Anthropogenic threats to benthic habitats

CHAPTER 3

Anthropogenic threats to benthic habitats Peter T. Harris UNEP/GRID-Arendal, Arendal, Norway

Abstract Anthropogenic threats to benthic habitats do not pose an equal risk, nor are they uniformly distributed over the broad depth range of marine habitats. Deep-sea benthic environments have, by and large, not been heavily exploited and most are in relatively good condition. In contrast, shelf and coastal habitats, and deep ocean pelagic fisheries, have been exploited extensively and human impacts here are locally severe. A critical point is that anthropogenic threats do not act in isolation; rather, they are cumulative and the impacts are compounded for every affected habitat. In general, the impacts of humans on benthic habitats are poorly understood. Habitat mapping provides condition assessments and establishes baselines against which changes can be measured. GeoHab scientists ranked the impacts on benthic habitats from fishing as the greatest threat, followed by pollution and litter, aggregate mining, oil and gas, coastal development, tourism, cables, shipping, invasive species, climate change, and construction of wind farms. The majority of authors (84%) reported that monitoring changes in habitat condition over time was a planned or likely outcome of the work carried out. In this chapter the main anthropogenic threats to benthic habitats are reviewed in relation to their potential impacts on benthic environments.

Keywords: Human impacts; cumulative impacts; fishing; pollution; litter; aggregate mining; oil and gas; coastal development; tourism; cables; shipping; invasive species; climate change; wind farms

Measuring and mapping human impacts It is important at the outset to emphasize that human impacts are cumulative; overfishing, pollution, noise, mining, etc. often affect the same areas and individual species are simultaneously affected by more than one stressor (Norse and Crowder, 2005; Hoyt, 2005; Halpern et al., 2008; Fig. 3.1). The cumulative impacts of human activities have affected all parts of the oceans to greater or lesser degrees, but the greatest impacts have been in the coastal and shelf environments. Separate impacts ranked in order of priority for percentage of species affected (Kappel, 2005), for example, show that a simple list of threats does not predict the combined effect of multiple stressors.

Seafloor Geomorphology as Benthic Habitat. DOI: https://doi.org/10.1016/B978-0-12-814960-7.00003-8 © 2020 Elsevier Inc. All rights reserved.

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Figure 3.1 Map showing the cumulative human impacts on ocean health based on the synthesis of 17 global data sets of anthropogenic drivers of ecological change. Note only a few areas of the Arctic and Antarctic oceans are assessed as having suffered very low impact. Source: After Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F., D’Agrosa, C., et al. (2008). A global map of human impact on marine ecosystems. Science 319, 948 952.

In order to detect anthropogenic impacts, measurements must first account for the natural variability that affects any signal. Baseline observations of dynamic systems must be referenced to a long time series of measurements in order to account for natural fluctuations that occur in many cases. For example, Gregg and Conkright (2002) estimate that global primary productivity has decreased by 6% between the 1980s and 1990s based on a comparative analysis of SeaWiffs satellite imagery. These authors attribute this decline to natural variability of ocean productivity over decadal timescales, and not to anthropogenic climate change. This study is an example of the complexity involved with measuring change in marine systems. The case studies presented in Part 2 of this book describe the relative naturalness of the studied habitats, that is, the extent to which a habitat or environment has been modified from its natural state by human activities and impacts (Norse and Crowder, 2005). Perhaps one of the greatest challenges facing the management of shelf and coastal marine environments is that pristine, benchmark sites are rare or absent, making the assessment of

Anthropogenic threats to benthic habitats 37 human impacts difficult. The goals for shelf and coastal conservation efforts are therefore frequently to do with restoration of previously existing ecosystems, rather than with maintenance of current status. A corollary of this observation is that the identification of remaining pristine sites is a priority for conservation, in order to help establish benchmarks and control sites for condition assessments and monitoring the performance of conservation measures. Out of 53 case studies included in this book, habitat mapping was intended to be part of an ongoing monitoring program in 32 cases. Eleven case studies specified that theirs was already part of an ongoing monitoring program (Chapters 9, 17, 18, 39, 47, 49, 51, 52, 59). From those 11 studies, four reported that monitoring had not yet detected any changes in habitat condition. One study from the Russian White Sea (Chapter 39: Geomorphological and habitat mapping of the glaciated shelf (the Velikaya Salma Strait of the Kandalaksha Gulf of the White Sea, Russia)) reported that the roles of the dominant species have partly changed over time.

