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MARINE MAMMAL SCIENCE, 33(3): 934–945 (July 2017)
©2017 Society for Marine Mammalogy
DOI: 10.1111/mms.12405
Complex prey handling of octopus by bottlenose dolphins
(Tursiops aduncus)
KATE R. SPROGIS,
1
Murdoch University Cetacean Research Unit, School of Veterinary and
Life Sciences, Murdoch University, Perth, Western Australia 6150, Australia; HOLLY C.
RAUDINO,
2
Murdoch University Cetacean Research Unit, School of Veterinary and Life
Sciences, Murdoch University, Perth, Western Australia 6150, Australia and Marine Science
Program, Department of Parks and Wildlife, Perth, Western Australia 6151, Australia;
DAVID HOCKING,School of Biological Sciences, Monash University, Melbourne, Victoria
3800, Australia; LARS BEJDER,Murdoch University Cetacean Research Unit, School of
Veterinary and Life Sciences, Murdoch University, Perth, Western Australia 6150, Australia.
Marine predators use prey handling behaviors that are best suited to the proper-
ties (e.g., size, shape, and texture) of the prey species being targeted (Hocking
et al. 2016, 2017). Predators that target large prey species that cannot be swal-
lowed whole are required to process prey extensively before consumption (either
breaking it into smaller pieces or softening it). For example, crocodiles and alliga-
tors perform a spinning “death roll” to dismember large prey items (Fish et al.
2007). Leopard seals (Hydrurga leptonyx) thrash sea birds and seal pups to break
them into edible pieces (Edwards et al. 2010). Australian fur seals (Arctocephalus
pusillus doriferus) shake and toss large fish and cephalopods before consumption
(Hocking et al. 2016). Similarly, for toothed whales, if prey items are too large to
swallow whole they also need to spend time processing prey. For example, killer
whales (Orcinus orca) shake sea lions and beluga whales (Delphinapterus leucas)
(Lopez and Lopez 1985, Frost et al. 1992), and toss dusky dolphins (Lagenor-
hynchus obscurus) and stingrays into the air (Constantine et al. 1998, Visser 1999).
Bottlenose dolphins (Tursiops spp.) shake and toss fish to break them into smaller
pieces and to soften them for ease of consumption (W€ursig and W€ursig 1979,
Shane 1990). Bottlenose dolphins also use complex prey handling to break giant
cuttlefish (Sepia apama) into manageable pieces, using a sequence of steps to
remove the head, ink, and cuttlebone before the flesh of the mantle is consumed
1
Corresponding author (e-mail: k.sprogis@murdoch.edu.au).
2
nee Smith.
934
(Finn et al. 2009, Smith and Sprogis 2016). Prey handling behaviors vary among
species and locations and are influenced by the availability of prey species.
Within a population, foraging for specific prey may be linked with ecological vari-
ables, age- and/or sex, and/or be socially learned from conspecifics (Weiss 2006, Sar-
geant et al. 2007, Torres and Read 2009, Patterson et al. 2016). For example, in
Shark Bay, Western Australia, “sponging” is a solitary foraging specialization where
predominantly adult female bottlenose dolphins (T. aduncus)useamarinespongeon
their rostrum as a protective tool to probe the seafloor to feed on burrowing fish (Pat-
terson and Mann 2011). Sponging is linked to specific environments, being mainly
employed in deep-water channels (>10 m) where conical marine sponges occur (Sar-
geant et al. 2007, Tyne et al. 2012). This foraging tactic is also vertically transmitted
from mother to female offspring (Kr€utzen et al. 2005), and requires an extensive
period of exposure to promote calf learning (Mann et al. 2008). Similarly to foraging
tactics, prey handling behaviors may also be linked to ecological variables, be
age/sex-specific, or socially learned from conspecifics.
In this study, we describe the complex prey handling behavior of benthic octopus
by T. aduncus in southwestern Australia. We investigate whether this behavior is (1)
associated with specific ecological variables, (2) is age- or sex-specific, and (3) is a
socially learned behavior.
The study region encompassed a 540 km
2
area in the temperate waters off Bunbury
(33°320S, 115°630E), Western Australia. Water depth ranged from <1 m in estuarine
waters and up to 24 m in open coastal waters. Data were collected year-round from
March 2007 to August 2013, and field methods were the same as for Sprogis et al.
