An animal's body condition provides valuable information for ecophysiological studies, and is an important measure of fitness in population monitoring and conservation. While both the external body shape of an animal and its internal tissues (i.e. fat content) can be used as a measure of body condition, the relationship between the two is not always linear. We compared the morphological body condition (external metric obtained through aerial photogrammetry) of migrating humpback whales (Megaptera novaeangliae) with their outer blubber lipid concentration (internal metric obtained through blubber biopsy sampling) off the coast of south-west Australia early and late in the breeding season (spanning ∼4.5 months). The external body condition index of juvenile and adult humpback whales decreased by 26.9 (from 18.8% to −8.1%) and 12.0 percentage points (from 8.6% to −3.4%), respectively, between the early and late phase. In contrast, we found no intra-seasonal change in blubber lipid concentration, and no difference between reproductive classes (juveniles, adults and lactating females); however, the small sample size prevented us from effectively testing these effects. Importantly, however, in the 33 animals for which paired metrics were obtained, we found no correlation between the morphometric body condition index and the blubber lipid concentration of individual whales. The lack of a linear relationship suggests that changes in outer blubber lipid concentration do not reflect external changes in body shape, thus limiting the utility of outer blubber lipid reserves for individual body condition evaluation. The wider spectrum of change in body morphometry captured with aerial photogrammetry supports the use of body morphometry as a reliable and well-tested method.

Body condition is a proxy for fitness in animals and can be expressed by any physiological index that represents its energy reserves (Hanks, 1981; Millar and Hickling, 1990). As body condition has a direct influence on the survival and reproductive success of individuals (Albon et al., 1983; Clutton-Brock and Sheldon, 2010; Gaillard et al., 2000; Loudon et al., 1983), it is a valuable metric in studies of behavioural ecology, ecophysiology and conservation biology (Stevenson and Woods, 2006). The body condition of individuals in a population can also provide a direct measure of population health, which can be used to detect early changes in vital rates and population dynamics resulting from natural and/or anthropogenic factors (Dobson, 1992; Rolland et al., 2016; Sæther, 1997). Utilizing body condition metrics that reliably capture the energy reserves of individuals in a population is hence of central importance for wildlife research, monitoring and conservation (Stevenson and Woods, 2006).

The body condition of an animal can be expressed by any variable that captures the energy reserves of the individual, independently from its structural body size (e.g. body length) (Green, 2001; Hayes and Shonkwiler, 2001). Although a wide range of body condition indices exist (Bolger and Connolly, 1989; Labocha and Hayes, 2012; Stevenson and Woods, 2006), most of these relate to external morphological characteristics, including body mass, volume, girth and width, and are often expressed in relation to (or as a ratio of) body length (structural size) or as the residual of the regression between the two variables (Green, 2001; Jakob et al., 1996; Moya-Laraño et al., 2008; Stevenson and Woods, 2006). Alternatively, measurements of internal lipid stores in the tissues of animals can provide a useful index of body condition, with lipids playing a fundamental role in many biological, physiological and metabolic processes (Allen, 1976; Waugh et al., 2012).

Most baleen whale species are capital breeders, meaning that they finance the cost of reproduction on low-latitude winter breeding grounds with stored energy acquired on high-latitude summer feeding grounds (Kasuya, 1995; Lockyer, 1987a). Individuals fast for extended periods of time whilst on their breeding grounds, although opportunistic feeding is known to occur in some populations (e.g. Stockin and Burgess, 2005). As such, they need sufficient energy reserves to cover their own metabolic needs (including maintenance and growth), as well as the high energetic costs associated with late pregnancy and early lactation for females (Christiansen et al., 2014, 2018; Lockyer, 1981, 2007). The importance of stored energy for migration and reproduction has resulted in numerous studies investigating seasonal and annual variation in body condition in baleen whales (Christiansen et al., 2013, 2016, 2018; Lockyer, 1981, 1987b; Niæss et al., 1998; Vikingsson, 1995). Consequently, several morphological variables have been used to represent the body condition of baleen whales, including body surface area (Christiansen et al., 2016), body mass (Lockyer, 1987b, 1990; Niæss et al., 1998), body volume (Christiansen et al., 2018; George et al., 2015), blubber volume (Christiansen et al., 2014) and body girth (Haug et al., 2002; Vikingsson, 1990). With lipids playing a central role in the energy stores of baleen whales, internal body tissue indices have also been developed, the most common being the percentage lipid content in blubber, muscle and visceral fats (Lockyer et al., 1984; Niæss et al., 1998).