Fishing Compared with all other human activities, fishing is, without a doubt, the most immediate and pervasive threat to marine ecosystems (Jackson, 2008; Pauly et al., 2005). In the modern industrial age, and especially over the past 50 years, fishing has expanded into almost every part of the world’s coastal and shelf seas (Fig. 3.2). The consequences have been severe; many fisheries have been overexploited to the point of permanent closure. Of particular significance to benthic habitats is the impact of towed fishing gear (trawls and dredges) which ploughs through soft sediments, destroying biological structures such as worm tubes and burrows, but also overturns rocks, levels bedforms, and dislodges sessile and colonial benthic animals such as sponges, corals, and bryozoans. An entire symposium volume of the American Fisheries Society is devoted to the subject (Barnes and Thomas, 2005) and in Norse and Crowder’s (2005) textbook, five out of the nine chapters devoted to human impacts on marine environments are concerned with the impacts of fishing. The most productive fisheries are concentrated in approximately 10% of the ocean, mainly on the continental shelf, while vast areas of the oceans are relatively unproductive (Fig. 3.2). The direct damage caused by fishing is most apparent on reefs, seamounts, ridges, and other rocky habitats where bottom trawling techniques are used. Trawl gear not only captures the target species (fish and shrimp) but doors, weights, and chains used to hold the nets open impact the bottom and kill or injure the nontarget benthic epifauna (Watling, 2005), such as cold-water coral and sponge communities (Fig. 3.3A and B). Seamount trawl fisheries have developed over the past 50 years and have a very poor track

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Figure 3.2 Global fish catch in 2004 (Nellemann et al., 2008). Most fish are caught in approximately 10% of the ocean area, mainly on the continental shelves where productivity is highest. High productivity is associated with freshwater runoff from land and upwelling onto the shelf of cold, nutrient-rich waters from deep ocean basins.

record for being managed sustainably. Unregulated fishing occurs on seamounts and ridges located in the high seas and the amount of damage caused is unknown, but experts agree that it is widespread and significant (Koslow et al., 2015). The amount of biodiversity at risk is probably large, based on biogeographic patterns from the few seamounts that have been studied (Pitcher et al., 2007). The sheer quantity of commercial, oceanic fishing has greatly reduced the uppermost sections of trophic levels. Fishing of pelagic top predators has reduced their numbers by around 90% of what existed prior to 1950 (Myers and Worm, 2005). With the higher predators removed, effort has switched to lower trophic levels (Pauly et al., 1998). For example, the extermination of the majority of baleen whales between 1950 and 1970 resulted in a so-called krill surplus of around 150 million tonnes per year, representing the amount of krill that was formerly consumed by whales and that was now available for human use. (Note: The current catch of Antarctic krill is only around 220,000 tonnes per year; CCAMLR, 2018). The effects of these dramatic changes in populations at the higher trophic levels on populations at lower levels (such as krill) are unknown (Nicol and Endo, 1999). Their effects on the ocean ecosystem as a whole are incredibly complex and may never be fully understood.

Anthropogenic threats to benthic habitats 39

Figure 3.3 (A) Bottom photographs showing seafloor before (left) and after (right) bottom trawling has occurred on deep-sea coral gardens on the continental slope off Norway. Note in photo on right the elongated trawl mark on the seafloor, resulting from dragging trawl doors. (B) Side scan sonograph showing elongated and curved tracks made by bottom trawl boards on the seabed of Moreton Bay, Australia. Light-toned areas are elongate trains of sand dunes. Source: (A) Photos from UN Environment/GRID-Arendal, Norway. (B) Image from Geoscience Australia.

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Oil and gas exploration and production The threats to marine life from the mining of hydrocarbons (not including the effects of climate change) are generally lower than for either fishing or mining (Watling, 2005). The risks of impact from oil spills are greatest during transport, from pipeline rupture, vessel loss, or spillage, when large volumes of oil can be released suddenly. Accidental (anthropogenic) spills are ecologically damaging because they result in unnatural concentrations of oil at a particular site that is incompatible with local marine life. However, crude oil is a naturally occurring substance on the earth and an amount of oil equal to or larger than that spilled accidentally by humans enters the oceans each year through natural seepage (Kvenvolden and Cooper, 2003). Natural seepage is a gradual, ongoing process and ecosystems have evolved that use it as a food source. Also it should be noted that accidental oil spills account for only a small percentage of the total volume of oil that enters the oceans due to humans. Most oil enters the ocean mixed with sewage and urban stormwater runoff (Table 3.1) but such diffuse sources do not have the same dramatic impact on ecosystems as a spill because the oil is delivered continuously in low concentrations over a broad area. The long-term effects of low-level oil pollution from diffuse sources are unknown (Pantin, 2007). Environmental impacts arise throughout petroleum exploration drilling production development operations, although the nature and degree of impact varies (Swan et al., 1994; Harris et al., 2016). Seismic surveys, oil and gas production, and transportation all have associated environmental impacts; these are described briefly in the following sections. Table 3.1: Estimates of global inputs of oil into the marine environment. Source

