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 commer- cially 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 un- coupled, 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 ana- tomical 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