Inhibitory learning of phototaxis by honeybees in a passive-avoidance task.

Honeybees are a standard model for the study of appetitive learning and memory. Yet, fewer attempts have been performed to characterize aversive learning and memory in this insect and uncover its molecular underpinnings. Here, we took advantage of the positive phototactic behavior of bees kept away from the hive in a dark environment and established a passive-avoidance task in which they had to suppress positive phototaxis. Bees placed in a two-compartment box learned to inhibit spontaneous attraction to a compartment illuminated with blue light by associating and entering into that chamber with shock delivery. Inhibitory learning resulted in an avoidance memory that could be retrieved 24 h after training and that was specific to the punished blue light. The memory was mainly operant but involved a Pavlovian component linking the blue light and the shock. Coupling conditioning with transcriptional analyses in key areas of the brain showed that inhibitory learning of phototaxis leads to an up-regulation of the dopaminergic receptor gene Amdop1 in the calyces of the mushroom bodies, consistently with the role of dopamine signaling in different forms of aversive learning in insects. Our results thus introduce new perspectives for uncovering further cellular and molecular underpinnings of aversive learning and memory in bees. Overall, they represent an important step toward comparative learning studies between the appetitive and the aversive frameworks.

Solutions for ecosystem-level protection of ocean systems under climate change.

The Paris Conference of Parties (COP21) agreement renewed momentum for action against climate change, creating the space for solutions for conservation of the ocean addressing two of its largest threats: climate change and ocean acidification (CCOA). Recent arguments that ocean policies disregard a mature conservation research field and that protected areas cannot address climate change may be oversimplistic at this time when dynamic solutions for the management of changing oceans are needed. We propose a novel approach, based on spatial meta-analysis of climate impact models, to improve the positioning of marine protected areas to limit CCOA impacts. We do this by estimating the vulnerability of ocean ecosystems to CCOA in a spatially explicit manner and then co-mapping human activities such as the placement of renewable energy developments and the distribution of marine protected areas. We test this approach in the NE Atlantic considering also how CCOA impacts the base of the food web which supports protected species, an aspect often neglected in conservation studies. We found that, in this case, current regional conservation plans protect areas with low ecosystem-level vulnerability to CCOA, but disregard how species may redistribute to new, suitable and productive habitats. Under current plans, these areas remain open to commercial extraction and other uses. Here, and worldwide, ocean conservation strategies under CCOA must recognize the long-term importance of these habitat refuges, and studies such as this one are needed to identify them. Protecting these areas creates adaptive, climate-ready and ecosystem-level policy options for conservation, suitable for changing oceans.

Impact of temperature on Downs herring (Clupea harengus) embryonic stages: First insights from an experimental approach.

Among all human-induced pressures, ocean warming is expected to be one of the major drivers of change in marine ecosystems. Fish species are particularly vulnerable during embryogenesis. Here, the impact of temperature was assessed on embryonic stages of Atlantic herring (Clupea harengus), a species of high socio-economic interest, with a particular focus on the under-studied eastern English Channel winter-spawning component (Downs herring). Key traits linked to growth and development were experimentally evaluated at three temperatures (8°C, 10°C and 14°C), from fertilization to hatching, in standardized controlled conditions. Overall negative impacts of increased temperature were observed on fertilization rate, mean egg diameter at eyed stage, hatching rate and yolk sac volume. A faster developmental rate and a change in development stage frequency of newly hatched larvae were also observed at higher temperature. Potential parental effects were detected for four key traits (i.e. fertilization rate, eyed survival rate, mean egg diameter and hatching rate), despite a limited number of families. For instance, a large variability among families was shown in survival rate at eyed stage (between 0 and 63%). Potential relationships between maternal characteristics and embryo traits were therefore explored. We show that a substantial proportion of variance (between 31 and 70%) could be explained by the female attributes considered. More particularly, age, traits linked to life history (i.e. asymptotic average length and Brody growth rate coefficient), condition and length were important predictors of embryonic key traits. Overall, this study constitutes a stepping-stone to investigate potential consequences of warming on Downs herring recruitment and provides first insights on potential parental effects.

A behavioral tagging account of kinase contribution to memory formation after spaced aversive training.

