Study of the life-history traits of two species of polychaetes, Arenicola marina and A. defodiens, implementation of a Dynamic Energy Budget model and conservation of the species

Les arénicoles sont des polychètes benthiques présentant un cycle de vie bentho-pélagique complexe avec deux phases de dispersion larvaire seulement partiellement décrit jusqu’à présent. Ces espèces sont intensément pêchées comme appât sur les plages de la Manche orientale, notamment au sein d’une aire marine protégée, le Parc naturel marin des estuaires picards et de la mer d’Opale. Sans mesures de gestion, cette activité pourrait entraîner une diminution des populations d’arénicoles tout en affectant les caractéristiques physiques des plages et la biodiversité associée. Tout d’abord, deux espèces d’arénicoles ont été identifiées, Arenicola marina et A. defodiens, et leurs abondances, leurs distributions spatiales, ainsi que certains de leurs traits de vie (période de ponte, taille de première maturité sexuelle) ont été mesurées sur 4 sites d’étude. Ces données ont été comparées à des données de pêche pour estimer si les populations d’arénicoles étaient exploitées durablement, et pour fournir de potentielles mesures de gestion (De Cubber et al., 2018). Sur l’un des sites étudiés, A. marina était présente en grands nombres en médiolittoral supérieur et moyen tandis que A. defodiens occupait les niveaux médiolittoral inférieur et infralittoral de l’estran. Sur les autres sites, les deux espèces occupaient les niveaux médiolittoral inférieur et infralittoral, et les individus de A. marina étaient moins nombreux, et sans recrus. Les pontes de A. marina ont eu lieu en début d’automne et celles de A. defodiens en fin d’automne. Le besoin de mise en place de mesures de gestion de A. marina a été mis en évidence sur un site en comparant les abondances et les données de pêche. Ensuite, un modèle de type Dynamic Energy Budget (DEB) a été appliqué à A. marina en combinant des données de terrain, des données expérimentales (de croissance et de consommation d’oxygène) et des données de la littérature pour reconstruire le cycle de vie et la croissance de l’espèce dans des conditions environnementales in situ (De Cubber et al., in press). La reconstruction de la chronologie des premiers stades de vie avec le modèle DEB pour A. marina en fonction des conditions environnementales in situ a permis de prédire une première phase de dispersion de 5 jours suivie d’une période d’installation temporaire de 7 mois avant une deuxième phase de dispersion au printemps, à la fin de la métamorphose, qui semble concorder avec les observations de terrain. Enfin, la structure en taille de la population de A. marina sur un des sites d’étude a été suivie pendant 1.5 an pour explorer les migrations des adultes vers le bas d’estran reportées par plusieurs auteurs. Pour cela, un modèle permettant la reconstruction de la température au sein du sédiment a été adapté d’un modèle de température pour la vase; le contenu en azote du sédiment a été mesuré et différents proxys pour la nourriture ont été testés. Les réponses métaboliques des arénicoles à la nourriture (réponse fonctionnelle) et à la température (intervalle de tolérance et température d’Arrhénius) ont été estimées. Ces données, combinées au modèle DEB pour A. marina ont permis d’étudier les effets de variations de la température et la de nourriture rencontrés par les arénicoles suivant leur position sur l’estran et la profondeur de leur galerie. Le suivi de la structure en taille de la population de A. marina a clairement indiqué la présence de migration au cours du temps vers le bas d’estran.Arenicola spp. are marine benthic polychaetes displaying a complex bentho-pelagic life cycle with two larval dispersal phases, only partially described up to now, and intensively dug for bait by anglers on many foreshores of the Eastern English Channel. Without regulation, this activity can lead to the decrease of lugworms’ population while affecting the physical characteristics of the beach and the associated biodiversity. First, we identified through morphology and genetics two species of lugworms, Arenicola marina and A. defodiens, and assessed their abundance and spatial distribution at four studied sites, as well as some life-history traits such as the spawning periods and the size at first maturity. These data were compared to lugworms’ collection data to estimate its sustainability and to provide potential management measures (De Cubber et al., 2018). At one studied site, A. marina was present in large numbers on the higher and middle shore, whereas A. defodiens occupied the lower shore. At the other sites, both species cooccurred on the lower shore, and A. marina individuals were less numerous and lacking recruits. Spawning periods for A. marina occurred in early autumn and in late autumn for A. defodiens. One site appeared in need for management when linking abundance data with bait collection, where harvest was above the carrying capacity of the beach for A. marina. Second, a Dynamic Energy Budget (DEB) model was applied to the species combining the former as well as new field data, experimental data (growth and oxygen consumption data), and literature data in order to reconstruct the life cycle and growth of A. marina under in situ environmental conditions (De Cubber et al., in press). The reconstruction of the early life-stages chronology by the DEB model for A. marina according to in situ environmental conditions indicated a first dispersal phase of 5 days followed by a 7 months’ temporary settlement before a second dispersal phase in spring, at the end of metamorphosis, which appeared consistent with field observations. Finally, we followed-up the population size structure of A. marina at one studied site during 1.5 year to explore the down shore migration of lugworms recorded by several authors. To do so, we adapted a sediment temperature model from a mud temperature model (Guarini et al., 1997), measured the nitrogen content and tested several proxys for the food sources. The metabolic responses of lugworms to food (scaled functional response) and temperature (temperature tolerance range and Arrhenius temperature) were then assessed. We combined those data with the former DEB model to explore the effects of the fine changes in temperature and food conditions met by the individuals along the foreshore gradient and according to the depth of their galleries. The follow-up of the population size structure of A. marina showed clearly a migration pattern. The effect of sediment temperature alone when migrating did not allow significantly higher growth and egg production, while an increase of food concentrations down the shore did. Other factors might be taken in consideration in further studies such as desiccation and anaerobic metabolism during emersion periods at low tide. All these data constitute valuable information for conservation managers to better understand and regulate the lugworm populations. Further combination of the DEB model developed in this study with an individual-based model and a larval dispersal model could enable to understand the dynamics of the local lugworm populations

