Philippa Kaur

Parasites have frequently been observed on the gills of coleoid cephalopods during ROV dives in the mesopelagic waters of the Monterey Submarine Canyon. Here, we demonstrate that at least two parasite species can be distinguished from ROV-collected specimens. Based on morphology, the first parasite was identified as the protist Hochbergia cf. moroteuthensis. Although the original description of H. moroteuthensis struggled to assign a taxonomic rank, the authors noted that the presence of trichocysts and an apical pore bear similarities to those of dinoflagellates in an encysted life stage29,30. Using Sanger sequencing and dinoflagellate cyst-specific primers, we confirm this parasite to be a dinoflagellate that forms a sister group to members of the Oodinium genus. The second parasite could not be matched to any documented morphological descriptions, and DNA barcoding was only able to resolve a short sequence that does not provide for a reliable identification.Hochbergia moroteuthensis appears to be a common parasite of midwater cephalopods and has previously been collected off the gills of twenty cephalopod species29,30. These include five taxa investigated here (C. calyx, V. infernalis, Galiteuthis spp., Gonatus spp. and Japetella diaphana), with Taonius sp. new to the list. While H. cf. moroteuthensis found in this study was somewhat smaller than the type series (0.5–1.4 mm versus 1.19–1.99)30, it was within the range of those reported by McLean et al.29 on the squids Stigmatoteuthis dofleini Pfeffer, 1912 and Abralia trigonura Berry, 1913 (i.e. 0.56 to 1.10 mm on average in length)29. The latter authors noticed that parasite size, color (i.e. white to yellow) and thecal plate morphology may differ between host species, which could indicate multiple Hochbergia species. It should, however, be noted that it is unknown whether H. moroteuthensis maximum growth is dependent on host size or whether the investigated parasites were simply in different growth stages given the study’s relatively small samples sizes. Although we did not compare H. cf. moroteuthensis morphology across hosts in great detail, the partial 18S rRNA sequences obtained for parasites on Gonatus berryi and Chiroteuthis calyx were identical. Further research is therefore warranted to investigate species-specific parasite differences and speciation among hosts.The genetic relatedness between H. cf. moroteuthensis and its Oodinium sister group is further supported by several morphological features. First, the lack of distinct dinoflagellate characters, ovoid shape and the presence of trichocysts, have also been noted for Oodinium cysts41,42,43. McLean et al.29 further reported that the nucleus of the single-celled H. moroteuthensis cyst contains diffuse chromatin, a feature unlike most dinoflagellates that possess well-defined rod-like chromosomes42. Remarkably, dinoflagellates within Oodinium are known to alternate between both non-dinokaryotic and dinokaryotic nuclei within their life cycles, which could explain H. moroteuthensis’ diffuse chromatin42,43. Similarities between H. moroteuthensis and Oodinium further extend to the parasitic life style with primarily pelagic hosts. Dinoflagellates in the Oodinium genus are all known to be ectoparasitic, infecting ctenophores, chaetognaths, annelids, larvaceans and a hydromedusa41,43,44,45,46.In spite of these similarities, there are also several noteworthy morphological differences between H. moroteuthensis and members of the Oodinium genus. Young Oodinium cysts generally have a white to yellow coloring, with older cysts taking a yellow–brown or dark brown tint41,43,44. Oodinium cysts also possess relatively simple thecal plates and above all, have a distinct peduncle, or stalk, with which they attach to the host and which is thought to serve as feeding apparatus41,43,47. Maximum lengths for Oodinium cysts have been reported up to 0.39 mm43,46. In contrast, cysts in H. moroteuthensis possess a white to yellow coloring, an intricate pattern of triangular plates, reach sizes up to 1.99 mm long, and have a simple holdfast area with an oval aperture that likely anchors them to the host30. Currently, both Oodinium and Hochbergia form a genetically distinct clade within the Dinophyceae and analysis of further specimens and genetic markers might provide more insight into their relatedness and specialization on primarily pelagic hosts. Additionally, analysis of fast- and slow-evolving genetic markers might resolve the polytomy observed in the phylogenetic trees, which were also present in the phylogenetic reconstruction of the DINOREF reference database by Mordret et al.32.The genetic similarity of H. cf. moroteuthensis to an unidentified eukaryote from the water column and the fact that we encountered the protozoans in an encysted stage, strongly suggests that these dinoflagellates infect their cephalopod hosts through a free-living life stage. Many parasitic dinoflagellates, including Oodinium, alternate between a motile free-living stage—the dinospore—that forms a vegetative feeding stage—the trophont—upon attachment to the host41,47,48. During this vegetative stage, the trophont grows greatly in size but without cellular division. Once mature, the trophont detaches from the host to divide into multiple flagellated dinospores. The dinospores disperse into the water column, free to infect new hosts (Fig. 6)41,47,48.Figure 6Theorized life cycle of Hochbergia moroteuthensis. (a) The vegetative trophont (feeding life stage) grows without cellular division on the cephalopod’s gills. (b) The mature trophont detaches and (c) divides into motile dinospores, (d) free to infect new hosts in the water column. Illustration (b) trophont adapted from Shinn & McLean30.Full size imageSuch a free-living life stage is consistent with H. moroteuthensis’ wide geographic distribution. Free-living dinospores are easily dispersed by ocean currents, and observations in both the North Pacific Ocean and the Gulf of Mexico could indicate large-scale ocean connectivity, potentially beyond the distribution reported here29. This dispersal may also offer H. moroteuthensis a wide range of infection possibilities and explain why trophonts are found in twenty-one different cephalopod taxa. Nevertheless, population genetic structure needs to be investigated, as it is currently unknown if the parasites represent multiple species.Free-living dinospores might also explain H. moroteuthensis’ location on the exterior gill tissue. With dinospores