Biodiversity Data Journal :
Taxonomic Paper
|
Corresponding author: Gerlien Verhaegen (gerlienverhaegen@hotmail.com)
Academic editor: Yasen Mutafchiev
Received: 29 May 2021 | Accepted: 03 Aug 2021 | Published: 16 Aug 2021
© 2021 Gerlien Verhaegen, Emiliano Cimoli, Dhugal Lindsay
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Verhaegen G, Cimoli E, Lindsay D (2021) Life beneath the ice: jellyfish and ctenophores from the Ross Sea, Antarctica, with an image-based training set for machine learning. Biodiversity Data Journal 9: e69374. https://doi.org/10.3897/BDJ.9.e69374
|
Southern Ocean ecosystems are currently experiencing increased environmental changes and anthropogenic pressures, urging scientists to report on their biodiversity and biogeography. Two major taxonomically diverse and trophically important gelatinous zooplankton groups that have, however, stayed largely understudied until now are the cnidarian jellyfish and ctenophores. This data scarcity is predominantly due to many of these fragile, soft-bodied organisms being easily fragmented and/or destroyed with traditional net sampling methods. Progress in alternative survey methods including, for instance, optics-based methods is slowly starting to overcome these obstacles. As video annotation by human observers is both time-consuming and financially costly, machine-learning techniques should be developed for the analysis of in situ /in aqua image-based datasets. This requires taxonomically accurate training sets for correct species identification and the present paper is the first to provide such data.
In this study, we twice conducted three week-long in situ optics-based surveys of jellyfish and ctenophores found under the ice in the McMurdo Sound, Antarctica. Our study constitutes the first optics-based survey of gelatinous zooplankton in the Ross Sea and the first study to use in situ / in aqua observations to describe taxonomic and some trophic and behavioural characteristics of gelatinous zooplankton from the Southern Ocean. Despite the small geographic and temporal scales of our study, we provided new undescribed morphological traits for all observed gelatinous zooplankton species (eight cnidarian and four ctenophore species). Three ctenophores and one leptomedusa likely represent undescribed species. Furthermore, along with the photography and videography, we prepared a Common Objects in Context (COCO) dataset, so that this study is the first to provide a taxonomist-ratified image training set for future machine-learning algorithm development concerning Southern Ocean gelatinous zooplankton species.
Southern Ocean, gelatinous zooplankton, siphonophore, video annotation, remotely-operated vehicle (ROV), Common Objects in Context (COCO), machine learning
Southern Ocean ecosystems have experienced increasing environmental changes over the last decades (
Gelatinous zooplankton, comprising jellyfish, ctenophores and chordate tunicates (
Recently, the drawbacks in the collection and identification of gelatinous zooplankton have slowly started to be overcome through progress in methodologies using, for instance, molecular tools (e.g. metabarcoding, environmental DNA:
Surveys of gelatinous zooplankton in the Southern Ocean flourished in the late 19th and early 20th centuries. These surveys were conducted during famous expeditions, such as the Gauss expedition 1901–1903 (that is the first German expedition to Antarctica, also known as the “Deutsche Südpolar-Expedition 1901–1903”) (e.g.
Reports employing alternative survey methods for gelatinous zooplankton in the Southern Ocean, such as genetics or optics-based surveys, are few. For instance, sequences suitable for DNA barcoding remain rare, especially at species-level taxonomic resolution, with the notable exceptions of some siphonophore species (e.g.
Imagery and video data of under-ice gelatinous zooplankton were acquired at Cape Evans (McMurdo Sound, Ross Sea) over two different field campaigns conducted during the period of November-December 2018 and 2019 (Antarctic summer). A field camp was established for a duration of 3 weeks for each campaign, and was located approximately 200 m from the coast on Antarctic fast-ice (77.637° S, 166.401°E) (Fig.
For both campaigns, a large 2 × 1.8 m ice-hole was made through a combination of 6” Jiffy auger holes and hot-water drilling (Fig.
Underwater footage of the entire study area was conducted using two different Remotely Operated Vehicles (ROVs), equipped with a GoPro Hero 5; a Seabotix LBV-300 ROV (Teledyne Marine, California, USA) for the 2018 campaign and a BlueROV2 (Blue Robotics, California, USA) for the 2019 campaign. Additional underwater footage straight beneath the ice hole was acquired using Boxfish 360’s three large Micro Four Thirds cameras (Boxfish Research Limited, Auckland, New Zealand) deployed at different depths of the water columns using a weighted rope.
