Infanticide in a mammal-eating killer whale population

Abstract

Infanticide can be an extreme result of sexual conflict that drives selection in species in which it occurs. It is a rarely observed behaviour but some evidence for its occurrence in cetaceans exists in three species of dolphin. Here we describe observations of an adult male killer whale (Orcinus orca) and his postreproductive mother killing a neonate belonging to an unrelated female from the same population in the North Pacific. This is the first account of infanticide reported in killer whales and the only case committed jointly by an adult male and his mother outside of humans. Consistent with findings in other social mammals, we suggest that infanticide is a sexually selected behaviour in killer whales that could provide subsequent mating opportunities for the infanticidal male and thereby provide inclusive fitness benefits for his mother.

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Scientific RepoRTS | (2018) 8:4366 | DOI:10.1038/s41598-018-22714-x
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Infanticide in a mammal-eating
killer whale population
Jared R. Towers1,2, Muriel J. Hallé2, Helena K. Symonds3, Gary J. Sutton2,
Alexandra B. Morton4, Paul Spong3, James P. Borrowman5 & John K. B. Ford1
Infanticide can be an extreme result of sexual conict that drives selection in species in which it occurs.
It is a rarely observed behaviour but some evidence for its occurrence in cetaceans exists in three species
of dolphin. Here we describe observations of an adult male killer whale (Orcinus orca) and his post-
reproductive mother killing a neonate belonging to an unrelated female from the same population
in the North Pacic. This is the rst account of infanticide reported in killer whales and the only case
committed jointly by an adult male and his mother outside of humans. Consistent with ndings in other
social mammals, we suggest that infanticide is a sexually selected behaviour in killer whales that could
provide subsequent mating opportunities for the infanticidal male and thereby provide inclusive tness
benets for his mother.
Conspecic infanticide occurs within many taxa. Among terrestrial mammals, it is mostly reported in primates,
carnivores and rodents1. However, compelling evidence for infanticide in cetaceans exists in three species of
dolphin. Patterson et al.2 and Dunn et al.3 found that dead neonate and juvenile common bottlenose dolphins
(Tursiops truncatus) in the eastern and western North Atlantic respectively had scarring that suggested they were
killed by conspecics. More recently, Kaplan et al.4, Robinson5, Perrtree et al.6 and Díaz López et al.7 witnessed
adult common bottlenose dolphins attack young in the North Atlantic. Furthermore, Zheng et al.8 documented
adult Indo-Pacic humpback dolphins (Sousa chinensis) killing neonates in the western North Pacic and in the
South Atlantic, an attack on a neonate Guiana dolphin (Sotalia guianensis) conducted by adults likely resulted in
its death9.
In many cases, it is dicult to put the causes and eects of infanticidal acts into context because the natural
occurrence of this behaviour is so rarely observed10,11. However, infanticide occurs in a myriad of dierent situ-
ations and several hypotheses have been proposed to explain it11–13. Salient among these is the sexual selection
hypothesis which states that infanticide can benet the tness of males that commit it because loss of a dependent
ospring ends lactational amenorrhea and can quickly return the mother to a fertile condition. In these cases,
infanticide not only creates a mating opportunity but can also remove the progeny of a competing male from the
gene pool12. e predation hypothesis suggests that infanticide precedes cannibalism and is more likely to take
place in energy-stressed populations13,14. However, cannibalism does appear to be a secondary benet of some
infanticide events best explained by the sexual selection hypothesis15,16. e resource competition hypothesis
predicts that the removal of an infant may provide greater access to prey, mates or habitat for the perpetrator
or its descendants12,13. Lastly, non-adaptive explanations for infanticide purport that it is a socially pathological
behaviour that may be conducted accidentally or as a result of environmental stressors17,18.
e risk and occurrence of infanticide is likely to have inuenced social structures and mating systems in
some species11,19. Although much research has been conducted on the social societies of cetaceans20, very little
is known of the reproductive behaviour of most odontocetes21. However, male Indo-Pacic bottlenose dolphins
(Tursiops aduncus) have been documented sexually coercing females by chasing, ramming and biting them22.
ese aggressive behaviours and incidents of newly acquired scars on females caused by the teeth of conspecics
are positively correlated with the timing of their reproductive cycles23,24. Additionally, while scars on several other
odontocete species are thought to occur in mating competitions between males25,26, these intraspecic agonistic
interactions are rarely observed. For example, although killer whales (Orcinus orca) are one of the most stud-
ied and widespread species of cetacean, only a few observations of aggression between individuals of the same
1Pacic Biological Station, Fisheries and Oceans Canada, 3190 Hammond Bay Road, Nanaimo, BC, V9T 6N7, Canada.
