RESEARCH NOTE
Observation of penis elongation in Onykia ingens: implications for
spermatophore transfer in deep-water squid
Alexander I. Arkhipkin and Vladimir V. Laptikhovsky
Falkland Islands Government Fisheries Department, PO Box 598, FIPASS, Stanley FIQQ 1ZZ, Falkland Islands
Correspondence: A.I. Arkhipkin; e-mail: aarkhipkin@fisheries.gov.fk
Cephalopod molluscs possess a variety of reproductive organs
and display diverse sexual behaviours, justifying their nick-
name as ‘oceanic intellectuals’ (Boyle & Rodhouse, 2005).
However, while courtship and mating of shallow-water cuttle-
fish, octopuses and squid have been filmed and well documen-
ted by divers and remotely operated vehicles (Sauer et al.,
1997; Hanlon, 1998), what happens during mating of deep-
water cephalopods remains largely a mystery (Nesis, 1995),
apart from one observation of possible mating behaviour in
Brachioteuthis beanii (Roper & Vecchione, 1996).
When squid mate, a male transfers its sperm to a female
enclosed in complex structures called spermatophores. These
are accumulated in the spermatophoric sac, a storage organ
inside the mantle cavity, before ejaculation through the penis.
Squid that spawn in shelf waters and epipelagic waters of the
open ocean usually have short penes hidden completely inside
the mantle. Males pick the ejaculated spermatophores from
inside their mantle with a specially modified arm called the
hectocotylus, to transfer them to the female. Females spawning
in shallow water have special places for spermatophore attach-
ment on the body, both externally (skin ring around the
mouth, and back of the head) and internally (oviducal gland
openings near gills) (Nesis, 1995). As female squid lack a
vagina, the use of a highly articulated arm (hectocotylus) for
transfer and placement of spermatophores is more precise than
by means of the comparatively poorly articulated penis.
The majority of squid spawning in deep water lack hectoco-
tyli (except Ancistrocheiridae and Cranchiinae; Nesis, 1995),
and they have longer penes than their shallow-water counter-
parts. The only exception is the giant squid Architeuthis dux,
which has the tips of both ventral arms modified and also a
long penis (Nesis, 1995; Gonzalez et al., 2002). However, it is
unknown whether the modifications of the ventral arms in A.
dux are functional hectocotyli involved in the transfer of sper-
matophores (Hoving et al., 2004). It has been suggested that
squid with long penes mate in a head-to-head position and
transfer spermatophores directly by using the penis, as in
Onykia ingens ( Jackson & Jackson, 2004). The location of sper-
matophore attachment in squid with long penes is more vari-
able than in squid with short penes, and can be virtually
everywhere outside the body and inside the mantle (Nesis,
1995). However, it has remained unclear how such males could
reach distant parts and internal areas of the female body,
because mating of deep-water squid has not been described.
Observations of captured and dead mature males have shown
that their penes are either almost entirely concealed within the
mantle with only the apical end protruding beyond the mantle
margin (Jackson & Jackson, 2004), or that they significantly
extend from the mantle (Jackson & Mladenov, 1994). It has
been speculated that the males may somehow hydraulically
‘inject’ their spermatophores ‘under pressure’ to the arms and
internal coverings of the females, as in giant squid A. dux
(Norman & Lu, 1997).
Journal of Molluscan Studies (2010) 76: 299–300. Advance Access Publication: 30 June 2010
# The Author 2010. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.
Here we report on a rare sighting of penis enlargement in a
deep-water squid, which sheds some light on the copulating
mode of these animals. A mature moribund male of the greater
hooked squid Onykia ingens (Smith, 1881) (38.5 cm mantle
length, 1180 g body mass) was caught on the Patagonian slope
south of the Falkland Islands (July 2006, 538200 S, 598310 W,
1050 m depth). When the mantle of the squid was opened for
Downloaded from http://mollus.oxfordjournals.org/ by guest on August 2, 2014
maturity assessment during processing of the catch onboard, the
penis of the squid, which previously had extended only slightly
beyond the mantle margin, suddenly started to erect. It became
rigid and quickly elongated to 67 cm total length, almost the
same length as the whole body of the animal (mantle, head and
arms; Fig. 1). Immediately after elongation, several spermato-
phores were ejaculated from the penis tip.
The capacity to elongate, or to erect, the penis in this way
has not previously been recorded in squid. This observation
suggests how mating may occur in deep-water squid that do
not have the modified arm (hectocotylus) to perform sperma-
tophore transfer. During copulation, the male probably holds
the female with its arms. The females of deep-water squid
usually lack special organs for spermatophore attachment, but
by means of such enormous penis elongation males could reach
everywhere on the female body, including internal organs
within the mantle cavity. In mature female O. ingens, sperma-
tangia (attached spermatophores) have been found beneath
the skin both inside and outside the mantle and funnel
( Jackson & Jackson, 2004). In other deep-water squid the pla-
cement of the spermatophores is more restricted, e.g. near the
mantle cuts in Chaunoteuthis mollis (Arkhipkin & Nigmatullin,
1997) or on the specially modified gelatinous and rugose tissue
on the mantle surface of Octopoteuthis sicula (Hoving, Lipinski
&Videler, et al., 2008), but within these areas precise targeting
is probably not necessary. After attachment, spermatophores
dissolve the outer tissues and penetrate the muscle where they
remain until spawning (Hoving & Laptikhovsky, 2007).
Insertion of spermatophores under the skin or through cuts
made by male hooks is likely painful or unpleasant for the
female (Nesis, 1995). One may assume that males need to act
quickly to avoid rejection, and direct transfer of spermato-
phores by the penis should be faster than indirectly by means
of a hectocotylus.
We suggest that evolutionary development of means of sper-
matophore transfer in squid has followed two distinct pathways.
The first is characteristic mainly of shelf and epi/mesopelagic
squid, and involved the development of specialized seminal
receptacles or spermatophore attachment sites (i.e. near ovidu-
cal gland openings) in females, and elaboration of modified
arms (hectocotyli) in males for the targeted placement of sper-
matophores in these sites/receptacles. The second pathway is
restricted mainly to deep-water squid, in which spermatophores
can be placed on any part of the female body by the long (in
the case of O. ingens erectile) penis, where they subsequently
penetrate under the skin to the muscle. This copulatory
doi:10.1093/mollus/eyq019
 RESEARCH NOTE
Figure 1. Mature males of deep-water squid Onykia ingens with
cut-open mantles showing non-erect (A) and fully erect (B) penes.
adaptation has placed deep-water squid as the record holders in
penis length among all mobile animals (more than total body
length). Only the impressive trunk-like penises of sessile barna-
cles described by Darwin (1854) are relatively longer.
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