1970s

1980s

1990s

Land-based sources: Urban runoff and discharges

2500

1175

Coastal refineries Other coastal effluents Oil transportation and shipping: Operational discharges from tankers Tanker accidents (ITOPF, 2007) Losses from nontanker shipping

200

1080 (500 1250) 100 (60 600) 50 (50 200) 700 (400 1500) 118 320 (200 600) 50 (40 60) 300 (50 500) 600 (200 2000) 3318

Offshore production discharges Atmospheric fallout Natural seeps (Kvenvolden and Cooper, 2003) Total discharges

1080 314 750 80 600 600 (200 2000) 61,240

564 114

47 306 600 (200 2000) 2806

Units are thousands tonnes per year with error range in brackets where available (“ ” indicates no data available). Source: Based on Swan et al. (1994), Balcomb and Claridge (2001), Kvenvolden and Cooper (2003), Pantin (2007) and Harris et al. (2016).

Anthropogenic threats to benthic habitats 41

Seismic surveys Marine acoustic survey equipment is used by the oil and gas industry as well as by the military and other marine industries to map the seafloor and to study the seafloor geology and the water column. These systems are generally far more powerful than equipment used for marine research or normal ship navigation (but see also below section on “Noise”). Equipment that is most likely to affect marine mammals and other life are air gun (seismic) arrays and low-frequency, high-power transducers with wide beam angles (deepwater multibeam sonar systems). Air guns employed to acquire seismic reflection data are far more powerful (225 255 dB re 1 µPa peak; Richardson et al., 1995) than equipment used for marine research or normal ship navigation. Air guns used in seismic reflection surveys emit sound at a frequency of typically approximately 100 Hz which overlaps with the range of marine mammals’ hearing and is therefore most likely to affect marine mammals and other marine life (Nowacek et al., 2007, 2013; CBD, 2014). Cetaceans have been observed avoiding powerful, low-frequency sound sources and there is at least one documented case of injury to whales and whale stranding caused by multiple, mid-frequency (2.6 8.2 kHz) military echo sounders (Balcomb and Claridge, 2001). The historical record of cetaceans stranding themselves prior to the industrial age includes the English Crown holding rights on stranded cetaceans from at least 1324, when they were known as “fishes royal” since the Crown had first claim on them (Fraser, 1977). However, an increase in the number of stranding events may be an indicator of human impact. In general, it seems that high-powered industrial seismic and military type sonar systems are likely to have the greatest impact on marine life (Boebel et al., 2005). In the case of marine animals other than cetaceans, there is some evidence for short-term displacement of seals and fish by seismic surveys, but there is little literature available (O’Brien et al., 2002; Thompson et al., 2013).

Drilling and production activities Drilling activities are carried out from ships or fixed platforms during exploration and to extract oil once it has been found. The number of offshore oil production platforms in the world is constantly changing in response to economic factors, but averages between around 6000 and 8000 facilities. Offshore production is around 27 million barrels per day. A further approximately 540 jack-up drill rigs are used for exploration in shallow (less than 100 m water depth) seas and a further 80 drillships and semisubmersible vessels are in operation globally (2014 figures; Harris et al., 2016). Direct damage to the seafloor is caused by the anchors used to hold the rig in place as well as by the impact of the drill itself. Drilling requires the use of lubricant (drilling mud) and the disposal of drill cuttings onto the seabed at the drill site. Drilling mud and some of the drill cuttings can be toxic and