The raw, untreated images and videos were used to build online datasets (see "Data resources" section). The brightness and contrast of the images to build the plates (Figs. 2-19) were sometimes altered to reveal underlying morphological structures. The Common Objects in Context (COCO) dataset was generated by annotating the specimens in the images and videos using the free, open source, Computer Vision Annotation Tool (CVAT) (https://github.com/openvinotoolkit/cvat). COCO is a large-scale object detection, segmentation and captioning dataset. It is the most popular type of dataset used for training deep learning programmes.
The occurence data reported in this paper are deposited at GBIF, the Global Biodiversity Information Facility, http://ipt.pensoft.net/resource?r=life_beneath_the_ice-jellyfish_and_ctenophores_from_the_ross_sea_antarctica&. The raw, untreated images and videos are available at http://morphobank.org/permalink/?P3993 and https://www.youtube.com/playlist?list=PL5Njywnb4yMJQa7koLOM3BhjKU7Ii2HiZ, respectively. The COCO datasets can be found on https://zenodo.org/ with the following DOI:10.5281/zenodo.5118013.
Southern Ocean, in the McMurdo Sound (
Original description after
Koellikerina maasi. A, B. Drawing from the original species description by
Additional information from specimens from the Southern Ocean: from Gauss Station (0-385 m depth) (
Additional information on specimens identified as same species from outside the Southern Ocean: from west coast of Madagascar (
Literature giving diagnostic characters without describing new specimens:
Description and comments on observed material (Fig.
New undescribed characteristics: Ex-umbrella not smooth, showing small concavities and warts; the radial canals departing from the manubrium bend downwards, extending over four small perradial mesogleal convexities with ovoid yellowish nodules, before bending back up again to run over the ectodermal cavity of the sub-umbrella to the bell rim. These perradial mesogleal convexities are similar to those seen in the Leptothecate medusa Modeeria rotunda Quoy & Gaimard, 1827 (
Characteristics differing from previous descriptions: mesogleal thickness between the ex- and sub-umbrella on the top of the bell ca. one fourth of the height of the ex-umbrella, similar to the drawing of the New Zealand specimen of
Southern Ocean, in the McMurdo Sound [described by Browne (1910) as a juvenile Perigonimus sp. according to
Original description after
Leuckartiara brownei. A. Line drawing of the holotype (bell height 10 mm) (
Additional information on specimens identified as same species from outside the Southern Ocean: from the Mediterranean Sea (
Literature giving diagnostic characters without describing new specimens:
Description of and comments on observed material (Fig.
Cosmopolitan (
Original description after
Solmundella bitentaculata. A. Drawing from the original description as Carybdea bitentaculata from Indonesia (
Additional information from specimens from the Southern Ocean: There is currently only one species of Solmundella, though historically they were long dissociated into the species S. bitentaculata (Quoy & Gaimard, 1833) and S. mediterranea (Müller, 1851), which were subsequently synonymised (
Additional information from specimens from outside the Southern Ocean: Solmundella bitentaculata is a cosmopolitan species, which may actually be composed of multiple cryptic species (
Characteristics of the observed material differing with previous descriptions (Fig.
Description of and comments on observed material: N = 1 in 2019 (Fig.
Description of and comments on observed material: N = 1 in 2019 (Fig.
Antarctica: Ross Sea from under the ice (
Original description after
Pyrostephos vanhoeffeni. Drawing from the original account by
Description after
Description of and comments on observed material (Fig.
Southern Ocean: off Anvers Island, Antarctic Peninsula (
Original description after
Juvenile Diplulmaris antarctica. A. Drawing from the original description (modified from
Adult Diplulmaris antarctica. A. Drawing from the original description by
Additional information from specimens from the Southern Ocean: from Gauss Station as Ulmaropsis drygalskii (
Additional information from specimens from outside the Southern Ocean: to our knowledge, no specimens have been described outside the Southern Ocean. The records from Madagascar (
Comments on observed material: N = 3 in 2019 [two juveniles (Fig.
Description of the genus Beroe: sac-like bodies without tentacles or tentacle sheaths, very large mouth and stomodaeum, eight meridional canals, connected orally and a row of branched papillae in a figure of eight at the aboral pole (
Morphological characteristics of Beroe species that have been reported for the Southern Ocean (the compared characters were chosen, based on those that were evident in our filmed specimens).
