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Reversal and transfer of spermatophores by Octopus vulgaris and O. hummelincki

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Abstract

Copulatory behavior in the octopus consists of a patterned series of movements whose individual functions are not well understood. Observations and experiments on mating in Octopus vulgaris and O. hummelincki from Bimini, Bahamas and Haiti were made over a number of years in the laboratory. The study reveals how the male octopus reverses its spermatophore prior to transferring it to the female. The male’s terminal organ (penis) extrudes the sperm end of the spermatophore as it exits from Needham’s sac up to the cap or filament thread and then, holding onto the cap thread, inserts the ejaculatory end of the spermatophore into the groove of the hectocotylus, thus reversing it. It is hypothesized that the primary function of the cap or filament thread, one part of the spermatophore, is to be a handle by which the reversal and transfer is accomplished. The siphon is merely a conduit through which the terminal organ functions and plays no role whatsoever in either the reversal of the spermatophore or in its insertion into the groove. The stimulus to which the male orients to find the groove of the hectocotylus is the apex of the retracted interbrachial membrane between the third and fourth right arms, which bears a fixed spatial relationship to the origin of the groove. A number of deviations from the successful transfer process, which represent loss of sperm from the reproductive process, are illustrated. Despite these deviations, the delicately balanced integration of the various movements serves to transfer the spermatophore to the female to ensure reproductive success.

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References

  • Bone Q, Pulsford AL, Chubb AD (1981) Squid mantle muscle. J Mar Biol Assoc UK 61:327–342

    Article  Google Scholar 

  • Dew B (1959) Some observations on the development of two Australian octopuses. Proc R Zool Soc N S W 1957(58):44–52

    Google Scholar 

  • Drew GA (1919) The structure and ejaculation of the spermatophore of Octopus americana. Carnegie Institution of Washington. Pap Tortugas Lab XIV:33–47

    Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, London, pp 1–232

    Google Scholar 

  • Hanson D, Mann T, Martin AW (1973) Mechanism of the spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini. J Exp Biol 58:711–723

    Google Scholar 

  • Mann T (1984) Spermatophores: Development, structure, biochemical attributes, and role in the transfer of spermatozoa. Springer, Berlin, pp 1–217

    Google Scholar 

  • Mann T, Martin AW, Thiersch JB (1966) Spermatophores and spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini. Nature 211:1279–1282. doi:10.1038/2111279a0

    Article  CAS  Google Scholar 

  • Mann T, Martin AW, Thiersch JB (1970) Male reproductive tract, spermatophores and spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini. Proc R Soc Lond B Biol Sci 175:31–61

    Article  CAS  Google Scholar 

  • Needham J (1745) New microscopical discoveries. F Needham, London

    Google Scholar 

  • Packard A, Trueman ER (1974) Muscular activity of the mantle of Sepia and Loligo (Cephalopoda) during respiratory movements and jetting, and its physiological interpretation. J Exp Biol 61:411–419

    CAS  PubMed  Google Scholar 

  • Racovitza EG (1894) Notes de biologie. I Accouplement et fécondation chez l’Octopus vulgaris Lam. Arch Zool Exp Gen 2:23–49

    Google Scholar 

  • Steenstrup J (1856) Die Hectocotylenbildung bei den Cephalopoden. Archival Naturegesch 22, 211–257 Translated in 1857. Hectocotylus-formation in Argonauta and Tremoctopus explained by observation on similar formations in the Cephalopoda in general. Ann Mag Nat Hist 20:81–116

    Article  Google Scholar 

  • Swammerdam J (1737) Biblia Naturae. Leyden: Isaack Severinus, Boubowyn Vander and Peter Vander. Translated in 1758 The Book of Nature CG Seyffert, London

  • Verrill AB (1882) The Cephalopods of the north-eastern coast of America. Part II: the smaller cephalopods, including the “squids” and the octopi, with other allied forms. Trans Conn Acad Arts Sci V:259–446

    Google Scholar 

  • Voight JR (2002) Morphometric analysis of male reproductive features of Octopodids (Mollusca: Cephalopoda). Biol Bull 202:148–155. doi:10.2307/1543651

    Article  Google Scholar 

  • von Orelli M (1962) Die Ubertragung der spermatophore von Octopus and Eledone (Cephalopoda). Rev Suisse Zool 69:93–102

    Google Scholar 

  • Ward DV (1972) Locomotory function of the squid mantle. J Zool 167:487–499

    Article  Google Scholar 

  • Ward DV, Wainwright SA (1972) Locomotory aspects of squid muscle structure. J Zool 167:437–449

    Article  Google Scholar 

  • Wells MJ, Wells J (1972) Sexual displays and mating of Octopus vulgaris Cuvier and O. cyanea Gray and attempts to alter performances by manipulating the glandular condition of the animals. Anim Behav 20:293–308. doi:10.1016/S0003-3472(72)80051-4

