You Are What You Eat: Foraging Specializations and Their Influence on the Social Organization and Behavior of Killer Whales

Abstract

The feeding ecology of predators can have a profound effect on their life history and behaviour. The killer whale—the apex marine predator—has a cosmopolitan distribution throughout the world’s oceans. Globally, it is a generalist predator with a diverse diet, but regionally, different socially and genetically isolated killer whale populations can have highly specialized foraging strategies involving only a few types of prey. In the eastern North Pacific, the three sympatric killer whale lineages have distinct dietary specializations: one feeds primarily on marine mammals, another on salmon, and the third appears to specialize on sharks. These ecological specializations are associated with distinct patterns of seasonal distribution, group size, social organization, foraging behavior, and acoustic activity. Divergent foraging strategies may have played a major role in the social isolation and genetic divergence of killer whale populations.

Full text

75
J. Yamagiwa and L. Karczmarski (eds.), Primates and Cetaceans: Field Research
and Conservation of Complex Mammalian Societies, Primatology Monographs,
DOI 10.1007/978-4-431-54523-1_4, © Springer Japan 2014
Chapter 4
You Are What You Eat: Foraging
Specializations and Their Infl uence
on the Social Organization and Behavior
of Killer Whales
John K.B. Ford and Graeme M. Ellis
J. K.B. Ford (*) • G. M. Ellis
Fisheries and Oceans Canada, Pacifi c Biological Station , Nanaimo , BC , Canada V9T 6N7
e-mail: John.K.Ford@dfo-mpo.gc.ca

76
Abstract The feeding ecology of predators can have a profound effect on their life
history and behaviour. The killer whale—the apex marine predator—has a cosmo-
politan distribution throughout the world’s oceans. Globally, it is a generalist preda-
tor with a diverse diet, but regionally, different socially and genetically isolated
killer whale populations can have highly specialized foraging strategies involving
only a few types of prey. In the eastern North Pacifi c, the three sympatric killer
whale lineages have distinct dietary specializations: one feeds primarily on marine
mammals, another on salmon, and the third appears to specialize on sharks. These
ecological specializations are associated with distinct patterns of seasonal distribu-
tion, group size, social organization, foraging behavior, and acoustic activity.
Divergent foraging strategies may have played a major role in the social isolation
and genetic divergence of killer whale populations.
Keywords Apex predator • Feeding ecology • Orcinus orca
4.1 Introduction
Ecological specialization is an important factor promoting the evolution of biologi-
cal diversity and speciation (Futuyma and Moreno 1988 ; Robinson et al. 1996 ;
Dieckmann and Doebeli 1999 ; Schluter 2001 ; V i a 2001 ). Optimal foraging theory
predicts that selection will generally favor dietary specialization, as specialists
have a competitive advantage over generalists in foraging effi ciency (as in the
adage, “the jack-of-all-trades is the master of none”) (Stephens and Krebs 1986 ;
Futuyma and Moreno 1988 ; Robinson et al. 1996 ). Such selection may drive the
divergent evolution of a wide variety of adaptive traits involving morphology,
physiology, and behavior of populations or subpopulations with different foraging
strategies or in contrasting environments. Divergent selection between sympatric
populations may lead to assortative mating, reproductive isolation, and, ultimately,
speciation (Dieckmann and Doebeli 1999 ; Schluter 2001 ; V i a 2001 ; McKinnon
et al. 2004 ) .
Killer whales, the largest of the dolphins (family Delphinidae), provide an excep-
tional opportunity to gain insight into the processes and outcomes of ecological
specialization and divergence in a highly social and versatile mammalian predator.
This species (only a single species, Orcinus orca , is currently recognized) is one of
the most widely distributed mammals on the planet. It has a cosmopolitan distribu-
tion in all the world’s oceans, from the pack ice edges in both the Northern and
Southern Hemispheres through the equatorial tropics (Ford 2002 ). Although rare in
many regions, it is relatively common in cool, productive, high-latitude waters, par-
ticularly in nearshore areas. Despite their wide distribution, killer whales are not
abundant, with a minimum estimated global population of 50,000, but probably not
greatly more (Forney and Wade 2006 ). Killer whales occupy the top trophic posi-
tion in the oceans and have no predators. As a species, killer whales could be con-
sidered generalist predators, with an extremely diverse array of more than 140
J.K.B. Ford and G.M. Ellis

77
species of vertebrates and invertebrates—from small schooling fi sh to the largest of
the cetaceans—recorded as prey (Ford 2009 ). However, fi eld studies in several
global regions have revealed that local populations can have remarkably specialized
diets and may forage selectively for only a very small subset of the prey species that
the predator is capable of consuming. In this chapter, we provide a description of
three distinct killer whale lineages that co-occur in coastal waters of the northeast-
ern Pacifi c, focusing in particular on the infl uence that ecological specialization
appears to have had on their divergent lifestyles, including habitat use patterns,
social structure, behavior, and use of underwater sound. We also provide a brief
overview of how these lineages came to be identifi ed and known in these waters and
of recent work in other regions that suggests that ecological specialization is char-
acteristic of this apex social predator.
4.2 Discovery of Killer Whale Lineages
in the Eastern North Pacifi c
Before the 1970s, scientifi c understanding of the killer whale was poor and was
based almost entirely on anecdotal or opportunistic observations rather than on
dedicated scientifi c studies (Martinez and Klinghammer 1970 ). However, a live-
capture fi shery for killer whales that developed during the late 1960s in nearshore
waters of southern British Columbia, Canada, and northern Washington State, USA,
highlighted the need for basic abundance and life history data for management. As
a result, in 1972 our late colleague, Michael Bigg, initiated fi eld studies of killer
whales in this area based primarily on the identifi cation of individuals from photo-
graphs of natural markings on the whales’ dorsal fi n and grey “saddle patch” at the
base of the fi n. This technique was considered quite novel and unproven at the time,
but Bigg quickly showed that it was an effective means of collecting reliable popu-
lation abundance and life history data on these diffi cult-to-study animals (Bigg et al.
1976 ). We joined this fi eld effort at different points in the 1970s and, working
together with Bigg and our colleague Ken Balcomb in Washington State, broadened
the study’s scope to include social organization, foraging ecology, behavior, and
vocalizations (Bigg et al. 1987 ).
By the late 1970s, it was apparent that two different types of killer whales coex-
isted in the region. One type, named “residents,” lived in stable groups of 10 to 25
and were found reliably in predictable “core areas” throughout at least summer and
fall. A second type was found in the same waters but only rarely and sporadically.
These whales were observed alone or in small groups of 2 to 6, tended to swim close
along shorelines, often erratically, and were never seen to mix with the larger “resi-
dent” groups. As it was thought that these whales were merely passing through the
home ranges of the residents, they were named “transients” (Bigg 1982 ). Resident
and transient killer whales were occasionally observed within a few hundred meters
of each other but showed no obvious reaction to the presence of the other whales
and did not intermingle. However, resident groups frequently mixed with other
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

