The association of argonauts with gelatinous plankton and other substrates

Abstract

With the growing development of recreational blackwater nocturnal diving around the world, a large number of images are shared by recreational divers on social media. These images provide a wealth of novel behavioral information of pelagic organisms rarely seen in their natural oceanic environment by scientific researchers. Here, we quantified for the first time the association between argonauts and other pelagic organisms, vegetal debris, and plastic waste they use as a substrate to move in the ocean, showing the usefulness of recreational diving and citizen science to increase scientific knowledge about oceanic organisms.

In the oceanic pelagic realm, many organisms live and interact during the diel vertical migration, which refers to a daily pattern of movement exhibited by many organisms, including planktonic species. During this migration, organisms move up toward the surface waters during the nighttime and return to deeper waters during the daytime, which represents the largest animal migration on Earth (Behrenfeld et al., 2019). The pelagic community involved in diel vertical migration includes larval fishes, crustaceans (such as copepods and krill), gelatinous plankton (like jellyfish and salps), cephalopods (like squids and octopods), and other invertebrates. Blackwater diving uses a series of underwater lights from a boat to attract these oceanic plankton during the nighttime (Bartick, 2022; Hegde et al., 2021; Milisen, 2020; Milisen et al., 2018; Nonaka et al., 2021; Pastana et al., 2022, 2023), and is usually performed from 5 to 30 m depth over bottom depths of 50–800 m (or more).

Among the most charismatic pelagic organisms seen by blackwater photographers are the argonauts or “paper nautilus,” a group of four species of octopods that spend their entire life cycle in the epipelagic zone (0–200 m depth) in subtropical and tropical waters of all oceans (Finn, 2013, 2018). A few opportunistic observations have showed argonauts associated with gelatinous plankton (Banas et al., 1982; Nesis, 1977) or preying upon them (Heeger et al., 1992). This association is difficult to prove using classical net-collected samples obtained during oceanographic cruises, as turbulence generated by the fishing net separates the animals or artificially entrains small animals within larger body cavities, and direct observations and sampling at sea have always been opportunistic (Rosa & Seibel, 2010). Direct observations with scuba have provided valuable information difficult to obtain by classical net samplings that has even changed concepts and knowledge about pelagic life and the relationships among organisms (Madin et al., 2013). This is particularly relevant for gelatinous plankton, which are undervalued by net sampling, making it very difficult to study their interaction with other organisms (Hamner et al., 1975). Here, we assemble global observations in the wild on this argonaut behavior obtained from 569 images collected around the world, mainly from Central Indo-Pacific (82%) and Tropical Atlantic (15%) during blackwater dives done by 171 recreational scuba divers and published in public websites and social networks, mainly from Instagram, which represented 89% of the observations. We selected underwater images where argonauts appeared attached to other organisms or floating structures in the wild. Images of argonauts swimming alone in the water column and not attached to any substrate were excluded from the analysis. These 569 selected images constituted 1% of the 55,100 images examined. Further methodological details are provided in Appendix S1: Section S1. This information allowed for the first time to quantify the diversity of substrates used by argonauts to move in the ocean. The images analyzed recorded the four extant species of argonauts: Argonauta argo, A. hians, A. nodosus, and A. nouryi, identified by the shells of subadult and adult females (Finn, 2013). The most photographed and identified species was A. hians females from Central Indo-Pacific area (30%), while unidentified Argonauta spp. represented 67% of total images.

Argonauts were attached to diverse substrates in the water column such as plastic waste (3%), vegetal debris (15%), and pelagic animals (82%). The last category comprised at least 44 taxa, including ctenophores, cnidarians, crustaceans, mollusks, thaliaceans, fishes, and conspecific individuals. The number and percentage of animal and inert substrates used by the argonauts from the images analyzed are included in Appendix S1: Table S1. Gelatinous plankton (salps, hydromedusae and scyphomedusae, jellyfishes, pyrosomes, and ctenophores) was the most abundant substrate used by argonauts, representing 73% of the total substrates selected to be attached. This preference for gelatinous plankton may be because it is more abundant than previously believed (Boero et al., 2008), providing a mobile substrate for many pelagic species (Gasca & Haddock, 2004). Argonauts exhibit extreme sexual dimorphism in size, and differences in substrate selection were detected according to argonaut sex and size. Subadult and adult females develop an external white shell (Figure 1a,b,f) used to brood the eggs. Until recently, the term “egg case” has been used instead of “shell” (Hoving et al., 2022). This shell is not homologous to the mollusk shell but an autapomorphy of Argonauta. Here, we prefer to use the term “shell,” following Finn and Norman (2010), as this study showed this thin calcareous structure also functions as a hydrostatic structure, employed by the female argonaut to precisely control buoyancy at varying depths. The most recent reviews on Argonauta also use the term shell (Finn, 2013, 2018). Males are dwarf, weighing 1/600th that of the largest female (Finn, 2013), never develop a shell, and can be recognized by the highly modified copulatory arm (Figure 1c,d,g). Images showed that small-sized argonauts such as males, juvenile females, and small unsexed individuals prefer mostly thaliaceans (36%) and hydromedusae (23%) as substrates, while subadult and adult females select inert substrates as plastic waste and vegetal debris (41%) and scyphomedusae (35%) (Appendix S1: Table S1).

