The Cost of Metamorphosis in Flatfishes ⁎ A.J

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Journal of Sea Research 58 (2007) 35–45 www.elsevier.com/locate/seares

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

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

Abstract

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

Keywords: Metamorphosis; Settlement; Feeding; Growth; Survival; Flatfish

1. Introduction Pleuronectidae and Soleidae have more variation in larval types. The unique characteristics of flatfish appear Flatfishes (Pleuronectiformes) are widespread glob- during metamorphosis, at the end of the larval period. ally and occur in a wide range of habitats: in fresh- The profound morphological changes have attracted waters, estuarine habitats and all major oceans out to the considerable research interest, and many aspects of the edge of the continental slopes (Munroe, 2005b). Flatfish developmental changes have been reviewed (Chambers juveniles and adults are readily identified by their and Leggett, 1987, 1992; Fuiman, 1997; Gibson, 1997). unique anatomy. However, as larvae they have a similar Information about distributions in time and space, range in shapes, sizes and anatomical variability as the diet, and growth of flatfish larvae is abundant, reaching rest of the teleosts (see e.g. Russell, 1976). In fact there back to the early 1900s. However, because these are are few fundamental differences between the early life field studies, they offer only a low level of resolution in stages of flatfish and other teleosts with pelagic larvae. space, time, and over individual variations. In addition, 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 ⁎ Corresponding author. Pacific, leaving the bulk of flatfishes with little data E-mail address: [email protected] (A.J. Geffen). about their biology in the wild (Munroe, 2005a). In

1385-1101/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2007.02.004 36 A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45 contrast, there is abundant information from laboratory organ system’. Though many authors likewise use a studies about larval development, growth, physiology, very general definition of metamorphosis, more practi- behaviour and responses to environmental conditions cal definitions restrict the process to the visible changes (see Gibson, 2005a). Larval nutrition, digestive physi- in morphology that begin with eye migration and end ology and morphological development have been stud- with the completion of squamation and full pigmenta- ied in detail for aquaculture purposes (Pittman et al., tion. Other authors have defined metamorphosis only by 1990; Bisbal and Bengtson, 1995; Rønnestad et al., stages of eye migration with the completion of 2000; Morais et al., 2004). These studies provide metamorphosis coinciding with the completion of eye information with a high level of resolution in time and migration (Hotta et al., 2001 cited in Wada et al., 2004). over individuals. Laboratory studies also focus on a In this review we consider metamorphosis as both the limited number of commercially important species, and process and the time period between the first morpho- in many cases the experimental conditions preclude logical asymmetry to the completion of juvenile insight into larvae in their natural environment. features. We use the term metamorphosis to define Synthesis of the existing information about the early morphological and physiological development, and the life history of flatfish for generalisation of the ecological term settlement to define behavioural and ecological significance of metamorphosis is difficult. Fuiman changes associated with the transition of larvae from the (1997) discussed the morphological characteristics, 3-dimentional planktonic environment to the 2-dimen- development, behaviour and performance of flatfish tional demersal way of life. larvae and suggested that the ontogenetic patterns held During metamorphosis and settlement flatfish larvae important clues about the adaptations of flatfish to spend varying amounts of time in the water column and benthic life. Larval development patterns differed on the bottom (Fig. 1). Metamorphosing larvae that are somewhat between flatfish and pelagic species, espe- pelagic (Fig. 1b) are ecologically part of the planktonic cially in later stages approaching settlement. Flatfish larval development is characterised by the transition to benthic habits, but these larvae must pass successfully through pelagic life in order to reach that point. The evolutionary aspects and functional demands of size at transformation were discussed by Osse and Van den Boogaart (1997), who linked species-specific size ranges to juvenile habitats and feeding. Metamorphosis might be a key process in overall population dynamics since it occurs in the early stages of recruitment (Leggett and DeBlois, 1994; Van der Veer et al., 