Adult-mediated connectivity and spatial population structure of sardine in the Bay of Biscay and Iberian coast

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Abstract

This work investigated adult-mediated connectivity and spatial population structure of sardine in the European Atlantic waters. The spatial and temporal progress of cohorts was modelled using abundance-at-age survey data by area in the period 2000–2016, covering the region from the northern Bay of Biscay to the eastern Gulf of Cadiz. A novel methodology was used to calculate indices of cohort movement between areas. Movement was relatively low between three large regions, the Bay of Biscay, the northern Spanish and Portuguese waters and the Gulf of Cadiz, each hosting a recruitment hotspot. On the other hand, one half of the sardines recruited in North Portugal and a quarter of those recruited in Southwest Portugal moved to northern Spanish waters and South Portugal, sustaining local populations and fisheries. Movement was mainly driven by recruitment strength and, in a less extent, by food availability during fall. The connectivity and dynamic patterns suggest a metapopulation with three weakly connected populations and density-dependent source-sink movement within the northern Spanish and Portuguese waters population. While the weak connectivity does not invalidate the management boundary between the Bay of Biscay and the Iberian Peninsula, the Gulf of Cadiz may be treated as a separate stock. Multi-area/metapopulation assessment approaches should be applied to account for complex population structure, the higher risks of depleting source areas and/or less productive populations.

Introduction

Marine fishes are often structured in multiple subpopulations connected by exchange of early life stages, juveniles and adults (Secor, 2015). Subpopulations are likely to have different life history traits and demographic characteristics reflecting genetic diversity and phenotypic plasticity, and may respond differently to environmental variability and fishing exploitation. Spatial population structure and connectivity influence population dynamics, therefore they must be taken into account in stock assessment and fisheries management (Cadrin et al., 2014, Goethel and Berger, 2017, Kerr et al., 2016, Pita et al., 2016).

Despite evidence of complex population structure and mixing within and between stocks, assessment and fisheries management advice still assume closed stocks for the majority of cases (Kerr et al., 2016). The spatial structure needs to be considered when addressing management issues otherwise the sustainability of resources and fishing activity might be impaired. If the closed stock assumption is violated, management of a mixed stock complex can potentially lead to overfishing of the less productive populations and underfishing the most productive populations (Kerr et al., 2010). Management of a portion of a stock may also lead to unsustainable exploitation as the stock distribution changes over time and there are spatial differences in demography and population dynamics.

To incorporate complex spatial population structure into assessment and management it is necessary to have knowledge of the connectivity between subpopulations, namely on the directions and rates of dispersal/transport and migration. Connectivity may be established at various life stages. Larval dispersal/transport has been given far more attention than juvenile or adult dispersal in studies of spatial population structure (Lipcius et al., 2008) but recent studies argue that adult-mediated connectivity is a widespread form of connectivity and plays an important role in the structure and dynamics of fish populations (Archambault et al., 2016, Frisk et al., 2014). Conceptual models of population structure based on larval-mediated connectivity (Lipcius et al., 2008) have been transposed to cases of adult-mediated connectivity (Secor et al., 2009).

Tagging, genetics, otolith microchemistry and parasite analyses are some of the approaches that may be used to estimate movement rates between sub-populations (Kerr and Campana, 2013, MacKenzie and Abaunza, 2013, Schwarz, 2013). Demography also provides information on the spatial structure of populations and may be used to derive qualitative indices of movement between subpopulations (Peoples and Frimpong, 2012). For example, Murta et al. (2008) described horse mackerel (Trachurus trachurus) ontogenetic migrations in the Iberian waters based on the geographic variation of the age composition of cohorts. This approach is particularly valuable to study metapopulations, a type of spatial structure and dynamics that has been frequently proposed for small pelagic fish (e.g. North Sea herring, Clupea harengus: Mcquinn, 1997; Ruzzante et al., 2006: blue whiting, Micromesistius poutassou: Was et al., 2008; sprat, Sprattus sprattus: Limborg et al., 2009). A metapopulation is a regional group of local subpopulations, each of which is generally self-sustained, but connected through dispersal of individuals and interbreeding (Kritzer and Sale, 2004).

Connectivity among subpopulations in a metapopulation may be driven by density-dependent or density-independent dispersal and may be unidirectional or bidirectional (Secor et al., 2009, Shepherd and Litvak, 2004). The type and degree of connectivity influence the similarity of life history and demographic traits, the stability and productivity of the various subpopulations and of the metapopulation (Cadrin and Secor, 2009, Kerr et al., 2010). When subpopulations differ in productivity, movement tends to be driven by population abundance and to run from the more productive to the less productive subpopulation, known as source-sink dynamics (Goethel and Berger, 2017). Source populations tend to have higher proportions of juveniles than adults whereas the opposite is seen in sink populations; the differences between age distributions may be used to assess movement between the two (Peoples and Frimpong, 2012). Differences in age structure are likely to be amplified for species that undergo ontogenetic changes in habitat from juvenile stages (in restricted nursery grounds) to subadult and adult stages (more widespread) (Vasconcelos et al., 2014).

