Phenotypic Responses to Lifelong Hypoxia in Cichlids Rutjes, Hendrikus Antonius

Phenotypic responses to lifelong hypoxia in cichlids Rutjes, Hendrikus Antonius Citation Rutjes, H. A. (2006, October 24). Phenotypic responses to lifelong hypoxia in cichlids. Retrieved from https://hdl.handle.net/1887/4925 Version: Corrected Publisher’s Version Licence agreement concerning inclusion of doctoral thesis in the License: Institutional Repository of the University of Leiden Downloaded from: https://hdl.handle.net/1887/4925 Note: To cite this publication please use the final published version (if applicable). PHENOTYPIC RESPONSES TO LIFELONG HYPOXIA IN CICHLIDS Cover and design H.A. Rutjes Figures Martin Brittijn Printed by Ponsen & Looijen BV. Wageningen, The Netherlands PHENOTYPIC RESPONSES TO LIFELONG HYPOXIA IN CICHLIDS Proefschrift ter verkrijging van de graad van Doctor aan de Universiteit Leiden, op gezag van de Rector Magnificus Dr.D.D.Breimer, hoogleraar in de faculteit der Wiskunde en Natuurwetenschappen en die der Geneeskunde, volgens besluit van het College voor Promoties te verdedigen op dinsdag 24 oktober 2006 klokke 15:00 uur door Hendrikus Antonius Rutjes geboren te Velp in 1977 PROMOTIECOMMISSIE Promotor Prof. Dr. M. K. Richardson Co-promotoren Dr. F. Witte Dr. G.J.E.E.M van den Thillart Referenten: Prof. Dr. L.J. Chapman (McGill University, Canada) Prof. Dr. G. Flik (Radboud Universiteit Nijmegen) Overige leden: Dr. F.E.. Sibbing (Wageningen Universiteit) Dr. E.K. Verheyen (Koninklijk Belgisch Instituut voor Natuur Wetenschappen) Prof. Dr. C.J. ten Cate Prof. Dr. P.J.J. Hooykaas Prof. Dr. H.P. Spaink Prof. Dr. R.E. Weber (Aarhus University Denmark) CONTENTS Chapter 1 General Introduction 7 Chapter 2 Unaffected oxygen consumption under lifelong hypoxia in tilapia 19 Chapter 3 Metabolism of hypoxia-raised Lake Victoria cichlids: is a normal life cycle possible under lifelong hypoxia? 39 Chapter 4 Dramatic increase in gill surface of a hypoxia-raised Lake Victoria cichlid 63 Chapter 5 A discriminating shape factor among African cichlids can be induced phenotypically 83 Chapter 6 Closely related fish species use different strategies to improve oxygen transport and metabolism under chronic hypoxia 103 Chapter 7 Synthesis 119 References 127 Nederlandse Samenvatting 142 Dankwoord 158 Curriculum Vitae 160 CHAPTER 1: GENERAL INTRODUCTION H.A. Rutjes, F. Witte and G.J.E.E.M. Van den Thillart Institute of Biology Leiden, Leiden University P.O. Box 9516, 2300 RA Leiden, The Netherlands Introduction 9 Introduction 9 LAKE VICTORIA AND ITS HISTORY before the lake desiccated. The fact is Lake Victoria is by surface the largest that the cichlid fauna of Lake Victoria tropical lake in the world. With a must have survived somewhere. Fryer maximum depth of 70 metres it is (2001) suggested that a remnant lake relatively shallow compared to the or lakes and, in contrast to Seehausen other Great Lakes of Africa (lakes (2001), not remnant streams and rivers Tanganyika and Malawi). Until the have formed the major refuges for the 1980s, the fish fauna was dominated by a ancestral cichlid species. Recently, in species flock of over 500 cichlid species a river north of the Kalahari Desert, (Greenwood, 1974, Witte and Van Oijen, Joyce et al. (2005) found a riverine 1995; Seehausen, 1996). Amongst these cichlid population of which the species, specialists to virtually every functional diversity is comparable to possible food source existed in the that of the functional diversity seen in lake (Greenwood, 1981; Witte and Van Lake Victoria. It was concluded that Oijen, 1995; Seehausen, 1996). The this radiation is a remnant from a lake lake itself is less than a million years that desiccated ~2000 years BP and old and the latest data suggest that that is currently a salt pan. Together, these a major desiccation event occurred in findings suggest that it is possible for the late Pleistocene. The lake refilled populations of fish to survive desiccation again about 14.000 years BP (14C events by using rivers as a refuge. 12,400 years). (Johnson et al., 1996). During the last century, Lake Victoria Whether the lake was completely dry and its fish fauna have been subject to during this desiccation event or if some anthropogenic perturbations leading remnant waters remained is still unclear to major ecological changes. Since (Johnson et al., 1996; Fryer, 1997, 2001; the beginning of last century, fishing Seehausen, 2002). Nagl et al., (2000) pressure continuously increased, leading suggested that the molecular diversity to decreased catches of the tilapiine of the Lake Victoria cichlid fauna came species (Fryer and Iles, 1972). In the into existence 250,000-750,000 years 1950s and 1960s, exotic tilapiine species ago. When the ancestral population of (Beauchamp, 1958; Welcomme, 1967) the modern species flock entered the and the predatory Nile perch Lates lake, when it refilled 14,000 years ago, niloticus (Arunga, 1981, Welcomme, their molecular polymorphism enabled 1988) were introduced. Initially, these fish to rapidly diversify and radiate populations of