(2016b). Boat-based, photographic-identification surveys of dolphins were conducted
along systematic line transects. Once dolphins were sighted, a dolphin group encoun-
ter began and photographs were taken of dolphin dorsal fins for identification pur-
poses (W€ursig and W€ursig 1977). The Global Positioning System (GPS) location,
depth, water temperature, turbidity (secchi depth), and dolphin group size were
recorded. During the first five minutes, the predominant group behavioral state (the
behavioral state that >50% of the group was engaged in) was recorded (i.e., foraging,
feeding, resting, socializing, travelling). During encounters, photographs of dolphins
handling octopus at the surface were taken and details were recorded (time, number
of tosses, and dolphin identification). Data were available on individual dolphins (in-
cluding sex and age class) from a long-term research program focused on the Bunbury
dolphin population (Smith et al. 2013, 2016; Sprogis et al. 2016a,b).
To explore if there was a relationship between octopus handling events and habitat
type, a benthic habitat map was created following Sprogis (2015). High-resolution
satellite imagery was validated via 185 validation points following the drop-down
camera methods described in Tyne et al. (2010). Each validation point was rated post
hoc for the percentage of habitat cover following Kohler and Gill (2006). To discrimi-
nate between benthic habitat types, a k-means unsupervised classification was con-
ducted and habitats were clustered into eight classes; reef, sand, seagrass, deep waters,
algae/reef, algae/sand, mud/sand, and mud/silt.
We explored whether octopus handling might be a socially transmitted behavior
by quantifying association histories of individual dolphins observed engaging in these
events over a 7 yr period. To test for preferred/avoided associations, association
indices between individuals were calculated to estimate the proportion of time they
were sighted together (Whitehead 2008). Pairs of individuals were assumed to be
associated if they were sighted in the same group. A group wasdefinedasoneormore
dolphins within 100 m of other individuals and behaving similarly (Irvine et al.
NOTES 935
1981, Wells et al. 1987). The simple ratio index (SRI, Ginsberg and Young 1992)
was used as we expected each individual to have an equal chance of being identified.
Association index values range from zero (never sighted together) to one (always
sighted together), and were calculated between (1) dolphins that were observed han-
dling octopus and (2) dolphins observed handling octopus with dolphins that were
not observed with octopus.
We tested for preferred/avoided associations using permutation analyses, where
the data were randomized multiple times (two-sided significance level =0.05,
Bejder et al. 1998, Whitehead et al. 2005). Analyses were run using SOCPROG
2.7 (Whitehead 2009) and only included dolphins that were sighted ≥5occasions.
The sampling period was set to five days, which was based on the mean number
of days needed to complete all transects in the main study area to optimize equal
probability of encountering individual dolphins (Sprogis et al. 2016a). To test
whether the observed data differed significantly from random, we determined the
number of permutations required to obtain an accurate P-value by increasing the
number of permutations (maximum 20,000) until the P-value stabilized (Bejder
et al. 1998), with 1,000–5,000 trials per permutation. To examine the strength of
associations between individual dolphins we compared the SRI values against the
randomly generated values. For long-term associations (between sampling periods)
the null hypothesis was rejected if the standard deviation (SD) and coefficient of
variation (CV) of the observed SRI value was significantly higher (P<0.05) than
the SD and CV of the randomly permuted data (Whitehead et al. 2005, White-
head 2008).
Our study resulted in 587 surveys completed with homogenous sampling effort
across seasons (Table S1), with 177 surveys conducted within bay and estuarine
waters and 410 surveys in open coastal waters (Table S2). A total of 1,567 dolphin
groups were sighted and photographed (Table S1). We observed 45 octopus handling
events, with 33 of these observed while on survey effort. Handling events occurred
during separate group encounters, apart from one group encounter where three differ-
ent individuals in the same group were observed handling octopus.
Dolphins were observed handling octopus using two different methods (Fig. 1,
Movie S1, Fig. S1). The first method (shake) involved dolphins arching and rotating
their body out of the water, while holding the octopus in the jaws and forcefully hit-
ting it onto the surface of the water (Fig. 1d, Movie S1). The second method (toss)
involved the dolphins also raising their head and/or body out of the water and flick-
ing the octopus out of the water, but instead of keeping their jaws closed, they
opened their mouths so that the octopus was released and tossed into the air, often
travelling over several meters (Fig. 1, Movie S1). The dolphin would subsequently
retrieve the octopus and continue to shake and toss it at the surface (commonly 10–
15 times). In some cases, a “shake” became a “toss” if the prey item tore and frag-
mented during the shake, and hence was then thrown across the water rather than
being hit onto the water’s surface.
The observed octopus handling events lasted from <1 min to >6min.Insome
instances, octopus handling had already commenced when dolphins were sighted, so
these are considered minimum durations for dolphins to process octopus. No observa-
tions were made underwater; therefore, it was not possible to determine whether any
processing occurred below the surface. Generally, the head and the mantle of the
octopus was removed prior to our observations, making it difficult to identify octopus
to the species level. We were not able to retrieve any octopus parts during sightings
for species verification.
