American Fisheries Society Symposium 63:xxx, 2008 © 2008 by the American Fisheries Society Energetics of Grenadier Fishes JEFFREY C. DRAZEN† University of Hawaii, Department of Oceanography, MSB606 1000 Pope Road, Honolulu, Hawaii 96822, USA Abstract.—Energetic parameters such as metabolism, growth, and reproduction rep- resent investments by an animal in maintenance and production. The available lit- erature was reviewed to examine trends in these parameters for grenadiers to better understand their biology in relationship to shallow living species. Grenadiers are adapted to deep-sea habitats that have fundamentally different environmental condi- tions than the continental shelves where most exploited fishes live. Grenadiers have very low metabolic rates, similar to other deep-sea demersal and pelagic fishes. This appears to be the result of a relaxation in the selective pressure for locomotory capac- ity in dim or totally dark waters. Longevities are variable and dependant, in part, on body size. Regardless of longevity, low rates of mass-specific growth are typical and may be limited by its relationship to metabolism. Finally, reproductive outputs may be much lower than originally anticipated from gross measures of fecundity, and at least some species may reproduce less often than annually. Energetic data are sparse but until more are available for diverse species, we must assume that with a similar body form, phylogeny, and habitat, that all grenadiers have low rates of metabolism, growth, and reproduction. Grenadiers are exceptionally diverse and certainly varia- tion exists, some of which can be explained by individual ecologies. Nevertheless it is clear that models based on the energetics of shallow living fishes cannot be used for grenadiers. Their energetic characteristics are different and make them extremely vulnerable to overexploitation. Grenadiers have become targets or major components of the bycatch in slope fisheries, so it is especially important that this basic fact be understood. Introduction for resources. Grenadiers, fishes in the family Macrouridae, are very abundant and often are Over the last several decades fisher- the dominant fishes at bathyal depths (Cailliet ies for deep-sea species have developed on et al. 1999; Lauth 2000; Marshall and Iwa- continental slopes and seamounts around moto 1973; Merrett 1992; Merrett and Hae- the world (Clark 2001; Devine et al. 2006; drich 1997; Pearcy et al. 1982; Stefanescu Garibaldi and Limongelli 2003; Koslow et et al. 1994; Williams et al. 2001). There are al. 2000; Merrett and Haedrich 1997; Moore ∼400 species worldwide (Iwamoto 2008, this 1999; Roberts 2002). This expansion is part- volume). Several fisheries have developed ly in response to collapses in shallow waters for them (Devine et al. 2006; Gordon 2001a; and the need to find new stocks. Fisherman Gordon 2001b; Lorance et al. 2001; Matsui will likely continue to explore deep waters et al. 1990) and in some cases they have be- come a major constituent of discards in slope †Corresponding author: [email protected] 1 2 Drazen fisheries directed at other species (Allain et et al. 1980; Drazen 2002a; Koslow 1996). al. 2003; Laptikhovsky 2005; Novikov 1970; Through the integration of individuals the Zenger and Sigler 1992). Some grenadier fish- resource requirements, productivity, and dy- eries have only recently been developed (An- namics of populations can be derived (Brown drews et al. 1999; Tuponogov et al. 2008, this et al. 2004). Potential population sizes could volume) whereas some that began decades be estimated from resource requirements and ago have already been exhausted (Devine et habitat productivity. Understanding popula- al. 2006; Haedrich et al. 2001). Many ecolog- tion dynamics leads to an understanding of ical and physiological studies have focused the response to fishing mortality. Therefore, on grenadiers because of these fisheries and a energetics is fundamentally important to fish- desire to understand their role in ecosystems eries science. (see Gage and Tyler 1991; Merrett and Haed- Here I review the information available rich 1997 and references therein). on each energetic component and whole en- Of great importance is an understanding ergy budgets for grenadiers. Comparisons of energetics, the rates at which these animals are made between grenadier species to assess consume and transform energy and ultimate- whether any commonalities exist. Gadiform ly, produce new biomass. Metabolism is a fishes are diverse and the shallow-living cods process of energy assimilation, transforma- and hakes are well studied because of the tion, and allocation. Growth represents the considerable fisheries for them (Cohen et al. fraction of energy stored by the individual 1990). Studies for grenadiers are fewer, thus as new mass. Reproduction can be defined it is tempting to extrapolate our more famil- as the energy allocated to gametes and re- iar knowledge of shallow species to the deep- productive behaviors. These processes are sea grenadiers. The energetics of grenadiers linked and metabolism influences, perhaps are compared