Morphological and ecological evidence for two sympatric forms of Type B killer whale around the Antarctic Peninsula
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Killer whales (Orcinus orca) are apex marine predators in Antarctica, but uncertainty over their taxonomic and ecological diversity constrains evaluations of their trophic interactions. We describe two distinct, sympatric forms sharing the characteristic pigmentation of Type B, the most common around the Antarctic Peninsula. Laser photogrammetry revealed nonoverlapping size differences among adults: Based on a body length index (BLI: blowhole to dorsal fin) adult females of the larger form (“B1”) were 20 % longer than the smaller form (“B2”), and adult males were 24 % longer on average. Dorsal fins of B1 adult females were 19 % taller than B2 females, and adult males 32 % taller. Both types were strongly sexually dimorphic, but B1 more so, including for BLI (B1 males = 1.07× females; B2 = 1.05×) and especially for dorsal fin height (B1 male fins = 2.33× female; B2 = 2.10×). The characteristically large Type B eye patch was more extensive for B1 than B2, comprising 41 and 37 % of BLI, respectively. Average group size was also significantly different, with B1s in smaller groups (mean 7, range 1–14) and B2s more gregarious (mean 36, range 8–75). Stable isotope analysis of skin biopsies indicated dietary differences: a significantly lower nitrogen 15N/14N ratio in B2s supported observations of feeding primarily on krill consumers (e.g., pygoscelid penguins), while B1s prey mainly on predators of krill consumers (e.g., Weddell seals Leptonychotes weddellii). These differences likely represent adaptations to distinct foraging niches, which has led to genetic divergence; their ecology now needs further study.
KeywordsPredator Cetacean Diet Stable isotopes Photogrammetry
There is increasing recognition of the importance of top-down forcing within Antarctic marine ecosystems (Ainley et al. 2007, 2010). Killer whales (Orcinus orca) are abundant within these systems (Branch and Butterworth 2001), most notably around the Antarctic Peninsula (Pitman and Ensor 2003). However, a great deal of uncertainty remains over the extent of their taxonomic and ecological diversity (Pitman et al. 2007), constraining an evaluation of key trophic interactions involving these apex predators. Type B killer whales are one of four currently recognized morphotypes of killer whale in Antarctic waters and are the most common type found around the Antarctic Peninsula (Pitman and Ensor 2003; Pitman et al. 2011). They are readily distinguished from the other types by a dark dorsal cape and lighter lateral fields, and a noticeably large post-ocular eye patch (Pitman and Ensor 2003). Recent analysis of mitogenomics has indicated that Type B is divergent from other Antarctic killer whales and may represent a distinct species (Morin et al. 2010).
Despite a superficial similarity, recent field observations have suggested the existence of two sympatric forms in the coastal waters of the Antarctic Peninsula, both sharing characteristics of the Type B pigmentation pattern (Pitman 2011). An ostensibly larger form has been observed to feed mainly on ice seals (Pitman and Durban 2012), and a smaller form has to date been observed feeding only on pygoscelid penguins (Pitman and Durban 2010), but may also feed on fish (Pitman 2011). Here we present data to support morphological and ecological separation of these two forms, suggesting adaptation to distinct foraging niches. This represents important information for evaluating and predicting the trophic interactions of killer whales in this rapidly changing environment (Stammerjohn et al. 2008).
Materials and methods
Individual whales were distinguished in high-quality photographs by variability in the shape of the saddle patch pigmentation, the shape of the dorsal fin, and patterns of naturally acquired notches in the fin (e.g., Durban et al. 2010). Where repeated measures of fin dimensions were available for the same whale, we selected the tallest and widest as the best to minimize negative bias from parallax errors, if the fin was imaged from slightly above, and horizontal-axis errors, if the whale’s body orientation was not completely parallel to the camera’s focal plane (Durban and Parsons 2006). Similarly, for the BLI, we selected the longest measurement that would be more robust to negative bias from slightly off-perpendicular orientation or when the whale surfaced with a rounded back. For meaningful size comparisons, we restricted our analysis to individuals that were ostensibly of adult size and behavior, in comparison with smaller subadults and juveniles in the groups. Group size was estimated by consensus from a minimum of two visual observers counting whales that came within 500 m of each other and behaved in a coordinated fashion. These estimates were corroborated by minimum photo-identification counts of distinct individuals.