2Bay Cetology, Box 554, Alert Bay, BC, V0N 1A0, Canada. 3OrcaLab, Pacic Orca Society, Box 510, Alert Bay, BC, V0N
1A0, Canada. 4Raincoast Research Society, Box 399, Sointula, BC, V0N 3E0, Canada. 5Whale Interpretive Centre, Box
2–3, Telegraph Cove, BC, V0N 3J0, Canada. Correspondence and requests for materials should be addressed to J.R.T.
(email: jrtowers@gmail.com)
Received: 8 December 2017
Accepted: 27 February 2018
Published: xx xx xxxx
OPEN
There are amendments to this paper
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population have been reported (see27). Nevertheless, individuals of all sex and age classes from many killer whale
populations around the world have scars on their bodies from the teeth of conspecics28–33. ese scars may orig-
inate from rough interactions between or within sex and age classes but, causes of their occurrence likely vary in
nature and among populations.
In the North Pacic Ocean several populations of both sh-eating and mammal-eating killer whale exist34.
Among those that prey on marine mammals (Bigg’s killer whales) are a number of genetically distinct populations
in the Gulf of Alaska35 as well as the West Coast Transient (WCT) population which is primarily found in coastal
waters and along the continental shelf edge from central California to southeastern Alaska36. is population is
currently considered reatened in Canada37 but has been growing at an average rate of about 3% per year since
1975 and now consists of several hundred individuals38,39. Social units in this population usually contain two
to six individuals and are typically composed of a reproductive female and her ospring. Both male and female
ospring are known to permanently or temporarily disperse as they mature but post-reproductive females oen
travel with their adult sons continuously40.
Field studies on WCT killer whales conducted by researchers aliated with the Pacic Biological Station in
British Columbia, Canada began in 197341. Aer more than 5300 photographically documented encounters with
WCT killer whales, an encounter on 2 December 2016 provided the rst direct observations of lethally agonistic
behaviour between individuals in this population as an adult male and his mother killed a neonate belonging
to a female that was not maternally related. e events leading up to and following the infanticide incident are
presented chronologically below and the occurrence of this phenomenon within WCT killer whale society is
discussed in context of the various hypotheses for this behaviour.
Results
At 09:59 WCT killer whale vocalizations were detected on a remote hydrophone station located near Robson
Bight in Johnstone Strait. By 10:10 vocalizations were also heard on two other hydrophone stations about ten km
to the west, indicating a westward movement of the whales (Fig.1). Between 10:06 and when the last vocalization
was recorded at 11:01, two or more individuals repeated several discrete and aberrant pulsed calls (Supplementary
Recording S1; Supplementary TableS1). At 10:55 a research boat was dispatched from Alert Bay to intercept the
Figure 1. Map of study area (created with ArcGIS v10.5 - https://www.esri.com/en-us/home). e locations
and acoustic range of hydrophone stations, place names, and positions of the encounter beginning, end and the
infanticide event are provided.
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whales and they were spotted heading west in western Johnstone Strait at 11:07. Adult female T068 (age ≥ 46 yr,
thus post-reproductive) and her adult son T068A (age 32) were travelling together about 200 m behind a young
mother T046B1 (age 13), her ospring T046B1A (age < 2 yr) and her sister T046B4 (age < 3 y r) (Fig.2). e three
T046B individuals were traveling rapidly between 11 and 17 km/h. T046B4 had fresh wounds from the teeth of
another whale on both anks and a noticeable kink on the dorsal surface of the ridge posterior to the dorsal n
that was associated with broken skin (Fig.3A). e wounds on the le ank were still bleeding (Fig.3A). e
T068s were keeping a steady pace behind and o to the side of the T046Bs. At 11:29, the mother of T046B1 and
T046B4, T046B (age 28 yr), was found west of Alert Bay about a kilometer ahead of the other whales with her
other daughters T046B2 (age 8 yr) and T046B3 (age 5 yr) and a neonate of unknown sex with visible fetal folds
and a dorsal n that was not yet entirely erect (T046B5) (Figs2 and 3B). ey remained ahead of the rest of the
T046Bs until 11:55 when they all came together near Haddington Island. e T068s remained roughly 200 m
behind. All whales were making a steady pace to the west.
