Ontogeny of oxygen stores and physiological diving capability in Australian sea lions
2007; Wiley; Volume: 21; Issue: 5 Linguagem: Inglês
10.1111/j.1365-2435.2007.01295.x
ISSN1365-2435
AutoresShannon L. Fowler, Daniel P. Costa, John P. Y. Arnould, Nicholas J. Gales, Jennifer M. Burns,
Tópico(s)Neuroscience of respiration and sleep
ResumoFunctional EcologyVolume 21, Issue 5 p. 922-935 Free Access Ontogeny of oxygen stores and physiological diving capability in Australian sea lions S. L. FOWLER, Corresponding Author S. L. FOWLER Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA, †Author to whom correspondence should be addressed. E-mail: fowler@biology.ucsc.eduSearch for more papers by this authorD. P. COSTA, D. P. COSTA Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA,Search for more papers by this authorJ. P. Y. ARNOULD, J. P. Y. ARNOULD School of Biological and Chemical Sciences, Deakin University, Burwood, Vic. 3125, Australia,Search for more papers by this authorN. J. GALES, N. J. GALES Australian Antarctic Division, Channel Highway, Kingston, Tas. 7050, Australia,Search for more papers by this authorJ. M. BURNS, J. M. BURNS Department of Biological Sciences, University of Alaska Anchorage, Anchorage, AK 99508, USASearch for more papers by this author S. L. FOWLER, Corresponding Author S. L. FOWLER Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA, †Author to whom correspondence should be addressed. E-mail: fowler@biology.ucsc.eduSearch for more papers by this authorD. P. COSTA, D. P. COSTA Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA,Search for more papers by this authorJ. P. Y. ARNOULD, J. P. Y. ARNOULD School of Biological and Chemical Sciences, Deakin University, Burwood, Vic. 3125, Australia,Search for more papers by this authorN. J. GALES, N. J. GALES Australian Antarctic Division, Channel Highway, Kingston, Tas. 7050, Australia,Search for more papers by this authorJ. M. BURNS, J. M. BURNS Department of Biological Sciences, University of Alaska Anchorage, Anchorage, AK 99508, USASearch for more papers by this author First published: 07 June 2007 https://doi.org/10.1111/j.1365-2435.2007.01295.xCitations: 60AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary 1 For air-breathing animals in aquatic environments, foraging behaviours are often constrained by physiological capability. The development of oxygen stores and the rate at which these stores are used determine juvenile diving and foraging potential. 2 We examined the ontogeny of dive physiology in the threatened Australian sea lion Neophoca cinerea. Australian sea lions exploit benthic habitats; adult females demonstrate high field metabolic rates (FMR), maximize time spent near the benthos, and regularly exceed their calculated aerobic dive limit (cADL). Given larger animals have disproportionately greater diving capabilities; we wanted to determine the extent physiological development constrained diving and foraging in young sea lions. 3 Ten different mother/pup pairs were measured at three developmental stages (6, 15 and 23 months) at Seal Bay Conservation Park, Kangaroo Island, South Australia. Hematocrit (Hct), haemoglobin (Hb) and plasma volume were analyzed to calculate blood O2 stores and myoglobin was measured to determine muscle O2. Additionally, FMR's for nine of the juveniles were derived from doubly-labelled water measurements. 4 Australian sea lions have the slowest documented O2 store development among diving mammals. Although weaning typically occurs by 17·6 months, 23-month juveniles had only developed 68% of adult blood O2. Muscle O2 was the slowest to develop and was 60% of adult values at 23 months. 5 We divided available O2 stores (37·11 ± 1·49 mL O2 kg−1) by at-sea FMR (15·78 ± 1·29 mL O2 min−1 kg−1) to determine a cADL of 2·33 ± 0·24 min for juvenile Australian sea lions. Like adults, young sea lions regularly exceeded cADL's with 67·8 ± 2·8% of dives over theoretical limits and a mean dive duration to cADL ratio of 1·23 ± 0·10. 