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so the environmental impacts of drilling may involve burial together with toxicity effects (Swan et al., 1994). The initial impact is generally confined to the immediate surrounds, typically within 150 m of the drill site. However, Olsgard and Gray (1995) reported barium, total hydrocarbons, zinc, copper, cadmium, and lead contamination sourced from production platforms on the Norwegian shelf had spread after a period of 6 9 years, so that evidence of contamination was found 2 6 km away from the platforms. During the production of oil and gas, water from the hydrocarbon reservoir is also brought to the surface. This so-called produced formation water (PFW) is a by-product of oil production and it is disposed of into the ocean (Swan et al., 1994). Compared with ambient seawater, PFW may contain elevated concentrations of heavy metals (e.g., arsenic, mercury, barium, copper, lead, and zinc), radium isotopes, as well as hydrocarbons. The proportion of oil/water varies between locations but generally the proportion of water increases over time as the oil deposit is depleted (i.e., older wells discharge more PFW than new wells). The proportion of water produced per barrel of oil typically ranges from around 3:1 to 7:1 although in some extreme cases the fluid pumped from a well might be 98% water and only 2% oil (Khatib and Verbeek, 2003). At the production platform, most of the PFW is separated from the oil, treated (typically to around 30 mg L21 hydrocarbon), and disposed of into the ocean. PFW forms a buoyant plume because it is typically 40 C 80 C warmer (and therefore less dense) than ambient seawater and thus it will be dispersed by wind and currents away from the production platform. Mixing and dilution with seawater results in toxic effects of PFW being generally confined to within 1 km of production platforms, although PFW plumes may be detected in surface waters for distances exceeding 10 km from the point source (Holdway and Heggie, 2000). Cases of coral discoloration (coral bleaching) have been attributed to dilute (approximately 12%) PFW concentrations (Jones and Hayward, 2003). Hence the situation of production platforms in relation to prevailing winds and currents and to the proximity of sensitive habitats is a consideration for offshore petroleum development. Once in place oil production platforms become habitat for benthic fauna. Furthermore, over the life span of a platform, shell debris derived from mollusks that colonize the platform legs accumulates at the base. The shell accumulation is draped over drill cuttings forming a mound-shaped deposit. The shell drape provides a new habitat that has different properties from the surrounding seabed and thus offers habitat to different species. Disturbance of the shell drape will expose the (potentially toxic) drill cuttings that are a factor for consideration for rig decommissioning. For this reason, a program known as “rigs to reefs” has been established in the US Gulf of Mexico, where there are about 2996 production platforms of which 813 are no longer producing. In 2010 the US Government issued notices to companies requiring them to dismantle about 650 unused oil and gas production platforms (Rach, 2013), and of these 420 have been granted permission to be transformed into artificial reefs. Apart from a few platforms converted to reefs in Brunei Darussalam

Anthropogenic threats to benthic habitats 43 and Malaysia, opposition to the practice has meant that none has been allowed off California or in the North Sea to date (Day, 2008; Macreadie et al., 2011, 2012; Jørgensen, 2012).

Oil spills Between 1970 and 2017 some 5.7 million tonnes of oil was accidentally spilled into the ocean from oil tankers and barges (ITOPF, 2017). It is significant that most of this oil was spilled during a few catastrophic events resulting from tankers running aground, colliding with other ships, or breaking up in stormy seas. Overall there have been 466 spills over 700 tonnes, with the rate of spills decreasing steadily from 24.5 spills per year between 1970 and 1979 to 18 spills per year between 2010 and 2017. Furthermore, the amount of oil spilled from tankers has decreased from nearly 3.5 million tonnes between 1970 and 1979 to around 47,000 tonnes between 2010 and 2017 (ITOPF, 2017). Of the accidents documented by ITOPF (2017), about 50% occurred during routine loading/unloading operations but resulted in very small volume spills. The worst year for the tanker industry was 1979 when some 670,000 tonnes of oil was spilled, of which 287,000 tonnes was from one ship (MV Atlantic Express). Oil pipelines also leak oil into the environment. Although corrosion is the most commonly cited cause of pipeline failure, corrosion-related ruptures do not result in significant release of oil into the environment. In fact 95% of the 250,000 barrels that leaked from pipelines in the Gulf of Mexico from 1967 to 1990 were caused by a ship’s anchor damage (Marine Board, 1994). Rach (2013) reported that 42% of existing (66,695 km) pipelines in the Gulf of Mexico are either abandoned, proposed to be abandoned, or are no longer in service. The OSPAR (North Sea) area has more than 50,000 km of pipelines transporting oil and gas products from around 1300 installations (OSPAR, 2009). In the 2010 Gulf of Mexico oil spill it is estimated that around 4.4 million barrels (about 600,000 tonnes, assuming a specific gravity of 0.88) was discharged into the sea before the well was capped, more oil than was spilled by the Exxon Valdez in 1989 (Crone and Tolstoy, 2010). The impacts of this huge volume of oil on deepwater habitats in the Gulf of Mexico were reviewed and summarized by Beyer et al. (2016). They concluded that concerns remain for the long-term impacts on seagrass habitat, large fish species, deep-sea corals, sea turtles, and cetaceans. Accidents that occur in coastal waters have the most severe environmental impact because of the fact that most oil floats on the sea surface and its effects are concentrated at the shoreline (Fig. 3.4). The coast is also a habitat for a diversity of species of birds, mammals, invertebrates, and marine plants. For this reason spills that impact the coast, such as the Exon Valdez spill that occurred in Alaska in 1989, have the greatest impact on the ecosystem (Shaw, 1992).

