Chronotypes-personality behavioural syndromes in wild marine fish.

Chronotypes, the individual differences in daily activity timing, have profound associations with numerous physiological processes. Despite this, the covariance between chronotypes and other aspects of an individual's behaviour has been infrequently explored in non-human animals. This study delves into individual's variation across four axes of personality in a controlled environment, utilising the pearly razorfish, a model species for fish chronotype studies. We identified behavioural types across the aggressiveness continuum and established behavioural syndromes amongst exploration, activity, and boldness, irrespective of body size and condition. Subsequent to this, the experimental subjects were reintroduced to their natural habitat and individually tracked using high-resolution technology to ascertain their chronotypes. Our results revealed that whilst the exploration-activity-boldness syndrome bore no correlation with chronotypes, a significant association was observed between aggressiveness and chronotype. Hence, individuals with later awakening times and rest onsets were more aggressive than their counterparts with earlier awakening times and rest onsets. This study provides pioneering evidence linking fish chronotypes with other behavioural traits, such as aggressiveness, suggesting that behavioural variation could be potentially linked to the individuals' variation in internal clocks and the environmental variables influencing their expression.

Chromosome-level assembly and annotation of the Xyrichtys novacula (Linnaeus, 1758) genome.

The pearly razorfish (Xyrichtys novacula), commonly known as raor in the Balearic Islands, is a wrasse within the family Labridae. This fish species has particular biological and socio-cultural characteristics making it an ideal model organism in the fields of behavioural ecology, molecular ecology and conservation biology. In this study, we present the first annotated chromosome-level assembly for this species. Sequencing involved a combination of long reads with Oxford Nanopore Technologies, Illumina paired-end short reads (2 × 151 bp), Hi-C and RNA-seq from different tissues. The nuclear genome assembly has a scaffold N50 of 34.33 Mb, a total assembly span of 775.53 Mb and 99.63% of the sequence assembled into 24 superscaffolds, consistent with its known karyotype. Quality metrics revealed a consensus accuracy (QV) of 42.92 and gene completeness > 98%. The genome annotation resulted in 26,690 protein-coding genes and 12,737 non-coding transcripts. The coding regions encoded 39,613 unique protein products, 93% of them with assigned function. Overall, the publication of the X. novacula's reference genome will broaden the scope and impact of genomic research conducted on this iconic and colourful species.

Disparate behavioral types in wild and reared juveniles of gilthead seabream.

Fish differ consistently in behavior within the same species and population, reflecting distinct behavioral types (BTs). Comparing the behavior of wild and reared individuals provides an excellent opportunity to delve into the ecological and evolutionary consequences of BTs. In this work, we evaluated the behavioral variation of wild and reared juvenile gilthead seabreams, Sparus aurata, a highly relevant species for aquaculture and fisheries. We quantified behavioral variation along the five major axes of fish behavioral traits (exploration-avoidance, aggressiveness, sociability, shyness-boldness, and activity) using standardized behavioral tests and a deep learning tracking algorithm for behavioral annotation. Results revealed significant repeatability in all five behavior traits, suggesting high consistency of individual behavioral variation across the different axes in this species. We found reared fish to be more aggressive, social and active compared to their wild conspecifics. Reared individuals also presented less variance in their aggressiveness, lacking very aggressive and very tame individuals. Phenotypic correlation decomposition between behavioral types revealed two different behavioral syndromes: exploration-sociability and exploration-activity. Our work establishes the first baseline of repeatability scores in wild and reared gilthead seabreams, providing novel insight into the behavior of this important commercial species with implications for fisheries and aquaculture.

Activity-Rest Circadian Rhythm of the Pearly Razorfish in Its Natural Habitat, before and during Its Mating.