Many of the existing body condition indices for baleen whales are based on measurements from dead animals. Relying on dead specimens, however, is limiting, as these individuals are often very young, old or otherwise weakened and do not represent the healthy population. Similarly, this approach does not allow for longitudinal studies of individuals (repeated sampling of the same individual over time) or sampling of small or vulnerable populations. Consequently, in recent decades, body condition indices have been developed based on non-invasive methods. Aerial photogrammetry methods can be used to measure morphological body condition indices of baleen whales, including body width (Durban et al., 2016; Miller et al., 2012), dorsal surface area (Christiansen et al., 2016) and body volume (Christiansen et al., 2018). Standard blubber biopsies can be used to measure tissue body condition indices, including lipid and fatty acid composition (Waugh et al., 2012), adipocyte volume metrics (Castrillon et al., 2017) and lipophilic persistent organic pollutant (POP) burden (Bengtson Nash et al., 2013, 2018). With aerial photogrammetry and blubber lipid percent analysis both offering promising avenues to assess body condition in baleen whales, research is needed to determine how these two indices correlate with each other.

In baleen whales, much of the lipid reserve is stored in the blubber layer, but considerable amounts are also stored in the muscle and as intra-abdominal fat (Lockyer, 1986, 1987b; Niæss et al., 1998; Vikingsson, 1995). While morphometric body condition generally encompasses all these tissues, as well as non-adipose tissues, blubber lipid concentration is only representative of a single tissue. Further, with the blubber of baleen whales being vertically stratified into three distinct layers, blubber biopsy samples generally only represent the lipid concentration in the outer layer, which is believed to play a lesser role in the deposition and mobilization of lipids (Aguilar and Borrell, 1990, 1991; Lockyer et al., 1984, 1985). The same stratification can also be found in the blubber of pinnipeds (Best et al., 2003; Wheatley et al., 2007), where the inner layer is more heavily metabolized during fasting (Strandberg et al., 2008). Based on this, seasonal changes in the morphometric body condition of baleen whales might not be reflected in their outer blubber lipid concentration. In fact, Kershaw et al. (2019) showed a lack of correlation between morphometric body condition (girth/length) and outer lipid content (from the dorsal area immediately caudal to the dorsal fin) in stranded balaenopterids (n=9). Still, many baleen whale species show intra-seasonal changes in both morphometric body condition and blubber lipid concentration, suggesting there could be a positive relationship. For example, aerial photogrammetry research off the coast of Western Australia (WA) demonstrated a linear decrease in the body surface area of adult and lactating humpback whales (Megaptera novaeangliae) through the breeding season (Christiansen et al., 2016), while blubber biopsy sampling off the eastern coast of Australia showed a significant decrease in the outer blubber lipid concentration in adult male humpback whales between early and late migrating cohorts (Bengtson Nash et al., 2013). Similarly, minke whales (Balaenoptera acutorostrata) feeding in Icelandic waters showed an increase in both their blubber volume (Christiansen et al., 2013) and lipid concentration (Vikingsson et al., 2013) through the summer feeding season. A correlation between body width and blubber thickness (arising from blubber lipid catabolism) was also found in right whales (Eubalaena spp.) (Miller et al., 2011, 2012). In light of these contrasting findings, further research into the relationship between morphometric body condition and outer blubber lipid concentration is needed using live whales across a large range of natural body conditions.

In this study, we investigated whether intra-seasonal changes in external morphometric body condition correlate with lipid changes in the outer blubber layer in free-living humpback whales. To do this, we combined two novel and minimally invasive methods: unmanned aerial vehicle (UAV) photogrammetry and blubber biopsy sampling. Paired metrics were collected off the coast of WA from individuals at the beginning and end of the breeding season to obtain a wide range of natural body conditions.

