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Mate selection & copulation

  Mate selection & copulation are dealt with in this section, while topics of EGG-LAYING, EMBRYONIC DEVELOPMENT, HATCHING & LARVAL LIFE, SETTLEMENT & METAMORPHOSIS, and ONTOGENETIC DEVELOPMENT OF BEHAVIOUR are considered elsewhere.
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  This section on mate-selection & copulation is arranged alphabetically by genus. The genus Hermissenda is considered here, while AEOLIDIA , ALDERIA, NAVANAX & OTHER CEPHALASPIDS, and APLYSIA & OTHER ANASPIDS are considered in their own sections.
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Research study 1

nudibranchs Hermissenda crassicornis engaged in precopulatory behaviourSeveral detailed accounts of agonistic1 behaviour in Hermissenda crassicornis done in Oregon and California later are thought to be most likely accounts of mating.  The reason for the misunderstanding owes in part to the extraordinary quickness of the actual copulatory act, which requires only 1-2sec.  The author never observes copulation in Hermissenda, in part because of a possible expectation of an activity that would last several minutes or even hours as is customary in other opisthobranchs.  The complexity of interactions involved in one of the studies is shown in this computer-simulated flow chart.  Be mindful as you go through it that the researcher is describing general behaviour in laboratory specimens with the understanding that it relates to agonism. With a bit of patience, and assuming that what is really being described is not agonism, but copulatory behaviour, the behavioural repertoire during mating can be noodled out to a few basic components. The line thicknesses in the diagram correspond with frequency of occurrence of any successive pair of behaviours.

With these assumptions, a copulatory encounter in Hermissenda begins with a touch of one individual by another, most commonly with tentacles or cerata. Since touch tentacle is the most likely of these events (based on observation of field animals and on the line-thickness2 on the diagram below) we’ll start there.  From touch tentacle we go to recoil (either or both individuals rear back), then to flagellate3(mutual tentacle touching), and sidle-ing, which is right-side to right-side orientation that places the gonopore openings of the 2 individuals opposite one another. 

schematic showing behavioral pathways involved in copulatory behaviour in the nudibranch Hermissenda crassicornisWe follow this particular route because it seems to be most likely to get us to "sidle", which we know is preparatory to copulation. However, because copulation is not in the author's mind, we have to choose a spot for it to happen. A possible spot for this is marked with a bright yellow blob on the flow diagram, its position4 being guessed at because it leads to "veer-ing off", and then to "withdraw" and "end" - all familiar from Research Study 1 above. The author observes damage done by biting (the jaws have serrated edges), describes  “winners” and “losers” in the encounters, and notes that 26% of the “winners”, presumably the ones that break away first, are the larger individuals of the pairs (thus, 74% of "winners" are smaller individuals). There are other behaviours shown in the diagram that may or may not play a role in copulation. Zack 1975 Behaviour 53: 238. Photograph courtesy Kevein Lee, Fullerton diverkevin.

NOTE1  a term used in studies of animal behaviour meaning “contest” (G.)

NOTE2  the chart has 37 connections, with the ones occurring more frequently being indicated by thicker lines

NOTE3 recall that the author believes the behaviour to be agonistic; hence, the "physical" nature of this term. Tentacle-touching is described by other authors as more of a "caressing"

NOTE4  this is only one possible route from "sidling" that could lead to insemination.  Another shorter one would be sidle to bite and then to end, but the arrow dimension indicates that bite-ing to end occurs with low frequency.  Another, more round-about route on the chart following from an hypothetical copulation after sidle-ing is: move cerata, lunge, bite, move cerata, withdraw, and then end, and this route also has the merit of large-dimension arrows.  The reason for speculating on possible post-sidle-ing routes will become clear when we examine Research Studies to follow

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photograph of copulation in the aeolid nudibranch Flabellina verrucosa taken from a video

CLICK HERE to see a video of Flabellina verrucosa copulating. Given that the behaviour in this species is likely similar to that described for Hermissenda crassicornis, we can describe an approach by one individual, touching another with its tentacles, withdrawal ("recoil") of the touched individual, mutual touching of tentacles ("flagellation"), and more withdrawals. This goes on for some time and the video switches to show full right side-to-right side touching ("sidling") and perhaps even copulation. It is understandable how the author of Research Study 1 above could initially interpret these behaviours as agonism.

