Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 June 2023 | 15(6): 23397–23402
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8215.15.6.23397-23402
#8215 | Received 02
October 2022 | Final received 21 March 2023 | Finally accepted 02 June 2023
Survey of Black Band
Disease-affected scleractinian corals via drone-based
observations in Okinawa, Japan
Rocktim Ramen Das 1 †, Parviz Tavakoli-Kolour 2 †,
Sanaz Hazraty-Kari 3
& James Davis Reimer 4
1,4 Molecular Invertebrate
Systematics and Ecology (MISE) Lab, University of the Ryukyus, Nishihara,
Okinawa 903-0213, Japan.
1,2 Graduate School of Engineering
and Science, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan.
3 Sesoko Station, Tropical Biosphere
Research Center (TBRC), University of the Ryukyus, Motobu,
Okinawa 905-0227, Japan.
4 Department
of Biology, Chemistry and Marine
Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa
903-0213, Japan.
4 TBRC, University of the Ryukyus,
Nishihara, Okinawa 903-0213, Japan.
1 asomorlora@gmail.com
(corresponding author), 2 p.tavakoli@hotmail.com, 3 s.hazrati@hotmail.com,
4 jreimer@sci.u-ryukyu.ac.jp
(corresponding author)
†Equal contribution
Editor: M. Nithyanandan,
Kuwait Institute for Scientific Research (KISR), Salmiya, Kuwait. Date of
publication: 26 June 2023 (online & print)
Citation: Das, R.R., P. Tavakoli-Kolour,
S. Hazraty-Kari & J.D. Reimer (2023). Survey of Black Band Disease-affected
scleractinian corals via drone-based observations in
Okinawa, Japan. Journal of
Threatened Taxa 15(6):
23397–23402. https://doi.org/10.11609/jott.8215.15.6.23397-23402
Copyright: © Das et al. 2023. Creative Commons Attribution 4.0 International License. JoTT allows
unrestricted use, reproduction, and distribution of this article in any medium
by providing adequate credit to the author(s) and the source of publication.
Funding: The APC was funded by an internal University of the Ryukyus project grant to J.D.R.
Competing interests: The authors declare no competing interests.
Author details: Rocktim Ramen Das is currently a PhD candidate at the MISE lab, University of the Ryukyus (UR). His main research interests lies
in understanding the Indo-Pacific coral health and diseases. Parviz Tavakoli-Kolour is a
PhD candidate at UR (based at the Sesoko Station). His research mainly focuses on mesophotic coral ecosystems especially related to acclimatization and plasticity potential of corals across depths. Sanaz Hazraty-Kari is a post-doc at the Sesoko Station (UR), where she primarily studies the effects of global warming on various stages of coral life. James Davis Reimer is a
professor at UR. His primary research interests are in understanding understudied invertebrate groups using field based and molecular techniques.
Author contributions: RRD-—conceptualization, writing - original draft, reviewing and editing, investigation, visualization, data curation, formal analysis, validation, funding acquisition, software. PTK—conceptualization, writing - review and editing, investigation, methodology, visualization, software. SHK—writing - review and editing, resources. JDR—writing - review and editing, funding acquisition, supervision.
Acknowledgements:
The authors are
grateful to the staff of Sesoko Station (University
of the Ryukyus) for providing the necessary facilities. The drone used in this
study is registered at the Drone/UAS Information Platform System ID:
JU3226D60F69 with the Ministry of Land Infrastructure, Transport and Tourism of
Japan. No specimens were collected during this study. The authors are grateful
to prof. Andrew H. Baird (James Cook University) for help with coral
identification and Dr. Taiga Kunishima
(Wakayama Prefectural Museum of Natural History) for help with the Japanese
abstract. Constructive comments and suggestions by three reviewers and the
section editor is appreciated.