Permits

All research was carried out under a research permit from the Department of Biodiversity, Conservation and Attractions, WA (permit no. 08-000702-1), and an animal ethics permit from Murdoch University (R2935/17). The UAV was operated under a UAV Operator Certificate (CASA.ReOC.0075) and a Remotely Piloted Aircraft System Licence in accordance with regulations by the Australian Civil Aviation Safety Authority.

Data collection and processing

Aerial photographs and blubber biopsy samples were obtained from migrating humpback whales, Megapteranovaeangliae Borowski 1781, off the coast of south-west Australia (Fig. 1). Western Australia constitutes the winter breeding ground for humpback whale breeding stock D, which spends the summer feeding in Antarctica in feeding area IV (Gill and Burton, 1995; Jenner et al., 2001). The whales migrate north along the WA coastline between April and August, with a peak in the number of migrating animals off the south-western coast in late June, to reach their main breeding grounds around Camden Sound (Chittleborough, 1965; Jenner et al., 2001). The southern migration back towards the feeding grounds takes place between August and November, with a peak in the number of migrating animals off the south-west coast in late October (Jenner et al., 2001). The south-west represents the area of both entry and exit for the majority of breeding stock D that feed in the eastern section of feeding area IV, in Antarctica (Chittleborough, 1965; Gill and Burton, 1995; Jenner et al., 2001). Consequently, the difference in body condition of whales passing this point early (during the northern migration) and late (during the southern migration) in the breeding season should represent the absolute loss in condition of whales whilst on the breeding grounds. Based on this assumption, our sampling period was during the early and late phase. The early phase, representing the whales' condition on arrival in Australian waters, took place between 2 and 18 June 2017, in Flinders Bay, Augusta (Fig. 1). The late phase, representing the whales' departure condition, took place between 1 and 19 October 2017, in Geographe Bay, Dunsborough (Fig. 1). In both locations, sampling was conducted from a small (∼6 m) research vessel operated within two nautical miles of the coast.

Fig. 1.

Map of the Flinders Bay and Geographe Bay sampling sites in south-west Australia. (A) The location of the study area. (B) South-west Australia with north-bound arrows depicting the northern migration and the south-bound arrow depicting the southern migration of humpback whales. (C) Geographe Bay off Dunsborough (sampling during the late phase of the southern migration). (D) Flinders Bay off Augusta (sampling during the early phase of the northern migration). Grey lines in C and D show the tracks of the research vessel and the coloured dots indicate the position of the sampled whales.

Fig. 1.

Map of the Flinders Bay and Geographe Bay sampling sites in south-west Australia. (A) The location of the study area. (B) South-west Australia with north-bound arrows depicting the northern migration and the south-bound arrow depicting the southern migration of humpback whales. (C) Geographe Bay off Dunsborough (sampling during the late phase of the southern migration). (D) Flinders Bay off Augusta (sampling during the early phase of the northern migration). Grey lines in C and D show the tracks of the research vessel and the coloured dots indicate the position of the sampled whales.

External body morphometrics: UAV aerial photogrammetry

A DJI Inspire 1 Pro UAV with a Zenmuse X5 camera and a 25 mm lens was flown above the humpback whales at altitudes from 19.0 to 65.6 m (mean±s.d. 32.0±6.03 m) and recorded videos of the whales as they surfaced to breathe. During post-processing, a still frame photograph of each whale was extracted from the videos. An ideal photograph represented a whale lying flat at the surface with its dorsal side visible, its body non-arching and the body contour (both length and width) clearly visible (Christiansen et al., 2016, 2018). If the whale rolled over during sampling, we also extracted photographs of the lateral side. Each photograph was quality graded (based on posture, clarity and contrast) following the protocol of Christiansen et al. (2018), and only photographs of adequate quality were included in analyses. No repeated measurements of the same individuals were obtained between the early and late phase; thus, the whales measured represent a cross-sectional sample of the population.

The body length and widths (at 5% increments along the entire body axis of the whale; Fig. 2) (for details, see Christiansen et al., 2016) of the whales were measured from the dorsal photographs using the custom-programmed Graphical User Interface developed by Dawson et al. (2017). Similarly, from the lateral photographs we measured the body height (dorso-ventral distance) at the same measurement sites (Fig. 2). All measurements were scaled (converted from pixels to metres) using the known altitude of the UAV (measured using a LightWare SF11/C laser range finder), the camera sensor size, focal length and image resolution (for details, see Christiansen et al., 2018).