Species |
Body length (L) adults (mm) |
Body shape |
Comb row length vs. body length adult |
Inter-comb plate distance |
Branching from meridional canals |
Colour |
Illustration |
Type locality |
B. compacta Moser, 1909 |
2.5 |
cylindrical |
whole body length (based on drawing) |
short |
/ |
opaque, shimmering yellowish between white comb rows |
Fig. |
Gauss Station, Antarctica |
B. cucumis Fabricius, 1780 |
/ |
oblong shape, elongated towards the extremities |
whole body length |
/ |
/ |
whitish with pink/red dots |
/ |
Greenland |
B. ovatus Bosc, 1802 |
/ |
oval |
whole body length (based on drawing) |
same as comb plate width (based on drawing) |
/ |
transparent with nine uncoloured comb rows |
Fig. |
“all seas” |
B. ovata sensu Chun, 1880 |
< 160 |
body elongated, cylindrical, not very noticeably compressed, gradually tapering towards the aboral pole in a semicircular arc |
3/4 (based on drawing) |
short (space between three comb plates ca. equal to width of comb plate, based on drawing) |
numerous diverticula, no anastomoses |
young transparent; adults during period of increased reproduction pink or bright red, otherwise unpigmented, grey-white or light transparent red |
Fig. |
Gulf of Naples, Mediterranean Sea |
B. ovata sensu Mayer, 1912 |
70-115 |
mitre-shaped with lateral compression very marked and mouth a wide-gaping slit |
3/4 (1/2 in juveniles) |
wide (space between two comb plates ca. equal to width of comb plate, based on drawing) |
loose network of numerous diverticula with few anastomoses |
dull-milky (in Florida) to highly coloured, with deep pink or reddish-brown canals (in northern waters as in Chesapeake Bay) |
Fig. |
Atlantic Coast of North America |
Beroe sp. A |
/ |
oval (body length ca. 2.4 times body width) |
ca. 2/3 of body length |
short (space between four comb plates ca. equal to width of comb plate) |
diverticula without anastomoses |
brownish-orange stomodeum and diverticula |
Fig. |
Mc Murdo Sound, this study |
Beroe sp. B |
ca. 35 |
oval (body length ca. 1.5 times body width) |
ca. 1/4 of body length |
short (space between 5 comb plates ca. equal to width of comb plate) |
no diverticula |
transparent to milky white |
Fig. |
Mc Murdo Sound, this study |
Beroe species recorded from the Southern Ocean
A similar brownish-orange undescribed Beroe species has been observed in Antarctica, in the Ross Sea (
Specimens of Beroe sp. A observed in the Ross Sea. a-c and e-f photos courtesy: E. Cimoli; d photo courtesy: Shawn Harper.
Description of and comments on observed material (Fig.
First reported observation.
Description of and comments on observed material: N = 1 in 2019 (Fig.
Antarctica: Ross Sea [photographed by ©Shawn Harper in
Original description after Moser (1909) (Fig.
Callianira cristata. A-B. Drawing from the original description (specimen length 12 mm) (modified from
Description and comments of observed material: N = 1 in 2019 (Fig.
first time observation.
Description of the family Mertensiidae: according to the key to Ctenophora by
Comments on observed material: N = 4 in 2018 and N = 2 in 2019 (Fig.
Mertensiidae sp. A. Lateral views (A-D), oral view (E) and aboral view (F) of specimens observed on 27/11/2018 (MCMEC2018_Mertensiidae_sp_A_c) (A) and 15/11/2019 (MCMEC2019_Mertensiidae_sp_A_a) (B-F). Abbreviations: ad-c., adradial canal; a.p., anal pore; c.g., ciliary grove; m., mouth; o.t.s.o., oral end opening of tentacle sheath; p.p., polar plate; s. o., tentacle sheath opening; st., statocyst; ss-cr., substomodeal comb row; st-cr., subtentacular comb row; t.b., tentacle bulb. C-H photos courtesy: E. Cimoli.
Mollusca was the third most-observed phylum (20% of all observations): Clione limacina antarctica (N = 2 in 2018, N = 1 in 2019) (Fig.