free in the water column, the fastest pathway to a cephalopod’s interior is through ‘inhalation’. In this process, cephalopods actively force water through their gills, making these the first organs Hochbergia would encounter. Respiratory organs give direct access to the cephalopod’s blood stream, and therefore offer a suitable environment (i.e. nutrient and oxygen rich) for development into a trophont. Gills also provide interstices that could simply trap dinospores. Either way, there was only one occasion (i.e. out of 355) where trophonts were seen on other body parts besides the gills (Fig. 4e). In comparison, several Oodinium parasites are also known to attach to specific host-body parts, apparently preferring sites involved in locomotor movement. For instance, Oodinium jordani McLean & Nielsen, 1989 is known to attach to the fin of the chaetognath Sagitta elegans Verrill, 187346, while O. pouchetti is mostly found on the tail of appendicularians41, and Oodinium sp. collected off various ctenophores appears to prefer attachment close to or within the beating comb rows44. Whether these surface areas offer highest encounter rates or provide a physical benefit such as enhanced oxygenation remains unknown.The increased prevalence of H. cf. moroteuthensis observed in the most abundant cephalopod, Chiroteuthis, and in the other adult cephalopods is in line with infection dynamics known from other wildlife parasites, where the probability of a parasitic infection increases with host density and age49,50,51. Following this, dinospores in the Monterey Submarine Canyon have more opportunities to encounter common squids like Chiroteuthis52 and longer-lived cephalopods. Alternatively, it is possible that the increased parasite load in adults is simply the result of larger gill surface areas when compared to juveniles. However, when comparing prevalence between host species, it should be noted that the maximum adult sizes for C. calyx (up to 100 mm in mantle length, ML) are smaller than those of Galiteuthis (500 mm ML), Taonius (660 mm ML) and Japetella (144 mm ML) among specimens found in the Monterey Submarine Canyon53,54.Other factors that might explain the observed prevalence include parasite preferences for host physiology (e.g. respiration rates) or confinement to a certain depth range18. Although Chiroteuthis, Galiteuthis, Taonius and Japetella partially overlap in their depth distributions, Chiroteuthis generally remains above the core of the oxygen minimum zone, located around 700 m in Monterey Bay52,55. Galiteuthis, on the other hand, has a bimodal distribution, with older individuals known to migrate below the oxygen minimum core52,55,56. If dinospore viability is restricted to more shallow depths, the probability of infection for Galiteuthis could decrease when living at deeper depths. This is further supported by Taonius, which showed a comparable bimodal distribution to Galiteuthis52 and shared a similar parasite prevalence. Furthermore, Japetella is the deepest living cephalopod investigated and harbored relatively few Hochbergia trophonts. In spite of this, it is unknown how long it takes for H. moroteuthensis dinospores to develop into mature trophonts and over what time frames they may accumulate on their hosts. Lab-based experiments with Oodinium sp. on the ctenophore Beroe abyssicola Mortensen, 1927 showed that trophonts needed approximately 20 days to grow from 35 µm in length to their mature size of 350 µm at 10 °C44. Given that H. moroteuthensis can grow over five times larger and lives at colder temperatures depending on its host distribution, growth periods may be substantially longer.When looking at the prevalence of H. cf. moroteuthensis over time, only Taonius appeared to be showing an increase in infected individuals over the years. Present results, however, are insufficient to determine whether this increase is the result of environmental change or part of natural variability. We therefore recommend continued monitoring to determine long term trends. Based on the monthly prevalence, it is likely that Chiroteuthis acts as a reservoir for Hochbergia parasites throughout the year. Galiteuthis, Japetella and Taonius show more seasonal dynamics. It may be that the reported seasonality is related to upwelling events or environmental cues promoting dinospore formation (e.g. increasing temperatures)50. Alternatively, cephalopods might be more susceptible to infections in certain months, or have higher resistance in others. Taonius, for example, had a markedly lower parasite load on average than Galiteuthis despite similar prevalence estimates (Tables 1 and 2), potentially indicating some sort of resistance mechanism. More research is warranted to confirm any host resistance and the influence of depth or seasonal effects.The other parasite type found in ROV-collected specimens of Vampyroteuthis infernalis and Gonatus spp. needs further characterization. Although DNA barcoding was able to resolve a short sequence that potentially places it within the phylum Apicomplexa, it appears more likely that this genetic material originated from contamination with a different parasite. Apicomplexa reported in cephalopods generally infect the digestive tract and are morphologically different from the parasites observed here19.In conclusion, our findings highlight the need for further investigation of cephalopods and their gill parasites. Considering that parasites influence biodiversity and that cephalopods form key links in pelagic food webs, future research should be focused at assessing potential effects on cephalopod physiology. For example, if H. moroteuthensis limits longevity or reproduction in common squids like C. calyx, then changes in parasite abundance might result in cascading effects on abundance of Chiroteuthis’ prey, predators and competitors. Additionally, baseline estimates of parasite prevalence are crucial to fully understand whether midwater host-parasite systems are at risk from increasing anthropogenic stressors and how they will change over time. While ROV observations have proven key to estimate prevalence and infection intensity here, trawled specimens continue to be valuable for verification of parasite species and obtaining material for genetic analyses, even if slightly damaged. We therefore recommend combining ROV observations with periodic trawling in future studies, since ROVs may not reveal smaller parasites, early infections or parasites in animals with tissue that is not transparent. More