78
residents and transients with other transients. Although residents and transients
were clearly socially isolated, it was not certain what these two types represented.
Initially it was thought that transients were individuals that had dispersed from resi-
dent groups, possibly in other regions, and were adopting a “low profi le” behavior
while transiting core areas of residents. However, subtle differences in dorsal fi n
shape and pigmentation suggested an underlying genetic distinction between them.
As the number of observations of feeding grew in the early 1980s, evidence mounted
that residents and transients were distinct ecotypes with fundamentally different
diets—residents prey on fi sh and transients on marine mammals (Bigg et al. 1985 ,
1987 ). That these two types of whales specialize on such different kinds of prey
helped explain the growing number of differences we observed in the movement
patterns, social structure, vocalizations, and behavior of residents and transients.
To our surprise, in the early 1990s we discovered a third type of killer whale,
named “offshores,” in British Columbian waters (Ford et al. 1992 ; Ford et al. 2000 ).
These whales have slightly different fi n shapes than residents and transients and
appear to be somewhat smaller in body size. Offshore killer whales generally prefer
the outer continental shelf, and it was only when we expanded our study area to
include these waters that we found these whales. Residents and transients also use
these outer waters, and offshores have recently made more frequent appearances in
nearshore areas (Dahlheim et al. 2008 ). Despite their mostly sympatric distribution,
all three killer whale types maintain social isolation from each other (Ford et al.
2000 ). From the few available observations of predation by offshore killer whales
and their patterns of behavior and vocal activity, it appears that they are primarily or
entirely fi sh feeders with a probable specialization on sharks (Ford et al. 2000 ,
2011 ; Jones 2006 ; Dahlheim et al. 2008 ).
In addition to our own long-term studies in British Columbia and Washington
State, numerous other researchers have undertaken fi eldwork on various aspects of
the life history, ecology, and behavior of killer whales, both in our study area and in
adjacent coastal waters. Over the years, these efforts have together provided a much
improved understanding of the divergent ecological specializations of residents and
transients and the role these have played in defi ning the lifestyles of these lineages.
4.3 Population Delineation of Lineages
Resident, transient, and offshore killer whale lineages are sympatric in coastal
waters of the eastern North Pacifi c from California to the Aleutian Islands in
Alaska. Molecular studies have confi rmed what earlier observations suggested —
that the three lineages are genetically distinct and gene fl ow between them is mini-
mal or absent (Stevens et al. 1989 ; Hoelzel et al. 1998 ; Barrett-Lennard 2000 ;
Morin et al. 2010 ). At least two of these lineages—residents and transients—are
represented by multiple discrete populations of typically a few hundred individuals.
Four populations have been described for residents (Matkin et al.
1999 ; Ford et al.
2000 ; Matkin et al. 2007a ). Each population ranges over roughly 1,300- to
J.K.B. Ford and G.M. Ellis

79
1,800-km sections of coastline that overlap substantially. Despite overlapping dis-
tribution, each population generally occupies rather discrete areas, especially dur-
ing summer and fall. Groups of resident whales from adjacent populations have
been observed in close proximity on a few occasions, but no intermingling has
taken place. However, groups belonging to the same population frequently join and
travel together, occasionally forming large multigroup aggregations that may per-
sist for several days. DNA fi ngerprinting indicates that mating takes place between
groups within each resident population, and intermating between populations is
extremely rare (Barrett- Lennard 2000 ) .
Transient killer whales are subdivided into at least fi ve regional populations,
each typically composed of 100–300 individuals (Bigg et al. 1987 ; Black et al.
1997 ; Ford and Ellis 1999 ; Matkin et al. 1999 , 2007a ). Groups of transients within
each population regularly intermingle and, in contrast to residents, they will also
associate with members of adjacent transient populations during the infrequent
occasions when they roam into the range of another population (Ford and Ellis
1999 ; Ford et al. 2007 ). Offshore killer whales appear to consist of a single popula-
tion of at least 250 animals that ranges widely over the continental shelf, from
southern California to the eastern Aleutian Islands, Alaska (Ford et al. 2000 ; Matkin
et al. 2007a ; Dahlheim et al. 2008 ). The extent of potential movements beyond the
continental shelf for any of these whales is unknown because of the lack of fi eld
effort in offshore waters.
4.4 Dietary Specialization
Gaining insight into the feeding habits of free-ranging cetaceans is diffi cult because
predation usually takes place underwater and out of sight. We have studied the diets
of resident, transient, and offshore killer whales using three different methods:
(1) direct observation of predation when it takes place at the surface, (2) collection
of prey fragments left in the water column following a kill, and (3) recovery of prey
remains from the stomachs of beach-cast carcasses. Others have also used chemical
analyses of skin and blubber biopsy samples collected from killer whales to infer
diet from stable isotope ratios, fatty acids, and levels of various types of contami-
nants (e.g., Krahn et al. 2007 ).
Surface observations and identifi cation of prey fragments from kills indicate that
the diet of resident killer whales in British Columbia (Fig. 4.1 ) consists primarily of
teleost fi shes, in particular the Pacifi c salmonids ( Oncorhynchus spp.) (Fig. 4.2 :
Ford et al. 1998 ; Saulitis et al. 2000 ; Ford and Ellis 2006 ). Non-salmonid fi shes
such as lingcod ( Ophiodon elongatus ), Dover sole ( Microstomus pacifi cus ), and
Pacifi c halibut ( Hippoglossus stenolepis ) have also been identifi ed from predation
events, but these represent less than 3 % of observed kills. A surprising result of our
prey fragment sampling has been the pronounced preference that residents have
for Chinook salmon ( Oncorhynchus tshawytscha ). In total, more than 70 % of iden-
tifi ed salmonid kills have been Chinook, despite this species being one of the least
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