6 Both dive depth and duration appear impacted by the slow development of oxygen stores. For species that operate close to, or indeed above their estimated physiological maximum, the capacity to increase dive depth, duration or foraging effort would be limited. Due to reduced access to benthic habitat and restricted behavioural options, young benthic foragers, such as Australian sea lions, would be particularly vulnerable to resource limitation. Introduction The question of when physiology limits behaviour is central to the field of physiological ecology (Costa & Sinervo 2004). For reptiles, birds and mammals that have successfully reinvaded aquatic environments, diving capability, which is critical to successful foraging, is often constrained by physiology (Kooyman 1989; Boyd & Croxall 1996; Costa, Gales & Goebel 2001). Not only are physiological limits different across species, but species dive differently with respect to limits (Ridgway & Johnston 1966; Lenfant, Johansen & Torrance 1970; Butler & Jones 1997). The aerobic component of diving metabolism (DMR) is thought to be the major determinant of diving capacity (Kooyman et al. 1980; Costa 1993; Ponganis, Kooyman & Castellini 1993). Theoretically, aerobic diving results in increased foraging time by minimizing variations in blood chemistry requiring extended recovery (Castellini, Davis & Kooyman 1988). Although diving anaerobically increases a single dive's duration, total time underwater is reduced as more time must be spent at the surface clearing accumulated lactate (LA) (Kooyman et al. 1980, 1983). Many air-breathing vertebrates dive within their limit of estimated O2 stores for the vast majority of dives (Kooyman et al. 1980; Dolphin 1988; Kooyman 1989). The aerobic dive limit (ADL), or diving lactate threshold (DLT), is experimentally defined as the maximum dive duration without increases in blood LA (Kooyman et al. 1980, 1983; Butler 2006). It has only been directly measured in a few species (Kooyman et al. 1980, 1983; Williams, Friedl & Haun 1993; Ponganis et al. 1997a,b; Ponganis, Kooyman & Winter 1997c; Shaffer et al. 1997). However, these studies found ADL could be predicted by dividing available O2 stores by O2 consumption rates. This equation, the calculated aerobic dive limit (cADL), is a conceptual tool used as an index of aerobic and physiological capacity (Kooyman 1989). In some species where adults are known to primarily dive aerobically, juveniles rely on energy produced anaerobically for a larger percentage of dives (Kooyman et al. 1983; Burns 1999). This is due to inexperience and a lower ADL. Divers are born with minimal O2 stores that develop as they mature (Davis 1991; Horning & Trillmich 1997; Ponganis et al. 1999). Young animals have intrinsically higher metabolic rates and costs associated with growth (Brody 1945; Schmidt-Nielsen 1984; Thorson & Le Boeuf 1994). They appear unable to regulate heart rate, respiration, vasoconstriction or body temperature as effectively as adults, which would also limit diving ability (Rea & Costa 1992; Ponganis et al. 1993; Greaves et al. 2005). Oxygen stores appear particularly important in determining dive potential (Horning & Trillmich 1997; Ponganis et al. 1999; Burns et al. 2005). Across different species, numerous studies found a positive relationship between total O2 stores and diving ability (Ridgway & Johnston 1966; Lenfant et al. 1970; Keijer & Butler 1982). Muscle myoglobin (Mb) tends to be the most prominent and consistent physiological predictor of breath-hold endurance (Kooyman 1989; Kooyman & Ponganis 1998; Ponganis et al. 1999). In previous studies, Mb has been the slowest O2 store to develop (Thorson & LeBoeuf 1994; Noren et al. 2001, Richmond, Burns & Rea 2006). Although few studies have examined otariids, they store proportionately more O2 in muscle than seabirds and phocids (Kooyman 1989), so extended Mb development may particularly constrain otariid pups. Australian sea lions Neophoca cinerea (Péron) are excellent subjects to study otariid diving ontogeny as they are non-migratory and demonstrate extended dependency, during which pups begin diving. Pups are suckled for 17·6 ± 0·1 months, one of the longest lactation periods in pinnipeds thought to have evolved as an adaptation to a marine environment where resources are limited