Recruitment

Chapter 6

Recruitment Henk W. Van der Veer and William C. Leggett

6.1 Introduction At the beginning of the last century Hjort (1914, 1926) advanced the hypothesis that yearclass strength in marine fishes is controlled during a ‘critical phase’ in the early life history. The mechanisms involved were thought to be a combination of density-independent processes related to fluctuations in the physical environment and density-dependent processes caused by either predation or food competition. After almost a century, this picture has altered very little: year-class strength in marine fishes appears to be primarily determined by mortality processes operating during the pre-juvenile stage of the life history. This process appears to result from a combination of coarse control during the period of egg and/or larval drift, followed by a second interval of finer-scale regulation later in the early life history (for review see Leggett & DeBlois 1994). While this general pattern of year-class regulation remains largely unaltered by a century of research, the intervening period has produced a large volume of excellent studies, primarily on recruitment processes in single species. A continuing debate reflected in all these studies is the extent to which the processes determining recruitment are species- and/or area-specific or are part of a more general pattern affecting more than one species or species group. Arguments in support of the presence of general patterns are founded on evidence of a link between the factors controlling recruitment and species- or group-specific early life history patterns in fishes (Roff 1982; Rothschild & DiNardo 1987). Further support for this view is provided by the fact that adjacent populations often show synchrony in year-class strength over spatial scales of hundreds of kilometres (Walsh 1994b; Myers et al. 1997; Fox et al. 2000). Additional evidence is provided by the observation that flatfishes, as a group, are characterised by a relatively low recruitment variability (Beverton 1995). This implies the existence of flatfish-specific life history characteristics that moderate recruitment variability. Miller et al. (1991) were among the first to examine the early life history patterns specific to flatfishes in the context of factors controlling recruitment. Their study, which was restricted to a qualitative analysis of the juvenile (demersal) phase of a subset of North American species, led to a series of explicit predictions which have subsequently been shown to be inconsistent with current knowledge about latitudinal variability in recruitment in these species (Leggett & Frank 1997; Philippart et al. 1998). To date, a quantitative framework for analysing and interpreting the relationship between flatfishes’ early life histories and factors regulating recruitment remains elusive. In this chapter the data and hypotheses relating to the generation

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and regulation of recruitment and recruitment variability in flatfishes are reviewed, and the ideas of Miller et al. (1991) extended to the pelagic life stage of flatfishes during which the coarse-grained determination of recruitment success appears to occur. The starting point for the analysis is the assumption that recruitment variability will be caused either by inter-annual variability in population egg production, by inter-annual variability in survival of these eggs and the resulting larvae or by a combination of both (Cushing 1995; Rickman et al. 2000). The approach taken is to identify relationships between flatfish life history traits and recruitment. More traditional overviews of recruitment variation in flatfishes can be found in Iles & Beverton (2000), Van der Veer et al. (2000), in the proceedings of five Flatfish Symposia, published by the (Netherlands) Journal of Sea Research (see Preface for details) and in Chapter 5 of this volume. From this perspective, three factors require analysis in the context of an understanding of recruitment processes in flatfishes: the distributional range of the species; the average level of recruitment achieved over time; and the annual variability in recruitment.

6.2 Range of distribution A general requirement for the development of a stable population by any species is the ability to close the life cycle. In flatfishes, the pelagic dispersal phase appears to be the most critical period, because settling occurs in specified nursery areas and therefore the duration of the egg and larval stage must conform to the length of the period of transport required to ensure metamorphosis. Otherwise, larvae will metamorphose and settle in suboptimal habitats and, as a consequence, experience reduced survival. Because development rate is strongly influenced by temperature conditions during drift (see for example, plaice (Pleuronectes platessa): Harding et al. 1978; Van der Veer & Witte 1999), this delicate balance between development time and settlement location is subject to temporal and spatial variation. Consequently, the time window for settlement, determined by the size and location of the nursery zone relative to the spawning site and the environmental conditions experienced en route, becomes critical. It is also probable that this temporal ‘window of opportunity’ will become progressively constrained toward the poles, a product of the protraction of spawning and the temperatureinduced reduction in development rate that occurs with latitude (Minami & Tanaka 1992). Should this reduction occur, the ‘window of opportunity’ could limit the species’ ability to close the life cycle, and hence its distribution. One solution to this latitudinal trend would be to increase the duration of drift (i.e. increase the distance between spawning and nursery sites) at higher latitudes in response to the declining average temperature during drift. However, the available evidence (Walsh 1994a) suggests that the period of larval drift does not increase meaningfully with latitude. A second solution, involving physiological adaptation to the decreased average temperatures experienced at higher latitudes, might involve counter-gradient growth compensation during the larval stage (Conover 1992). To date, there has been no systematic investigation of this possibility. The prolonged development times of eggs and larvae spawned at higher latitudes should also increase the potential for mixing between populations, perhaps destroying their integrity or negating population-specific adaptations. The increase in egg and larval development time with latitude could also serve to limit the geographic distribution of the species

