The love lives of lone limpets may be lackluster, but limpets in pairs are luckier in love. A new study conducted by researchers at the Smithsonian Tropical Research Institute and the University of Hawaiʻi at Mānoa revealed that lowly limpets have fascinating mating behavior!

You may have seen its hat-shaped shell at the beach, but what exactly is a limpet? Limpets are marine gastropods (the group of animals that includes snails and slugs) with conical shells. They are commonly found along rocky coasts worldwide, from tropical shores to temperate areas such as California. Limpets eat by scraping algae and microorganisms off the rocks with a specialized tongue structure called a radula while they crawl around on their foot, the muscular organ under the shell, which they use to scoot along like a snail.

The study by Schaefer et al. features a particularly large and charismatic species of limpet: Siphonaria gigas, the giant siphon limpet. This organism can reach up to 8 cm in shell length. Like many gastropods, S. gigas are hermaphrodites—that is, each individual contains male and female reproductive organs and can produce both eggs and sperm. This means that for hermaphrodites, every individual encountered is a potential mate.

However, mating in S. gigas is not so simple as sidling up to their nearest neighbor and exchanging gametes. Each limpet spends most of its time on its home scar, a particular spot on the rocks that acts like a home base for that individual. Limpets are mobile and move around to feed and mate, but they always return to their home scar. A previous study on S. gigas found that rather than spacing themselves out evenly or forming their scars at random locations like some other gastropods, Siphonaria gigas tend to form home scars in pairs [1]. A pair of S. gigas is usually so tight that their shells touch when both limpets are on their home scars (pictured below). This pattern in itself is intriguing—but why does this species of limpet live in pairs and not others?

Paired limpets on their home scars at Punta Culebra, Panama. Limpets tend to form their scars along crevices in the rocks. White scale bars indicate 5 cm. Photos by John Christy and Jessica Schaefer.

Schaefer et al. suggest the spatial pairing of S. gigas may be related to reproduction. Because the limpets don’t move very often or very far, leaving their scars only when the tide falls and the rocks are moist, their access to potential mates is limited. Perhaps pairing is one way to ensure they always have a partner in foot’s reach to pass and receive sperm.

S. gigas mate by raising their shells and overlapping their reproductive organs to pass sperm from one to the other. Photo by John Christy.

To test this idea and investigate the connection between pair-living and reproduction, Schaefer et al. conducted a study of S. gigas in the Punta Culebra Nature Reserve at a rocky intertidal site near the Pacific entrance to the Panama Canal. First, researchers marked the animals by gluing ID tags to their shells. Then, they tracked the behavior of the limpets over 2.5 months and recorded their movements, mating habits, and production of egg masses (pictured below). They also collected samples from the adult limpets and their eggs to conduct a DNA analysis of parentage. The goal was to determine if limpets living in pairs mate exclusively with each other, or alternatively, whether paired limpets produce eggs fertilized by limpets other than their social partner (i.e., the limpet they live next to). A small proportion of S. gigas are solitary, lacking a social partner, but they can still produce egg masses. So, in addition to paired limpets, the authors monitored mating of solitary limpets and tested the parentage of their offspring. Without a long-term partner right next door, with whom do solitary S. gigas mate, and do they obtain sperm from just one or several individuals to fertilize their eggs?

Left: the study was conducted at the Smithsonian Tropical Research Institute’s Punta Culebra Nature Center on the Pacific coast of Panama (inset graph shows zoomed out view). Right: S. gigas inhabit the rocky intertidal zone, the area along the coast that is exposed to the air during low tide (as pictured here) but submerged in water at high tide. Photo by Jessica Schaefer.

The study found that there was a connection between pairing and reproductive success: paired limpets mated more often and produced almost twice as many clutches of eggs as solitary limpets. This difference in reproductive output suggests that paired limpets, without needing to look far for a mate, have ample opportunity to mate and produce offspring, while solo limpets may struggle finding a partner to fertilize their eggs.

After mating and receiving sperm to fertilize their eggs, S. gigas produce a spiral-shaped egg mass—a coiled ribbon of gelatin-like substance containing tens of thousands of tiny embryos! The limpet embryos develop for about 8 days, then hatch into swimming larvae that live in the ocean for several weeks before they return and settle on the shore. White scale bar indicates 5 cm. Photo by John Christy.

However, there is more to the story.  Genetic parentage analysis of limpet eggs revealed that paired limpets were not strictly monogamous: 3 out of every 16 egg masses showed evidence of multiple paternity, meaning more than one limpet contributed sperm to a single batch of eggs. In addition, extra-pair paternity was detected in at least three egg masses, meaning that some of the eggs in those masses were fertilized by a limpet other than the social partner of the limpet that produced the egg mass. Such patterns are actually quite common in marine gastropods; for example, in whelks (a type of marine snail), more than a dozen different fathers may fertilize one batch of eggs [2]!

Total number of egg masses produced by paired and solitary S. gigas over 2.5 months. Limpets living with a partner produced almost twice as many egg masses as solitary limpets on average. Graph provided by Jessica Schaefer.

Even if pairing in S. gigas is an adaptation to enhance reproduction, as the study suggests, questions remain . . . for example, if mate access is the key factor driving pair formation, why don’t limpets form home scars in groups larger than two, giving them more opportunities to mate? According to Schaefer et al., one possible answer is that many large limpets living in close proximity would face intense competition for food in the harsh intertidal habitat where they live. Intriguingly, the researchers observed limpets occasionally change the location of their home scar and swap partners! Just like animals such as birds and mammals that look for specific qualities in a mate, limpets might prefer certain characteristics in a partner, causing them to switch locations and pair with more attractive individuals. The drivers of these spatial and social dynamics in S. gigas are unknown, but future studies may unravel more mysteries of these capricious coastal creatures.

Limpets occasionally change the location of their home scar and even switch partners. The limpets marked 53 and 54 were initially paired, and limpet 27 was initially solitary. This photo shows all limpets sitting on their new home scars after limpets 27 and 53 switched locations as indicated by the arrow. Photo by Jessica Schaefer.

---

For more information:

*Schaefer, J. L., Christy, J. H., Marko, P. B. (2020). Multiple and extra-pair mating in a simultaneous hermaphrodite, the intertidal limpet Siphonaria gigas. Integrative Organismal Biology 2(1), 1–15. https://doi.org/10.1093/iob/obaa013

*Stars denote UC Davis Animal Behavior Graduate Group affiliated authors

References

1. Lombardo, R. C., Christy, J. H., & Cipriani, R. (2013). The false limpet Siphonaria gigas, a simultaneous hermaphrodite, lives in pairs in rock fissures on the Pacific coast of Panama. Marine Biology 160, 729–735. https://doi.org/10.1007/s00227-012-2127-y
2. Kamel, S. J., *Grosberg, R. K. (2012). Exclusive male care despite extreme female promiscuity and low paternity in a marine snail. Ecology Letters 15, 1167–1173. https://doi.org/10.1111/j.1461-0248.2012.01841.x

[Edited by: Alexandra McInturf]