A total of 49 individuals were observed during the summer of 2018 (N = 25) and 2019 (N = 24). The majority of observed specimens belonged either to the phylum Cnidaria (36.7%) or Ctenophora (30.6%), whereas the remaining observed phyla, namely Mollusca (22.4%), Arthropoda (8.1%) and Annelida (2.0%), were less represented. The observed species are summarised in Table
Phylum |
Taxa |
Species |
N (2018) |
N (2019) |
First time report for the Ross sea? |
Figures |
|
Cnidaria |
Hydrozoa (class) |
Anthoathecata (order) |
Koellikerina maasi |
2 |
1 |
no |
Fig. 2 |
Leuckartiara brownei |
2 |
1 |
no |
Fig. 3 |
|||
Leptothecata (order) |
Leptomedusa sp. A |
0 |
1 |
yes |
Fig. 5 |
||
Leptomedusa sp. B |
0 |
1 |
no (if our proposed species assignment is correct) |
Fig. 6 |
|||
Narcomedusae (order) |
Solmundella bitentaculata |
1 |
0 |
no |
Fig. 4 |
||
Siphonophorae (order) |
Pyrostephos vanhoeffeni |
4 |
2 |
no |
Fig. 7 |
||
Scyphozoa (class) |
Semaeostomeae (order) |
Diplulmaris antarctica |
0 |
3 |
no |
Figs. 8-9 |
|
Ctenophora |
Beroida (order) |
Beroe sp. A |
3 |
4 |
yes (previously only images erroneously assigned to Beroe cucumis were published, online) |
Fig. 10 |
|
Beroe sp. B |
0 |
1 |
yes |
Fig. 11 |
|||
Cydippida (order) |
Callianira cristata |
0 |
1 |
yes (previously only images assigned to Mertensiidae were published, online) |
Fig. 12 |
||
Mertensiidae sp. A |
4 |
2 |
yes |
Fig. 13 |
|||
Mollusca |
Pteropoda (order) |
Clione limacina antarctica |
2 |
1 |
no |
Fig. 14 |
|
Spongiobranchaea australis |
1 |
0 |
no |
Fig. 15 |
|||
Limacina helicina antarctica |
0 |
2 |
NA |
Fig. 16 |
|||
incertae sedis |
Gastropoda larvae |
3 |
2 |
NA |
Fig. 17 |
||
Arthropoda |
Amphipoda (order) |
Eusiridae |
3 |
1 |
NA |
Fig. 18 |
|
Annelida |
Polychaeta (class) |
Syllidae |
0 |
1 |
NA |
Fig. 19 |
|
Total |
25 |
24 |
In this study, we conducted an in situ /in aqua optical survey of gelatinous zooplankton from under the ice in the McMurdo Sound, Antarctica. Our study represents the first formal optics-based survey of gelatinous zooplankton in the Ross Sea and the first study to use in situ /in aqua observations to describe taxonomic and a few trophic and behavioural characteristics of gelatinous zooplankton from the Southern Ocean. The Ross Sea has seen numerous net sampling surveys of gelatinous zooplankton in the past (e.g.
Our study demonstrates how valuable optical in situ observations are to investigate gelatinous zooplankton. Nonetheless, our study also encountered a few limitations. For example, despite most of the studied species being transparent, the observation of internal morphological characters is difficult without the collection and dissection of the specimens. A second limitation lies in the identification of certain species, based on morphological traits alone, especially for genera with numerous species, such as Beroe spp., where the type specimens are no longer extant. For one leptomedusan and three ctenophore species, their morphology did not match that of any species previously reported from the Southern Ocean. They could potentially be undescribed species, although this needs to be confirmed through DNA barcoding of all the described species from their type localities and further morphological comparisons. The future of gelatinous zooplankton studies lies in the integration of different methodologies, including appropriate collection methods, optical survey tools and molecular genetic comparisons.
Fieldwork was supported by the New Zealand Antarctic Research Institute (NZARI) grant under project code K043. We are grateful for the support of Antarctica New Zealand and the rest of the K043 team for field-based operation and logistics involved in the acquisition of the imagery. Particular thanks go to Dr. Vanessa Lucieer and Dr. Zbyněk Malenovský of the University of Tasmania (Australia) for support in acquiring the images. We thank Shawn Harper of the North Carolina Aquarium on Roanoke Island (USA) for providing one of his Beroe pictures from the Ross Sea. Dr. Naoto Jimi of the National Institute of Polar Research (Japan) is thanked for the identification of the Polychaete family and Svenja Halfter of the University of Tasmania (Australia) for the Amphipod family. We are also grateful to George Branch (University of Cape Town, South Africa) for literature support. The following reviewers are thanked for their constructive comments on the previous version of the manuscript: Dr. Horia Galea (Hydrozoan Research Laboratory, France), Dr. Steven Haddock (Monterey Bay Aquarium Research Institute, USA), Dr. Gillian Mapstone (The National History Museum, UK) and Dr. Otto Oliveira (Universidade Federal do ABC, Brazil). This publication was within the scope of the Research Fellowship project VE 1192/1-1 to GV, funded by the Deutsche Forschungsgemeinschaft (DFG) and a contribution to the Belmont Forum Project “World Wide Web of Plankton Image Curation”, (Belmont Forum grant 18076935 to DL).
GV wrote the main manuscript, described the specimens, prepared the figures, and annotated the images and videos to obtain the Common Objects in Context (COCO) dataset for machine learning. EC conducted the fieldwork and wrote the methods part. DL identified the species, revised the taxonomy and aided in the conceptualisation of the study. GV, DL and EC reviewed and edited the manuscript.
Licence number: 5119250419357