80
common of the fi ve salmonid species available in the whales’ habitat (Ford and Ellis
2006 ). Chinook predominated in our samples even when other salmonids, such as
sockeye ( O. nerka ) and pink ( O. gorbuscha ) salmon, were far more abundant in
foraging areas during summer spawning migrations, outnumbering Chinook by as
many as 500 fi sh to 1 (Ford et al. 1998 ; Ford and Ellis 2006 ). Chum salmon ( O. keta )
are signifi cant prey during a short period in the fall, but Chinook still appear to be
taken preferentially. Prey remains recovered from beach-cast carcasses of residents
are generally consistent with our observations of predation. Chinook salmon has
been identifi ed in most stomach contents to date, and various non-salmonids and
squid have also been represented occasionally (Ford et al. 1998 ).
I t i s m o s t p r o b a b l e t h a t t h e w h a l e s ’ p r e f e r e n c e f o r d i f f e r e n t s a l m o n i d s — a n d o t h e r
prey species for that matter—is proportional to their relative profi tability. Chinook
are by far the largest of the Pacifi c salmon, commonly reaching sizes of more than
20 kg, and they tend to have the highest lipid content of the salmonids, enhancing
their net energy density. Chum salmon are the second largest salmonid and can reach
10 kg or more. The much smaller sockeye and pink salmon seem to be of little inter-
est to the whales, despite their brief but often great abundance during summer.
In striking contrast to resident killer whales, transient killer whales (Fig. 4.3 )
have only been observed to hunt and consume endothermic prey, primarily marine
mammals and occasionally seabirds. In British Columbia, Washington State, and
Southeast Alaska, the most frequent prey species by far (about 50 % of kills) is the
harbour seal ( Phoca vitulina ), a small (average, 60–80 kg) pinniped that is common
throughout nearshore waters of the region (Fig. 4.2 ) (Ford et al. 1998 ; Matkin et al.
Fig. 4.1 A male resident killer whale surfaces following capture of a Chinook salmon, the primary
prey species of this ecotype. (Photograph by M. Malleson)
J.K.B. Ford and G.M. Ellis

81
2007a , b ) . H a r b o u r p o r p o i s e ( Phocoena phocoena ) a n d D a l l ’ s p o r p o i s e ( Phocoenoides
dalli ) t o g e t h e r m a k e u p a b o u t o n e - q u a r t e r o f o b s e r v e d k i l l s , w i t h t h e r e m a i n d e r c o m -
posed of Steller sea lions ( Eumetopias jubatus ) , C a l i f o r n i a s e a l i o n s ( Zalophus cali-
fornianus ) , P a c i fi c white-sided dolphins ( Lagenorhynchus obliquidens ) , m i n k e
whales ( Balaenoptera acutorostrata ) , n o r t h e r n e l e p h a n t s e a l s ( Mirounga angustiros-
tris ) , a n d v a r i o u s s e a b i r d s p e c i e s ( F o r d e t a l . 1998 , 2005 ) . S w i m m i n g d e e r
( Odocoileus hemionus ) a n d m o o s e ( Alces alces ) h a v e o n r a r e o c c a s i o n s b e e n r e p o r t e d
to be killed by killer whales in the region, almost certainly transients (Pike and
MacAskie
1969 ; M a t k i n e t a l . 1999 ) . S e a b i r d s d o n o t s e e m t o b e a n i m p o r t a n t p r e y
item of transient killer whales. Only a minority of seabirds that are harassed and
killed by transients are ultimately consumed: most are abandoned. Interaction with
seabirds usually involves juvenile whales and may represent play behavior that ulti-
mately functions to develop prey handling skills (Ford et al. 1998 ; S a u l i t i s e t a l . 2000 ) .
Transients have not been observed to take any fi sh species, nor have any fi sh remains
been identifi ed in stomach contents of beach-cast carcasses of transients (Ford et al.
1998 ; Saulitis et al. 2000 ; Heise et al. 2003 ).
Fig. 4.2 Frequency distribution of prey species observed to be consumed by resident ( top , n = 439
kills) and transient ( bottom , n = 251 kills) killer whales in coastal waters of British Columbia,
Washington State, and southeastern Alaska. [Data from Ford et al. (
1998 ), Ford and Ellis ( 2006 ),
and Ford and Ellis (unpublished data)]
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

82
There is little evidence that transient individuals or matrilines specialize on par-
ticular types or species of marine mammals, despite the very different tactics needed
to capture and kill them (harbour seals versus Dall’s porpoise, for example; Ford
et al. 1998 ). Our long-term monitoring of transient predation has shown that the
variety of prey species taken by particular individuals or groups is strongly corre-
lated with the cumulative number of predation events documented for those animals
(Ford et al. 1998 ). Predation of minke whales by transients in our study area is
uncommon, but a particular matriline (the T18 group) has been involved in more
cases than one would expect by chance (Ford et al. 2005 ; J.K.B.F. and G.M.E.,
unpublished data). This matriline also hunts more typical prey, such as harbour seals
and porpoises. There are no records of transients in our study area having success-
fully killed large whales such as adult gray ( Eschrichtius robustus ), humpback
( Megaptera novaeangliae ), fi n ( Balaenoptera physalus ), or blue ( Balaenoptera
musculus ) whales. Indeed, foraging transients rarely show any reaction to these
potential prey species despite their frequent presence in their vicinity (Jefferson
et al. 1991 ). This indifference is likely related to the diffi culty in catching the fast-
swimming fi n and blue whales and the risk of injury posed by defensive responses
from gray and, especially, humpback whales (Ford and Reeves 2008 ). Gray whale
calves and juveniles, however, are frequently targeted by foraging transients in cen-
tral California (Ternullo and Black 2002 ) and around the eastern Aleutian Islands,
Alaska (Barrett-Lennard et al. 2005 ; Matkin et al. 2007 ).
Offshore killer whales are the least known of the three lineages in the region.
They have been observed consuming a probable Pacifi c halibut (Jones 2006 ) and
possibly blue sharks ( Prionace glauca ) and Chinook salmon (Dahlheim et al. 2008 ).
Fig. 4.3 A female transient killer whale hunting for the preferred prey of this ecotype, harbour
seals. (Photograph by J. Towers)
J.K.B. Ford and G.M. Ellis

