Biology subjects

Paula, J. R.

Publications and source records attributed to Paula, J. R..

10 recordsLinked to original sources

bioRxiv2026

Early-Life Exposure to Warming Enhances Sea Urchin Heatwave Tolerance but Fails under Extreme Stress

The exposure to environmental stressors early in life can shape organisms to express more tolerant phenotypes to the same conditions during adulthood, a process called developmental plasticity. However, this acquired acclimation ability might depend on the intensity of the stimulus perceived later in life. Here, we took advantage of a purple sea urchin Paracentrotus lividus population developed at abnormally high sea temperature in the proximity of a power plant to test the limits of their developmentally acquired plasticity to increased water temperature. We simulated two marine heatwaves, a category I (moderate) and IV (extreme), and exposed the power plant population as well as a naive population developed in natural sea conditions. We measured their respiration rate and molecular responses to these two heatwaves. Regardless of the population of origin, sea urchins exposed to heatwaves showed higher oxygen consumption, indicating an increase in metabolic rates. At the molecular level, the biggest difference between the two populations was found following the moderate heatwave. Compared to the developmentally acclimated sea urchins, the naive population expressed genes coding for proteins with stress response, chromatin remodeling and RNA splicing functions, while suppressing immune response, revealing that developmental exposures can aid in priming the responses of adults to moderate temperature increases. However, a stronger heatwave leveled the differences between the two populations, with sea urchins from both locations expressing genes involved in proteostasis and detoxification. Nevertheless, regardless of the simulated marine heatwave intensity, sea urchins from the naive population always showed enrichment of the spliceosome pathway compared to power plant urchins, which activated immune response genes instead, reflecting fundamentally different thermal stress-coping strategies shaped by their developmental environments. Overall, our results demonstrate the critical yet context-dependent role of developmental plasticity in shaping the resilience of marine ectotherms to climate change.

evolutionary biology↗

bioRxiv2025

Interspecific variation in cleaning behaviour and honesty among cleaner wrasses

Mutualism is an interspecific interaction in which both partners gain a net fitness benefit. However, mutualisms are vulnerable to conflict because one partner may increase its benefits at the others expense (cheating). In coral reef cleaning mutualisms, cleaner fishes may cheat by feeding on client mucus rather than ectoparasites, imposing costs on clients and potentially destabilising cooperation. Here, using a standardised experimental framework, we examined cheating behaviour, measured via client jolts as a proxy, in four dedicated (relying on cleaning for sustenance) and three non-dedicated (opportunistic) cleaner fish using an interaction test with three client types (predatory, visitor and resident), and the bystander test, to evaluate potential behavioural changes in the presence of a bystander. When exposed to the same standardised social stimuli, dedicated cleaners responded differently across species, showing pronounced interspecific variation in both interaction time and client jolt frequency, whereas non-dedicated cleaners showed broadly uniform behavioural profiles with rare client jolts. Although captive interactions produced generally lower jolt rates than those typically reported in the wild, cleaner responses still differed across client types, suggesting context-dependent shifts in investment and exploitation with client identity. Bystander effects were weak overall; however, Labroides bicolor significantly reduced jolt expression when a bystander was present, suggesting that reputation-related adjustment may be species-specific. These findings highlight the capacity of cleaner species to respond differently to the same social environment, revealing species-specific behavioural strategies with potential consequences for mutualism stability and the selective pressures shaping cooperation-exploitation trade-offs.

animal behavior and cognition↗

bioRxiv2025

Using supervised machine learning to quantify cleaning behaviour

Cleaner fish engage in mutualistic interactions by removing ectoparasites from client species, a behaviour that has traditionally been quantified through labour-intensive manual video analysis. This method is not only time-consuming but also susceptible to human error and bias. In this study, we developed a semi-automated system to track and classify cleaning interactions between the cleaner wrasse (Labroides dimidiatus) and the powder blue tang (Acanthurus leucosternon) in a controlled three-dimensional laboratory setting. We employed DeepLabCut (DLC), a deep learning-based tool for markerless pose estimation, to track both fish species simultaneously. The resulting model reliably tracked both individuals with low error rates. Using the tracking data, we designed a classification algorithm that detected cleaning interactions with 90% accuracy. Although the algorithm misclassified approximately 15% of non-interactions as interactions, it successfully identified 25% of video content as containing interactions, thereby reducing the amount of footage requiring manual annotation by 75%. This approach significantly decreases human labour while maintaining high classification performance. Overall, our system represents a valuable step toward automating behavioural analysis in marine mutualisms and can serve as a foundation for broader applications in ethology and conservation research.

animal behavior and cognition↗

bioRxiv2024

Developmental and transcriptomic responses of Hawaiian bobtail squid early stages to ocean warming and acidification