NOTE  the video replays automatically

NOTE  however, anthropomorphism is all too common in interpretation of animal behaviour. In this case, the terms "flagellate", "sidle", "winners", and "losers", are highly suggestive. Is it possible that their initial selection may have prevented the author from standing back and viewing the behaviours more objectively?

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Research study 2

photo/schematic of the head end of the nudibranch Hermissenda crassicornis showing partsWhat explains the author's focus on "agonism" in Hermissenda?  No other nudibranch species appears to exhibit it, nor is it a feature known to be particularly common in gastropods. The author remarks on never having seen agonistic behaviour in Hermissenda in the field.  As to the function of the putative agonistic behaviour, the author speculates that it may aid in food-getting and be a means of warding off predators.  In another publication on the same subject the author tests what effect food deprivation has on the “agonistic” behaviour?  In these latter experiments, after 1-3d without food there is an increase in locomotory activity and an increase in "agonistic" interactions.  Also, with each progressive day the frequency of encounters involving biting goes up, suggesting to the author that hunger may be the cause of the “fighting” behaviourZack 1974 Behav Biol 12: 223, 525.

NOTE  a common behaviour in nudibranchs when food is scarce or lacking, however, is to copulate.  This makes sense because most species of nudibranchs live seasonally and, when their prey items are in short supply, they spend more time copulating...not fighting

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Research study 3

In a follow-up study in Oregon the same author investigates the possible role of nematocysts in "agonistic" behaviour in Hermissenda crassicornis. Although the study may not be as relevant to “agonistic” behaviour as the author intended, the technique used may be useful for other types of experiments.  In the present experiments, the author pinches off all cerata from several Hermissenda with forceps, provides clam tissues as food, and waits until the cerata are regenerated.  At this time the cnidosacs should be empty of nematocysts.  The author then compares the behaviour of these “nematocyst-free” animals with that of normal control animals and finds no difference in level of “agonistic” behaviour.  The technique, although not working out in the way that the author intended could, nevertheless, be a useful way to produce nematocyst-free aeolids for other types of experiments, for example, to assess the defensive efficacy of the secondarily acquired nematocysts against fishes and other biting predators. This is not a new idea, but appears not to have been done with west-coast nudibranchs. Zack 1975 Veliger 17: 271.

NOTE  later studies by researchers at Friday Harbor Laboratories, Washington indicate that rather than being agonism, the behaviour described for Hermissenda is just normal reproductive acitivity; see Research Study 6 below

NOTE  the author is not able to check whether the cnidosacs were actually nematocyst-free, as all the animals die before this could be done.  Healthy Hermissenda can, however, be raised on non-hydroid diets over several generations, and these individuals do become nematocyst-free

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Research study 4

schematic of duration of copulatory behaviours in the nudibranch Hermissenda crassicornis Several years later, in a follow-up study on the interactions described above for Hermissenda crassicornis, a second author agrees with the first that the species does engage in aggressive interactions with conspecifics.  However, what is missing in the first descriptions, acording to the second author, is information on the temporal aspects of the interaction, specifically the timing of events from first contact to onset of sidling, and then to cerata movement, lunging and biting, withdrawing, and ending.  These events are observed in specimens of H. crassicornis from Elkhorn Slough, California and recorded on videotape for time-motion analysis.  Note in the data presentation that the mean duration of these activities is only about 80 seconds.  The author comments that “although the animals are poised in copulation-like posture during sidling, it seems clear, as Zack suggested, that these interactions are not copulatory since the time between initiation of sidling and cerata movement is on the average less than 10 seconds”.  In discussing the results, the author provides 2 possible explanations for flagellation and sidling: 1) to assess the aggressive motivation and size of the other individual, or 2) to assess the willingness of the other individual to mate.  The author concludes by suggesting that more observations are needed to clarify the matter.  Rutowski 1981 Veliger 24: 227.

