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Brooding in a gonatid squid off northern Japan.

Brooding of egg masses by a squid in Japan is described. Brooding females were photographed in situ, and the females, their eggs, and their hatchlings were collected. The squid had all undergone gelatinous degeneration and swam slowly and continuously by undulating the fins and expelling water sporadically through the funnel. Eggs were held together by a dark, viscous material that formed a single-layer, sheet-like mass, from which hatchlings were seen to emerge. The annual appearance of brooding females in surface waters during spring suggests that they transport their egg masses from deep water to the surface before the eggs hatch. Genetic analyses identified the squid as Gonatus madokai (family Gonatidae), now the second gonatid and third squid known to brood.

Until 1991, squids were thought to spawn either by attaching egg capsules to solid substrates (nearshore species) or releasing free-floating eggs or egg masses (oceanic species). But that year, a diver off Rausu, Hokkaido, in northern Japan noticed something extraordinary--squid brooding egg masses attached to their arms (1). The squid measured about 60 cm in mantle length (ML) and were not identified to species level, but appeared to belong to the family Gonatidae, which comprises 16 known species in the North Pacific (2). Since then, the brooding squid have been observed annually in shallow waters off Rausu during mid-April to mid-June (K. Seki, pers. obs.). but have remained unidentified.

In 2005, similar brooding behavior was reported in squid off California (3). They were identified as Gonatus onyx Young, 1972, making this species the first documented to brood. Gonatus onyx, however, reaches a maximum ML of 15 cm (2), suggesting that the Japanese squid belong to a different species. Here we describe brooding by the squid in Japan and identify them as G. madokai Kubodera and Okutani, 1977, now the second gonatid squid known to brood.

A scuba diver, with a supporting crew in an outboard skiff, conducted a search for brooding squid during 17-21 May 2010 in nearshore waters off Rausu (44[degrees]00'45" N, 145[degrees]12'15" E). During the nearly 10 h of total dive time, five females (ML range: 38-43 cm) were observed at 5-20-m depth with eggs attached to their arms (Fig. 1A). Each squid was photographed in situ, and the squid and its eggs were collected by hand. Seawater temperature in the collection area ranged from 0 to 4 [degrees]C. Brooding females were also photographed and videotaped in the same area in May 2006 and April--May 2010 at 1-20-m depth.

Frozen tissue samples from two of the collected females were analyzed to identify the species. A 658-bp sequence of the mitochondrial cytochrome c oxidase subunit I (COI) gene was extracted, amplified, cloned, and sequenced as described in Carlini and Graves (4). These sequence data were compared with sequence data for 11 gonatid species from Genbank and at the National Museum of Nature and Science (Japan); Architeuthis sp. was included for out-group comparison. Details on the sources of these data are given in the caption to Figure 2. MEGA 5.0 (5) was used to compute the maximum likelihood tree. The tree was generated using the nearest neighbor interchange (NNI) heuristic method and the Kimura two-parameter substitution model. The tree was computed using gamma distributed with invariant sites for rate among sites (G+1) and 1000 bootstrap replicates. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 639 positions in the final dataset.

Nucleotide-sequence divergences from pairwise comparisons among gonatid COI sequences indicate that the two brooding females analyzed differed from a voucher specimen of G. madokai by 0.94%-1.25%, whereas comparisons between Gonatus congeners ranged from 5.26% to 11.25% (Table 1). In the consensus tree generated from the maximum likelihood analysis (Fig. 2), the 95% bootstrap support for the clade containing the two brooding females and the voucher G. madokai specimen also supports the identification of the brooding females as G. madokai.

Table 1 Pairwise genetic distances (% divergence) between cytochrome
c oxidase I sequences among II gonatid species and 2 brooding females
calculated using MEGA5 (5)

                        1       2      3       4      5      6     7
1.Architeutlzis
sp. (001)

2. Gonatopsis       19.54
borealis (075. T)

3. Gonatopsis       20.02   12.53
octopedatus
(321, SJ)

4. Berryteuthis     22.29   13.85  14.96
anonychus (080, T)

5. Benyteuthis      24.14   12.07  16.12   14.81
magister (139, T)

6. Eogonatus        21.13   12.66   9.00   12.80  14.06
tinro (079, T)

7. Gonatus          18.81   11.10   9.03   12.78  14.08  10.33
fabricii
(AF131873)

8. Gonatus onyx     20.04   12.61   9.24   14.72  15.21  10.54  9.84
(AF00041)

9. Gonatus onyx     20.28   12.61   9.06   14.51  15.00  10.54  9.65
(086, T)

10. Gamuts          20.95   11.16   8.47   13.45  14.31   8.28  7.75
berryi (100, T)

11. Gonatus         21.08   12.04   8.05  1.3.11  13.80   7.85  9.71
pyros (068, T)

12.Gonatus          21.90   11.32   9.82   11.25  12.33   9.07  7.89
kamtschaticus
(071 T)

