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SHORT COMMUNICATION
Ocean-bottom krill sex
SO KAWAGUCHI 1*, ROBBIE KILPATRICK 1, LISA ROBERTS 2, ROBERT A. KING 1 AND STEPHEN NICOL 1
1
DEPARTMENT OF SUSTAINABILITY, ENVIRONMENT, WATER, POPULATION AND COMMUNITIES, AUSTRALIAN ANTARCTIC DIVISION, CHANNEL HIGHWAY, KINGSTON,
7050, AUSTRALIA AND 2INDEPENDENT RESEARCHER, ARTIST AND ANIMATOR, SYDNEY, NEW SOUTH WALES 2042, AUSTRALIA
TASMANIA
*CORRESPONDING AUTHOR: so.kawaguchi@aad.gov.au
Corresponding editor: Mark J. Gibbons
For the first time the entire sequence of the mating behaviour of Antarctic krill
(Euphausia superba) in the wild is captured on underwater video. This footage also
provides evidence that mating can take place near the seafloor at depths of 400 –
700 m. This observation challenges the generally accepted concept of the pelagic
lifestyle of krill. The mating behaviour observed most closely resembles the mating
behaviour reported for a decapod shrimp (Penaeus). The implications of the new
observation are also discussed.
KEYWORDS: Antarctic krill; mating behaviour; underwater camera; Southern
Ocean; animation
The euphausiid crustacean, Antarctic krill (Euphausia
superba Dana), is reputed to have the largest biomass
of any single metazoan species on the planet, playing
a key role in the structure and function of the
Southern Ocean ecosystem. Antarctic krill serve as
both important grazers and critical prey for whales,
seals and seabirds (Everson, 2000). Krill are one of
the best-studied species of pelagic animals, yet there
are still considerable uncertainties about key elements
of their biology with few published accounts of their
in situ behaviour (Nicol, 2006). Reproductive behaviour, in particular, is poorly described. There are very
limited descriptions of mating behaviour for this, or
any of the 85 species of euphausiid, either in the field
or the laboratory (Ross and Quetin, 2000). The only
reported observation of reproductive behaviour made
in the wild is by Naito et al. (Naito et al., 1986), who
photographed mating behaviour of the surface swarms
of Antarctic krill from the deck of a research vessel.
Part of reproductive behaviour has also been reported
in captive krill with observations of male krill chasing
gravid female krill and making brief contact (Ross
et al., 1987).
Here, for the first time, we report the entire
sequence of mating behaviour of Antarctic krill in
the wild captured on underwater video and then
traced and interpreted using digital animation. This
imagery at the same time provides evidence that
mating behaviour can take place near the seafloor at
depths of 400– 700 m.
The traditional view of krill reproduction is that they
mate and lay eggs in the surface layer (0 – 200 m). The
embryos subsequently sink, then hatch at depths of
700 – 1000 m (Ross and Quetin, 1984) and the
doi:10.1093/plankt/fbr006, available online at www.plankt.oxfordjournals.org. Advance Access publication February 20, 2011
# The Author 2011. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/
licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is
properly cited.
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Received November 21, 2010; accepted in principle January 12, 2011; accepted for publication January 16, 2011
S. KAWAGUCHI ET AL.
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ANTARCTIC KRILL MATING BEHAVIOUR
shape and prominent antennae; gravid females are distinguished by their markedly swollen thorax (Clarke and
Tyler, 2008). At all sites where krill were encountered at
high densities, they were moving rapidly and many
gravid females were observed. We frequently observed
male krill chasing gravid females, which indicated a
population of krill in an active reproductive state.
Conspicuous mating behaviour is apparent in video
sequences that were captured, which show mating behaviour lasting for ≏12 s (Supplementary Material II).
The initial behaviour consists of “chase”, “probe”,
“embrace” and “flex” (Fig. 1), which resembles
the mating behaviour of decapod shrimp (Penaeus;
Misamore and Browdy, 1996). The latter half of the
mating behaviour observed here we refer to as “push”
and this gesture seems to be specific to krill (Fig. 1,
Supplementary Material III). Our observations also
clearly show that two males can be involved in pursuing
a single female at the same time.
