Content uploaded by Anastasia V. Korosteleva
Author content
All content in this area was uploaded by Anastasia V. Korosteleva on Dec 12, 2022
Content may be subject to copyright.
ВОДНЫЕ БИОРЕСУРСЫ И СРЕДА ОБИТАНИЯ ТОМ 5, НОМЕР 4, 2022
Водные биоресурсы и среда обитания
2022, том 5, номер 4, с. 120–124
http://journal.azniirkh.ru, www.azniirkh.ru
doi: 10.47921/2619-1024_2022_5_4_120
ISSN 2618-8147 print, ISSN 2619-1024 online
Aquatic Bioresources & Environment
2022, vol. 5, no. 4, pp. 120–124
http://journal.azniirkh.ru, www.azniirkh.ru
doi: 10.47921/2619-1024_2022_5_4_120
ISSN 2618-8147 print, ISSN 2619-1024 online
Информационные сообщения
УДК 591.5:569.536
FIRST REPORT OF EPIMELETIC BEHAVIOUR IN A
BLACK SEA HARBOUR PORPOISE (PHOCOENA PHOCOENA
RELICTA ABEL, 1905) TOWARDS A DEAD CALF
© 2022 A. V. Korosteleva, A. N. Postnikova, I. V. Suvorova, K. G. Kuklin
Marine Mammal Research, Rescue and Rehabilitation Center “Serene Sea”, Moscow 109044, Russia
E-mail: sereneseadolphins@gmail.com
Abstract. The term “epimeletic” (“caregiving”) is used to represent a range of cetacean behavioural patterns
directed at dead or distressed conspecifics, including accompanying, lifting to the surface, and protecting
from apparent threats. This behaviour has been described in the literature for various cetacean species;
however, such reports have not yet involved members of the Phocoenidae family. The Black Sea harbour
porpoise (Phocoena phocoena relicta Abel, 1905) is an endangered subspecies that is endemic to the Black
Sea. Despite the proximity of its habitats to the coast, many aspects of its biology, including behaviour,
remain poorly studied. In this paper, we present the first report of epimeletic behaviour in a wild Black
Sea harbour porpoise towards a dead calf. The observation took place during the marine mammal stranding
network operation off the Crimean coast in July 2018. A recently deceased harbour porpoise calf was found
floating on the water surface close to the shore, where it was escorted by a live adult porpoise. We performed
a physical examination and an autopsy of the calf, which revealed pulmonary edema, esophagitis, and
enteritis. Milk was present in the stomach, indicating recent feeding. We assume that the adult individual
could be a lactating female. This observation is probably the only indication to date of the possibility of wild
harbour porpoises showing epimeletic behaviour towards dead calves, which emphasizes the importance of
conducting wider in-depth studies on their behavioural characteristics and social interaction.
Keywords: harbour porpoise, Black Sea, cetaceans, epimeletic behaviour, marine mammals, Phocoena
phocoena
ВОДНЫЕ БИОРЕСУРСЫ И СРЕДА ОБИТАНИЯ ТОМ 5, НОМЕР 4, 2022
FIRST REPORT OF EPIMELETIC BEHAVIOUR IN A BLACK SEA ...
ПЕРВЫЙ СЛУЧАЙ РЕГИСТРАЦИИ ЭПИМЕЛЕТИЧЕСКОГО ПОВЕДЕНИЯ
ЧЕРНОМОРСКОЙ МОРСКОЙ СВИНЬИ (PHOCOENA PHOCOENA RELICTA
ABEL, 1905) В ОТНОШЕНИИ ПОГИБШЕГО ДЕТЕНЫША
А. В. Коростелева, А. Н. Постникова, И. В. Суворова, К. Г. Куклин
Центр изучения, спасения и реабилитации морских млекопитающих «Безмятежное Море»,
Москва 109044, Россия
E-mail: sereneseadolphins@gmail.com
Аннотация. Термин «эпимелетический» («поддерживающий») используется для обозначения ряда
поведенческих паттернов китообразных по отношению к мертвым или умирающим сородичам,
включая их сопровождение, поддержку на поверхности воды и попытки защиты от очевидной угрозы.
