Not to be cited without prior reference to the authors ICES CM 2004/CC:31 Interannual variation in life-cycle characteristics of the veined squid (Loligo forbesi) G.J. Pierce, A.F. Zuur, J.M. Smith, M.B. Santos, N. Bailey & P.R. Boyle The loliginid squid Loligo forbesi has a flexible life-cycle, involving variable size and age at maturity, presence of summer and winter breeding populations, and extended periods of breeding and recruitment. This paper reviews life history data collected since 1983 from the commercial fishery in Scottish (UK) waters and examines (a) the relationship between size and timing of maturation, (b) evidence for shifts in the relative abundance of the summer and winter breeding populations, and (c) the role of environmental signals in determining the timing of breeding. Evidence from fishery data suggests that, since the 1970s, the summer breeding population has declined while the winter breeding population now dominates and breeds later than was previously the case. Length-weight relationships and size at maturity showed significant inter-annual and seasonal variation during the period 1983-2001 and provide no evidence that there is currently a summer breeding population. Males are shown to decline in relative weight as they mature while females increase in relative weight. There is evidence that timing of breeding and size at maturity are related to environmental variation (winter NAO index). Key words: life history, time series, environmental factors G.J. Pierce, J.M. Smith, M.B. Santos, P.R. Boyle: University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK [tel: +44 1224 272866, fax: +44 1224 272396, e-mail: [email protected]]. A. Zuur: Highland Statistics Ltd, 6 Laverock Road, Newburgh, Aberdeenshire, AB41 6FN, UK [tel: +44 1358 788177, email: [email protected]]. N. Bailey: Fisheries Research Services, The Marine Laboratory, PO Box 101, Victoria Road, Aberdeen, AB11 9DB, UK [tel: +44 1224 876544, e-mail: [email protected]] INTRODUCTION The veined squid Loligo forbesi has been exploited as a fishery resource around the British Isles for at least 100 years (see Thomas, 1969; Thomas & Davidson, 1972; Howard, 1979; Pierce et al., 1994a). Interest in its biology dates back at least to the 1970s, when Holme (1974) published a short description of the life history of the species in the English Channel. This work already provided some clues as to the complexity of the life-cycle for, although the species was apparently annual, two breeding populations were apparently present, a one breeding in winter and one breeding in summer. In Scottish waters (Figure 1), two PhDs during the second half of the 1980s (Ngoile, 1987; Lum-Kong, 1989) provided further information on life-cycle biology and reproduction. The basic pattern that emerged was of an annual, winter breeding population. However, two peaks of recruitment were seen, in April and in autumn. Further indications of flexibility and/or complexity included evidence of two sizes at maturity (Boyle & Ngoile 1993a), recruitment throughout the year and the possible existence of morphologically distinct “stocks” (Boyle & Ngoile, 1993b) at Rockall and in coastal waters. Further studies (e.g. during several EC-funded research projects) in Scottish waters between 1990 and 2001 focused on distribution and abundance (Pierce et al., 1998, 2001; Waluda & Pierce, 1998; Bellido et al., 2001; Bellido, 2002; Pierce & Boyle, 2003; Zuur & Pierce, 2004; Young et al., in press), stock structure (Pierce et al., 1994 b, c; Brierley et al., 1995; Shaw et al., 1999) and ecology (Pierce et al., 1994d; Collins & Pierce, 1996; Pierce & Santos, 1996; Daly et al,, 2001). However, several studies have also examined development and growth (Yau, 1994; Martins, 1997; Hughes, 1998; Pierce et al., 1999; Craig, 2001; Gowland, 2002) as well as reproduction and recruitment (Pierce et al., 1994e; Boyle et al., 1995; Collins et al., 1997, 1999; Shaw & Boyle, 1997; Challier et al., in press). These studies essentially confirmed the picture established by Ngoile (1987) of an annual life- cycle with a winter breeding peak and two periods of recruitment. However, it is apparent that there are two or three micro-cohorts of Loligo forbesi present in Scottish waters, following different growth trajectories (Collins et al., 1999). It may be argued that some of the apparent variability in life history patterns reflects the persistence of summer and winter breeding populations in various proportions (Zuur & Pierce, 2004): the observed month-to-month pattern of maturation may be interpreted as two periods of recruitment and two periods of maturation. Shaw et al. (1997) confirmed that squid from offshore waters (around Rockall and Faroe) show some genetic differences from the coastal population. Thus, superimposed on the basic annual life-cycle there may be (in addition to individual variation) variation due to presence of winter and summer breeders, inshore and offshore populations, large and small sizes at maturity,. Unlike relatively long-lived fish species, squid populations are not buffered against