936 MARINE MAMMAL SCIENCE, VOL. 33, NO. 3, 2017
Octopus handling events occurred throughout all seasons (Poisson generalized lin-
ear model, P=0.05), with the majority of sightings in winter and spring (Fig. 2).
Events took place in water temperatures ranging from 14.4°C to 23.3°C(x=18.4°C
0.47 SE, Fig. 2). Sightings were in water depths between 0.8 m and 14.7 m
(x=9.09 m 0.66 SE) and in waters with a turbidity ranging from 0.8 to 10 m
(x=3.30 m 0.38 SE). Events took place predominantly over sand, algae/sand, and
mud/silt habitats (33.3%, 21.2%, 21.2%, respectively; Fig. 3).
Of the 33 octopus handling events observed while on survey, six dolphins were
unable to be identified and 26 were known from our photo-identification catalogue
(with one individual observed handling octopus on two occasions). Of these known
Figure 1. A sequence of an octopus handling event by an adult male bottlenose dolphin off
Bunbury, Western Australia. This event lasted for approximately 5 min, with 12 octopus
shakes and/or tosses observed. Each row (a–f) represents consecutive actions, displaying exam-
ples of the different types of handling methods: shaking (d) and tossing (a, b, c, e, f).
NOTES 937
dolphins, 20 were adults, 4 were juveniles, and 2 were calves. Sex was determined for
14 females and 4 males, while 8 animals were of unknown sex. The mean group size
of all encountered dolphin groups was 5.98 (0.14 SD, range 1–45 dolphins,
Table S1). For foraging and feeding groups, mean group size was 4.38 (4.41 SD) and
4.82 (7.09 SD), respectively (Table S3). For octopus handling events, the mean group
size was 9.55 (9.55 SD, range =1–36 dolphins). Octopus handling was observed in
conjunction with all group behavioral activities, with traveling and feeding groups
the most likely groups to observe a dolphin handling octopus (30.3% and 27.3% of
the events, respectively).
Of the 26 dolphins identified handling octopus, 25 were sighted on five or more
occasions and were used in the permutation analyses. Over the long-term (between
sampling periods), there was indication of long-term preferred associations between
dolphins that handled octopus, as both the observed SD and CV of the SRI were
significantly higher than the randomized SD (observed =0.052, randomized =
0.048, P=<0.0001) and CV (observed =1.605, randomized =1.500, P=0.0001),
with 8 pairs among 25 dolphins (dyadic P>0.97).
Associations were tested between the 25 dolphins handling octopus and the
remaining 280 dolphins in the population that met the threshold of five or more
occasions. For long-term associations, both the observed SD and CV of the SRI were
significantly higher than the randomized SD (observed =0.049, randomized =
0.042, P=0.0001) and CV (observed =2.404, randomized =2.110, P=<0.0001),
indicating the occurrence of preferred (189 pairs, dyadic P>0.975) and avoided asso-
ciations (50 pairs, dyadic P<0.025).
The behavior of octopus handling (shaking and tossing) is previously undescribed.
We suggest that T. aduncus shake octopus forcefully onto the water’s surface and toss
octopus several meters into the air multiple times to (1) remove the octopus head and
mantle, (2) tenderize and ensure the arms are inactive, and (3) break the octopus into
smaller pieces for easier consumption. We documented that octopus handling behav-
ior (1) was a seasonal occurrence, peaking during winter and spring in water
Figure 2. The cumulative number of octopus handling events (gray bars, n=33) and the
mean sea surface temperature (black dots) during each austral season between Autumn 2007
and Spring 2013. Continuity between dots is not implied.
938 MARINE MAMMAL SCIENCE, VOL. 33, NO. 3, 2017
temperatures around 18°C, (2) was most prevalent among adult females, and (3) was
conducted by dolphins that showed a close association with other dolphins that han-
dled octopus.
Figure 3. Locations of octopus handling events (black circles, n=33) by Indo-Pacific bot-
tlenose dolphins off Bunbury, Western Australia, over benthic habitat consisting of sand,
algae/sand, and mud/silt, and seagrass.
NOTES 939
Octopus can be difficult for dolphins to handle (see dos Santos and Lacerda 1987,
Orbach and Kirchner 2014), and in our study area dolphins were required to arch
their head and/or body out of the water in order to shake or toss octopus clear of the
water. As a result, this handling method involves a large body movement that is
likely energetically expensive. Although more energetically demanding, this complex
prey handling behavior allows dolphins to process large prey type that may be risky
to consume without processing (dos Santos and Lacerda 1987).