Long-term memory (LTM) can be induced by repeated spaced training trials. Using the weak inhibitory avoidance (wIA) task, we showed that one wIA session does not lead to a 24-h LTM, whereas two identical wIA sessions spaced by 15 min to 6 h induce a 24-h LTM. This LTM promotion depends both on hippocampal protein synthesis and the activity of several kinases. In agreement with the behavioral tagging (BT) hypothesis, our results suggest that the two training sessions induce transient learning tags and lead, via a cooperative effect, to the synthesis of plasticity-related proteins (PRPs) that become available and captured by the tag from the second session. Although ERKs1/2 are needed for PRPs synthesis and CaMKs are required for tag setting, PKA participates in both processes. We conclude that the BT mechanism accounts for the molecular constraints underlying the classic effect of spaced learning on LTM formation.

Inferences to estimate consumer's diet using stable isotopes: Insights from a dynamic mixing model.

Stable isotope ratios are used to reconstruct animal diet in trophic ecology via mixing models. Several assumptions of stable isotope mixing models are critical, i.e., constant trophic discrimination factor and isotopic equilibrium between the consumer and its diet. The isotopic turnover rate (λ and its counterpart the half-life) affects the dynamics of isotopic incorporation for an organism and the isotopic equilibrium assumption: λ involves a time lag between the real assimilated diet and the diet estimated by mixing models at the individual scale. Current stable isotope mixing model studies consider neither this time lag nor even the dynamics of isotopic ratios in general. We developed a mechanistic framework using a dynamic mixing model (DMM) to assess the contribution of λ to the dynamics of isotopic incorporation and to estimate the bias induced by neglecting the time lag in diet reconstruction in conventional static mixing models (SMMs). The DMM includes isotope dynamics of sources (denoted δs), λ and frequency of diet-switch (ω). The results showed a significant bias generated by the SMM compared to the DMM (up to 50% of differences). This bias can be strongly reduced in SMMs by averaging the isotopic variations of the food sources over a time window equal to twice the isotopic half-life. However, the bias will persist (∼15%) for intermediate values of the ω/λ ratio. The inferences generated using a case study highlighted that DMM enhanced estimates of consumer's diet, and this could avoid misinterpretation in ecosystem functioning, food-web structure analysis and underlying biological processes.

Redefining Single-Trial Memories in the Honeybee.

Research on honeybee memory has led to a widely accepted model in which a single pairing of an odor stimulus with sucrose induces memories that are independent of protein synthesis but is unable to form protein-synthesis-dependent long-term memory (LTM). The latter is said to arise only after three or more pairings of odor and sucrose. Here, we show that this model underestimates the capacity of the bee brain to form LTMs after a unique appetitive experience. Using state-of-the art conditioning setups and individual-based analyses of conditioned responses, we found that protein-synthesis-dependent memories are formed already 4 h after the single conditioning trial and persist even 3 days later. These memories (4 h, 24 h, and 72 h) exhibit different dependencies on transcription and translation processes. Our results thus modify the traditional view of one-trial memories in an insect with a model status for memory research.

Seasonal and ontogenetic variation of whiting diet in the Eastern English Channel and the Southern North Sea.

An accurate description of trophic interactions is crucial to understand ecosystem functioning and sustainably manage marine ecosystems exploitation. Carbon and nitrogen stable isotopes were coupled with stomach content analyses to investigate whiting (Merlangius merlangus, Linnaeus, 1758) feeding behavior in the Eastern English Channel and Southern North Sea. Whiting juveniles and adults were sampled in autumn and winter to investigate both ontogenetic and seasonal changes. In addition, queen scallops (Aequipecten opercularis) samples were collected along with fish to be used as isotopic benthic baseline. Results indicated an ontogenetic diet change from crustaceans to fish and cephalopods. In autumn, δ15N values generally increased with fish size while in winter, a decrease of δ15N values with fish size was observed, as a potential result of spatial variation in baseline δ15N values. In winter, a nutrient-poor period, an increase in feeding intensity was observed, especially on the copepod Temora longicornis. This study provides further insights into whiting trophic ecology in relation to ontogenetic and seasonal variations, and it confirms the importance of combining several trophic analysis methods to understand ecosystem functioning.

Spatial-Memory Formation After Spaced Learning Involves ERKs1/2 Activation Through a Behavioral-Tagging Process.