environmental change by the presence of several age classes: any factor which affects recruitment success has an immediate impact on population size and, potentially, subsequent reproductive success. There is considerable evidence that distribution and local abundance are affected by environmental variation (see above) and we might logically expect recruitment success, growth, fecundity and breeding success to reflect environmental conditions. If the life-cycle of Loligo forbesi does indeed display substantial plasticity, we hypothesize that (a) changes in life-cycle characteristics would be evident over the medium- to long-term and that (b) such changes may occur in response to changing environmental conditions. We now have access to life history and fishery data on the species in Scottish waters collected over more than 15 years. In this paper we examine interannual variation in the relative importance of summer and winter breeding, length-weight relationships, size at maturity and the timing of maturity, and ask whether such variation can be related to environmental signals, notably the North Atlantic Oscillation Index – which provides a general indication of the strength of Atlantic inflow into coastal waters of Scotland. To measure the relative importance of winter and summer breeding, abundance data are needed. Catch-per-unit effort data from commercial trawling may be used as an approximate relative abundance index (see Pierce et al., 1994a; Pierce & Boyle, 2003). It can also be argued that the peak of the fishery is driven by recruitment (see Figure 2, data from Pierce et al., 1994a, e) and is normally 3-4 months ahead of the peak in the proportion of mature animals. Thus by examining interannual trends in the month-to-month pattern of CPUE we may obtain an indication of interannual variation in the importance of winter and summer breeding. A formal analysis of interannual trends in monthly CPUE series was presented in Zuur & Pierce (2004). Here we briefly re-present the same data in terms of the likely interpretation in terms of the timing of breeding. We go on to examine variation in two basic biological variables, weight at length and maturity at length. Weight at length is expected to follow a standard exponential curve. However, we might also expect variation in relation to the process of maturation. Thus, growing gonads may incur a different energetic cost to growing somatic tissue, mature animals may feed less actively, and gonad growth may involve utilisation of some somatic tissues as an energy source. Seasonal variation might also be expected, relating to changers in food availability, although it may be difficult to disentangle this effect from the effect of maturation. Lastly, we may expect year-to-year differences in growth patterns, related to differences water temperature (see Forsythe, 1993) and/or food supply. Maturation is commonly assumed to be size-dependent, with the proportion of animals that are mature typically increasing with body length following a logistic curve. However, maturation may also require a seasonal trigger and/or depend on accumulation of sufficient energy reserves. Thus we might expect to see both seasonal and interannual variation. In the case of both weight and maturity at length, differences are expected between males and females. For example previous studies show that males can mature at smaller sizes than females and may mature slightly earlier in the year (Pierce et al., 1994e; Boyle et al., 1995). If it is possible to tease out interannual differences in weight and maturity at length it might be hypothesised that these could be linked to environmental variation (e.g. larger weight and earlier maturation in warmer years). Another possibility is that there will be a relationship between size and abundance: positive if both parameters represent a response to environmental conditions, negative (at least at high abundance levels) if there is density- dependent competition. The present study aims to test these hypotheses. METHODS (1) Winter and summer breeding Commercial landings of squid (kg) and fishing effort (hours) data for UK-registered fishing vessels landing in Scotland during the period 1970-2000 were extracted from the Marine Laboratory FRS database. Since discarding of Loligo is thought to be minimal (Young et al., In Press), landings are assumed to accurately reflect catches. To obtain a reasonably consistent CPUE index we restricted the extraction to “light” and “heavy” single demersal trawls (henceforth referred to as “trawling”) from ICES areas IVa and VIa (henceforth referred to as “coastal waters”) and calculated an overall monthly CPUE index as total landings divided by total effort. Since 1998, Scottish fishing effort data are considered to be unreliable (A. Shanks, FRS Marine Laboratory, pers. comm.). However, as we will demonstrate, although there is evidence that CPUE in 1999 and 2000 was underestimated, the month-to-month pattern is driven by the landings data and examination of the latter confirmed that the underlying seasonal trend remains well-represented.