followed by decrease after t1:24 S. senegalensis L Growth rate decreases, but feeding Fernandez-Diaz et al. (2001) continues, confirmed with biochemical measures t1:25 Solea solea F Feeding continues throughout Lagardere et al. (1999) metamorphosis, behaviour cued to light cycle t1:26 L=laboratory, F=field, M=mesocosm.

324 with metamorphosis, and that development could be creased in this species prior to metamorphosis, fol- 334 325 delayed until the larvae had accumulated sufficient lowed by a decline in energy content (Yufera et al., 335 326 reserves. This accounted for the wide variation in size 1999). Gavlik and Specker (2004) inferred that 336 327 andageatmetamorphosis,andexplainedwhymeta-UNCORRECTEDincreased growth of metamorphosing summer flounder 337 328 morphosis was not size (length)-dependent. in lower salinity (20 psu) was due to a release of ener- 338 329 In S. senegalensis, growth rate (Cañavate et al., gy otherwise required for osmoregulation in higher 339 330 2006) and the C:N ratio (Fernandez-Diaz et al., 2001) salinities. 340 331 decreased during metamorphosis. The observed de- Japanese flounder Paralichthys olivaceus, show de- 341 332 crease in C:N ratio indicates utilisation of carbohydrate creases in growth and nutritional condition (based on 342 333 and lipid resources. Furthermore, energy storage in- RNA/DNA and protein/DNA) at the beginning of 343

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344 and throughout metamorphosis (Gwak et al., 2003). response to favourable conditions such as substratum 396 345 RNA/DNA, increased rapidly just before metamorpho- (Gibson and Batty, 1990). However, Markle et al. 397 346 sis started, and then remained level or declined until (1992) discuss the possibility of delayed metamorphosis 398 347 after metamorphosis was complete. Growth during in Pacific Dover sole. Klokseth and Øiestad (1999) 399 348 metamorphosis seems to be accomplished by hypertro- transferred metamorphosing halibut to very shallow 400 349 phy (increase in cell size), which is an energy-saving (7 mm water depth) raceways and were able to induce 401 350 way of increasing size. Gwak et al. (2003) argued that settlement within two days. Larger individuals settled 402 351 the flounder larvae conserve energy for the end of sooner than smaller individuals in this case. 403 352 metamorphosis, until they can begin feeding properly. 353 During this period the larvae may be using energy stored 3.3. Impact on mortality 404 354 earlier in the liver (Tanaka et al., 1996). 355 Metamorphosis in Pacific Dover sole (Microstomus Direct measurements of larval mortality during 405 356 pacificus) may take up to one year to complete. Otolith- metamorphosis are rare, and mortality rates are often 406 357 based age estimates suggest that growth (in length and inferred from studies either just prior to, after or 407 358 weight) ceases, perhaps due to low food availability spanning settlement (Chambers et al., 2001). In the 408 359 (Markle et al., 1992; Butler et al., 1996). Kramer (1991) study by Pearcy (1962) the catch curve data did not 409 360 used size-at-age data to confirm that the growth rates of include metamorphosing larvae and Pearcy (1962) 410 361 California halibut were lowest immediately after acknowledged that his pelagic gear under-sampled 411 362 metamorphosis. These patterns lead to wide size settling larvae. Chambers et al. (2001) therefore did 412 363 distributions in post-settlement fish, presumably be- not consider his data as appropriate for examining the 413 364 PROOF 414 cause those individuals that complete metamorphosis possibility of a critical period concurrent with settle- 365 first resumed feeding and growth first, and often at a ment. Hovenkamp (1992) estimated that the survival 415 366 higher rate on the new food. Information about growth rates of slow-growing individuals during metamorpho- 416 367 during the period of metamorphosis is vital for models sis were much lower compared to the fast-growing 417 368 of settlement and mortality. The growth of plaice individuals. The pattern of cohort decline in plaice does 418 369 decreases around the time of metamorphosis and not suggestED increased mortality during metamorphosis 419 370 settlement in many experimental studies. (Fig. 2), although the resolution of the observation 420 371 In laboratory conditions it is possible to experimen- might have been too low to detect any effect. Starvation- 