Fig. 2.

Humpback whale aerial photogrammetry measurement sites. Example aerial photographs of humpback whale adults taken (A) early and (B) late in the breeding season. The position of the body length (BL) and body width (W) measurement sites (from 5% to 85% BL from the rostrum) is shown by the white arrows in A. (C) Lateral side photograph of a humpback whale used to measure body height (dorso-ventral distance) at the same measurement sites as in A. The red rectangle indicates the area where outer blubber biopsies were obtained, from either side of the animal. Note that all photographs are of different whales.

Fig. 2.

Humpback whale aerial photogrammetry measurement sites. Example aerial photographs of humpback whale adults taken (A) early and (B) late in the breeding season. The position of the body length (BL) and body width (W) measurement sites (from 5% to 85% BL from the rostrum) is shown by the white arrows in A. (C) Lateral side photograph of a humpback whale used to measure body height (dorso-ventral distance) at the same measurement sites as in A. The red rectangle indicates the area where outer blubber biopsies were obtained, from either side of the animal. Note that all photographs are of different whales.

Each whale was classified into a specific reproductive class: calf, juvenile, adult and lactating. Calves and lactating females were classified based on their relative size (calves are <2/3 the length of their mothers; Christiansen et al., 2016) and close association with each other. Juveniles and adults (sexually mature animals that were not pregnant or lactating) were separated based on a body length threshold of 11.2 m (Chittleborough, 1955a,b; Christiansen et al., 2016).

Internal tissue metric: biopsy sampling

Blubber biopsies were collected from a sub-set of the humpback whales that were video-recorded with the UAV. A modified 0.22 calibre Paxarms rifle was used together with flotation darts with 7 mm diameter and 40 mm length cutting heads. The size of the cutting heads was intended to sample the outer blubber layer of the animals. Although the outer blubber layer in baleen whales is believed to be metabolically less active than the inner blubber layer (Aguilar and Borrell, 1990; Olsen and Grahl-Nielsen, 2003), Waugh et al. (2014) found no significant difference in blubber lipids between inner and outer layers of blubber of adult male humpback whales. During biopsy sampling, the whales were approached from the rear and side by the research vessel at a slow and steady speed until the boat was positioned perfectly parallel to the whales and transiting in the same direction. Biopsies were collected from distances between 15 and 30 m, from the dorsal surface, ventral and caudal to the dorsal fin [located at about 70% body length (BL) from the rostrum] (Lambertsen et al., 1994) (Fig. 2C). The darts had a floating chamber and were collected by hand from the water's surface after sampling. The samples were immediately cut into pieces, for storage in either a cooler or a liquid nitrogen dewar.

Body condition indices

External morphometric body condition: UAV aerial photogrammetry

The morphometric body condition of humpback whales was calculated from the residual of the relationship between body volume and body length (Christiansen et al., 2018). While this body condition index (BCI) encompasses both adipose (blubber, muscle and visceral fats) and non-adipose tissues, we assumed that most effects on changes in body dimension would arise from lipid mobilization, and hence be captured by this metric. First, we used the body length, width and height data to estimate the body volume of the whales. Although often assumed to be circular, the cross-sectional body shape of the whales is elliptical, with the height:width (HW) ratio varying across the body axis of the whales (Christiansen et al., 2019; Lockyer et al., 1985). To account for this, the HW ratio of the whales was first calculated for each reproductive class (Table S1, Fig. S1), using the data from whales for which both dorsal width (W) and lateral height (H) measurements had been obtained. Once the HW ratio had been established for each measurement site, we modelled the whale's body as a series of infinitesimal ellipses and calculated the body volume (V) of each body segment (s, the section of the body between two adjacent width/height measurement sites), following the methods of Christiansen et al. (2019):
formula
(1)
where BLi is the total body length of whale i, WA,s,i and HA,s,i are the anterior width and height measurements of body segment s for individual i, and WP,s,i and HP,s,i are the posterior width and height measurements of segment s for individual i, respectively. To account for the gradual decrease in height and width towards the end points of the whale, the segments closest to the rostrum (0–5% BL from the rostrum) and the end of the tail region (85–100% BL from rostrum) were modelled as elliptical cones (Christiansen et al., 2019). The total volume, VTotal, of whale i was then obtained by calculating the sum of the volumes of all body segments s (20 segments in total):
formula
(2)
While an elliptical model might not capture the cross-sectional body shape of odontocetes (Adamczak et al., 2019), Christiansen et al. (2019) demonstrated that the body girth and volume of mysticetes could be closely approximated by an elliptical model. From the body volume estimates, a morphometric BCI was calculated following the methods of Christiansen et al. (2018):
formula
(3)
where BVobs,i is the observed body volume of whale i (in m3) and BVexp,i is the expected (or predicted) body volume of whale i (in m3) from the linear relationship between body volume and length on the log–log scale.

