Hapalochlaena (Blue Ring Octopuses)

Science Friday Cephalopod Week Article 2014 June 25

This story is part of SciFri's #CephalopodWeek. For more on these marine animals, check out the videos here.

The venomous cephalopod above has a bit of a reputation—of 280 described octopus species, it’s probably one of the deadliest to humans. It contains a type of neurotoxin throughout its body called tetrodotoxin (the same as what’s found in puffer fish), which causes paralysis in bite victims by disrupting communication between nerves and muscles. Unable to breathe, a sufferer can die.

Yet, while this particular species—a type of blue-ringed octopus called Hapalochlaena fasciata—has caused one known death in Australia, where the animal is found, it's generally a pacifist. “They are dangerous, and people need to be educated about them, but they're not out hunting humans or trying to bite us," says Julian Finn, senior curator of marine invertebrates at the Museum Victoria in Melbourne. He would know: “I've observed hundreds of blue-ringed octopus underwater, and none of them have ever tried to attack me; they've all been going about their business.” (The victim who died, back in 1967, had taken the octopus out of the water, according to Finn.)

Also known as a blue-lined octopus (for the cobalt streaks on its body that match the rings on its arms), H. fasciata is one of four described blue-ringed octopus species. Based on specimens collected throughout the Indo-Pacific, however, there are probably 15 more species that have yet to be named, according to Finn, who has been studying the group for three years.

Although H. fasciata is common along Australia's eastern coast, casual swimmers tend to overlook it because it’s typically camouflaged to blend into its surroundings, according to Finn. Like its well-studied brethren, it only seems to reveal its cool coloring when it’s threatened or angry—and it does so by relaxing its muscles to expose structures called iridophores, which reflect blue-green light. To enhance the effect, the cephalopod darkens the skin surrounding the iridophores, resulting in a dazzling iridescent blue pattern that probably best translates to “back off.”
Yet, blue-ringed octopuses like H. fasciata don’t seem anxious to wield the toxic bite advertised by their colorful bark. When hunting, for instance, they appear to rely more on stealth to attack prey, such as crabs, rather than immediately subduing it with venom (injected by biting), according to Finn. “They tend to just grab prey that they can handle, and they can handle it really quickly, and there's no indication that they're using their venom,” he says.

Aside from its seeming reluctance to wield poison, H. fasciata has another quirk: Males don't appear capable of distinguishing between sexes. “You would think that an animal, with such amazing ability of color change, would convey [their sex] to the other members of their population, but they don't,” Finn says. Mating thus becomes a bit of a crapshoot, with males lusting after both sexes. “They just have no clue when it comes to spotting the girls,” says Finn.

The mating process is even more theatrical given the fact that males also have a physical handicap, so to speak. In octopus species, males have a modified arm that they use to deliver a packet of sperm into a female’s oviducts, which are located in a space in her sack-like body called the mantle cavity (“essentially, he hands [the sperm] to her,” says Finn). In the well-studied blue-ringed octopus species, that reproductive arm is shorter than the other arms, which means that a male needs to grab onto a female in order to successfully insert the sperm. As a result, if a male H. fasciata mistakenly latches onto another male, “it’s not until he’s actually got his reproductive arm inside the mantle cavity [that] he goes, ‘Oop! Sorry—you're a bloke!’” says Finn. He then lets go of the embrace and keeps on trying until he gets it right.

The inability to discern among sexes has been observed in another species of blue-ringed octopus in an aquarium setting, but Finn has witnessed the behavior firsthand among H. fasciata in the wild. “They must have greater success just by grabbing every other blue-ringed octopus that goes past as opposed to wasting time trying to distinguish,” he says. “It must be working for them.”
 
Mating behaviour and postcopulatory fertilization patterns in the southern blue-ringed octopus, Hapalochlaena maculosa
Peter Morse, Christine L. Huffard, Mark G. Meekan, Mark I. Mccormick Kyall R. Zenger 2017 (Science Direct subscription)
Female octopuses are known to store sperm from multiple males they encounter throughout a breeding season, before laying a single clutch with mixed paternity. Although octopuses display a broad range of precopulatory behaviours, and both sperm competition and cryptic female choice have been hypothesized to occur, the current understanding of how these processes influence resulting paternity remains limited. This study aimed to identify behavioural factors associated with paternity patterns and the capacity of females to bias paternity postcopulation to specific males in the southern blue-ringed octopus, Hapalochlaena maculosa. Genetic markers and controlled, sequential, laboratory pairings of genotyped individuals were used to examine paternity patterns and compare them to relative signatures of male sperm remaining in female oviducal glands after egg laying. Multiple paternity was discovered in all 12 laboratory-reared clutches. There was no indication that the relative time spent in copulation affected the resulting paternity. Males that waited for females to terminate the copulation had greater paternity when they were the first candidate male, but this was not the case among second candidate males. The relative quantities of candidate male alleles detected in female oviducal glands after egg laying were consistent with relative paternity of the candidate males in all but three cases. In one of these, sibship analysis revealed that the male that obtained less paternity than expected was in fact the female's full-sibling brother. Although this study found no evidence for female postcopulatory selection of male sperm, anecdotal evidence suggests that female H. maculosa might benefit from polyandry if chemical processes can favour clutch fertilization by unrelated males. Future studies, investigating paternity bias among genotyped males of varying, but known relatedness to the female, might help to validate this pattern.
 
Genome-wide comparisons reveal a clinal species pattern within a holobenthic octopod—the Australian Southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)
Peter Morse, Shannon R. Kjeldsen, Mark G. Meekan, Mark I. Mccormick, Julian K. Finn, Christine L. Huffard, Kyall R. Zenge 2018 (Wiley Online, Ecology and Evolution Open access)

Abstract
The southern blue-ringed octopus, Hapalochlaena maculosa (Hoyle, 1883) lacks a planktonic dispersal phase, yet ranges across Australia's southern coastline. This species’ brief and holobenthic life history suggests gene flow might be limited, leaving distant populations prone to strong genetic divergence. This study used 17,523 genome-wide SNP loci to investigate genetic structuring and local adaptation patterns of H. maculosaamong eight sampling sites along its reported range. Within sites, interrelatedness was very high, consistent with the limited dispersal of this taxon. However, inbreeding coefficients were proportionally lower among sites where substructuring was not detected, suggesting H. maculosa might possess a mechanism for inbreeding avoidance. Genetic divergence was extremely high among all sites, with the greatest divergence observed between both ends of the distribution, Fremantle, WA, and Stanley, TAS. Genetic distances closely followed an isolation by geographic distance pattern. Outlier analyses revealed distinct selection signatures at all sites, with the strongest divergence reported between Fremantle and the other Western Australian sites. Phylogenetic reconstructions using the described sister taxon H. fasciata (Hoyle, 1886) further supported that the genetic divergence between distal H. maculosa sites in this study was equivalent to that of between established heterospecifics within this genus. However, it is advocated that taxonomic delineations within this species should be made with caution. These data indicate that H. maculosa forms a clinal species pattern across its geographic range, with gene flow present through allele sharing between adjacent populations. Morphological investigations are recommended for a robust resolution of the taxonomic identity and ecotype boundaries of this species.
 
Toxicity and Toxin Composition of the Greater BlueRinged Octopus Hapalochlaena lunulata from Ishigaki Island, Okinawa Prefecture, Japan
Manabu Asakawa, Takuya Matsumoto, Kohei Umezaki, Kyoichiro Kaneko, Ximiao Yu, Gloria Gomez-Delan, Satoshi Tomano, Tamao Noguchi, Susumu Ohtsuka MDPI Toxins 2019 (PDF attached)
 

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