421 372 tally manipulate metamorphosis and regulate settlement induced mortality at least does not seem likely because 422 373 by the administration of thyroid hormones, allowing the plaice larvae at this stage can survive 25 days without 423 374 uncoupling of growth and development. Development food (Wyatt, 1972). Gwak et al. (2003), however, found 424 375 can be arrested, depending on the timing of administra- that mortality increased at the end of metamorphosis in 425 376 tion of thyroid hormone, either accelerating or arresting Japanese flounder. Nash and Geffen (2000) sampled 426 377 metamorphosis (e.g. Schreiber, 2001). In summer 378 flounder there was a continuation of growth even 379 though development was prolonged, indicating that 380 feeding and growth can continue through metamorpho- 381 sis (Gavlik et al., 2002). Solbakken and Pittman (2004) 382 traced the interaction of melatonin and thyroid hormone 383 through photoperiod manipulation and observed direct 384 links between development and growth. They also 385 suggested that, in Atlantic halibut, neural changes are 386 initiated first during metamorphosis, followed by 387 growth and skeletal changes, then the development of 388 haemoglobin and finally pigmentation. These experi- 389 ments clearlyUNCORRECT show that growth can continue when 390 metamorphosis is artificially arrested. Growth and 391 development may also be uncoupled in nature, and 392 respond semi-independently to environmental condi- Fig. 2. Changes in the abundance of a cohort from egg production to 393 the end of the first or second year of life. Figure as in Bailey et al. tions and external cues. (2005) but redrawn from the data presented in Van der Veer (1986), 394 There is no evidence that flatfish can control their Beverton and Iles (1992) and Nash (1998). Rectangle=metamorphosis 395 growth rate directly in order to manipulate settling in and settlement period.

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427 newly-settled plaice and estimated that their mortality growth rate and size at metamorphosis are not always 477 428 rates were higher than for juveniles after settlement had linked, especially where growth and development 478 429 been completed. Alhossaini et al. (1989) measured respond differently to temperature conditions (Benoit 479 430 similarly high mortality rates during settlement using and Pepin, 1999). For example, slower-growing larval 480 431 otolith primary increments to identify settling sub-co- plaice and Japanese flounder were longer at metamor- 481 432 horts of plaice. phosis (Seikai et al., 1986; Hovenkamp and Witte, 482 1991). Chambers and Leggett (1987) reviewed labora- 483 433 4. Relationship between metamorphosis and settlement tory data on flatfish growth and metamorphosis and 484 concluded that the variation in size at metamorphosis is 485 434 Although metamorphosis results in changes that greater than the variation in age at metamorphosis. 486 435 adapt individuals for future life in a benthic habitat, Similar observations were seen in wild caught sole 487 436 metamorphosis and settlement are two separate pro- larvae (Boulhic et al., 1992; Amara and Lagardere, 488 437 cesses. Settlement and metamorphosis coincide in the 1995) and arrowtooth flounder (Atheresthes stomias) 489 438 majority of flatfish species, but there are also well- (Bouwens et al., 1999). 490 439 known examples of species where these two separate At higher taxonomic levels the relationship between 491 440 processes are de-coupled, and temporally separated. At age and size at metamorphosis (or settlement) may have 492 441 one extreme is the marbled sole (Pseudopleuronectes some ecological significance. Osse and Van den 493 442 yokohamae) where settling begins together with the start Boogaart (1997) divided flatfish into three groups: 494 443 of eye migration and the development of most of the plaice-like species that feed on epi-benthic prey, sole- 495 444 traits associated with metamorphosis are completed after like species that settle at very small sizes and have 496 445 settlement (Fukuhara, 1988; Joh et al., 2005). At the restricted areas forPROOF settlement, and bothid-types that 497 446 other extremes are Dover sole (Microstomus pacificus) settle at large sizes over wide areas. These divisions may 498 447 and slime flounder (M. achne) where metamorphosed not be completely accurate, but they represent an 499 448 individuals may remain pelagic for many months attempt to link growth and metamorphosis and to the 500 449 (Markle et al., 1992; Aritaki and Tanaka, 2003). habitat immediately post-settlement. Benoit and Pepin 501 450 The de-coupling of metamorphosis and settlement (1999) and Benoit et al. (2000) used a more analytical 502 451 may be related to plasticity in larval growth rate, size, approach to examine the relationship between growth 503 452 and metamorphosis. Overall, it is apparent that in some rate, age at metamorphosis and size at metamorphosis. 