The superiority of spaced over massed learning is an established fact in the formation of long-term memories (LTM). Here we addressed the cellular processes and the temporal demands of this phenomenon using a weak spatial object recognition (wSOR) training, which induces short-term memories (STM) but not LTM. We observed SOR-LTM promotion when two identical wSOR training sessions were spaced by an inter-trial interval (ITI) ranging from 15 min to 7 h, consistently with spaced training. The promoting effect was dependent on neural activity, protein synthesis and ERKs1/2 activity in the hippocampus. Based on the "behavioral tagging" hypothesis, which postulates that learning induces a neural tag that requires proteins to induce LTM formation, we propose that retraining will mainly retag the sites initially labeled by the prior training. Thus, when weak, consecutive training sessions are experienced within an appropriate spacing, the intracellular mechanisms triggered by each session would add, thereby reaching the threshold for protein synthesis required for memory consolidation. Our results suggest in addition that ERKs1/2 kinases play a dual role in SOR-LTM formation after spaced learning, both inducing protein synthesis and setting the SOR learning-tag. Overall, our findings bring new light to the mechanisms underlying the promoting effect of spaced trials on LTM formation.

Ontogenetic shift in the energy allocation strategy and physiological condition of larval plaice (Pleuronectes platessa).

Condition indices aim to evaluate the physiological status of fish larvae by estimating both the level of starvation and potential of survival. Histological indices reveal direct effects of starvation whereas biochemical indices such as lipid classes or RNA:DNA ratios are used as proxies of condition, giving information on the amount of energy reserves and growth rate, respectively. We combined these three indices to evaluate ontogenetic variations of growth performance, lipid dynamics and nutritional condition of plaice larvae caught in the field during winter 2017 in the eastern English Channel and the Southern Bight of the North Sea. RNA:DNA ratios showed that larvae at the beginning of metamorphosis (stage 4) had a lower growth rate than younger individuals (stages 2 and 3). A significant increase in the proportion of triglycerides also occurred at stage 4, indicating energy storage. Histological indices indicated that most of the larvae were in good condition, even younger ones with low lipid reserves. There was, however, an increase in the proportion of healthy individuals over ontogeny, especially with respect to liver vacuoles which were larger and more numerous for stage 4 larvae. Combined together, these condition indices revealed the ontogenetic shift in the energy allocation strategy of plaice larvae. Young larvae (stages 2 and 3) primarily allocate energy towards somatic growth. The decrease in growth performance for stage 4 was not related to poor condition, but linked to a higher proportion of energy stored as lipids. Since the quantity of lipid reserves is particularly important for plaice larvae to withstand starvation during metamorphosis, this could be considered as a second critical period after the one of exogenous feeding for larval survival and recruitment success.

Daily changes in the electric behavior of weakly electric fish naturally persist in constant darkness and are socially synchronized.

Daily rhythms allow anticipation of changes and allocation of energy to better cope with predictable events. Rhythms in behavior result from a complex combination of physiological processes timed by the nervous system and synchronized with external information. We aimed to understand how rhythmic behaviors arise in nature, when weakly electric fish are exposed to cyclic environmental influences and social context. Gymnotus omarorum is a South American nocturnal pulse-type gymnotiform. Its electric behavior encodes information about species, sex and physiological state. The rate of emission of the electric organ discharge (EOD-BR) is modulated by exploratory activity and by physical and social environmental stimuli. We show that the EOD-BR increases during the night in the natural habitat even in individuals maintained in constant dark conditions. Locomotor activity is higher at night, however the nocturnal increase of EOD-BR still occurs in motionless fish, demonstrating an independent origin for the locomotor and electric components of exploratory behavior. When fish are observed in nature, social context exerts a synchronizing role on electric behavior. G. omarorum emerges as an exciting wild model for the study of daily rhythms arising in the complexity of the real world, integrating environmental, physical and social cues in the modulation of rhythmic behavior.

A Climate-Driven Functional Inversion of Connected Marine Ecosystems.

Sustainably managing natural resources under climate change requires understanding how species distribution shifts can impact ecosystem structure and functioning. While numerous studies have documented changes in species' distributions and abundances in response to warming [1, 2], the consequences for the functional structure of ecosystems (i.e., composition of species' functional traits) have received less attention. Here, using thirty years of fish monitoring, we show that two connected North Atlantic ecosystems (E. English Channel and S. North Sea) underwent a rapid shift in functional structure triggered by a climate oscillation to a prevailing warm-phase in the late-1990s. Using time-lag-based causality analyses, we found that rapid warming drove pelagic fishes with r-selected life history traits (e.g., low age and size at maturity, small offspring, low trophic level) to shift abruptly northward from one ecosystem to the other, causing an inversion in functional structure between the two connected ecosystems. While we observed only a one-year time-lag between the climate oscillation and the functional shift, indicating rapid responses to a changing environment, historical overfishing likely rendered these ecosystems susceptible to climatic stress [3], and declining fishing in the North Sea may have exacerbated the shift. This shift likely had major consequences for ecosystem functioning due to potential changes in biomass turnover, nutrient cycling, and benthic-pelagic coupling [4-6]. Under ongoing warming, climate oscillations and extreme warming events may increase in frequency and severity [7, 8], which could trigger functional shifts with profound consequences for ecosystem functioning and services.

