Size-dependent change in body shape and its possible ecological role in the Patagonian squid (Doryteuthis gahi) in the Southwest Atlantic

Abstract

Cephalopods are a versatile group with several mechanisms in place to ensure the success of future generations. The Patagonian long-finned squid (Doryteuthis gahi) populations on the southern Patagonian shelf are believed to be genetically homogenous but mechanisms connecting them geographically and temporally are unresolved. Individual growth is highly variable within cephalopod populations and is likely to affect individual patterns of migration and, thus, population connectivity as a whole. Therefore, this study aimed to make inferences about 2 population structure by analysing the size at which individuals were mature and aimed to describe the intrapopulation growth (allometric) trajectories of body shape, using landmark-based geometric morphometric techniques to describe phenotypes. Samples were collected from June 1999 to November 2017 around 52 o S and 58 o W. Smoothing curves from binomial generalised additive models (GAMs) suggested two size modes of maturity in females and one or multiple modes in males dependent on year and season. There was a gradual elongation of the mantle and an increase in the relative fin size throughout ontogeny. Shape scores from geometric morphometric shape coordinates revealed a continuous non-linear allometric trajectory with a significantly different slope angle for males exceeding 20.1 cm dorsal mantle length (DML). At the extreme of this continuum, the largest 'super-bull' form had a substantially more elongated body shape, a heavier fin and a larger fin area compared to the rest of the population, a body shape associated with enhanced swimming performance which may help to maintain population connectivity. The prevalence of these rare super-bulls in the fishery varied widely between years, suggestive of phenotypic plasticity. This study provides evidence that the D. gahi population on the southern Patagonian shelf has a complex population structure with high intraspecific variation. 1 Introduction Populations of animals often incidentally assume risk-spreading strategies that reduce the potential for population collapse. In many cases, a multi-generational structure provides a reserve of several year-classes of reproductively viable adults and genetic variability that reduces this risk of collapse or extinction (O'Dor 1998). Conversely, most cephalopods are characterised by short, often annual life-cycles with a complete turnover in biomass every one to two years. They therefore do not have a multi-generational structure to buffer against fluctuations in spawning and recruitment success (Pierce and Guerra 1994; Boyle and Rodhouse 2008). The flexibility inherent within many cephalopod populations may allow them to persist within the heterogeneous marine environment without a multi-generational buffer in place (O'Dor 1998). Although this is a group selectionist argument for phenotypic plasticity, it is plausible if many populations exist and population persistence depends on plasticity. Virtually every facet of cephalopod life-history examined to date has revealed an incre...

'Superbull' males: what role do they play and what drives their appearance within the Doryteuthis gahi Patagonian Shelf population?

“…This study has made several steps in advancing our understanding of why superbull males exist within the D. gahi population using a toolbox approach. The streamlined shape and large fins characteristic of the superbull morph are hypothesised to result in an extension of their migratory routes, providing a population-level benefit by connecting geographically separate subpopulations within Falkland Islands waters (Arkhipkin et al 2015a;Jones et al 2019). In addition to this connectivity between remote spawning areas, it is also possible that these squid provide temporal connectivity between spawning cohorts.…”

“…Several mechanisms have been proposed to allow for interbreeding between different seasonal cohorts, including early maturation and mating of males with mature females from the previous cohort, a wide variation in spawning time resulting in overlap or an extended life cycle of more than 1 year for some individuals (Mesnil 1977;Boyle et al 1995;Arkhipkin et al 2013). Therefore, superbulls were hypothesised to have a life cycle exceeding 1 year (including the period of embryogenesis), providing the population level benefit of temporal connectivity (Jones et al 2019). In order for a population-level benefit to occur, these squid would have to be reproductively viable.…”

“…Some authors have pointed to evidence for the existence of more than two size groups in males, for example Collins et al (1999) for Loligo forbesii, implying that plasticity in growth form extends beyond the existence of two reproductive strategies in males. Anomalously large males, much larger than the typical mature males, have been found to occur in populations of several loliginid squid (Mangold 1987;Pierce et al 2013;Jones et al 2019). A recent study investigating the intrapopulation body shape variation of D. gahi found that males exceeding 20-25 cm DML had a significantly different body shape than the rest of the population and were suggested to be a third 'superbull' morph (Jones et al 2019).…”

“…Anomalously large males, much larger than the typical mature males, have been found to occur in populations of several loliginid squid (Mangold 1987;Pierce et al 2013;Jones et al 2019). A recent study investigating the intrapopulation body shape variation of D. gahi found that males exceeding 20-25 cm DML had a significantly different body shape than the rest of the population and were suggested to be a third 'superbull' morph (Jones et al 2019). These superbull males had a substantially more elongated body, a heavier fin and a larger fin area than the rest of the population.…”

“…Owing to the streamlined shape and large fins characteristic of this morph, it is likely that these superbull males have enhanced gliding abilities and are able to undertake longer migrations than the rest of the population (Arkhipkin et al 2015a). It was therefore hypothesised that these superbull males extend their migratory routes, providing geographic connectivity by migrating between remote spawning areas (Jones et al 2019). In other species, anomalously large individuals have delayed maturation and an extended life cycle.…”