Recent technological advances in marine biotelemetry have demonstrated that marine fish species perform activity-rest rhythms that have relevant ecological and evolutionary consequences. The main objective of the present report is to study the circadian rhythm of activity-rest of the pearly razorfish, Xyrichtys novacula in its own habitat, before and during the reproduction season using a novel biotelemetry system. This fish species is a small-bodied marine species that inhabits most shallow soft habitats of temperate areas and has a high interest for commercial and recreational fisheries. The activity of free-living fish was monitored by means of high-resolution acoustic tracking of the motor activity of the fish in one-minute intervals. The obtained data allowed the definition of the circadian rhythm of activity-rest in terms of classical non-parametric values: interdaily stability (IS), intradaily variability (IV), relative amplitude (RA), average activity during the most-active period of consecutive 10 h (M10), and average activity during the least-active period of consecutive 5 h (L5). We observed a well-marked rhythm, with little fragmentation and good synchrony with the environmental cycle of light-darkness, regardless of sex and the period studied. However, the rhythm was found to be slightly more desynchronized and fragmented during reproduction because of variations in the photoperiod. In addition, we found that the activity of the males was much higher than that of the females (p < 0.001), probably due to the peculiar behavior of the males in defending the harems they lead. Finally, the time at which activity began in males was slightly earlier than it was in females (p < 0.001), presumably due to the same fact, as differences in activity or for the individual heterogeneity of this species in the time of awakening are considered to be an independent axis of the fish's personality. Our work is novel, as it is one of the first studies of activity-rest rhythm using classical circadian-related descriptors in free-living marine fish using locomotory data facilitated by novel technological approaches.

Food determines ephemerous and non-stable gut microbiome communities in juvenile wild and farmed Mediterranean fish.

Novel insights were provided by contrasting the composition of wild and farmed fish gut microbiomes because the latter had essentially different environmental conditions from those in the wild. This was reflected in the gut microbiome of the wild Sparus aurata and Xyrichtys novacula studied here, which showed highly diverse microbial community structures, dominated by Proteobacteria, mostly related to an aerobic or microaerophilic metabolism, but with some common shared major species, such as Ralstonia sp. On the other hand, farmed non-fasted S. aurata individuals had a microbial structure that mirrored the microbial composition of their food source, which was most likely anaerobic, since several members of the genus Lactobacillus, probably revived from the feed and enriched in the gut, dominated the communities. The most striking observation was that after a short fasting period (86 h), farmed gilthead seabream almost lost their whole gut microbiome, and the resident community associated with the mucosa had a very much reduced diversity that was highly dominated by a single potentially aerobic species Micrococcus sp., closely related to M. flavus. The results pointed to the fact that, at least for the juvenile S. aurata studied, most of the microbes in the gut were transient and highly dependent on the feed source, and that only after fasting for at least 2 days could the resident microbiome in the intestinal mucosa be determined. Since an important role of this transient microbiome in relation to fish metabolism could not be discarded, the methodological approach needs to be well designed in order not to bias the results. The results have important implications for fish gut studies that could explain the diversity and occasional contradictory results published in relation to the stability of marine fish gut microbiomes, and might provide important information for feed formulation in the aquaculture industry.

Toward a decade of ocean science for sustainable development through acoustic animal tracking.

The ocean is a key component of the Earth's dynamics, providing a great variety of ecosystem services to humans. Yet, human activities are globally changing its structure and major components, including marine biodiversity. In this context, the United Nations has proclaimed a Decade of Ocean Science for Sustainable Development to tackle the scientific challenges necessary for a sustainable use of the ocean by means of the Sustainable Development Goal 14 (SDG14). Here, we review how Acoustic animal Tracking, a widely distributed methodology of tracking marine biodiversity with electronic devices, can provide a roadmap for implementing the major Actions to achieve the SDG14. We show that acoustic tracking can be used to reduce and monitor the effects of marine pollution including noise, light, and plastic pollution. Acoustic tracking can be effectively used to monitor the responses of marine biodiversity to human-made infrastructures and habitat restoration, as well as to determine the effects of hypoxia, ocean warming, and acidification. Acoustic tracking has been historically used to inform fisheries management, the design of marine protected areas, and the detection of essential habitats, rendering this technique particularly attractive to achieve the sustainable fishing and spatial protection target goals of the SDG14. Finally, acoustic tracking can contribute to end illegal, unreported, and unregulated fishing by providing tools to monitor marine biodiversity against poachers and promote the development of Small Islands Developing States and developing countries. To fully benefit from acoustic tracking supporting the SDG14 Targets, trans-boundary collaborative efforts through tracking networks are required to promote ocean information sharing and ocean literacy. We therefore propose acoustic tracking and tracking networks as relevant contributors to tackle the scientific challenges that are necessary for a sustainable use of the ocean promoted by the United Nations.

