Mating in cephalopods has been analyzed in the

natural environment (Boletzky and Hanlon 1983)

as well as in the laboratory (Wood et al. 1998;

Gutiérrez et al. 2012), observing complex behav-

iors between male and female during courtship

(pre-copulation) and copulation (Huffard et al.

2008). This complexity has consequences at the

individual, population and productive systems

levels (Sims et al. 2001). In addition, marked sep-

aration by age, size or proportion of individuals

during reproduction in different octopus species

have been described (Sims et al. 2001).

Patagonian octopus Octopus tehuelchus

(Orbigny, 1834) (Cephalopoda: Octopodidae) is

an endemic, semelparous, small-sized species

(< 150 g) inhabiting the Southwestern Atlantic

Ocean, from south of Brazil (16° S) to the northern

part of the Argentine Patagonia (44° S). It is found

in rocky substrates from low intertidal to the shal-

low subtidal zone, up to 100 m depth (Iribarne

1991; Ré 1998; Narvarte et al. 2006; Storero et al.

2010; Ré and Ortiz 2011) (Figure 1). Females fix

egg clutches to a hard substrate, usually a hole in

the rock, empty shells or artificial shelters. In this

way, embryos are safe from predators, oxygen

level is high by fanning water currents, and incu-

bation area is free from dead embryos and debris

(Ré 1998). This species is caught by an artisanal

fishery community in the northern Patagonian

coast of Argentina (Iribane 1991; Ré 1998; Nar-

varte et al. 2006) and it has been the subject of bio-

logical and fishery studies in the last decades

MARINE AND FISHERY SCIENCES 33 (1): 115-120 (2020). https://doi.org/10.47193/mafis.3312020061807

NOTE

MATING BEHAVIOR OF PATAGONIAN OCTOPUS (Octopus tehuelchus)

UNDER LABORATORY CONDITIONS

MERCEDES BERRUETA1, JULIÁN A. DESIDERIO1, FLORENCIA AGLIANO2, ANDREA VICTORIA LÓPEZ1,

EDDIE O. ARISTIZABAL ABUD1, 2 and NICOLÁS ORTIZ3

1Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP),

Paseo Victoria Ocampo Nº 1, Escollera Norte, B7602HSA - Mar del Plata, Argentina

e-mail: mberrueta@inidep.edu.ar

2Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales, Universidad

Nacional de Mar del Plata (UNMdP), Funes 3350, B7602AYL - Mar del Plata, Argentina

3Laboratorio de Cefalópodos, Instituto de Biología de Organismos Marinos

(IBIOMAR-CONICET), Blvd. Brown 2915, U9120ACD - Puerto Madryn, Argentina

ABSTRACT. Patagonian octopus (Octopus tehuelchus) is a species that holds an artisanal fishery in the northern

area of the Argentine Patagonian coast and has a potential for aquaculture development. This work aimed to characte-

rize the mating behavior of four pairs of Patagonian octopuses under laboratory conditions. Results showed that this

species has a complex reproductive behavior. Remarkably, female remained inside her shelter during pre-copula, copu-

lation and intercourse events. Male and female faced by the oral face during sexual intercourse, which lasted 3 to 5 min.

The observations will contribute to the better management of the reproductive specimens of the species in captivity.

Key words: Octopus tehuelchus, aquaculture, copula, hectocotyle.

115

(Pujals 1982; Narvarte et al. 1996, 2007; Storero et

al. 2012; Fassiano et al. 2017). Recently O.

tehuelchus has been considered as a potential

aquaculture resource (Berrueta et al. 2018a,

2018b), but the lack of understanding of some

aspects of reproductive behavior useful for devel-

oping an incubation plant, hinders the develop-

ment of mass cultivation technology of this

species. The objective of this work was to describe

male-female interactions during mating of O.

tehuelchus under controlled aquarium conditions.

Octopuses hatched in captivity at the Estación

Experimental de Maricultura, Instituto Nacional

de Investigación y Desarrollo Pesquero (INIDEP).

They were maintained individually in 30 l aquaria

connected to a recirculation aquaculture system

(RAS). Seashells were provided as individual

shelters. Photoperiod was set at 12:12 h (light :

dark). Water quality parameters were monitored

daily and maintained at 15.5 ±1.1 °C (Earth

Industries heater/cooler, Japan), pH 7.7 ±0.2

(Oakton pH/temperature Series110 RM232),

salinity 34 ±1 (Tanaka NewS-100 light refrac-

tometer), and total ammonia concentration 0.0 ±

0.5 mg NH4+L-1 (Merck colorimetric kit). Four

pairs (male-female) of adult octopuses (nine-

month-old) were used to record the events during

the mating courtship. Prior to weighting and han-

dling, individuals were anesthetized with 2.5%

ethyl alcohol in sea water, following bioethical

guidelines by Fiorito et al. (2014) and Butler-

Struben et al. (2018). Total weight was registered

by using a Mettler Toledo PB 602-S. Initial

weight range was 100-125 g and 38-48 g for

females and males, respectively. Each couple was

placed in an 80 l aquarium with seashells and fed

ad libitum with fresh shrimp (Artemesia longi-

naris). Male-female interactions were recorded

during daytime hours. Mating behavior of Patag-

onian octopus was classified following the crite-

116 MARINE AND FISHERY SCIENCES 33 (1): 115-120 (2020)

Figure 1. Geographic distribution of Octopus tehuelchus in the Southestern Atlantic Ocean (Ré 1998, 2008).