Nearing Ledge Point at 12:18, a portable hydrophone was deployed ahead of the whales, but no vocalizations
were heard. A few minutes later, aer the whales had passed about 500 m to the west, erratic movements and
splashing suggestive of a predation event were observed. Upon arriving on scene at 12:27, T068A was approx-
imately 150 m from the other whales and moving away from them. e other whales followed. ey all came
Figure 2. Genealogicalschematic of present individuals. e identities and where known, sex and birth year of
all whales present and their maternal relations to each other (see original schematics in Towers et al.30) displayed
in colour coded statuses. Purple: post-reproductive female, Blue: reproductive male, Fuscia: reproductive
females, Pink: juvenile females, Yellow: juvenile of unknown gender, Gray: neonate of unknown gender.
Figure 3. Observations leading to infanticide. (A) Fresh wounds on le ank and kinked spine anterior to
dorsal n on T046B4. (B) T046B with ospring T046B2 and (neonate) T046B5. (C) T068A surrounded by
T046B, T046B1 and T046B1A. (D) T046B ramming T068A from below sending spray and blood into the air.
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together aer 1–2 minutes and began circling vigorously (Fig.3C). It was realized that the neonate T046B5 was
not surfacing next to its mother T046B or in the vicinity and then T068A swam close past the research boat
and the uke of the neonate could be seen in his mouth with the body intact trailing underneath his lower
jaw. Movements of all whales were erratic but the neonate’s mother T046B appeared to be chasing the male
T068A while his mother, T068 attempted to manoeuvre between them (Supplementary MovieS1). Intense vocal
activity could be heard through the hull of the boat so the hydrophone was deployed. A wide variety of excited
discrete and aberrant pulsed calls (Supplementary TableS1), whistles, and percussive sounds were recorded
(Supplementary Recording S2). Underwater video obtained during this time shows T068A with an object par-
tially white in colour in his mouth, closely anked by T068 (Supplementary MovieS2). At 12:35, T046B rammed
T068A near the surface with sucient force to cause a noticeable undulation through his body, sending blood
and water into the air (Fig.3D).
At 12:43 the activity began to subside. Fresh teeth wounds that were not present before the incident were
visible on T068A’s le and right anks (Fig.4A), rostrum, and base of dorsal n and on T068’s melon. T068A
and T068 began to withdraw from the others and slowly travel west. T068A still had the neonate by the uke in
his mouth (Fig.4A). At 13:07, his mother T068 was lmed and photographed packing the neonate by the uke
(Supplementary MovieS3; Fig.4B). e T046Bs remained 200–300 m behind and o to the side of the T068s, sur-
facing together and travelling slowly. At 13:42 all whales were o Pulteney Point and the dorsal n of the neonate
was seen above the surface on T068’s right side as she surfaced, indicating she was holding its le pectoral ipper
in her mouth. At one point she pushed the neonate along in front of her and its head was visible above the surface
before sinking back down into the water. A few minutes later the T046Bs slowly approached them from behind.
T046B came out ahead of the others within about 50 m of the T068s but then reversed direction and re-joined
her group. Aer this the T046Bs remained grouped up within a kilometre of the T068s for the duration of the
encounter. At 14:20, underwater footage of the T068s showed neither of them to be holding T046B5, but just prior
to this they had begun to circle at the surface aer making long dives indicating that the neonate may have been
below them. At 14:50 it was visually conrmed that the T046Bs were not in possession of the neonate. Aer not
seeing T046B5 since before 14:00, T068A surfaced at 16:00 with its dorsal n visible o the le side of his head
(Fig.4C), indicating he held its right pectoral ipper in his mouth. He was photographed surfacing rostrum to
rostrum with the dead neonate a few minutes later (Fig.4D). Its body appeared to be intact. Aer unsuccessfully
attempting to acquire a biopsy sample of T068A, observations ended at 16:15 due to failing daylight. No evidence
of feeding behaviour such as oil slicks or birds becoming interested in the whales were observed at any point.
Figure 4. Observations following infanticide. (A) T068A with the uke of T046B5 in the le side of his mouth.