Measuring inter-individual differences in behavioural types of gilthead seabreams in the laboratory using deep learning.

Deep learning allows us to automatize the acquisition of large amounts of behavioural animal data with applications for fisheries and aquaculture. In this work, we have trained an image-based deep learning algorithm, the Faster R-CNN (Faster region-based convolutional neural network), to automatically detect and track the gilthead seabream, Sparus aurata, to search for individual differences in behaviour. We collected videos using a novel Raspberry Pi high throughput recording system attached to individual experimental behavioural arenas. From the continuous recording during behavioural assays, we acquired and labelled a total of 14,000 images and used them, along with data augmentation techniques, to train the network. Then, we evaluated the performance of our network at different training levels, increasing the number of images and applying data augmentation. For every validation step, we processed more than 52,000 images, with and without the presence of the gilthead seabream, in normal and altered (i.e., after the introduction of a non-familiar object to test for explorative behaviour) behavioural arenas. The final and best version of the neural network, trained with all the images and with data augmentation, reached an accuracy of 92,79% ± 6.78% [89.24-96.34] of correct classification and 10.25 ± 61.59 pixels [6.59-13.91] of fish positioning error. Our recording system based on a Raspberry Pi and a trained convolutional neural network provides a valuable non-invasive tool to automatically track fish movements in experimental arenas and, using the trajectories obtained during behavioural tests, to assay behavioural types.

Aggressiveness-related behavioural types in the pearly razorfish.

Behavioural types (i.e., personalities or temperament) are defined as among individual differences in behavioural traits that are consistent over time and ecological contexts. Behavioural types are widespread in nature and play a relevant role in many ecological and evolutionary processes. In this work, we studied for the first time the consistency of individual aggressiveness in the pearly razorfish, Xyrichtys novacula, using a mirror test: a classic method to define aggressive behavioural types. The experiments were carried out in semi-natural behavioural arenas and monitored through a novel Raspberry Pi-based recording system. The experimental set up allowed us to obtain repeated measures of individual aggressivity scores during four consecutive days. The decomposition of the phenotypic variance revealed a significant repeatability score (R) of 0.57 [0.44-0.60], suggesting high predictability of individual behavioural variation and the existence of different behavioural types. Aggressive behavioural types emerged irrespective of body size, sex and the internal condition of the individual. Razorfishes are a ubiquitous group of fish species that occupy sedimentary habitats in most shallow waters of temperate and tropical seas. These species are known for forming strong social structures and playing a relevant role in ecosystem functioning. Therefore, our work provides novel insight into an individual behavioural component that may play a role in poorly known ecological and evolutionary processes occurring in this species.

A state-space model to derive motorboat noise effects on fish movement from acoustic tracking data.

Motorboat noise is recognized as a major source of marine pollution, however little is known about its ecological consequences on coastal systems. We developed a State Space Model (SSM) that incorporates an explicit dependency on motorboat noise to derive its effects on the movement of resident fish that transition between two behavioural states (swimming vs. hidden). To explore the performance of our model, we carried out an experiment where free-living Serranus scriba were tracked with acoustic tags, while motorboat noise was simultaneously recorded. We fitted the generated tracking and noise data into our SSM and explored if the noise generated by motorboats passing at close range affected the movement pattern and the probability of transition between the two states using a Bayesian approach. Our results suggest high among individual variability in movement patterns and transition between states, as well as in fish response to the presence of passing motorboats. These findings suggest that the effects of motorboat noise on fish movement are complex and require the precise monitoring of large numbers of individuals. Our SSM provides a methodology to address such complexity and can be used for future investigations to study the effects of noise pollution on marine fish.

Complete mitochondrial genome of the pearly razorfish Xyrichtys novacula: phylogenetic analysis of its placement within the Labridae family.

In this paper, we report the complete mitochondrial genome (17,306 bp) of the pearly razorfish Xyrichtys novacula Linnaeus, 1758, a labrid that inhabits tropical and temperate Atlantic waters and the Mediterranean Sea. The circular double-stranded sequence contains the typical teleost gene order with 13 protein-coding genes, 22 tRNA, 2 rRNA, 1 control region, and 2 intergenic spacers between the rRNAs. Using the sequences of all protein-coding genes, we inferred the phylogeny for the Labriade family using 24 labrids and 3 outgroup species that placed X. novacula in a monophyletic group including species from the Pseudocheilines, Pseudolabrines, and Julidines.