to those of cods, in particular, even controls, the others (Brown et al. 2004; throughout this review because the cods are McNab 2002). Information on metabolism, a familiar benchmark, are phylogenetically growth and reproductive expenditures can be related to grenadiers, and to show that such brought together to form an animal’s energy extrapolations are not justified. I summarize budget. An energy budget assumes that the with comparisons to other groups of deep- energy consumed in food must be spent by sea fishes to place grenadier energetics into a the fish in growth, reproduction, metabolism, broader context. or lost as wastes (Brett and Groves 1979; Jobling 1993), such that Metabolism consumption (C) = metabolism (M) + growth Many factors are known to have im- (G) + reproduction (R) + excretion (E) (1) portant effects on animal metabolic rates. Among the best described are temperature The budgets can be used to compare data and body mass. Temperature affects metabo- from each parameter converted to units of en- lism, presumably through kinetic effects on ergy and to assess the validity of parameters reaction rates although the precise link is that were assumed or estimated rather than poorly understood. Broadly speaking, higher measured, not an unusual situation in deep-sea temperatures lead to higher metabolic rates studies. Energy budget approaches can com- within a species (Clarke 2004; Clarke and pare energetic strategies provide estimates Johnston 1999). Body size also has dramatic of consumption, potential for growth and re- effects on metabolism. The classic “mouse to productive output of individuals (Childress elephant” curve relates the variation in meta- Energetics of Grenadier Fishes 3 10 ) ) -1 –1 h h -1 –1 g g 2 2 1 Coryphaenoides armatus Coryphaenoides acrolepis Gadus morhua Gadus macrocephalus 0.1 Theragra chalcogramma oxygen consumption (umol O oxygen consumption (umol O 0.01 1 10 100 1000 10,000 mass (g) Figure 1. Oxygen consumption as a function of fish mass for grenadiers and shallow living gadids. All measurements are adjusted to 5°C. All individual measurement for grenadiers are shown. Data for the grenadiers were taken from the sources listed in the text. Data for gadids are represented by many measurements and the published mass scaling relationships are shown. Data are from the following sources: Gadus morhua (Saunders 1963), Gadus macrocephalus (Paul et al. 1988), Theragra chalcogramma (Smith et al. 1988). bolic rates to body sizes with a power law. of grenadiers have been measured direct- Although the exact slope of the relationship ly using in situ respirometers (Bailey et al. is actively debated (Bokma 2004; Clarke and 2002; Smith 1978; Smith and Hessler 1974) Johnston 1999; Glazier 2005; Suarez et al. and high pressure systems which retrieve the 2004), smaller animals generally have higher animals from depth under in situ conditions mass-specific metabolic rates (Clarke and (Drazen et al. 2005). Due to the difficulty and Johnston 1999; Darveau et al. 2002; Suarez et expense, there are relatively few measure- al. 2004). Even after taking into account the ments. Comparisons to shallow living but important effects of body size and tempera- phylogenetically related gadids (Drazen and ture, grenadiers have an order of magnitude Seibel, in revision) clearly indicate that gren- lower metabolic rates than shallow living adiers have routine metabolic rates an order species. Grenadiers do not survive recovery of magnitude lower (Figure 1). to the surface without the aid of pressure re- Due to the difficulties associated with taining vessels (Phleger et al. 1979; Wilson direct measurements, several biochemical and Smith 1985) so routine metabolic rates proxies for metabolism have been used (Dal- 4 Drazen hoff 2004; Graham et al. 1985). The most requirements while activities of aerobic en- commonly employed are measurements of zymes scale to body size in a very similar key enzymes of intermediary metabolism. fashion to mass specific aerobic metabolism Several studies have found that they cor- (Childress and Somero 1990; Somero and relate well with oxygen consumption rates Childress 1980; 1985). These effects do not (Childress and Somero 1979; Dalhoff 2004; explain the majority of variation in the rates Moyes and LeMoine 2005). Several enzyme seen in Table 1. For instance, if we assumed activities have been measured in grenadiers. that the LDH activity of carapine grenadier Both lactate dehydrogenase (LDH) and py- Coryphaenoides carapinus (4.70 units g−1 ruvate kinase (PK) are active in glycolysis wet weight at an average mass of 80 g) scaled and are indicative of anaerobic metabolism. with an exponent of 0.4, an average for many LDH activity is thought to be closely linked species (Childress and Somero 1990), then at with burst swimming performance (Dalhoff 500 g its LDH activity would be ∼9.8 units 2004; Somero and Childress 1980; Sullivan g−1 wet weight, still dramatically different and Somero 1980). Citrate synthetase (CS), than Pacific grenadier C. acrolepis for in- active in the Krebs cycles, is an indicator of stance (Table 1).