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Flatfishes

and to induce variability in recruitment. The data currently available are insufficient to assess this hypothesis. Overall, there is little doubt that the most important factor governing the distributional range of the flatfishes is temperature. Dominating this regulating influence is the absolute temperature tolerance limit of each species, and the effect of temperature on the abundance of the key prey of one or more life stages. This influence may vary between species depending on which of the many life stages is the most sensitive to these direct or indirect temperature effects. The distribution of many flatfish species (e.g. Atlantic halibut (Hippoglossus hippoglossus), plaice), extends to, or close to, the poles (Wheeler 1978; see also Chapter 3). In these species, therefore, latitudinal distribution appears to be limited only by temperatures at the warm-water limits of their ranges. Adult body size in flatfishes declines toward the equator (Pauly 1994; Van der Veer et al. 2003), a response generally attributed to the decline in ocean productivity and the resulting limitation of food supply at lower latitudes (Gross et al. 1988). The warm-water limit of distribution of flatfishes may, therefore, be defined by the point at which energy uptake can no longer compensate for metabolic costs. In species where this energetic constraint operates at the adult level, compensation may be achieved through migration which takes the adult to more favourable feeding environments during some portion of the year, a behaviour exhibited by plaice (Harden Jones 1968; Greer Walker et al. 1978). An alternative, and perhaps more likely, limitation on distribution may be imposed by the effects of energy limitations on egg size. Egg size, like adult body size, declines with decreasing latitude in cold water-adapted flatfishes (see Miller et al. 1991; and for a general overview see Chambers 1997). When energy available for egg production, or the effects of limitations in the energy available to embryos and early stage larvae become limiting, the life cycle can no longer be closed. This limitation could be imposed by a paucity of energy for egg production, or the interacting effects of low egg energy and higher metabolic rates during development imposed by the higher ambient temperatures experienced at lower latitudes. In these situations, too, behavioural adaptations such as a shift in the timing of spawning to earlier in the seasonal cycle of temperature could compensate, in part, but ultimately behavioural adaptations will also prove ineffective. The data currently available on patterns in the timing of spawning at lower latitudes are inadequate to assess the possibility of this trend. Temperate zone flatfish species appear to experience both warm and cold water limits to their distribution. The limiting processes likely to be operating at low latitudes are described above. Temperate species living near the northern limit of their distribution appear to compensate in at least two ways: (1) through an increase in egg size (developmental energy reserve) with latitude which supports a higher development rate and shorter hatching times at higher latitudes (Kooijman 2000), and (2) a corresponding shift in the period of spawning to later in the season when temperatures are approaching their seasonal peak. Both patterns have been reported (see Minami & Tanaka 1992). In these species one limit to their distribution may be the point at which increases in egg size reach a maximum (possibly constrained by energy availability to the adult, or by the trade-off between egg size and number), thereby limiting the capacity to compensate for the effects of further decreases in temperature on development times. Tropical flatfish species, in contrast, appear to be limited only by cold waters, these limits occurring at both the southern and northern limits of their ranges. The limiting factors in their

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distribution are likely, therefore, to mirror those experienced by temperate flatfishes occupying habitats near the northern limit of their range. However, for tropical flatfishes the limits to their distribution are also likely to be influenced by the higher average temperatures and the relative paucity of food in the habitats they occupy, both of which would tend to limit adult body size and egg size, thereby limiting their scope for adaptive responses. It follows from the above that, for tropical species, egg size (which is typically small) will remain relatively constant over the protracted spawning period that is typical at those latitudes. Furthermore, because of their small egg, the high temperatures they experience, and the corresponding short development period they exhibit, spawning locations should be closer to the nursery areas. Walsh (1994a) reported a strong relationship between latitude, egg size, the season of spawning and the duration of the transport phase towards the nursery areas – all of which are consistent with the above expectations.

6.3 Average recruitment levels In the standard analysis of recruitment processes, as applied to most marine fish populations including the flatfishes, total egg production at spawning (total reproductive effort) is considered to be directly proportional to the total biomass of the parent stock. While there are good theoretical reasons to expect a decoupling at large stock sizes (Beverton & Holt 1957), experience has shown the biomass of the parent stock to be largely independent of recruitment over a wide range of parent stock sizes (Rothschild 1988; Hilborn & Walters 1992). This implies that either (1) density-dependent factors sufficient in magnitude to dampen and possibly even offset any relationship between spawning stock biomass or total egg production operate during the egg and larval stages or (2) the assumption of a causal relationship between spawning stock biomass, total egg production and recruitment is flawed. While density-dependent forces clearly operate at the juvenile stage (Leggett 1977; Van der Veer 1986), and these appear to be particularly important in flatfishes (Beverton & Iles 1992a, b), evidence in support of the existence of density-dependent regulation during the egg and larval stages is virtually non-existent, notwithstanding the frequent assumption of its importance (Iles 1994; Iles & Beverton 1998). The existence of density-dependent mortality during the egg stage is highly unlikely because developing embryos rely exclusively on stored energy reserves. Density-dependent predation is a possibility, but is unlikely to be a significant factor. Densities during the egg stage are relatively low even in the most concentrated egg patches (typically