Figure 1 - available via license: Creative Commons Attribution 4.0 International
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Representative diagram of the behavioural arenas. Behavioural arenas were composed by an aquarium (container where the fish were held captive) connected to the filtering water system through a small sink. The tank contained seawater and sand that served as refuge for the fish. A filtration system was installed behind the tank, consisting of two sponges of different thickness, a biological filtration system and a skimmer responsible for removing the excess of urea. An airstone aerator, a water heater and a water pump were located in the filtration section. The recording system consisted of a Raspberry Pi computer and a Raspberry Pi camera. This system was mounted in front of the aquarium to have a frontal vision during the aggressiveness tests. On the photo, a fish can be seen swimming in an aquarium during the experimental period (diagram by Javier Sanllehi Hansson). Full-size DOI: 10.7717/peerj.10731/fig-1
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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...
Citations
... Indeed, some individuals are intrinsically more aggressive than others and this has been linked to their personality (Briffa et al., 2015). Consistency in aggressiveness over time and context has been detected in numerous marine fish species Martorell-Barceló et al., 2021;Sanllehi Hansson, 2020), and so is considered as PT (Fig. 8.2). Such a stability is tightly linked to the social structure of the group, as this PT might directly impact sociability (Martorell-Barceló et al., 2021) or, on the contrary, would emerge from social interactions (Geffroy et al., 2014). ...
... Consistency in aggressiveness over time and context has been detected in numerous marine fish species Martorell-Barceló et al., 2021;Sanllehi Hansson, 2020), and so is considered as PT (Fig. 8.2). Such a stability is tightly linked to the social structure of the group, as this PT might directly impact sociability (Martorell-Barceló et al., 2021) or, on the contrary, would emerge from social interactions (Geffroy et al., 2014). ...
Like other vertebrates, marine fishes not only exhibit a complex
array of behaviors expressing a certain degree of stability
(i.e., personality traits) but also display some flexibility to
cope with various situations. At the same time, individuals of a population can strongly differ in their behavior and relative differences between individuals can remain constant over time and
contexts: Personality. While environmental conditions
have been proposed to favor one type of behavior
over another, the diversity of the
phenotypes is considered a major component of the capacities
of a population or species to adapt to new environmental
conditions. Hence, the study of the behavior of marine
fishes between and within species can provide incredible
information for better understanding the consequences of
environmental modifications. Here, we review the literature,
focusing on five main Personality Traits: activity, boldness, aggressiveness, sociality, and reproductive behavior
... Similar to other studies in fish (Gatto et al., 2020;Gatto et al., 2021;Martorell-Barceló et al., 2021;Randlett, 2023;Tomihara et al., 2021), we use the low-cost single-board computer Raspberry Pi (Raspberry Zero W) to control electronic components of the setup. It is well suited for researchers with different levels of programming experience and enables users to implement non-proprietary userdefined functionality through Python. ...
... Such a system then could also be coupled to a dedicated camera module (e.g., Raspberry Pi 12MP HQ camera with Sony IMX477R Sensor; Raspberry Pi Ltd, 2023) for onboard video and data acquisition. Examples of use cases integrating video input include work in insects (Cano-Ferrer et al., 2023;Krupa et al., 2021;Tadres et al., 2024a,b;Tadres & Louis, 2020), amphibians (Groffen & Hoskin, 2024), rodents (Centanni & Smith, 2023, Vassilev et al., 2020Benedict & Cudmore, 2023), birds (Hereward et al., 2021), and fish (Signaroli et al., 2022;Todd et al., 2017;Li, Hao, et al., 2022;Li, Wu, et al., 2022;Randlett, 2023;Martorell-Barceló et al., 2021). Following the WIFI remote control documented in this study, such stand-alone systems could be an excellent choice for field work of neurobiological approaches (e.g., Campbell & Jones, 2020;Maia Chagas et al., 2017). ...