2000). Here we consider the physiological and anatomical changes associated with metamorphosis in relation to the behavioural and ecological changes involved in settlement. We ask to what extent these two processes may be temporally or spatially uncoupled, and examine their ecological consequences through their impact on feeding, growth and mortality. Numerous terms have been used for the developmental stages and the process of development from flatfish larvae to juveniles. Since many of the processes are different in mechanism (being physiological, behavioural, or anatomical in basis), it is critical to define the terms for each application. The process of metamorphosis may begin with physiological changes well before any outward sign of morphological change (Schreiber, 2001). Sæle et al. Fig. 1. Flatfish (Pleuronectes platessa) during metamorphosis, ‘ 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 morphological change from the larval to the sexually and start of settlement, (c) demersal larva at end of metamorphosis and immature juvenile’, encompassing ‘changes in every settlement. Scale bar=1 mm. A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45 37 community as is illustrated by the fact that they consume a small volume aids survival due to its lower main- primarily pelagic prey. Metamorphosing larvae that are tenance costs. Fluctuating food densities at high lati- demersal (or benthic, Fig. 1c) are associated with the tudes select for larger larvae, because a large volume epi-benthic or benthic community and their diet is com- gives better survival over patchy prey availability posed of benthic or epi-benthic prey items. (Gross et al., 1988). Towards the end of the pelagic stage, larvae which 2. Pre-metamorphosis stage are smaller at the start of metamorphosis will have a lower food demand than larger larvae, but contain Size and timing of metamorphosis may logically be relatively lower energy reserves (Kooijman, 2000). The considered to be adaptations to juvenile habitats. How- general latitudinal gradient in size at metamorphosis fits ever, there may be some influence of larval character- the pattern of more constant food densities at lower istics and pelagic conditions. latitudes and more fluctuating food densities at high Body size scaling relationships and a general theory latitudes. However, because temperature in tropical and of energy allocation (Kooijman, 2000) accurately subtropical waters is higher, small larvae in these waters predict that maximum adult body size increases with will have a much higher energy turn-over rate. latitude both within and among flatfish species (Van der During metamorphosis there are changes in swim- Veer et al., 2003). This latitudinal trend also influences ming posture that may serve to maintain binocular other correlates of maximum body size, such as egg vision while late stage larvae are still pelagic (Schreiber, sizes, incubation times, larval size at hatching and size at 2006). Demersal larvae continue to consume pelagic metamorphosis (Miller et al., 1991; Van der Veer et al., plankton prey until settlement is complete (Jenkins, 2003). 1987; Fernandez-Diaz et al., 2001). In this way the early Egg size in flatfishes ranges between 0.50 and larval feeding patterns may continue to influence 4.25 mm, and does not seem to differ from that in other feeding during metamorphosis. However, most teleost teleosts (Rijnsdorp and Witthames, 2005). Between larvae exhibit ontogenic shifts in prey, and learn new species, larger eggs result in a larger larva at hatching feeding patterns during metamorphosis. and, because it takes more time to ‘build’ a larva that is bigger at hatching, larger eggs have a longer develop- 3. Metamorphosis ment time. This relationship is confirmed by analysis of hatching time in marine fish eggs in relationship to It is clear that flatfish species are extremely variable in temperature and size (Pauly and Pullin, 1988). They the patterns of metamorphosis that they exhibit. Size at concluded that larger eggs develop more slowly than metamorphosis, duration of metamorphosis and syn- small eggs, all other factors being equal. Within a chrony of metamorphosis with settlement vary between species, there is a complex relationship between egg and sometimes within species. The order of ontogenic size, temperature, and development rate, as demonstrat- events may also differ. For example, jaw elements ossifiy ed for plaice (Fox et al., 2003). There is some variability early in metamorphosis in halibut (Sæle et al., 2004), but in the relationship between individual egg size and at the end of metamorphosis in winter flounder (Hunt individual larval size at hatching, although on average, von Herbing, 2001). Osse and Van den Boogaart (1997) larger eggs produce larger larvae (Chambers and constructed two general patterns of metamorphosis Leggett, 1996). which they termed ‘plaice-like’ and ‘sole-like’. Plaice- Prey abundance for the developing flatfish larvae is like metamorphosis occurred at larger sizes whereas the positively correlated with latitude (Petersen and Curtis, sole-like pattern occurred at smaller sizes and was of 1980; Gross et al., 1988). At high latitudes, seasonal shorter duration. These generalisations echo the earlier temperature oscillations divide the year into times of flatfish groupings based on adult feeding patterns (De very high and very low production. The consequence is Groot, 1969; Gibson, 2005b): visual feeding piscivores that during periods of high food production the energy (Bothids), mainly visual feeders (flounders) and mainly available per individual is high. In the tropics, temper- olfactory feeders (soles). Metamorphosis must reflect ature oscillations are much reduced, as are seasonal adaptations to juvenile and adult habitats but these variations in production. Food availability per individ- generalisations are too broad to explain the extensive ual is therefore more constant year round and culling species-specific variations. If metamorphosis is a critical effects are likely to be gradual rather than episodic as in period in flatfish recruitment, then these diverse patterns temperate or polar regions. The more constant food may reveal the ecological consequences in terms of densities at lower latitudes select for small larvae, since feeding, growth and survival (Yamashita et al., 2001). 38 A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45

3.1. Impact on feeding in most species the stomach and gut development is not complete until after metamorphosis. Turbot larvae Metamorphosis is assumed to be an energy-demand- have same digestive efficiency throughout development ing process (Brewster, 1987; Gwak et al., 2003), and (6 – 49 mm) when feeding on natural zooplankton, but may interfere with growth in size if the developmental absorption of lipids is incomplete (Conway et al., 1993). changes cause difficulties in feeding (Wyatt, 1972; Brewster (1987) suggested that flatfish larvae increase Keefe and Able, 1993). The evidence from field and their storage of lipids obtained from planktonic prey laboratory studies has not produced any systematic species and that these nutrients are utilised for trends, and it is difficult to generalize about feeding metamorphosis. during metamorphosis. It is usually assumed that flatfish suffer during metamorphosis due to changes in 3.2. Impact on growth behaviour or to the inability to process visual information and thus feed effectively (Neave, 1985). In the case Many studies of flatfish metamorphosis have as- of turbot, visual acuity reaches its maximum after meta- sumed that the developmental changes resulting in morphosis, whereas in plaice the eye is fully developed asymmetry take place at the cost of somatic growth, before metamorphosis (Neave, 1984). especially growth in length (Osse and Van den Metamorphosing summer flounder had the lowest Boogaart, 1997). There are species-specific differences indication of food consumption in field studies (Grover, in feeding ability, and digestion and assimilation are not 1998), but this is not the case for all species, for example equally efficient in all groups. These differences could sole which continue to feed throughout metamorphosis be reflected in changes in growth rate during metamor- and settlement (Lagardere et al., 1999). Early field phosis. Larvae of most teleosts go through develop- studies indicated that Solea senegalensis did not feed mental changes and metamorphosis, and declines in during metamorphosis, though more recently it has been growth rate are a general feature of this transition period. shown that feeding continues, but not as effectively Both laboratory and field studies have observed changes (Yufera et al., 1999) and prey ingestion and daily ration in growth during metamorphosis (Table 1), but only a (food ingested by fish weight) decline at early meta- few have specifically considered the impact on nutri- morphosis (Cañavate et al., 2006). S. solea continue tional condition or the energetic cost of metamorphosis. feeding during metamorphosis (Amara et al., 1993) The actual energy budgets for metamorphosis are not and begin to feed on epi-benthic prey while still con- known but it is likely that the process of metamorphosis suming planktonic prey (Lagardere et al., 1999). In S. has an added energy cost that is higher in flatfish than in senegalensis, the stomach and gut are not fully other groups. In plaice, for example, the metabolic costs 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 case for many, but not all flatfish. Japanese flounder, (Van der Veer et al., 2001). For a plaice larva beginning Paralichthys olevaceus, cease feeding at metamorphosis metamorphosis at 10 mm with a body mass of about and settlement, and can remain on the bottom for up to 0.01 – 0.015 g wet body mass (Hovenkamp, 1991; Van two days without feeding (Tanaka et al., 1989, 1996). der Veer et al., 2001), this means an energy demand in Lack of feeding was also noted in marbled sole Pseu- the order of 0.2 – 0.3Jd− 1. This demand could be dopleuronectes yokohamae (Fukuhara, 1988), English met by consumption of 30 – 60 harpacticoid co- sole (Rosenberg and Laroche, 1982) and plaice (Lock- pepods (3811 J g− 1 wet wt, Boldt and Haldorson, 2002; wood, 1984; Hamerlynck et al., 1989). 