What goes on at night in the sex life of giant siphon limpets?


Fig. 1. Siphonaria gigas at Cabo Blanco Absolute Natural Reserve, Costa Rica, with these giant siphon limpets often occurring in pairs (upper right) and nocturnally laying egg masses (lower right), as studied in a similar protected seashore reserve in Panama by Schaefer et al. (2020 [link to article in current issue of IOB]). Schaefer and co-authors documented that S. gigas individuals in pairs were more successful, on average, in their reproduction, but those siphon limpets in pairs were not strictly monogamous. Photography by Kimberly García Méndez, used with permission.

As someone who has long been fascinated by limpets, whatever their size, I have often persuaded my students to consider studying one of the smaller of our many California limpet species, which can be incredibly common and likely engaged in important ecological and behavioral interactions, making up for their small stature. They are also normally overlooked by human and even shorebird foragers, and any experiments are unlikely to make a dent in their ubiquity. Earlier limpet investigators might have avoided them because small limpets can be notoriously difficult identify to species. Thanks to advances in technology, we can now either routinely sequence their DNA or employ other molecular approaches for identification and genetic comparisons, and can track individuals equipped with epoxied bee tags or more elaborate physiological recording devices. However, some mornings I wake up and wish that we had chosen to study one of our larger and easier to identify limpet species.

Some limpet species can attain impressively large body size, and these species seem to also have some of the most fascinating natural history. In California, limpets typically have separate sexes, but an exception is our large sex-changing and territorial owl limpet, Lottia gigantea. Owl limpets first mature as “satellite” males, ready at any time to take over the vigorously defended territory of a much larger female (Wright and Lindberg, 1982; Wright 1988). Large females are a lethal threat, but small males also stand to benefit if they are in her general vicinity when she free spawns, as owl limpets and their “true” limpet (Patellogastropoda) relatives typically do. Scutellastra mexicana is another even larger (in fact, the largest) patellogastropod limpet, whose maximum recorded shell length is 35 cm (13.8 inches). It manages to attain that size by its gardening of a patch of its home-depression real estate (Lindberg 2007). Today, it is restricted to some scattered islands off western Mexico and is threatened with extinction (Carballo et al. 2019).

A study in the current IOB issue by Jessica Schaefer and co-authors (2020) features another large bodied “limpet” grazer, Siphonaria gigas. These siphon limpets were studied at Smithsonian Tropical Research Institute’s (STRI’s) Punta Culebra Nature Center on a long peninsula off the Pacific entrance to the Panama Canal within mintues of Panama City, but fortunately their intertidal habitat is afforded protection from limpet poachers. I cannot speak from personal experience, but my understanding is that these giant siphon limpets were apparently good to eat, and especially larger ones were pretty much picked clean throughout most of their quite restricted Central American Pacific coast range. Whereever they are accessible to hungry collectors, who call them burgados or affectionately as pecho de niña, the giant-sized siphon limpets are a distant memory. My Costa Rican friend, Kimberly García-Méndez, who is a sea slug specialist currently studying as a graduate student near to me at Cal Poly Pomona, has kindly given me permission to include her images (Fig. 1) of the same species of giant siphon limpets and their egg masses, taken more than a decade ago Costa Rica’s Cabo Blanco Absolute Natural Reserve. Like Schaefer et al.’s (2020) study site in Panama, these protected reserves provide rare refugia where these giant siphon limpets are able to attain their normal adult size to reproduce as described in their fascinating study.

I am a fan of all of the many limpet-like groups of gastropod limpets, including the giant siphon limpets (Siphonariidae) studied by Schaefer et al. While only distantly related to “true” limpets, they have fooled many a non-limpet specialist because they have similar conical shells and a lifestyle of using their hardened teeth of their radula to scrape their scuzzy algal food off rocks. Yet siphon and patellogastropod limpets could not be more distantly related within gastropods. A cone- or cap-like “limpet” shell has evolved repeatedly within gastropods, and while in the deep ocean this might be a relatively low-investment strategy in comparison to more elaborate coiled shells (Vermeij 2016), the seashore loving patellogastropods and siphon limpets are not only subjected to all sorts of harsh environmental challenges on the rocky shores they normally inhabitat, but there seem to be no shortage of competitors and predators that are constant threats. Giant siphon limpets are highly tenacious on their excavated home scar during the day, and move about to feed or reproduce at night while being washed by the shifting tides.