83
Stomach contents of a killer whale identifi ed as an offshore by mtDNA analysis
included two carcharinid sharks and two opah ( Lampris regius , a large pelagic tele-
ost fi sh; Morin et al. 2006 ). Recently, we observed offshore killer whales feeding on
multiple Pacifi c sleeper sharks ( Somniosus pacifi cus ) (Ford et al. 2011 ). A diet con-
sisting largely of sharks, with their abrasive skin, might explain the extreme tooth
wear that appears to be common in offshore killer whales (Ford et al. 2011 ). Stable
isotope ratios and fatty acid profi les determined from skin and blubber biopsy sam-
ples also suggest that the diet of offshore killer whales is distinct from that of either
resident or transient lineages (Herman et al. 2005 ; Krahn et al. 2007 ).
4.5 Social Organization
Similar to most delphinids, killer whales are highly social, group-living animals.
However, the social structure of resident, transient, and offshore killer whales dif-
fers considerably, and these differences appear to be related to and are likely deter-
mined by their respective ecological specializations. Resident killer whales live in
matrilines that are exceptionally stable in composition. A typical matriline is com-
posed of an older female, her sons and daughters, and the offspring of her daughters.
Because longevity of females can reach 80 years and females have their fi rst viable
calf at about 14 years (Olesiuk et al. 2005 ), a matriline may contain as many as four
generations of maternally related individuals. More than 30 years of demographic
data have demonstrated that dispersal from the matriline is virtually absent in resi-
dent killer whales—both males and females remain in their natal group for life
(Bigg et al. 1990 ; Ford et al. 2000 ; Ellis et al. 2007 ). In no case has an individual
whale been observed to leave its matriline and join another on a long-term basis,
other than in a few rare cases involving orphans.
Members of resident matrilines travel together and they seldom separate by more
than a few kilometers or for more than a few hours. Contact is maintained among
matriline members by the exchange of discrete, stereotyped underwater calls that
are unique to the group (Ford 1989 , 1991 ; Miller et al. 2004 ). Matrilines frequently
travel in the company of certain other matrilines that are closely related, based on
high degrees of call similarity, and likely shared a common maternal ancestor in the
recent past. Matrilines that spend the majority of their time together are designated
as pods (Bigg et al. 1990 ). Pods are less stable than matrilines, and member matri-
lines may spend days or weeks apart. However, matrilines still spend more time
with others from their pod than with those from other pods. In British Columbia,
resident pods are on average composed of three matrilines (range = 1–11; Ford et al.
2000 ), with a mean total size of 18 whales (range = 2–49; Ford et al. 2000 ). Residents
often form large temporary aggregations involving multiple matrilines and pods,
especially at times when prey densities are high.
A level of social structure above the resident pod is the clan, which is defi ned by
patterns of call similarity. Clans are composed of pods that share a portion of their
repertoire of stereotyped calls. Different clans have no calls in common. Pods
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

84
belonging to a clan are likely descendants of an ancestral pod, and their acoustic
similarities refl ect this common heritage. Call repertoires are traditions passed on
across generations by vocal learning, and calls actively or passively change in struc-
ture or use over time. Calls are retained within the lineage because of the lack of
dispersal from matrilines. Clans are sympatric, and the two to nine pods that make
up each clan frequently travel together as well as with pods from different clans
(Ford 1991 ; Yurk et al. 2002 ).
Transient killer whale society lacks the closed, strictly matrilineal structure seen
in residents. Transients usually travel in groups of two to six individuals, much
smaller than the typical size of resident matrilines and pods. In contrast to residents,
offspring often disperse from the natal matriline for extended periods or perma-
nently (Bigg et al. 1987 ; Ford and Ellis 1999 ; Baird and Whitehead 2000 ). Female
offspring usually leave their natal group around the time of sexual maturity and
travel with other transient groups. These young females usually give birth to their
fi rst calf shortly after dispersing. Once dispersed, these females may rejoin their
natal matriline occasionally, but generally only for brief periods after they have
calves of their own. Male dispersal does take place, but the pattern is less clear
because of uncertainty in the status of many individuals in the population. The
range of transients appears to extend beyond our study area, possibly into offshore
waters, and gaps of many years can occur between sightings of individuals (Ford
and Ellis 1999 ; Ford et al. 2007 ). There are numerous cases of mothers and a single
adult son staying together for decades, but few where a mother and more than one
adult son have persisted. Male siblings may disperse from these groups at puberty,
but if so they must leave our study area as none has been resighted after disappearing
from the natal group, either as a member of another group or as a lone individual.
All lone adult males found in the study area appear to have lost their mothers
through mortality. These individuals often travel alone or associate with a variety of
different transient matrilines, but rarely with other lone males. The associations of
transient matrilines are very dynamic, and they do not form consistent groupings
equivalent to resident pods. Also, in contrast to residents, transient populations do
not seem to be acoustically subdivided into clans. Instead, all transients in a popula-
tion share a distinctive set of calls, although some additional calls or variants of
shared calls may be specifi c to a subregion or portion of the population (Ford 1984 ;
Deecke et al. 2005 ) .
The typically small size of transient groups is likely a result of the foraging strat-
egy of this lineage. Transients generally hunt other marine mammals with stealth:
they swim quietly to prevent detection by their acoustically sensitive prey, and
attack using the element of surprise (Ford 1984 ; Barrett-Lennard et al. 1996 ). This
strategy no doubt constrains group size, as larger groups such as those of residents
would increase the probability of the predators being detected by their prey. Small
groups may also be most energetically effi cient for transients when hunting smaller
marine mammals such as harbour seals (Baird and Dill 1996 ).
A s w i t h m o s t d e t a i l s o f t h e i r l i f e h i s t o r y a n d b e h a v i o r , t h e s o c i a l o r g a n i z a t i o n o f
offshore killer whales is poorly understood. Their group sizes tend to be relatively
large, certainly much larger than those of transients, and possibly larger on average
J.K.B. Ford and G.M. Ellis