Argonauts have a varied diet, feeding on gastropods, crustaceans, fishes, cephalopods, and jellyfishes (Heeger et al., 1992; Nesis, 1977; Okutani, 1960; Sukhsangchan et al., 2009). However, we concluded that direct predation is not the only reason for the association of argonauts with gelatinous plankton. In fact, most gelatinous plankton with attached argonauts showed perfect contour and were undamaged. Accompanying fauna sharing the same substrate with the argonauts was observed in 13% of the images analyzed, with the presence of amphipods (5%), unidentified crustaceans (4%), and fishes (4%) in addition to copepods, isopods, cirripeds, acari, and paralarvae of benthic octopus (Figure 1a) on the same substrates. This accompanying fauna is similar to the observed prey (Heeger et al., 1992; Nesis, 1977) and may suggest that argonauts also find food in the substrates they use as transport devices. In fact, commensal amphipods and other crustaceans are known to inhabit salps and other gelatinous organisms (Madin & Harbison, 1977), and hyperiid amphipods require association with these organisms to fully develop their life cycles (Laval, 1980; Madin et al., 2013). More than one argonaut sharing the same substrate or forming a chain were observed in 7% of the images, showing an incipient social character in these animals, rare in other octopods (Rosa & Seibel, 2010). In addition, mimetic coloration according with substrate can be observed in some of the images analyzed (see, e.g., Figure 1d,g–i). We suspect that transport, camouflage, predation, and perhaps defense are possible benefits for the argonauts associated with gelatinous plankton and other substrates, as observed in other argonautoids, including Haliphron (Hoving & Haddock, 2017; Hunt et al., 2019; Rosa et al., 2019) and Tremoctopus (Norman et al., 2002).

The images of underwater fauna available in social media are not a random sample of the fauna existing in the area because photographers select their images for different reasons such as beauty, photographic technique, and originality, among others. Even so, the information offered by these images can be scientifically relevant by showing biological or behavioral aspects previously unknown. The behavioral information reported here highlights the importance of the images obtained in situ by recreational scuba divers and shared in social media as a scientific resource. This information allows for the first time the characterization of the diversity of substrates that argonauts select as floating devices in the open ocean and their accompanying fauna. Indeed, in a hypothetical research project aimed at studying the associative behavior of argonauts, the sampling effort required to obtain the same information gathered here by 171 recreational scuba divers would have been tremendous, if not practically impossible. This result shows the value of citizen science in environmental and ecological sciences (Fraisl et al., 2022).

Photos of live gelatinous plankton and soft cephalopods in their habitat have complementary advantages over preserved material collected with conventional plankton nets, which are almost always damaged or distorted, with specimens shrunken and discolored after fixation. Therefore, a combination of live photos and preserved specimens can provide a more comprehensive understanding of habitat, behavior, and natural history of these groups of pelagic animals. Finally, the analyzed images have also proved useful in detecting the argonaut/marine litter association, particularly with plastic substrates, which highlights the adaptive plasticity of argonauts in the Anthropocene. Thus, the data collected through high-quality images obtained during blackwater dives offer a novel approach for scientific researchers to investigate the behavior and interactions of oceanic pelagic organisms.

Roger Villanueva conceptualized the study and was responsible for data gathering and analysis. Roger Villanueva and Fernando Ángel Fernández-Álvarez were responsible for cephalopod taxonomy and Josep-Maria Gili for cnidarian taxonomy. Roger Villanueva wrote the original draft of the manuscript and all authors reviewed and edited the manuscript.

The authors declare no conflicts of interest.