Social Dynamics Obscure the Effect of Temperature on Air Breathing in Corydoras Catfish Mar Pineda, Isabel Aragao, David Mckenzie, Shaun Killen

Social dynamics obscure the effect of temperature on air breathing in Corydoras catfish Mar Pineda, Isabel Aragao, David Mckenzie, Shaun Killen To cite this version: Mar Pineda, Isabel Aragao, David Mckenzie, Shaun Killen. Social dynamics obscure the effect of temperature on air breathing in Corydoras catfish. Journal of Experimental Biology, Cambridge University Press, 2020, 223, 10.1242/jeb.222133. hal-03097340 HAL Id: hal-03097340 https://hal.archives-ouvertes.fr/hal-03097340 Submitted on 5 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb222133. doi:10.1242/jeb.222133 RESEARCH ARTICLE Social dynamics obscure the effect of temperature on air breathing in Corydoras catfish Mar Pineda1, Isabel Aragao1, David J. McKenzie2 and Shaun S. Killen1,* ABSTRACT Resource acquisition is often cited as a key benefit of group- In some fishes, the ability to breathe air has evolved to overcome living, but the focus has predominantly been on foraging (Killen constraints in hypoxic environments but comes at a cost of increased et al., 2018; McKenzie et al., 2016). However, one resource that is predation. To reduce this risk, some species perform group air vital for survival yet often overlooked, is oxygen. In some breathing. Temperature may also affect the frequency of air breathing environments and for some taxa, sufficient oxygen can be in fishes, but this topic has received relatively little research attention. especially difficult to obtain. For example, tropical freshwater This study examined how acclimation temperature and acute environments can often become oxygen poor, or hypoxic. exposure to hypoxia affected the air-breathing behaviour of a social Although some animals have developed mechanisms to escape catfish, the bronze corydoras Corydoras aeneus, and aimed to hypoxia (Graham, 1994) others, such as pond-dwelling fishes, are determine whether individual oxygen demand influenced the often unable to escape. It is in these hypoxic and closed behaviour of entire groups. Groups of seven fish were observed in environments where it is thought that the ability to breathe air an arena to measure air-breathing frequency of individuals and in some fishes first evolved. consequent group air-breathing behaviour, under three oxygen The morphological and physiological specialisations for air concentrations (100%, 60% and 20% air saturation) and two breathing are generally well established, yet little is known about the acclimation temperatures (25 and 30°C). Intermittent flow behavioural and ecological aspects of air breathing in fishes. To respirometry was used to estimate oxygen demand of individuals. breathe air, an individual must surface, rendering them visible to Increasingly severe hypoxia increased air breathing at the individual aerial and terrestrial predators (Kramer and Graham, 1976). and group levels. Although there were minimal differences in air- Consequently, air-breathing fishes can have disproportionately breathing frequency among individuals in response to an increase in high predation rates compared with non-air-breathing species that temperature, the effect of temperature that did exist manifested as an live in the same habitat (Biro et al., 2004; Kramer and Braun, 1983; increase in group air-breathing frequency at 30°C. Groups that were Mangel and Stamps, 2001). To offset the risk associated with more socially cohesive during routine activity took more breaths but, surfacing, some air-breathing species engage in group air breathing. in most cases, air breathing among individuals was not temporally This social surfacing reduces the risk of predation for each clustered. There was no association between an individual’s oxygen individual (Kramer and Graham, 1976) and results in temporally demand and its air-breathing frequency in a group. For C. aeneus, clustered air-breathing events known as synchronised air breathing although air-breathing frequency is influenced by hypoxia, (Hill, 1972; Killen et al., 2018; Kramer and Graham, 1976; Shlaifer behavioural variation among groups could explain the small overall and Breder, 1940). effect of temperature on group air-breathing frequency. The occurrence of social air-breathing is remarkable given that groups consist of individuals with differing oxygen requirements KEY WORDS: Air-breathing fish, Environmental stress, Metabolic (McKenzie et al., 2016). Within animal species, there is rate, Oxygen, Social behaviour considerable among-individual variation in the minimal metabolic rate needed to sustain life (standard metabolic rate in ectotherms; INTRODUCTION SMR). In air-breathing fishes, individuals with a higher basal Group-living is widespread throughout the animal kingdom and is oxygen demand may be driven to breathe air more often than those associated with a variety of costs and benefits (Ward and Webster, with a lower oxygen demand (Lefevre et al., 2016; McKenzie et al., 2016). Living in a group can be detrimental due to increased risk 2016). There is also wide variation among individuals in the of competition (Rubenstein, 1978), parasitism (Rifkin et al., proportion of baseline oxygen requirements that are met by air 2012) and disease (Krause and Ruxton, 2002). Despite this, breathing. In Clarias gariepinus, for example, individuals vary individuals within groups can obtain significant benefits. between approximately 25 and 80% of the oxygen required for SMR coming from air (Mckenzie et al., 2016). Thus, when coordinating social air-breathing, individuals may compromise their own oxygen 1Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, demand or willingness to perform risky air breathing to remain UK. 2MARBEC, Universitéde Montpellier, CNRS, Ifremer, IRD, 9190 Montpellier, within a group (Killen et al., 2018). One of the major questions in France. air-breathing fish research, therefore, is to determine whether key *Author for correspondence ([email protected]) individuals play a significant role in shaping the behaviour of entire groups. Knowing more about this mechanism could then, in turn, S.S.K., 0000-0003-4949-3988 provide insight into the importance of individual heterogeneity in This is an Open Access article distributed under the terms of the Creative Commons Attribution the overall functioning of social groups across taxa (Jolles et al., License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. 2020). There has been a steady increase in research into individual variation and the impact of key individuals on overall group Received 22 January 2020; Accepted 17 September 2020 behaviour (Modlmeier et al., 2014), spanning a large variety of taxa Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb222133. doi:10.1242/jeb.222133 (Ballard and Robel, 2012; Dornhaus et al., 2008; Knörnschild et al., MATERIALS AND METHODS 2010), with potentially important effects on a range of ecological Study species phenomena including group movements and spatial positioning Adult bronze corydoras catfish, Corydoras aeneus (T. N. Gill 1858), (Killen et al., 2012; Killen et al., 2017; McLean et al., 2018), of unknown sex were acquired from an ornamental fish supplier. sociability and dominance (Killen et al., 2016; Metcalfe et al., The fish were semi-domesticated and bred in ponds from wild 1995), and group decision-making, foraging and learning broodstock. After transport to aquarium facilities at the University (Mamuneas et al., 2015). Due to their acute need for oxygen, an of Glasgow (Glasgow, UK), 42 fish (average wet mass 1.651 g, easily quantifiable air-breathing response, air-breathing fishes average total length 43.2 mm) were randomly split among six well- provide an excellent model for studying the role of the individual aerated tanks (60 cm×40 cm×30 cm) so that each tank held a group in the functioning of social groups. of seven individuals. Tanks were supplied with recirculating, UV- Central to the expression of physiological and behavioural traits, treated freshwater at 25°C under a 12 h light:12 h dark photoperiod, however, is the environment. For example, both oxygen availability and equipped with shelter, plastic plants and a sandy substrate. All and water temperature induce a wide range of physiological and neighbouring tanks were divided by an opaque barrier to prevent behavioural responses in fishes (Clark et al., 2013; Domenici et al., fish from observing or interacting with individuals from other 2007; Domenici et al., 2017; Killen et al., 2013). In animal social groups. All fish were acclimated to these conditions for 2 months groups, acute hypoxia can decrease social cohesion and coordination prior to experiments. At the start of the acclimation period, among individuals (Domenici et

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