Automation of experimental setups is a promising direction in behavioral research because it can facilitate the acquisition of data while increasing its repeatability and reliability. For example, research in spatial cognition can benefit from automated control by systematic manipulation of sensory cues and more efficient execution of training procedures. However, commercial solutions are often costly, restricted to specific platforms, and mainly focused on the automation of data acquisition, stimulus presentation, and reward delivery. Animal welfare considerations as well as experimental demands may require automating the access of an animal or animals to the experimental arena. Here, we provide and test a low‐cost, versatile Raspberry Pi‐based solution for such use cases. We provide four application scenarios of varying complexities, based on our research of spatial orientation and navigation in weakly electric fish, with step‐by‐step protocols for the control of gates in the experimental setups. This easy‐to‐implement, platform‐independent approach can be adapted to various experimental needs, including closed‐loop as well as field experiments. As such, it can contribute to the optimization and standardization of experiments in a variety of species, thereby enhancing the comparability of data.
... Individuals are territorial and males defend smaller female territories within their own from other males (mean size of territories: 88.5 ± 82.2 m 2 for females and 326.1 ± 211.2 m 2 for males). In natural populations, individuals exhibit a diverse range of behaviours, including high aggression (Martorell-Barcel o et al., 2021) and highly exploratory and active spatial behavioural types (Al os et al., 2016). Pearly razorfish also exhibit burrowing behaviour, where individuals emerge from the sand in the morning, forage during the day, and bury themselves in the sand at night to rest and avoid nocturnal predators (Al os et al., 2012). ...
... The others provided data, but these lacked the resolution necessary to derive chronotype information, possibly due to tag malfunction or individual behavioural anomalies stemming from the tagging. The number of individuals used was adjusted to the scope of a larger project that goes beyond the reach of this work (Aspillaga, Arlinghaus, Martorell-Barcel o, Barcelo-Serra, et al., 2021;Aspillaga, Arlinghaus, Martorell-Barcel o, Follana-Bern a, et al., 2021;Barcelo-Serra et al., 2020). ...
... Socially, they form harem-like structures where males defend their territory and the females in it 27 . Different behavioural types have been described in wild populations of pearly razorfish, including spatial-behavioural syndromes 28 and more recently, aggressiveness-related behavioural types under laboratory conditions 29 . Like other razorfish species, pearly razorfish individuals bury themselves in the sand to rest and protect themselves from predators 30 . ...
... The closed-water system facilitated temperature control and aquarium maintenance throughout the experimental period. We placed an EHEIM powerLED+ ® light display on top of each behavioural arena to create optimal light conditions for the pearly razorfish and the recording system (see below), with 12 h of light and 12 h of dark with sunrise set at 7:00 and sunset at 19:00, following Martorell-Barceló et al. 29 . We maintained the water temperature constant at 21 °C (mean and s.d. ...
... Principal component analysis We extracted various behavioural metrics for each of the four laboratory-based traits. To investigate patterns of co-variation among these metrics and identify the ones that best explained each trait, we conducted a Principal Component Analysis (PCA) on the normalised and mean-centred variables following the approach described by Martorell-Barceló et al. 29 . ...
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.
... In our study, a mirror was placed in contact with one side of the behavioral arena, simulating the presence of a conspecific at close range (Table 1). We measured the number of aggressive and hostile "approaches" the fish gave to the mirror per hour by manually visualizing the videos 36,37 . We defined a hostile "approach" as a fast movement with physical contact to the mirror, including instances of attempted biting and the extension of the dorsal fin 36 . ...
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.
... The behavior and social structure of the pearly razorfish suggest that aggression is a critical component of their social interactions and territorial defense. The facts that both males and females exhibit aggressive behavior toward each other and maintain separate territories suggest that aggression is not limited to a specific gender and is, instead, an inherent aspect of their species' behavior [36]. This is a common pattern in many animal species, where individuals may exhibit different levels of aggression depending on their sex, social status, or reproductive state. ...
Simple Summary
Understanding the circadian rhythm of activity–rest in marine fish is essential for comprehending their ecological and evolutionary adaptations. By using a new tracking method to extract locomotory data from free-living marine fish, we have opened up new possibilities for studying the biology, behavior, and ecology of many other species in their natural conditions. Furthermore, this tracking method can help researchers identify how different environmental factors, such as temperature and light, affect the circadian rhythm of activity–rest in marine animals. This information can be used to predict the response of marine animals to changes in their environment and, ultimately, help guide conservation efforts. We found that the activity–rest circadian rhythm of Xyrichtys novacula was well synchronized by the environmental cycle of light–darkness regardless of gender and the period studied. However, the reproductive season caused direct effects on the rhythm, resulting in increased fragmentation and decreased synchronization in both genders.