It is apparent that octopus handling is a risky behavior, as within our study area a
known adult male stranded and a necropsy confirmed the cause of death was from
suffocation from a large 2.1 kg octopus.
3
The dolphin had attempted to swallow the
octopus, however, the octopus was found almost intact, with the head and the mantle
of the octopus in the dolphin’s stomach and the 1.3 m long arms separated from the
head and extending out of its mouth.
3
Similarly, another T. aduncus died from sus-
pected asphyxiation due to an octopus lodged in its mouth and pharynx approxi-
mately 140 km north of our study area (Shoalwater Bay Islands Marine Park).
4
In
these two cases, the dolphins may not have processed the octopus sufficiently by shak-
ing and tossing it to ensure the arm’s reflex withdrawal responses were inactive. Octo-
pus arms have a defensive response, as their receptors can detect stimuli that cause
damage to their tissues (Hague et al. 2013). These receptors allow octopus arms to
continue reacting even after the arms have been detached from the head, allowing the
arms to coordinate a reflex withdrawal response (Hague et al. 2013). Dolphins must
therefore process the octopus sufficiently to reduce the arms reflex withdrawal
response and limit their suckers adhering to them, which otherwise would make
them difficult to swallow.
The species of octopus that the dolphin suffocated on in Bunbury was identified as
the benthic-dwelling Maori octopus (Macroctopus maorum).
5
This octopus is robust
and muscular, and is the largest octopus found in Australasia weighing >10 kg with
an arm span of over 3 m (Norman 1999, Norman and Reid 2000). It occurs over soft
sediment and reefs where it occupies rocky lairs (Anderson 1999, Norman and Reid
2000). Other octopus species found within the study area are the common Perth octo-
pus (Octopus (cf.) tetricus) and the velvet octopus (Grimpella thaumastocheir).
5
The com-
mon Perth octopus is medium sized (mean 4 kg; Joll 1976) and inhabits rocky reefs,
seagrass meadows and sandy substrates (Hart et al. 2016). The velvet octopus is a
smaller species that has an arm span <60 cm (Norman and Reid 2000) and has been
caught in traps in Bunbury inner waters (McCluskey et al. 2016). Due to the larger
size of octopus observed during feeding events, dolphins off Bunbury are most likely
handling the Maori and common Perth octopus.
Octopus handling events occurred more often during winter and spring when the
water temperature reached approximately 18°C (Fig. 2). Although the ecology of the
Maori octopus is poorly understood in Western Australia, in New Zealand the mat-
ing period for this octopus is in spring with the optimal water temperature for eggs
to hatch at 18°C (Anderson 1999). Similarly, the optimal water temperature for the
eggs of the common Perth octopus to hatch is under 22°C(Hartet al. 2016). How-
ever, the common Perth octopus has no distinct mating period and they are able to
3
Unpublished data, Nahiid Stephens, veterinary pathologist, Murdoch University Cetacean Research
Unit, School of Veterinary and Life Sciences, Murdoch University, Perth, Western Australia, Australia.
4
Personal communication from Douglas Coughran, Department of Parks and Wildlife, Perth,
Australia. 2 September 2015.
5
Personal communication from Stephen Leporati, SCS Global Services, 19 October 2015.
940 MARINE MAMMAL SCIENCE, VOL. 33, NO. 3, 2017
spawn throughout the year (Hart et al. 2016). Octopus are semelparous, once
males mate and females brood their eggs they become senescent until their death
(Anderson et al. 2002). Senescence occurs for approximately one month, during
which octopus have uncoordinated movements, suboptimal camouflage abilities
and a deteriorating physical condition. Senescence may put octopus in a compro-
mised state, increasing their risk of predation (Anderson et al. 2002). As such, it
is likely that the opportunity for dolphins to capture octopus is increased in win-
ter and spring.
Octopus handling events occurred, on average, in 9 m depth and in turbid (x=
3.30 m) waters, predominantly over sand, algae/sand, and mud/silt habitat types. As
benthic habitat type in Bunbury is highly heterogeneous it was difficult to determine
exactly which habitat octopus were captured from. Furthermore, the octopus species
found off Bunbury occur over a range of habitats, therefore the capture of octopus
appears to be opportunistic over various habitats.