Australia’s tropical rainforests are some of the oldest in the world.Credit: Alexander Schenkin

The rate of tree dying in the old-growth tropical forests of northern Australia each year has doubled since the 1980s, and researchers say climate change is probably to blame.The findings, published today in Nature1, come from an extraordinary record of tree deaths catalogued at 24 sites in the tropical forests of northern Queensland over the past 49 years.“Trees are such long-living organisms that it really requires huge amounts of data to be able to detect changes in such rare events as the death of a tree,” says lead author David Bauman, a plant ecologist at the University of Oxford, UK. The sites were initially surveyed every two years, then every three to four years, he explains, and the analysis focused on 81 key species.Bauman and his team recorded that 2,305 of these trees have died since 1971. But they calculated that, from the mid-1980s, tree mortality risk increased from an average of 1% a year to 2% a year (See ‘Increasing death rate’).

Bauman says that trees help to slow global warming because they absorb carbon dioxide, so an increase in tree deaths reduces forests’ carbon-capturing ability. “Tropical forests are critical to climate change, but they’re also very vulnerable to it,” he explains.Climate changeThe study found that the rise in death rate occurred at the same time as a long-term trend of increases in the atmospheric vapour pressure deficit, which is the difference between the amount of water vapour that the atmosphere can hold and the amount of water it does hold at a given time. The higher the deficit, the more water trees lose through their leaves. “If the evaporative demand at the leaf level can’t be matched by water absorption in fine roots, it can lead to leaves wilting, whole branches dying and, if the stress is sustained, to tree death,” Bauman says.The researchers looked at other climate-related trends — including rising temperatures and an estimate of drought stress in soils — but they found that the drying atmosphere had the strongest effect. “What we show is that this increase [in tree mortality risk] also closely followed the increase in atmospheric water stress, or the drying power of air, which is a consequence of the temperature increase due to climate change,” Bauman explains.Of the 81 tree species that the team studied, 70% showed an increase in mortality risk over the study period, including the Moreton Bay chestnut (Castanospermum australe), white aspen (Medicosma fareana) and satin sycamore (Ceratopetalum succirubrum).The authors also saw differences in mortality in the same tree species across plots, depending on how high the atmospheric vapour pressure deficit was in each plot.“This is one data set where the trees have been monitored in reasonably good detail since the early ’70s, and this is a really top-notch analysis of it,” says Belinda Medlyn, an ecosystem scientist at University of Western Sydney, Australia.But she says that more experiments are needed to determine whether the vapour pressure deficit is the biggest climate-related contributor to the increase in tree deaths. More

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