Abstract: Diseases are a growing global
threat to scleractinian corals. This study used a
relatively inexpensive commercial drone flown simultaneously along with reef
walking/snorkeling to confirm the presence of cyanobacterial Black Band Disease
(BBD) on a reef in subtropical Okinawa, Japan. At the surveyed reef, the scleractinian corals included encrusting forms (12.57% ±
5.72 coverage), followed by massive/submassive (6.09%
± 4.05) and tabular corals (2.66% ± 1.19). Our survey is unique in that drone
research has not been previously applied to BBD surveys, followed by ground
truthing. Thus, this study can be regarded as an example of using drones during
coral disease assessments.
Keywords:
coral disease, subtropical, coral reef, Montipora.
INTRODUCTION
Coral
diseases are one of the major factors implicated in the decline of shallow
water coral reef ecosystems worldwide (Sutherland et al. 2004; Hazraty-Kari et al. 2021). Among the diseases recognized to
date, cyanobacterial Black Band Disease (BBD) is one of most well-studied
diseases, affecting at least 24 scleractinian, one
hydrozoan, and six gorgonian species in the Atlantic and Indo-Pacific
oceans/seas (Antonious 1973; Bruckner 2015; Roff 2016). Within the Japanese archipelago, BBD has been
reported from both mesophotic and shallow reefs affecting six coral genera: Montipora, Acropora, Echinopora,
Pachyseris, Goniastrea
and Gardineroseris (Wada et al. 2017; Kubomura et al. 2018; Das et al. 2022a) and among these,
the encrusting form of genus Montipora can be
considered one of the primary hosts in the region (Wada et al. 2018; Das et al.
2022a).
Coral
diseases have been widely studied by field-based in situ observations, which
obviously provide several benefits such as ease of observation and the need for
few pieces of equipment. However, such observer-based data are also prone to
bias and inconsistency, as well as often only being able to cover only limited
areas. An alternate method of observation to cover large areas is remote
sensing-based disease assessments (Kabiri et al.
2013; Maynard et al. 2015), although such methods have their own limitations
such as interference via clouds and dust (Purkis
2018). Recently, consumer-grade drones have been increasingly used to monitor
coral reef ecosystems (Casella et al. 2017; Kabiri
et al. 2020), and this relatively low-cost equipment can clearly increase the
ease of monitoring coral reefs (Murfitt et al. 2017).
While the commercialization of cheap drones is recent, the concept existed
earlier with suggestions of utilizing high-resolution cameras along with
multiple spectrum/hyper-spectral sensors on hexacopters,
and the usage of hydrogen balloons (Rützler 1978; Kabiri et al. 2014). Here, we utilized such drone
technology to detect and identify cyanobacterial BBD infecting individual coral
colonies on a nearshore intertidal habitat in Okinawa, Japan.
MATERIALS
AND METHODS
On a clear
day on the 09th of September 2021, we flew a commercial drone
(Mini2, DJI Technology Co. Ltd.) equipped with a 1/2.3” inch CMOS sensor camera
(12 MP) over the shallow nearshore reefs of Sesoko
Island (off central western Okinawajima Island), near
Sesoko Station, University of the Ryukyus
(26.6340°N, 127.8641°E) (Das &
Yamashiro 2018; Das et al. 2022a). The
reef in this area is comprised of various morphotypes and species of the genus Montipora, such as Montipora
cf. aequituberculata, Montipora
cf. digitata, and encrusting Montipora cf. informis,
Montipora cf. efflorescens,
and other Montipora spp. (Yamashiro et al.
2000; Baird et al. 2018; Das et al. 2022a). Montipora
spp. in Okinawa have been recently reported to be easily infected by
BBD (Das et al. 2022a). The time and the day of our survey were chosen based on
low wind and tidal conditions. We identified BBD-infected encrusting Montipora colonies from drone imagery.
Simultaneously, reef walking and snorkeling was conducted to locate and confirm
BBD-infected colonies initially identified by the drone imagery.
In this
study, a total number of 148 images (4000 x 2250 pixels) and four videos (1920
x 1080 p; obtained between 9000 h to 1600 h) were taken from different heights
between 30 to <100 m.
