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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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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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