В литературе данный тип поведения был описан для различных видов китообразных, однако подобные
сообщения еще не затрагивали представителей семейства Phocoenidae. Черноморская морская свинья
(Phocoena phocoena relicta Abel, 1905) — эндемичный для Черного моря подвид, чья численность
постоянно сокращается. Несмотря на близость местообитаний азовки к побережью, многие аспекты
ее биологии, включая поведение, остаются малоизученными. В данной работе мы приводим первое
описание эпимелетического поведения черноморской морской свиньи относительно мертвого
детеныша. Наблюдение состоялось в рамках работы сети мониторинга выбросов китообразных на
побережье Крыма в июле 2018 г. Свежий труп молодой азовки был найден в воде на расстоянии
от берега, где его сопровождала живая взрослая особь. Нами были проведены физикальный осмотр
детеныша и патологоанатомическое вскрытие, по результатам которого выявлены отек легких,
эзофагит и энтерит. В желудке присутствовало молоко, свидетельствующее о недавнем кормлении,
на основании чего мы предполагаем, что сопровождающая особь могла являться кормящей самкой.
Сегодня это наблюдение, вероятно, является единственным указанием на возможность проявления
дикими морскими свиньями поддерживающего поведения в отношении погибшего потомства,
что напоминает о важности проведения более широких и углубленных исследований социального
взаимодействия и поведенческих особенностей данного вида.
Ключевые слова: морская свинья, азовка, Черное море, китообразные, эпимелетическое
поведение, морские млекопитающие, Phocoena phocoena
INTRODUCTION
The harbour porpoise is a relatively small cetacean
with a rounded head and a short rostrum, small
spatulate teeth with a fl attened crown, rounded
pectoral fi ns and a low triangular dorsal fi n. These
characteristics separate them from dolphins, which
are generally larger and tend to have longer tapered
rostra and cone-shaped teeth [1]. Harbour porpoises
have shorter gestation, lactation periods and lifespans
than most other cetaceans [2]. Little is known about
porpoise species compared to many dolphin species as
they generally exhibit elusive behaviour, avoid human
attention, and are rarely active near the water surface,
with the exception of respiration, which limits the
possibilities for studying their behaviour. However,
the fi nless porpoise and the harbour porpoise have
been kept in human care for many years with success,
contributing to knowledge on their social interac-
tions, breeding behaviour, and sensory physiology [1].
In the wild, porpoises usually tend to occur in small
fl uid groups of 1–10 individuals. The only strong bond
between individuals seems to be formed by mother–
calf pairs that possibly stay together for 1 year until
the next calf is born or possibly 2 years if the female
becomes pregnant every other year [3, 4].
To date, harbour porpoise is the most well-studied
species of the Phocoenidae family, with representa-
tives of the subspecies P. p. relicta Abel, 1905, which
distinction is based on a number of morphological and
genetic characteristics, being the smallest cetacean of
the Azov and Black Sea Basin. Despite the extensive
studies on the Black Sea harbour porpoise biology,
published data on its behaviour in the natural environ-
ment are almost completely absent—little is known
about it at the individual and social group levels. In
this paper, we describe the behavioural responses of
a wild Black Sea harbour porpoise (presumably a
lactating female) to a dead calf.
ВОДНЫЕ БИОРЕСУРСЫ И СРЕДА ОБИТАНИЯ ТОМ 5, НОМЕР 4, 2022
A. V. KOROSTELEVA, A. N. POSTNIKOVA, I. V. SUVOROVA, K. G. KUKLIN
MATERIALS AND METHODS
Since April 2017, we conduct a year-round
cetacean stranding network operation in the Republic
of Crimea. The data on dolphin and porpoise stranding
are received by the organization's hotline directly from
vacationers, local residents, employees of government
agencies, and through the Integrated Duty Dispatcher
Service (IDDS). The stranded mammals are regularly
examined.