65° W 60° W 55° W 50° W 45° W

45° S

40° S

35° S

30° S

25° S

Argentina

Paraguay Brazil

Uruguay

0 330 660

Kilometers

ria proposed by Huffard et al. (2008), Rodrigues et

al. (2009) and Caldwell et al. (2015), which were

described as pre-copulatory (swimming, display,

and contact) and copulatory behavior. Once the

mating was over, male and female were left in the

mating tank until the experience ended. After

intercourse, females were sedated and examined

to verify the presence of spermatophores in the

distal oviducts. Octopus behavior in each aquari-

um was recorded and photographed daily with a

Sony Lens G camera.

Three pre-copulatory events (male display,

female display, and contact) and one copulatory

behavior (intercourse) were observed. Male

exhibited an intense and changing reddish color

during the display, moving around female’s shel-

ter (Figure 2 A) and also returning back to his

own shelter. Female exhibited a pale and homo-

geneous coloration, remaining inside the shelter

and displaying her arms outside and directs them

towards the male (Figure 2 B). Contact event con-

sisted of touching each other with one or more

arms for short intervals of time (5-10″) (Figure 2

C). During copulation male moved towards the

female and partially or totally surrounded her

with his arms (Figure 2 D). Female remained in

her shelter exposing her oral surface with her

arms folded towards her mantle while male per-

formed the insemination process by intruding the

hectocotylized arm into the female’s mantle

accompanied by occasional changes in body col-

oration patterns (Figure 2 E and F). The approxi-

mate duration of the copula was 3 to 5 min. After

that, male returned to his shelter. Copulation

event was repeated 2 to 3 times during the same

day, always preceded by the display of the female

and the contact of the arms. Couples remained

together (from a few days to weeks) in the same

tank until female’s aggressive behavior towards

the male was observed, including the removal of

male’s shelters. Coincidently with this behavior,

egg clutches were found in female’s shelters in all

cases and males were consequently removed

from the mating tanks.

Courtship is an important mechanism in the

couple’s choice (Krebs and Davies 1993). Huffart

et al. (2008) reported a pre-copulatory behavior

characterized for a recognition interaction at

species and sex level during the onset of courtship

in Abdopus aculeatus. Gutierrez et al. (2012) indi-

cated that a pre-copulatory behavior in Enterocto-

pus megalocyathus begun with the approach with-

out physical contact followed by three consecu-

tive events: swimming, exhibition and contact. In

the present work, both male and female exhibited

display behaviors, remarkable changes in col-

oration and contact between the arms, confirming

that a pre-copulatory behavior was present.

Copulation mode and chromatic changes

varies significantly in cephalopods (Mangold

1987; Hanlon and Messenger 1996). In squids

like Sepioteuthis lessoniana and S. australis mat-

ing position is called ‘head to head’, where male

holds the female with the arms (Boal and Gonza-

lez 1998). In sepiolids, however, the copulatory

strategy observed is the so-called ‘male to female

neck’, accompanied by intense color patterns

characteristic for each sex (Moynihan 1983; Nab-

hitabhata et al. 2005; Rodrigues et al. 2009).

Mangold (1987) observed two mating positions

in specimens of Family Octopodidae: the ‘dis-

tance position’ in which male and female remain

separated during the copulation (only joined by

the hectocotyle), and the ‘close position’ in which

the male rides the female. In both cases, the inter-

actions can last from a few minutes to hours.

Authors such as Hanlon and Messenger (1996)

and Wells and Wells (1972), determined that cop-

ula positions in octopuses are of ‘distance’ or

‘assembly’, or an intermediate positions between

the two. Oral surface of female O. tehuelchus

faces out of the shelter while the mantle looks

towards the eggs during parental care. This mat-

ing position was described previously as ‘beak to

beak’ by Caldwell et al. (2015) for the Great

Pacific Striped Octopus (LPSO). The same

authors indicated that, unlike the ‘distance’ and

‘assembly’ positions observed in other types of

117

BERRUETA ET AL.: MATING OF THE OCTOPUS TEHUELCHUS IN CAPTIVITY

octopus, the ‘beak to beak’ mating implies an

effective grip and allows a complete wrapping of

the male over the female’s oral region, as well as

conferring specific advantages such as protection

of eggs clutches by female. Generally, in octopus-

es that have other mating positions such as O.

cyanea (Tsuchiya and Uzu, 1997), Vulcanoctopus

hydrothermalis (Rocha et al. 2002), O. kaurna

118 MARINE AND FISHERY SCIENCES 33 (1): 115-120 (2020)

Figure 2. Detail of mating events of Patagonian octopus Octopus tehuelchus. Precopulatory behavior: male display (the arrow

indicates the movement of the male) (A), female display (B), contact (C). Copulatory behavior: copula (D-F).