Annelid polychaetes experience metabolic acceleration as other Lophotrochozoans: inferences on the life cycle of Arenicola marina with a Dynamic Energy Budget model

International audienceArenicola marina is a polychaete (Lophotrochozoan) displaying a complex bentho-pelagic life cycle with two larval dispersal phases, only partially described up to now. A Dynamic Energy Budget (DEB) model was applied to the species in order to reconstruct its life cycle and growth under in situ environmental conditions. Two types of DEB models are usually applied to other Lophotrochozoans displaying similar life cycles: the standard (std-) model, applied to polychaetes (5 entries among the 1524 of the Add-my-Pet database on the 18/10/2018), and the abj-model, which includes an acceleration of metabolism between birth and metamorphosis, and which has been applied to most molluscs (77 abj-entries out of the 80 mollusc entries) enabling better fit predictions for the early life stages. The parameter estimation was performed with both models to assess the suitability of an abj-model for A. marina. The zero-variate dataset consisted of length and age data at different life cycle stages, the lifespan, the maximum observed length, and the wet weight of an egg. The uni-variate dataset consisted of two growth experiments from the literature at two food levels and several temperatures, laboratory data of oxygen consumption at several temperatures, and fecundity for different lengths. The predictions of the abj-model fitted better to the data (SMSE = 0.29). The acceleration coefficient was ca 11, which is similar to mollusc values. The field growth curves and the scaled functional responses (as a proxy of food levels) were suitably reconstructed with the new parameter set. The reconstruction of the early life-stages chronology according to in situ environmental conditions of a temperate marine ecosystem indicated a first dispersal phase of 5 days followed by a 7 months temporary settlement before a second dispersal phase in spring, at the end of metamorphosis. We emphasize the need for using abj-models for polychaetes in future studies

Linking life-history traits, spatial distribution and abundance of two species of lugworms to bait collection: A case study for sustainable management plan

