Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

E., Kroeger, Caitlin; E., Crocker, Daniel; A., Orben, Rachael; R., Thompson, David; G., Torres, Leigh; M., Sagar, Paul; A., Sztukowski, Lisa; Timothy, Andriese,; P., Costa, Daniel; A., Shaffer, Scott

doi:10.1242/jeb.228585

Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

E., Kroeger, Caitlin;E., Crocker, Daniel;A., Orben, Rachael;R., Thompson, David;G., Torres, Leigh;M., Sagar, Paul;A., Sztukowski, Lisa;Timothy, Andriese,;P., Costa, Daniel;A., Shaffer, Scott 2020-12-01 00:00:00 © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 RESEARCH ARTICLE Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies 1, ,‡ 2 3 4 5 Caitlin E. Kroeger * , Daniel E. Crocker , Rachael A. Orben , David R. Thompson , Leigh G. Torres , 6 7,8 9 10 9 Paul M. Sagar , Lisa A. Sztukowski , Timothy Andriese , Daniel P. Costa and Scott A. Shaffer KEY WORDS: Seabirds, Doubly labeled water, Field metabolic rate, ABSTRACT Foraging behavior, Daily energy expenditure, GPS tracking, Understanding the environmental and behavioral factors that Life history influence how organisms maintain energy balance can inform us about their potential resiliency to rapid environmental changes. INTRODUCTION Flexibility in maintaining energy balance is particularly important to Animals adjust their behavior to maintain homeostasis when energy long-lived, central-place foraging seabirds that are constrained when costs become too great (Schneider, 2004), such as during extreme locating food for offspring in a dynamic ocean environment. To temperature or weather events (Wingfield, 2013). For example, understand the role of environmental interactions, behavioral Arabian oryx (Oryx leucoryx) shift to nocturnal foraging as flexibility and morphological constraints on energy balance, we environmental heat loads increase (Hetem et al., 2012) and little used doubly labeled water to measure the at-sea daily energy penguins (Eudyptula minor) increase dive frequency to locate expenditure (DEE) of two sympatrically breeding seabirds, Campbell dispersed prey after storm surges (Pelletier et al., 2012). However, if (Thalassarche impavida) and grey-headed (Thalassarche behavioral changes are energetically maladaptive (e.g. if increased chrysostoma) albatrosses. We found that species and sexes had dives do not increase foraging success; Berlincourt and Arnould, similar foraging costs, but DEE varied between years for both species 2015), long-lived animals may favor self-maintenance over and sexes during early chick rearing in two consecutive seasons. For breeding, as predicted by life-history theory (Costa, 1991; both species, greater DEE was positively associated with larger Stearns, 1992), and populations may decline (Tuomainen and proportional mass gain, lower mean wind speeds during water Candolin, 2011). Species with long-lived individuals depend on −1 take-offs, greater proportions of strong tailwinds (>12 m s ), and phenotypic (e.g. physiological or behavioral) plasticity to adjust younger chick age. Greater proportional mass gains were to the rapid pace of climate change (Reed et al., 2011). Thus, marginally more costly in male albatrosses that already have studying behavioral strategies and environmental factors that higher wing loading. DEE was higher during flights with a greater can influence how individuals maintain energy balance may proportion of strong headwinds for grey-headed albatrosses only. inform us about a population’s short-term resiliency to rapid Poleward winds are forecasted to intensify over the next century, environmental changes. which may increase DEE for grey-headed albatrosses that heavily Environmental factors can affect the energy balance of organisms use this region during early chick rearing. Female Campbell in addition to intrinsic variability from factors such as breeding albatrosses may be negatively affected by forecasted slackening status or sex (Schneider, 2004; Wingfield et al., 2011). The problem winds at lower latitudes due to an expected greater reliance on less of maintaining energy balance in a changing world is acutely energy efficient sit-and-wait foraging strategies. Behavioral plasticity relevant to breeding seabirds that face a multitude of climate-driven associated with environmental variation may influence future and human-induced environmental challenges (Croxall et al., 2012; population responses to climate change of both species. Daunt and Mitchell, 2013). Seabirds are central-place foragers, thus constrained by both time and distance when locating patchily Department of Ocean Sciences, 1156 High Street, University of California at Santa distributed food during the energetically intensive breeding season Cruz, Santa Cruz, CA 95064, USA. Department of Biology, Sonoma State 3 (Ydenberg et al., 1994). Accordingly, when changes occur in the University, 1801 E Cotati Avenue, Rohnert Park, CA 94928, USA. Department of Fisheries and Wildlife, Oregon State University, 2030 SE Marine Science Drive, accessibility or abundance of resources, individuals can incur Newport, OR 97365, USA. National Institute of Water and Atmospheric Research energy deficits that influence reproductive investment (Kitaysky Ltd (NIWA), 301 Evans Bay Parade, Hataitai, Wellington 6021, New Zealand. et al., 2010; Suryan et al., 2006; Thorne et al., 2015; Weimerskirch, Department of Fisheries and Wildlife, Marine Mammal Institute, Oregon State University, 2030 SE Marine Science Drive, Newport, OR 97365, USA. National 2007). When individuals are near their energetic limits, extrinsic Institute of Water and Atmospheric Research Ltd (NIWA), 10 Kyle Street, Riccarton, perturbations have a greater impact on energy balance and can affect Christchurch 8011, New Zealand. Marine Biology & Ecology Research Centre, reproductive success and survival (Elliott et al., 2014; Weiner, Plymouth University, Plymouth PL4 8AA, UK. Department Commonwealth of the Northern Mariana Islands, Department of Lands and Natural Resources, Division of 1992). In some cases, however, external changes can be Fish and Wildlife, PO Box 10007, Saipan, MP 96950. Department of Biological energetically beneficial. For example, wandering albatrosses Sciences, San Jose State University, One Washington Square, San Jose, CA 95192, USA. Department of Ecology and Evolution, University of California (Diomedea exulans) showed improved energy intake and Santa Cruz, Santa Cruz, CA 95062, USA. reproductive success from strengthening wind patterns that have *Present address: Farallon Institute, 101 H Street Suite Q, Petaluma, CA 94954, reduced commute times to foraging habitat in the Southern Ocean USA. (Weimerskirch et al., 2012). Author for correspondence ([email protected]) The energetics of long-lived seabirds foraging at sea has been well studied, particularly in albatrosses that are well known for their C.E.K., 0000-0002-7797-4386; L.A.S., 0000-0002-1418-7211 energy-efficient soaring flight (Costa and Prince, 1987; Sachs et al., Received 10 May 2020; Accepted 12 October 2020 2012; Shaffer et al., 2001a, 2004; Weimerskirch et al., 2000; Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Table 1. Sample sizes for each species and year to depict data usage Weimerskirch et al., 2005). However, few studies have integrated measures of daily energy expenditure (DEE) from related, Campbell Grey-headed sympatrically breeding species that exhibit contrasting foraging albatrosses albatrosses strategies and life histories across multiple breeding seasons (but see 2011 2012 2011 2012 Antolos et al., 2017). Comparing the energetic cost of differing Initial sample size 17 20 14 20 chick provisioning strategies from sister groups – and sexes within Missing tracks, only TBW estimated0120 those groups – may highlight the relative efficiency of certain Missing tracks, DEE estimated 1300 strategies. From this comparison of strategies, combined with DLW technique failure 5124 examining energetic responses to environmental variability across Final sample size (male/female) 11 (6/5) 15 (8/7) 10 (7/3) 16 (11/5) years, we can improve our understanding of life-history patterns and Individuals without tracks or final samples were still used to estimate total body which populations may be advantaged or disadvantaged when water (TBW) and for predictive equations in the single-sample method. If responding to forecasted environmental changes. tracking data were missing but departure and arrival times were recorded, individuals were still used for estimates of daily energy expenditure (DEE). In this study, we measure the at-sea DEE of two congeneric Birds with doubly labeled water (DLW) technique failure were excluded from seabird species with contrasting foraging strategies and life the estimation of TBW and DEE. histories – the Campbell (Thalassarche impavida) and grey- headed (Thalassarche chrysostoma) albatrosses – during early chick rearing across 2 years. Campbell albatrosses are annually Field procedures breeding neritic foragers with a population that steeply declined Nest attendance was monitored starting in late incubation to obtain from 1996 to 1984 but showed an increasing trend until the last two pre-trip fasting durations. Mates were differentiated using decades (Sagar, 2014; Waugh et al., 1999c). Grey-headed non-toxic, temporary livestock paint sprayed on the breast albatrosses are biennially breeding oceanic foragers and the feathers. After eggs hatched, an adult from each pair was captured population on Campbell Island, New Zealand, has been in just before departure to sea. A background blood sample was continuous decline since the 1940s, potentially as a result of collected (0.5–1 ml) from a tarsal or brachial vein with a 22-gauge environmental conditions (Waugh et al., 1999c). However, this needle and 1 ml syringe then transferred into dry spray-coated decline has shown signs of stabilizing in the last two decades (Sagar, lithium heparin blood collection tubes (BD Vacutainer plastic in 2014). Our objective was to measure energetic costs of foraging 2011; BD Vacutainer glass in 2012). Doubly labeled water across species, sexes and years, and to identify important behavioral (DLW; 1.8 ml) containing 0.9% NaCl with 42.15 atom percent 18 −13 18 and environmental factors that influence variations in DEE. We excess (APE) O and 5.39 MBq g H (2011) or 43.70 APE O −13 18 −1 hypothesize that (1) the biennially breeding grey-headed albatrosses and 5.91 MBq g H (2012) or 43.87 APE O and 5.91 MBq g will have higher DEE, as high breeding costs are thought to cause a H (also 2012) was then injected intraperitoneally (2011) or deferral of reproduction in favor of self-maintenance in the intramuscularly (2012). Syringes containing DLW were weighed following year (Ryan et al., 2006), consistent with life-history before and after injection on the same surface using a portable theory, and (2) differences in DEE between years or sexes for both balance. Prior to each weight, the same empty syringe was weighed species are driven by environmental (e.g. wind speed or sea surface for calibration. Annually, a subset of six to eight birds from each temperature) differences across years or foraging areas. This study species were contained for an equilibration period of 90 min illuminates the phenotypic plasticity of seabirds and identifies (Shaffer et al., 2001b), after which a second blood sample was energetically expensive environmental conditions, enabling us to obtained for the calculation of total body water (TBW) (Nagy and better anticipate population-level impacts of environmental Costa, 1980). This subset approach allowed us to use the single- changes. sample method of determining TBW on the remaining birds to minimize disturbance and potential changes in natural behaviors MATERIALS AND METHODS (Schultner et al., 2010; Speakman, 1997). Ethics statement After DLW injection, birds were weighed using a spring-loaded Field research was carried out under the following approvals and Pesola scale (to nearest 25 g). To calculate an index of body size for permits: San Jose State University Institutional Animal Care and estimating body condition, the minimum bill depth, maximum bill Use Committee Protocol no. 976 and New Zealand Wildlife Act length and tarsus length were measured with calipers to the nearest Permit no. SO-26385-FAU. Blood samples were imported into the 0.02 mm, and a relaxed wing chord was measured using a wing chord USA for analysis using permits issued by the United States ruler from the bend in the wrist to the tip of the primaries to the nearest Department of Agriculture Animal and Plant Health Inspection 1 mm. To measure foraging behaviors, GPS devices [igot-U, GT-120 Service (USDA-APHIS; 119370). (2011) or GT-600 (2012), Mobile Action Technology Inc.], were secured to dorsal feathers with Tesa cloth tape. All devices were Study species and site removed from their original plastic casing and waterproofed with Campbell albatrosses, Thalassarche impavida (Mathews 1912), and heat-shrink tubing before deployment (total package mass <32 g with grey-headed albatrosses, Thalassarche chrysostoma (Forster 1785), tape) and each recorded a position at 10 min (2011) or 5 min (2012) were studied during the guard stage (early chick rearing) in intervals. Once birds returned from foraging trips, they were captured December 2011 and 2012. Both species breed in adjoining colonies and a final blood sample (final 1) was collected to measure isotope at Bull Rock located on the north cape of Campbell Island (52°S, turnover (Lifson and McClintock, 1966). Birds were weighed to 169°E), New Zealand Subantarctic territory. Pairs raise one chick measure mass change and GPS devices were removed. For birds that per breeding season and, for 3 weeks post-hatch, mates alternate remained on the nest for another 24–48 h guarding the chick, an between foraging trips at sea and guarding the nest (Warham, 1990). additional mass measurement and a second final blood sample Each season, up to 20 Campbell and 20 grey-headed albatrosses (final 2) were collected. were sampled to measure DEE, foraging behavior and mass In December 2011, samples were packaged and stored in a cool gain (Table 1). location (approximately 10°C) until they could be frozen (−20°C) in Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 January 2012. The following year, blood samples were stored in a subtracting the GPS-determined at-sea time from the total time from cooler with icepacks until they could be transported (within injection to the final sample. 