Internal tissue body condition: outer blubber lipid concentration

Around 20 mg of blubber was used for each extraction. Samples were extracted overnight using a methanol/dichloromethane (DCM)/water extraction (2:1:0.8 v/v/v). The following day, DCM/water was added, yielding a final solvent ratio of 1:1:0.9 v/v/v methanol/DCM/water. After that, samples were left to partition into the aqueous and DCM phases for at least 2 h. The lower DCM phase was collected and reduced by rotary evaporation at 40°C to obtain the total lipid extract. After drying under a stream of nitrogen gas, the total lipid extract was re-weighed to determine total lipid content (expressed as percent lipid of the original blubber sample).

Intra-seasonal changes in body condition – external versus internal metrics

To quantify the intra-seasonal changes in the external morphometric BCI of humpback whales through the breeding season, the BCI of juveniles and adults was compared between the early and late phase, using linear models in R v.3.5.3 (http://www.R-project.org/). Separate models were fitted for each reproductive class. As calves and lactating females were only measured during the late phase, their change in body condition could not be assessed. Similarly, to quantify the change in outer blubber lipid concentration in humpback whales throughout the breeding season, the blubber lipid concentration of juveniles and adults was compared between the two phases, again using linear models fitted separately for each reproductive class. Finally, the morphometric BCI of individual whales was compared with their lipid concentration using linear models. The effect of reproductive class and sampling period on the BCI–lipid concentration relationship was also tested using a linear model. For each model, model validation tests were performed to test for homogeneity and normality of residuals, as well as influential data points and outliers. All model assumptions were fulfilled.

Humpback whales were sampled across 10 days in Flinders Bay during the early phase and across 11 days in Geographe Bay during the late phase. A total of 306 morphometric measurements (292 dorsal and 14 lateral) were obtained with the UAV, representing 193 individual whales (12 with both dorsal and lateral photographs). After filtering the data based on picture quality, a total of 167 measurements of individual whales remained, 56 from the early period and 111 during the late period (Table 1). The dataset comprised 24 calves (BL: 5.4–7.6 m), 55 juveniles (BL: 7.1–11.1 m), 67 adults (BL: 11.2–15.3 m) and 21 lactating females (BL: 11.1–14.6 m). A total of 33 biopsy samples were collected, 15 during the early and 18 during the late period, comprising 16 juveniles, 9 adults and 8 lactating females (Table 1).

Table 1.

Composition of the humpback whales measured by unmanned aerial vehicle (UAV) photogrammetry and blubber biopsy sampling, by reproductive class and sampling period (early versus late phase)

Composition of the humpback whales measured by unmanned aerial vehicle (UAV) photogrammetry and blubber biopsy sampling, by reproductive class and sampling period (early versus late phase)
Composition of the humpback whales measured by unmanned aerial vehicle (UAV) photogrammetry and blubber biopsy sampling, by reproductive class and sampling period (early versus late phase)

Body shape and volume

The HW ratio of humpback whales across their body was calculated for 3 calves, 5 juveniles and 4 adults (Fig. S1, Table S1). No lateral photographs were obtained from lactating females. For the three measured reproductive classes, the cross-sectional body shape of the anterior half of the body was close to circular (HW ratio≈1), whereas the posterior half of the body was significantly flattened in the lateral plane (Fig. S1, Table S1). The HW ratio across the posterior half of the body was higher for calves, while adults were more circular in shape, followed by juveniles which were circular in cross-sectional shape down to 60% BL from the rostrum. Because of the low sample size, we used the average HW ratio of all reproductive classes when modelling the body volume of the whales. While this could have biased our body volume estimates, by changing the intercept of the body volume to body mass relationship, it would not affect the seasonal change in body volume within reproductive classes, as the intercept would change equally for early and late phase animals.