The majority of dolphins handling octopus were adults (20 of the 26 identified
dolphins), suggesting that there may be differences in physical abilities and/or learn-
ing experiences between adults and juveniles/calves. Similarly, in the case of foraging
tactics, bottlenose dolphins generally show differences between ages, which may
reflect energy requirements throughout life history stages and/or reflect a required
learning period (Patterson et al. 2016). In addition, of the adults observed handling
octopus (n=20), 60% were female and 20% were male (20% unknown sex). Thus,
adult females were the most prevalent age-sex class to handle octopus, however, more
data are needed to confirm that this sex-specific finding is not an artefact of females
having smaller home ranges (Sprogis et al. 2016b), and therefore being observed more
frequently throughout the year than males (Sprogis et al. 2016a).
Group size for octopus handling events was nearly twice the average group size for
feeding and foraging groups. Bottlenose dolphins are known to be a highly social
species (Connor et al. 2000), and in our study area adult females display low-level
associations among a large number of females and these associations re-form season-
ally (Smith et al. 2016). Adult males exhibit strong bonds with other adult males
(Sprogis et al. 2016a). Given their social nature, we explored whether there were pre-
ferred associations between dolphins observed handling octopus. There was evidence
of long-term preferred associations between dolphins handling octopus, however,
similar long-term preferred associations were also evident between dolphins with
octopus and dolphins never sighted predating on octopus. These initial findings are
not surprising given the strong social bonds that exist in this dolphin population.
Further information on the number of different dolphins that handle octopus is
needed to determine if octopus handling is indeed a socially learned behavior.
Off Bunbury, stomach content analyses of stranded dolphins (n=13) identified
squid beaks (n=6 of 10 that had prey parts), however octopus beaks were not
recorded.
6
As the head of the octopuses were already removed during several of our
observations the heads may not have always been consumed, thus the beaks would
not be found in stomach contents. Therefore, the importance of octopus in the diet of
the Bunbury dolphin population remains unknown. However, octopuses, like other
cephalopods, are a source of high protein content and are common in the diet of
toothed whales (Clarke 1996, Santos et al. 2001a). From stomach content analysis,
6
Unpublished data, Shannon McCluskey, Ph.D. candidate, Murdoch University Cetacean Research
Unit, School of Veterinary and Life Sciences, Murdoch University, Perth, Western Australia, Australia.
NOTES 941
benthic octopus are found in the diet of Tursiops spp.off the Spencer Gulf, Australia
(Gibbs et al. 2011), Brazil (dos Santos and Haimovici 2001), Hong Kong (Barros
et al. 2000), South Africa (Cockcroft and Ross 1990), Scotland (Santos et al. 2001b),
Ireland (Hernandez-Milian et al. 2015), and the Mediterranean Sea (Miokovic et al.
1999, Blanco et al. 2001, Pedaet al. 2015). Evolution of novel methods for process-
ing cephalopods could therefore have an important influence on the success of ceta-
cean species targeting these prey types.
This research complements the limited studies demonstrating that bottlenose dol-
phins carry out complex handling of prey. Octopus handling is a highly risky behav-
ior for bottlenose dolphins, especially if processing is not executed correctly. For an
animal to engage in such a risky behavior, the nutritional value of the prey must be
substantial. Hence, while octopus handling appears to be relatively rare in the popu-
lation, this prey and handling behavior might still be of great importance for dol-
phins, especially during periods when alternate prey may be limited.
Acknowledgments
Thank you to S. Leporati and F. Brice~no for discussions on octopus and assistance in species
identification. We thank our research assistants and S. McCluskey, M. Cannon, D. Chabanne,
V. Buchanan, and K. Nicholson, who participated with fieldwork and data processing. Thanks
to S. Allen, J. Symons, D. Harvey, and F. Harvey for off-survey effort octopus handling
records. We thank the partners of the South West Marine Research Program for financial sup-
port: Bemax Cable Sands, BHP Billiton Worsley Alumina Ltd, Bunbury Dolphin Discovery
Centre, Bunbury Port Authority, City of Bunbury, Cristal Mining, the Western Australian
Department of Parks and Wildlife, Iluka, Millard Marine, Naturaliste Charters, Newmont
Boddington Gold, South West Development Commission, and WA Plantation Resources. All
research was approved and permitted through the Department of Parks and Wildlife
(SF005811, SF007986, SF008624) and Murdoch University’s Animal Ethics Committee
(W2009/06, W2342/10). KS conceived the study. KS and HR carried out the field research
and analyses. LB conceived and obtained funding for the long-term research program. DH
assisted with video and photo analysis. KS wrote the paper with input from DH, LB, and HR.
Literature Cited
Anderson, T. J. 1999. Morphology and biology of Octopus maorum Hutton 1880 in northern
New Zealand. Bulletin of Marine Science 65:657–676.
Anderson, R. C., J. B. Wood and R. A. Byrne. 2002. Octopus senescence: The beginning of
the end. Journal of Applied Animal Welfare Science 5:275–283.