On July 24, 2018, stranding network coordina-
tors received a message about a dead porpoise calf
near Solnechnogorskoe Settlement (Alushta District).
The deceased animal was sighted in the water at a
distance of about thirty meters from the shore. During
the entire observation period, an escorting live adult
porpoise was in close proximity to it (the sex could not
be reliably identifi ed). Stranding network coordinators
received a video recording of its behaviour. According
to the materials obtained, the adult animal had normal
swimming pattern and adequate respiratory rate; any
external visible signs of exhaustion and/or diseases
were absent. When it became apparent that the calf
was dead, the observers made the decision to remove
it from the water (fi g. 1).
When people entered the water and approached,
despite a potential threat, the adult porpoise continued
to stay nearby even when the distance to them was
reduced considerably. Eyewitnesses slowly began to
move the dead calf towards the shore. At the same
time, the adult individual was observed to exhibit
accelerated, agitated swimming along its previous
trajectory. Since the observation took place in
the evening, the rapid onset of darkness made it
impossible to estimate how long the adult porpoise
continued to stay near the site. At our request,
the eyewitnesses put the dead calf in a cool place
and covered it with a wet cloth. Due to technical
impossibility of its on-site autopsy, the body was
frozen at -20 °C. The autopsy was performed later on
April 29, 2019 (fi g. 2).
RESULTS AND DISCUSSION
During the examination, we found that the dead
individual was a female with the body length of
71.5 cm, in good physical condition and in a normal
state of nutrition. On the basis of the available literature
data [5], the female was classifi ed as a neonate in
the fi rst month of life, which was evidenced by a
combination of characteristics, such as its body length,
recently healed umbilical wound, and unerupted teeth.
Autopsy and macroscopical examination revealed
pulmonary edema, esophagitis, and enteritis. Milk
Fig. 1. Escorting porpoise and the eyewitness carrying the dead calf to the shore. Solnechnogorskoe, the Republic
of Crimea
Рис. 1. Сопровождающая азовка и очевидец, толкающий к берегу мертвого детеныша. Пос. Солнечногорское,
Республика Крым
ВОДНЫЕ БИОРЕСУРСЫ И СРЕДА ОБИТАНИЯ ТОМ 5, НОМЕР 4, 2022
FIRST REPORT OF EPIMELETIC BEHAVIOUR IN A BLACK SEA ...
was present in the stomach, indicating recent feeding.
It is impossible to speak defi nitively about the cause
of death without histological examination, but we
can rule out starvation due to the loss of a nursing
female, which is a common cause of death among
the Black Sea harbour porpoise calves in spring and
summer, probably resulting from gillnet bycatch [6, 7].
Female caregivers are often inferred to be the mothers
of the dead or dying calves, but parenthood is rarely
confi rmed [8]. Since the calf fed on milk shortly before
death, we assume that the adult individual could be
a lactating female, and her behavior was caregiving,
based on the motives of the epimeletic type. The term
“epimeletic” (but also “caregiving,” “supporting,”
“nurturant”) has been employed with reference to
cetacean behaviour toward the dead or dying. This is an
umbrella term characterizing a range of behavioural
patterns encompassing rescue attempts, postmortem
bereavement, the use of surrogates, and compulsive
stereotypic behavior [9]. Caldwell and Caldwell [10]
divided the epimeletic behaviour of cetaceans into
3 categories: 1) “standing by” (animals remain close
to the distressed individual, accompanying it but not
providing aid); 2) “excitement” (rapid circling the
distressed individual, displaying aggressive behavior
towards an apparent threat (e. g., approaching boat
or diver); and 3) supportive behavior (keeping on
the surface of the water). Epimeletic behaviours also
include prolonged contact with a dead individual
(including decomposed) and are often observed
in cetaceans, frequently with a female caregiver
(presumed mother) supporting a dead calf by
carrying, lifting, or sinking it, generally accompanied
by other escorting individuals [11]. The most common
target (age) group of death-related supportive
behaviour toward dead conspecifi cs is newborns,
which may be due to the higher mortality rate in
newborns than in older calves and juveniles [12, 13].