The body volume of humpback whales ranged from 2.12 to 6.32 m3 (mean±s.d. 4.24±1.18 m3) for calves, 6.96 to 21.97 m3 (13.59±3.75 m3) for juveniles, 18.07 to 41.43 m3 (26.14±4.27 m3) for adults and 17.03 to 41.15 m3 (27.32±6.31 m3) for lactating females (Fig. 3A). There was a strong linear relationship between body volume and body length on the log–log scale [log(BV)=−3.70+2.77×log(BL); F1,165=3586, P<0.001, R2=0.96] (Fig. 3B).

Fig. 3.

Humpback whale body volume versus body length relationship. (A) Humpback whale body volume as a function of body length for different reproductive classes and periods (see key). The solid line represents the back-transformed fitted values of the linear model. (B) The log–log relationship between body volume (m3) and body length (m) for the same dataset, with the solid line representing the fitted values of the linear model [log(BV)=−3.70+2.77×log(BL); F1,165=3586, P<0.001, R2=0.96]. N=167 whales.

Fig. 3.

Humpback whale body volume versus body length relationship. (A) Humpback whale body volume as a function of body length for different reproductive classes and periods (see key). The solid line represents the back-transformed fitted values of the linear model. (B) The log–log relationship between body volume (m3) and body length (m) for the same dataset, with the solid line representing the fitted values of the linear model [log(BV)=−3.70+2.77×log(BL); F1,165=3586, P<0.001, R2=0.96]. N=167 whales.

External morphometric and internal tissue body condition

The calculated morphometric BCI of humpback whales varied between −25.5% and 53.6% (Fig. S2). There was a significant difference (F1,53=52.1, P<0.001, R2=0.50) in the BCI of juvenile humpback whales between the early (mean±s.e.m. 18.8±2.13%) and late (−8.1±3.73%) phase (Fig. 4A). Similarly, there was a significant difference (F1,65=20.3, P<0.001, R2=0.24) in the BCI of adult humpback whales between the early (mean±s.e.m. 8.6±2.25%) and late (−3.4±2.65%) phase (Fig. 4A). The effect size was a 26.9 (from 18.8% to −8.1%) and 12.0 percentage point (from 8.6% to −3.4%) decrease in BCI for juveniles and adults, respectively (Fig. 4A).

Fig. 4.

Intra-seasonal variation in humpback whale external and internal body condition indices. Boxplots of (A) external morphometric body condition and (B) internal body condition (outer blubber lipid concentration) of humpback whale juveniles and adults measured early (light grey) and late (dark grey) in the season. The sample size for each reproductive class is given below each boxplot. The dashed red horizontal line in A represents a humpback whale of average body condition (body condition index, BCI=0).

Fig. 4.

Intra-seasonal variation in humpback whale external and internal body condition indices. Boxplots of (A) external morphometric body condition and (B) internal body condition (outer blubber lipid concentration) of humpback whale juveniles and adults measured early (light grey) and late (dark grey) in the season. The sample size for each reproductive class is given below each boxplot. The dashed red horizontal line in A represents a humpback whale of average body condition (body condition index, BCI=0).

The measured blubber lipid concentration ranged between 16.4% and 73.2% (mean±s.d. 48.2±12.8%) (Fig. S3). Lipid concentration did not vary between sampling periods or reproductive classes (Fig. 4B). The small sample size for each reproductive class and migration phase however prevented confident evaluation of inter-season and inter-class variation in lipid concentration, although the available data revealed little variation. Further, there was no relationship between the morphometric BCI and the corresponding outer blubber lipid concentration of individual humpback whales (F1,31=0.778, P=0.384, R2=0.024; Fig. 5). The inclusion of reproductive class and sampling period, as well as interaction terms between the explanatory variables in the model, did not reveal any patterns in the lipid concentration of humpback whales.

Fig. 5.

Correlation between external and internal BCI in humpback whales. Internal body condition (outer blubber lipid concentration) versus external morphometric (BCI) for humpback whale juveniles (N=16), adults (N=9) and lactating females (N=8), sampled during the early (open circles) and late phase (filled circles) of the season. Morphometric BCI, reproductive class and sampling period did not affect lipid concentration.