1–6 days) to a solar-charged battery-powered freezer (−15°C, Waeco CF18 fridge/freezer). Samples were then stored at −80°C in Calculation of daily energy expenditure −1 January 2013. All samples were transported from New Zealand to Production of CO was converted to a measure of DEE (kJ day ; the USA on dry-ice and subsequently stored at −80°C. Gessaman and Nagy, 1988). This was calculated using a conversion −1 −1 factor of 26.74 J ml (grey-headed albatross) or 26.58 J ml Estimates of energy expenditure (Campbell albatross) (Adams et al., 1986; Costa and Prince, 1987). Laboratory analysis These constants were created based on the protein (P), lipid (L) and Whole blood samples were used because samples could not be carbohydrate (C) composition of fecal DNA relative read abundance centrifuged before red blood cells lysed. A portion of each sample derived diet from breeding Campbell albatrosses consisting of was distilled using a variation of the freeze-capture method (Ortiz approximately 40% fishes, 37% jellyfish, 22% crustacea and 1% et al., 1978) and the distillate was measured in triplicate in 7 ml cephalopod (McInnes et al., 2017), and a combination of stomach EcoLite(+) scintillation cocktail (MP Biomedicals, Solon, OH, content and temperature-logger derived diets from grey-headed USA) with a scintillation spectrometer (Beckmann LS3801) to albatrosses consisting of approximately 72% squid, 25% jellyfish determine specific activity of the H isotope. The specific activity of and 3% fish (Catry et al., 2004a; Waugh et al., 1999b). The energy the O isotope was measured by isotope-ratio mass spectrometry equivalents of CO were approximated using the dry mass of (Metabolic Solutions, Nashua, NH, USA). nutrients per 100 g of diet (see equation for birds in appendix B of Gessaman and Nagy, 1988). The dry masses of nutrients from each Calculation of total body water, pool sizes and water flux dietary component were weighted by relative proportions in the Total body water was calculated from the dilution space of the O species-specific diet, and then summed. The dry masses of P, L and isotope using an equation from Nagy (1983; see their Appendix I) to C that were used, respectively, for each dietary component account for changes in percentage of TBW across the foraging trip were: 53.3 g P, 37.1 g L and 5.2 g C for fish (Lenky et al., 2012); (Shaffer et al., 2006). This was compared against the dilution space 57.9 g P, 32.9 g L and 0.7 g C for squid (Eder and Lewis, 2005); 3 3 from the H isotope to assess the percentage of error ( H typically over- 16.5 g P, 0.5 g L and 0.9 g C for jellyfish (Doyle et al., 2007); and estimates the body water pool by about 4%; Nagy and Costa, 1980; 8.2 g P, 14.0 g L and 3.5 g C for crustacea (Holland and Walker, Shaffer et al., 2006; Speakman, 1997). The plateau approach was also 1975). Cost of flight was then calculated for each species following 18 3 used to estimate the Oand H dilution spaces of the isotopes with Costa and Prince (1987) as: [DEE −(% trip on water×mean at-sea eqn 17.11 from Speakman (1997). The percent mass approach was DEE )]/(1−% trip on water). on-nest used to estimate final 1 and final 2 TBW (Speakman, 1997). The dilution space ratio of each bird and the ratio of mean isotopic turnover Sex determination 3 18 rates of Hto O were calculated to ensure reliable estimates of CO Bird sexes were identified from background blood samples by production, and any birds that had dilution space ratios outside 0.97– amplification of the sex chromosomes using polymerase chain 1.1 or turnover rate ratios outside 0.5–0.9 were excluded from further reaction (PCR) methods described in Quintana et al. (2008) with energetics calculations (Table 1; Speakman, 1997). For single- minor modifications. The molecularly determined sexes matched sampled birds, the initial isotope enrichments and pool sizes were 99% of observation-based estimates of sex when both adults of a estimated from linear models derived from the two-sample birds using pair were present and sexual size dimorphism was apparent; initial body mass and moles of injectate as predictors (Speakman, however, these observations are not likely to be more accurate than −1 −1 1997). Water influx and efflux (ml kg day ) were calculated using the molecular methods as copulation or egg-laying was not eqns 4 and 6, respectively, from Nagy and Costa (1980). observed. For birds without background blood samples (N=3), sex was assigned with discriminant function analyses using post- Calculation of CO production foraging mass, minimum bill depth and wing chord morphometric −1 −1 CO production (ml g h ) was calculated using a one-pool data (Dechaume-Moncharmont et al., 2011). The Campbell method: eqn 2 from Nagy (1980). Nagy’s (1980) one-pool equation albatross data were supplemented with molecularly sexed birds was used for analyses because this method adjusts for changes in from a previous study (N=37; Sztukowski et al., 2017). Box’s water space and is potentially more accurate for species that have M-tests confirmed homogeneity of the variance–covariance higher elimination rates, which is probable for seabirds foraging in matrices of the morphometric measurements for each species the ocean and ingesting seawater with prey (Shaffer, 2011; (‘biotools’; da Silva et al., 2017). Discriminant function analysis Speakman and Hambly, 2016). This approach has also been used correctly assigned the sex of Campbell albatrosses 79% of the time in other studies of albatross energetics (Antolos et al., 2017; Shaffer with a cut-off of 0.10 (N=68), and correctly assigned the sex of grey- et al., 2001a, 2003), which facilitated comparison with this previous headed albatrosses 87% of the time with a cut-off of 0.30 (N=31; research. Nevertheless, results derived from Speakman’s (1997) regression equations in Kroeger et al., 2019). one-pool method are also reported. To account for periods of inactivity after release and before recapture (Costa and Prince, 1987; Morphometrics Shaffer et al., 2001a), all estimates of CO production were Wing loading corrected using on-nest CO production derived from subtracting Wing traces were used from 10 random individuals of each species to the CO production calculated with final sample 2 from the CO calculate wing loading and wing aspect ratios (Pennycuick, 2008). 2 2 production calculated with final sample 1. The average on-nest CO Surface area of the wing was determined following the methods of production for each species was applied in the following equation Shaffer et al. (2001a), with the exception that the mean shoulder for the birds without final sample 2 to calculate at-sea CO width (19.5 cm, N=20) of black-browed albatrosses, Thalassarche production: (total CO production×total time−nest-only CO ×total melanophrys, breeding on Kerguelen Island (49°S, 70°E) was used to 2 2 nest time)/total at-sea time. Total nest time was determined by estimate the root-box (S.A.S., unpublished data) as these data were Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 not collected for grey-headed and Campbell albatrosses from this Foraging behavior study. In addition, mean masses of grey-headed and Campbell Before calculating foraging trip metrics, raw GPS data were filtered −1 albatrosses were used to calculate wing loading. to remove points that produced speeds >150 km h and rediscretized at 10 min intervals (‘adehabitatLT’; Calenge, 2006). Body condition A high cut-off speed was chosen based on the ability of albatrosses −1 The body condition of birds from each species was determined after to gain fast (>127 km h ), sustained travel speeds during storm increasing the sample size with measurements from additional field events (Catry et al., 2004b). Points over land were identified seasons (Campbell albatross: N=68; grey-headed albatross: N=121). (ArcGIS) to separate on-land and at-sea behaviors and were Morphometric measurements (minimum bill depth, maximum bill excluded from further analyses along with any points at the length and tarsus) were reduced with principle components analysis beginning of trips that overlapped with doubly labeled water into a single body size index (Shaffer et al., 2001c) taken from the equilibration periods. Foraging trip metrics (i.e. total trip duration, scores of the first principal component (PC1 explained 59% maximum range, total distance and mean ground speed) were then variance in Campbell albatrosses and 64% variance in grey-headed calculated. Density utilization maps were created after removing albatrosses; ‘biotools’; da Silva et al., 2017). Body condition was transit points (classification described below) to map foraging calculated from the residuals of body mass on PC1 (i.e. size- areas using a smoothing factor of 1.5% (33.9 km) and cell size of corrected mass) as this index has been shown to be a better predictor 0.2% (4.5 km) of the mean X and Y data spatial extents, allowing of total lipids in Procellariiformes with high percentage body lipids us to optimize visualization at any scale (‘adehabitatHR’; Calenge, (Jacobs et al., 2012). 2006; Fig. 1). Fig. 1. Kernel density estimates depicting foraging patterns during the guard stage for AB Campbell and grey-headed albatrosses in 2011 and 2012. Campbell albatross density is shown in red; grey-headed albatross density shown in blue. Top panels: 2011; bottom panels: 2012. Arrowheads depict monthly (December) wind direction and speed, measured at 1000 mb atmospheric pressure from a base period of 1971 to 2000, with the size of the arrow head scaled to the magnitude of the wind speed. The dashed lines delineate the Subantarctic (upper) and Polar (lower) Fronts. The black star represents breeding colony on Campbell Island. Inset is provided for orientation on the globe. Map boundaries: 45°S to 65°S and 157.5°E to 172.5°W. CD 0 500 Kilometers Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 To classify behavioral states at sea, data points corresponding to significant and three-way ANOVAs were re-run to report F-statistics area restricted search (ARS), rest and transit were identified using and P-values. Differences in the mean angle of the wind on the bird the residence space and time (RST) method with dynamically scaled were tested separately for each term with circular ANOVAs radii as described by Torres et al. (2017). To correct potentially (‘circular’). For the linear ANOVAs, residuals were visually −1 misidentified resting points, all points with speeds <5 km h were inspected for normality and heteroscedasticity. Where assigned as rest. During the guard stage, albatrosses typically only assumptions of normality were violated, variables were log rest on the water after landing for a feeding event because take-offs transformed (DEE, water influx, initial body mass), Box–Cox are energetically expensive (Shaffer et al., 2001a; Weimerskirch power transformed ( O percentage TBW, mean air flight speed, et al., 2000). The proportion of time spent on the water during a mean T at rest; boxcox, ‘MASS’; Venables and Ripley, 2002), or SS foraging trip was calculated using all rest locations divided by the analysed using a gamma distribution (pre-trip fasting, post-trip nest total number of locations. The number of daily take-offs from the time; ‘gamlss’; Rigby and Stasinopoulos, 2005). In the case of water, which we equated to foraging effort as defined by daily water proportion variables with high zero frequency (percentage light landings, were calculated from the number of transitions from rest to winds, percentage strong head/tailwinds), a compound Poisson- ARS or transit divided by the length of the foraging trip in days. gamma distribution was used (‘tweedie’; Dunn and Smyth, 2008). Foraging effort is relative rather than absolute because successive Welch’s two-sample t-tests were used to compare body condition water landings can occur within 10 min intervals (Weimerskirch indices across years for each species, and paired t-tests were used to and Guionnet, 2002). Foraging success was determined by the assess changes in body condition after foraging. Power analysis was proportion of mass gained relative to the birds’ initial body mass. used to determine the difference in DEE between species that would be significant (P=0.05) at 80% power ( pwr.2p2n.test, ‘pwr’; https:// Environmental metrics CRAN.R-project.org/package=pwr). −1 Wind and sea surface temperature data extraction DEE (kJ day ) was regressed on: foraging metrics (foraging Ocean surface wind vectors (meridional and zonal at 10 m altitude) duration, daily distance, maximum range, daily take-offs, and sea surface temperature (T ) were extracted at 31 km grid cell percentage rest on water, mean flight air speed), environmental SS and 3 h resolution from the ERA5 climate re-analysis dataset along metrics (mean wind speed at take-off, percentage light winds, the albatross tracks. At the recorded mean maximum bird ground percentage strong headwinds, percentage strong tailwinds, −1 speed (∼25 m s ) from this study, an albatross should have at least percentage crosswinds, mean wind bearing on bird, wind-drift one point within gridded datasets. compensation magnitude, mean T ) and morphometrics (body SS condition before and after foraging, percentage body mass gain) Wind and sea surface temperature interactions with species, year and sex as factors (lm, base R 3.3). Highly First, the bearing of each bird between consecutive locations was correlated variables and variables with variance inflation factors calculated (a=6378137, f=1/298.26; bearing, ‘geosphere’; https:// (VIF) >4 were removed backwards stepwise from a base linear CRAN.R-project.org/package=geosphere). Bird ground speed was model (vif, ‘car’; Fox and Weisberg, 2011). The number of daily reduced to vector components and the bird air speed was then landings and percentage light wind were negatively correlated with calculated as described by Shamoun-Baranes et al. (2007). The mean take-off wind speed; thus, the former two were removed. bearing of the wind towards each bird location was calculated in Body condition after foraging, daily distance, maximum range, degrees as 180×(1+atan2(u,v)/pi), where u and v are wind mean wind speed and mean flight air speed were also removed. The components in the east and north direction, respectively. The remaining variables were placed into a global model that was bearing of the wind towards the bird relative to bird flight direction automatically subset to generate a list of models (dredge, ‘MuMIn’; was then calculated as the wind bearing subtracted from the bird https://CRAN.R-project.org/package=MuMIn). A model was bearing with 360 added to values <0. The angle of the wind on the selected from the list using model.avg on a subset with ΔAIC less bird was converted to a single side of the bird (0 to 180 deg) than 2. After selecting the most important variables, continuous and for assessment of wind effects from head to tail irrespective of binary interactions were tested. A model was selected based on lowest the side of the bird, and the mean angle was calculated AICc scores and greatest weights. A second model was run with the (circular.mean, ‘circular’; https://r-forge.r-project.org/projects/ addition of chick age, time on nest before departure and duration of circular/). The magnitude of flight compensation for the wind previous foraging trip, and these results are presented separately from compared with drift was estimated for transit states as described by the first model due to sample size reduction (N=52 to N=47). Any Tarroux et al. (2016). variables identified as important in the second model were tested in The percentage of strong headwinds experienced during the trip the first, and vice versa, and the AIC scores and weights were −1 was calculated as the proportion of winds >12 m s and from 330 evaluated again to refine the final models. Residuals from each model to 360 deg and 0 to 30 deg during flight (ARS and transit states). were visually assessed to meet assumptions of normality and The percentage of strong tailwinds was similarly calculated, but for homoscedasticity. All analyses were run in R 3.1.0 and R 3.3.3 angles between 150 and 210 deg. The percentage of light winds was (https://www.R-project.org/) unless stated otherwise. R packages are −1 calculated using speeds less than 5 m s at any angle. The delimited with apostrophes and functions are italicized. percentage of crosswinds was calculated for all wind speeds at angles between 60 and 120 deg and 140 and 300 deg. Finally, the RESULTS mean T experienced was calculated from periods of contact with Final sample sizes for each species by field season and sex are SS the water (i.e. rest). provided in Table 1. Mean chick age during initial sampling was 2.6 days older in grey-headed albatross compared with Campbell Statistical analysis albatross (Table S1). Time fasting on the nest before trips was Differences in energy expenditure, foraging behavior and equivalent across species, sex and years (Table S1). Time on the nest environmental conditions between species and years were tested after foraging before capture was also equivalent across species, sex with three-way ANOVAs. Interaction terms were removed when not and years (Table S1). Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Fig. 2. Updated allometric relationship between body mass and daily energy expenditure for albatross species on logarithmic scale. Regression line includes: Species black-browed (Thalassarche melanophrys, BBA), black- BBA footed (Phoebastria nigripes, BFA), Campbell (Thalassarche impavida, CAA), grey-headed BFA (Thalassarche chrysostoma, GHA Bird Island and GHA CAA Campbell Island), Indian yellow-nosed (Thalassarche carteri, IYA), Laysan (Phoebastria immutabilis, LAA) and GHA (Bird Island) shy albatrosses (Thalassarche cauta, SHA), and female GHA (Campbell Island) and male wandering albatrosses (Diomedea exulans, WAAf IYA and WAAm; see appendix A in Shaffer, 2011 and Antolos et al., 2017). The allometric equation is LAA DEE=0.98+0.66×body mass. SHA WAAf WAAm 2000 3000 5000 10,000 Body mass (g) Total body water, water flux and energy expenditure condition was greater than pre-foraging condition only in Campbell The effect of species on TBW varied by year and sex, with highest albatrosses in 2011 (t=−4.0, d.f.=10, P=0.003). estimated total body water in male grey-headed albatrosses in 2012 (60%) and the lowest estimated in female Campbell albatrosses in Foraging behaviors 2012 (50%; Table S1). Moreover, male grey-headed albatrosses had Campbell albatross foraging was primarily concentrated over the 8% lower TBW in 2011 compared with 2012 (Table S1). These Campbell Plateau northeast of Campbell Island in both years, with TBW values are consistent with previously reported ranges in some foraging extending over deeper waters southward towards the Thalassarche albatrosses (Antolos et al., 2017; Costa and Prince, Subantarctic Front (Fig. 1A,B). The maximum range for individuals 1987; Shaffer et al., 2004). Water influx rate was higher in grey- was similar across years, but Campbell albatrosses – particularly −1 headed albatrosses by 32% (63 ml day ) in 2012 compared with females – traveled less daily distance in 2011 with slower airspeeds −1 2011, and by 26% (54 ml day ) compared with Campbell albatrosses in 2012 (Table S1). There were no significant 2.5 differences in water influx rate between years in Campbell albatrosses, between species in 2011, or between sexes (Table S1). The mean DEE of both species were above the regression line for the allometric equation for smaller albatrosses (Fig. 2; adjusted 2.0 −1 from Antolos et al., 2017): mean DEE was 2039±571 kJ day (655± −1 −1 −1 172 kJ kg day ) for Campbell albatrosses and 2163±672 kJ day −1 −1 (684±223 kJ kg day ) for grey-headed albatrosses. Mean DEE 1.5 was 29% higher for Campbell albatrosses in 2011 compared with 2012 and 23% higher for grey-headed albatrosses in 2011 compared with 2012, but was similar between species and sex (Table S1). 1.0 −1 −1 Power analysis determined that a difference of 491 kJ kg day would have been required to detect a significant difference between species at 80% power. The power to detect the observed difference was low at 0.11; however, a logistically challenging sample size of 340 individuals from each group would have been required. Campbell and grey-headed albatross field metabolic rates (FMR) at sea were both 2.2 times greater than their estimated basal metabolic rates (BMR; Ellis and Gabrielsen, 2002; Fig. 3) and, respectively, Fig. 3. Relative differences in energy expenditure across albatross 2.1 and 2.2 times greater than FMR on the nest. species based on expressing field metabolic rate as a multiple of basal metabolic rate. FMR, field metabolic rate; BMR, basal metabolic rate. The Morphometrics horizontal line at 2BMR represents the mean ratio across species. Bars are Grey-headed albatrosses had greater wing loading than Campbell ordered by body mass from largest to smallest. Blue bars represent −2 albatrosses breeding in the North Pacific and green bars represent those albatrosses (118 versus 109 N m ; t=−2.7, d.f.=12.4, P=0.019). breeding in the Southern Ocean. Light green bars represent albatrosses Likewise, estimated mean aspect ratio of grey-headed albatrosses from this study. The figure includes: wandering (Diomedea exulans, WAA), was higher than Campbell albatrosses (14.3 versus 13.5; t=−3.6, shy (T. cauta, SHA), black-browed (T. melanophrys, BBA), grey-headed d.f.=11.9, P=0.004). (T. chrysostoma, GHA from Bird Island and Campbell Island), black-footed Within both Campbell albatrosses and grey-headed albatrosses, (P. nigripes, BFA), Campbell (T. impavida, CAA), Laysan (P. immutabilis, LAA), pre-foraging and post-foraging body condition (size-corrected and Indian yellow-nosed albatrosses (T. carteri, IYA; see Appendix A; mass) did not differ across years (P>0.05). Post-foraging body Shaffer, 2011 and Antolos et al., 2017). WAA SHA BBA GHA (Bird Island) BFA GHA (Campbell Island) CAA LAA IYA −1 DEE (kJ day ) FMR (multiples of BMR) Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 than in 2012 (Table S2). Additionally, in 2011 Campbell albatrosses year. However, female Campbell albatrosses experienced almost performed 45% more daily water take-offs and spent a greater zero strong tailwinds, while female grey-headed albatrosses percentage of their foraging trip on the water (48 versus 25% in experienced the greatest, although the amount was minimal at 2% 2012; Table S2) and gained less mass as a proportion of their pre- (Table S3). The mean proportion of light winds experienced varied trip body mass (1.8 versus 10% in 2012; Table S1). Moreover, between species depending on year and sex: female Campbell females spent 30% more time on the water than males in 2011, albatrosses experienced twice the mean amount of light winds despite a similar number of take-offs and proportional mass gain during flight of all individuals during 2012 (9.1%), while male (Tables S1 and S2). Campbell albatrosses experienced almost no light winds during Grey-headed albatross foraging was concentrated southeast near flight (0.4%; Table S3). The mean proportion of crosswinds in flight the shelf of the Campbell Plateau and between the Subantarctic and was lowest for female Campbell albatrosses at only 18% in 2011 Polar Fronts (Fig. 1C,D). The maximum range for individuals was compared with roughly 48% for female grey-headed albatrosses in similar between years, but grey-headed albatrosses traveled shorter 2011 (Table S3). daily distances in 2011 with slower air speeds (Table S2). In 2011, The mean bearing of the wind on birds during flight was only slightly more daily water take-offs were detected, and birds consistent between species, sexes and years, with birds primarily spent a greater percentage of their foraging trip on the water (34% experiencing crosswinds (Table S3). No significant differences or versus 19%; Table S2). Proportional mass gain was also lower for interactions between species, sex and year were found in the grey-headed albatross in 2011 (11% versus 18% of pre-trip body magnitude of compensation for the wind during transit (Table S2). mass; Table S1). In contrast to Campbell albatrosses, female grey- Mean T encountered by birds on the water was lower for grey- SS headed albatrosses spent less time on the water and had the fastest air headed albatrosses by about 2°C (Table S3). Mean T at rest for all SS speeds compared with males, despite similar take-offs and individuals ranged from 3.2 to 9.4°C; however, female Campbell proportional mass gain (Tables S1 and S2). albatrosses did not travel to waters below 4°C, unlike male For both species and years, males had further maximum ranges Campbell albatrosses. and longer foraging trips than females (Table S2). In both years, grey-headed albatrosses exhibited greater trip duration, daily Factors influencing daily energy expenditure distance, maximum range, air speed and proportional mass gain Linear models were tested to identify factors that influenced DEE, compared with Campbell albatrosses (Tables S1 and S2). In 2011, and two final models are presented. Model 1 has a larger sample size Campbell albatrosses performed significantly more daily water (N=52) but does not include chick age. When chick age was take-offs than grey-headed albatrosses and spent a larger portion of included in Model 2, the sample size was reduced (N=47). In their foraging trips on the water (Table S2). Model 2, younger chicks were associated with greater DEE in adults (Table 2). Year had the largest effect in both models, with higher Environmental metrics DEE in 2011 (Table 2), although this effect was largely influenced Mean wind speeds encountered by Campbell and grey-headed by male albatrosses in 2011 (Fig. 4A). There were no significant −1 albatrosses were, respectively, 2.2 and 1.3 m s higher in 2012 interactions of year with any other variable. Mass gain positively compared with 2011. Female grey-headed albatrosses encountered affected DEE in both models, with males marginally expending greater mean wind speeds than female Campbell albatrosses more energy to achieve higher proportional mass gain than females −1 (2.3 m s higher average), but windspeeds experienced by males in Model 2 (Fig. 4B). Species had no main effect on DEE, but the did not differ between species (Table S3). Correspondingly, wind effect of the proportion of high headwinds on DEE depended on speeds during water take-offs were lowest for female Campbell species, with a positive relationship observed only in grey-headed albatrosses in 2011 and highest for female grey-headed albatrosses albatrosses (Table 2; Fig. 4C). Species also interacted with mean in 2012 (Table S3). There were no significant differences in the take-off wind speed in Model 1 (Table 2). In this model, mean take- proportions of strong headwinds experienced across species, sex or off wind speed did not significantly affect DEE in Campbell Table 2. Linear model assessing factors influencing DEE during early chick rearing Model 1 (N=52) Model 2 (N=47) Standardized β Centered β coefficient Standardized β Centered β coefficient ¶ ¶ ‡ ¶ Year −0.74 −919 (−1182, −655) −1.08 −1380 (−1640, −1120) ‡ ‡ ‡ ‡ Sex −0.44 −547 (−871, −224) −0.38 −784 (−1070, −501) Species −0.62 −71.3 (−281, 138) −0.35 −39.3 (−221, 142) ¶ ¶ Chick age n.a. n.a. −0.50 −63.5 (−83.4, −43.5) § § ¶ ¶ Mass gain (%) 0.42 26.0 (14.3, 37.6) 0.66 41.5 (27.4, 55.6) High headwind in flight (%) −0.29 −106 (−182, −29.7)* 0.06 24.7 (−46.9, 96.3) § § High tailwind in flight (%) −− 0.33 122 (58.1, 186) § § Mean wind speed at take-off 0.09 27.2 (−46.7, 101) −0.36 −106 (−158, −53.7) ‡ ‡ § § Year: sex 0.42 597 (208, 987) 0.56 825 (467, 1180) Mass gain (%): sex –– −0.38* −25.1 (−44.1, −6.21)* ¶ ¶ ¶ ¶ High headwind in flight (%): species 0.80 430 (299, 561) 0.52 282 (167, 397) ‡ ‡ Mean wind speed at take-off: species −1.30 −157 (−259, −55.2) –– ¶ ¶ ¶ ¶ Intercept 0.00 2770 (2530, 3020) 0.00 3080 (2860, 3310) 2 2 R (adjusted R ) 0.59 (0.49) 0.78 (0.72) Residual standard error 429 338 ¶ ¶ F statistic 5.96 (d.f.=10, 41) 11.5 (d.f.=11, 35) −1 ‡ § ¶ The dependent variable was DEE (kJ day ). Model 85% confidence intervals are given in parentheses. *P<0.1; P<0.05; P<0.01; P<0.001. n.a., not applicable. Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 AB C Female Campbell Male Grey-headed 2500 3000 2011 2012 010 20 30 0246 Year Mass gain (%) High head winds (%) Fig. 4. Interaction plot depicting predicted daily energy expenditure regressed against year by sex, mass gain as a percentage of pre-foraging body mass by sex and the proportion of high headwinds during foraging by species. DEE was fitted from the Model 2 (Table 2) function using (A) grey-headed albatrosses, (B) grey-headed albatrosses in 2011 or (C) males in 2011 and the means of the remaining independent variables in the model (predict function, R 3.3). The trend for plot C is representative of each year and species as these factors did not differ in slope, only intercept. Likewise, the trend in plot B is representative of each sex and year as slopes did not differ; however, the intercept for males was lower than females for both species in 2012 (and both intercepts in 2012 were lower than 2011). Bars represent standard error of the fit. albatrosses (estimate=27.3, s.e.=50.4, t=0.54, P=0.59; outcome was unexpected based on the contrasting life-history ‘interactions’ package, R 3.3) but, relative to Campbell patterns of these species, as biennial instead of annual breeding is albatrosses, DEE was higher at low take-off wind speeds and suggested to result from the need to recover body condition after lower at high take-off windspeeds for grey-headed albatrosses higher breeding costs resulting from time and energy deficits (Fig. 5). Finally, the proportion of high tailwinds positively (Jouventin and Dobson, 2002; Ryan et al., 2006). We note that it is −1 influenced DEE in Model 2 (Table 2). possible that a difference (>491 kJ day ) was not detected due to our low sample size. However, significant annual differences in DISCUSSION DEE were detected at this sampling magnitude. Biennially breeding Campbell and grey-headed albatrosses exhibited similar DEE while grey-headed albatrosses also had greater wing loading due to both foraging during the guard-stage, including when physiological, morphological differences and greater proportional mass gains at behavioral and environmental conditions were considered. This sea, which we expected to contribute to higher foraging costs in lower wind fields. However, these birds are probably aided by the use of favorable wind fields associated with their preferred foraging location along the Antarctic Circumpolar Current (Fig. 1; Wakefield et al., 2009; Weimerskirch et al., 2000), including high wind speeds at take-off that influenced lower DEE. Male albatrosses of both Campbell 4000 species expended more energy to achieve high proportional mass Grey-headed gain compared with females with similar proportional mass gains. Again, this result is consistent with greater wing loading in male albatrosses (Phillips et al., 2004; Shaffer et al., 2001c). However, we found that males had higher DEE in 2011 when their mass gain was lower than that observed in 2012. DEE was higher in 2011 overall (for both species and sexes), consistent with more daily take-offs and lower take-off wind speeds during foraging. High headwinds and tailwinds both increased DEE, but greater proportions of high headwinds had a greater effect on DEE in grey-headed albatrosses despite similar proportions experienced by both species. Finally, grey-headed albatross parents had older chicks when sampled pre-trip, and parents with older chicks expended less energy while foraging, but the cost associated with achieving higher mass gains (e.g. greater food loads) may explain why DEE was not lower than observed for 0 5 10 15 Campbell albatrosses. −1 Mean take-off wind speed (m s ) Fig. 5. Interaction plot depicting predicted daily energy expenditure Species differences in daily energy expenditure regressed against mean take-off wind speed by species. Daily energy Campbell and grey-headed albatrosses had similar energy expenditure (DEE) was fitted from the Model 1 (Table 2) function using male expenditures at sea compared with other Thalassarche species albatrosses in 2011 and the means of the remaining independent variables in relative to both body size and BMR (with the exception of the much the model (predict function, R 3.3). The trend is representative of each sex and smaller Indian yellow-nosed albatross, Thalassarche carteri, which year as these factors did not differ in slope, only intercept. Bars represent standard error of the fit. appear to be even more economical; Figs 2 and 3). Campbell and −1 DEE (kJ day ) −1 DEE (kJ day ) Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 grey-headed albatrosses had similar absolute and mass-corrected Morphology and foraging success DEE during guard-stage foraging trips due to similarities in mean Higher lipid reserves in guard-stage Campbell albatrosses relative to body mass. Both species had smaller mean body mass and lower grey-headed albatrosses could be associated with wing loading absolute DEE at sea than late chick-rearing grey-headed albatrosses differences (this study