Valentine’s Day: The Weirdest Love Rituals in The Animal Kingdom

If the animal kingdom is anything to go by, love is, indeed, a many-splendored thing. We humans may have slightly over-complicated the process, with our penchant for ever-changing hairstyles and a plethora of complex mating rituals, including, for better or worse, Valentine’s Day.

But we’re not the only animals who take the business of making love very, very seriously.

Put a ring on it
In 1995, Japanese divers spotted ‘mystery circles’ on the ocean floor that turned out to be the handiwork of the male pufferfish in the Torquigener genus. Female pufferfish, it seems, appreciate artistic gestures when it comes to romance.

The male pufferfish digs a complex pattern of valleys and peaks in a circle, and decorates the peaks with fragments of shell. The final product is certainly impressive: A ring of intricate sandy markings encircles the middle patch of fine sand, perfect for laying eggs in.

Evolution Made Love Weird, And These Animal Courtship Rituals Prove It
The male pufferfish gets points for creativity and effort. (Kawase et al., Scientific Reports, 2013)
«The circular structure not only influences female mate choice but also functions to gather fine sand particles in nests, which are important in female mate choice,» scientists explained in a 2013 paper describing the discovery.

It takes the fish about seven to nine days to construct this throne for his queen, but after mating, the elaborate artwork is left abandoned, with males starting entirely from scratch each time.

I’ve got you under my skin
The male deep-sea anglerfish (Ceratioidei) knows that when he finds a decent woman in the vast and dark pelagic zone, he’d better hold on tight.

He’s very small compared to his sexual counterpart, and lacks the signature light-up lure which the female fish uses to attract and eat her prey. His whole MO, therefore, is sniffing out a large, luminous lady, to whom he clings with his small, sharp teeth – in some species, becoming permanently fused to her side.

The female receives a lifetime’s supply of sperm in exchange for doling out crumbs to her suitors (she usually collects quite a few hungry little males in her travels). Co-dependent, much?

Arrow shows a 23.5-millimeter male fused onto a female anglerfish. (Edith A. Widder)
Arrow shows a 23.5-millimeter male fused onto a female anglerfish. (Edith A. Widder)
A token of my gratitude
Female argonauts are similarly gigantic compared to their male counterparts: they can grow to more than 20 centimeters, whereas males only reach a meager two centimeters.

What they lack in size, these cephalopod gentlemen make up for with their hectocotylus, a fully-detachable arm used to deliver sperm to the formidable females from a safe distance.

nine photos show a disembodied, white, tentacle-like hectocotylus in different positions around a paper argonaut brood shell
The disembodied hectocotylus on its doomed mission to fertilize some eggs. (Battaglia et al., The European Zoological Journal, 2021)
Scientists found one of these ‘detachable penises’, still alive and fully mobile even after seven hours without water, wriggling around inside an empty brood case that had washed up on a beach in Sicily. Even after the scientists removed it from the case, it found its way back, perhaps in search of shelter or eggs to fertilize. Now that’s dedication.

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Sweet little lies
In certain spider species, it is customary for male suitors to offer their female of interest a ‘nuptial gift’, a kind of spider dowry, usually in the form of a silk-wrapped fly or other delicious treat. The gift is meant to impress the female sufficiently that she decides not to eat him.

However, the bridal gift spider (Pisaura mirabilis), literally named for its gift-giving tendencies, isn’t always as generous as it may seem. One study showed males sometimes give their mates a decoy gift: the empty exoskeleton of an insect, or an inedible part of a plant.

This deception is successful enough that it’s persisted through spider evolution. But it’s not ideal: The females wise up to the ploy pretty quickly, ending mating prematurely. This shorter mating reduces sperm transfer and the trickster’s reproductive success compared to males who offer bona-fide gifts.