    Article  CAS  Google Scholar 

  • Wodinsky J (1972) Breeding season of Octopus vulgaris. Mar Biol (Berl) 16:59–63. doi:10.1007/BF00347848

    Article  Google Scholar 

  • Wodinsky J (1973) Ventilation rate and copulation in Octopus vulgaris. Mar Biol (Berl) 20:154–164. doi:10.1007/BF00351454

    Article  Google Scholar 

  • Wolterding MR (1971) The rearing and maintenance of Octopus briareus in the laboratory, with aspects of their behaviour and biology. MA Thesis, University of Miami

Download references

Acknowledgments

I gratefully thank Joel Cohen, Jean Fraser, Barbara Gruenthal, Mark Jacquin, David Lewkowitz, Jennifer Mather, Nancy Sack, Gayle Schectman, David Segal, Nedra Shulkin, and Dr. James Goldberg for assistance in various phases of this research. I thank the New England aquarium for its generous supply of filtered seawater. I thank Harvey Wang for Figures 1, 2, and 3. I thank Drs. Philip Zeigler and Peter Moller for their helpful comments on the manuscript. I thank Keren Klein and Phil Gnatowski for preparation of the manuscript. I also thank the reviewers of Marine Biology for their detailed, helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Psychology, MS 062, Brandeis University, 415 South Street, Waltham, MA, 02454-9110, USA

    Jerome Wodinsky

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  1. Jerome Wodinsky
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Correspondence to Jerome Wodinsky.

Additional information

Communicated by J.P. Grassle.

Appendices

Appendix 1

Experiment 2 for O. vulgaris (including Number of Tests, Number of Tests with no A and Ps, Number of A and Ps, Duration of Tests)

(a) First cut

Subject

Days

Number of tests

Number of tests with no As and Ps

Test duration (min)

Number of As and Ps

Cut

R

Cut

R

Cut

R

Cut

R

Cut

R

8

1–23

 

9

 

2

 

77

 

27

 
 

24–37

 

5

 

0

 

91

 

38

4

1–26

 

11

 

5

 

66

 

9

 
 

27–36

 

4

 

0

 

76

 

47

12

1–24

 

10

 

6

 

61

 

10

 
 

25–38

 

5

 

0

 

88

 

54

20

1–26

 

11

 

11

 

74

 

0

 
 

27–36

 

4

 

0

 

90

 

68

Total

  

41

18

23

0

\( \overline x \) = 69.5

\( \overline x \) = 86.2

46

207

(b) second cut

Subject

Days

Number of tests

Test duration (min)

Number of As and Ps

Number of tests with no As and Ps

     

8

17

6

73

27

2

     

4

17

6

88

0

6

     

12

16

6

88

8

2

     

20

16

6

101

2

4

     

Total

 

24

\( \overline x \)  = 87.5

37

14

     
  1. Cut refers to the ligula and calamus ablated. R refers to regeneration

Appendix 2

Latencies to first Arch and Pump for O. vulgaris in Experiment 2 (min)

 

Day 1–24

Day 26–38

Day 1–17 (2nd Cut)

Mean (SD)

39.62 (25.08)

23.17 (19.87)

39.8 (33.08)

n

17

19

11

Range

6.25–85.5

1.38–58.49

5.37–97.03

Appendix 3

Latencies (min) for O. hummelincki number 21 in Experiment 4 (Tear in the interbrachial membrane)

Test numbers

Number of A and P

Mean latency to 1st A and P (SD)

Observation of spermatophore

1–9

134

6.12 (4.65)

All seen

10–19

137

12.35 (15.73)

Some seen

20–32

112

22.38 (17.22)

None seen

Appendix 4

Latencies in Experiment 4 for O. hummelincki) pre- and post-surgery on interbrachial membrane (Time in min)

Measure

Subject

Number 3 pre-surgery

Number 3 post-surgery

Number 4 pre-surgery

Number 4 post-surgery

Number 16 pre-surgery

Number 16 post surgery

Number of tests

21

3

18

21

30

21

Mean days between tests

2.7

3

2.8

2.8

2.7

4.7

Total number of A and P’s

222

0

150

170

275

88

Mean latency to 1st A and P (SD)

11.92 (8.33)

 

12.33 (11.55)

 

9.92 (6.93)

31.87 (18.12)

Tests with no A and Ps

5

3

3

4

7

11

Appendix 5

Spermatophoric ejaculatory times for O. hummelincki (Mean 69.0 ± 22.13 s; n = 238).

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Wodinsky, J. Reversal and transfer of spermatophores by Octopus vulgaris and O. hummelincki . Mar Biol 155, 91–103 (2008). https://doi.org/10.1007/s00227-008-1010-3

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