13.Gonatus          20.32   12.61   9.43   12.83  14.25   9.85  8.91
rnadokai (083, 1)

14. Brooding        19.82   12.38   9.23   13.24  15.10  10.01  9.08
female #1 (398)

15.Brooding         19.57   12.78   9.60  1.3.25  15.09  10.01  9.26
female #2 (399)

                        8      9    10    11    12    13    14
1.Architeutlzis
sp. (001)

2. Gonatopsis
borealis (075. T)

3. Gonatopsis
octopedatus
(321, SJ)

4. Berryteuthis
anonychus (080, T)

5. Benyteuthis
magister (139, T)

6. Eogonatus
tinro (079, T)

7. Gonatus
fabricii
(AF131873)

8. Gonatus onyx
(AF00041)

9. Gonatus onyx      0.16
(086, T)

10. Gamuts           9.26   9.07
berryi (100, T)

11. Gonatus          9.78   9.59  7.19
pyros (068, T)

12.Gonatus          10.42  10.23  7.92  7.72
kamtschaticus
(071 T)

13.Gonatus          11.25  11.06  8.47  9.38  5.26
rnadokai (083, 1)

14. Brooding        10.65  10.46  8.09  9.03  5.61  0.94
female #1 (398)

15.Brooding         10.65  10.46  8.08  8.66  5.78  1.25  0.62
female #2 (399)
Sequence data for (7) Gonatus fabricii and (8) Gonatus onyx came from
GenBank. GenBank Accession Numbers: (7) Gonatus fabricii, AF131873: (8)
Gonatus onyx, AF00041. All other sequence data came from the National
Museum of Nature and Science (Japan). Three-digit number indicates
museum's registration number. T: collected off Tohoku.
Japan: SJ: collected in the Sea of Japan.


The five collected females had all undergone gelatinous degeneration and showed little resemblance to the G. madokai holotype (ML 33 cm) described by Kubodera and Okutani (6); their bodies were fragile, had the consistency of jellyfish, and lacked the long, pointed tails present in younger stages (cf. fig. 229 in 2). Brooding females swam slowly and continuously by undulating the fins and expelling water sporadically through the funnel (supplementary video; http://www.biolbull.org/contentisupplemental/). They lacked tentacles (only stubs were present) and grasped the egg mass using hooks on the three dorsal-most pairs of arms (arms I, II, and 111). Presumably this precluded prey capture and feeding, and the stomachs of all brooding squid were empty.

Eggs were held together by a dark, viscous material to form a single-layer, sheet-like mass that billowed behind the female as she swam (Fig. 1B). Most of the egg masses comprised tattered stands of eggs (supplementary video; http://www.biolbull.org/content/supplemental/); one, however, appeared to form an elongated, hollow tube resembling those of G. onyx (3). Hatchlings, measuring 5.5-6.0 mm in ML (after fixation and preservation), were seen emerging from the egg masses (Fig. 1C), and any handling of the egg masses caused mass outbursts of hatching. Even after all eggs had hatched, egg-mass remnants (dark, viscous strands) remained attached to the arm hooks.

Dead, post-spawning females were nearly neutrally buoyant, and some floated near the ocean surface, where their internal organs were selectively fed on by slaty-backed gulls (Larus schistisagus Stejneger, 1884). Similar postmortem ascent has been reported in other gonatid species (e.g., 7. 8). The remains of dead squid were also observed on the seafloor being eaten by starfish.

Goncaus madokai paralarvae and juveniles occur at epipelagic depths (6), (9), but as females approach maturity, they descend to mesopelagic and bathypelagic depths (10), where spawning is thought to begin in winter (11). Our observations suggest they brood at depth for several months until they appear in surface waters during mid-April to mid-June, which is the only time of the year they are observed off Rausu (K. Selci, pers. obs.) and coincides with the main hatching period for G. mackkai in the Sea of Okhotsk (March--May; 10). Gonatus onyx females are also thought to transport their egg masses to the surface before the eggs hatch, but following a longer (6-9 month) brooding period (12).

While G. madokai is now the second gonatid species known to brood, egg-mass remnants have been observed on the arms of females in three other gonatid species--G. fabricii (Lichtenstein, 1818) (13), G. antarcticus Lonnberg, 1898 (14), and Eogonatus tinro Nesis, 1972 (0. N. Katugin, Pacific Research Fisheries Centre, Vladivostok, Russia; pers. comm.)--which suggests that this behavior is more widespread within the family. The recent report of brooding in a deep-sea squid from another family (Bathyteuthidae; 15) further suggests that more brooding squids await discovery in the deep sea.

Acknowledgments

We thank Brad Seibel and Richard Young for reviewing the manuscript. We also thank Tsuneo Kakuda (National Museum of Science and Nature, Japan), Satoshi Nishizawa (Hokkaido Broadcasting Co., Ltd.), Masanori Ishigame and the Rausu Fishery Cooperative.