Fig. 5.

Correlation between external and internal BCI in humpback whales. Internal body condition (outer blubber lipid concentration) versus external morphometric (BCI) for humpback whale juveniles (N=16), adults (N=9) and lactating females (N=8), sampled during the early (open circles) and late phase (filled circles) of the season. Morphometric BCI, reproductive class and sampling period did not affect lipid concentration.

The annual migration of baleen whales between summer feeding grounds and winter breeding grounds is often reflected in seasonal variation in energy reserves (Christiansen et al., 2013, 2016; Lockyer, 1987a,b; Niæss et al., 1998; Vikingsson, 1990, 1995). During the breeding season, lactating southern right whale (Eubalaena australis) females lose between 14.6% and 37.0% of their body volume to support themselves and their dependent calf (Christiansen et al., 2018). The body condition of the mother will directly determine the growth rate of the calf (Christiansen et al., 2018), and its likely survival (McMahon et al., 2000). Adult males also spend considerable amounts of energy during the breeding season, searching for and often competing for females (Baker and Herman, 1984; Christiansen et al., 2013, 2016). Hence, sufficient energy reserves are key to the reproductive success of baleen whales and developing metrics that accurately capture the body condition of free-living baleen whales is fundamental to understanding their physiology, bioenergetics and reproductive biology.

The aim of this study was to determine whether there was a measurable relationship between external changes in morphometrically derived body condition and internal changes in outer blubber lipid concentration of humpback whales through the breeding season. While the morphometric body condition of juvenile and adult humpback whales decreased significantly between the early and late sampling period, we found no change in blubber lipid concentration. More interestingly, of the 33 individuals for which paired blubber lipid and morphometric body condition were captured, no relationship was found. Our findings agree with those of Lockyer (1987a), who found an increase in the body girth of juvenile and adult North Atlantic fin whales (Balaenoptera physalus) through the feeding season, but no seasonal increase in lipid concentration. The same, however, was not found for Icelandic minke whales (B. acutorostrata), which increased both their blubber volume and lipid content through the feeding season (Christiansen et al., 2013; Vikingsson et al., 2013).

One might not expect a linear relationship between external body shape and outer blubber lipid concentration, at least in healthy animals, as the blubber of cetaceans, including baleen whales, is not homogeneous throughout its depth. In many species, blubber is vertically stratified into three distinct layers, with the outer (external) and middle layer containing higher concentrations of lipids compared with the inner layer (Aguilar and Borrell, 1990, 1991; Koopman et al., 1996; Lockyer et al., 1984, 1985). Apart from serving as an energy store, the outer blubber layer also supports body structure, aids in streamlining and locomotion, provides thermal insulation and contributes to buoyancy (Dunkin et al., 2005, 2010; Koopman, 2007; Koopman et al., 2002; Lockyer, 1991; Struntz et al., 2004). Maintenance lipids in the outer blubber layers are therefore thought to be more conservative, placing a limit on the amount of lipids that can be metabolized from the external layer, without jeopardizing ancillary functions (Bengtson Nash et al., 2013; Castrillon et al., 2017). Aguilar and Borrell (1990, 1991) found that the lipid content of the outer blubber layer was more stable than that of the more active, inner layer, and did not vary between juvenile and adult fin whales. Further, Lockyer et al. (1985) found that for fin and sei whales (Balaenoptera borealis), significant amounts of visceral fats were only present in animals that had obtained a thick blubber layer, suggesting that visceral fats might be mobilized before blubber lipids. The same holds true for pinnipeds, where the main function of the outer blubber layer is primarily structural and thermoregulatory (Strandberg et al., 2008). For example, no relationship between maternal post-partum mass and total body lipid concentration was found in Weddell seals (Leptonychotes weddellii; Wheatley et al., 2006). In Pacific walrus (Odobenus rosmarus) and Steller sea lions (Eumetopias jubatus), changes in morphometric body condition (body mass/body length) was only captured by variation in blubber thickness at a few specific measurement sites (Mellish et al., 2007; Noren et al., 2015). In contrast, however, in southern elephant seals (Mirounga leonina) and harbour seals (Phoca vitulina), all blubber measurement sites were positively correlated with morphometric body condition (Mellish et al., 2007; Slip et al., 1992). While our findings suggest that the utility of the outer blubber layer for body condition metric analysis is limited in humpback whales, similar studies need to be conducted on other baleen whale species to determine whether this varies between species.