0.51 – 10 μg individual dry wt, Goodman, 1980). The Osse and Van den Boogaart (1997) suggested that diet of newly settled plaice (15 mm) is comprised of flatfish larvae should be inactive during metamorphosis harpacticoid copepods and polychaetes (Amara et al., to allow recalibration of binocular vision after eye 2001), but without precise estimates of the energetic migration. However, neuronal and behavioural changes demand during the period of metamorphosis (10 – can occur very early in metamorphosis (Schreiber, 2001; 15 mm), it is difficult to evaluate whether consumption Solbakken and Pittman, 2004) so that the transition is rates meet the needs and sustain growth. gradual, rather than an abrupt shift. In many flatfish Brewster (1987) refers to observations by Evseenko species the larvae continue to feed on planktonic prey (1978), who suggested that flatfish larvae accumulate a throughout metamorphosis (Jenkins, 1987; Fernandez- large food reserve in the liver which they utilised dur- Diaz et al., 2001), which also suggests that feeding ing metamorphosis, when he assumed that they had efficiency may be maintained in some species. Diges- reduced feeding abilities. Brewster (1987) then con- tion and assimilation may be less efficient because cluded that significant energetic costs were associated A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45 39

Table 1 Examples of changes in feeding and growth associated with metamorphosis Species Source Response Reference Scophthalmus aquosus L, F Growth rate declines prior to settlement, Neuman et al. (2001) based on otolith analysis Pleuronectes platessa F Growth rate reduced in newly settled fish Amara and Paul (2003) P. platessa F No feeding during metamorphosis Hamerlynck et al. (1989) P. platessa L Growth ceases during metamorphosis, Christensen and Korsgaard (1999) confirmed with protein metabolism, RNA/DNA Pseudopleuronectes americanus L Feeding in the water column during Jearld et al. (1993) metamorphosis, activity and growth rates decline P. americanus L Growth cessation, latency period defined Bertram et al. (1997) Pseudopleuronectes yokohamae L Growth ceases during first half of Fukuhara (1988) metamorphosis, then resumes at end of metamorphosis P. yokohamae F Growth ceases and growth rate becomes Joh et al. (2005) negative before and during metamorphosis Pseudopleuronectes herzensteini L No cessation of growth or feeding Aritaki and Seikai (2004) Verasper variegates L Growth and feeding continues through late Wada et al. (2004) metamorphosis Glyptocephalus cynoglossus L Growth cessation during metamorphosis Bidwell and Howell (2001) Parophrys vetulus F Reduced growth during metamorphosis Rosenberg and Laroche (1982) Microstomus pacificus L, F Growth rate declines prior to settlement, Butler et al. (1996) based on otolith analysis M. pacificus F Growth cessation during metamorphosis, Markle et al. (1992) based on size-at-stage Platichthys flesus M Growth and feeding continues through Engell-Sørensen et al. (2004) metamorphosis Platichthys stellatus L Growth rate reduced at metamorphosis Campana (1984) Platichthys olivaceus L Growth rate reduction through Gwak et al. (2003) metamorphosis, confirmed with RNA/DNA Paralichthys dentatus L Feeding ceases in early metamorphosis Keefe and Able (1993) stages, (stage G), recommences at end of metamorphosis (stages H, H+) Paralichthys olivaceus L Feeding ceases during metamorphosis Tanaka et al. (1996) and settlement Solea senegalensis L Increase in energy content prior to Yufera et al. (1999) metamorphosis, followed by decrease after S. senegalensis L Growth rate decreases, but feeding Fernandez-Diaz et al. (2001) continues, confirmed with biochemical measures Solea solea F Feeding continues throughout Lagardere et al. (1999) metamorphosis, behaviour cued to light cycle L=laboratory, F=field, M=mesocosm. with metamorphosis, and that development could be creased in this species prior to metamorphosis, fol- delayed until the larvae had accumulated sufficient lowed by a decline in energy content (Yufera et al., reserves. This accounted for the wide variation in size 1999). Gavlik and Specker (2004) inferred that andageatmetamorphosis,andexplainedwhymeta- increased growth of metamorphosing summer flounder morphosis was not size (length)-dependent. in lower salinity (20 psu) was due to a release of ener- In S. senegalensis, growth rate (Cañavate et al., gy otherwise required for osmoregulation in higher 2006) and the C:N ratio (Fernandez-Diaz et al., 2001) salinities. decreased during metamorphosis. The observed de- Japanese flounder, show decreases in growth and crease in C:N ratio indicates utilisation of carbohydrate nutritional condition (based on RNA/DNA and protein/ and lipid resources. Furthermore, energy storage in- DNA) at the beginning of and throughout metamorphosis 40 A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45