In cetaceans, these types of behavior are best described
in bottlenose dolphins Tursiops truncatus and short-
fi nned pilot whales Globicephala macrorhynchus,
and, to a lesser extent, in a number of other species;
however, there were no published reports concerning
harbour porpoises.
In the social system of dolphins, like in all
mammalian social systems, the mother–calf bond is the
core unit [14]. Strong social bonds, prolonged periods
of maternal care (a long phase of immaturity), and
even apparent training to hunt have been extensively
recorded for several species of cetaceans [15–18], but
are less well-known for elusive species such as the
harbour porpoise. The process of juveniles learning
hunting has been described for harbour porpoises
in the North Sea: the adult female was observed
releasing live caught fi sh in front of her calf, giving it
a chance to catch (or miss) the prey instead of
feeding it directly [19]. The available research on
the behavior of porpoise mother–calf pairs indicates
that, despite the generally accepted idea of them as
animals without strong social relations, the bond
between female porpoises and their off spring can
be as strong as in other cetaceans.
Fig. 2. Deceased female porpoise taken out of water and prepared for its autopsy
Рис. 2. Труп самки азовки, извлеченный из воды и доставленный для проведения аутопсии
ВОДНЫЕ БИОРЕСУРСЫ И СРЕДА ОБИТАНИЯ ТОМ 5, НОМЕР 4, 2022
A. V. KOROSTELEVA, A. N. POSTNIKOVA, I. V. SUVOROVA, K. G. KUKLIN
The existence of epimeletic behaviour towards
dead individuals in harbour porpoises is a reminder
of the importance of conducting wider and in-depth
studies on their behavioural characteristics and
social interaction, which is extremely relevant for the
subspecies inhabiting the Azov and Black Sea Basin.
ACKNOWLEDGMENTS
The authors express their gratitude to Kelyukh
Ekaterina Denisovna for her assistance in translating
the article into English.
REFERENCES
1. Teilmann J., Sveegaard S. Porpoises the world over:
Diversity in behavior and ecology. In: Ethology and
behavioral ecology of odontocetes. B. Würsig (Ed.).
Galveston, Texas: Springer, 2019, pp. 449–464.
doi: 10.1007/978-3-030-16663-2_21.
2. Braulik G., Minton G., Amano M., Bjørge A. Phocoena
phocoena, harbor porpoise. The IUCN Red List of
Threatened Species, 2020, e.T17027A50369903. doi:
10.2305/IUCN.UK.2020-2.RLTS.T17027A50369903.
en.
3. Teilmann J., Larsen F., Desportes G. Time allocation
and diving behaviour of harbour porpoises (Phocoena
phocoena) in Danish waters. Journal of Cetacean
Research and Management, 2007, vol. 9, issue 3,
pp. 35–44.
4. Read A.J. Porpoise, overview. In: Encyclopedia of
marine mammals. B. Würsig, J.G.M. Thewissen,
K. Kovacs (Eds.). San Diego, California: Academic
Press, 2018, pp. 770–772.
5. Lockyer C. Investigations of aspects of the life
history of the harbour porpoise, Phocoena phocoena,
in British waters. Reports of International Whaling
Commission, 1995, spec. issue 16, pp. 189–197.
6. Birkun A.A.Jr., Krivokhizhin S.V., Gridin V.Yu.,
Zhbanov A.V., Zanin A.V., Masberg I.V. Strandings
of neonate Black Sea harbour porpoises (Phocoena
phocoena) as a probable consequence of the nursing
females’ death in fi shing gear. In: Marine mammals of
the Holarctic. Collection of scientifi c papers after the
3rd International Conference (Koktebel, 11–17 October,
2004). Moscow: Marine Mammal Council Publ., KMK
Scientifi c Press Ltd., 2004, pp. 59–64.