Aerial
photographs were converted from initial .jpg to .tiff format. Three photographs
were specifically chosen based on clarity and low sea surface reflection (sun
glint), and in each of them a 5x5m quadrat was delineated. Additionally,
wherever possible, in-situ images of the infected colonies were taken during
reef walking/snorkeling (Olympus TG-5 camera/PT-058 housing). The drone images
were then uploaded into open-sourced Coral-Net software (Beijbom et al. 2012) for benthic analyses. The benthic
components were classified as tabular, encrusting, foliose, massive/submassive hard corals, dead coral, hard substrate/sand,
and others. A total of 175 randomly generated points were created in each of
the three 5x5 quadrats and were categorized accordingly. The categories were
then identified visually based on the above-mentioned classification. Automatic
annotation was not applicable since a minimum of twenty images are required to
train the AI-based classification algorithm in Coral Net to provide
satisfactory results (Chen et al. 2021).
RESULTS AND
DISCUSSION
Benthic
analyses revealed encrusting hard corals had the highest percentage cover
within quadrats (12.57% ± 5.72 SD), followed by massive/submassive
(6.09% ± 4.05 SD) and tabular corals (2.66% ± 1.19 SD) (Supplementary Table 1).
Soft corals along with other benthos accounted for 23.05% ± 4.01 SD, while dead
corals accounted for 2.48% ± 2.16 SD. A total of six encrusting Montipora colonies with BBD were identified through
these drone images and videos. The dead white bare skeleton along with
neighboring healthy tissue was clearly visible through the high-resolution
images (Image 1A–C, C1; 2A, B, B1). To our knowledge, this is the first study
where cyanobacterial BBD affected areas were surveyed through drones.
Globally,
coral reef health has been successfully monitored through the usage of
commercial drones. Within the Persian Gulf, commercial drones have been used to
map coral reefs, revealing coral mortality and bleaching (Kabiri
et al. 2020). In a similar study at Kaneohe Bay, Hawaii, coral bleaching was
observed using drones (Levy et al. 2018). In the current study, we specifically
focused on a readily observable disease (BBD) within a specific study area,
combined with simultaneous in situ verification.
A fully
developed BBD has a thick microbial consortium, generally black/dark in color,
the dark coloration from the dominant cyanobacterium Roseofilum
reptotaenium (Hutabarat
et al. 2018). Wada et al. (2017), in research at Akajima,
Okinawa (~40 km from Sesoko Is.), further showed four
different types of BBD patterns; black bands; grey bands; mottled black bands,
and an absence of bands, all affecting encrusting Montipora.
At greater depths of >30m, BBD appears purple-black due to the lack of
sulfide oxidizing (SO) bacteria Beggiatoa sp.
(Kubomura et al. 2018). These SO bacteria form a
major population within shallow water BBD bacterial mats and are thought to be
responsible for the whitish coloration of BBD during the night (Richardson
1996).
In future
studies, there remains a necessity to focus on more diverse coral genera which
are affected by numerous other diseases and pathogens. Thus, this work
demonstrates the potential of incorporating drones while concurrently doing
field observations under appropriate conditions (low wind, low surface sunlight
reflection, etc.). Additionally, drone usage will be very effective if diseases
have reached epizootic levels within a given reef. Further, recurrent
observations of the same reef could also provide time-series datasets.
Additionally, we were able to cover a large reef area in much shorter time than
when compared to snorkeling/free swimming methods. The drone was flown over an
area of 7,000 m2 with approximately 75 m2 (n = 3 of 5 X 5
m quadrats) was considered for analyses of coral percent coverage. It can be
argued that drone-based observations are only limited to shallow reef
ecosystems, but reefs in such shallow waters are often diverse and are among
the most threatened by anthropogenic factors (Richards et al. 2015). We suggest
the use of similar methodology to understand other forms of coral diseases, such
as the coral-killing sponge Terpios hoshinota (“Black Disease”), which threatens intertidal
reefs in many areas of southern Japan (e.g., Reimer et al. 2010, 2011) and
elsewhere in the Indo-Pacific (e.g., Montano et al. 2015; Das et al. 2020).
