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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 20 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 commer- cially 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 1385-1101/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2007.02.004 Please cite this article as: Geffen, A.J. et al. The cost of metamorphosis in flatfishes. J. Sea Res. (2007), doi:10.1016/j.seares.2007.02.004 ARTICLE IN PRESS 2 A.J. Geffen et al. / Journal of Sea Research xx (2007) xxx–xxx 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. Please cite this article as: Geffen, A.J. et al. The cost of metamorphosis in flatfishes. J. Sea Res. (2007), doi:10.1016/j.seares.2007.02.004 ARTICLE IN PRESS A.J. Geffen et al. / Journal of Sea Research xx (2007) xxx–xxx 3 123 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).