Previous anatomical observations of krill indicate
that the transfer of spermatophores is carried out by
the use of special hooks developed in the front two
pairs of male pleopods ( petasma). The hooks fix the
spermatophores in the female’s genital area (the thelycum) while lying abdomen-to-abdomen “embracing”
(e.g. Bargmann, 1937). However, the actual position
adopted by krill during spermatophore transfer has
not yet been subjected to detailed observation. Ross
et al. (Ross et al., 1987) wrote: “the contact point was
the ventral surface of the female just behind the thelycum and the head of the male near the base of the
antennae”. Our observations lead us to speculate that
this position is the prologue to mating. In decapod
Table I: Details of sites observed
Region
SHELF BREAK
CANYON
Sample
code
Start date/time
Bottom time
(h:mm)
Start
latitude
Start
longitude
End
latitude
End
longitude
Start bottom
depth (m)
End Bottom
depth (m)
LC01
LC02
LC03
LC04
LC05
LC06
LL28
LC07
LC08
BTC29
LC09
LC10
LC11
LC12
LC13
LC14
LC15
LC16
BTC30
6
6
6
6
6
7
7
7
7
8
8
8
8
8
8
8
8
8
8
0:13
0:14
0:06
0:06
0:46
0:23
8:22
0:17
0:18
0:03
0:05
0:06
0:07
0:06
0:08
0:08
0:08
0:07
0:05
265.86
265.85
265.84
265.85
265.87
265.90
265.89
265.88
265.87
265.87
265.85
265.86
265.84
265.84
265.73
265.72
265.72
265.82
265.84
88.87
88.87
88.85
88.84
88.87
89.21
89.14
89.08
89.07
89.03
89.32
89.34
89.42
89.53
89.97
89.97
89.97
89.53
89.54
265.86
265.85
265.84
265.85
265.86
265.90
265.88
265.88
265.88
265.87
265.85
265.86
265.83
265.84
265.73
265.72
265.72
265.82
265.83
88.87
88.87
88.85
88.84
88.85
89.19
89.06
89.08
89.07
89.04
89.32
89.34
89.42
89.52
89.97
89.97
89.97
89.53
89.54
452
535
837
578
400
393
493
507
588
561
779
534
601
576
467
636
664
654
547
462
562
869
576
417
416
422
481
571
588
781
535
598
578
460
630
659
668
502
January
January
January
January
January
January
January
January
January
January
January
January
January
January
January
January
January
January
January
2010/16:34
2010/17:57
2010/19:29
2010/20:28
2010/22:00
2010/1:00
2010/9:57
2010/20:56
2010/22:58
2010/4:42
2010/4:42
2010/5:59
2010/7:49
2010/10:31
2010/14:37
2010/15:55
2010/17:03
2010/20:08
2010/22:45
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developing larvae actively swim upwards, reaching the
surface in autumn (the “developmental ascent”, Marr,
1962). There is, however, growing evidence of krill
inhabiting much deeper water (Kawaguchi et al., 1986;
Gutt and Seigel, 1994; Clarke and Tyler, 2008), and our
current observations reinforce the importance of the
ocean bottom as a habitat for krill.
In this paper, we first describe the entire process of
krill mating behaviour, and second, discuss the implication of our observation of this process occurring at
the ocean floor.
Observations were conducted by using an autonomous submersible video camera [Benthic Impacts
Camera System (BICS); Kilpatrick et al., 2011] by
lowering the system vertically to the seafloor. For
details on the sampling gear, see Supplementary
Material I.
Deployments of the underwater camera were conducted at 16 stations off East Antarctica from the RV
Aurora Australis (between 6 and 8 January 2010; Table I).
Video footage of krill mating behaviour was digitally
traced frame by frame, by using Flash animation software. Tracings of live krill were combined with animated drawings traced from illustrations of krill
anatomy (Kirkwood, 1982).
The presence of Antarctic krill near the seafloor was
confirmed for all the 16 stations where the camera gear
was deployed, and at 14 of these krill occurred in high
densities. In most of the cases, very high densities of
krill surrounded the light source within 2 min after the
camera reached the bottom.
Adult Antarctic krill can be recognized easily from
their size and shape: mature male krill have an elongate
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mating, the involvement of the antennae is thought to
indicate the role of a sex pheromone (Misamore and
Browdy, 1996).
In order to mate, male krill must first prepare the
spermatophores on their first pair of petasmas (on their
pleopods). This process is unlikely to take place until
the male finishes the “chase”, because preparing spermatophores on the pleopods (swimming appendages)
for mating would significantly reduce his capacity to
swim. However, while in the “embrace” position, the
male’s pleopods can be free to transfer spermatophore
in the manner described in Bargmann (Bargmann,
1937): he can withdraw spermatophores from his
genital pores, using the 2nd petasma, and then pass
them to his 1st petasma for transferring to the female’s
thelycum.
Spermatophore transfer seems to take place towards
the end of embracing position, or when the male wraps
his abdomen around the female’s abdomen (“flex” position; Fig. 1). On one occasion in the video footage
(Supplementary Material II), two males appear to be
involved in mating one female at the same time. The
“flex” and “wrapping” gestures with rapid spinning,
lasted for ≏5 s, and there was only a limited opportunity within these 5 s for sexual organs to make contact
in order for spermatophore transfer to occur.
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Fig. 1. Sequence of Antarctic krill mating behaviour. Left panels, frames from the video with mating krill circled; centre panels, close ups of
mating krill and right panels, line drawings of each of the mating phase. (a) Chase, (b) probe, (c) embrace, (d) flex, and (e) push.
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The current conceptual understanding of the life
history of krill has largely been based on research activities that focus on the pelagic zone. The upper reaches
of the ocean (,200 m) are accessible for sampling by
nets and acoustics (Kawaguchi and Nicol, 2007) and the
general assumption is that an insignificant portion of
the krill population lives below 200 m (Atkinson et al.,
2009). Recent observations, including ours, are challenging this assumption and this may have considerable
implications for understanding the Antarctic marine
ecosystem and for management of the krill fishery.
Our study for the first time described the entire
sequence of Antarctic krill’s mating behaviour and reveals
that the process is similar to the general mating behaviour
reported in decapod shrimp (Penaeus). At the same time,
our observation raises important questions about the life
history of krill as well as their population structure.
S U P P L E M E N TA RY DATA
Supplementary data can be found online at http://
plankt.oxfordjournals.org.
FUNDING
This work was supported by the Australian Antarctic
Division, the Australian Fisheries Research and
Development Corporation, industry stakeholders (Petuna
Sealord and Austral Fisheries), and the Australian Fisheries
Management Authority.
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After this act, both males appear to continue
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upwelling that would help their larvae to reach the
surface. Alternatively, krill larvae might be able to find
suitable food at depth and may not need to undergo
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