NOTE  the diagram shows the durations of 4 sets of activities from first contact: begin sidling, move cerata, withdraw, and end. Each horizontal set includes overall range, standard deviation, and mean for each set of activities. The vertical blue dotted line shows the mean end time in seconds for 19 individual nudibranchs

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Research study 5

In a research “note” immediately following the Research Study 6 paper in the same journal volume, the author remarks that the Longleys’ paper (see Research Study 6 below) describes only one outcome of interaction between Hermissenda, and that Zack's original paper (Research Studies 1 & 3) makes it clear that there may be other possible outcomes, including aggression.  Rutowski 1981 Veliger 24: 231.

NOTE  because the 2 papers (Research Studies 4 & 6) were submitted for review at the same time for publication in the same volume of Veliger, out of courtesy and interest the Editor allowed each set of authors to read the other’s submission and to make comments.  The set of 4 articles in Veliger is unique and makes for interesting reading

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Research study 6

nudibranchs engaging in pre-copulatory head-butting, Hermissenda crassicornisIn the same journal as the foregoing publications (Research Studies 4 & 5) is a paper entitled, “Hermissenda: agonistic behavior or mating behavior?”  In this paper researchers at Friday Harbor Laboratories, Washington note that agonism is not seen in the field in H. crassicornis, and describe the following pre-copulatory behaviours in laboratory specimens: 1) one animal follows another, 2) front individual turns, 3) they meet head-to-head , 4) make tentacle/tentacle contact, 5) withdraw, 5) make tentacle/cerata contact, 6) withdraw, 7) make tentacle/foot contact, 8) advance, and 9) jockey back-and-forth.  Time required: 10-30min. 

The individuals then align their bodies on the right sides (1-3min), evert penises, expand penis ends into bulbs, and simultaneously ejaculate sperm in muscular contractions.  The sperm is emitted in mucus.  Time for copulatory ejaculation: 1-2sec.  The authors observe no biting damage, but suggest that the function of pre-copulatory contact may be to reduce the probablility of being eaten.  This seems to confirm that aggression occurs, sometimes leading to “cannibalism”, but the authors reiterate their belief that agonistic behaviour does not normally ocur in the field in H. crassicornis.  The authors conclude that Zack’s observations are just of mating behaviour, and not anything else.  Longley & Longley 1981 Veliger 24: 230; Longley & Longley 1981 Veliger 24: 232. Photograph courtesy Kevein Lee, Fullerton diverkevin.


Two Hermissenda crassicornis engaged
in precopulatory head-butting 1.5X


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photograph of Hermissenda crassicornis about to copulate taken from a video, courtesy Roger Longley CLICK HERE to see a video of Hermissenda crassicornis copulating. Video and descrptive headings courtesy Roger & Alison Longley, Friday Harbor Laboratories.
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Research study 7

A later study on mating and egg-mass production in Hermissenda crassicornis in Santa Cruz, California provides further detail on copulation and efficacy of sperm transfer.  First, the rapidity of the copulatory event (about 4sec on average) markedly decreases the chance of complete transfer of sperm.  In photograph of aeolid nudibranch Hermissenda crassicornis 37 videotaped sequences of attempted copulation (defined as 2 individuals with penises everted), almost half lead to failed sperm transfer in one or both individuals.  Interestingly, a frequent behaviour following sloppy sperm transfer is for an individual to twist its head backwards and consume all or part of the semen in the vicinity of the gonopore.  If an individual is allowed to become sperm-depleted in isolation and then allowed to copulate once, the sperm received at that copulation is apportioned such that even after a sixth egg mass is deposited (after about 4wk), 20% of the eggs are still fertile.  This strategy leads to great wastage of eggs and jelly mass.  An alternative strategy would be to use up all stored sperm in the first few layings, which would minimise wastage.  Although not discussed by the author, perhaps the “dribble” of fertility ensures at least some production of larvae over a longer period, and may therefore represent a kind of bet-hedging strategy until the next copulation occurs.  Rutowski 1983 Biol Bull 165: 276.

NOTE  defined by the author as producing an egg mass with less than 50% of fertile eggs

Hermissenda crassicornis showing
rhinophores and oral tentacles 2X

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