Abstract
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.
... Many of the causes and consequences of sh BTs have been studied on freshwater shes, mainly on zebra sh, Danio rerio 17 , three-spined stickleback, G. aculeatus 18 , and guppy, Poecilia reticulata 19 . In marine species, consistency in individual behavior has been reported, for example, for two-spotted goby, Gobiusculus avescens 20 , gilthead seabream, Sparus aurata 21 , European seabass, Dicentrarchus labrax 22 and pearly razor sh, Xyrichtys novacula 23,24 . In this study, we examine the degree of consistency of individual behavior in wild and reared samples of juvenile gilthead seabreams. ...
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.
... Video postprocessing has been adduced as one of the major disadvantages of cameras in regard to censuses (Mallet and Pelletier, 2014). However, deep learning algorithms (Connolly et al., 2021;Ditria, 2020;Salman et al., 2019;Tabak et al., 2019) for automatically extracting information from fish images and videos are currently exploding in use (Álvarez-Ellacuría et al., 2019;Connolly et al., 2021;Martorell-Barceló et al., 2021;Moen et al., 2018;Palmer et al., 2022). Some operational (i.e., real-time) applications for counting fish may even be plausible soon (Meng et al., 2018), which may circumvent the memory bottleneck for video storage. ...
Accurate and precise monitoring of the absolute density (i.e., number of fish per area or volume unit) of exploited fish stocks would be strongly advisable for deriving stock status and for designing proper management plans. Moreover, monitoring should be achieved at relevant (i.e., sufficiently large) temporal and spatial scales. This objective is particularly challenging for data-poor fisheries, as is often the case for recreational fisheries. Therefore, the feasibility of underwater video monitoring (vertical unbaited cameras) for estimating, as a proof of concept, the absolute density (and its ecological drivers) of a coastal sedentary fish species is demonstrated. The absolute density of a small serranid (Serranus scriba) targeted by recreational fishing was estimated along the southern coast of Mallorca Island (nearly 100 km). The median fish density ranged between 111 ind/km² (Es Molinar) and 14,110 ind/km² (Cabrera). Absolute density was correlated with fishing exposure, habitat, and depth. Site specific, seemingly long-term, effects of fishing exposure were negatively correlated with fish density, but short-term effects (assessed by the interaction between fishing exposure and before/after the season when recreational fishing occurred in the study area) were not detected. We suggest that the short-term effects of fishing may remain undetected because highly exploited sites could contain fish that are already not vulnerable to recreational fishing gear, irrespective of the short-term fishing pressure exerted. Such a process may explain some hyper-depletion patterns and should preclude the use of fisheries-dependent data for monitoring fish density. The results reported here indicate that monitoring fish abundance with vertical unbaited cameras at large spatial and temporal scales can be a reliable alternative for many species.
Most organisms synchronize to an approximately 24-hour (circadian) rhythm. This study introduces a novel deep learning-powered video tracking method to assess the stability, fragmentation, robustness and synchronization of activity rhythms in Xyrichtys novacula. Experimental X. novacula were distributed into three groups and monitored for synchronization to a 14/10 hours of light/dark to assess acclimation to laboratory conditions. Group GP7 acclimated for 1 week and was tested from days 7 to 14, GP14 acclimated for 14 days and was tested from days 14 to 21 and GP21 acclimated for 21 days and was tested from days 21 to 28. Telemetry data from individuals in the wild depicted their natural behavior. Wild fish displayed a robust and minimally fragmented rhythm, entrained to the natural photoperiod. Under laboratory conditions, differences in activity levels were observed between light and dark phases. However, no differences were observed in activity rhythm metrics among laboratory groups related to acclimation period. Notably, longer acclimation (GP14 and GP21) led to a larger proportion of individuals displaying rhythm synchronization with the imposed photoperiod. Our work introduces a novel approach for monitoring biological rhythms in laboratory conditions, employing a specifically engineered video tracking system based on deep learning, adaptable for other species.
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.