Arenicola spp. are marine benthic polychaetes dug for bait by anglers. Without regulation, this activity can lead to the decrease of lugworms' population meanwhile affecting the physical characteristics of the beach and the biodiversity. Here, we identified through morphology and genetics two species of lugworms, Arenicola marina and A. defodiens, within a Marine Protected Area of the Eastern English Channel (France). For each species, abundance and spatial distribution were assessed using a stratified random sampling and interpolation at four studied sites, as well as some life-history traits. These data were compared to lugworms' collection data to estimate its sustainability and to provide potential management measures. At one site, A. marina was present in large numbers on the higher and middle shore, whereas A. defodiens occupied the lower shore. At the other sites, both species co-occurred on the lower shore, and A. marina individuals were less numerous and lacking recruits. Spawning periods for A. marina occurred in early autumn and in late autumn for A. defodiens. The size at first maturity of A. marina was at 3.8 cm of trunk length (between 1.5 and 2.5 years old). One site (Au) appeared in need for management when linking abundance data with bait collection, where harvest of both species represented ∼14% of the total amount of lugworms and was above the carrying capacity of the beach for A. marina. The retail value associated to lugworm harvesting within the MPA was estimated at the same level as the shrimp retail value. Our results highlight the need for some fishery regulations

Unravelling mechanisms behind population dynamics, biological traits and latitudinal distribution in two benthic ecosystem engineers: A modelling approach

The mechanistic approach consisting of coupling Dynamic Energy Budget (DEB) models to Individual-BasedModels (IBMs) allows simulating individual and population biological traits and their dynamics. This approachwas developed here to study population dynamics of two sympatric intertidal ecosystem engineers, Arenicolamarina and Arenicola defodiens (Annelida Polychaeta) occurring in the North-East Atlantic from Portugal toSweden. Latitudinal heterogeneity of the two species’ performances were investigated in terms of populationdynamics and biological traits using latitudinal differences in environmental forcing variables. The impactof the forcing variables on population dynamics processes (shore colonisation and migration, spawning andrecruitment, etc.) within a specific foreshore (mean values and seasonal patterns) was also assessed. PublishedDEB parameters were used for A. marina and a specific calibration was undertaken for A. defodiens, combiningliterature data and new laboratory experiments and field data. Our DEB-IBM simulated super-individuals’growth and reproduction while lugworms were colonising, migrating and dying over a simulated foreshore.Density rules affected population dynamics. Environmental forcings consisted in monthly values of chlorophylla(chl-a) concentrations and daily values of SST. Scenarios focusing on the two most contrasted of theseforcing variables time series were used to explore their relative effects over populations’ dynamics and onshoreprocesses were investigated at two sites displaying highly different simulated population abundances.Overall, northern sites with higher chl-a levels performed better displaying higher biomass, maximum lengthand reproductive outputs for both species. As expected, Sea Surface Temperature (SST) changes between sitesdid not impact greatly populations dynamics. Under favourable environmental conditions, intra- and interspecificcompetitions emerged from the model. Under non-favourable environmental conditions, A. defodiens’populations crashed and A. marina displayed atypical population processes, with rare spawning events barelyallowing the population’s renewal, and lower size at maturity. Further use and development of this model willlead to better insights on the lugworm populations’ evolution over the next decades

A generalized Dynamic Energy Budget model including 3D shape changes for modeling small pelagic fish growth