Barros, N. B., E. C. M. Parsons and T. A. Jefferson. 2000. Prey of offshore bottlenose dolphins
from the South China Sea. Aquatic Mammals 26:2–6.
Bejder, L., D. Fletcher and S. Br€ager. 1998. A method for testing association patterns of social
animals. Animal Behaviour 56:719–725.
Blanco, C., O. Salomon and J. A. Raga. 2001. Diet of the bottlenose dolphin (Tursiops
truncatus) in the western Mediterranean Sea. Journal of the Marine Biological Association
of the United Kingdom 81:1053–1058.
Clarke, M. R. 1996. Cephalopods as prey. III. Cetaceans. Philosophical Transactions of the
Royal Society of London Series B: Biological Sciences 351:1053–1065.
Cockcroft, V. G., and G. J. B. Ross. 1990. Food and feeding of the Indian Ocean bottlenose
dolphin off Southern Natal, South Africa. Pages 295–328 in S. Leatherwood and R. R.
Reeves, eds. The bottlenose dolphin. Academic Press Inc., San Diego, CA.
942 MARINE MAMMAL SCIENCE, VOL. 33, NO. 3, 2017
Connor, R. C., R. S. Wells, J. Mann and A. J. Read. 2000. The bottlenose dolphin: Social
relationships in a fission-fusion society. Pages 91–126 in J. Mann, R. C. Connor, P. L.
Tyack and H. Whitehead, eds. Cetacean societies: Field studies of dolphins and whales.
The University of Chicago Press, Chicago, IL.
Constantine, R., I. Visser, D. Buurman, R. Buurman and B. McFadden. 1998. Killer whale
(Orcinus orca) predation on dusky dolphins (Lagenorhynchus obscurus)inKaikoura,New
Zealand. Marine Mammal Science 14:324–330.
dos Santos, R. A., and M. Haimovici. 2001. Cephalopods in the diet of marine mammals
stranded or incidentally caught along southeastern and southern Brazil (21–34°S).
Fisheries Research 52:99–112.
dos Santos, M. E., and M. Lacerda. 1987. Preliminary observations of the bottlenose dolphin
(Tursiops truncatus) in the Sado estuary (Portugal). Aquatic Mammals 13:65–80.
Edwards, E. W. J., J. Forcada and G. T. Crossin. 2010. First documentation of leopard seal
predation of South Georgia pintail duck. Polar Biology 33:403–405.
Finn, J., T. Tregenza and M. Norman. 2009. Preparing the perfect cuttlefish meal: Complex
prey handling by dolphins. PLoS ONE 4:e4217.
Fish, F. E., S. A. Bostic, A. J. Nicastro and J. T. Beneski. 2007. Death roll of the alligator:
Mechanics of twist feeding in water. Journal of Experimental Biology 210:2811–2818.
Frost, K. J., R. B. Russell and L. F. Lowry. 1992. Killer whales, Orcinus orca,inthe
southeastern Bering Sea: Recent sightings and predation on other marine mammals.
Marine Mammal Science 8:110–119.
Gibbs, S. E., R. G. Harcourt and C. M. Kemper. 2011. Niche differentiation of bottlenose
dolphin species in South Australia revealed by stable isotopes and stomach contents.
Wildlife Research 38:261–270.
Ginsberg, J. R., and T. P. Young. 1992. Measuring association between individuals or groups
in behavioral studies. Animal Behaviour 44:377–379.
Hague, T., M. Florini and P. L. R. Andrews. 2013. Preliminary in vitro functional evidence
for reflex responses to noxious stimuli in the arms of Octopus vulgaris. Journal of
Experimental Marine Biology and Ecology 447:100–105.
Hart, A. M., S. C. Leporati, R. J. Marriott and D. Murphy. 2016. Innovative development of
the Octopus (cf ) tetricus fishery in Western Australia. FRDC Project No 2010/200.
Fisheries Research Report No. 270, Department of Fisheries, Western Australia. 120 pp.
Hernandez-Milian, G., S. Berrow, M. B. Santos, D. Reid and E. Rogan. 2015. Insights into
the trophic ecology of bottlenose dolphins (Tursiops truncatus) in Irish waters. Aquatic
Mammals 41:226–239.
Hocking, D. P., E. M. G. Fitzgerald, M. Salverson and A. R. Evans. 2016. Prey capture and
processing behaviors vary with prey size and shape in Australian and subantarctic fur
seals. Marine Mammal Science 32:568–587.
