Can Threshold Foraging Responses of Basking Sharks Be Used to Estimate Their Metabolic Rate?
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MARINE ECOLOGY PROGRESS SERIES Vol. 200: 289-296,2000 Published July 14 Mar Ecol Prog Ser ~ NOTE Can threshold foraging responses of basking sharks be used to estimate their metabolic rate? David W. Sims* Department of Zoology, University of Aberdeen. Tillydrone Avenue. Aberdeen AB24 2TZ. United Kingdom ABSTRACT: Empirical and theoretical determinations of There are 3 species of filter-feeding shark, the whale minimum threshold prey densities for filter-feeding basking shark ~hi~~~d~~typus of warm-temperate and tropical sharks Cetorhinus maximus were used to test the idea that threshold foraging behaviour could provide a means for esti- seas worldwide, the basking shark Cetorhinus max- mating oxygen consumption (a proxy for metabolic rate). The im~~that inhabits warm-temperate to boreal waters threshold feeding levelrepres&nts the prey density at which circumglobally, and the megamouth shark Mega- there will be no net energy gain (energy intake equals expen- chasms pelagjos occurs in the Pacific and At- diture). Basking sharks were observed to cease feeding at lantic, primarily in deep water (Compagno 1984, Yano their theoretical threshold; thus, the assumption underpin- ning the concept presented here was that over the narrow et They are the largest marine verte- range of zooplankton prey densities that induce 'switching' brates attaining body lengths of up to 14, 10 and 6 m re- between feeding and non-feeding in basking sharks, the spectively. Comparatively little is known about the bi- energetic value of the minimum threshold prey density is ology of planktivorous sharks despite the fact that they equivalent to the shark's instantaneous level of energy expen- diture. Four independent estimates of the lower threshold are unique within the shark group in that they consume prey density obtained for C. maximus in the English Channel zooplankton directly, which results in them being at the were converted to equivalent rates of oxygen consumption. apex of a relatively short food chain with the potential Best estimates ranged from 62.5to 91.1 mg 0, kg-' h-' (mean, to influence the density and diversity of plankton com- 80.7 mg 0, kg-' h-', & 20.1 [95% confidence interval, CI]) for munities. Although the foraging behaviour of whale a shark of 5 m total body length (LT)weighing 1000 kg. Sensi- tivity analysis using 'low' and 'high' possible values in the sharks (Clark & Nelson 1997) and basking sharks (e.g. model for mouth gape area, proportion of prey filtered, buccal Sims & Quayle 1998) has begun to be studied in detail flow velocity, prey energy content and energy absorption, recently, there have been no determinations of the yielded low and high rates of 23.2 and 192.1 mg 0, kg-' h-', magnitude or rates of vertical energy flux attributable respectively. Varying estimated body mass of 1000 kg in the model by r 200 kg gave an oxygen consumption range of 67.2 to these species. In this context, measurements of en- to 100.8 mg O2kg-' h-'; a range within the 95 % C1 of the best ergy expenditure in plankton feeding sharks at differ- estimate mean. For comparison, a new routine oxygen con- ent levels of activity would provide important infor- sumption- body mass relationship was determined for sharks mation on the level of zooplankton (energy) intake (body mass range, 0.35 to 140 kg) and was described by the required by these animals to meet active metabolism, equation V02= 0.30~~,~~,where V02 is oxygen consumption in mg O2 h-' and M is mass in grams. When corrected for and, set against the calorific value of prey densities likely energy costs associated with filter-feeding, this rela- utilised by them, would enable calculation of the quan- tionship and 2 other metabolic rate scaling relationships in tity of energy potentially available for growth. How- the literature gave expected rates between 52.0 and 99.2 mg ever, measurement of energy expenditure in planktivo- Oz kg-' h-' for a fish of 1000 kg body mass. The threshold- converted and expected oxygen consumption values al- rous sharks is yet to be attempted. though derived from different methods show good agree- Numerous investigations have measured meta- ment, an observation that warrants further investigation. To bolic rates in a variety of shark species using the in- verify the concept it will be necessary to obtain threshold- direct, oxycalorific method (e.g. Pritchard et al. 1958, converted rates of oxygen consumption from a wide size Hughes & Umezawa 1968, Brett & Blackburn 1978, range of basking sharks (1.5 to 10.0 m LT) to determine whether rates scale predictably with body mass as does actual Bushnell et al. 1989, Sims 1996). The oxygen con- metabolism. sumption rates of large species (> 1 m in length), how- KEY WORDS: Feeding . Energetics . Swimming speed . Zooplankton . Scaling 'E-mail: [email protected] O Inter-Research 2000 Resale of full article not permitted 290 Mar Ecol Prog Ser ever, cannot be measured using