Marta C. Soares

Hormonal mechanisms of cooperative behaviour

Research on the diversity, evolution and stability of cooperative behaviour has generated a considerable body of work. As concepts simplify the real world, theoretical solutions are typically also simple. Real behaviour, in contrast, is often much more diverse. Such diversity, which is increasingly acknowledged to help in stabilizing cooperative outcomes, warrants detailed research about the proximate mechanisms underlying decision-making. Our aim here is to focus on the potential role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviour in vertebrates. We first provide a brief introduction into the neuroendocrine basis of social behaviour. We then evaluate how hormones may influence known cognitive modules that are involved in decision-making processes that may lead to cooperative behaviour. Based on this evaluation, we will discuss specific examples of how hormones may contribute to the variability of cooperative behaviour at three different levels: (i) within an individual; (ii) between individuals and (iii) between species. We hope that these ideas spur increased research on the behavioural endocrinology of cooperation.

Tactile stimulation lowers stress in fish

In humans, physical stimulation, such as massage therapy, reduces stress and has demonstrable health benefits. Grooming in primates may have similar effects but it remains unclear whether the positive effects are due to physical contact or to its social value. Here we show that physical stimulation reduces stress in a coral reef fish, the surgeonfish Ctenochaetus striatus. These fish regularly visit cleaner wrasses Labroides dimidiatus to have ectoparasites removed. The cleanerfish influences client decisions by physically touching the surgeonfish with its pectoral and pelvic fins, a behaviour known as tactile stimulation. We simulated this behaviour by exposing surgeonfish to mechanically moving cleanerfish models. Surgeonfish had significantly lower levels of cortisol when stimulated by moving models compared with controls with access to stationary models. Our results show that physical contact alone, without a social aspect, is enough to produce fitness-enhancing benefits, a situation so far only demonstrated in humans.

Arginine Vasotocin Regulation of Interspecific Cooperative Behaviour in a Cleaner Fish

In an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.

Does cleanerfish service quality depend on client value or choice options

Cleaning fish mutualisms appear to be good examples of biological markets. Two classes of traders exist: cleaner fish and their fish clients, each of which supplies a commodity required by the other (ectoparasite removal and a meal, respectively). However, clients are not all treated similarly by cleaners. There is evidence that clients with choice options (with potential access to more than one cleaner) have priority of access over clients without choice options. Market theory predicts that client value (i.e. ectoparasite load) should also influence cleaning service quality. We examined the relative roles of client choice options and client value in determining the duration of cleaning interactions between bluestreak cleaner wrasse, Labroides dimidiatus, and their clients across three geographically distant sites. We found a lack of covariation between client choice options and gnathiid ectoparasite loads. Geographical differences in gnathiid availability altered the importance of client gnathiid load as a determinant of client inspection duration. As predicted, clients with both choice options and high gnathiid loads were inspected for longer, but this was observed only in an area with a relatively high incidence of parasitism. These correlational results suggest that the importance of client choice for aspects of cleaner fish service quality may be modulated by parasite availability.

Client preferences by Caribbean cleaning gobies: food, safety or something else?

Predation risk is amongst the most pervasive selective pressures influencing behaviour and animals have been repeatedly shown to trade-off foraging success for safety. We examined the nature of this trade-off in cleaning symbioses amongst Caribbean coral reef fishes. We predicted that cleaning gobies (Elacatinus evelynae and Elacatinus prochilos) should prefer fish clients that pose a low risk of predation (e.g. herbivores) over clients that may have more ectoparasites but pose a higher risk (e.g. piscivores). Our field observations revealed that cleaners did clean preferentially client species with more parasites but predatory and non-predatory clients had similar ectoparasite loads. Despite the lack of a foraging advantage for inspecting predators, cleaners did not avoid risky clients. On the contrary, a larger proportion of visiting predators than non-predators was inspected, gobies initiated more interactions with predatory clients, and predators were attended to immediately upon arrival at cleaning stations. This preferential treatment of dangerous clients may allow the rapid identification of cleaners as non-prey item or may be due to the effect of predators on the rest of the cleaners’ clientele, which avoided cleaning stations whilst predators were present. Dealing with potentially risky clients may allow gobies to regain access to their main food source: non-predatory clients.

Face your fears: cleaning gobies inspect predators despite being stressed by them.

Social stressors typically elicit two distinct behavioural responses in vertebrates: an active response (i.e., “fight or flight”) or behavioural inhibition (i.e., freezing). Here, we report an interesting exception to this dichotomy in a Caribbean cleaner fish, which interacts with a wide variety of reef fish clients, including predatory species. Cleaning gobies appraise predatory clients as potential threat and become stressed in their presence, as evidenced by their higher cortisol levels when exposed to predatory rather than to non-predatory clients. Nevertheless, cleaning gobies neither flee nor freeze in response to dangerous clients but instead approach predators faster (both in captivity and in the wild), and interact longer with these clients than with non-predatory clients (in the wild). We hypothesise that cleaners interrupt the potentially harmful physiological consequences elicited by predatory clients by becoming increasingly proactive and by reducing the time elapsed between client approach and the start of the interaction process. The activation of a stress response may therefore also be responsible for the longer cleaning service provided by these cleaners to predatory clients in the wild. Future experimental studies may reveal similar patterns in other social vertebrate species when, for instance, individuals approach an opponent for reconciliation after a conflict.