Despite the physiological limitations of the outer blubber layer and the assumed asymptotic relationship between lipid loss and whole-body condition, this does not rule out a measurable change in blubber metrics relative to body condition, if standardized by sex and migration time point. Bengtson Nash et al. (2013) measured a 23% decrease in outer blubber lipid concentration in adult male humpback whales between early and late migrating cohorts off the eastern coast of Australia (breeding stock E). Further, adult humpback whales had a smaller adipocyte volume during years of low summer sea-ice concentrations (Bengtson Nash et al., 2018). Any measurable difference in early and late phase migrating individuals in the current study could have been partly obscured by the mixed demography of the samples, or the relatively small number of lipid measures for each demographic grouping. Lipid measurements obtained from remote biopsy are also known to be prone to errors resulting from small samples (i.e. weight) and lipid loss during sampling and storage (McKinney et al., 2014). With lipid concentration of blubber varying with depth (Aguilar and Borrell, 1990, 1991; Koopman et al., 1996; Lockyer et al., 1984, 1985) and location on the body of baleen whales (Lockyer et al., 1985; Vikingsson et al., 2013), the remote biopsy technique is also vulnerable to minor inter-individual variation in sampling location. To validate our findings, we therefore encourage expanded studies on known sex, age and reproductive state (including reproductive history) individuals, as well as repeated measurements from the same individuals on arrival and departure from the breeding grounds.

Utilizing body condition metrics that reliably capture the energy reserves of individuals in a population is of importance for wildlife research, monitoring and conservation (Stevenson and Woods, 2006). In the current study, we examined the intra-seasonal change in body condition in migrating humpback whales and found that the external morphometric approach using aerial photogrammetry from non-invasive UAVs did not correlate with outer blubber lipid concentration. We detected a 26.9 and 12.0 percentage point decrease in morphometric body condition for juvenile and adult humpback whales, respectively, across 4.5 months in which the capital breeders were not feeding. Our findings correspond well with those of Chittleborough (1965), who found a 20% decrease in oil yields between humpback whales caught off Carnarvon, north-west WA, between the northern and southern migration. Similarly, Christiansen et al. (2016) documented a linear decline in the body condition of adult and lactating humpback whales in Exmouth Gulf, WA, over a 45 day period. A linear decrease in body condition through the breeding season has also been recorded for lactating southern right whale females (Christiansen et al., 2018). Here, we validate these earlier studies by showing that body morphometry is a reliable, non-invasive method to measure body condition in baleen whales.

We thank Interspacial Aviation Services Pty Ltd (www.interspacialaviation.com.au) for training in UAV operations and safety. Thank you to Nick Sargeant for UAV technical support and the Caravan Shed, Perth, Australia, for logistical support. Sincere thanks to Turners Caravan Park, Augusta, and Dunsborough Lakes Holiday Resort for providing accommodation space during fieldwork. We thank Whale Watch Western Australia (www.whalewatchwesternaustralia.com) for their assistance and collaboration in the field. Thank you to Lars Bejder for logistical support and Jessica Blakeway for help with data processing.

Author contributions

Conceptualization: F.C., S.B.N.; Methodology: F.C., S.B.N.; Software: E.L.; Formal analysis: F.C., J.G., J.C.; Investigation: F.C., K.R.S.; Resources: K.R.S., H.A.W., S.B.N.; Writing - original draft: F.C.; Writing - review & editing: K.R.S., J.G., J.C., H.A.W., E.L., S.B.N.; Visualization: K.R.S.; Project administration: F.C., K.R.S., S.B.N.; Funding acquisition: F.C., S.B.N.

Funding

F.C. received funding from the AIAS-COFUND II fellowship programme that is supported by the Marie Skłodowska-Curie actions under the European Union's Horizon 2020 (grant agreement no. 754513) and the Aarhus University Research Foundation.

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Competing interests

The authors declare no competing or financial interests.

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