85
than residents. Groups of 2 to 100 or more individuals have been documented in
encounters with offshores off the coast of British Columbia, with about half involv-
ing 20 or more individuals. These larger groups probably represent temporary gath-
erings of smaller social units, possibly related to prey density as in residents. We
have documented persistent bonds lasting more than a decade between females and
adult males, which likely represent mothers and their adult sons. However, we have
not observed long-term associations between reproductive females, as seen in the
multi-generation matrilines of residents. This fi nding suggests a dynamic society
with dispersal from the natal matriline as in transients, but frequent formation of
larger aggregations as in residents.
4.6 Seasonality and Habitat Use
All three lineages of killer whales are found in coastal waters of the northeastern
Pacifi c throughout the year, but there are signifi cant differences in their seasonality
and patterns of habitat use. The seasonal movements of resident killer whales are
closely tied to those of their primary prey. Several studies have demonstrated cor-
relations between resident whale occurrence in nearshore waters and the aggregate
abundance of multiple salmon species migrating through nearshore waters to coastal
spawning rivers in British Columbia and Washington State (Heimlich-Boran 1986 ;
Guinet 1990 ; Nichol and Shackleton 1996 ). However, these analyses were under-
taken before it was known that these whales forage selectively for Chinook salmon
and shun the smaller but much more abundant pink and sockeye salmon (Ford et al.
1998 ; Ford and Ellis 2006 ). Correlations of whale occurrence with these abundant
salmonids are thus incidental, and the whales are instead attracted by migrating
Chinook salmon, which pass through these migratory corridors in lower numbers
but concurrently with the smaller species. Movements of resident killer whales in
this area during October and November are clearly associated with fall migrating
chum salmon, which the whales do consume (Nichol and Shackleton 1996 ; Ford
and Ellis 2006 ). Interestingly, a different population of resident killer whales in
south-central Alaska moves into Prince William Sound during midsummer, where
they forage extensively for coho salmon ( Oncorhynchus kisutch ) (Saulitis et al.
2000 ). Neither Chinook nor chum salmon are common in this area at this time of
year, although these same whales feed on Chinook and chum salmon in other areas
and times of year (C. Matkin, personal communication).
During winter and spring, resident whales mostly vacate their summer habitat in
nearshore waters and appear to range widely along the outer exposed coast. It is
likely that the whales maintain their focus on Chinook salmon prey during this time
of year. Most other salmonid species are pelagic and unavailable to the whales
during this time of year, but nonmigratory or early spawning runs of Chinook are
found in these outer coast waters (Ford and Ellis 2006 ). Residents may also increase
their consumption of non-salmonid species such as Pacifi c halibut during winter
and spring.
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

86
Compared to residents, transient killer whales have a relatively uniform pattern
of occurrence in nearshore waters throughout the year, likely because their primary
prey species—harbour seal, harbour porpoise, Dall’s porpoise, and Steller sea
lion—are nonmigratory and available in all months of the year. However, there is an
interesting seasonal peak in local occurrence along the west coast of North America
that appears to coincide with the pupping season of harbour seals. In Glacier Bay,
the northern limit of the range of the so-called “West Coast” transient population
(~58°30′N latitude), transient whale occurrence peaks in June and July ( Matkin
et al. 2007 ). Near the southern extent of their range, around Vancouver Island (~48°
to 51°N latitude), there is an obvious peak in occurrence during August and
September (Baird and Dill 1995 ). Both these periods coincide with local peaks of
pupping and weaning of harbour seals, which exhibits a latitudinal cline in timing
along the West Coast (Temte et al. 1991 ). Pups are likely easy and abundant prey for
transients, and the whales appear to move in accordance with their seasonal
availability.
Offshore killer whales appear to exhibit a diffuse seasonal shift in distribution
along the West Coast of North America. The majority of sightings in the southern
portion of their known range, off central and south California, have been recorded
during fall and winter (September to March; Dahlheim et al. 2008 ). Sightings in
Alaska, the northern portion of the range of offshore killer whales, have taken place
only during April to September, but there is minimal observer effort during winter
in this area (Dahlheim et al. 2008 ; C. Matkin, personal communication). Off British
Columbia, roughly the latitudinal midpoint of their range, sightings of offshores
have been recorded in all months. Without a better understanding of the primary
prey species of offshore killer whales, it is not possible to interpret the signifi cance
of this apparent seasonal distribution shift.
Differences are also apparent in fi ner-scale patterns of habitat use by the three
killer whale lineages. Residents congregate during summer and fall in core feeding
areas in locations where geography and tidal currents act to concentrate migratory
salmon (Heimlich-Boran 1988 ; Nichol and Shackleton 1996 ; Saulitis et al. 2000 ;
Ford 2006 ). During the peak of salmon abundance, the majority of matrilines in a
resident population may gather in these core areas, and individual matrilines or pods
may spend weeks in a relatively restricted area that the whales could transit in a day
or two. There are distinctions among the movement patterns of different resident
pods within a population’s overall range. Although most resident groups may be
observed in most parts of the range, particular pods and matrilines have preferred
areas that they frequent more often than other groups (Osborne 1999 ; Ford 1991 ,
2006 ; Ford et al. 2000 ; Hauser et al. 2007 ), likely because of the benefi t of foraging
in familiar areas where individuals have experience in locating local concentrations
of prey.
While in their core summer feeding areas, resident killer whales spend
50–65 % of their time foraging (Heimlich-Boran 1988 ; F o r d 1989 ; Morton 1990 ).
Between foraging bouts, the whales group together and socialize or rest, which
together represent about 30–40 % of their time. In at least two resident populations,
the whales may also spend considerable time rubbing their bodies on certain
J.K.B. Ford and G.M. Ellis