A crossbow (67 kg draw Barnett Wildcat) was used to project floating bolts with a 3.5-cm-long and 0.6-cm-diameter cutting tip (e.g., Hooker et al. 2001) to collect skin samples from the same groups for which photogrammetry data were collected. Stable isotope analysis of epidermis from these biopsies was conducted on lipid-extracted tissue as described previously (e.g., Herman et al. 2005). Three replicate analyses of each skin sample were conducted, and stable isotope values of carbon and nitrogen were compared between B1 and B2 whales to examine ecological differences.
Results and discussion
In addition to size differences, these forms had subtle, but significant, pigmentation differences that facilitated their identification in the field. The characteristic large Type B eye patch was conspicuous on both forms, but was significantly more extensive for B1 than B2 (t test, p = 0.04), comprising x = 41 % (n = 8, SD = 4 %) and x = 37 % (n = 11, SD = 3 %) of the BLI, respectively (Fig. 2). These forms were also distinguished by typical group sizes, with B1 being encountered in significantly smaller groups (x = 7, SD = 4, range 1–14) and B2 being more gregarious (x = 36, SD = 24, range 8–75; t test, p = 0.0002).
These results confirm our field observations of two distinct forms of Type B killer whale around the Antarctic Peninsula. Their morphological and ecological variability likely represents adaptation to distinct foraging niches, and over time might be expected to lead to genetic structuring. Analysis of mitochondrial genomes from a global dataset of killer whales placed Type B whales sampled around the Antarctic Peninsula into a monophyletic mitochondrial lineage, which is a sister clade to the Type C killer whale form found on the other (eastern) side of the Antarctic continent (Morin et al. 2015). However, Type B1 and B2 individuals sampled and sequenced to date do not share any mitochondrial haplotypes and appear to form two distinct subclades; they are also significantly differentiated at nuclear loci based on 91 nuclear single-nucleotide polymorphisms (Morin et al. 2015), and based on a whole genome comparison (Foote et al. in press). These results suggest that mating is not random among Type B killer whales, but rather that there is limited or no mating between Type B1 and Type B2.
This sympatric separation of B1 and B2 whales is similar to the reproductive isolation between sympatric killer whale ecotypes found in the NE Pacific (Morin et al. 2010; Parsons et al. 2013). However, genetic data suggest a relatively recent divergence of the B1 and B2 forms in Antarctica, following the release of habitat after the Last Glacial Maximum (see Morin et al. 2015; Foote et al. in press). Furthermore, in the NE Pacific, the dietary specializations between the ecotypes (e.g., mammal-eating “Transients” and the fish-eating “Residents”) are well established (Ford et al. 1998; Herman et al. 2005), but further work is needed to elucidate the prey preferences and ecotypic distinction of B1 and B2 killer whales, and other Antarctic types (de Bruyn et al. 2013). Because the general Type B morphotype of killer whale has been documented around the Antarctic continent (Pitman and Ensor 2003), future work should also seek to identify the geographical extent of the B1/B2 variation to better parameterize models of trophic dynamics within Antarctica’s changing marine ecosystems.
Field efforts were supported by Lindblad Expeditions, National Geographic Society, and the BBC Natural History Unit. Jerome and Dion Poncet provided shipboard support; Stephanie Martin, Jason Kelley, and Lisa Kelley provided field assistance. Research was conducted under ACA Permit 2009-013, and MMPA Permits 774-1714 and 14097 issued to NOAA Southwest Fisheries Science Center. Phil Morin and Andy Foote provided useful comments on an earlier draft of this paper.
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