Please cite this article in press as: Lin et al., Using Soundscapes to Assess Deep-Sea Benthic Ecosystems, Trends in Ecology & Evolution (2019), https://doi.org/10.1016/j.tree.2019.09.006
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Using Soundscapes to Assess Deep-Sea Benthic Ecosystems Tzu-Hao Lin,1,4,@,* Chong Chen,2,4,@ Hiromi Kayama Watanabe,2,@ Shinsuke Kawagucci,2 Hiroyuki Yamamoto,1 and Tomonari Akamatsu3 Targets of deep-sea mining commonly coincide with biodiversity hotspots, such as hydrothermal vents. The resilience of these ecosystems relies on larval dispersal, which may be directed by habitat-specific soundscapes. We urge for a global effort to implement soundscape as a conservation tool to assess anthropogenic disruption to deep-sea benthic ecosystems. We know more about Mars than the deep sea floor visually, but soon also aurally, despite the latter being threatened by our exploitation. We have made little effort to eavesdrop on the bathyal world, but the deep is far from silent. Interest in mining the deep seabed is increasing with rising global demand for metals and rare-earth elements. As of 2019, the International Seabed Authority (ISA) (see Glossary) has granted 29 deep-sea mining exploration licenses in international waters, and countries such as Papua New Guinea and Japan have shown interest in such activities in their Exclusive Economic Zones [1]. Locations for deep-sea mining coincide with ‘hotspots’ hosting unique, abundant biodiversity, such as cold seeps rich in methane hydrate, hydrothermal vents producing massive sulfide, manganese nodule fields on the abyssal plain, and seamounts covered in metal-rich crusts [1]. Organisms inhabiting these ecosystems are
highly adapted, and most are endemics that cannot live anywhere else. Hydrothermal vents, for example, exhibit high biomass comparable to tropical coral reefs and about 70% of species are endemic [1]. Despite the impressive array of novel species, many of which remain undiscovered, these environments are threatened from potentially irreversible mining impacts. Biodiversity hotspots in the deep sea are often distant from one another; for example, a cold-water coral reef on a seamount is commonly tens to hundreds of kilometres away from its nearest neighbour. After mining impacts, recovery depends on recolonisation from these distant neighbours [2]. Difficulties and costs associated with accessing the deep means we have a limited understanding of how animals maintain populations among these patchy habitats. Although the only viable method for benthic species to do so is larval dispersal, we know next to nothing about extrinsic cues deepsea larvae use to recognise suitable habitats [2]. Putting this into a spatial context, vents are smaller than football fields, while larvae may travel hundreds of kilometres before settling. How do they know where to settle down in the gloomy, light-less deep?
Soundscape: Acoustic Signpost in the Deep Sea The answer may lie in the sound. There is evidence that larvae of coral, mollusc, and reef-associated fish in shallow waters use sound for settlement [3,4]. While light is quickly diminished in seawater, sound can travel a long distance for larvae to sense the acoustic heterogeneity [4]. By detecting soundscapes, composed of various sources of geophony and biophony, specific to their preferred habitats, larvae exhibit positive phonotaxis and actively direct their movement to settle in suitable en-
vironments, as has been shown for keystone and ecosystem engineering species such as reef-building corals [4]. We propose that habitat-specific soundscapes may be important in the resilience of deep-sea environments by acting as settlement cues (Figure 1). Hydrothermal vents emit significant acoustic energy from vigorous venting activities and eruptions that occur nearby. Recordings have indicated sound levels of 10–50 dB above the ambient depending on activity levels, with different vent structures likely producing different geophony [5]. Additionally, fish and soft-bodied invertebrates have been shown to produce significant biophony [6], differences in sounds produced by habitat-specific species add to the uniqueness of soundscapes. Glass sponge reefs, for example, exhibit site-specific soundscapes and similar reefs are common in the deep [7]. Disparity in community structure at various stages of ecological succession may be communicated to larvae through biophony, allowing them to select a locality that is not only environmentally suitable but also temporally ideal. Larvae also detect habitats using chemical cues, but these signals only rise a few hundred metres above the seafloor before being diluted below detectable levels and cannot be the sole settlement cue for larvae dispersing in surface waters [8]. Chemical cues are heavily influenced by currents, whereas sounds propagate in all directions and potentially serve as signposts for the deep-sea larvae to listen for their home.
Anthropogenic Disruption of Soundscapes and Resilience Anthrophony disrupts the response of coral and fish larvae to reef soundscapes [4] and deep-sea soundscapes are not free from human disturbances.
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Please cite this article in press as: Lin et al., Using Soundscapes to Assess Deep-Sea Benthic Ecosystems, Trends in Ecology & Evolution (2019), https://doi.org/10.1016/j.tree.2019.09.006
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mask the natural soundscape and render the immediate habitat, and likely nearby ones, undetectable for larvae. As such, one instance of mining may significantly reduce the connectivity of deep-sea ecosystems within a larger area, which should be considered when planning for marine protected areas.
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Figure 1. Soundscape as a Settlement Cue for Deep-Sea Larvae. Schematics showing how deep-sea larvae may use habitat-specific soundscape to detect their habitats, and how anthrophony from mining disrupts this process through masking geophony and reducing biophony by wiping out parts of the animal community producing it.