and Warham, 1977), where lower wing from Bird Island (Costa and Prince, 1987) and incubation-stage loading in Campbell albatrosses allows for accessing more energy- black-browed albatrosses from Kerguelen Island (Shaffer et al., dense prey in lighter winds further north during the incubation stage 2004). These differences in mass and absolute DEE could be a result (Furness and Bryant, 1996; Louzao et al., 2014; Sztukowski, 2015; of breeding stage (Shaffer et al., 2003); however, incubating Wakefield et al., 2009). The proportion of light winds experienced Campbell albatrosses (Kroeger et al., 2019) are still 24% smaller in varied by species, sex and year, but female Campbell albatrosses mass than incubating black-browed albatrosses (Shaffer et al., generally experienced the greatest proportion of lighter winds. Their 2004), and grey-headed albatrosses on Campbell Island are known DEE, however, was less affected by light winds at take-off, perhaps to be smaller than conspecifics elsewhere (Waugh et al., 1999a). because lower wing loading reduced effort relative to male Moreover, grey-headed albatrosses from Bird Island and black- Campbell albatrosses and grey-headed albatrosses under these browed albatrosses have more energy-dense diets than the conditions. Campbell albatrosses also have lower aspect ratios that respective Campbell Island species (Clarke and Prince, 1980; increases maneuverability in lighter winds and may aid in foraging McInnes et al., 2017; Waugh et al., 1999b; Xavier et al., 2003), efficiency (Pennycuick, 2008; Phillips et al., 2004; Rayner, 1988). which should produce larger individuals with greater energy We were unable to directly test the effect of wing loading because requirements. The absolute energy requirements of black-browed we did not have wing measurements from individuals that were albatrosses may contribute to their near-absence from breeding on sampled for energy expenditure. However, differences in wing Campbell Island relative to the endemic Campbell albatross (ACAP, loading between species probably has a functional significance (e.g. 2009), especially if black-browed albatrosses do not raise young as flight costs) given that wing morphologies are believed to restrict the successfully on lower energy income. This could be tested by breeding ranges of other albatross species (Suryan et al., 2008). measuring DEE from guard-stage black-browed albatrosses The DEE of both Campbell and grey-headed albatrosses is higher breeding on Campbell Island for a more direct comparison, if a relative to body mass compared with other albatross species (Fig. 3), sufficient sample size could be found. as expected from Southern Ocean species that forage in more The similar guard-stage costs of Campbell albatrosses and grey- productive waters than North Pacific albatrosses (Antolos et al., headed albatrosses on Campbell Island were inconsistent with our 2017; Shaffer, 2011). Species that can gain more energy should be predictions based on their differing life histories and foraging willing to expend more energy (Jodice et al., 2006). However, strategies. Biennial breeding is thought to result, in part, from higher individuals that gain more mass relative to their body size will also breeding costs associated with traveling further distances to forage, expend more energy due to increased wing loading unless foraging which extends the breeding season and leaves little time to recover in stronger winds where heavier loads increase flight stabilization body reserves before breeding again (Dobson and Jouventin, 2010; and costs can be offset (Pennycuick, 1982; Warham, 1977). Indeed, Jouventin and Dobson, 2002). Indeed, grey-headed albatrosses grey-headed albatrosses recovered a higher proportion of their pre- travel further distances during the guard stage, but breeding duration foraging body mass – as might be expected from this species that for this species overlaps with the annually breeding Campbell consistently traveled further distances to the windy and nutrient-rich albatrosses (chick rearing lasts approximately 116–152 versus Subantarctic Front – yet they did not expend more energy than 130 days, respectively (ACAP, 2010; Moore and Moffat, 1990) and Campbell albatrosses. Within species and years, albatrosses with is shorter than other annual breeders (Jouventin and Dobson, 2002). higher proportional mass gain exhibited greater DEE, especially Therefore, similar foraging costs during the guard stage suggest that males, suggesting that structurally smaller females with lower wing poorer food quality or higher energy deficits incurred during other loading can gain more proportional mass at less cost in similar wind breeding stages (e.g. incubation or late chick-rearing) or post- conditions. Given within-year effects of mass gain, it is notable that breeding may affect the breeding frequency of grey-headed both species gained significantly more proportional mass in 2012 albatrosses (Crossin et al., 2013). Grey-headed albatrosses in when DEE was lower. Foraging behaviors, wind interactions or 2012 were leaner (higher total body water in males) and also had factors not measured, such as preferred prey abundance, are likely higher water influx than Campbell albatrosses, suggesting prey with important drivers of yearly differences in foraging efficiency. lower energy density (e.g. greater proportions of salps). Grey- headed albatrosses primarily forage on squid that contain four to six Foraging behaviors times less calcium and less energy than the krill and fish (Clarke and Individuals that took off from the water in higher wind speeds Prince, 1980) typically consumed by annual breeders (Hedd and expended less energy, consistent with the effect of take-offs on Gales, 2001; Waugh et al., 1999b). However, grey-headed albatross energy expenditure observed in other albatrosses (Sakamoto et al., chicks grow at faster rates and fledge at greater body mass than 2013; Shaffer et al., 2001a; Weimerskirch et al., 2000). When take-off Campbell albatross chicks (Moore and Moffat, 1990). Grey-headed wind speeds were lower, individuals performed more water landings, albatross parents forage in predictable, strong westerly winds that spent more time resting on the water, had lower foraging success and probably offset wing loading and reduce the cost of larger food expended more energy (Tables S1 and S2). Gaining less mass with loads that may compensate for lower quality (Table S1; more water landings and performing more landings in energetically Weimerskirch et al., 2012). A greater allocation of energy to expensive wind speeds are somewhat counterintuitive because birds chicks rather than self-maintenance, however, may necessitate a should limit landings to when food is located to conserve time and longer self-recovery period or influence feather molt timing, which energy during chick rearing (Shaffer et al., 2001a; Weimerskirch could interfere with breeding frequency (Edwards, 2008; et al., 2000). In 2011, Campbell albatrosses that had the highest mean McNamara and Houston, 2008). Additionally, calcium limitation take-off rates also spent a greater proportion of their total trip on the within the adult could delay egg production and lead to biennial water, possibly because certain prey types required more surface time breeding (Edwards, 2008; McNamara and Houston, 2008). to exploit before resuming aerial searching (Weimerskirch, 2007; Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Weimerskirch and Pinaud, 2007). These individuals may have Implications and future directions consumed smaller or less energy-dense prey types such as jellyfish Overall, we were able to link a suite of behavioral, morphometric (McInnes et al., 2017) and employed a sit-and-wait strategy to and environmental measures to variations in DEE in two sympatric conserve energy while optimizing net energy gain (Conners et al., southern albatross species. Although grey-headed albatrosses had 2015; Louzao et al., 2014). In 2011, albatrosses may have employed greater foraging success and similar energy expenditure to this strategy if lower wind speeds reduced in-flight search efficiency Campbell albatrosses, their primary prey source and guard-stage and take-off efficiency (Spear and Ainley, 1997; Wakefield et al., body reserves indicate that grey-headed albatrosses may incur 2009; Weimerskirch et al., 2000). Furthermore, when take-off wind greater self-maintenance costs consistent with their life history as speeds were higher, individuals may have spent less time on the water biennial breeders. Future changes in prey availability are thus an during feeding events, which could have led to under-represented important consideration for future modeling efforts as climate landing frequencies given the sampling interval (10 min) of the GPS change is expected to affect productivity in the Southern Ocean loggers in this study. Thus, mean wind speed at take-off may be a (Constable et al., 2014). In addition, wind fields are projected to more reliable predictor of DEE than the number of take-offs when weaken towards lower latitudes while becoming stronger towards sampling intervals are potentially greater than landing intervals. higher latitudes (Lovenduski and Gruber, 2005; Thompson and Wallace, 2000), which may reduce foraging opportunities for some Environmental interactions species (this study) while enhancing opportunities for others In addition to the effects of proportional mass gain and take-off wind (Weimerskirch et al., 2012). A decrease in wind strength in lower speed, DEE was also affected by the proportion of strong headwinds latitudes where Campbell albatrosses range (Lovenduski and −1 during flight (>12 m s ). Strong headwinds can offset flight Gruber, 2005) could entail more individuals using a less direction and potentially force more energetically expensive energetically efficient sit-and-wait strategy. In contrast, an corrective maneuvering (Louzao et al., 2014; Tarroux et al., 2016; increase in wind strength at higher latitudes where grey-headed Wakefield et al., 2009), particularly in species with higher wing albatrosses range (Lovenduski and Gruber, 2005) could aspect ratios like grey-headed albatrosses. Grey-headed albatrosses increase flight costs. Understanding the factors that influence also encountered higher mean wind speeds than Campbell albatrosses the DEE of animals, such as changing wind fields, is essential (Table S3), so the proportion of strong headwinds encountered should for assessing the vulnerability of species in the face of climate be costlier. Albatrosses are known to use looping flight paths while change. This information is also crucial for management transiting to foraging destinations (Weimerskirch et al., 2000) – efforts, especially as species less tolerant to environmental keeping the wind at low-cost angles – but time and space constraints perturbations may require management to reduce more during early chick-rearing can limit the use of efficient flight remediable stressors (Cooke et al., 2013). strategies (Kroeger, 2019). Accordingly, DEE was higher when the Acknowledgements proportion of strong headwinds was higher for grey-headed We thank the New Zealand Department of Conservation for permitting this project albatrosses compared with Campbell albatrosses under the same and providing logistical support; Henk Haazen and crew for providing safe model conditions. Furthermore, although the consequences of strong transportation to and from Campbell Island; Joy Sagar for field assistance; Kyle Morrison, Ray Bucheit and Rob Dunn for field support; Jen Jelincic for laboratory tailwinds on soaring seabirds has received less attention (but see analysis assistance; Jonathan Felis for geographic information system mapping; Alerstam et al., 2019; Spear and Ainley, 1997) and most cost models and Rachel Holser for providing thoughtful feedback on initial drafts of the do not include this effect (Felicisimo et al., 2008; Louzao et al., 2014; manuscript. We also thank Jeff Pentel and the numerous people listed in the funding Raymond et al., 2010), we found that a greater proportion of strong section for their generous financial donations that made this work possible. tailwinds was also energetically costly for both species. This cost may Competing interests result from light wing loads while transiting from the nest to foraging The authors declare no competing or financial interests. grounds that are primarily downwind (Fig. 1), as this transit occurred when strong tailwinds could be most destabilizing to flight due to Author contributions reduced body mass (Alerstam et al., 2019). Conceptualization: C.E.K., D.E.C., D.P.C., S.A.S.; Methodology: C.E.K.; Formal analysis: C.E.K., D.E.C., S.A.S.; Investigation: C.E.K., D.E.C., R.A.O., P.M.S., L.A.S., T.A.; Resources: D.E.C., D.R.T., L.G.T., P.M.S., L.A.S., T.A., S.A.S.; Writing - The influence of chick age original draft: C.E.K.; Writing - review & editing: D.E.C., R.A.O., D.R.T., L.G.T., Although the sample size decreased when chick age was P.M.S., L.A.S., D.P.C., S.A.S.; Visualization: C.E.K.; Supervision: S.A.S.; Project considered, DEE was found to be lower in parents rearing older administration: D.R.T., L.G.T.; Funding acquisition: D.R.T., L.G.T., P.M.S. chicks. Sampling occurred at roughly the same duration after a foraging trip, but those with larger chicks were probably able to Funding This work was supported by the New Zealand Ministry of Business, Innovation and offload more food to their chick before recapture, weighing and Employment (contract CO1X0905); MARES program (grant FPA 2011-0016); re-sampling (Huin et al., 2000). Partially, or even fully, digested American Ornithologists’ Union; Earl H. and Ethel M. Myers Oceanographic and food in the forestomach may not fully equilibrate with total body Marine Biology Trust; Jim Brown Award; San José State University Graduate water (Ricklefs et al., 1986). Thus, it is conceivable that body water Student Research Award; and crowd-source funding from Experiment.com (individual donors: Jeff Pentel, Wayne Sentman, Jill Marketos Milburn, Laura pool sizes were over-estimated relative to the concentration of Wagner, Mark Kroeger, David Thompson, Sadie Birdfeather, Jen Jelincic, Amy isotopes in the blood at the time of weighing. This effect would Lush, Paul Richard Wagner, Lucius Bono, Scott Shaffer, Beth Flint, Anita Phagan, inflate the estimates of metabolic rate in adults with younger chicks. Cassie Marketos, Anne Cassell, Dan Saltman, Sandra Machado, Herma Van However, in 2012, individuals that were more successful foragers Gerner, Annie Schmidt, Renee Murphy Shaffer, Heather Day, Corey Clatterbuck, and probably retained more stomach contents at the time of re- Emily Nichols, Susy Alarcon Arriaga, Cleo Small, Devon O’Meara, Mary Moskal, Wynter Skye Standish, Rachael Orben, sampling (Huin et al., 2000) had lower DEE that year. Hence it is Hannah Madden, Oscar Jasklowski and Cindy Wu). more likely that as chicks age, food delivery is less frequent, allowing parents to use more energy-efficient foraging strategies to Supplementary information obtain food and maintain homeostasis (Weimerskirch and Lys, Supplementary information available online at 2000; Weimerskirch et al., 2003). https://jeb.biologists.org/lookup/doi/10.1242/jeb.228585.supplemental Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 References Elliott, K. H., Le Vaillant, M., Kato, A., Gaston, A. J., Ropert-Coudert, Y., Hare, ACAP (2009). ACAP Species Assessment: Black-browed Albatross Thalassarche J. F., Speakman, J. R. and Croll, D. (2014). Age-related variation in energy melanophris. Agreement on the Conservation of Albatrosses and Petrels. 1-22. expenditure in a long-lived bird within the envelope of an energy ceiling. J. Anim. ACAP (2010). 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Publisher: The Company of Biologists
Copyright: © 2021 The Company of Biologists. All rights reserved.