(Gwak et al., 2003). RNA/DNA, increased rapidly just (1992) discuss the possibility of delayed metamorphosis before metamorphosis started, and then remained level or in Pacific Dover sole. Klokseth and Øiestad (1999) declined until after metamorphosis was complete. Growth transferred metamorphosing halibut to very shallow during metamorphosis seems to be accomplished by (7 mm water depth) raceways and were able to induce hypertrophy (increase in cell size), which is an energy- settlement within two days. Larger individuals settled saving way of increasing size. Gwak et al. (2003) argued sooner than smaller individuals in this case. that the flounder larvae conserve energy for the end of metamorphosis, until they can begin feeding properly. 3.3. Impact on mortality During this period the larvae may be using energy stored earlier in the liver (Tanaka et al., 1996). Direct measurements of larval mortality during Metamorphosis in Pacific Dover sole (Microstomus metamorphosis are rare, and mortality rates are often pacificus) may take up to one year to complete. Otolith- inferred from studies either just prior to, after or based age estimates suggest that growth (in length and spanning settlement (Chambers et al., 2001). In the weight) ceases, perhaps due to low food availability study by Pearcy (1962) the catch curve data did not (Markle et al., 1992; Butler et al., 1996). Kramer (1991) include metamorphosing larvae and Pearcy (1962) used size-at-age data to confirm that the growth rates of acknowledged that his pelagic gear under-sampled California halibut were lowest immediately after settling larvae. Chambers et al. (2001) therefore did metamorphosis. These patterns lead to wide size not consider his data as appropriate for examining the distributions in post-settlement fish, presumably be- possibility of a critical period concurrent with settle- cause those individuals that complete metamorphosis ment. Hovenkamp (1992) estimated that the survival first resumed feeding and growth first, and often at a rates of slow-growing individuals during metamorpho- higher rate on the new food. Information about growth sis were much lower compared to the fast-growing during the period of metamorphosis is vital for models individuals. The pattern of cohort decline in plaice does of settlement and mortality. The growth of plaice not suggest increased mortality during metamorphosis decreases around the time of metamorphosis and (Fig. 2), although the resolution of the observation settlement in many experimental studies. might have been too low to detect any effect. Starvation- In laboratory conditions it is possible to experimen- induced mortality at least does not seem likely because tally manipulate metamorphosis and regulate settlement plaice larvae at this stage can survive 25 days without by the administration of thyroid hormones, allowing the food (Wyatt, 1972). Gwak et al. (2003), however, found uncoupling of growth and development. Development that mortality increased at the end of metamorphosis in can be altered, depending on the timing of administration Japanese flounder. Nash and Geffen (2000) sampled of thyroid hormone, either accelerating or arresting newly-settled plaice and estimated that their mortality metamorphosis (e.g. Schreiber, 2001). In summer rates were higher than for juveniles after settlement had flounder there was a continuation of growth even though development was prolonged, indicating that feeding and growth can continue through metamorphosis (Gavlik et al., 2002). Solbakken and Pittman (2004) traced the interaction of melatonin and thyroid hormone through photoperiod manipulation and observed direct links between development and growth. They also suggested that, in Atlantic halibut, neural changes are initiated first during metamorphosis, followed by growth and skeletal changes, then the development of haemoglobin and finally pigmentation. These experiments clearly show that growth can continue when metamorphosis is artificially arrested. Growth and development may also be uncoupled in nature, and respond semi-independently to environmental conditions and external cues. There is no evidence that flatfish can control their Fig. 2. Changes in the abundance of a cohort from egg production to the end of the first or second year of life. Figure as in Bailey et al. growth rate directly in order to manipulate settling in (2005) but redrawn from the data presented in Van der Veer (1986), response to favourable conditions such as substratum Beverton and Iles (1992) and Nash (1998). Rectangle=metamorphosis (Gibson and Batty, 1990). However, Markle et al. and settlement period. A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45 41 been completed. Alhossaini et al. (1989) measured respond differently to temperature conditions (Benoit similarly high mortality rates during settlement using and Pepin, 1999). For example, slower-growing larval otolith primary increments to identify settling sub-co- plaice and Japanese flounder were longer at metamor- horts of plaice. phosis (Seikai et al., 1986; Hovenkamp and Witte, 1991). Chambers and Leggett (1987) reviewed labora- 4. Relationship between metamorphosis and settlement tory data on flatfish growth and metamorphosis and concluded that the variation in size at metamorphosis is Although metamorphosis results in changes that greater than the variation in age at metamorphosis. adapt individuals for future life in a benthic habitat, Similar observations were seen in wild caught sole metamorphosis and settlement are two separate pro- larvae (Boulhic et al., 1992; Amara and Lagardere, cesses. Settlement and metamorphosis coincide in the 1995) and arrowtooth flounder (Atheresthes stomias) majority of flatfish species, but there are also well- (Bouwens et al., 1999). known examples of species where these two separate At higher taxonomic levels the relationship between processes are de-coupled, and temporally separated. At age and size at metamorphosis (or settlement) may have one extreme is the marbled sole (Pseudopleuronectes some ecological significance. Osse and Van den yokohamae) where settling begins together with the start Boogaart (1997) divided flatfish into three groups: of eye migration and the development of most of the plaice-like species that feed on epi-benthic prey, sole- traits associated with metamorphosis are completed after like species that settle at very small sizes and have settlement (Fukuhara, 1988; Joh et al., 2005). At the restricted areas for settlement, and bothid-types that other extremes are Dover sole (Microstomus pacificus) settle at large sizes over wide areas. These divisions may and slime flounder (M. achne) where metamorphosed not be completely accurate, but they represent an individuals may remain pelagic for many months attempt to link growth and metamorphosis and to the (Markle et al., 1992; Aritaki and Tanaka, 2003). habitat immediately post-settlement. Benoit and Pepin The de-coupling of metamorphosis and settlement (1999) and Benoit et al. (2000) used a more analytical may be related to plasticity in larval growth rate, size, approach to examine the relationship between growth and metamorphosis. Overall, it is apparent that in some rate, age at metamorphosis and size at metamorphosis. species metamorphosis is a size-related phenomenon, The complex variations in age and size at metamorpho- whereas in other species it is dependent on larval growth sis, especially in relation to temperature and larval rate rather than size. There have been a large number of growth rate, have been analysed using correlation laboratory and field studies investigating the inter- analysis, multivariate techniques and event analysis relationships between these traits. In some species the (Chambers and Leggett, 1989; Benoit and Pepin, 1999). size threshold for metamorphosis or settling is quite It may also be revealing to express some of the wide (Benoit and Pepin, 1999; Gavlik et al., 2002); relationships through reaction norms. however, in other species there is a narrow size threshold resulting in a fairly synchronised settling 5. Discussion and uniform post-settlement size distribution (Fernan- dez-Diaz et al., 2001). Locally fluctuating environmen- Studies of flatfish metamorphosis are complicated by tal conditions will also affect the larval growth rate of a the fact that numerous staging systems have been species and this can affect both the growth during and published to categorise the development of flatfish pattern of metamorphosis. For example, in poor feeding larvae. Some staging systems include quite detailed conditions, Senegal sole grew more slowly, and were substages to cover morphological changes associated smaller at metamorphosis, and metamorphosis was with metamorphosis (Fukuhara, 1988; Keefe and Able, relatively unsynchronised across the population (Fer- 1993; Neuman and Able, 2002), and a few include nandez-Diaz et al., 2001). Summer flounder larvae grew important developmental changes in behaviour (Pittman faster at higher temperatures and tended to be more et al., 1990). Most schemes emphasise the externally synchronised in metamorphosis and settlement (Burke recognisable changes in eye migration andasymmetry, et al., 1999). whereas many other anatomical, physiological, and Elevated temperatures lead to an increase in growth behavioural changes are unmarked (Ryland, 1966; rate and, for many species, this leads to metamorphosis Minami, 1982; Hotta et al., 2001 cited in Wada et al., at a larger size (Benoit and Pepin, 1999). However, 2004). growth rate and size at metamorphosis are not always The morphological and physiological changes that linked, especially where growth and development occur during larval development in all species require 42 A.J. Geffen et al. / Journal of Sea Research 58 (2007) 35–45 energy and at the same time confer advantages that on growth or size. Settlement can be triggered or improve feeding performance and growth efficiency. delayed by environmental cues such as current speed, However, it is often difficult to imagine how feeding, salinity, light, or prey density (Bailey et al., 2005). Such assimilation and growth can continue during the re- an overlapping system of endogenous and exogenous modelling that occurs in flatfish larvae. In fact, there controls and triggers is highly adaptive and supports the seems to be a wide variation among flatfish species in the wide variety of species of flatfish, and the wide range of timing, order, and synchronicity of the different organ environments that they settle in. changes. This may explain the species differences in the Whether metamorphosis or settlement represents a extent of growth and feeding during metamorphosis and critical period in terms of recruitment for the population settlement. In some species the ability to store energy is not clear. Major recruitment variations are induced by prior to metamorphosis may allow growth to continue. processes operating in the pelagic phase (Leggett and Extended metamorphosis in other species may allow the DeBlois, 1994; Van der Veer et al., 2000), although larvae to continue to feed efficiently as changes in processes operating after settlement can also signifi- neuroanatomy and eye migration occur gradually. cantly affect abundance. For decades it has been Flatfish larvae may be particularly vulnerable to assumed that the obvious physical transformations of predation if vision and other senses are impaired during flatfish metamorphosis must entail elevated mortality, metamorphosis, although one study showed that the and must influence recruitment. Shifts in mortality rates escape response of winter flounder was not worse during metamorphosis ‘should’ occur for a variety of during metamorphosis (Williams and Brown, 1992). reasons such as errors in cell division, insufficient Vulnerability to predation may also increase if growth energy reserves or increased predation. So why is it so rate decreases at metamorphosis, since slower-growing difficult to find evidence of enhanced vulnerability larvae may suffer higher predation mortality rates during metamorphosis? One reason is the inadequate (Nielsen and Munk, 2004). and non-representative sampling of metamorphosing Metamorphosis is often assumed to be a critical flatfish, which hinders the estimation of mortality rates period, in the classic sense of being a process that associated with metamorphosis and settlement. We also determines year-class strength. Metamorphosis and lack estimates of the energy demands of metamorphosis, settlement may be energetically demanding because of making it difficult to assess prey availability and sub- the extra requirements of physical remodelling together sequent impact on mortality. Metamorphosis in flatfish with added hormone production and also because of the is probably equally as critical as it is in other groups. problem of energy acquisition. Prey capture may be Behavioural and habitat changes at settlement may problematic if the ability to search, locate, and capture prove to be more significant for recruitment than the prey is decreased during metamorphosis. The transition process of metamorphosis. Considering the wide variety from pelagic larva to benthic juvenile also means that of flatfish dispersal patterns and nursery habitats it is not new prey models and responses must be learned. Prey surprising to find that the flexibility of adaptations availability may be reduced at the end of the pelagic associated with settlement may be more important than phases because of season or because of moving into the evolutionary patterns of metamorphosis in deter- deeper water, but the abundance of new epibenthic prey mining survival and recruitment in flatfishes. is not likely to be limiting. Larval size at metamorphosis should be a major factor in determining the energy Acknowledgements reserves and amount of time that an individual has in order to make the transition to a settled juvenile. Species The authors gratefully acknowledge the constructive that metamorphose at larger sizes may be more flexible comments made by three anonymous reviewers. in response to environmental triggers for settlement and less controlled by purely physiological triggers. 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