Effects of ambient oxygen and size-selective mortality on growth and maturation in guppies

Volume 5 • 2017 10.1093/conphys/cox010 Research article Effects of ambient oxygen and size-selective mortality on growth and maturation in guppies Beatriz Diaz Pauli1,†,‡, Jeppe Kolding1,2, Geetha Jeyakanth1 and Mikko Heino1,3,4,* 1 Department of Biology, University of Bergen and Hjort Centre for Marine Ecosystem Dynamics, Bergen, Norway IUCN Commission of Ecosystem Management, Fisheries Expert Group (IUCN-CEM-FEG), Gland, Switzerland 3 Institute of Marine Research, Bergen, Norway 4 Evolution and Ecology Program, International Institute for Applied Systems Analysis, Laxenburg, Austria 2 *Corresponding author: Department of Biology, University of Bergen and Hjort Centre for Marine Ecosystem Dynamics, Bergen, Norway. Tel: +47 55 588137. Email: ; .............................................................................................................................................................. Growth, onset of maturity and investment in reproduction are key traits for understanding variation in life-history strategies. Many environmental factors affect variation in these traits, but for fish, hypoxia and size-dependent mortality have become increasingly important because of human activities, such as increased nutrient enrichment (eutrophication), climate warming and selective fishing. Here, we study experimentally the effect of oxygen availability on maturation and growth in guppies (Poecilia reticulata) from two different selected lines, one subjected to positive and the other negative size-dependent fishing. This is the first study to assess the effects of both reduced ambient oxygen and size-dependent mortality in fish. We show that reduced ambient oxygen led to stunting, early maturation and high reproductive investment. Likewise, lineages that had been exposed to high mortality of larger-sized individuals displayed earlier maturation at smaller size, greater investment in reproduction and faster growth. These life-history changes were particularly evident for males. The widely reported trends towards earlier maturation in wild fish populations are often interpreted as resulting from size-selective fishing. Our results highlight that reduced ambient oxygen, which has received little experimental investigation to date, can lead to similar phenotypic changes. Thus, changes in ambient oxygen levels can be a confounding factor that occurs in parallel with fishing, complicating the causal interpretation of changes in life-history traits. We believe that better disentangling of the effects of these two extrinsic factors, which increasingly affect many freshwater and marine ecosystems, is important for making more informed management decisions. Key words: Eutrophication, fishing selection, hypoxia, life history, Poecilia reticulata, water management Editor: Steven Cooke Received 24 October 2016; Revised 12 January 2017; Editorial Decision 20 January 2017; accepted 6 February 2017 Cite as: Diaz Pauli B, Kolding J, Jeyakanth G, Heino M (2017) Effects of ambient oxygen and size-selective mortality on growth and maturation in guppies. Conserv Physiol 5(1): cox010; doi:10.1093/conphys/cox010. .............................................................................................................................................................. † Department of Biosciences, Centre for Ecological and Evolutionary Syntheses (CEES), University of Oslo, Oslo, Norway Inst. d’Ecologie et des Sciences de l’Environnement – Paris (iEES-Paris), Sorbonne Universités/UPMC Univ Paris 06/CNRS/INRA/IRD/Paris Diderot Univ Paris 07/UPEC/, Paris, France ‡ .............................................................................................................................................................. © The Author 2017. Published by Oxford University Press and the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 Research article Conservation Physiology • Volume 5 2017 .............................................................................................................................................................. Introduction Maturation determines the beginning of the reproductive part of an individual’s life cycle and is costly in terms of survival and energy. The age and size at which an individual matures are therefore key life-history traits. Growth determines the relationship between age and size, with the latter also being a key determinant of survival and fecundity. Thus, studying the effects of different extrinsic factors on growth and maturity is important for understanding the variation in life-history strategies (Roff, 1992; Stearns, 1992, 2000). Many different environmental factors, such as food availability, temperature, oxygen and presence of predators, affect the acquisition and allocation of resources to growth, maturation and reproduction (Berner and Blanckenhorn, 2007; Enberg et al., 2012). Two factors affecting life-history traits are of particular interest in fishes, namely oxygen and size-dependent mortality. Oxygen is one of the most critical physical constraints for aquatic animals (Ross, 2000; Pauly, 2010): water is a dense, viscous medium that contains little oxygen in comparison to air; only small quantities of oxygen can be dissolved, and respiratory areas do not grow as fast as body weight (Pauly, 1981, 2010). Oxygen demand is proportional to the rate of metabolism and increases with, e.g. body size and stress. Low-oxygen conditions occur naturally in many closed water bodies and in the oxygen minimum zones of the World Ocean, but oxygen depletion is also becoming increasingly prevalent in freshwater and marine ecosystems because of increasing eutrophication and temperature (Diaz and Rosenberg, 2008; Doney et al., 2012; Jenny et al., 2016). Importantly, temperature plays a dual role: increasing temperature reduces the solubility of oxygen, while in ectotherms, it also increases the metabolic demand for oxygen (Pörtner and Knust, 2007; Holt and Jørgensen, 2015). Similar to oxygen depletion, size-dependent mortality occurs naturally but can be influenced by human activities. Size-dependent natural mortality is driven by the presence of predators that commonly prey more heavily on smaller size classes, i.e. it is negatively size selective (Lorenzen, 1996; Sogard, 1997; Gislason et al., 2010). In contrast, fishing most often targets large fish (i.e. it is positively size selective). Fishing pressure has increased since the middle of the past century, mainly targeting large individuals and higher trophic levels (Pauly et al., 2002; Kolding et al., 2016). Importantly, reduced oxygen levels and increased size-selective fishing cooccur in many aquatic ecosystems, for instance in Lake Victori (...truncated)