87
shelving, pebble beaches that have been used traditionally for many years (Ford 1989 ;
Matkin et al. 1999 ).
In contrast to resident whales, transient killer whales typically do not remain for
long in any particular location. They are almost constantly on the move, swimming
from one prey hotspot to the next. Because of their apparent reliance on stealth for
capturing marine mammals, it is no doubt more productive for transients to hunt
elsewhere once potential prey is alert to their presence. By covering 75–150 km of
coastline per day, transients tend to undergo more frequent extensive travel through-
out their range than do residents. Nonetheless, as with residents, at least some tran-
sient groups have preferred areas within the overall population range, where local
knowledge of the location of pinniped haulouts or predictable concentrations of
small cetaceans may serve to improve hunting effi ciency (Ford and Ellis 1999 ).
Compared to residents, transients dedicate considerably more time to foraging and
traveling (>75 % of their activity budget: Morton 1990 ; Baird and Dill 1995 ).
Socializing and resting activities, which comprise about one-third of the activity
budget for residents, are seldom exhibited by transients (<10 % of activities; Morton
1990 ; Baird and Dill 1995 ; Barrett-Lennard et al. 1996 ; Deecke et al. 2005 ). Beach
rubbing has not been reported for transients.
Details of habitat use by offshore killer whales are not yet clear because of the
comparatively infrequent encounters with this population. Long-distance move-
ments appear to be undertaken frequently by offshore whales. Several identifi ed
individuals have been observed at the extremities of the population’s known range,
which extends more than 4,000 km from the Aleutian Islands to Southern California
(Dahlheim et al. 2008 ). Any potential habitats that may be used preferentially by a
subset of the offshore population, and what prey species may drive their move-
ments, have yet to be described.
4.7 Foraging Behavior
The distinct diets of killer whale lineages are associated with corresponding con-
trasts in their foraging behavior. When foraging, members of a resident killer whale
matriline or pod spread out, often over areas of several square kilometers, with
individuals or small subgroups diving and surfacing independently while swimming
generally in the same direction. They maintain contact and likely coordinate move-
ments through the frequent exchange of loud underwater calls, which are effective
to ranges of 10–25 km (Ford 1989 ; Miller et al. 2004 ; Miller 2006 ). When foraging
in coastal inlets, channels, and straits, individuals and small maternal groups usually
forage along the shoreline, while other whales, particularly mature males, forage
alone farther from shore and in deeper water. Foraging resident whales dive for
2–3 min (Ford 1989 ; Morton 1990 ) to depths typically less than 30 m, but occasion-
ally to more than 150 m (Baird et al. 2005a ). These depths are similar to those used
by their primary prey species, Chinook salmon (Candy and Quinn 1999 ).
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

88
Foraging resident killer whales fi nd prey using echolocation, which may be
effective for detecting Chinook salmon at ranges of 100 m or more (Au et al. 2004 ).
By foraging in loosely dispersed groups, the detection rate of scattered salmon is
likely enhanced. However, residents whales do not appear to cooperatively herd or
capture prey. Rather, prey capture is undertaken primarily by individuals with occa-
sional cooperation from offspring, siblings, or other close matrilineal kin. The
majority of salmonid prey items captured by adult females and subadults are brought
to the surface, where they are broken up for sharing within the matriline or for pro-
visioning young offspring (Ford and Ellis 2006 ). Adult males usually capture and
consume salmonid prey alone.
In contrast to residents, transient killer whales forage in near silence in an appar-
ent attempt to minimize detection by their acoustically sensitive marine mammal
prey (Ford 1984 ; Morton 1990 ; Barrett-Lennard et al. 1996 ; Deecke et al. 2005 ).
Transients rarely exchange underwater calls while hunting for prey (Deecke et al.
2005 ), and echolocation click production is also greatly suppressed (Barrett-
Lennard et al. 1996 ). Both pinniped and cetacean prey have excellent hearing abili-
ties at the frequencies used by killer whales for calling and echolocation and could
detect and potentially evade approaching transients if they were to vocalize (Barrett-
Lennard et al. 1996 ; Deecke et al. 2005 ). As vocalizing would likely incur high
costs in terms of reduced rates of prey capture, transients appear to depend on pas-
sive listening to detect and approach prey from a distance, likely cueing on the
animals’ vocalizations or swimming noises (Barrett-Lennard and Heise 2006 ).
There is little cost associated with the production of underwater sounds for resident
whales because salmonids and most other fi sh have relatively low hearing sensitiv-
ity to such frequencies and are unlikely to detect approaching whales at a distance
(Barrett-Lennard et al. 1996 ; Deecke et al. 2005 ).
T r a n s i e n t k i l l e r w h a l e s e m p l o y t w o f a i r l y d i s t i n c t m o d e s o f f o r a g i n g : n e a r s h o r e
and open water. When foraging nearshore, the whales swim in relatively tight groups
and follow the contour of the shoreline, round headlands, and enter bays without
hesitation (Morton 1990 ; B a r r e t t - L e n n a r d e t a l . 1996 ) . T h e y o f t e n c i r c l e s m a l l i s l e t s
and reefs, particularly those that serve as pinniped haulouts. Resident whales, in
contrast, forage along more direct routes, usually swimming from headland to head-
land. Dive durations of foraging transient whales are typically twice the duration of
the 2- to 3-min dives of residents, and may exceed 10 min (Morton 1990 ) . N e a r s h o r e
foraging is generally associated with capture of pinniped prey, particularly harbour
seals (Baird and Dill 1995 ; B a r r e t t - L e n n a r d e t a l . 1996 ; S a u l i t i s e t a l . 2000 ) . W h e n
foraging in open water, transient groups spread out over a larger area, with individu-
als swimming several hundred meters apart, often roughly abreast. Most prey cap-
tured during open water foraging are porpoises or dolphins, but seals or sea lions
may also be taken (Barrett-Lennard et al. 1996 ; S a u l i t i s e t a l . 2000 ) .
Transients share the majority of their prey (Baird and Dill 1995 ), likely to an
even greater extent than do residents because of the larger body masses of most
marine mammal prey items. Transient group members frequently use cooperative
hunting tactics to catch and subdue their prey (Baird and Dill 1995 ; Ford et al.
1998 ). Predation on Steller sea lions, for example, can be extended events that
J.K.B. Ford and G.M. Ellis