ISSN: 0022-0949
eISSN: 0022-0949
DOI: 10.1242/jeb.228585
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Abstract

© 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 RESEARCH ARTICLE Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies 1, ,‡ 2 3 4 5 Caitlin E. Kroeger * , Daniel E. Crocker , Rachael A. Orben , David R. Thompson , Leigh G. Torres , 6 7,8 9 10 9 Paul M. Sagar , Lisa A. Sztukowski , Timothy Andriese , Daniel P. Costa and Scott A. Shaffer KEY WORDS: Seabirds, Doubly labeled water, Field metabolic rate, ABSTRACT Foraging behavior, Daily energy expenditure, GPS tracking, Understanding the environmental and behavioral factors that Life history influence how organisms maintain energy balance can inform us about their potential resiliency to rapid environmental changes. INTRODUCTION Flexibility in maintaining energy balance is particularly important to Animals adjust their behavior to maintain homeostasis when energy long-lived, central-place foraging seabirds that are constrained when costs become too great (Schneider, 2004), such as during extreme locating food for offspring in a dynamic ocean environment. To temperature or weather events (Wingfield, 2013). For example, understand the role of environmental interactions, behavioral Arabian oryx (Oryx leucoryx) shift to nocturnal foraging as flexibility and morphological constraints on energy balance, we environmental heat loads increase (Hetem et al., 2012) and little used doubly labeled water to measure the at-sea daily energy penguins (Eudyptula minor) increase dive frequency to locate expenditure (DEE) of two sympatrically breeding seabirds, Campbell dispersed prey after storm surges (Pelletier et al., 2012). However, if (Thalassarche impavida) and grey-headed (Thalassarche behavioral changes are energetically maladaptive (e.g. if increased chrysostoma) albatrosses. We found that species and sexes had dives do not increase foraging success; Berlincourt and Arnould, similar foraging costs, but DEE varied between years for both species 2015), long-lived animals may favor self-maintenance over and sexes during early chick rearing in two consecutive seasons. For breeding, as predicted by life-history theory (Costa, 1991; both species, greater DEE was positively associated with larger Stearns, 1992), and populations may decline (Tuomainen and proportional mass gain, lower mean wind speeds during water Candolin, 2011). Species with long-lived individuals depend on −1 take-offs, greater proportions of strong tailwinds (>12 m s ), and phenotypic (e.g. physiological or behavioral) plasticity to adjust younger chick age. Greater proportional mass gains were to the rapid pace of climate change (Reed et al., 2011). Thus, marginally more costly in male albatrosses that already have studying behavioral strategies and environmental factors that higher wing loading. DEE was higher during flights with a greater can influence how individuals maintain energy balance may proportion of strong headwinds for grey-headed albatrosses only. inform us about a population’s short-term resiliency to rapid Poleward winds are forecasted to intensify over the next century, environmental changes. which may increase DEE for grey-headed albatrosses that heavily Environmental factors can affect the energy balance of organisms use this region during early chick rearing. Female Campbell in addition to intrinsic variability from factors such as breeding albatrosses may be negatively affected by forecasted slackening status or sex (Schneider, 2004; Wingfield et al., 2011). The problem winds at lower latitudes due to an expected greater reliance on less of maintaining energy balance in a changing world is acutely energy efficient sit-and-wait foraging strategies. Behavioral plasticity relevant to breeding seabirds that face a multitude of climate-driven associated with environmental variation may influence future and human-induced environmental challenges (Croxall et al., 2012; population responses to climate change of both species. Daunt and Mitchell, 2013). Seabirds are central-place foragers, thus constrained by both time and distance when locating patchily Department of Ocean Sciences, 1156 High Street, University of California at Santa distributed food during the energetically intensive breeding season Cruz, Santa Cruz, CA 95064, USA. Department of Biology, Sonoma State 3 (Ydenberg et al., 1994). Accordingly, when changes occur in the University, 1801 E Cotati Avenue, Rohnert Park, CA 94928, USA. Department of Fisheries and Wildlife, Oregon State University, 2030 SE Marine Science Drive, accessibility or abundance of resources, individuals can incur Newport, OR 97365, USA. National Institute of Water and Atmospheric Research energy deficits that influence reproductive investment (Kitaysky Ltd (NIWA), 301 Evans Bay Parade, Hataitai, Wellington 6021, New Zealand. et al., 2010; Suryan et al., 2006; Thorne et al., 2015; Weimerskirch, Department of Fisheries and Wildlife, Marine Mammal Institute, Oregon State University, 2030 SE Marine Science Drive, Newport, OR 97365, USA. National 2007). When individuals are near their energetic limits, extrinsic Institute of Water and Atmospheric Research Ltd (NIWA), 10 Kyle Street, Riccarton, perturbations have a greater impact on energy balance and can affect Christchurch 8011, New Zealand. Marine Biology & Ecology Research Centre, reproductive success and survival (Elliott et al., 2014; Weiner, Plymouth University, Plymouth PL4 8AA, UK. Department Commonwealth of the Northern Mariana Islands, Department of Lands and Natural Resources, Division of 1992). In some cases, however, external changes can be Fish and Wildlife, PO Box 10007, Saipan, MP 96950. Department of Biological energetically beneficial. For example, wandering albatrosses Sciences, San Jose State University, One Washington Square, San Jose, CA 95192, USA. Department of Ecology and Evolution, University of California (Diomedea exulans) showed improved energy intake and Santa Cruz, Santa Cruz, CA 95062, USA. reproductive success from strengthening wind patterns that have *Present address: Farallon Institute, 101 H Street Suite Q, Petaluma, CA 94954, reduced commute times to foraging habitat in the Southern Ocean USA. (Weimerskirch et al., 2012). Author for correspondence ([email protected]) The energetics of long-lived seabirds foraging at sea has been well studied, particularly in albatrosses that are well known for their C.E.K., 0000-0002-7797-4386; L.A.S., 0000-0002-1418-7211 energy-efficient soaring flight (Costa and Prince, 1987; Sachs et al., Received 10 May 2020; Accepted 12 October 2020 2012; Shaffer et al., 2001a, 2004; Weimerskirch et al., 2000; Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Table 1. Sample sizes for each species and year to depict data usage Weimerskirch et al., 2005). However, few studies have integrated measures of daily energy expenditure (DEE) from related, Campbell Grey-headed sympatrically breeding species that exhibit contrasting foraging albatrosses albatrosses strategies and life histories across multiple breeding seasons (but see 2011 2012 2011 2012 Antolos et al., 2017). Comparing the energetic cost of differing Initial sample size 17 20 14 20 chick provisioning strategies from sister groups – and sexes within Missing tracks, only TBW estimated0120 those groups – may highlight the relative efficiency of certain Missing tracks, DEE estimated 1300 strategies. From this comparison of strategies, combined with DLW technique failure 5124 examining energetic responses to environmental variability across Final sample size (male/female) 11 (6/5) 15 (8/7) 10 (7/3) 16 (11/5) years, we can improve our understanding of life-history patterns and Individuals without tracks or final samples were still used to estimate total body which populations may be advantaged or disadvantaged when water (TBW) and for predictive equations in the single-sample method. If responding to forecasted environmental changes. tracking data were missing but departure and arrival times were recorded, individuals were still used for estimates of daily energy expenditure (DEE). In this study, we measure the at-sea DEE of two congeneric Birds with doubly labeled water (DLW) technique failure were excluded from seabird species with contrasting foraging strategies and life the estimation of TBW and DEE. histories – the Campbell (Thalassarche impavida) and grey- headed (Thalassarche chrysostoma) albatrosses – during early chick rearing across 2 years. Campbell albatrosses are annually Field procedures breeding neritic foragers with a population that steeply declined Nest attendance was monitored starting in late incubation to obtain from 1996 to 1984 but showed an increasing trend until the last two pre-trip fasting durations. Mates were differentiated using decades (Sagar, 2014; Waugh et al., 1999c). Grey-headed non-toxic, temporary livestock paint sprayed on the breast albatrosses are biennially breeding oceanic foragers and the feathers. After eggs hatched, an adult from each pair was captured population on Campbell Island, New Zealand, has been in just before departure to sea. A background blood sample was continuous decline since the 1940s, potentially as a result of collected (0.5–1 ml) from a tarsal or brachial vein with a 22-gauge environmental conditions (Waugh et al., 1999c). However, this needle and 1 ml syringe then transferred into dry spray-coated decline has shown signs of stabilizing in the last two decades (Sagar, lithium heparin blood collection tubes (BD Vacutainer plastic in 2014). Our objective was to measure energetic costs of foraging 2011; BD Vacutainer glass in 2012). Doubly labeled water across species, sexes and years, and to identify important behavioral (DLW; 1.8 ml) containing 0.9% NaCl with 42.15 atom percent 18 −13 18 and environmental factors that influence variations in DEE. We excess (APE) O and 5.39 MBq g H (2011) or 43.70 APE O −13 18 −1 hypothesize that (1) the biennially breeding grey-headed albatrosses and 5.91 MBq g H (2012) or 43.87 APE O and 5.91 MBq g will have higher DEE, as high breeding costs are thought to cause a H (also 2012) was then injected intraperitoneally (2011) or deferral of reproduction in favor of self-maintenance in the intramuscularly (2012). Syringes containing DLW were weighed following year (Ryan et al., 2006), consistent with life-history before and after injection on the same surface using a portable theory, and (2) differences in DEE between years or sexes for both balance. Prior to each weight, the same empty syringe was weighed species are driven by environmental (e.g. wind speed or sea surface for calibration. Annually, a subset of six to eight birds from each temperature) differences across years or foraging areas. This study species were contained for an equilibration period of 90 min illuminates the phenotypic plasticity of seabirds and identifies (Shaffer et al., 2001b), after which a second blood sample was energetically expensive environmental conditions, enabling us to obtained for the calculation of total body water (TBW) (Nagy and better anticipate population-level impacts of environmental Costa, 1980). This subset approach allowed us to use the single- changes. sample method of determining TBW on the remaining birds to minimize disturbance and potential changes in natural behaviors MATERIALS AND METHODS (Schultner et al., 2010; Speakman, 1997). Ethics statement After DLW injection, birds were weighed using a spring-loaded Field research was carried out under the following approvals and Pesola scale (to nearest 25 g). To calculate an index of body size for permits: San Jose State University Institutional Animal Care and estimating body condition, the minimum bill depth, maximum bill Use Committee Protocol no. 976 and New Zealand Wildlife Act length and tarsus length were measured with calipers to the nearest Permit no. SO-26385-FAU. Blood samples were imported into the 0.02 mm, and a relaxed wing chord was measured using a wing chord USA for analysis using permits issued by the United States ruler from the bend in the wrist to the tip of the primaries to the nearest Department of Agriculture Animal and Plant Health Inspection 1 mm. To measure foraging behaviors, GPS devices [igot-U, GT-120 Service (USDA-APHIS; 119370). (2011) or GT-600 (2012), Mobile Action Technology Inc.], were secured to dorsal feathers with Tesa cloth tape. All devices were Study species and site removed from their original plastic casing and waterproofed with Campbell albatrosses, Thalassarche impavida (Mathews 1912), and heat-shrink tubing before deployment (total package mass <32 g with grey-headed albatrosses, Thalassarche chrysostoma (Forster 1785), tape) and each recorded a position at 10 min (2011) or 5 min (2012) were studied during the guard stage (early chick rearing) in intervals. Once birds returned from foraging trips, they were captured December 2011 and 2012. Both species breed in adjoining colonies and a final blood sample (final 1) was collected to measure isotope at Bull Rock located on the north cape of Campbell Island (52°S, turnover (Lifson and McClintock, 1966). Birds were weighed to 169°E), New Zealand Subantarctic territory. Pairs raise one chick measure mass change and GPS devices were removed. For birds that per breeding season and, for 3 weeks post-hatch, mates alternate remained on the nest for another 24–48 h guarding the chick, an between foraging trips at sea and guarding the nest (Warham, 1990). additional mass measurement and a second final blood sample Each season, up to 20 Campbell and 20 grey-headed albatrosses (final 2) were collected. were sampled to measure DEE, foraging behavior and mass In December 2011, samples were packaged and stored in a cool gain (Table 1). location (approximately 10°C) until they could be frozen (−20°C) in Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 January 2012. The following year, blood samples were stored in a subtracting the GPS-determined at-sea time from the total time from cooler with icepacks until they could be transported (within injection to the final sample. 