1Cephalopods play a central ecological role across all oceans and realms. However, under the current climate crisis, their physiology and behaviour are impacted, and we are beginning to comprehend the effects of environmental stressors at a molecular level. Here, we study the Hawaiian bobtail squid (Euprymna scolopes), known for its specific binary symbiosis with the bioluminescent bacterium Vibrio fischeri acquired post-hatching. We aim to understand the response (i.e., developmental and molecular) of E. scolopes after the embryogenetic exposure to different conditions: i) standard conditions (control), ii) increased CO2 ({Delta}pH 0.4 units), iii) warming (+3{o}C), or iv) a combination of the two treatments. We observed a decrease in hatching success across all treatments relative to the control. Using transcriptomics, we identified a potential trade-off in favour of metabolism and energy production, at the expense of development under increased CO2. In contrast, elevated temperature shortened the developmental time and, at a molecular level, showed signs of alternative splicing and the potential for RNA editing. The data also suggest that the initiation of the symbiosis may be negatively affected by these environmental drivers of change in the biosphere, although coping mechanisms by the animal may occur.

ecology↗

bioRxiv2024

Cleaner gobies can solve a biological market task when the correct cue is larger

Animal cognition is deeply influenced by interactions with the environment. A notable example of sophisticated cognition in the animal kingdom is described by the mutualistic relationship between cleaner fish and clients, where decision-making processes play a pivotal role in partner choice and fish survival. In this context, while extensive research has explored the cognition of the cleaner wrasse Labroides dimidiatus, its Caribbean counterparts, Elacatinus spp., have been comparatively inadequately evaluated. In this study, we used plexiglass plates as surrogates for clients and assessed the ability of cleaner gobies, Elacatinus oceanops, to solve a biological market task where prioritising an ephemeral food plate over a permanent one would double the food reward. We varied cue-based decision-making using both ecologically relevant cues (plate size and colour) and non-relevant ones (presentation side). Additionally, we tested their capacity for reversal learning, an indicator of complex cognitive abilities. Notably, cleaner gobies were able to solve the biological markets task when the distinguishing cue was a larger plate size. Given that these gobies tend to prioritise larger predatory clients in nature, our results align with their natural inclination. Furthermore, considering these gobies were bred in captivity and never experienced cleaning interactions in their lifetime, our data might suggest that their intrinsic cognitive abilities are shaped by evolutionary pressures rooted in their ecological roles. In essence, even in the absence of direct ecological interactions, innate cognitive abilities in cleaner gobies seem to be deeply influenced by evolutionary forces tied to their natural ecological functions. However, their inability to solve the same task involving other cues, may be influenced by factors such as captivity-reared fish or limitations in the experimental design. Further research, including wild individuals, is essential to elucidate the cognitive abilities of the studied species and its implications in the ecological context and evolutionary history.

animal behavior and cognition↗

bioRxiv2024

Sickness behaviour within cleaning interactions

When facing diseases, strategies such as social distancing have proven effective in preventing disease spread. Cleaning interactions are social interactions where cleaner organisms remove ectoparasites from clients. These interactions can be potential vectors of infectious diseases in reef fishes. Here, we aimed to determine if cleaner wrasses (Labroides dimidiatus) employ social distancing and other behavioural tactics to prevent disease spread within the context of cleaning interactions. To this end, we used bacterial lipopolysaccharides (LPS) immunostimulation to induce "sickness" behaviour in cleaners. After LPS injection, we performed four behavioural trials: social preference (from cleaner and client perspectives), social interaction, and bystander cooperativeness tests. In the social preference test, LPS-injected cleaners showed lower activity rates but no change in their social preference. However, some clients preferred "sick" cleaners. Contrarily, during the social interaction test, cleaners reduced the number of interactions, despite clients willingness to interact. For the bystander test, LPS-injected cleaners were unable to adjust their behaviour to be more cooperative. Reduced activity levels revealed lethargy, which may lead to passive self-isolation, allowing for some social distancing of healthy individuals. This suggests that immune-stimulated cleaners undergo changes in their behaviour which can be viewed as a passive social distancing preventing disease spread.