Fresh scars from the teeth of another whale can be seen on his le ank and rostrum. (B) T068 surfacing with
the uke of T046B5 visible in the le side of her mouth. (C) T068A surfacing with the dorsal n of T046B5
visible o the le side of his melon. (D) T068 rostrum to rostrum with T046B5 approximately 215 minutes aer
its death.
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Discussion
WCT killer whales may be well adapted behaviourally for performing infanticide because of their experience kill-
ing other small cetaceans. Individuals typically dispatch these prey by ramming or crushing them with their ros-
trums or tails36. Observations of infanticidal behaviour towards young common bottlenose dolphins, Indo-Pacic
humpback dolphins and a Guiana dolphin by conspecics have included repeated ramming and crushing actions
but also forced submergence4–9. Although we did not observe the rst few minutes of this incident closely enough
to determine the details of interactions that took place, it appeared as though T046B5 was quickly immobilized by
having its tail gripped in the teeth of T068A and subsequently drowned because there was no opportunity to sur-
face and breath due to his consistent forward motion. Although both T068 and T068A were observed with fresh
teeth scars aer the incident, the only ramming behaviour we observed was performed by T046B toward her neo-
nate’s killer. is combative behaviour is similar to actions directed towards infanticidal males by the mothers of
targeted infants in several rodent, primate and carnivore species (see review in13). e ramming occurred approx-
imately ten minutes aer the incident began, at which point the neonate would have been either close to or freshly
drowned, which is probably why the ght did not persist. e brevity of this physical aggression might be typical
of agonistic interactions between members of the WCT killer whale population. is, in addition to the fact that
most exchanges between individuals take place below the surface, may help explain why none of this nature have
previously been observed. Similarly, anomalistic calls are not commonly made by whales in this population42, but
as many animals are known to produce atypical sounds under stressful situations43, the high number of aberrant
and discrete pulsed calls and other excited sounds recorded before and during the infanticide event likely reect
the levels of intensity in the complex interactions taking place between individuals. For example, the fresh trauma
observed on T046B4 at the beginning of this encounter indicates that other rough interaction between the whales
occurred prior to our arrival. is may have caused the T046Bs to separate into two groups to benet the neonate
and the other young animals through their disassociation from it, but vocalizations between them and their ulti-
mate re-grouping may have revealed their locations to the T068s.
e motivation for T068A and T068 to make this attack is of particular interest, but that they carried it
out cooperatively is not surprising because bonds between maternally related killer whales can be particularly
strong34. In sympatric populations, post-reproductive female killer whales increase the survival of adult sons
by sharing ecological knowledge and prey with them44,45. is benets inclusive tness of the female because a
positive relationship exists between reproductive success and age in male killer whales45,46. is combined with
a prediction by Connor et al.47 that post-reproductive female killer whales may play a role in acquiring mates for
their adult male ospring suggests that T068’s active involvement in this event was sexually selected, especially
considering that T068A is of a reproductively mature age30,46. e sexual selection hypothesis requires that the
infanticidal male does not kill his own ospring, that the event provides a near future mating opportunity with
the infants’ mother and that he sires ospring with her12. Although it has been conrmed in many other mammal
species that infanticidal males are not the fathers of their victims48–55 and that they subsequently sire ospring
with the infants mothers13,15,51,53,55–57, in this incident the neonate’s carcass could not be recovered, T068A was not
biopsied for DNA analysis and T046B has not yet had another calf.
However, further evidence also suggests that the infanticidal teamwork of T068 and T068A was motivated by
potential to increase their inclusive tness. For example, young ospring are oen selected for infanticide because
new mothers return to estrus much quicker than those that have been lactating for longer periods of time12. In
this case, we know that T046B5 was less than a few days old and that suckling stimulates lactation in female killer
whales whose postpartum return to estrus is much longer (5–32 months) when lactating than when not (1–4
months)58. Secondly, females in some animal societies copulate more with coercive males59,60 that restrict parental
investment and improve the female condition by committing infanticide to increase their tness61. In this case,
although it is not clear if the attack on T046B4 was attempted juvenilicide, this whale (although third youngest
in the group) was T046Bs second youngest ospring, so its death along with loss of her neonate could have ben-
etted her condition by reducing any prohibitive physical costs associated with caring for either of them. is
would help restrict parental investment towards any forthcoming ospring of T068A if he successfully mated with
T046B. Furthermore, infanticidal males are typically not familiar with the infant’s mothers13 and although unre-
lated matrilineal groups of WCT killer whales have oen been known to spend several weeks together40 in what
have generally been perceived to be mutual associations, T068A, T068 and T046B had only been documented
together on two previous occasions – once in 2005 and again in 2007. e apparent low levels of association
between these individuals suggest that they are not well known to each other and this may be reective of inherent
sexual conict between their diering sex and age classes.