Schaefer et al. have just revealed that the reproductive success of a pair of these shore grazers is more complex than a simple monogamous arrangement, and even so it apparently pays to pair up. Siphon limpets are more closely related (but still quite distant) to pulmonate snails and slugs, and their somewhat more distant sea slug kin such as sacoglossans, sea hares, and nudibranchs within heterobranch gastropods, most of which are simultaneous hermaphrodites (not sequential hermaphrodites as in owl limpets). As is generally true for heterobranchs, giant siphon limpets are simultaneous hermaphrodites with internal fertilization, known to form pairs of limpets on adjacent home scars close enough to touch shells (Lombardo et al. 2013), and one wonders what might go on late at night on a starlit night. The end results of these mutual copulations are neatly laid ribbons of egg masses that might be mistaken for the egg mass of their sea slug relatives. Various siphon limpet species hatch out of these jelly ribbons as planktonic feeding larvae, known as veligers. Other species emerge as creeping tiny juveniles, ready to graze. All this reproductive complexity is in contrast to the quite invariant usual free-spawning of patellogastropod limpets, with subsequent strictly non-feeding brief planktonic larval life. It seems a cruel twist of fate that “true” limpets will never experience internal fertilization.

The new study is based on Schaefer’s Masters research, which was earned in 2016 at the University of Hawaii, Manoa as mentored by genetics and snail wizard, Dr. Peter Marko. Her research was conducted at a different tropical location while visiting STRI in Panama. Schaefer has since gone on to pursue a Ph.D. at the University of California, Davis, but while in Panama she was introduced to the giant siphon limpets there by Dr. John Christy, STRI marine behavioral ecologist, and co-author on the earlier study (Lombardo et al. 2013). Many familiar animals form pairs in mating, but often this is associated with guarding of a nest of eggs. With no such guarding behavior, giant siphon limpets would be expected to have other adaptive advantages for pairing, and alternative possibilities are considered. Schaefer et al. investigated whether the paired limpets were truly more successful at reproducing than unpaired individuals. They were able to both quantify reproductive output and couple it to a new microsatellite-based paternity, contrasting paired versus unpaired individuals. They found support for greater average reproductive output of paired siphon limpets, even though their paternity tests revealed that some lurkers in the vicinity of a pair must have contributed sperm.

May the giant siphon limpets have many more nights to get out and about.
Douglas J. Eernisse is Professor of Biology at Cal State Fullerton, where he teaches field marine biology, biogeography, and other courses and enjoys research on chitons, limpets, and even some of their coiled relatives on occasion.

References

Carballo, Jose Luis, Benjamín Yáñez, Eric Bautista, Jesus Emilio Michel-Morfin, et al. 2019. Decimation of a population of the endangered species Scutellastra mexicana (Broderip and Sowerby, 1829) (Mollusca, Gastropoda) in the Marías Island (Eastern Ocean Pacific) Biosphere Reserve. Aquatic Conservation Marine and Freshwater Ecosystems DOI: 10.1002/aqc.3239

Lindberg, David R. 2007. Reproduction, ecology, and evolution of the Indo-Pacific limpet Scutellastra flexuosa. Bulletin of Marine Science 81: 219-234.

Schaefer, J. L. B., J. H. Christy, and Peter B. Marko. 2020. Multiple and extra-pair mating in a pair-Living hermaphrodite, the intertidal limpet Siphonaria gigas. Integrative Organismal Biology, current volume.

Vermeij, G. 2016. The limpet form in gastropods: Evolution, distribution, and implications for the comparative study of history. Biol. J. Linn. Soc. 120, 22–37. DOI: 10.1111/bij.12883

Wright, W. G. 1988. Sex change in the Mollusca. Trends Ecol. Evol. 3: 137-140.

Wright, W. G. and D. R. Lindberg. 1982. Direct observation of sex change in the patellacean limpet Lottia gigantea. J. Mar. Biol. Assoc. U.K. 62: 737-738.

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