Phase II Study of Celecoxib with Cisplatin Plus Etoposide in Extensive-Stage Small Cell Lung Cancer

We performed a phase II trial to test whether a cyclooxygenase (COX-2) inhibitor, celecoxib, added to standard first-line combination chemotherapy (CT) and as maintenance therapy would improve outcomes in extensive-stage (ES) small-cell lung cancer (SCLC). This was a multicenter trial in CT-naive patients with ES-SCLC. They received standard cisplatin and etoposide (EP) up to 6 cycles and celecoxib 400 mg PO bid continuously until disease progression. Primary end points were response rate (RR), time to progression (TTP), and toxicity. Secondary were overall survival (OS) and quality of life. Of 74 expected patients, only 24 were enrolled and the study stopped earlier because of the published safety concerns about celecoxib. The patients, all male, were between 38 and 74 years. A total of 130 cycles of CT were administered. Toxicity associated with celecoxib was minimal. The RR was 56.5%. Median TTP and OS were 8.6 and 11.3 months, respectively. These data suggest that celecoxib may safely be combined with EP for treatment of ES-SCLC. This combination showed a promising activity and, despite the safety concerns regarding celecoxib, it would be interesting to further evaluate this regimen.

Dopamine disruption increases negotiation for cooperative interactions in a fish

Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit a distinct behavioural response. Here, we tested the effect of exogenously administered dopaminergic compounds on a cooperative vertebrate’s decision-making process, in a natural setting. We show, in the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus, that blocking dopamine receptors in the wild induces cleaners to initiate more interactions with and to provide greater amounts of physical contact to their client fish partners. This costly form of tactile stimulation using their fins is typically used to prolong interactions and to reconcile with clients after cheating. Interestingly, client jolt rate, a correlate of cheating by cleaners, remained unaffected. Thus, in low effective dopaminergic transmission conditions cleaners may renegotiate the occurrence and duration of the interaction with a costly offer. Our results provide first evidence for a prominent role of the dopaminergic system in decision-making in the context of cooperation in fish.

Hereditary gastrointestinal stromal tumors sharing the KIT Exon 17 germline mutation p.Asp820Tyr develop through different cytogenetic progression pathways

Hereditary gastrointestinal stromal tumor (GIST) syndrome is a rare autosomal dominant genetic disorder originated by germline mutations in the KIT or PDGFRA genes. We report the third family with hereditary predisposition to GIST due to the KIT Exon 17 germline mutation p.Asp820Tyr and characterize the cytogenetic progression pathways followed by different GIST sharing the same primary genetic event, using a combination of chromosome banding, comparative genomic hybridization (CGH), and fluorescence in situ hybridization (FISH) analyses. The missense mutation p.Asp820Tyr was detected in the probands rectal and gastric GIST, as well as in his aunts GIST epiplon metastasis. The mutation p.Asp820Tyr was subsequently also found in the probands peripheral blood DNA, as well as in that of 4 of 10 relatives thus far analyzed. CGH analysis revealed loss of 14q and 15q in the probands gastric lesion, whereas FISH analysis of the probands rectal GIST did not detect loss of 14q and 15q, but instead loss of 4q and 22q and gain of 20q, indicating that the two tumors were independent GIST. Chromosome banding and CGH analyses of the aunts GIST epiplon metastasis revealed multiple cytogenetic alterations, including 1p loss, but none in common with the two probands GIST. We conclude that, although the patients share the same KIT Exon 17 germline mutation, the multiple GIST analyzed followed different pathogenetic progression pathways, each of which did not significantly differ from what has been described in sporadic GIST.

Interspecific differences in foraging behaviour and functional role of Caribbean parrotfish

Herbivory is one of the most important biological processes influencing coral reefs. In the highly diverse Indo-Pacific reef fish communities, different herbivores can have strikingly different functions. We investigated the extent of functional diversity among herbivorous parrotfish of the more species-depauperate Caribbean Sea. We carried out observations of seven species of parrotfish (Scarus taeniopterus, Sc. vetula, Sc. iserti, Sparisoma viride, Sp. aurofrenatum, Sp. rubripinne and Sp. chrysopterum) on four Barbadian coral reefs to collect information on foraging techniques, rates, and targets, and found marked interspecific variation. Species of the genus Scarus had higher foraging rates than those of the genus Sparisoma . Different species took varying amounts of live coral, turf algae and macroalgae. A functional categorization based first on foraging technique (contact or no contact with the substratum) and secondarily on the more conventional criterion of foraging target (macroalgae, turf algae and live coral) allowed us to classify Sc. taeniopterus and Sc. iserti as ‘scrapers’, Sp. aurofrenatum , Sp. rubripinne and Sp. chrysopterum as ‘grazers’, Sp. viride as a ‘bioeroder’ and Sc. vetula as a ‘bioeroder/scraper’. This functional group affiliation, together with species-specific foraging rates, allows us to predict the role of Caribbean parrotfish on major coral reef processes and their impact on coral reef benthic communities.