conventional meth- tinued to feed in areas with low prey density for ods because the size of most water-tunnel respiro- extended periods of time the energy that could be meters limits experiments to small specimens or juve- gained from filtered prey would not be sufficient to niles (Graham et al. 1990). The logistical problems cover the costs of its collection. The density of zoo- associated with capturing large pelagic sharks, keep- plankton at which energy intake equals expenditure is ing them in a respirometer and maintaining them termed the threshold prey density, and below this level alive for long enough such that near-normal rates of net energy gain cannot be achieved. metabolism can be determined have meant only a Theory predicts that filter-feeding swimming speed small number of sub-adult individuals of large, active will be lower in higher densities of zooplankton, but species have been examined (e.g.lemon shark Nega- will increase as prey becomes sparse in order that opti- prion brevirostns and shortfin mako Isurus oxynn- mum rates of prey capture are maintained (Ware 1978, chus; Graham et al. 1990). Priede 1985).A recent study on basking sharks demon- Most commonly the routine oxygen consumption- strated empirically that individual sharks increase body mass relationship derived from small to medium- swimming speed in low prey densities and cease feed- sized fish species has been used to estimate metabolic ing at their theoretical threshold prey density deter- rates of large sharks indirectly by simple extrapolation mined from energy intake-output calculations (Sims (e.g. Stillwell & Kohler 1982). This approach provides 1999). Below the threshold level, feeding stopped in only an estimate of routine oxygen consumption and preference to lower cost (low drag) cruise swimming does not take into account species-specific differences with the mouth closed. In this paper I suggest a poten- in physiology and behaviour, such as the regional het- tial method for estimating oxygen consumption rate in erothermy in certain predatory shark species (e.g. the basking shark using determinations of their thres- white shark Carcharodon carcharias) and its effects on hold foraging responses. In the light of the abovemen- heat conservation, metabolic rate and activity levels. tioned study, I reason that, at the threshold prey den- Hence, whilst it is generally accepted that extrapola- sity which induces 'switching' between feeding and tion of routine oxygen consumption-body mass rela- non-feeding in basking sharks, the energy value of the tionships (to obtain estimates of active metabolism in minimum threshold prey density should (after taking large sharks) will not provide accurate estimates on a into account additional factors) be equivalent to the species-by-species basis, there have been no sugges- shark's instantaneous level of energy expenditure at tions of other indirect methods that could indicate the onset of filter-feeding (i.e. an active metabolic metabolism in species too large to be kept in the rate). In this study I use the concept of this energetic laboratory. Therefore, in the absence of very large tun- balance point together with previously published nel respirometers for measuring oxygen consumption threshold response data (Sims 1999) to estimate oxy- directly or comprehensive oxygen consumption- body gen consumption rate in a basking shark of 5 m total mass relationships that include large-bodied shark body length (LT).Comparisons are made between this species, it seems the energy expenditure of filter-feed- threshold-converted oxygen consumption rate and ing sharks must be estimated in other ways. those derived from 2 new routine oxygen consump- Whale sharks and megamouth sharks primarily tion- body mass relationships for sharks, and 2 general utilise suction or gulp feeding to obtain sufficient par- fish relationships. ticulate prey (Compagno 1990, Colman 1997), where Methods. Threshold foraging behaviour determina- the controlled increase in volume of the shark's bucco- tion~:The minimum threshold prey densities for bask- pharyngeal cavity results in an internal pressure ing sharks that were used in this study to calculate oxy- reduction which, when the mouth opens, acts to draw gen consumption were determined from behavioural water (containing prey) into the mouth. In contrast, studies carried out in a 350 km2 study area in the Eng- basking sharks feed by swimming forwards with the lish Channel off Plymouth, UK (for map see Sims & mouth open to overtake zooplankton prey that are fil- Merrett 1997, their Fig. 1). Detailed descriptions of the tered from the passive water flow across the gills by methodologies used to determine threshold foraging comb-like rakers attached to the gill arches; a strategy responses are given in Sims (1999).In the latter study 4 known as ram filter-feeding. Basking sharks are independent field methods that related observations of dependent therefore on forward swimming speed to shark behaviour to variations in zooplankton prey den- regulate rates of prey capture (energy intake).