International audienceUnderstanding pelagic fish growth patterns from early life stages to adulthood is fundamental to accurately predict larval survival and predator-prey dynamics, which are influenced by individual size. Dynamic Energy Budget (DEB) models constitute useful tools to predict and explain these patterns in changing environments. In DEB models, fish individuals are usually assumed to grow either isomorphically, or to experience a metabolic acceleration phase between birth (b) and metamorphosis (j), during which the shape coefficient changes and both the maximum surface-area specific assimilation rate and the energy conductance are multiplied by a metabolic acceleration coefficient function of structural length. Here we propose a different growth model based on a Dynamic Energy Budget model (modified as in Maury, 2019 to properly account for the size-dependence of maintenance) that captures deviations from pure isomorphy, allowing length and width to grow non-proportionally. Our model represents the fish’s structural body as an ellipsoid and differentially allocates volumetric growth to length, height and width as a function of the distance between the current shape and characteristic stage-dependent shape attractors (expressed as width/length and height/width ratios). The resulting changes of the structural surface-to-volume ratios due to changing shape mechanistically explain the “metabolic acceleration” phenomenon that is often invoked to interpret early life growth patterns. We estimated model parameters for the European anchovy Engraulis encrasicolus, using data covering growth at all life-stages, observed shapes at early life stages, transitions between life-stages, and reproduction. The calibrated model accurately reproduces the observed deviations from isomorphy, with exponential length-dominated growth until metamorphosis, then a shift to height- and width-dominated growth (with a corresponding deceleration of growth in length) until the adult shape is reached, and finally isomorphic (characteristic von Bertalanffy) length growth. These deviations from the usual von Bertalanffy growth model could profoundly affect our understanding of larval survival, predator-prey and ecosystem-dynamics

A generalized Dynamic Energy Budget model including 3D shape changes for modeling small pelagic fish growth

Understanding pelagic fish growth patterns from early life stages to adulthood is fundamental to accurately predict larval survival and predator-prey dynamics, which are influenced by individual size. Dynamic Energy Budget (DEB) models constitute useful tools to predict and explain these patterns in changing environments. In DEB models, fish individuals are usually assumed to grow either isomorphically, or to experience a metabolic acceleration phase between birth (b) and metamorphosis (j), during which the shape coefficient changes and both the maximum surface-area specific assimilation rate and the energy conductance are multiplied by a metabolic acceleration coefficient function of structural length. Here we propose a different growth model based on a Dynamic Energy Budget model (modified as in Maury, 2019 to properly account for the size-dependence of maintenance) that captures deviations from pure isomorphy, allowing length and width to grow non-proportionally. Our model represents the fish’s structural body as an ellipsoid and differentially allocates volumetric growth to length, height and width as a function of the distance between the current shape and characteristic stage-dependent shape attractors (expressed as width/length and height/width ratios). The resulting changes of the structural surface-to-volume ratios due to changing shape mechanistically explain the “metabolic acceleration” phenomenon that is often invoked to interpret early life growth patterns. We estimated model parameters for the European anchovy Engraulis encrasicolus, using data covering growth at all life-stages, observed shapes at early life stages, transitions between life-stages, and reproduction. The calibrated model accurately reproduces the observed deviations from isomorphy, with exponential length-dominated growth until metamorphosis, then a shift to height- and width-dominated growth (with a corresponding deceleration of growth in length) until the adult shape is reached, and finally isomorphic (characteristic von Bertalanffy) length growth. These deviations from the usual von Bertalanffy growth model could profoundly affect our understanding of larval survival, predator-prey and ecosystem-dynamics

Robust identification of potential habitats of a rare demersal species (blackspot seabream) in the Northeast Atlantic

Species distribution models (SDM) are commonly used to identify potential habitats. When fitting them to heterogeneous, opportunistically collated presence/absence data, imbalance in the number of presence and absence observations often occurs, which could influence results. To robustly identify potential habitats for blackspot seabream (Pagellus bogaraveo) throughout its distribution area in the Northeast Atlantic and the western Mediterranean Sea, we used an ensemble species distribution modelling (eSDM) approach, modelling gridded presence–absence data with environmental predictors for two types of occurrence data sets. The first data set displayed the observed unbalanced spatially heterogeneous presence/absence ratio and the second a balanced presence/absence ratio. The data covered the full distribution area, including the European Atlantic shelf, the Azorean region and the Western Mediterranean Sea. Across these regions, populations display variable status. The main environmental predictors for potential habitats were bathymetry and annual maximum SST. The fitted ensemble compromise (eSDM) was projected over the whole grid to create a habitat suitability map. This map exhibited higher probabilities of presence for the balanced-ratio data set. A binary presence–absence map was then generated using optimized presence probability thresholds for four validation indices. Using the true skill statistic to optimize the threshold, the surface areas of the binary presence–absence map was 53% smaller for the balanced data set than for the observed unbalanced data set. However, the choice of validation index had an even greater impact (up to 15 000%). This indicates that studies using opportunistic data for SDM fitting need to pay attention to the effects of presence/absence data imbalance and the choice of validation index to fully evaluate uncertainty. © 2022 Elsevier B.V. All rights reserved.The study received financial support from France Filière Pêche (project DynRose) and the European Union’s Horizon 2020 research and innovation programme under Grant Agreement No 773713 (PANDORA).Pagellus bogaraveo; Species distribution models; Ensemble modelling; Heterogeneous data set; Presence–absence imbalancePeer reviewe