♀

♂

♀

♂

♀

♂

♀

♂

♀

♂

Hectocotylized arm

(Norman 2000) and O. bimaculoides (Hanlon and

Messenger 1996) females can mate with several

males simultaneously.

Although many aspects of the mating behavior

of O. tehuelchus are similar to those reported for

LSPO, including the ‘beak to beak’ mating posi-

tion, it should be noted that female Patagonian

octopus remains in the shelter during the pre-cop-

ula and copula events. The observations obtained

during the present work showed complex behav-

iors between males and females during mating

events, such as a protective behavior of the put-

ting in parallel with the rejection of the already

copulated male by female. In this sense, and from

a zootechnical point of view, these data are highly

relevant for the handling of specimens during

reproductive conditioning of O. tehuelchus in the

laboratory.

INIDEP contribution no. 2210.

REFERENCES

BERRUETA M, ARISTIZABAL ABUD E, RICCI E,

BOCCANFUSO J. 2018a. Avances en el desarro-

llo de tecnología de producción comercial de

juveniles de pulpito Octopus tehuelchus 2016-

2017. Inf Ases Transf INIDEP N° 12/2018. 15

BERRUETA M, RADONIC M, LÓPEZ A, DESIDERIO J,

ORTIZ N. 2018b. Modelo predictivo para la

evaluación del estatus reproductivo del pulpi-

to Octopus tehuelchus mediante el uso de la

técnica ecográfica. Inf Invest INIDEP N°

110/2018. 16 p.

BOAL JG, GONZALEZ SA. 1998. Social behaviour

of individual oval squids (Cephalopoda,

Teuthoidea, Loliginidae, Sepioteuthis lessoni-

ana) within a captive school. Ethology. 104:

161-178.

BOLETZKY S, HANLON RT. 1983. A review of the

laboratory maintenance, rearing and culture of

cephalopod molluscs. Mem Natl Mus Victoria.

44: 147-187.

BUTLER-STRUBEN HM, BROPHY SM, JOHNSON

NA, CROOK RJ. 2018. In vivo recording of

neural and behavioral correlates of anesthesia

induction, reversal, and euthanasia in cephalo-

pod molluscs. Front Physiol. 9: 109-112.

CALDWELL RL, ROSS R, RODANICHE A, HUFFARD

CL. 2015. Behavior and body patterns of the

larger Pacific striped octopus. PLOS ONE. 10

(8): e0134152.

FASSIANO A, ORTIZ N, RÍOS DE MOLINA MC.

2017. Reproductive status, antioxidant

defences and lipid peroxidation in Octopus

tehuelchus (Cephalopoda: Octopodidae)

females. J Nat Hist. 51: 2645-2660.

FIORITO G, AFFUSO A, ANDERSON DB, BASIL J,

BONNAUD L, BOTTA G, COLE A, D’ANGELO L,

DEGIROLAMO P, DENNISON N, DICKEL L, et al.

2014. Cephalopods in neuroscience: regula-

tions, research and the 3Rs. Invert Neurosc.

14: 13-36.

GUTIÉRREZ R, FARÍAS A, YANY G, URIARTE I.

2012. Interacciones macho-hembra del pulpo

rojo patagónico Enteroctopus megalocyathus

(Cephalopoda: Octopodidae) durante el com-

portamiento de apareamiento. Lat Am J Aquat

Res. 40: 808-812.

HANLON RT, MESSENGER JB. 1996. Cephalopod

behavior. Cambridge: Cambridge University

Press. 232 p.

HUFFARD CL, CALDWELL RL, BONEKA F. 2008.

Mating behavior of Abdopus aculeatus (d’Or-

bigny 1834) (Cephalopoda: Octopodidae) in

the wild. Mar Biol. 154: 353-362.

IRIBARNE O. 1991. Intertidal harvest of the Patag-

onian octopus, Octopus tehuelchus (d’Or-

bigny). Fish Res. 12: 375-390.

KREBS JR, DAVIES NB. 1993. An introduction to

behavioural ecology. 3th ed. Oxford: Black-

well Scientific Publications. 420 p.