and show little seasonal fluctuation (Higgins 1993; Gales, Shaughnessy & Dennis 1994). As a result of small population size, small breeding colony size, exposure to human activities and evidence of population declines, Australian sea lions have recently been listed as threatened (EPBC Act 2000). The Australian sea lion provides an intriguing system as one of few species in which adults regularly exceed cADL's, with almost 80% of dives over predicted limits (Costa et al. 2001). Adults spend 58% of time at-sea underwater and exhibit high field metabolic rates (FMR) (Costa & Gales 2003). Given the extreme foraging behaviour of adults and the potentially limited capabilities of younger animals, we wanted to examine diving ability in Australian sea lion pups and juveniles. We investigated the ontogeny of O2 stores (hematocrit (Hct), haemoglobin (Hb), plasma volume, Mb), FMR and cADL in Australian sea lions. Although many studies have looked at one or more aspects of cADL development in marine mammals, this is the first to simultaneously measure blood and muscle O2 stores with FMR. By examining the extent physiology limits dive behaviour in young Australian sea lions, we can answer a central question in physiological ecology for this species, provide insight into its threatened status, and contribute to the emerging field of conservation physiology (Wikelski & Cooke 2006). Materials and methods Fieldwork was conducted between June 2001 and August 2003 at Seal Bay Conservation Park, Kangaroo Island, South Australia (35°41′S, 136°53′E). A known-aged cohort of 55 pups (28 males and 27 females) was flipper-tagged in 2001 (Fowler et al. 2006). To ensure individuals were only measured once, mothers and pups received a subcutaneous passive microtransponder chip (Destron Fearing Corporation, South St Paul, MN, USA). Mother/pup pairs were captured simultaneously, sedated with Isoflurane gas anaesthesia, and weighed with a digital scale (± 0·1 kg) (Gales & Mattlin 1998). Pairs were captured during three field seasons: (i) 6-month pups (March 2002); (ii) 15-month pups (November 2002); and (iii) 23-month juveniles (July 2003). Ten different mother/pup pairs were captured each season, with the exception of two 15-month pups and five 23-month juveniles, which were never observed suckling and were captured alone. Adult females suckling young pups were captured in place of their mothers. The remaining 23-month juveniles were observed suckling at least once during the field season, despite the fact weaning usually occurs by 17·6 months (Higgins 1993). In July 2003, only six 23-month juveniles (not sampled in March or November 2002) could be located. Therefore, age for the remaining juveniles was estimated using pelage condition and growth curves constructed from data on mass and standard length (Fowler 2005). One independent juvenile from the previous cohort (aged c. 3 years) was also captured and sampled in July 2003. haematology Hematocrit (Hct) declines as the spleen expands under general anaesthesia, so we took initial blood samples using manual restraint (Zapol et al. 1989; Ponganis et al. 1992; Costa, Gales & Crocker 1998). We measured Hct in quadruplicate the same day of collection in capillary tubes following centrifugation for 5 min at 11 500 r.p.m. For individuals that could not be sampled using manual restraint (one 6-month pup, one 15-month pup, two 23-month juveniles), we used a minimum of three sampling points and linear regression to hindcast Hct before administration of anaesthesia. To determine whole-blood haemoglobin concentration (Hb), 10 µL whole blood were added to 2·5 mL Drabkins solution (Kit 525A, Sigma Diagnostics, St Louis, MO, USA) and later assayed in duplicate using the cyan-methhaemoglobin photometric method (ICSH 1967). Samples were read at 540 nm (Spectronic 1001, Bausch & Lomb, Rochester, NY, USA) and Hb was determined by comparison with standard dilution curves. Following methods for Hct, linear regression was used to hindcast Hb when necessary. We determined mean corpuscular haemoglobin content (MCHC) using the equation: MCHC = (Hb × 100) × Hct − 1. plasma volume Plasma volume was determined