Sperm consumption has been reported for the first time in female southern bottletail squid, and it looks like they’re using this nutrient-rich ejaculate to maintain steady egg production and healthy bodies.

Southern bottletail squid (Sepiadarium austrinum) are found in the shallow, coastal waters of southern Australia, and grow to only about 4 cm long. They spend their days buried in the sand, only coming out at night to feed on small crustaceans, and they’ll defend themselves by releasing a large amount of mucous at their predators.

"Nothing had been done on them before, with not a single scientific paper in the literature," says Benjamin Wegener from Monash University in Melbourne, lead author of a Biology Letters paper published today about the mating habits of this tiny, translucent species. "Given we were starting from scratch, I decided the best way to get a handle on their reproductive behaviour was to put a male and female together and see if they mate. The male immediately grabbed the female and they went for it."

Eschewing any obvious form of courtship, southern bottletail squid will mate head to head, the male depositing sperm packages called spermatophores onto the female's buccal cavity - an external, fleshy pouch located just below the mouth. The female will then extract mature eggs from her mantle and pass them against the stored spermatophores before depositing them, now fertilised, at the base of seagrasses, seaweeds or rock crevices. The females can store spermatophores in their buccal cavities for up to three weeks after an encounter with a male. They'll also scrape a number of these spermatophores off the buccal cavity membrane and eat them.

Late last year, Wegener and his colleagues discovered that small females consumed significantly more spermatophores than the large ones, and the males showed a distinct preference for the large females. This could be one of a series of possible strategies used by both the males and the females to influence the paternity of the offspring, they suggested, because by choosing the larger females that consume less spermatophores, the males are effectively lessening this threat to their potential offspring.

But the researchers also found that this preference for larger females didn’t influence the males to impart any less of their spermatophore stores to the smaller, ‘hungrier’ females, and this suggested that by eating spermatophores, the smaller females might be able to produce higher numbers of healthier offspring than they could otherwise manage.

To test this, the team, which included evolutionary biologist Devi Stuart-Fox from the University of Melbourne and Mark Norman from Museum Victoria, observed the mating habits of 51 southern bottletail squid collected in Port Phillip Bay. The males were fed radioactive amphipods (small shrimp-like crustaceans) until they reached sexual maturity, at which point they started to produce radioactive spermatophores. When the females ate the spermatophores, and all of them did, the researchers could trace the radioactivity levels to see how they had been incorporated around the body to deliver nutrients to various tissues and unfertilised eggs. "Even though Mark had mentioned that [spermatophore consumption] might be a possibility, actually seeing something for the first time, and realising you’re probably the first person in the world to have actually done so… that was pretty special," says Wegener.

The experiments also revealed more about how a complex battle over paternity was being waged between the males and the females. The males could attempt to scoop a rival's spermatophores out of the female's buccal cavity and replace it with his own, and they appear to minimise spermatophore consumption by strategically depositing their ejaculates in an area of the female's buccal cavity that she couldn't reach - "prime real estate", says Wegener - near the base of the beak. This was confirmed by the presence of numerous spermatophores lining the base of the beak when the females were dissected within three weeks of mating.

They also appear to know that it is advantageous to mate with a female that is closest to being in an egg-laying condition, because if she's not, they could be unwittingly helping a rival to produce offspring instead. "These females are using the nutrients from males to develop her unfertilised eggs," says Wegener. "If she doesn't lay eggs soon after mating, the males could completely miss out on fertilising her eggs, and instead act as a contributor to the next male that comes along."

There is also the potential for some female control in the paternity of her offspring after copulation, with the possibility that she is selectively eating the spermatophores of less desirable mates and saving those of the more attractive ones, in a similar manner to the way male gulf pipefish selectively abort the embryos of unattractive females to consume their nutrients, but this has yet to be explored. What Wegener is now working on is the possibility that the males are taking advantage of any opportunity to rid themselves of lower quality spermatophores, which would help to explain why they deposit the majority of their spermatophore stores with each sexual encounter, regardless of how much of it is likely to be eaten by his mate.

Papers cited:

Benjamin J. Wegener, Devi Stuart-Fox, Mark D. Norman and Bob B. M. Wong (2013). Spermatophore consumption in a cephalopod

Biology Letters

Wegener, B., Stuart-Fox, D., Norman, M., & Wong, B. (2013). Strategic male mate choice minimizes ejaculate consumption Behavioral Ecology, 24 (3), 668-671 DOI: 10.1093/beheco/ars216


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