89
may entail risk of injury to the attacking whales. These prey can be large (up to
1,000 kg in males) with sizeable canine teeth that can infl ict signifi cant wounds
during defensive or retaliatory actions. Groups of transient killer whales attack
single sea lions in open water by circling the animal so as to prevent it from reach-
ing shore, while individuals take turns rushing toward the prey and ramming it or
striking it with their tail fl ukes. This action may continue for 1–2 h until the animal
is suffi ciently debilitated so that it can be safely grasped, drowned, and shared
among group members. Transients may also hunt fast-swimming Dall’s porpoise
using a cooperative “tag team” tactic where individuals take turns chasing the prey
animal to exhaustion. Transients have been also been observed to herd groups of
50+ Pacifi c white- sided dolphins into confi ned or shallow bays where individuals
can be readily captured. Transients hunt these diffi cult-to-capture species in sig-
nifi cantly larger groups than when foraging for the smaller harbour seals (Ford
et al. 1998 ). These groups often represent temporary associations of smaller, stable
social units.
4.8 Acoustic Communication
As do most delphinids, killer whales have a well-developed acoustic communica-
tion system. However, as noted earlier, the types and extent of vocalization show
major differences among lineages. Resident killer whales frequently exchange stri-
dent calls from stable repertoires of a dozen or more call types. These learned call
types or their variants are specifi c to clans, pods, and matrilines, and thus encode the
matrilineal genealogy of individuals (Ford 1991 ). This specifi city likely enhances
the effectiveness of these calls as intragroup contact signals, especially when whales
are dispersed and traveling in association with other matrilines or pods. These
group-specifi c dialects may also play a role as a behavioral mechanism to prevent
inbreeding. As there is no dispersal from the natal matriline, resident killer whales
would be at considerable risk of inbreeding without a reliable means of distinguish-
ing between kin and non-kin mating partners. Group-specifi c call repertoires appear
to serve such a function (Ford 1991 ), and genetic studies have shown that resident
whales mate with individuals that are outside the pod or clan and are acoustically
dissimilar (Barrett-Lennard 2000 ).
Although transient killer whales spend much of their time foraging for marine
mammals in silence, they become highly vocal while attacking and consuming their
prey (Ford 1984 ; Deecke et al. 2005 ). Calling at such times likely carries little cost
as stealth is no longer needed, and it may help coordinate cooperative attack tactics
within the group or serve other social functions after the kill is made. Similar to resi-
dent killer whales, transients have repertoires of distinctive stereotyped call types.
Unlike residents, however, these repertoires generally do not differ among groups.
As there is dispersal from the natal matriline in this ecotype, group-specifi c calls
would not be expected. Also, dispersal reduces the risk of inbreeding, so the require-
ment for an acoustic outbreeding mechanism may be reduced in transients.
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

90
The fi sh-eating offshore killer whales are as vocal as resident killer whales.
Preliminary analyses indicate that offshores produce stereotyped calls that are dis-
tinct from any of those of residents or transients, but it is not yet known whether any
calls are specifi c to particular groups. As our understanding of the social dynamics
of this poorly known lineage improves, patterns of call use should become clearer.
4.9 Specializations in Other Regions
Field studies in other global regions have provided additional evidence that ecologi-
cal specializations are typical of most killer whale populations. Although these
populations are not as well known as resident and transients in the eastern North
Pacifi c, it is apparent that at least in some cases their specializations have had simi-
lar infl uences on patterns of social structure, behavior, and vocal activity. Off the
northern coast of Norway, a population of killer whales moves seasonally in relation
to their primary prey, the Atlantic herring ( Clupea harengus ) (Similä 1997 ). In
coastal fjords where herring congregate in high densities during fall and winter, the
whales employ a cooperative foraging tactic known as “carousel feeding” to capture
these small schooling fi shes: this involves a group of whales encircling and herding
a school of herring into a tight ball close to the surface. Once the school is concen-
trated, individuals dive under the school and strike it with their tail fl ukes. Fish
stunned directly by the physical blow from the fl ukes or the associated loud cavita-
tion sound are then eaten individually (Similä and Ugarte 1993 ; Simon et al. 2005 ).
These herring-eating killer whales appear to live in matrilineally organized pods
similar in size to those of fi sh-feeding resident killer whales, but it is not known
whether they share the same extreme stability (Similä 1997 ). They are highly vocal
and have pod-specifi c call repertoires as observed in resident killer whales (Strager
1995 ), which would suggest a stable pod structure.
In the Strait of Gibraltar, a small population of killer whales appears to specialize
on predation of bluefi n tuna ( Thunnus thynnus ) as the fi shes enter and exit the
Mediterranean Sea during their breeding migration (Reeves and Notarbartolo di
Sciara 2006 ). To catch these swift tuna, the whales employ an endurance-exhaustion
technique involving protracted chases at swimming speeds of 12–14 km/h for peri-
ods of 30–40 min (Guinet et al. 2007 ). Killer whales can sustain suffi cient swim-
ming speeds necessary to catch small to medium (0.8–1.5 m) tuna using this
technique but appear unable to match the swimming ability of larger fi sh.
On the coast of Patagonia, Argentina, a small population of killer whales uses a
novel, but risky, hunting technique that involves intentional stranding in the shal-
lows to capture young southern sea lions ( Otaria fl avescens ) and southern elephant
seals ( Mirounga leonina ) at the water’s edge (Lopez and Lopez 1985 ). Whales hunt
cooperatively and share their prey with others in the group (Hoelzel 1991 ). A simi-
lar beaching tactic is used by killer whales in the sub-Antarctic Crozet Islands when
hunting southern elephant seal pups (Guinet 1992 ). As do mammal-hunting tran-
sients in the northeastern Pacifi c, whales in both these Southern Hemisphere
J.K.B. Ford and G.M. Ellis