using Evans Blue dilution (ICSH 1967). A 10-mL blood sample was drawn from the caudal gluteal vein, followed by an intravenous injection of pre-weighed Evans Blue dye (Sigma Diagnostics) approximating a dosage of 0·6 mg kg−1 (Costa et al. 1998). The syringe was flushed with blood to ensure injections were intravenous and all dye was administered. Two to three serial samples followed at 10 min intervals. Blood samples were kept on ice until centrifuged the same day for 10 min at 3400 revs min−1. Plasma was kept frozen for a maximum of 3 months, when samples were thawed and centrifuged for 10 min. Plasma optical densities were determined at 624 and 740 nm following El-Sayed, Goodall & Hainsworth (1995), with modifications by Foldager & Blomqvist (1991). Adjusted absorbances were logarithmically transformed and linear regression used to determine dye concentration at time of injection. If the regression was not significant or the line's slope was positive (two 6-month pups and three 23-month juveniles), adjusted absorbance values were averaged (Jørgensen et al. 2001; Arnould et al. 2003). Plasma volume was calculated as distributional volume of injected dye (El-Sayed et al. 1995). myoglobin Biopsies were collected from the dorsal triceps and pectoralis complex locomotor muscles to analyze Mb. Additionally, we obtained muscle opportunistically from 10 fresh carcasses, ranging in age from 1 week to adult. Samples were frozen at −80 °C until analyses. We determined Mb following methodology detailed in Reynafarje (1963), as modified by Castellini & Somero (1981). Buffer blanks and elephant seal muscle of known Mb were used as assay controls. total oxygen stores We determined total available O2 stores by adding stores in blood, muscle and lungs (Lenfant et al. 1970; Kooyman et al. 1983; Kooyman 1989). Blood O2 stores were calculated as the sum of arterial and venous O2: where Vb is blood volume, 0·33 is the percentage arterial blood, 0·66 is the percentage venous blood, (capacitance coefficient of O2 in blood) = Hb × 1·34 mL O2, and is O2 saturation of venous blood. An O2 carrying capacity of 1·34 mL O2 (g−1) was assumed (Kooyman 1989). We also assumed 75% of arterial blood O2 was available during a dive (with 15% used to maintain vital body and brain functions; 95% O2 saturation to 20%: Ponganis et al. 1997c; Costa et al. 2001) and mixed venous blood had an O2 content 5% by volume less than initial (Ponganis et al. 1993), so = [( – 50) ()−1] × 100 (Davis & Kanatous 1999). Muscle O2 stores were calculated using the equation: where 0·3 is the fraction of muscle mass in the body (Kooyman et al. 1983). This is also identical to the fraction of muscle mass found from complete dissection of 1-month Steller sea lion Eumetopias jubatus pups (Richmond et al. 2006). For two 23-month-old juveniles for which muscle biopsies were not available, mean Mb determined for the age class was used to calculate muscle O2. Following Costa et al. (2001), lung O2 stores were derived from allometric estimates of lung volume for otariids: where Vi (diving lung volume) = 0·5 × 0·10 × mass0·95 and 0·15 FO2 is O2 extracted from air in the lungs (Kooyman et al. 1971; Kooyman 1989). field metabolic rates (fmr) Concurrent measurements of CO2 production and diving behaviour were carried out on eight of the 23-month Australian sea lions and the one 3-year-old to determine at-sea metabolism using oxygen-18 doubly-labelled water (Lifson & McClintock 1966; Nagy & Costa 1980; Speakman 1997). For comparison with published adult FMR, methodologies were identical to Costa & Gales (2003). Pre-injection blood samples were taken to determine isotope background values, followed by intraperitoneal injections of 60–80 mL 15% oxygen-18 water (H218O) and 18·5 MBq/mL tritiated water (HTO) in 3 mL sterile saline. Syringes were weighed ( ± 0·001 g) before and after injections to determine masses injected. After 3 h equilibration, body mass was recorded and a 10 mL blood sample collected to determine isotope concentrations at the start of the experimental period. Juveniles were equipped with Wildlife Computers (Redmond, WA, USA) time/depth recorders (TDR's) and