Hocking, D. P., M. A. Ladds, D. J. Slip, E. M. G. Fitzgerald and A. R. Evans. 2017. Chew,
shake, and tear: Prey processing in Australian sea lions (Neophoca cinerea). Marine
Mammal Science 33.
Irvine, A. B., M. D. Scott, R. S. Wells and J. H. Kaufmann. 1981. Movements and activities
of the Atlantic bottlenose dolphin (Tursiops truncatus) near Sarasota, Florida. Fishery
Bulletin 79:671–688.
Joll, L. M. 1976. Mating, egg-laying and hatching of Octopus tetricus (Mollusca-Cephalopoda)
in laboratory. Marine Biology 36:327–333.
Kohler, K. E., and S. M. Gill. 2006. Coral Point Count with Excel extensions (CPCe): A
Visual Basic program for the determination of coral and substrate coverage using random
point count methodology. Computers & Geosciences 32:1259–1269.
Kr€utzen, M., J. Mann, M. R. Heithaus, R. C. Connor, L. Bejder and W. B. Sherwin. 2005.
Cultural transmission of tool use in bottlenose dolphins. Proceedings of the National
Academy of Sciences of the United States of America 102:8939–8943.
Lopez, J. C., and D. Lopez. 1985. Killer whales (Orcinus orca) of Patagonia, and their behavior
of intentional stranding while hunting nearshore. Journal of Mammalogy 66:181–183.
NOTES 943
Mann, J., B. L. Sargeant, J. J. Watson-Capps, Q. A. Gibson, M. R. Heithaus, R. C. Connor
and E. Patterson. 2008. Why do dolphins carry sponges? PLoS ONE 3:12.
McCluskey, S. M., L. Bejder and N. R. Loneragan. 2016. Dolphin prey availability and calorific
value in an estuarine and coastal environment. Frontiers in Marine Science 3:1–30.
Miokovic, D., D. Kovacic and S. Pribanic. 1999. Stomach content analysis of one bottlenose
dolphin (Tursiops truncatus, Montague 1821) from the Adriatic Sea. Natura Croatica 8:61–65.
Norman, M. 1999. Octopus maorum. Australian Biological Resources Study. Australian Faunal
Directory. 7 April 2016. Available at http://www.environment.gov.au/cgi-bin/species-ba
nk/sbank-treatment2.pl?id=69264.
Norman, M. D., and A. Reid. 2000. A guide to squid, cuttlefish and octopuses of Australasia.
CSIRO, Mooabbin, Australia. 96 pp.
Orbach, D. N., and T. Kirchner. 2014. Armed escorts: Dusky dolphin (Lagenorhynchus
obscurus) interactions with octopuses (Pinnoctopus cordiformis) in New Zealand. Aquatic
Mammals 40:285–292.
Patterson, E. M., and J. Mann. 2011. The ecological conditions that favor tool use and
innovation in wild bottlenose dolphins (Tursiops sp.). PLoS ONE 6:e22243.
Patterson, E. M., E. Krzyszczyk and J. Mann. 2016. Age-specific foraging performance and
reproduction in tool-using wild bottlenose dolphins. Behavioral Ecology 27:401–410.
Peda, C., P. Battaglia, A. Scuderi, A. Voliani, C. Mancusi, F. Andaloro and T. Romeo. 2015.
Cephalopod prey in the stomach contents of odontocete cetaceans stranded in the
western Mediterranean Sea. Marine Biology Research:1–10.
Santos, M. B., M. R. Clarke and G. J. Pierce. 2001a. Assessing the importance of cephalopods
in the diets of marine mammals and other top predators: Problems and solutions.
Fisheries Research 52:121–139.
Santos, M. B., G. J. Pierce, R. J. Reid, I. A. P. Patterson, H. M. Ross and E. Mente. 2001b.
Stomach contents of bottlenose dolphins (Tursiops truncatus) in Scottish waters. Journal of
the Marine Biological Association of the United Kingdom 81:873–878.
Sargeant, B., A. Wirsing, M. Heithaus and J. Mann. 2007. Can environmental heterogeneity
explain individual foraging variation in wild bottlenose dolphins (Tursiops sp.)?
Behavioral Ecology and Sociobiology 61:679–688.
Shane, S. 1990. Comparison of bottlenose dolphin behavior in Texas and Florida, with a
critique of methods for studying dolphin behavior. Pages 541–558 in S. Leatherwood
and R. R. Reeves, eds. The bottlenose dolphin. Academic Press Inc., San Diego, CA.
Smith, H. C., and K. R. Sprogis. 2016. Seasonal feeding on giant cuttlefish (Sepia apama)by
Indo-Pacific bottlenose dolphins (Tursiops aduncus) in south-western Australia. Australian
Journal of Zoology 64:8–13.