Finally, we
provide a few considerations and suggestions for utilizing drones to monitor
coral reefs. Drone flight is feasible only under optimal environmental
conditions, with successful flights and good-quality image acquisition hampered
by strong winds, rain, or even too much sunshine. Additionally, even if drones
can cover large areas, it is possible to overlook colonies that have just begun
to exhibit early signs of infection. For instance, BBD initially develops
as a cyanobacterial patch (Sato et al. 2009), and because these early phases
may not have considerable tissue loss, such colonies can be easily overlooked.
Similar issues may exist in the case of other diseases and should be
considered before research planning. Another issue is that drones can only clearly
view very shallow or intertidal reefs, and to reach deeper reefs, submersible
drones would be necessary (Das et al. 2022b). Finally, if there is a large
population of marine birds in the survey region, drone flights should be
carefully monitored or should be flown at a suitable height.
Therefore,
based on these limitations and recommendations, we conclude that drones
can be regarded as tools to be included when or if the weather conditions are
suitable. Such technologies can significantly improve the efficiency of surveys
of coral diseases and aid in creating effective management strategies for the
preservation of the coral reef ecosystems.
Supplementary
Table 1. Percent coverage of benthic categories obtained from CoralNet.
|
Image ID |
Image name |
Annotation status |
Points |
51_tabular_hard_coral |
Hard Coral (encrusting) |
Hard Coral (foliose) |
Hard Coral (massive/submassive) |
Dead coral |
Hard Substrate/Sand |
Other |
|
2293735 |
Drone-Q1-RRD-Sesoko-5x5-DJI_0385.JPG |
Confirmed |
175 |
4 |
18.286 |
1.143 |
1.714 |
4 |
47.429 |
23.429 |
|
2293736 |
Drone-Q2-RRD-Sesoko-5x5-DJI_0346.JPG |
Confirmed |
175 |
2.286 |
12.571 |
0 |
6.857 |
0 |
59.429 |
18.857 |
|
2295906 |
Drone-Q3-RRD-Sesoko-5x5-DJI_0451.JPG |
Confirmed |
175 |
1.714 |
6.857 |
0 |
9.714 |
3.429 |
51.429 |
26.857 |
|
|
|
Average |
|
2.666666667 |
12.57133333 |
0.381 |
6.095 |
2.4763333 |
52.76233333 |
23.048 |
|
|
|
SD |
|
1.189592087 |
5.714500007 |
0.659911358 |
4.05406993 |
2.163488 |
6.110100927 |
4.0136 |
Supplementary Video 1. In situ observation
of BBD-infected encrusting Montipora colony.
Supplementary Video 2. In situ observation
of BBD-infected encrusting Montipora colony.
For images and supplementary files - - click
here for full PDF
References
Antonious A. (1973). 10th
Meeting of the Association of Island Marine Laboratories of the Caribbean,
University of Puerto Rico (Mayaguez).
Baird, A.H., S.A. Keith, E. Woolsey, R. Yoshida & T. Naruse (2018). Rapid coral mortality following
unusually calm and hot conditions on Iriomote, Japan.
F1000 Research 6: 1728. https://doi.org/10.12688/f1000research.12660.2
Beijbom, O., P.J.
Edmunds, D.I. Kline, B.G. Mitchell, D. Kriegman (2012).
Automated annotation of coral reef survey images. In Proceedings of the 2012
IEEE Conference on Computer Vision and Pattern Recognition (IEEE), Providence,
RI, USA, 16–21 June 2012; pp. 1170–1177. https://doi.org/10.1109/CVPR.2012.6247798
Bruckner A.W. (2015). History of coral disease research, pp. 52–84.
In: Woodley, C.M., C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway
(eds.), Disease of Coral. Wiley, Hoboken.