animal behavior and cognition↗

bioRxiv2023

Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions

Mutualistic interactions, which constitute some of the most advantageous interactions among fish species, are highly vulnerable to environmental changes. A key mutualistic interaction is the cleaning service rendered by the cleaner wrasse, Labroides dimidiatus, which involves intricate processes of social behaviour to remove ectoparasites from client fish and can be altered in near-future environmental conditions. Here, we evaluated the neuromolecular mechanisms behind the behavioural disruption of cleaning interactions in response to future environments. We subjected cleaner wrasses and surgeonfish (Acanthurus leucosternon, serving as clients) to elevated temperature (Warming, 32{degrees}C), increased levels of CO2 (High CO2, 1000 ppm), and a combined condition of elevated CO2 and temperature (Warming & High CO2, 32{degrees}C & 1000 ppm) for 28 days. Each of these conditions resulted in behavioural disruptions concerning the motivation to interact and the quality of interaction (High CO2 -80.7%, Warming - 92.6%, Warming & High CO2 -79.5%, p<0.001). Using transcriptomic of the fore-, mid-, and hindbrain, we discovered that most transcriptional reprogramming in both species under warming conditions occurred primarily in the hind- and forebrain. The associated functions under warming were linked to stress, heat shock proteins, hypoxia, and behaviour. In contrast, elevated CO2 exposure affected a range of functions associated with GABA, behaviour, visual perception, and circadian rhythm. Interestingly, in the combined Warming & High CO2 condition, we did not observe any expression changes of behaviour. However, we did find signs of endoplasmic reticulum stress and apoptosis, suggesting not only an additive effect of the environmental conditions but also a trade-off between physiological performance and behaviour in the cleaner wrasse. We suggest that impending environmental shifts can affect the behaviour and molecular processes that sustain mutualistic interactions between L. dimidiatus and its clients, which could have a cascading effect on their adaptation potential and possibly cause large-scale impacts on coral reef ecosystems.

animal behavior and cognition↗

bioRxiv2023

Oxygen loss compromises the survival and cognition of a coastal cephalopod

The ocean is undergoing deoxygenation and the spread of hypoxic areas. Ocean deoxygenation and standing levels of hypoxia are shrinking fundamental niches, particularly in coastal areas, yet documented repercussions on species development and behavior are limited. Here, we tackled the impacts of deoxygenation (7 mg O2 L-1), mild hypoxia (nocturnal 5 mg O2 L-1), and severe hypoxia (2 mg O2 L-1) on cuttlefish (Sepia officinalis) development (hatching success, development time, mantle length) and behavior, i.e., ability to learn (associative-and socially), to camouflage, and to explore its surroundings spatially. We found that hypoxia yielded lower survival rates, smaller body sizes and inhibited predatory (increased latency to attack the prey) and anti-predator (camouflage) behaviors. Acute and chronic exposure to low oxygen produced similar effects on cognition (inability to socially learn, increased open-field activity levels, no changes in thigmotaxis). It is thus expected that, although cuttlefish can withstand oxygen limitation to a certain degree, expanding hypoxic zones will diminish current habitat suitability.

animal behavior and cognition↗

bioRxiv2023

Transgenerational exposure to deoxygenation and warming disrupts mate-detection in Gammarus locusta

Ocean deoxygenation and warming have been shown to pose a growing threat to the health of marine organisms and ecosystems. Yet, the potential for acclimation and adaptation to these threats remains poorly understood. The aim of this study was to evaluate the effects of transgenerational exposure to reduced oxygen availability and elevated seawater temperature on the chemosensory-dependent mating mechanisms of male amphipods Gammarus locusta. After exposure, the number of individuals that reached adulthood (in F0 and F2) was gauged, and adult males from F0 and F1 were subjected to behavioral trials to assess their capacity of long-distance female cue detection through quantification of (i) response time; (ii) first direction of movement; (iii) activity rate and (iv) proportion of time spent in female scent cues. Ocean warming induced mortality (especially in F2), and reduced oxygen availability had adverse effects on each of the investigated behavioral traits, which were amplified when combined with elevated temperature. Still, when compared to F0, the F1 generation demonstrated more adaptability (i.e., higher activity rate and preference for female odors) to the combination of the two stressors, suggesting positive carry-over effects. Nevertheless, full recovery to control levels was not observed. Altogether, this study indicates that future scenarios of ocean deoxygenation and warming have the potential to disrupt chemosensory-dependent mate-detection in amphipods, but also suggests possible behavioral adaptations. We call for greater research efforts on long-term impacts of ocean change on the behavioral and physiological processes of benthic coastal communities.

ecology↗

bioRxiv2021

Neuro-molecular characterization of fish cleaning interactions

Coral reef fish exhibit a large variety of behaviours crucial for fitness and survival. The cleaner wrasse Labroides dimidiatus displays cognitive abilities during interspecific interactions by providing services of ectoparasite cleaning, thus serving as a good example to understand the processes of complex social behaviour. However, little is known about the molecular underpinnings of cooperative behaviour between L. dimidiatus and a potential client fish (Acanthurus leucosternon). Therefore, we investigated the molecular mechanisms in three regions of the brain (fore-, mid-, and hindbrain) during the interaction of these fishes. Here we show, using transcriptomics, that most of the transcriptional response in both species was regulated in the hindbrain and forebrain regions and that the interacting behaviour responses of L. dimidiatus involved immediate early gene alteration, dopaminergic and glutamatergic pathways, the expression of neurohormones (such as isotocin) and steroids (e.g. progesterone and estrogen). In contrast, in the client, fewer molecular alterations were found, mostly involving pituitary hormone responses. The particular pathways found suggested learning and memory processes in the cleaner wrasse, while the client indicated stress relief.

animal behavior and cognition↗