Adaptive responses of tropical tuna purse-seiners under temporal regulations.

The failure to achieve fisheries management objectives has been broadly discussed in international meetings. Measuring the effects of fishery regulations is difficult due to the lack of detailed information. The yellowfin tuna fishery in the eastern Pacific Ocean offers an opportunity to evaluate the fishers' responses to temporal regulations. We used data from observers on-board Mexican purse-seine fleet, which is the main fleet fishing on dolphin-associated tuna schools. In 2002, the Inter-American Tropical Tuna Commission implemented a closed season to reduce fishing effort for this fishery. For the period 1992-2008, we analysed three fishery indicators using generalized estimating equations to evaluate the fishers' response to the closure. We found that purse-seiners decreased their time spent in port, increased their fishing sets, and maintained their proportion of successful fishing sets. Our results highlight the relevance of accounting for the fisher behaviour to understand fisheries dynamics when establishing management regulations.

Fishing for space: fine-scale multi-sector maritime activities influence fisher location choice.

The European Union and other states are moving towards Ecosystem Based Fisheries Management to balance food production and security with wider ecosystem concerns. Fishing is only one of several sectors operating within the ocean environment, competing for renewable and non-renewable resources that overlap in a limited space. Other sectors include marine mining, energy generation, recreation, transport and conservation. Trade-offs of these competing sectors are already part of the process but attempts to detail how the seas are being utilised have been primarily based on compilations of data on human activity at large spatial scales. Advances including satellite and shipping automatic tracking enable investigation of factors influencing fishers' choice of fishing grounds at spatial scales relevant to decision-making, including the presence or avoidance of activities by other sectors. We analyse the determinants of English and Welsh scallop-dredging fleet behaviour, including competing sectors, operating in the eastern English Channel. Results indicate aggregate mining activity, maritime traffic, increased fishing costs, and the English inshore 6 and French 12 nautical mile limits negatively impact fishers' likelihood of fishing in otherwise suitable areas. Past success, net-benefits and fishing within the 12 NM predispose fishers to use areas. Systematic conservation planning has yet to be widely applied in marine systems, and the dynamics of spatial overlap of fishing with other activities have not been studied at scales relevant to fisher decision-making. This study demonstrates fisher decision-making is indeed affected by the real-time presence of other sectors in an area, and therefore trade-offs which need to be accounted for in marine planning. As marine resource extraction demands intensify, governments will need to take a more proactive approach to resolving these trade-offs, and studies such as this will be required as the evidential foundation for future seascape planning.

Supporting fisheries management by means of complex models: can we point out isles of robustness in a sea of uncertainty?

Ecosystems are usually complex, nonlinear and strongly influenced by poorly known environmental variables. Among these systems, marine ecosystems have high uncertainties: marine populations in general are known to exhibit large levels of natural variability and the intensity of fishing efforts can change rapidly. These uncertainties are a source of risks that threaten the sustainability of both fish populations and fishing fleets targeting them. Appropriate management measures have to be found in order to reduce these risks and decrease sensitivity to uncertainties. Methods have been developed within decision theory that aim at allowing decision making under severe uncertainty. One of these methods is the information-gap decision theory. The info-gap method has started to permeate ecological modelling, with recent applications to conservation. However, these practical applications have so far been restricted to simple models with analytical solutions. Here we implement a deterministic approach based on decision theory in a complex model of the Eastern English Channel. Using the ISIS-Fish modelling platform, we model populations of sole and plaice in this area. We test a wide range of values for ecosystem, fleet and management parameters. From these simulations, we identify management rules controlling fish harvesting that allow reaching management goals recommended by ICES (International Council for the Exploration of the Sea) working groups while providing the highest robustness to uncertainties on ecosystem parameters.