91
locations have small group sizes, hunt mostly in silence, and appear to locate prey
by passive listening (Guinet 1992 ; J.K.B.F., unpublished data).
Three distinct forms of killer whales—known as types A, B, and C—have been
described in circumpolar waters of the Antarctic (Pitman and Ensor 2003 ). These
sympatric forms differ in pigmentation patterns, genetic structure (mtDNA
sequences), patterns of habitat use, and diet (Pitman and Ensor 2003 ; Krahn et al.
2008 ; LeDuc et al. 2008 ). Type A killer whales are found mostly in ice-free waters
where they apparently feed mainly on cetaceans, particularly Antarctic minke
whales ( Balaenoptera bonaerensis ). Type B whales forage primarily in loose pack
ice and appear to specialize on seals. These whales exhibit a novel hunting tactic in
which group members coordinate their swimming movements to create a large wave
that washes seals off ice fl oes (Visser et al. 2008 ). Type C whales inhabit dense pack
ice and appear to be fi sh feeders, having been observed preying on Antarctic tooth-
fi sh ( Dissostichus mawsoni ) (Pitman and Ensor 2003 ; Krahn et al. 2008 ). They are
substantially smaller than other Antarctic killer whales, with adults approximately
1–3 m shorter in length than type A individuals (Pitman et al. 2007 ). Type C whales
tend to have larger group sizes than mammal-hunting types A and B, which is con-
sistent with the pattern of group sizes versus prey type in the northeastern Pacifi c.
Unfortunately, too little is known about these Antarctic ecotypes to determine
whether ecological specialization has infl uenced their social structure, behavior,
and acoustics in ways similar to those of lineages in other regions.
4.10 Conclusions
The killer whale is a highly versatile social predator that has evolved to successfully
occupy a variety of specialized ecological niches in the world’s oceans. In so doing,
this species has assumed a variety of distinct lifestyles that have been shaped by
these ecological specializations. In the eastern North Pacifi c, the three killer whale
lineages have distinct patterns of seasonal distribution, group size, social organiza-
tion, foraging behavior, and acoustic activity, which can be related to their preferred
type of prey and the strategies the animals use to acquire it. Some similar patterns
are apparent among killer whales in other regions, although a lack of fi eld data pre-
vents a more complete assessment of the parallels between ecotype and life history
or behavior for these populations.
Although different killer whale lineages may be genetically distinct, there is no
evidence that dietary preferences result from any genetic predisposition. Globally,
there is no congruence between killer whale ecotype and genotype (Hoelzel et al.
2002 ; LeDuc et al. 2008 ). Instead, ecological specializations appear to represent
behavioral traditions that likely evolved independently in different regions. It is
plausible that ecological divergence could arise in sympatry with, for example, the
innovation of a novel foraging tactic in a particular matriline that allowed predation
on a new type of prey. If this matriline and its descendants became further special-
ized on this prey type, rates of association with other groups that do not adopt this
4 You Are What You Eat: Foraging Specializations and Their Infl uence…

92
new diet may diminish over time, leading to social segregation and reproductive
isolation. Such a process could lead ultimately to speciation. Resident and transient
killer whale lineages in the northeastern Pacifi c have been suggested to represent
incipient species (Baird et al. 1992 ) and Antarctic type A, B, and C killer whales to
represent distinct species (LeDuc et al. 2008 ).
There are still many questions concerning ecological specialization in killer
whales that remain to be answered. For example, to what extent might specializa-
tions constrain a lineage’s ability to switch to alternative prey species in a changing
environment? The preferences for fi sh and marine mammal prey exhibited by resi-
dent and transient killer whales, respectively, are extremely strong, and there is no
evidence that one ecotype ever switches to the prey type of the other or has the
behavioral fl exibility to do so. Marine mammals in coastal waters of the northeast-
ern Pacifi c can discriminate between lineages and will fl ee from transients but show
indifference to residents (Ford and Ellis 1999 ; Deecke et al. 2002 ), suggesting that
if residents ever hunt marine mammals, it must occur extremely rarely. The suite of
specialized behaviors that make resident killer whales adept at locating and catching
Chinook salmon likely would be ineffective for hunting marine mammals. Transients
would similarly be ill equipped to adopt a fi sh-feeding lifestyle.
The extent of dietary fl exibility of killer whales has implications for their poten-
tial role in driving marine ecosystem dynamics. It has been proposed that a shift to
sea otter predation by mammal-hunting killer whales in the Aleutian Islands resulted
in a precipitous decline in sea otter abundance that started in the mid-1980s (Estes
et al. 1998 ). This shift is thought to be a response to reduced availability of the
whale’s presumed primary prey in the region, harbour seals and Steller sea lions.
In an extension of this hypothesis, Springer et al. ( 2003 ) postulated that the decline
of sea otters was the last in a series of population collapses of prey species of
mammal- hunting killer whales in the northern Gulf of Alaska that was triggered by
the decimation of the great whales by industrial whaling in the nineteenth and twen-
tieth centuries. This hypothesis has been challenged on various grounds (Trites et al.
2007 ; Wade et al. 2007 ), particularly because there is no evidence that the great
whales (especially adults) have ever played an important role in the diet of killer
whales (Mizroch and Rice 2006 ; Ford and Reeves 2008). Although it may be
possible that predation by killer whales could result in depletion of targeted prey
species, dietary specializations could have signifi cant constraints on the directions
that subsequent prey shifts may take.
To date, most ecologically specialized killer whale populations, including sym-
patric fi sh-eating and mammal-eating ecotypes, have been described in highly pro-
ductive cold temperate or polar waters, likely the result of the diversity of abundant
prey types available in these high latitudes, which has provided the opportunity for
niche partitioning. It may well be that killer whales in less productive tropical or
subtropical waters are generalist predators that include a greater variety of prey in
their diets (Baird et al. 2005b ). For example, a high incidence of killer whale teeth
scars on humpback whales using breeding grounds off the west coast of Mexico
suggests that predation in this area, especially on calves, may be extensive (Steiger
et al.
2008 ). This prey resource is seasonal, however, as humpbacks only occupy
J.K.B. Ford and G.M. Ellis

93
these breeding grounds for 3 to 5 months in winter. Because there is no evidence
that killer whales follow migrating humpback whale mothers and calves to their
high-latitude feeding grounds, it is likely that the predators shift to alternative prey
species for the remainder of the year.
Globally, killer whales form a mosaic of distinct populations, some overlapping
and others geographically discrete, that are ecologically specialized to greater or
lesser degrees. Each population is likely to have foraging tactics, activity patterns,
social organization, and acoustic behavior that have been shaped by its dietary spe-
cialty. Highly specialized populations can be expected to have lifestyles that are
closely adapted to their foraging strategy, whereas more generalist populations may
be relatively less constrained by any particular prey type. In certain regions, such as
the northeastern Pacifi c, some parts of this mosaic are becoming fairly clear. In
other regions, such as the Antarctic, a fascinating picture is emerging but signifi cant
knowledge gaps remain to be fi lled. In regions where killer whales are little studied,
such as in sparsely inhabited tropical waters, there is much yet to be discovered.
Only when all the components of this global mosaic of killer whale populations
have been described will we have a complete appreciation of the range of ecological
specializations and lifestyles of this multifaceted and resourceful predator.
Acknowledgments We thank R. Baird, C. Chapman, V. Iriarte, C. Matkin, and J. Watson for
helpful comments on earlier drafts of this chapter, and M. Malleson and J. Towers for kindly
allowing us to use their photographs.
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