504 453 species metamorphosis is a size-related phenomenon, The complex variations in age and size at metamorpho- 505 454 whereas in other species it is dependent on larval growth sis, especially in relation to temperature and larval 506 455 rate rather than size. There have been a large number of growth rate, have been analysed using correlation 507 456 laboratory and field studies investigating the inter- analysis, multivariate techniques and event analysis 508 457 relationships between these traits. In some species the (Chambers and Leggett, 1989; Benoit and Pepin, 1999). 509 458 size threshold for metamorphosis or settling is quite It may also be revealing to express some of the 510 459 wide (Benoit and Pepin, 1999; Gavlik et al., 2002); relationships through reaction norms. 511 460 however, in other species there is a narrow size 461 metamorphosis threshold resulting in a fairly synchro- 5. Discussion 512 462 nised settling and uniform post-settlement size distribu- 463 tion (Fernandez-Diaz et al., 2001). Locally fluctuating Studies of flatfish metamorphosis are complicated by 513 464 environmental conditions will also affect the larval the fact that numerous staging systems have been 514 465 growth rate of a species and this can affect both the published to categorise the development of flatfish 515 466 growth during and pattern of metamorphosis. For larvae. Some staging systems include quite detailed 516 467 example, in poor feeding conditions, Senegal sole substages to cover morphological changes associated 517 468 grew more slowly, and were smaller at metamorphosis, with metamorphosis (Fukuhara, 1988; Keefe and Able, 518 469 and metamorphosis was relatively unsynchronised 1993; Neuman and Able, 2002), and a few include 519 470 across the populationUNCORRECTED (Fernandez-Diaz et al., 2001). important developmental changes in behaviour (Pittman 520 471 Summer flounder larvae grew faster at higher tempera- et al., 1990). Most schemes emphasise the externally 521 472 tures and tended to be more synchronised in metamor- recognisable changes in eye migration andasymmetry, 522 473 phosis and settlement (Burke et al., 1999). whereas many other anatomical, physiological, and 523 474 Elevated temperatures lead to an increase in growth behavioural changes are unmarked (Ryland, 1966; 524 475 rate and, for many species, this leads to metamorphosis Minami, 1982; Hotta et al., 2001 cited in Wada et al., 525 476 at a larger size (Benoit and Pepin, 1999). However, 2004). 526

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527 The morphological and physiological changes that changes are dependent on growth rate in some species 579 528 occur during larval development in all species require but not others, where metamorphosis is less dependent 580 529 energy and at the same time confer advantages that on growth or size. Settlement can be triggered or 581 530 improve feeding performance and growth efficiency. delayed by environmental cues such as current speed, 582 531 However, it is often difficult to imagine how feeding, salinity, light, or prey density (Bailey et al., 2005). Such 583 532 assimilation and growth can continue during the re- an overlapping system of endogenous and exogenous 584 533 modelling that occurs in flatfish larvae. In fact, there controls and triggers is highly adaptive and supports the 585 534 seems to be a wide variation among flatfish species in the wide variety of species of flatfish, and the wide range of 586 535 timing, order, and synchronicity of the different organ environments that they settle in. 587 536 changes. This may explain the species differences in the Whether metamorphosis or settlement represents a 588 537 extent of growth and feeding during metamorphosis and critical period in terms of recruitment for the population 589 538 settlement. In some species the ability to store energy is not clear. Major