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Figure 3.4 On March 24, 1989, the supertanker Exxon Valdez grounded on a rocky reef in Prince William Sound, Alaska, spilling about 100,000 tonnes of crude oil into the sea (USGS photo).

The impacts of oil spills range from the immediate effects of oiling to longer term consequences of habitats being modified by the presence of oil and tar balls. Traces of hydrocarbons can remain in coastal sediments for many years after an oil spill (Hester and Mendelssohn, 2000). Some species exhibit reduced abundance associated with the timing of spills (Sa´nchez et al., 2006), although direct causal evidence is not always available (Carls et al., 2002). Some opportunistic species are able to take advantage of the changed habitat conditions and the attendant reduced abundance of some species, giving rise to a short-term increase in local biodiversity (Edgar et al., 2003; Yamamoto et al., 2003); this is an example of why biodiversity statistics alone are not a reliable indicator of environmental health. Recovery time for sites varies as a function of the type of oil spilled, the biological assemblage impacted, substrate type, climate, wave/current regime, and coastal geomorphology and ranges from years to decades depending on these and other factors (Ritchie, 1993; Jewett et al., 1999; French-McCay, 2004; Harris et al., 2016).

Seabed mining Mining of the seabed is carried out in mostly shallow shelf and coastal waters to extract heavy minerals, gold, diamonds, tin, and sand and gravel to nourish beaches and as a source of shell and aggregate for use in making concrete (Ellis, 2001). Such activities have the

Anthropogenic threats to benthic habitats 45 potential to impact upon benthic flora and fauna, planktonic ecosystems, fisheries, and marine mammals that utilize the area being mined. Where mining activities result in the removal of large volumes of bed material, changes in wave transformation, storm surge, bottom currents, and the dynamics of the shoreline can occur (Hobbs, 2002). Of all seabed mining activities aggregate extraction is by far the largest and most widespread. Statistics are difficult to obtain from most countries. However, in the United Kingdom, around 20 million tonnes of sand and gravel is extracted from an area of seabed equal to about 1500 km2 each year (Marinet, 2007). Studies on the impacts of sand/gravel extraction have been carried out in several countries including Japan (Tsurusaki et al., 1988), Australia (Poiner and Kennedy, 1984; Pattiaratchi and Harris, 2002), the United States (Drucker et al., 2004), and the United Kingdom (Hitchcock and Bell, 2004). Recovery from the effects of aggregate mining at three sites in the United Kingdom was studied by Boyd et al. (2004). These workers found that evidence of physical disturbance of the seabed and perturbation of benthic fauna was detectable from 3 and up to 7 years after mining had ceased. Disturbance of the sediments from mining can make available organic matter previously trapped among sediment particles, thus driving a temporary increase in the abundance of benthos (Boyd et al., 2004). Mining in the deep sea has, at the present time, not progressed beyond a few pilot studies to extract manganese nodules. Mining of metal rich sulfide deposits associated with an extinct hydrothermal vent system in the Manus Basin area of Papua New Guinea (http://www.nautilusminerals.com/s/Home.asp) is being planned but is yet to commence (Beaudoin and Smith, 2012). Hein et al. (2010) evaluated seamount-associated manganese crusts as a source of high-tech minerals, such as tellurium, cobalt, bismuth, thallium, and others. Recovery of mined sites is not expected to occur over timescales relevant to human life spans. In 1989 a group of German marine scientists started the DISCOL (DISturbance and reCOLonization) experiment in the Peru Basin of the eastern South Pacific Ocean. An area of seabed was ploughed and manganese nodules were removed over a control area to mimic the impact of mining operations. When the site was revisited in 2015, 26 years later, there was no evidence of recolonization or recovery of the disturbed area of seabed (Marcon et al., 2016). If commercial-scale mining for manganese nodules and/or metalliferous hydrothermal vent deposits were to proceed on a broad scale, there would potentially be significant environmental impacts, including loss of biodiversity (Van Dover et al., 2017). Impacts would include: (1) destruction of benthic communities where nodules/ore deposits are removed; (2) impacts on the benthos due to deposition of mobilized sediment; and (3) impacts in the water column in cases where mining vessels discharge a plume of sediment near the sea surface, thus affecting photosynthesizing biota and pelagic fish (Morgan et al., 1999; Sharma, 2001).