Smith, H. C., K. Pollock, K. Waples, S. Bradley and L. Bejder. 2013. Use of the robust design
to estimate seasonal abundance and demographic parameters of a coastal bottlenose
dolphin (Tursiops aduncus) population. PLoS ONE 8:e76574.
Smith, H., C. Frere, H. Kobryn and L. Bejder. 2016. Dolphin sociality, distribution and
calving as important behavioural patterns informing management. Animal Conservation
19:462–471.
Sprogis, K. R. 2015. Sex-specific patterns in abundance, home ranges and habitat use of Indo-
Pacific bottlenose dolphins (Tursiops aduncus) in south-western Australia. Ph.D. thesis,
Murdoch University, Perth, Australia. 168 pp.
Sprogis, K. R., K. H. Pollock, H. C. Raudino, et al.2016a. Sex-specific patterns in abundance,
temporary emigration and survival of Indo-Pacific bottlenose dolphins (Tursiops aduncus)
in coastal and estuarine waters. Frontiers in Marine Science 3:1–12.
Sprogis, K. R., H. C. Raudino, R. Rankin, C. D. MacLeod and L. Bejder. 2016b.Homerange
size of adult Indo-Pacific bottlenose dolphins (Tursiops aduncus) in a coastal and estuarine
system is habitat and sex-specific. Marine Mammal Science 32:287–308.
Torres, L. G., and A. J. Read. 2009. Where to catch a fish? The influence of foraging tactics on
the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. Marine
Mammal Science 25:797–815.
944 MARINE MAMMAL SCIENCE, VOL. 33, NO. 3, 2017
Tyne, J. A., N. R. Loneragan, M. Kr€utzen, S. J. Allen and L. Bejder. 2010. An integrated data
management and video system for sampling aquatic benthos. Marine and Freshwater
Research 61:1023–1028.
Tyne, J. A., N. R. Loneragan, A. M. Kopps, S. A. Allen, M. Kr€utzen and L. Bejder. 2012.
Ecological characteristics contribute to sponge distribution and tool use in bottlenose
dolphins Tursiops sp. Marine Ecology Progress Series 444:143–153.
Visser, I. 1999. Benthic foraging on stingrays by killer whales (Orcinus orca) in New Zealand
waters. Marine Mammal Science 15:220–227.
Weiss, J. 2006. Foraging habitats and associated preferential foraging specializations of
bottlenose dolphin (Tursiops truncatus) mother-calf pairs. Aquatic Mammals 32:10–19.
Wells, R. S., M. D. Scott and A. B. Irvine. 1987. The social structure of free-ranging
bottlenose dolphins. Pages 247–305 in H. H. Genoways, ed. Current mammalogy.
Plenum Press, New York, NY.
Whitehead, H. 2008. Analyzing animal societies: Quantitative methods for vertebrate social
analysis. The University of Chicago Press, Chicago, IL.
Whitehead, H. 2009. SOCPROG programs: Analysing animal social structures. Behavioral
Ecology and Sociobiology 63:765–778.
Whitehead, H., L. Bejder and C. A. Ottensmeyer. 2005. Testing association patterns: Issues
arising and extensions. Animal Behaviour 69:e1–e6.
W€ursig, B., and M. W€ursig. 1977. The photographic determination of group size,
composition, and stability of coastal porpoises (Tursiops truncatus). Science 198:755–756.
W€ursig, B., and M. W€ursig. 1979. Behavior and ecology of the bottlenose dolphin, Tursiops
truncatus, in the South Atlantic. Fishery Bulletin 77:399–412.
Received: 14 November 2016
Accepted: 8 February 2017
Supporting Information
The following supporting information is available for this article online at http://
onlinelibrary.wiley.com/doi/10.1111/mms.12405/suppinfo.
Table S1. Survey effort pooled by austral season from March 2007 to August 2013,
including the number of on-effort sightings and average end group size (standard
deviation).
Table S2. Summary of annual survey effort by transect location from March 2007
to August 2013.
Table S3. Mean dolphin group size (standard deviation) for each of the behavioral
categories.
Figure S1. Octopus tossing and shaking; row (a) an adult male dolphin tossing octo-
pus and leaping out of the water with the octopus still in its mouth, and row (b) an
adult female dolphin with a large shark bite on her left side (bottom left image) arch-
ing her body to shake octopus.
Movie S1. An octopus handling event by an adult male Indo-Pacific bottlenose dol-
phin off Bunbury, Western Australia, showing the different types of handling meth-
ods (shake and toss) used to process the octopus for easier consumption.
NOTES 945