7. Öztürk A.A., Tonay A.M., Raykov V., Dede A. High
mortality of harbour porpoise neonates in the south-
western Black Sea in 2010 and 2011. In: Abstracts
of the 26th Annual Conference European Cetacean
Society (Galway, Ireland, 24–28 March, 2012).
Galway, 2012, pp. 90.
8. Bearzi G., Eddy L., Piwetz S., Reggente M.A.L.,
Cozzi B. Cetacean behavior toward the dead and
dying. In: Encyclopedia of animal cognition and
behavior. J. Vonk, T.K. Shackelford (Eds.). Cham:
Springer International Publishing, 2017, pp. 1–8.
doi: 1007/978-3-319-47829-6_2023-1.
9. Bearzi G., Reggente M.A.L. Epimeletic behavior.
In: Encyclopedia of marine mammals. B. Würsig,
J.G.M. Thewissen, K. Kovacs (Eds.). San Diego,
California: Academic Press, 2017, pp. 337–338.
10. Caldwell M.C., Caldwell D.K. Epimeletic (care-giving)
behavior in Cetacea. In: Whales, porpoises and
dolphins. K.S. Norris (Ed.). Berkeley: University of
California Press, 1966, pp. 755–789.
11. Pedrazzi G., Giacomini G., Pace D.S. First report of
epimeletic and acoustic behavior in Mediterranean
common bottlenose dolphins (Tursiops truncatus)
carrying dead calves. Biology (Basel), 2022, vol. 11,
issue 2, pp. 337. doi: 10.3390/biology11020337.
12. Caughley G. Mortality patterns in mammals. Ecology,
1966, vol. 47, no. 6, pp. 906–918.
13. Whitehead H., Mann J. Female reproductive strategies
of cetaceans: Life histories and care. In: Cetacean
societies: Field studies of dolphins and whales.
J. Mann, R.C. Connor, P.L. Tyack, H. Whitehead (Eds.).
Illinois, Chicago: University of Chicago Press, 2000,
pp. 219–246.
14. Eisenberg J.F. Dolphin behavior and cognition:
Evolutionary and ecological aspects. In: Dolphin
cognition and behavior: A comparative approach.
R.J. Shusterman, J.A. Thomas, F.G. Wood (Eds.).
Hillsdale, New Jersey: Lawrence Erlbaum Associates,
Hillsdale, 1986, pp. 261–270.
15. Whitehead H. Babysitting, dive synchrony, and
indications of alloparental care in sperm whales.
Behavioral Ecology and Sociobiology, 1996, vol. 38,
pp. 237–244.
16. Addink M.J., Smeenk C. Opportunistic feeding
behaviour of rough-toothed dolphins Steno breda-
nensis off Mauritania. Zoologische Verhandelingen
Leiden, 2001, vol. 334, pp. 37–48.
17. Miles J.A., Herzing D.L. Underwater analysis of
the behavioral development of free-ranging Atlantic
spotted dolphin (Stenella frontalis) calves (birth to
4 years of age). Aquatic Mammals, 2003, vol. 29,
issue 3, pp. 363–377.
18. Bender C.E., Herzing D.L., Björklund D.F. Evidence
of teaching in Atlantic spotted dolphins (Stenella
frontalis) by mother dolphins foraging in the presence
of their calves. Animal Cognition, 2018, vol. 12, issue 1,
pp. 43–53. doi: 10.1007/s10071-008-0169-9.
19. Camphuysen K.C.J., Krop A. Maternal care, calf-
training and site fi delity in a wild harbour porpoise
in the North Sea. Lutra, 2011, vol. 54, issue 2,
pp. 123–126.
Поступила 05.07.2022
Принята к печати 03.08.2022