1–6 days) to a solar-charged battery-powered freezer (−15°C, Waeco CF18 fridge/freezer). Samples were then stored at −80°C in Calculation of daily energy expenditure −1 January 2013. All samples were transported from New Zealand to Production of CO was converted to a measure of DEE (kJ day ; the USA on dry-ice and subsequently stored at −80°C. Gessaman and Nagy, 1988). This was calculated using a conversion −1 −1 factor of 26.74 J ml (grey-headed albatross) or 26.58 J ml Estimates of energy expenditure (Campbell albatross) (Adams et al., 1986; Costa and Prince, 1987). Laboratory analysis These constants were created based on the protein (P), lipid (L) and Whole blood samples were used because samples could not be carbohydrate (C) composition of fecal DNA relative read abundance centrifuged before red blood cells lysed. A portion of each sample derived diet from breeding Campbell albatrosses consisting of was distilled using a variation of the freeze-capture method (Ortiz approximately 40% fishes, 37% jellyfish, 22% crustacea and 1% et al., 1978) and the distillate was measured in triplicate in 7 ml cephalopod (McInnes et al., 2017), and a combination of stomach EcoLite(+) scintillation cocktail (MP Biomedicals, Solon, OH, content and temperature-logger derived diets from grey-headed USA) with a scintillation spectrometer (Beckmann LS3801) to albatrosses consisting of approximately 72% squid, 25% jellyfish determine specific activity of the H isotope. The specific activity of and 3% fish (Catry et al., 2004a; Waugh et al., 1999b). The energy the O isotope was measured by isotope-ratio mass spectrometry equivalents of CO were approximated using the dry mass of (Metabolic Solutions, Nashua, NH, USA). nutrients per 100 g of diet (see equation for birds in appendix B of Gessaman and Nagy, 1988). The dry masses of nutrients from each Calculation of total body water, pool sizes and water flux dietary component were weighted by relative proportions in the Total body water was calculated from the dilution space of the O species-specific diet, and then summed. The dry masses of P, L and isotope using an equation from Nagy (1983; see their Appendix I) to C that were used, respectively, for each dietary component account for changes in percentage of TBW across the foraging trip were: 53.3 g P, 37.1 g L and 5.2 g C for fish (Lenky et al., 2012); (Shaffer et al., 2006). This was compared against the dilution space 57.9 g P, 32.9 g L and 0.7 g C for squid (Eder and Lewis, 2005); 3 3 from the H isotope to assess the percentage of error ( H typically over- 16.5 g P, 0.5 g L and 0.9 g C for jellyfish (Doyle et al., 2007); and estimates the body water pool by about 4%; Nagy and Costa, 1980; 8.2 g P, 14.0 g L and 3.5 g C for crustacea (Holland and Walker, Shaffer et al., 2006; Speakman, 1997). The plateau approach was also 1975). Cost of flight was then calculated for each species following 18 3 used to estimate the Oand H dilution spaces of the isotopes with Costa and Prince (1987) as: [DEE −(% trip on water×mean at-sea eqn 17.11 from Speakman (1997). The percent mass approach was DEE )]/(1−% trip on water). on-nest used to estimate final 1 and final 2 TBW (Speakman, 1997). The dilution space ratio of each bird and the ratio of mean isotopic turnover Sex determination 3 18 rates of Hto O were calculated to ensure reliable estimates of CO Bird sexes were identified from background blood samples by production, and any birds that had dilution space ratios outside 0.97– amplification of the sex chromosomes using polymerase chain 1.1 or turnover rate ratios outside 0.5–0.9 were excluded from further reaction (PCR) methods described in Quintana et al. (2008) with energetics calculations (Table 1; Speakman, 1997). For single- minor modifications. The molecularly determined sexes matched sampled birds, the initial isotope enrichments and pool sizes were 99% of observation-based estimates of sex when both adults of a estimated from linear models derived from the two-sample birds using pair were present and sexual size dimorphism was apparent; initial body mass and moles of injectate as predictors (Speakman, however, these observations are not likely to be more accurate than −1 −1 1997). Water influx and efflux (ml kg day ) were calculated using the molecular methods as copulation or egg-laying was not eqns 4 and 6, respectively, from Nagy and Costa (1980). observed. For birds without background blood samples (N=3), sex was assigned with discriminant function analyses using post- Calculation of CO production foraging mass, minimum bill depth and wing chord morphometric −1 −1 CO production (ml g h ) was calculated using a one-pool data (Dechaume-Moncharmont et al., 2011). The Campbell method: eqn 2 from Nagy (1980). Nagy’s (1980) one-pool equation albatross data were supplemented with molecularly sexed birds was used for analyses because this method adjusts for changes in from a previous study (N=37; Sztukowski et al., 2017). Box’s water space and is potentially more accurate for species that have M-tests confirmed homogeneity of the variance–covariance higher elimination rates, which is probable for seabirds foraging in matrices of the morphometric measurements for each species the ocean and ingesting seawater with prey (Shaffer, 2011; (‘biotools’; da Silva et al., 2017). Discriminant function analysis Speakman and Hambly, 2016). This approach has also been used correctly assigned the sex of Campbell albatrosses 79% of the time in other studies of albatross energetics (Antolos et al., 2017; Shaffer with a cut-off of 0.10 (N=68), and correctly assigned the sex of grey- et al., 2001a, 2003), which facilitated comparison with this previous headed albatrosses 87% of the time with a cut-off of 0.30 (N=31; research. Nevertheless, results derived from Speakman’s (1997) regression equations in Kroeger et al., 2019). one-pool method are also reported. To account for periods of inactivity after release and before recapture (Costa and Prince, 1987; Morphometrics Shaffer et al., 2001a), all estimates of CO production were Wing loading corrected using on-nest CO production derived from subtracting Wing traces were used from 10 random individuals of each species to the CO production calculated with final sample 2 from the CO calculate wing loading and wing aspect ratios (Pennycuick, 2008). 2 2 production calculated with final sample 1. The average on-nest CO Surface area of the wing was determined following the methods of production for each species was applied in the following equation Shaffer et al. (2001a), with the exception that the mean shoulder for the birds without final sample 2 to calculate at-sea CO width (19.5 cm, N=20) of black-browed albatrosses, Thalassarche production: (total CO production×total time−nest-only CO ×total melanophrys, breeding on Kerguelen Island (49°S, 70°E) was used to 2 2 nest time)/total at-sea time. Total nest time was determined by estimate the root-box (S.A.S., unpublished data) as these data were Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 not collected for grey-headed and Campbell albatrosses from this Foraging behavior study. In addition, mean masses of grey-headed and Campbell Before calculating foraging trip metrics, raw GPS data were filtered −1 albatrosses were used to calculate wing loading. to remove points that produced speeds >150 km h and rediscretized at 10 min intervals (‘adehabitatLT’; Calenge, 2006). Body condition A high cut-off speed was chosen based on the ability of albatrosses −1 The body condition of birds from each species was determined after to gain fast (>127 km h ), sustained travel speeds during storm increasing the sample size with measurements from additional field events (Catry et al., 2004b). Points over land were identified seasons (Campbell albatross: N=68; grey-headed albatross: N=121). (ArcGIS) to separate on-land and at-sea behaviors and were Morphometric measurements (minimum bill depth, maximum bill excluded from further analyses along with any points at the length and tarsus) were reduced with principle components analysis beginning of trips that overlapped with doubly labeled water into a single body size index (Shaffer et al., 2001c) taken from the equilibration periods. Foraging trip metrics (i.e. total trip duration, scores of the first principal component (PC1 explained 59% maximum range, total distance and mean ground speed) were then variance in Campbell albatrosses and 64% variance in grey-headed calculated. Density utilization maps were created after removing albatrosses; ‘biotools’; da Silva et al., 2017). Body condition was transit points (classification described below) to map foraging calculated from the residuals of body mass on PC1 (i.e. size- areas using a smoothing factor of 1.5% (33.9 km) and cell size of corrected mass) as this index has been shown to be a better predictor 0.2% (4.5 km) of the mean X and Y data spatial extents, allowing of total lipids in Procellariiformes with high percentage body lipids us to optimize visualization at any scale (‘adehabitatHR’; Calenge, (Jacobs et al., 2012). 2006; Fig. 1). Fig. 1. Kernel density estimates depicting foraging patterns during the guard stage for AB Campbell and grey-headed albatrosses in 2011 and 2012. Campbell albatross density is shown in red; grey-headed albatross density shown in blue. Top panels: 2011; bottom panels: 2012. Arrowheads depict monthly (December) wind direction and speed, measured at 1000 mb atmospheric pressure from a base period of 1971 to 2000, with the size of the arrow head scaled to the magnitude of the wind speed. The dashed lines delineate the Subantarctic (upper) and Polar (lower) Fronts. The black star represents breeding colony on Campbell Island. Inset is provided for orientation on the globe. Map boundaries: 45°S to 65°S and 157.5°E to 172.5°W. CD 0 500 Kilometers Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 To classify behavioral states at sea, data points corresponding to significant and three-way ANOVAs were re-run to report F-statistics area restricted search (ARS), rest and transit were identified using and P-values. Differences in the mean angle of the wind on the bird the residence space and time (RST) method with dynamically scaled were tested separately for each term with circular ANOVAs radii as described by Torres et al. (2017). To correct potentially (‘circular’). For the linear ANOVAs, residuals were visually −1 misidentified resting points, all points with speeds <5 km h were inspected for normality and heteroscedasticity. Where assigned as rest. During the guard stage, albatrosses typically only assumptions of normality were violated, variables were log rest on the water after landing for a feeding event because take-offs transformed (DEE, water influx, initial body mass), Box–Cox are energetically expensive (Shaffer et al., 2001a; Weimerskirch power transformed ( O percentage TBW, mean air flight speed, et al., 2000). The proportion of time spent on the water during a mean T at rest; boxcox, ‘MASS’; Venables and Ripley, 2002), or SS foraging trip was calculated using all rest locations divided by the analysed using a gamma distribution (pre-trip fasting, post-trip nest total number of locations. The number of daily take-offs from the time; ‘gamlss’; Rigby and Stasinopoulos, 2005). In the case of water, which we equated to foraging effort as defined by daily water proportion variables with high zero frequency (percentage light landings, were calculated from the number of transitions from rest to winds, percentage strong head/tailwinds), a compound Poisson- ARS or transit divided by the length of the foraging trip in days. gamma distribution was used (‘tweedie’; Dunn and Smyth, 2008). Foraging effort is relative rather than absolute because successive Welch’s two-sample t-tests were used to compare body condition water landings can occur within 10 min intervals (Weimerskirch indices across years for each species, and paired t-tests were used to and Guionnet, 2002). Foraging success was determined by the assess changes in body condition after foraging. Power analysis was proportion of mass gained relative to the birds’ initial body mass. used to determine the difference in DEE between species that would be significant (P=0.05) at 80% power ( pwr.2p2n.test, ‘pwr’; https:// Environmental metrics CRAN.R-project.org/package=pwr). −1 Wind and sea surface temperature data extraction DEE (kJ day ) was regressed on: foraging metrics (foraging Ocean surface wind vectors (meridional and zonal at 10 m altitude) duration, daily distance, maximum range, daily take-offs, and sea surface temperature (T ) were extracted at 31 km grid cell percentage rest on water, mean flight air speed), environmental SS and 3 h resolution from the ERA5 climate re-analysis dataset along metrics (mean wind speed at take-off, percentage light winds, the albatross tracks. At the recorded mean maximum bird ground percentage strong headwinds, percentage strong tailwinds, −1 speed (∼25 m s ) from this study, an albatross should have at least percentage crosswinds, mean wind bearing on bird, wind-drift one point within gridded datasets. compensation magnitude, mean T ) and morphometrics (body SS condition before and after foraging, percentage body mass gain) Wind and sea surface temperature interactions with species, year and sex as factors (lm, base R 3.3). Highly First, the bearing of each bird between consecutive locations was correlated variables and variables with variance inflation factors calculated (a=6378137, f=1/298.26; bearing, ‘geosphere’; https:// (VIF) >4 were removed backwards stepwise from a base linear CRAN.R-project.org/package=geosphere). Bird ground speed was model (vif, ‘car’; Fox and Weisberg, 2011). The number of daily reduced to vector components and the bird air speed was then landings and percentage light wind were negatively correlated with calculated as described by Shamoun-Baranes et al. (2007). The mean take-off wind speed; thus, the former two were removed. bearing of the wind towards each bird location was calculated in Body condition after foraging, daily distance, maximum range, degrees as 180×(1+atan2(u,v)/pi), where u and v are wind mean wind speed and mean flight air speed were also removed. The components in the east and north direction, respectively. The remaining variables were placed into a global model that was bearing of the wind towards the bird relative to bird flight direction automatically subset to generate a list of models (dredge, ‘MuMIn’; was then calculated as the wind bearing subtracted from the bird https://CRAN.R-project.org/package=MuMIn). A model was bearing with 360 added to values <0. The angle of the wind on the selected from the list using model.avg on a subset with ΔAIC less bird was converted to a single side of the bird (0 to 180 deg) than 2. After selecting the most important variables, continuous and for assessment of wind effects from head to tail irrespective of binary interactions were tested. A model was selected based on lowest the side of the bird, and the mean angle was calculated AICc scores and greatest weights. A second model was run with the (circular.mean, ‘circular’; https://r-forge.r-project.org/projects/ addition of chick age, time on nest before departure and duration of circular/). The magnitude of flight compensation for the wind previous foraging trip, and these results are presented separately from compared with drift was estimated for transit states as described by the first model due to sample size reduction (N=52 to N=47). Any Tarroux et al. (2016). variables identified as important in the second model were tested in The percentage of strong headwinds experienced during the trip the first, and vice versa, and the AIC scores and weights were −1 was calculated as the proportion of winds >12 m s and from 330 evaluated again to refine the final models. Residuals from each model to 360 deg and 0 to 30 deg during flight (ARS and transit states). were visually assessed to meet assumptions of normality and The percentage of strong tailwinds was similarly calculated, but for homoscedasticity. All analyses were run in R 3.1.0 and R 3.3.3 angles between 150 and 210 deg. The percentage of light winds was (https://www.R-project.org/) unless stated otherwise. R packages are −1 calculated using speeds less than 5 m s at any angle. The delimited with apostrophes and functions are italicized. percentage of crosswinds was calculated for all wind speeds at angles between 60 and 120 deg and 140 and 300 deg. Finally, the RESULTS mean T experienced was calculated from periods of contact with Final sample sizes for each species by field season and sex are SS the water (i.e. rest). provided in Table 1. Mean chick age during initial sampling was 2.6 days older in grey-headed albatross compared with Campbell Statistical analysis albatross (Table S1). Time fasting on the nest before trips was Differences in energy expenditure, foraging behavior and equivalent across species, sex and years (Table S1). Time on the nest environmental conditions between species and years were tested after foraging before capture was also equivalent across species, sex with three-way ANOVAs. Interaction terms were removed when not and years (Table S1). Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Fig. 2. Updated allometric relationship between body mass and daily energy expenditure for albatross species on logarithmic scale. Regression line includes: Species black-browed (Thalassarche melanophrys, BBA), black- BBA footed (Phoebastria nigripes, BFA), Campbell (Thalassarche impavida, CAA), grey-headed BFA (Thalassarche chrysostoma, GHA Bird Island and GHA CAA Campbell Island), Indian yellow-nosed (Thalassarche carteri, IYA), Laysan (Phoebastria immutabilis, LAA) and GHA (Bird Island) shy albatrosses (Thalassarche cauta, SHA), and female GHA (Campbell Island) and male wandering albatrosses (Diomedea exulans, WAAf IYA and WAAm; see appendix A in Shaffer, 2011 and Antolos et al., 2017). The allometric equation is LAA DEE=0.98+0.66×body mass. SHA WAAf WAAm 2000 3000 5000 10,000 Body mass (g) Total body water, water flux and energy expenditure condition was greater than pre-foraging condition only in Campbell The effect of species on TBW varied by year and sex, with highest albatrosses in 2011 (t=−4.0, d.f.