Parent and offspring genotypes influence gene expression in early life.

Parents can have profound effects on offspring fitness. Little, however, is known about the mechanisms through which parental genetic variation influences offspring physiology in natural systems. White-throated sparrows (Zonotrichia albicollis, WTSP) exist in two genetic morphs, tan and white, controlled by a large polymorphic supergene. Morphs mate disassortatively, resulting in two pair types: tan male × white female (T × W) pairs, which provide biparental care and white male × tan female (W × T) pairs, which provide female-biased care. To investigate how parental composition impacts offspring, we performed RNA-seq on whole blood of WTSP nestlings sampled from nests of both pair types. Parental pair type had a large effect on nestling gene expression, with 881 genes differentially expressed (DE) and seven correlated gene coexpression modules. The DE genes and modules expressed at higher levels in W × T nests with female-biased parental care function in metabolism and stress-related pathways resulting from the overrepresentation of proteolysis and stress-response genes (e.g., SOD2, NR3C1). These results show that parental genotypes and/or associated behaviours influence nestling physiology, and highlight avenues of further research investigating the ultimate implications for the maintenance of this polymorphism. Nestlings also exhibited morph-specific gene expression, with 92 differentially expressed genes, comprising immunity genes and genes encompassed by the supergene. Remarkably, we identified the same regulatory hub genes in these blood-derived expression networks as were previously identified in adult WTSP brains (EPM2A, BPNT1, TAF5L). These hub genes were located within the supergene, highlighting the importance of this gene complex in structuring regulatory networks across diverse tissues.

Actuarial senescence in a dimorphic bird: different rates of ageing in morphs with discrete reproductive strategies.

It is often hypothesized that intra-sexual competition accelerates actuarial senescence, or the increase in mortality rates with age. However, an alternative hypothesis is that parental investment is more important to determining senescence rates. We used a unique model system, the white-throated sparrow (Zonotrichia albicollis), to study variation in actuarial senescence. In this species, genetically determined morphs display discrete mating strategies and disassortative pairing, providing an excellent opportunity to test the predictions of the above hypotheses. Compared to tan-striped males, white-striped males are more polygynous and aggressive, and less parental. Tan-striped females receive less parental support, and invest more into parental care than white-striped females, which are also more aggressive. Thus, higher senescence rates in males and white-striped birds would support the intra-sexual competition hypothesis, whereas higher senescence rates in females and tan-striped birds would support the parental investment hypothesis. White-striped males showed the lowest rate of actuarial senescence. Tan-striped females had the highest senescence rate, and tan-striped males and white-striped females showed intermediate, relatively equal rates. Thus, results were inconsistent with sexual selection and competitive strategies increasing senescence rates, and instead indicate that senescence may be accelerated by female-biased parental care, and lessened by sharing of parental duties.

Morph-Specific Patterns of Reproductive Senescence: Connections to Discrete Reproductive Strategies.

How reproductive strategies contribute to patterns of senescence in natural populations remains contentious. We studied reproductive senescence in the dimorphic white-throated sparrow, an excellent species for exploring this issue. Within both sexes the morphs use distinct reproductive strategies, and disassortative pairing by morph results in pair types with distinct parental systems. White morph birds are more colorful and aggressive than tan counterparts, and white males compete for extrapair matings, whereas tan males are more parental. Tan males and white females share parental care equally, whereas white males provide little parental support to tan females. We found morph-specific patterns of reproductive senescence in both sexes. White males exhibited greater reproductive senescence than tan males. This result likely reflects the difficulty of sustaining a highly competitive reproductive strategy as aging progresses rather than high physiological costs of competitiveness, since white males were also long-lived. Moreover, morph was not consistently related to reproductive senescence across the sexes, arguing against especially high costs of the traits associated with white morph identity. Rather, tan females exhibited earlier reproductive senescence than white females and were short-lived, perhaps reflecting the challenges of unsupported motherhood. Results underscore the importance of social dynamics in determining patterns of reproductive senescence.