MANGOLD K. 1987. Reproduction. In: BOYLE PR,

editor. Cephalopod life cycles: Volume II

comparative reviews. London: Academic

Press. p. 157-200.

119

BERRUETA ET AL.: MATING OF THE OCTOPUS TEHUELCHUS IN CAPTIVITY

MOYNIHAN M. 1983. Notes on the behavior of

Euprymna scolopes (Cephalopoda: Sepioli-

dae). Behaviour. 85: 25-41.

NABHITABHATA J, NILAPHAT P, PROMBOON P,

JAROONGPATTANANON C. 2005. Life cycle of

cultured bobtail squid, Euprymna hyllebergi

(Nateewathana, 1997). Phuket Mar Biol Cent

Res Bull. 66: 351-365.

NARVARTE M, GONZÁLEZ R, FILIPPO P. 2007. Arti-

sanal mollusk fisheries in San Matías Gulf

(Patagonia, Argentina): An appraisal of the

factors contributing to unsustainability. Fish

Res. 87: 68-76.

NARVARTE M, GONZÁLEZ R, FERNÁNDEZ M. 2006.

Comparison of tehuelchus octopus (Octopus

tehuelchus) abundance between an open-

access fishing ground and a marine protected

area: evidence from a direct development

species. Fish Res. 79: 112-119.

NARVARTE M, GONZÁLEZ R, SICA I. 1996. Estado

actual de la pesquería de pulpito patagónico

Octopus tehuelchus en el Golfo San Matías.

Informes Técnicos del Plan de Manejo Inte-

grado de la Zona Costera Patagónica, Puerto

Madryn, Argentina. 19. 33 p.

NORMAN M. 2000. Cephalopods: a world guide.

Hackenheim: ConchBooks. 318 p.

PUJALS MA. 1982. Contribución al conocimiento

de la biología de Octopus tehuelchus d’Or-

bigny (Mollusca: Cephalopoda). Acad. Nac.

Cs. Serie I - Ciencias. 46: 30-71.

RÉME. 1998. Pulpos octopódidos (Cephalopoda:

Octopodidae). In: BOSCHI EE, editor. El Mar

Argentino y sus recursos pesqueros. Tomo 2.

Los moluscos de interés pesquero. Cultivos y

estrategias reproductivas de bivalvos y equinoi-

deos. Mar del Plata: Instituto Nacional de

Investigación y Desarrollo Pesquero (INIDEP).

p. 69-98.

Ré ME. 2008. Cefalópodos. In: BOLTOVSKOY D,

editor. Atlas de sensibilidad del mar y la costa.

http://geoportal.ddns.net/atlasambiental/index.

htm.

RÉME, ORTIZ N. 2011. Cefalópodos capturados

en la Campaña “CONCACEN – Noviembre

2009”, B/O Puerto Deseado. VIII Congreso

Latinoamericano de Malacología. Libro de

resúmenes. p. 249.

ROCHA F, GONZÁLEZ A, SEGONZAC M, GUERRA A.

2002. Behavioural observations of the

cephalopod Vulcanoctopus hydrothermalis.

Cah Biol Mar. 43: 299-302.

SIMS DW, NASH JP, MORRITT D. 2001. Move-

ments and activity of male and female dogfish

in a tidal sea lough: alternative behavioural

strategies and apparent sexual segregation.

Mar Biol. 139: 1165-1175.

RODRIGUES M, GARCÍ M, GUERRA A, TRONCOSO J.

2009. Mating behavior of the Atlantic bobtail

squid Sepiola atlantica (Cephalopoda: Sepiol-

idae). Vie et Milieu. 59: 271-275.

STORERO LP, NARVARTE M, GONZÁLEZ RA. 2012.

Reproductive traits of the small Patagonian

octopus Octopus tehuelchus. Helgol Mar Res.

66: 651-659.

STORERO LP, OCAMPO-REINALDO M, GONZÁLEZ

RA, NARVARTE M. 2010. Growth and life span

of the small octopus Octopus tehuelchus in

San Matías Gulf (Patagonia): three decades of

study. Mar Biol. 157: 555-564.

TSUCHIYA K, UZU T. 1997. Sneaker male in octo-

pus. Venus Jap J Malacol. 56: 177-181.

WELLS MJ, WELLS J. 1972. Sexual displays and

mating of Octopus vulgaris Cuvier and O.

cyanea Gray and attempts to alter perform-

ance by manipulating the glandular condition

of the animals. Anim Behav. 20: 293-308.

WOOD JB, KENCHINGTON E, O’DOR RK. 1998.

Reproduction and embryonic development

time of Bathypolypus arcticus, a deep-sea

octopod (Cephalopoda: Octopoda). Mala-

cología. 39: 11-19.

Received: 15 January 2020

Accepted: 3 February 2020

120 MARINE AND FISHERY SCIENCES 33 (1): 115-120 (2020)