=10, P=0.003). estimated total body water in male grey-headed albatrosses in 2012 (60%) and the lowest estimated in female Campbell albatrosses in Foraging behaviors 2012 (50%; Table S1). Moreover, male grey-headed albatrosses had Campbell albatross foraging was primarily concentrated over the 8% lower TBW in 2011 compared with 2012 (Table S1). These Campbell Plateau northeast of Campbell Island in both years, with TBW values are consistent with previously reported ranges in some foraging extending over deeper waters southward towards the Thalassarche albatrosses (Antolos et al., 2017; Costa and Prince, Subantarctic Front (Fig. 1A,B). The maximum range for individuals 1987; Shaffer et al., 2004). Water influx rate was higher in grey- was similar across years, but Campbell albatrosses – particularly −1 headed albatrosses by 32% (63 ml day ) in 2012 compared with females – traveled less daily distance in 2011 with slower airspeeds −1 2011, and by 26% (54 ml day ) compared with Campbell albatrosses in 2012 (Table S1). There were no significant 2.5 differences in water influx rate between years in Campbell albatrosses, between species in 2011, or between sexes (Table S1). The mean DEE of both species were above the regression line for the allometric equation for smaller albatrosses (Fig. 2; adjusted 2.0 −1 from Antolos et al., 2017): mean DEE was 2039±571 kJ day (655± −1 −1 −1 172 kJ kg day ) for Campbell albatrosses and 2163±672 kJ day −1 −1 (684±223 kJ kg day ) for grey-headed albatrosses. Mean DEE 1.5 was 29% higher for Campbell albatrosses in 2011 compared with 2012 and 23% higher for grey-headed albatrosses in 2011 compared with 2012, but was similar between species and sex (Table S1). 1.0 −1 −1 Power analysis determined that a difference of 491 kJ kg day would have been required to detect a significant difference between species at 80% power. The power to detect the observed difference was low at 0.11; however, a logistically challenging sample size of 340 individuals from each group would have been required. Campbell and grey-headed albatross field metabolic rates (FMR) at sea were both 2.2 times greater than their estimated basal metabolic rates (BMR; Ellis and Gabrielsen, 2002; Fig. 3) and, respectively, Fig. 3. Relative differences in energy expenditure across albatross 2.1 and 2.2 times greater than FMR on the nest. species based on expressing field metabolic rate as a multiple of basal metabolic rate. FMR, field metabolic rate; BMR, basal metabolic rate. The Morphometrics horizontal line at 2BMR represents the mean ratio across species. Bars are Grey-headed albatrosses had greater wing loading than Campbell ordered by body mass from largest to smallest. Blue bars represent −2 albatrosses breeding in the North Pacific and green bars represent those albatrosses (118 versus 109 N m ; t=−2.7, d.f.=12.4, P=0.019). breeding in the Southern Ocean. Light green bars represent albatrosses Likewise, estimated mean aspect ratio of grey-headed albatrosses from this study. The figure includes: wandering (Diomedea exulans, WAA), was higher than Campbell albatrosses (14.3 versus 13.5; t=−3.6, shy (T. cauta, SHA), black-browed (T. melanophrys, BBA), grey-headed d.f.=11.9, P=0.004). (T. chrysostoma, GHA from Bird Island and Campbell Island), black-footed Within both Campbell albatrosses and grey-headed albatrosses, (P. nigripes, BFA), Campbell (T. impavida, CAA), Laysan (P. immutabilis, LAA), pre-foraging and post-foraging body condition (size-corrected and Indian yellow-nosed albatrosses (T. carteri, IYA; see Appendix A; mass) did not differ across years (P>0.05). Post-foraging body Shaffer, 2011 and Antolos et al., 2017). WAA SHA BBA GHA (Bird Island) BFA GHA (Campbell Island) CAA LAA IYA −1 DEE (kJ day ) FMR (multiples of BMR) Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 than in 2012 (Table S2). Additionally, in 2011 Campbell albatrosses year. However, female Campbell albatrosses experienced almost performed 45% more daily water take-offs and spent a greater zero strong tailwinds, while female grey-headed albatrosses percentage of their foraging trip on the water (48 versus 25% in experienced the greatest, although the amount was minimal at 2% 2012; Table S2) and gained less mass as a proportion of their pre- (Table S3). The mean proportion of light winds experienced varied trip body mass (1.8 versus 10% in 2012; Table S1). Moreover, between species depending on year and sex: female Campbell females spent 30% more time on the water than males in 2011, albatrosses experienced twice the mean amount of light winds despite a similar number of take-offs and proportional mass gain during flight of all individuals during 2012 (9.1%), while male (Tables S1 and S2). Campbell albatrosses experienced almost no light winds during Grey-headed albatross foraging was concentrated southeast near flight (0.4%; Table S3). The mean proportion of crosswinds in flight the shelf of the Campbell Plateau and between the Subantarctic and was lowest for female Campbell albatrosses at only 18% in 2011 Polar Fronts (Fig. 1C,D). The maximum range for individuals was compared with roughly 48% for female grey-headed albatrosses in similar between years, but grey-headed albatrosses traveled shorter 2011 (Table S3). daily distances in 2011 with slower air speeds (Table S2). In 2011, The mean bearing of the wind on birds during flight was only slightly more daily water take-offs were detected, and birds consistent between species, sexes and years, with birds primarily spent a greater percentage of their foraging trip on the water (34% experiencing crosswinds (Table S3). No significant differences or versus 19%; Table S2). Proportional mass gain was also lower for interactions between species, sex and year were found in the grey-headed albatross in 2011 (11% versus 18% of pre-trip body magnitude of compensation for the wind during transit (Table S2). mass; Table S1). In contrast to Campbell albatrosses, female grey- Mean T encountered by birds on the water was lower for grey- SS headed albatrosses spent less time on the water and had the fastest air headed albatrosses by about 2°C (Table S3). Mean T at rest for all SS speeds compared with males, despite similar take-offs and individuals ranged from 3.2 to 9.4°C; however, female Campbell proportional mass gain (Tables S1 and S2). albatrosses did not travel to waters below 4°C, unlike male For both species and years, males had further maximum ranges Campbell albatrosses. and longer foraging trips than females (Table S2). In both years, grey-headed albatrosses exhibited greater trip duration, daily Factors influencing daily energy expenditure distance, maximum range, air speed and proportional mass gain Linear models were tested to identify factors that influenced DEE, compared with Campbell albatrosses (Tables S1 and S2). In 2011, and two final models are presented. Model 1 has a larger sample size Campbell albatrosses performed significantly more daily water (N=52) but does not include chick age. When chick age was take-offs than grey-headed albatrosses and spent a larger portion of included in Model 2, the sample size was reduced (N=47). In their foraging trips on the water (Table S2). Model 2, younger chicks were associated with greater DEE in adults (Table 2). Year had the largest effect in both models, with higher Environmental metrics DEE in 2011 (Table 2), although this effect was largely influenced Mean wind speeds encountered by Campbell and grey-headed by male albatrosses in 2011 (Fig. 4A). There were no significant −1 albatrosses were, respectively, 2.2 and 1.3 m s higher in 2012 interactions of year with any other variable. Mass gain positively compared with 2011. Female grey-headed albatrosses encountered affected DEE in both models, with males marginally expending greater mean wind speeds than female Campbell albatrosses more energy to achieve higher proportional mass gain than females −1 (2.3 m s higher average), but windspeeds experienced by males in Model 2 (Fig. 4B). Species had no main effect on DEE, but the did not differ between species (Table S3). Correspondingly, wind effect of the proportion of high headwinds on DEE depended on speeds during water take-offs were lowest for female Campbell species, with a positive relationship observed only in grey-headed albatrosses in 2011 and highest for female grey-headed albatrosses albatrosses (Table 2; Fig. 4C). Species also interacted with mean in 2012 (Table S3). There were no significant differences in the take-off wind speed in Model 1 (Table 2). In this model, mean take- proportions of strong headwinds experienced across species, sex or off wind speed did not significantly affect DEE in Campbell Table 2. Linear model assessing factors influencing DEE during early chick rearing Model 1 (N=52) Model 2 (N=47) Standardized β Centered β coefficient Standardized β Centered β coefficient ¶ ¶ ‡ ¶ Year −0.74 −919 (−1182, −655) −1.08 −1380 (−1640, −1120) ‡ ‡ ‡ ‡ Sex −0.44 −547 (−871, −224) −0.38 −784 (−1070, −501) Species −0.62 −71.3 (−281, 138) −0.35 −39.3 (−221, 142) ¶ ¶ Chick age n.a. n.a. −0.50 −63.5 (−83.4, −43.5) § § ¶ ¶ Mass gain (%) 0.42 26.0 (14.3, 37.6) 0.66 41.5 (27.4, 55.6) High headwind in flight (%) −0.29 −106 (−182, −29.7)* 0.06 24.7 (−46.9, 96.3) § § High tailwind in flight (%) −− 0.33 122 (58.1, 186) § § Mean wind speed at take-off 0.09 27.2 (−46.7, 101) −0.36 −106 (−158, −53.7) ‡ ‡ § § Year: sex 0.42 597 (208, 987) 0.56 825 (467, 1180) Mass gain (%): sex –– −0.38* −25.1 (−44.1, −6.21)* ¶ ¶ ¶ ¶ High headwind in flight (%): species 0.80 430 (299, 561) 0.52 282 (167, 397) ‡ ‡ Mean wind speed at take-off: species −1.30 −157 (−259, −55.2) –– ¶ ¶ ¶ ¶ Intercept 0.00 2770 (2530, 3020) 0.00 3080 (2860, 3310) 2 2 R (adjusted R ) 0.59 (0.49) 0.78 (0.72) Residual standard error 429 338 ¶ ¶ F statistic 5.96 (d.f.=10, 41) 11.5 (d.f.=11, 35) −1 ‡ § ¶ The dependent variable was DEE (kJ day ). Model 85% confidence intervals are given in parentheses. *P<0.1; P<0.05; P<0.01; P<0.001. n.a., not applicable. Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 AB C Female Campbell Male Grey-headed 2500 3000 2011 2012 010 20 30 0246 Year Mass gain (%) High head winds (%) Fig. 4. Interaction plot depicting predicted daily energy expenditure regressed against year by sex, mass gain as a percentage of pre-foraging body mass by sex and the proportion of high headwinds during foraging by species. DEE was fitted from the Model 2 (Table 2) function using (A) grey-headed albatrosses, (B) grey-headed albatrosses in 2011 or (C) males in 2011 and the means of the remaining independent variables in the model (predict function, R 3.3). The trend for plot C is representative of each year and species as these factors did not differ in slope, only intercept. Likewise, the trend in plot B is representative of each sex and year as slopes did not differ; however, the intercept for males was lower than females for both species in 2012 (and both intercepts in 2012 were lower than 2011). Bars represent standard error of the fit. albatrosses (estimate=27.3, s.e.=50.4, t=0.54, P=0.59; outcome was unexpected based on the contrasting life-history ‘interactions’ package, R 3.3) but, relative to Campbell patterns of these species, as biennial instead of annual breeding is albatrosses, DEE was higher at low take-off wind speeds and suggested to result from the need to recover body condition after lower at high take-off windspeeds for grey-headed albatrosses higher breeding costs resulting from time and energy deficits (Fig. 5). Finally, the proportion of high tailwinds positively (Jouventin and Dobson, 2002; Ryan et al., 2006). We note that it is −1 influenced DEE in Model 2 (Table 2). possible that a difference (>491 kJ day ) was not detected due to our low sample size. However, significant annual differences in DISCUSSION DEE were detected at this sampling magnitude. Biennially breeding Campbell and grey-headed albatrosses exhibited similar DEE while grey-headed albatrosses also had greater wing loading due to both foraging during the guard-stage, including when physiological, morphological differences and greater proportional mass gains at behavioral and environmental conditions were considered. This sea, which we expected to contribute to higher foraging costs in lower wind fields. However, these birds are probably aided by the use of favorable wind fields associated with their preferred foraging location along the Antarctic Circumpolar Current (Fig. 1; Wakefield et al., 2009; Weimerskirch et al., 2000), including high wind speeds at take-off that influenced lower DEE. Male albatrosses of both Campbell 4000 species expended more energy to achieve high proportional mass Grey-headed gain compared with females with similar proportional mass gains. Again, this result is consistent with greater wing loading in male albatrosses (Phillips et al., 2004; Shaffer et al., 2001c). However, we found that males had higher DEE in 2011 when their mass gain was lower than that observed in 2012. DEE was higher in 2011 overall (for both species and sexes), consistent with more daily take-offs and lower take-off wind speeds during foraging. High headwinds and tailwinds both increased DEE, but greater proportions of high headwinds had a greater effect on DEE in grey-headed albatrosses despite similar proportions experienced by both species. Finally, grey-headed albatross parents had older chicks when sampled pre-trip, and parents with older chicks expended less energy while foraging, but the cost associated with achieving higher mass gains (e.g. greater food loads) may explain why DEE was not lower than observed for 0 5 10 15 Campbell albatrosses. −1 Mean take-off wind speed (m s ) Fig. 5. Interaction plot depicting predicted daily energy expenditure Species differences in daily energy expenditure regressed against mean take-off wind speed by species. Daily energy Campbell and grey-headed albatrosses had similar energy expenditure (DEE) was fitted from the Model 1 (Table 2) function using male expenditures at sea compared with other Thalassarche species albatrosses in 2011 and the means of the remaining independent variables in relative to both body size and BMR (with the exception of the much the model (predict function, R 3.3). The trend is representative of each sex and smaller Indian yellow-nosed albatross, Thalassarche carteri, which year as these factors did not differ in slope, only intercept. Bars represent standard error of the fit. appear to be even more economical; Figs 2 and 3). Campbell and −1 DEE (kJ day ) −1 DEE (kJ day ) Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 grey-headed albatrosses had similar absolute and mass-corrected Morphology and foraging success DEE during guard-stage foraging trips due to similarities in mean Higher lipid reserves in guard-stage Campbell albatrosses relative to body mass. Both species had smaller mean body mass and lower grey-headed albatrosses could be associated with wing loading absolute DEE at sea than late chick-rearing grey-headed albatrosses differences (this study and Warham, 1977), where lower wing from Bird Island (Costa and Prince, 1987) and incubation-stage loading in Campbell albatrosses allows for accessing more energy- black-browed albatrosses from Kerguelen Island (Shaffer et al., dense prey in lighter winds further north during the incubation stage 2004). These differences in mass and absolute DEE could be a result (Furness and Bryant, 1996; Louzao et al., 2014; Sztukowski, 2015; of breeding stage (Shaffer et al., 2003); however, incubating Wakefield et al., 2009). The proportion of light winds experienced Campbell albatrosses (Kroeger et al., 2019) are still 24% smaller in varied by species, sex and year, but female Campbell albatrosses mass than incubating black-browed albatrosses (Shaffer et al., generally experienced the greatest proportion of lighter winds. Their 2004), and grey-headed albatrosses on Campbell Island are known DEE, however, was less affected by light winds at take-off, perhaps to be smaller than conspecifics elsewhere (Waugh et al., 1999a). because lower wing loading reduced effort relative to male Moreover, grey-headed albatrosses from Bird Island and black- Campbell albatrosses and grey-headed albatrosses under these browed albatrosses have more energy-dense diets than the conditions. Campbell albatrosses also have lower aspect ratios that respective Campbell Island