Casella, E., A. Collin, D. Harris, S. Ferse,
S. Bejarano, V. Parravicini,
J.L. Hench & A. Rovere (2017). Mapping
coral reefs using consumer-grade drones and structure from motion
photogrammetry techniques. Coral Reefs 36: 269–275. https://doi.org/10.1007/s00338-016-1522-0.
Chen, Q., O. Beijbom, S. Chan, J. Bouwmeester
& D. Kriegman (2021). A new deep
learning engine for Coral-Net, pp. 3693–3702. In Proceedings of the IEEE/CVF
International Conference on Computer Vision. https://doi.org/10.1109/ICCV48922.2021
Das, R.R. & H. Yamashiro (2018). Corals
dominate monofilament lines in Sesoko Island, Japan. Current
Science 114: 730–731.
Das, R.R., C.R. Sreeraj, G. Mohan, K.R.
Abhilash, V.K.D. Samuel, P. Ramachandran & R. Ramachandran (2020). Incursion
of the killer sponge Terpios hoshinota Rützler & Muzik, 1993 on the coral reefs of the Lakshadweep
Archipelago, Arabian Sea. Journal of Threatened Taxa 12: 17009–17013. https://doi.org/10.11609/jott.5790.12.14.17009-17013
Das, R.R., H. Wada, G.D. Masucci, T. Singh, P.
Tavakoli-Kolour, N. Wada, S-L. Tang, H. Yamashiro
& J.D. Reimer (2022a). Four-year field survey of black band disease
and skeletal growth anomalies in encrusting Montipora
spp. corals around Sesoko island, Okinawa. Diversity
14: 32. https://doi.org/10.3390/d14010032
Das, R.R., T. Immanuel, R.K. Lakra, K. Baath
& G. Thiruchitrambalam (2022b). First
report of marine sponge Chelonaplysilla delicata (Demospongiae: Darwinellidae) from the Andaman Sea/Indian Ocean with
baseline information of epifauna on a mesophotic shipwreck. Journal of
Threatened Taxa 14(10): 21961–21967. https://doi.org/10.11609/jott.7495.14.10.21961-21967
Hazraty-Kari, S.,
P. Tavakoli-Kolour, R.R. Das, M. Farhadi,
A. Barkhordari-Ahmadi, M. Yahyavi
& H. Rezai (2021). Baseline
assessment of coral diseases in an environmentally extreme environment of the
northern Persian Gulf. Marine Pollution Bulletin 171: 112707. https://doi.org/10.1016/j.marpolbul.2021.112707
Hutabarat, P.U.B.,
X.H. Nguyen & S. Suda (2018).
Black Band disease-related (BBD) cyanobacterium from Okinawan corals. Journal
of Applied Phycology 30: 3197–3203. https://doi.org/10.1007/s10811-018-1507-1
Kabiri, K., B.
Pradhan, K. Samimi-Namin & M. Moradi (2013).
Detecting coral bleaching, using QuickBird
multi-temporal data: a feasibility study at Kish Island, the Persian Gulf. Estuarine,
Coastal and Shelf Science 117: 273–281. https://doi.org/10.1016/j.ecss.2012.12.006
Kabiri, K., H. Rezai, M. Moradi & F. Pourjomeh
(2014). Coral reefs mapping using parasailing aerial
photography-feasibility study: Kish Island, Persian Gulf. Journal of Coastal
Conservation 18: 691–699. https://doi.org/10.1007/s11852-014-0345-9
Kabiri, K., H. Rezai & M. Moradi (2020).
A drone-based method for mapping the coral reefs in the shallow coastal waters
– case study: Kish Island, Persian Gulf. Earth Science Informatics 13:
1265–1274. https://doi.org/10.1007/s12145-020-00507-z
Kubomura, T., H.
Yamashiro & J.D. Reimer (2018). Appearance
of an anomalous black band disease at upper mesophotic depths after coral
bleaching. Diseases of Aquatic Organisms 131: 245–249. https://doi.org/10.3354/dao03292
Levy, J., C. Hunter, T. Lukacazyk & E.C.