Sexually selected infanticide in WCT killer whales has important implications for our understanding of the
social behaviour and evolution of this species (Supplementary Discussion S1) and although in this case, the
hypothesis cannot be proven, there is more supporting evidence for it than other hypotheses for this behav-
iour. For example, WCT killer whales are well known for their dramatic hunting behaviour and protracted kills
that typically result in immediate vocal and social activity, including division and consumption of mammalian
prey36,62. However, in this incident the vocal and social activity subsided once the kill was made and although the
dead neonate was kept in the possession of its killers for at least 220 minutes, there was no indication that it was
dismembered or consumed. Additionally, most prey species that WCT killer whales target have been steadily
increasing in coastal waters over the last few decades63–69. ese increases in prey availability have been commen-
surate with increasing social activity70 and higher recruitment within the WCT population39 suggesting that it is
not nutritionally stressed. us, this incident is not easily explained by the predation hypothesis. Furthermore,
although the WCT population has more than doubled in size since 199039, there is little evidence available to
suggest that individuals within it compete for habitat or prey71. Regardless, these and the availability of other
resources such as mates would not easily be threatened by an infant of either sex due to the slow rate of matu-
ration in this species. us, this incident is not easily explained by the resource competition hypothesis. Finally,
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there is little support for interpreting infanticide as a non-adaptive behaviour other than when it occurs by acci-
dent or under unnatural conditions13,53,72 and contrary to accidental or pathological explanations, the infanticidal
behaviour of T068A and T068 appeared goal oriented because their chase led to an attack that was maintained
until a particular outcome had been achieved. Once it had, their behaviour immediately changed.
In conclusion, given that infanticide is so rarely observed in terrestrial mammals it is not surprising that it has
taken many years of directed eld observations to conrm that it does occur in cetaceans and more specically, in
killer whales. is species shares many life history traits with other mammals that are known to commit infanti-
cide (see1), such as a high lactation to gestation ratio58, a society where individuals live in stable mixed sex groups
where calves are born year round71 and a breeding system that is monopolized by a minority of mature males46.
As a result, this phenomenon might be expected to occur in more killer whale populations than just the WCT. In
any case, additional study is required to investigate any impacts that this phenomenon may have on the evolution
of the social structure of this population and the behaviour of individuals within it.
Methods
Underwater acoustic data were transmitted live from three xed hydrophone stations maintained by OrcaLab in
or adjacent to Johnstone Strait to monitors in Alert Bay, Telegraph Cove and on Malcolm Island. Vocalizations
were digitally recorded and classied through visual and aural comparison using Audacity spectrograms and call
type catalogues for this population provided in Ford73 and Deecke62. Calls were considered aberrant if they were
similar but not identical to stereotyped calls. Vocalizations that were impossible to identify due to signal strength
and/or interference were classied as unidentied. Digital audio, video and images were obtained in the eld
while observations were taking place from a 5 metre motor vessel. e individual killer whales and their geneal-
ogies were identied using Towers et al.30. Data on age, sex, associations and observations from other encounters
were obtained from the database on this population maintained for the Pacic Biological Station (Fisheries and
Oceans Canada).
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Acknowledgements
We thank Shari Willmott, Eva Stredulinsky, Natalie Barefoot and the late Twyla Roscovich for helping prepare
materials, David Cannamore for helping to record acoustic data and take notes during this encounter, Volker
Deecke for assistance with call classication, and James Pilkington for reviewing a dra of the manuscript. is
research and preparation of this paper has been funded in part through the Fisheries and Oceans Canada Species-
at-Risk Program and the Annenberg Foundation.
Author Contributions
Observational data on the infanticide event featured in this article were collected by J.R.T., M.J.H. and G.J.S.
under Canadian marine mammal research license MML-01. Acoustic data were collected by H.K.S., A.B.M., P.S.,
J.P.B. and J.R.T. e acoustic data were analyzed by H.K.S. Funding was directed to this project by J.K.B.F. and
J.R.T. e article was draed by J.R.T. with input from all authors.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-018-22714-x.
Competing Interests: e authors declare no competing interests.
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