Sound recordings from the Earth’s deepest point – the Challenger Deep in Mariana Trench just shy of 11 km deep, tell us that anthrophony generated at the surface propagates to any depth in our oceans [9]. Mining activity disrupts soundscapes by generating noise from shipping, drilling, and mineral-retrieval machinery, as well as
discarding of cuttings (Table 1). Recordings from offshore drilling and excavation showed source levels of 174.9 and 193.3 dB re 1 mPa, respectively [10]; much higher than the aforementioned geophony. Even ongoing scientific and premining investigations with submersibles and seismic explorations generate noise pollution. These
Table 1. Soundscape components of deep-sea hotspotsa Maximum SLb
Temporal scale
Detection ratec
Ambient
100
Continuous
Always
Venting
135
Continuous
High
Explosive eruption
>250
Hours–days
Moderate
Earthquake
>250
Minutes
Low
Soniferous fish
160
Transient
Unknown
Source Geophony
Biophony
Anthrophony
Soniferous invertebrates
190
Transient
Unknown
Nonsoniferous animals (producing sound but not for communication)
130
Transient
Unknown
Shipping
200
Hours
High
Drilling
185
Weeks
High
Scientific submersible
200
Hours–days
Moderate
Seismic survey
250
Days–months
Moderate
Scraping
195
Months–years
High
a
Presented as an estimated framework of likely components using an active hydrothermal vent as an example, including sounds from mining-related activities. b SL, Source Level (dB re 1 mPa @ 1 m) c Detected by a sound recorder or a passive acoustic observatory, such as those discussed in [11].
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We argue that the influence of miningrelated anthrophony on natural soundscapes of benthic ecosystems needs to be included in impact assessments. This is especially urgent as ongoing scientific expeditions, including many funded as baseline research for mining, are likely already impacting the soundscape. Currently, the ISA Mining Code makes no mention of soundscapes. The Mining Code is still under development with the review process being open to the scientific community, and we suggest adding ocean sound as a baseline data category.
Listening to the Deep: a New Conservation Tool The monitoring of soundscape has the strength to provide an index of biodiversity of an entire habitat over a long time from a few hydrophones (Table 1), instead of mapping the entire area with underwater robots [11]. This corroborates data from other newly arising techniques, such as environmental DNA and RNA [11], serving as independent and complementary datasets in assessing mining impact and ecosystem resilience. Moreover, knowing what these habitats sound like will help us manage anthropogenic activities and protect soundscapes crucial for deep-sea ecosystems. We further urge for a global collaborative effort in using soundscape as a new deep-sea conservation tool, to assess resilience and anthropogenic disruption of
Please cite this article in press as: Lin et al., Using Soundscapes to Assess Deep-Sea Benthic Ecosystems, Trends in Ecology & Evolution (2019), https://doi.org/10.1016/j.tree.2019.09.006
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ecosystem connectivity; by acquiring data of soundscapes describing healthy ecosystems, those disturbed by anthropogenic activities, and monitoring changes over time. This is entirely in line with the recently outlined scientific need for globally integrated deep-ocean observing [12] – a crucial step towards truly sustainable use of the ocean in the coming decades. The science of studying mutual interactions among soundscapes, marine fauna, and society is relatively new; the majority of studies have focused on soniferous animals such as whales, dolphins, and fish. Soundscape monitoring can be implemented using existing observatories targeting soniferous animals and is less costly compared with deep submersibles [11]. Knowledge of how larvae at vents and other deep-water habitats use sound for orientation is still lacking. Global research efforts on how soundscapes influence settlement of deep-sea larvae are therefore also critical and should be carried out simultaneously and preferably in a coordinated manner. The deep seabed of international waters is a common heritage of humankind. Mining activities are imminent, and the need to rapidly observe and document deep-sea ecosystems has never been greater. We humans and deep-sea animals are alike in using all five senses to perceive each other and the (fast-changing) world. So, why limit ourselves to less in deep-sea exploration and conservation? 1Research
Institute for Global Change, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2–15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
2X-STAR,
Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2–15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
3National
Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
4These
authors made an equal contribution
@Twitter:
@HarryLin4 (T.-H. Lin), @squamiferum (C. Chen), and @hwatanabekayama (H.K. Watanabe). *Correspondence:
[email protected] https://doi.org/10.1016/j.tree.2019.09.006 ª 2019 Elsevier Ltd. All rights reserved.
ores of minerals such as copper, zinc, gold, and silver. Mining Code: overall body of rules, regulations, and procedures combined to regulate the exploration and exploitation of marine mineral resources in international waters, currently under development by the ISA with drafts being released intermittently. Phonotaxis: ability of an organism to actively orientate itself to a source of sound. Soniferous animals: animals producing sound for orientation and communication. Soundscape: total, characteristic, sound of an environment.
References
Glossary Anthrophony: sounds generated by human activities. Common underwater sources of anthrophony including maritime traffic, submersibles, sonar, acoustic communications, and resource exploitation activities. Biophony: sounds generated by nonhuman organisms. Organisms may produce sounds intentionally or unintentionally, depending on behavioural contexts, species, and even populations. Exclusive Economic Zones: waters extending 200 nautical miles from the shoreline, within which nations have sovereign rights to the waters and any resources found there. Recognised by the United Nations Convention on the Law of the Sea (UNCLOS). Geophony: sounds produced from geological or geophysical activities, such as wind, rainfall, earthquake, volcanic eruptions, hydrothermal vents. Hydrophone: specialized microphone designed to record underwater sounds. International Seabed Authority (ISA): international body that oversees and regulates all mining activities in international waters. Observer to the United Nations General Assembly. International waters: ocean beyond national jurisdiction regulated solely by international agreements, accounting for 64% of the total ocean surface and 95% of its volume. Marine protected areas: space in the ocean dedicated to the protection and maintenance of biodiversity, natural and cultural resources, with various degrees of limitations for exploitation with their boundaries. The United Nation targets for at least 10% of coastal and marine areas to be protected by 2020 under the Aichi Target 11 of the Convention on Biological Diversity. Implementation within waters under national jurisdictions are the responsibility of respective countries. Massive sulfides: hydrothermally formed polymetallic sulfide deposits that are high-grade
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