Franklin (2018). Assessing the spatial distribution of coral
bleaching using small unmanned aerial systems. Coral Reefs 37:
373–387. https://doi.org/10.1007/s00338-018-1662-5
Maynard, J., R.V. Hooidonk, C.M. Eakin, M. Puotinen, M. Garren, G. Williams,
S.F. Heron, J. Lamb, E. Weil, B. Willis & C.D. Harvell (2015).
Projections of climate conditions that increase coral disease susceptibility
and pathogen abundance and virulence. Nature Climate Change 5:
688–695. https://doi.org/10.1038/NCLIMATE.2625
Montano, S., W-H. Chou, C.A. Chen, P. Galli & J.D. Reimer (2015). First
record of the coral-killing sponge Terpios hoshinota in the Maldives and Indian Ocean.
Bulletin of Marine Science 91(1): 000-000.
http://dx.doi.org/10.5343/bms.2014.1054
Murfitt, S.L.,
B.M. Allan, A. Bellgrove, A. Rattray, M.A. Young
& D. Ierodiaconou (2017).
Applications of unmanned aerial vehicles in intertidal reef monitoring. Scientific
Reports 7: 10259. https://doi.org/10.1038/s41598-017-10818-9
Purkis, S.J.
(2018). Remote sensing tropical coral reefs: The view from above. Annual
Review of Marine Science 10: 4.1–4.20.
https://doi.org/10.1146/annurev-marine-121916-063249
Reimer, J.D., Y. Nozawa & E. Hirose
(2010). Domination and disappearance of the black sponge: A quarter century
after the initial Terpios outbreak in Southern
Japan. Zoological Studies 50: 394.
Reimer, J.D., M. Mizuyama, M. Nakano, T. Fujii & E. Hirose (2011). Current
status of the distribution of the coral-encrusting cyanobacteriosponge
Terpios hoshinota
in southern Japan. Galaxea, Journal of
Coral Reef Studies 13: 35–44.
Richardson, L.L. (1996). Horizontal and vertical
migration patterns of Phormidium corallyticum and Beggiatoa
spp. associated with Black-Band Disease of corals. Microbial Ecology 32:
323–335.
Richards, Z.T., R.A. Garcia, C.C. Wallace, N.L. Rosser & P.R. Muir
(2015). A diverse assemblage of reef corals thriving in a dynamic intertidal
reef setting (Bonaparte Archipelago, Kimberley, Australia). Plos
One 10(2): e0117791. https://doi.org/10.1371/journal.pone.0117791
Roff, G.
(2016). Earliest record of a coral disease from the Indo-Pacific? Coral
Reefs 35: 457. https://doi.org/10.1007/s00338-016-1416-1
Rützler, K.
(1978). Photogrammetry of reef environments by helium balloon. Coral Reefs:
Research Methods. UNESCO, Paris.
Sato, Y., B.L. Willis & D.G. Bourne (2009).
Successional changes in bacterial communities during the development of black
band diseases on the reef coral, Montipora hispida. The ISME Journal 4: 203–214. https://doi.org/10.1038/ismej.2009.103
Sutherland, K.P., J.W. Porter & C. Torres (2004). Disease
and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Marine
Ecology Progress Series 266: 273–302.
Wada, N., N. Mano, Y. Yanagisawa & T. Mori (2017). Occurrence
of coral diseases at Akajima, Okinawa, Japan in 2010
and 2011. Galaxea, Journal of Coral Reef
Studies 19: 35–44.
Wada, N., Ohdera A & Mano N., 2018. Coral
disease in Japan, pp. 41–62. In: Iguchi, A. & C. Hongo,
(ed.). Coral Reef Studies in Japan. Springer, Singapore, 179 pp.
Yamashiro, H., M. Yamamoto & R.V. Woesik
(2000). Tumor formation on the coral Montipora
informis. Diseases of Aquatic Organisms
41: 211–217.