A generalized Dynamic Energy Budget model including 3D shape changes for modeling small pelagic fish growth

International audienceSmall pelagic fish (SPF) are key components of marine ecosystems, transporting energy from the lower to the upper trophic levels and thereby influencing the dynamics of the entire ecosystem. Understanding their complex growth patterns from early life stages to adulthood is fundamental to accurately predict larval survival and predator-prey dynamics, which are influenced by individual size. However, growth models are generally unable to accurately reproduce the growth acceleration and deceleration phases observed, particularly during early life stages. Here we propose a growth model based on a Dynamic Energy Budget model (modified as in Maury, 2019 to properly account for size-dependence of maintenance) that captures deviations from pure isomorphy. It represents the fish’s body as an ellipsoid and differentially allocates volumetric growth to length, height and width as a function of the distance between the current shape and characteristic stage-dependent shape attractors (expressed as width/length and height/width ratios). The resulting surface-to-volume ratios mechanistically explain the “metabolic acceleration” often invoked to explain early life growth patterns. We estimated model parameters for three important SPF species in the Benguela upwelling system, using data covering growth at all life-stages, transitions between life-stages, and reproduction. The calibrated models reproduced the observed deviations from isomorphy, with exponential length-dominated growth until metamorphosis, then a shift to height- and width-dominated growth (with a corresponding deceleration of length growth) until the adult shape is reached, and finally isomorphic (characteristic von Bertalanffy) length growth. These deviations from the usual von Bertalanffy growth model could profoundly affect our understanding of larval survival, predator-prey and ecosystem-dynamic

A generalized Dynamic Energy Budget model including 3D shape changes for modeling small pelagic fish growth

Small pelagic fish (SPF) are key components of marine ecosystems, transporting energy from the lower to the upper trophic levels and thereby influencing the dynamics of the entire ecosystem. Understanding their complex growth patterns from early life stages to adulthood is fundamental to accurately predict larval survival and predator-prey dynamics, which are influenced by individual size. However, growth models are generally unable to accurately reproduce the growth acceleration and deceleration phases observed, particularly during early life stages. Here we propose a growth model based on a Dynamic Energy Budget model (modified as in Maury, 2019 to properly account for size-dependence of maintenance) that captures deviations from pure isomorphy. It represents the fish’s body as an ellipsoid and differentially allocates volumetric growth to length, height and width as a function of the distance between the current shape and characteristic stage-dependent shape attractors (expressed as width/length and height/width ratios). The resulting surface-to-volume ratios mechanistically explain the “metabolic acceleration” often invoked to explain early life growth patterns. We estimated model parameters for three important SPF species in the Benguela upwelling system, using data covering growth at all life-stages, transitions between life-stages, and reproduction. The calibrated models reproduced the observed deviations from isomorphy, with exponential length-dominated growth until metamorphosis, then a shift to height- and width-dominated growth (with a corresponding deceleration of length growth) until the adult shape is reached, and finally isomorphic (characteristic von Bertalanffy) length growth. These deviations from the usual von Bertalanffy growth model could profoundly affect our understanding of larval survival, predator-prey and ecosystem-dynamic