Sardine (Sardina pilchardus, Walbaum) is a valuable fishing resource in Europe with annual landings from the Bay of Biscay and Iberian Peninsula above 100,000 t since the late 1970s (Silva et al., 2015). Assessment and management assume three stocks in European Atlantic waters: the Bay of Biscay (BoB) stock, the Iberian Peninsula (IP) stock and the southern Celtic Seas-English Channel (CS) stock, recently considered to be separate from the BoB stock (ICES, 2017a). Over the last 15 years, the IP stock decreased severely due to prolonged low recruitment and high catch levels, with serious social and economic impact on the Portuguese and Spanish purse seine fishery. The BoB stock is healthy with recent increases in its fishery yields (since 2012), partly as a result of restricted fishing for the IP stock. Knowledge of the CS stock is limited due to the lack of monitoring; available data restricted to landings and acoustic surveys covering part of the stock in recent years, do not raise concern about fishing levels.

The existence of sardine subpopulations in the Bay of Biscay and Iberian Peninsula has been suggested by geographical differences in biological traits and demographic rates (e.g. morphometrics, growth, recruitment) although the boundaries and connectivity between putative subpopulations are unclear (ICES, 2016 and references therein). Regional age structures typical of source-sink dynamics have been suggested (Silva et al., 2009). The contrasting abundance trends between the BoB and the IP stocks provided an opportunity to improve knowledge on connectivity between areas and how it is affected by abundance/density and environmental conditions. Within the region there are contrasting oceanographic and environmental features, that may be responsible not only for the observed differences between subpopulations but also for the movement of sardines between areas. Sardine larvae growth and survival were shown to be highly dependent on temperature (Garrido et al., 2015), which is probably reflected in the local variability of recruitment success. On the other hand, sardines are exclusive planktivorous fish, feeding on small zoo- and phytoplankton prey (Garrido et al., 2015), therefore, sardine population dynamics are probably related to plankton productivity.

This study aims to investigate the magnitude of movement of adult sardines within the region from the northern Bay of Biscay to the eastern Gulf of Cadiz, to identify the main connectivity paths between areas, and identify drivers of movement. The results will improve knowledge of the spatial structure and dynamics of populations, assist the re-evaluation of stock boundaries and provide information to develop multi-area stock assessment models and test spatial management strategies for the sardine fisheries.

Section snippets

Data

Total biomass (thousand t), total abundance and abundance-at-age (billions of individuals), and distribution area (nm2) were obtained from annual acoustic surveys carried out by France (PELGAS, since 2000), Spain (PELACUS, March/April since 1996) and Portugal (PELAGO, March/May, since 1996 with gaps in 2004 and 2012) that covered the whole study area. Mean fish density was calculated as total abundance/distribution area (billions of individuals/nm2). Details on the methodology of the surveys

Overview of sardine abundance, fishery and environmental conditions

In the period 2000–2016, the total abundance of sardine in the study region varied from 7.1 to 34.0 billion individuals (mean ± SD =16.7 ± 7.6 billion individuals). Mean abundance peaked in BISC and NPOR, was lower in SWPOR and southern Iberia and the lowest in northern Spanish waters (Fig. 2a). The pattern of mean density by area contrasted with that of abundance showing the lowest values in the BISC as a result of the large continental shelf area (Fig. 2b). Total biomass varied from 309 to

Discussion

Two types of spatial population structure are frequently postulated for pelagic fish: discrete subpopulations and metapopulations (Goethel and Berger, 2017, Secor, 2015). Discrete subpopulations are reproductively isolated but mix outside the spawning season or area. Population structure is maintained by segregation of spawning grounds in space and/or time coupled with mechanisms of natal homing and larval retention. Natal homing has been detected in large pelagics such as tuna (Rooker et al.,

Conclusions

This study indicated that sardines distributed within the region from the northern Bay of Biscay to the eastern Gulf of Cadiz in the period 2000–2016 were connected by movement of adults. There were large differences between areas with respect to the magnitude of fish flow. Flow rates between three large areas, the Bay of Biscay, the northern Spanish and Portuguese waters and the Gulf of Cadiz, were relatively low. The existence of recruitment hotspots within each of the three areas supports

Acknowledgements

The collection of acoustic and fisheries data on sardine within Iberian waters and the French Bay of Biscay result from the work of several researchers and technicians in the past three decades. E. Soares, D. Morais, R. Milhazes, A.V. Silva and J. Barra (IPMA, Lisbon, Portugal), M. Bernal, C. Porteiro and E. Peleteiro (IEO,Vigo, Spain), J. Massé (IFREMER, Nantes, France), and P. Alvarez and I. Rico (AZTI, Pasaia, Spain) are some of the people to whom we are grateful, but many others are

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