recruitment variations are induced by 590 539 prior to metamorphosis may allow growth to continue. processes operating in the pelagic phase (Leggett and 591 540 Extended metamorphosis in other species may allow the DeBlois, 1994; Van der Veer et al., 2000), although 592 541 larvae to continue to feed efficiently as changes in processes operating after settlement can also signifi- 593 542 neuroanatomy and eye migration occur gradually. cantly affect abundance. For decades it has been 594 543 Flatfish larvae may be particularly vulnerable to assumed that the obvious physical transformations of 595 544 predation if vision and other senses are impaired during flatfish metamorphosis must entail elevated mortality, 596 545 metamorphosis, although one study showed that the and must influence recruitment. Shifts in mortality rates 597 546 escape response of winter flounder was not worse during metamorphosis ‘should’ occur for a variety of 598 547 PROOF 599 during metamorphosis (Williams and Brown, 1992). reasons such as errors in cell division, insufficient 548 Vulnerability to predation may also increase if growth energy reserves or increased predation. So why is it so 600 549 rate decreases at metamorphosis, since slower-growing difficult to find evidence of enhanced vulnerability 601 550 larvae may suffer higher predation mortality rates during metamorphosis? One reason is the inadequate 602 551 (Nielsen and Munk, 2004). and non-representative sampling of metamorphosing 603 552 Metamorphosis is often assumed to be a critical flatfish,ED which hinders the estimation of mortality rates 604 553 period, in the classic sense of being a process that associated with metamorphosis and settlement. We also 605 554 determines year-class strength. Metamorphosis and lack estimates of the energy demands of metamorphosis, 606 555 settlement may be energetically demanding because of making it difficult to assess prey availability and sub- 607 556 the extra requirements of physical remodelling together sequent impact on mortality. Metamorphosis in flatfish 608 557 with added hormone production and also because of the is probably equally as critical as it is in other groups. 609 558 problem of energy acquisition. Prey capture may be Behavioural and habitat changes at settlement may 610 559 problematic if the ability to search, locate, and capture prove to be more significant for recruitment than the 611 560 prey is decreased during metamorphosis. The transition process of metamorphosis. Considering the wide variety 612 561 from pelagic larva to benthic juvenile also means that of flatfish dispersal patterns and nursery habitats it is not 613 562 new prey models and responses must be learned. Prey surprising to find that the flexibility of adaptations 614 563 availability may be reduced at the end of the pelagic associated with settlement may be more important than 615 564 phases because of season or because of moving into the evolutionary patterns of metamorphosis in deter- 616 565 deeper water, but the abundance of new epibenthic prey mining survival and recruitment in flatfishes. 617 566 is not likely to be limiting. Larval size at metamorphosis 567 should be a major factor in determining the energy Acknowledgements 618 568 reserves and amount of time that an individual has in 569 order to make the transition to a settled juvenile. Species The authors gratefully acknowledge the constructive 619 570 that metamorphose at larger sizes may be more flexible comments made by three anonymous reviewers. 620 571 in response to environmental triggers for settlement and 572 less controlledUNCORRECT by purely physiological triggers. The References 621 573 ability to feed during metamorphosis may be a key to 574 retaining flexibility in settlement, but the ability to Alhossaini, M., Liu, Q., Pitcher, T.J., 1989. Otolith microstructure 622 575 indicating growth and mortality among plaice, Pleuronectes platessa 623 withstand food deprivation is also important. – 624 576 L., post-larval sub-cohorts. J. Fish Biol. 35 (Suppl. A), 81 90. The highly complex physiological changes, and the Amara, R., Lagardere, F., 1995. Size and age at onset of meta- 625 577 profound morphological changes that they induce, are morphosis in sole (Solea solea (L)) of the Gulf of Gascogne. ICES 626 578 generally sensitive to temperature. The developmental J. Mar. Sci. 52, 247–256. 627

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