VHF radio transmitters (Sirtrack Ltd, Havelock, New Zealand) (Fowler et al. 2006). Juveniles were recaptured after 5–8 days to record body mass, collect final blood samples, and recover TDR's. Tritium specific activity was determined by scintillation spectrometry (Tri-Carb 2100TR, Packard, Canberra, ACT, Australia) of duplicate aliquots 0·2 mL pure water (distilled from plasma samples) in 10 mL scintillation fluid (Ultima Gold scintillation fluid, Packard Bio Science, Meriden, CT, USA). Specific activity of H218O was determined by mass ratio spectro-metry (Metabolic Solutions, Nashua, NH, USA). Initial dilutions of H218O were used to determine total body water (TBW) (Nagy & Costa 1980). Final TBW was calculated by the equation from initial TBW corrected for change in mass. We calculated lean body mass from TBW, assuming a hydration constant of 74·2% reported for California sea lions Zalophus californianus (Oftedal, Iverson & Boness 1987), and calculated CO2 production using Speakman's (1997) two-pool model to correct for errors associated with isotope fractionation. Water influx was calculated using equations (5) and (6) in Nagy & Costa (1980), assuming an exponentially changing body water pool. As Australian sea lions' diet is not well-known and six juveniles were observed suckling at least once during the field season, we followed calculations for Steller sea lion juveniles (Richmond et al. 2006) and used a respiratory quotient (RQ) of 0·76 (19·3 kJ L−1 O2). This assumes a 50 : 50 lipid : protein fuel source intermediate between nursing pups' lipid-rich diet and foraging adult's protein-rich diet (Schmidt-Nielsen 1997; Iverson, Frost & Lang 2002). Assuming a diet of 100% lipid or 100% protein alters the RQ by less than 5%. We divided CO2 production by RQ to determine O2 consumption. Data collected over measurement intervals included variable amounts of onshore FMR and were normalized to estimate metabolism at-sea. Percentages of time spent at-sea were calculated from TDR data and following methods from Costa & Gales (2003) for adult Australian sea lions, we plotted FMR data (containing both at-sea and onshore components) as a function of percentage time spent at-sea. Least squares linear regression was used to predict FMR for each animal at their respective percentage time spent at-sea (Costa & Gales 2003). The difference (residual) between predicted and actual FMR was added to extrapolated FMR where the animal spent 0% time at-sea to determine onshore metabolism. At-sea FMR was calculated from the equation: FMR = at-sea FMR (% time at-sea) + onshore FMR (% time ashore). calculated aerobic dive limit (cadl) We calculated cADL's based on equations from Kooyman et al. (1980, 1983): cADL (min) = total O2 (available blood O2+ muscle O2+ lung O2) (at-sea FMR)−1. Dive behaviour data recorded from these juveniles and reported in Fowler et al. (2006) were used to calculate percentages of dives over cADL and ratios of mean dive duration to cADL. For comparison with at-sea FMR, we substituted estimates of otariid DMR from the literature and recalculated cADL's for juvenile Australian sea lions. Hastie, Rosen & Trites (2006) used metabolic rates of Steller sea lion females trained to dive to depth in the open ocean to construct a model predicting O2 consumption. Although some studies have shown during prolonged breath-holds adult pinnipeds may lower metabolism to resting (Hurley & Costa 2001; Sparling & Fedak 2004), young pinnipeds have less metabolic control and juvenile Weddell seals Leptonychotes weddellii appear unable to do so; cADL's based on resting metabolism (RMR) overestimated ADL's indicated by changes in LA by 60% (Rea & Costa 1992; Ponganis et al. 1993; Burns & Castellini 1996). We therefore chose 2 × RMR (determined by multiplying BMR by age-specific scaling factors estimated for Steller sea lions: Winship, Trites & Rosen 2002) to represent minimum cost of transport (Feldkamp 1987; Costa 1991; Arnould & Boyd 1996). Finally, based on the only direct measurements of ADL in an otariid, we used a value of 17·8 mL O2 min−1 kg−1 determined by measuring post-submersion blood LA in similarly-sized (41·4 