species (Clarke and Prince, 1980; increases maneuverability in lighter winds and may aid in foraging McInnes et al., 2017; Waugh et al., 1999b; Xavier et al., 2003), efficiency (Pennycuick, 2008; Phillips et al., 2004; Rayner, 1988). which should produce larger individuals with greater energy We were unable to directly test the effect of wing loading because requirements. The absolute energy requirements of black-browed we did not have wing measurements from individuals that were albatrosses may contribute to their near-absence from breeding on sampled for energy expenditure. However, differences in wing Campbell Island relative to the endemic Campbell albatross (ACAP, loading between species probably has a functional significance (e.g. 2009), especially if black-browed albatrosses do not raise young as flight costs) given that wing morphologies are believed to restrict the successfully on lower energy income. This could be tested by breeding ranges of other albatross species (Suryan et al., 2008). measuring DEE from guard-stage black-browed albatrosses The DEE of both Campbell and grey-headed albatrosses is higher breeding on Campbell Island for a more direct comparison, if a relative to body mass compared with other albatross species (Fig. 3), sufficient sample size could be found. as expected from Southern Ocean species that forage in more The similar guard-stage costs of Campbell albatrosses and grey- productive waters than North Pacific albatrosses (Antolos et al., headed albatrosses on Campbell Island were inconsistent with our 2017; Shaffer, 2011). Species that can gain more energy should be predictions based on their differing life histories and foraging willing to expend more energy (Jodice et al., 2006). However, strategies. Biennial breeding is thought to result, in part, from higher individuals that gain more mass relative to their body size will also breeding costs associated with traveling further distances to forage, expend more energy due to increased wing loading unless foraging which extends the breeding season and leaves little time to recover in stronger winds where heavier loads increase flight stabilization body reserves before breeding again (Dobson and Jouventin, 2010; and costs can be offset (Pennycuick, 1982; Warham, 1977). Indeed, Jouventin and Dobson, 2002). Indeed, grey-headed albatrosses grey-headed albatrosses recovered a higher proportion of their pre- travel further distances during the guard stage, but breeding duration foraging body mass – as might be expected from this species that for this species overlaps with the annually breeding Campbell consistently traveled further distances to the windy and nutrient-rich albatrosses (chick rearing lasts approximately 116–152 versus Subantarctic Front – yet they did not expend more energy than 130 days, respectively (ACAP, 2010; Moore and Moffat, 1990) and Campbell albatrosses. Within species and years, albatrosses with is shorter than other annual breeders (Jouventin and Dobson, 2002). higher proportional mass gain exhibited greater DEE, especially Therefore, similar foraging costs during the guard stage suggest that males, suggesting that structurally smaller females with lower wing poorer food quality or higher energy deficits incurred during other loading can gain more proportional mass at less cost in similar wind breeding stages (e.g. incubation or late chick-rearing) or post- conditions. Given within-year effects of mass gain, it is notable that breeding may affect the breeding frequency of grey-headed both species gained significantly more proportional mass in 2012 albatrosses (Crossin et al., 2013). Grey-headed albatrosses in when DEE was lower. Foraging behaviors, wind interactions or 2012 were leaner (higher total body water in males) and also had factors not measured, such as preferred prey abundance, are likely higher water influx than Campbell albatrosses, suggesting prey with important drivers of yearly differences in foraging efficiency. lower energy density (e.g. greater proportions of salps). Grey- headed albatrosses primarily forage on squid that contain four to six Foraging behaviors times less calcium and less energy than the krill and fish (Clarke and Individuals that took off from the water in higher wind speeds Prince, 1980) typically consumed by annual breeders (Hedd and expended less energy, consistent with the effect of take-offs on Gales, 2001; Waugh et al., 1999b). However, grey-headed albatross energy expenditure observed in other albatrosses (Sakamoto et al., chicks grow at faster rates and fledge at greater body mass than 2013; Shaffer et al., 2001a; Weimerskirch et al., 2000). When take-off Campbell albatross chicks (Moore and Moffat, 1990). Grey-headed wind speeds were lower, individuals performed more water landings, albatross parents forage in predictable, strong westerly winds that spent more time resting on the water, had lower foraging success and probably offset wing loading and reduce the cost of larger food expended more energy (Tables S1 and S2). Gaining less mass with loads that may compensate for lower quality (Table S1; more water landings and performing more landings in energetically Weimerskirch et al., 2012). A greater allocation of energy to expensive wind speeds are somewhat counterintuitive because birds chicks rather than self-maintenance, however, may necessitate a should limit landings to when food is located to conserve time and longer self-recovery period or influence feather molt timing, which energy during chick rearing (Shaffer et al., 2001a; Weimerskirch could interfere with breeding frequency (Edwards, 2008; et al., 2000). In 2011, Campbell albatrosses that had the highest mean McNamara and Houston, 2008). Additionally, calcium limitation take-off rates also spent a greater proportion of their total trip on the within the adult could delay egg production and lead to biennial water, possibly because certain prey types required more surface time breeding (Edwards, 2008; McNamara and Houston, 2008). to exploit before resuming aerial searching (Weimerskirch, 2007; Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Weimerskirch and Pinaud, 2007). These individuals may have Implications and future directions consumed smaller or less energy-dense prey types such as jellyfish Overall, we were able to link a suite of behavioral, morphometric (McInnes et al., 2017) and employed a sit-and-wait strategy to and environmental measures to variations in DEE in two sympatric conserve energy while optimizing net energy gain (Conners et al., southern albatross species. Although grey-headed albatrosses had 2015; Louzao et al., 2014). In 2011, albatrosses may have employed greater foraging success and similar energy expenditure to this strategy if lower wind speeds reduced in-flight search efficiency Campbell albatrosses, their primary prey source and guard-stage and take-off efficiency (Spear and Ainley, 1997; Wakefield et al., body reserves indicate that grey-headed albatrosses may incur 2009; Weimerskirch et al., 2000). Furthermore, when take-off wind greater self-maintenance costs consistent with their life history as speeds were higher, individuals may have spent less time on the water biennial breeders. Future changes in prey availability are thus an during feeding events, which could have led to under-represented important consideration for future modeling efforts as climate landing frequencies given the sampling interval (10 min) of the GPS change is expected to affect productivity in the Southern Ocean loggers in this study. Thus, mean wind speed at take-off may be a (Constable et al., 2014). In addition, wind fields are projected to more reliable predictor of DEE than the number of take-offs when weaken towards lower latitudes while becoming stronger towards sampling intervals are potentially greater than landing intervals. higher latitudes (Lovenduski and Gruber, 2005; Thompson and Wallace, 2000), which may reduce foraging opportunities for some Environmental interactions species (this study) while enhancing opportunities for others In addition to the effects of proportional mass gain and take-off wind (Weimerskirch et al., 2012). A decrease in wind strength in lower speed, DEE was also affected by the proportion of strong headwinds latitudes where Campbell albatrosses range (Lovenduski and −1 during flight (>12 m s ). Strong headwinds can offset flight Gruber, 2005) could entail more individuals using a less direction and potentially force more energetically expensive energetically efficient sit-and-wait strategy. In contrast, an corrective maneuvering (Louzao et al., 2014; Tarroux et al., 2016; increase in wind strength at higher latitudes where grey-headed Wakefield et al., 2009), particularly in species with higher wing albatrosses range (Lovenduski and Gruber, 2005) could aspect ratios like grey-headed albatrosses. Grey-headed albatrosses increase flight costs. Understanding the factors that influence also encountered higher mean wind speeds than Campbell albatrosses the DEE of animals, such as changing wind fields, is essential (Table S3), so the proportion of strong headwinds encountered should for assessing the vulnerability of species in the face of climate be costlier. Albatrosses are known to use looping flight paths while change. This information is also crucial for management transiting to foraging destinations (Weimerskirch et al., 2000) – efforts, especially as species less tolerant to environmental keeping the wind at low-cost angles – but time and space constraints perturbations may require management to reduce more during early chick-rearing can limit the use of efficient flight remediable stressors (Cooke et al., 2013). strategies (Kroeger, 2019). Accordingly, DEE was higher when the Acknowledgements proportion of strong headwinds was higher for grey-headed We thank the New Zealand Department of Conservation for permitting this project albatrosses compared with Campbell albatrosses under the same and providing logistical support; Henk Haazen and crew for providing safe model conditions. Furthermore, although the consequences of strong transportation to and from Campbell Island; Joy Sagar for field assistance; Kyle Morrison, Ray Bucheit and Rob Dunn for field support; Jen Jelincic for laboratory tailwinds on soaring seabirds has received less attention (but see analysis assistance; Jonathan Felis for geographic information system mapping; Alerstam et al., 2019; Spear and Ainley, 1997) and most cost models and Rachel Holser for providing thoughtful feedback on initial drafts of the do not include this effect (Felicisimo et al., 2008; Louzao et al., 2014; manuscript. We also thank Jeff Pentel and the numerous people listed in the funding Raymond et al., 2010), we found that a greater proportion of strong section for their generous financial donations that made this work possible. tailwinds was also energetically costly for both species. This cost may Competing interests result from light wing loads while transiting from the nest to foraging The authors declare no competing or financial interests. grounds that are primarily downwind (Fig. 1), as this transit occurred when strong tailwinds could be most destabilizing to flight due to Author contributions reduced body mass (Alerstam et al., 2019). Conceptualization: C.E.K., D.E.C., D.P.C., S.A.S.; Methodology: C.E.K.; Formal analysis: C.E.K., D.E.C., S.A.S.; Investigation: C.E.K., D.E.C., R.A.O., P.M.S., L.A.S., T.A.; Resources: D.E.C., D.R.T., L.G.T., P.M.S., L.A.S., T.A., S.A.S.; Writing - The influence of chick age original draft: C.E.K.; Writing - review & editing: D.E.C., R.A.O., D.R.T., L.G.T., Although the sample size decreased when chick age was P.M.S., L.A.S., D.P.C., S.A.S.; Visualization: C.E.K.; Supervision: S.A.S.; Project considered, DEE was found to be lower in parents rearing older administration: D.R.T., L.G.T.; Funding acquisition: D.R.T., L.G.T., P.M.S. chicks. Sampling occurred at roughly the same duration after a foraging trip, but those with larger chicks were probably able to Funding This work was supported by the New Zealand Ministry of Business, Innovation and offload more food to their chick before recapture, weighing and Employment (contract CO1X0905); MARES program (grant FPA 2011-0016); re-sampling (Huin et al., 2000). Partially, or even fully, digested American Ornithologists’ Union; Earl H. and Ethel M. Myers Oceanographic and food in the forestomach may not fully equilibrate with total body Marine Biology Trust; Jim Brown Award; San José State University Graduate water (Ricklefs et al., 1986). Thus, it is conceivable that body water Student Research Award; and crowd-source funding from Experiment.com (individual donors: Jeff Pentel, Wayne Sentman, Jill Marketos Milburn, Laura pool sizes were over-estimated relative to the concentration of Wagner, Mark Kroeger, David Thompson, Sadie Birdfeather, Jen Jelincic, Amy isotopes in the blood at the time of weighing. This effect would Lush, Paul Richard Wagner, Lucius Bono, Scott Shaffer, Beth Flint, Anita Phagan, inflate the estimates of metabolic rate in adults with younger chicks. Cassie Marketos, Anne Cassell, Dan Saltman, Sandra Machado, Herma Van However, in 2012, individuals that were more successful foragers Gerner, Annie Schmidt, Renee Murphy Shaffer, Heather Day, Corey Clatterbuck, and probably retained more stomach contents at the time of re- Emily Nichols, Susy Alarcon Arriaga, Cleo Small, Devon O’Meara, Mary Moskal, Wynter Skye Standish, Rachael Orben, sampling (Huin et al., 2000) had lower DEE that year. 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Ecol. 72, water flux and body composition in glaucous gulls (Larus hyperboreus). 79, 836-845. 500-508. doi:10.1046/j.1365-2656.2002.00720.x Shamoun-Baranes, J., Loon, E., Van, Liechti, F. and Bouten, W. (2007). Weimerskirch, H., Gault, A. and Cherel, Y. (2005). Prey distribution and Analyzing the effect of wind on flight: pitfalls and solutions. J. Exp. Biol. 210, 82-90. doi:10.1242/jeb.02612 patchiness: factors in foraging success and efficiency of wandering albatrosses. Speakman, J. R. (1997). Doubly Labelled Water: Theory and Practice. Chapman & Hall. Ecology 86, 2611-2622. doi:10.1890/04-1866 Speakman, J. R. and Hambly, C. (2016). Using doubly-labelled water to measure Weimerskirch, H., Guionnet, T., Martin, J., Shaffer, S. A. and Costa, D. P. (2000). free-living energy expenditure: some old things to remember and some new things Fast and fuel efficient? Optimal use of wind by flying albatrosses. Proc. R Soc. B to consider. Comp. Biochem. Physiol. A 202, 3-9. doi:10.1016/j.cbpa.2016.03.017 267, 1869-1874. doi:10.1098/rspb.2000.1223 Journal of Experimental Biology RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb228585. doi:10.1242/jeb.228585 Weimerskirch, H., Louzao, M. and Delord, K. (2012). Changes in wind pattern Wingfield, J. C., Kelley, J. P. and Angelier, F. (2011). What are extreme alter albatross distribution and life- history traits. Science 335, 211-214. doi:10. environmental conditions and how do organisms cope with them? Curr. Zool. 57, 1126/science.1210270 363-374. doi:10.1093/czoolo/57.3.363 Weiner, J. (1992). Physiological limits to sustainable energy budgets in birds and Xavier, J. C., Croxall, J. P. and Reid, K. (2003). Interannual variation in the diets of two mammals: ecological implications. Trends Ecol. Evol. 7, 384-388. doi:10.1016/ albatross species breeding at South Georgia: implications for breeding performance. 0169-5347(92)90009-Z Ibis (Lond 1859) 145, 593-610. doi:10.1046/j.1474-919X.2003.00196.x Wingfield, J. C. (2013). Ecological processes and the ecology of stress: the impacts Ydenberg, R. C., Welham, C. V. J., Schmid-Hempel, R., Schmid-Hempel, P. and of abiotic environmental factors. Funct. Ecol. 27, 37-44. doi:10.1111/1365-2435. Beauchamp, G. (1994). Time and energy constraints and the relationships between 12039 currencies in foraging theory. Behav. Ecol. 5, 28-34. doi:10.1093/beheco/5.1.28 Journal of Experimental Biology

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Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

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Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies

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