these fish did not increase into the species flock that is known in and fisheries were not boosted. In the the present day. It was suggested by 1960s a light fishery was developed Verheyen et al. (2003) that all haplotypes for the small zooplanktivore cyprinid known in the modern Lake Victoria are Rastrineobola argentea, and in 1976 much older than the desiccation event trawl fisheries began on haplochromine 14,000 years ago and that the major cichlids, locally affecting cichlid diversification had already occurred populations. In the beginning of the 10 Phenotypic responses to lifelong hypoxia in cichlids Chapter 1 Introduction 11 1980s, the Nile perch populations richness and densities of zooplankton, boomed, simultaneously with a collapse crustaceans and fish (Pihl et al., 1991, of the cichlid fauna (Barel et al., 1985; 1992; Pearson and Rosenberg, 1992; Ogutu-Ohwayo, 1990; Witte et al., 1992). Roman et al., 1993; Diaz and Rosenberg, Populations of R. argentea seemed to 1995; Karlson et al., 2002; Wu , 2002). profit from the decline in cichlid numbers Seasonal or periodic recurrence of and populations increased considerably hypoxia causes large-scale defaunation (Ogutu-Ohwayo, 1990; Wanink, 1991; through migration and/or mortality. In Witte et al., 1999; Wanink and Witte, Lake Victoria, upwelling of hypoxic 2000b). The occurrence of algae blooms, water, which causes massive fish kills, mainly of cyanobacteria increased in has increased in frequency (Ochumba, the 1980s. Cyanobacteria replaced the 1990; Ochumba et al., 1993; Wanink et diatoms that previously dominated in al., 2001). If possible, fish tend to avoid Lake Victoria (Verschuren et al., 1998). exposure to low O2 levels (Wannamaker Data derived from sediment cores in the and Rice, 2000; Wanink et al., 2001), but deepest part of the lake revealed that during such upwelling events, fish are eutrophication, the probable cause of exposed to hypoxia suddenly and they are these algae blooms, must already have unable to flee or adjust their metabolism started between the 1920s and 1930s (Randall, 1970). In Lake Victoria, (Hecky, 1993; Verschuren et al., 1998, chronic hypoxia is nowadays present in 2002). The eutrophication of the lake much larger areas and for longer periods was strongly correlated with the increase than before (Kaufman, 1992; Hecky, of the human population in the region 1993; Hecky et al., 1994; Wanink et (Verschuren et al., 1998, 2002). al., 2001). In the deep waters of Lake -1 Victoria, severe hypoxia (<1 mg O2 L ) OCCURENCE OF HYPOXIA was present from October to March at The story of Lake Victoria is not depths of 40 to 54 meters (35% of the unique. Human induced perturbations lake’s bottom area) in 1990-91, whereas leading to eutrophication, algae this level of hypoxia was observed only blooms, and concomitant large-scale below 60 meter in 1960-61 (Hecky et al., detrimental effects on aquatic life 1994). In the more shallow Mwanza Gulf occur worldwide, correlated with the (<20m) in the South of the lake, periods increase in human population (De of hypoxia became longer and the 1 and -1 Jonge et al., 2002). Examples of factors 5 mg O2 L isopleths moved upward in leading to eutrophication are run off the water column between 1979 and from agricultural areas, deforestation, 1988 (Wanink et al. 2001). This makes industrial discharge, and domestic the lower part of the water column a less wastewater. With eutrophication, suitable habitat for demersal fish species. hypoxia is often introduced in waters Not surprisingly, several researchers where it was uncommon before. This has have hypothesised that, apart from the a dramatic impact on distribution, species introduction of Nile perch, hypoxia was 10 Phenotypic responses to lifelong hypoxia in cichlids Chapter 1 Introduction 11 an important factor in the decline of the tolerance. When fish are given time haplochromine cichlids in Lake Victoria to habituate to the new environment, (Kaufman, 1992; Hecky et al., 1994; metabolism can be decreased and stress Verschuren, 2002). responses minimised and tolerance is higher (Randall, 1970; Ultsch et al., PHYSIOLOGY AND HYPOXIA 1981). The ability to tolerate short-term The duration of exposure to hypoxia hypoxia is partly dependent on the has a large influence on the responses coping strategy of the animal. From of fish. These responses can be studies on sole, Solea solea, (Van den behavioural, physiological, biochemical Thillart et al., 1994) and rainbow trout, or anatomical. However, the relation Oncorhynchus mykiss, (Van Raaij et al., between the duration of hypoxia and 1996) it is known that animals can either the type of response is almost never react with tranquil behaviour, or show categorised. Especially physiological escape responses. In the latter case, high responses to hypoxia can be very levels of catecholamines and cortisol and different depending on the duration low survival can be observed. of hypoxia. Thus, I distinguish short- Upon gradually induced short-term term hypoxia from chronic hypoxia.

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