kg) juvenile California sea lions (Ponganis et al. 1997c). Using the different estimates of DMR, surface metabolic rates (MR) were then calculated from: at-sea FMR = DMR (% time diving) + surface MR (% surface time). When statistical differences were determined by one-way analysis of variance, post-hoc comparisons were made using Tukey tests. If transforming data did not achieve normality and equal variances, differences were determined by Kruskal–Wallis one-way analysis of variance on ranks and Dunn's post-hoc test was used. Results haematology Australian sea lions had fully developed adult Hct and Hb by 15 months (Table 1). Six-month pups were the only age class with significantly lower Hct and Hb (Hct: H3 = 28·85, P < 0·001; Hb: H3 = 24·21, P < 0·001). Values for adult females agree closely with published values for this species (Costa et al. 2001). As there were no significant differences between sexes within age classes, data were combined (t-test: t7 = 0·11, P = 0·92). There were no significant differences between age classes for MCHC (F3,46 = 2·19, P = 0·10), which remained relatively constant throughout development and was 34·6 ± 0·5 g/dL at 6 months, 35·4 ± 0·9 g/dL at 15 months, 38·5 ± 0·6 g/dL at 23 months and 35·8 ± 1·1 g/dL for adult females. Table 1. Summary of O2 storage parameters for different age classes of Australian sea lions (mean ± SE); * = values significantly different from adult. Ranges of ages are reported in parentheses following mean ages and n is given in parentheses below other values. Although hematocrit and haemoglobin were fully developed by 15 months, plasma volume, blood volume, and muscle myoglobin were slower to develop Age (months) Mass (kg) Hematocrit (%) Haemoglobin (g dL−1) Plasma volume (L) Plasma volume (mL kg−1) Blood volume (L) Blood volume (mL kg−1) Myoglobin (g%) 6·1 ± 0·2 (5·4–7·1) 30·0 ± 1·7* (10) 39·3 ± 1·0* (10) 13·6 ± 0·5* (10) 1·6 ± 0·1* (7) 52·4 ± 5·4* (7) 2·6 ± 0·2* (7) 83·5 ± 7·5* (7) 0·8 ± 0·2* (4) 14·5 ± 0·2 (13·4–15·7) 44·5 ± 2·0* (10) 51·4 ± 0·7 (10) 18·2 ± 0·4 (10) 2·0 ± 0·2* (10) 45·6 ± 3·4* (10) 4·2 ± 0·4* (10) 93·8 ± 7·1* (10) 1·3 ± 0·1* (5) 22·6 ± 0·2 (22·1–22·9) 48·3 ± 2·6* (9) 49·5 ± 1·0 (9) 19·0 ± 0·4 (9) 2·8 ± 0·3* (8) 60·1 ± 4·1 (8) 5·7 ± 0·6* (8) 120·9 ± 8·6* (8) 1·6 ± 0·2* (6) 3 years 65·0 (1) 51·6 (1) 19·6 (1) 4·4 (1) 68·0 (1) 9·1 (1) 140·6 (1) 2·2 (1) Adult 88·2 ± 2·1 (21) 51·7 ± 0·5 (21) 18·6 ± 0·6 (21) 6·7 ± 1·3 (2) 83·7 ± 12·5 (2) 14·2 ± 3·0 (2) 178·3 ± 30·9 (2) 2·7 ± 0·1 (3) plasma volume Plasma and blood volumes were slower to develop (Table 1). Well beyond the age of average weaning, 23-month juveniles demonstrated mass-specific blood volumes only 68% of adult blood volumes. Pups had significantly lower mass-specific plasma and blood volumes than adult females (plasma volume: F3,20 = 6·89, P = 0·002; blood volume: F3,20 = 10·03, P < 0·001) and although plasma volumes for 23-month juveniles were lower than adult values, this was not significant (P = 0·08). Plasma volume was 10% of lean body mass in both juvenile and adult Australian sea lions. myoglobin Muscle Mb increased linearly with age (r2 = 0·82, P < 0·001) and mass (r2 = 0·80, P < 0·001). However, development was comparatively slow: 23-month juveniles only developed Mb to 60% of adult capacities (Table 1). Muscle Mb was significantly different across age classes (F4,16 = 49·63, P < 0·001), with the exception of values between 15 and 23 months (P = 0·07). The measured Mb for adult females (2·7 ± 0·1 g/100 g wet tissue) agrees closely with the published value (2·8 g%) and the difference is within the assay's resolution (Costa et al. 2001). total oxygen stores Mass-specific blood, muscle and total O2 stores were significantly higher in older animals (blood: F3,20 = 19·28, P < 0·001; muscle: F3,14 = 58·46, P < 0·001; total: F3,27 = 56·73, P < 0·001) and had not reached adult capacities by 23 months (Fig. 1). Even by 3 years, mass-specific blood O2 was only 29·0 mL O2 kg−1, muscle O2 was 8·7 mL O2 kg−1 and total stores were 43·8 mL O2 kg−1 (78% of adult total stores). Total available mass-specific O2 stores increased significantly with age (r2 = 0·66, P < 0·001) and mass (r2 = 0·70, P < 0·001). Figure 1Open in figure viewerPowerPoint Mean mass-specific O2 stores for different age classes of Australian sea lions. Each bar's height represents total stores and bars are divided into three shades to depict different storage compartments. The percentage of total O2 represented by each compartment is written in the bar. Mean and maximum dive depth (Fig. 2a,b), and mean (r2 = 0·51, P < 0·001), and maximum dive duration (r2 = 0·56, P < 0·001) increased with increasing O2 stores (Fowler et al. 2006). Figure 2Open in figure viewerPowerPoint Total mass-specific O2 stores in relation to dive depth for different age classes of Australian sea lions (Fowler et al. 2006). Symbols represent individual animals. (a) Mean (r2 = 0·67, P < 0·001) and (b) maximum (r2 = 0·68, P < 0·001) dive depth increased significantly with O2 stores. field metabolic rates (fmr) Mean FMR for 23-month juveniles was 15·44 ± 1·30 mL O2 min−1 kg−1 (see Appendix for FMR data). Field metabolism for the 3-year-old was 18·25 mL O2 min−1 kg−1. Mass-specific FMR's were slightly higher for juveniles than values calculated for adult Australian sea lions using Speakman's (1997) two-pool model (Costa & Gales 2003), although this was not significant (t27 = 0·26, P = 0·80). At-sea FMR was calculated to be 15·78 ± 1·29 mL O2 min−1 kg−1 at 23 months and 18·41 mL O2 min−1 kg−1 at 3 years. calculated aerobic dive limit (cadl) By dividing total available O2 by at-sea FMR, we found juvenile Australian sea lions developed a cADL of 2·33 ± 0·24 min by 23 months (Table 2). Like adults, juveniles exceeded cADL's on the majority of dives (Table 2). Furthermore, there were no significant differences between ratios of mean dive duration to cADL for adults and juveniles (t17 = –1·29, P = 0·90), indicating both groups exceeded cADL's to similar extents. Table 2. Calculated aerobic dive limits (cADL) for Australian sea lions (mean ± SE). Values for adult females from Costa et al. (2001); * = values significantly different from adult. Masses are presented as means from initial captures and recaptures. At-sea field metabolic rates (FMR) were calculated using equations from Speakman (1997) and corrected for percentage of time spent onshore. Juvenile total available O2 stores were significantly lower than adult (t19=−7·72, P < 0·001), but juveniles exceeded cADL's as often (t16 = 1·81, P = 0·09) Animal ID Age (months) Mean mass (kg) Total available O2 (mL) At-sea FMR (mL O2 min−1) cADL (min) Mean dive duration (min) Dives > cADL (%) Mean dive duration (cADL)−1 AD 22·1 58·5 1456 780·25 1·87 2·96 73·5 1·59 ED 22·4 43·9 1907 659·05 2·89 2·79 63·8 0·96 EL 22·8 40·8 1281 771·07 1·66 2·50 67·4 1·50 FI 22·9 59·8 2421 944·78 2·56 2·50 55·2 0·98 GO 22·2 45·8 1449 526·53 2·75 2·80 67·8 1·02 LE 22·6 50·1 1698 1005·45 1·66 2·61 78·2 1·58 WI 22·8 41·5 1619 468·87 3·45 3·70 69·5 1·07 MA 22·9 41·1 1519 834·47 1·82 2·14 66·9 1·18 Juvenile mean 22·6 ± 0·1 47·7 ± 2·7* 1668·8 ± 126·2* 748·81 ± 66·67* 2·33 ± 0·24 2·75 ± 0·16* 67·8 ± 2·8 1·23 ± 0·10 SC 3 years 67·7 2849 1246·57 2·29 2·75 68·70 1·20 Cow mean Adult 77·8 ± 3·8 3656·0 ± 179·0 1589·91 ± 101·53 2·34 ± 0·11 3·14 ± 0·16 79·4 ± 4·8 1·38 ± 0·11 There were no significant differences between DMR's determined from FMR, at-sea FMR, predicted O2 consumption, 2 × RMR, and post-submersion LA (F4,38 = 1·41, P = 0·25: Table 3). The mass-specific value predicted for Steller sea lions diving to 50 m was remarkably similar to FMR and at-sea FMR measurements for juvenile Australian sea lions diving to depths of 44 ± 4 m (Fowler et al. 2006; Hastie et al. 2006; Table 3). There were also no significant differences between percentages of dives over cADL (F4,33 = 0·44, P = 0·78), ratios of mean dive duration to cADL (F4,38 = 1·16, P = 0·35), or surface MR (F4,30 = 0·10, P = 0·98; Table 3). Table 3. Summary of different diving metabolic rates (DMR) used to calculate aerobic dive limits (cADL) in juvenile Australian sea lions (n= 8, mean ± SE). Field metabolism (FMR) was determined using doubly-labelled water (Lifson & McClintock 1966); at-sea FMR (bold) was corrected for percentage of time spent onshore. For co
Referência(s)