Literature Cited

(1.) Okutani, T., I. Nakamura, and K. Seki. 1995. An unusual egg-brooding behavior of an oceanic squid in the Okhotsk Sea. Venus 54: 237-239.

(2.) FAO (Food and Agriculture Organization of the United Nations). 2010. Cephalopods of the World: An Annotated and Illustrated Catalogue of Cephalopod Species Known to Date, Vol. 2, Myopsid and Oegopsid Squids, P. Jereb and C. F. E. Roper, eds. FAO, Rome. 605 pp.

(3.) Seibel, B. A., B. H. Robison, and S. H. D. Haddock. 2005. Post-spawning egg care by a squid. Nature 438: 929.

(4.) Carlini, D. C., and J. E. Graves. 1999. Phylogenetic analysis of cytochrome c oxidase I sequences to determine higher-level relationships within the coleoid cephalopods. Bull. Mar. Sci. 64: 57-76.

(5.) Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance. and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.

(6.) Kubodera. T., and T. Okutani. 1977. Description of a new species of gonatid squid. Gonatus madokai, n. sp., from the Northwest Pacific, with notes on morphological changes with growth and distribution in immature stages (Cephalopoda: Oegopsida). Venus 36: 123-151.

(7.) Young, R. E. 1973. Evidence for spawning by Gonatus sp. (Cephalopoda: Teuthoidea) in the high Arctic Ocean. Nautilus 87: 53-58.

(8.) Nesis, K. N. 1993. Spent females of deep-water .squid Gonatopsis octopedatus Sasaki, 1920 (Gonatidae) in the epipelagic layer of the Okhotsk and Japan seas. Ruthenica 3: 153-158.

(9.) Okutani, T., T. Kubodera, and K. Jefferts. 1988. Diversity, distribution and ecology of gonatid squids in the subarctic Pacific: a review. Bull. Ocean Res. Inst. Univ. Tokyo 26: 159-192.

(10.) Nesis, K. N. 1997. Gonatid squids in the subarctic North Pacific: ecology, biogeography, niche diversity and role in the ecosystem. Adv. Mar. Biol. 32: 243-324.

(11.) Katugin, 0. N., G. A. Shevtsov, and M. A. Zuev. 2004. Distribution, biology, and life cycle of Gonatus madokai (Cephalopoda, Go-natidae) in the Sea of Okhotsk and Pacific waters off the Kurile Islands. Pp. 66-69 in Abstracts of the Conference Mollusks of the Northeastern Asia and Northern Pacific: Biodiversity, Ecology. Biogeography and Faunal History. October 4-6. 2004. Dalnauka, Vladivostok. Russia. [Online]. Available http://rfems.dvo.ru/conference_2004/Malacological_Conference_2004-Abstracts.pdf [2012, 2 November].

(12.) Seibel, B. A.. F. G. Hochberg, and D. B. Carlini. 2000. Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Mar. Biol. 137: 519-526.

(13.) Biorke, H., K. Hansen, and R. C. Sundt. 1997. Egg masses of the squid Gonatus fabricii (Cephalopod. Gonatidae) caught with pelagic trawl off northern Norway. Sarsia 82: 149-152.

(14.) Lapdkhovsky, V. V., A. I. Arkhipkin, and H. J. T. Hoving. 2007. Reproductive biology in two species of deep-sea squids. Mar. Biol. 152: 981-990.

(15.) Bush, S. L.. H. J. T. Hoving, C. L. Huffard, B. H. Robison, and L. D. Zeidberg. 2012. Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). J. Mar. Biol. Assoc. UK 92: 1629-1636.

JOHN R. BOWER (1), *, KATSUNORI SEKI (2), TSUNEMI KUBODERA (3), JUN YAMAMOT0 (4), AND TAKAHTRO NOBETSU (5)

(1.) Faculty of Fisheries Sciences, Hokkaido University, Hakodate Hokkaido 041-8611, Japan; (2.) Shirctoko Diving Kikaku, Rausu Hokkaido 086-1842, Japan; (3.) National Museum of Science and Nature, Shinjukuku, Tokyo 169-0073,. Japan; (4.) Field Science Center for Northern Biosphere, Hokkaido University, Hakodate Hokkaido 041-8611, Japan; and (5.) Shiretoko Nature Foundation, Shari Hokkaido 0994356, Japan

Received 24 May 2012; accepted 24 September 2012.

* To whom correspondence should be addressed. E-mail: akaika@fish. hokudai.ac.jp
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Author:Bower, John R.; Seki, Katsunori; Kubodera, Tsunemi; Yamamoto, Jun; Nobetsu, Takahiro
Publication:The Biological Bulletin
Geographic Code:9JAPA
Date:Dec 1, 2012
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