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Pollution Throughout the 20th century, there has been widespread use of the oceans as a global waste repository, for dredge spoil, sewage sludge, industrial chemical waste, worn-out ships, unwanted military hardware, and radioactive waste (Norse and Crowder, 2005; USCAE, 2007; Galgani et al., 2000). To this we must add the waste and litter that is inadvertently washed or blown into the oceans from land. One Remotely Operated Vehicle (ROV) survey on the mid-Atlantic ridge reported the “frequent occurrence of garbage (e.g., plastic bags and other objects) at all depths over very wide areas” (Galgani et al., 2000; see also Pham et al., 2014; UNEP and GRID-Arendal, 2016). Seafloor observations taken on 27 marine surveys carried out in European waters between 50 and 2700 m water depth were compiled by Galgani et al. (2000) who reported maximum concentrations of garbage (mostly plastic bags and bottles) of over 100,000 pieces of debris per km2. Some geomorphic features, like submarine canyons, interact with currents such that they become focal points for attracting litter (e.g., Mordecai et al., 2011). The effects of litter on marine biota are poorly understood. Since the London Convention on ocean dumping came into force in 1975 most countries have gradually reduced waste disposal in the ocean, although much (mostly inert) material is still disposed of into the ocean today. For example, in the United States, about 52 million m3 of dredged material from ports and shipping channels is disposed of at sea each year (USCAE, 2007). The disposal of all radioactive waste into the oceans was finally banned in 1994 under amendments made to the London Convention. Disposal has generally been proximal to the point of origin (closest deepwater area to major ports) although deep ocean trenches have been proposed for the disposal of various kinds of waste. The effects of waste disposal on marine biota are poorly understood.

Coastal development A major cause of habitat loss in coastal and inner-shelf environments derives from coastal development, the discharge of untreated sewage into coastal waters and other land-based discharges from various human activities. In their assessment of 12 once diverse and productive estuaries and coastal seas, Lotze et al. (2006) found that human impacts have depleted 90% of formerly important species, destroyed 65% of seagrass and wetland habitat and degraded water quality. In the Caribbean, Africa, and Latin America 80% 90% of sewage discharged into coastal waters is untreated, leading to widespread eutrophication, harmful algal blooms, and oxygen depletion (Rabalais, 2005). Apart from sewage, other land-derived pollutants are introduced as a result of agriculture (fertilizers and pesticides), logging (sediment), and mining (sediment and heavy metals). These effects can be locally cumulative, resulting in significant impacts on marine

Anthropogenic threats to benthic habitats 47 ecosystems and habitats.1 The degradation and destruction of coastal habitats resulting from human activities means a reduction in the available habitat for the maintenance of biodiversity (Rabalais, 2005).

Submarine cables It is estimated that there are approximately 430 submarine cables in current use, 1.1 million km in total length, draped across the seabed in the world ocean. When they are broken or become antiquated, the cables are abandoned. The exact number of abandoned cables is unknown but may equal many times the amount in current use. Close to the coast, submarine cables are laid in machine-excavated trenches where waves or strong currents prevail but otherwise they are simply draped across the seabed. Apart from damage caused by trenching, subsequent vibration or movement of the cable can damage the seabed. On the remote Lord Howe Rise in the South Pacific, the only human impact on the benthic environment detected was the identification of elongate furrows in bottom photographs attributed to telecommunication cable-laying activities, presumably caused by simply lowering the cable onto the seabed (Harris et al., 2012). Two studies on the impacts of submarine cables published from sites in the Baltic Sea (Kogan et al., 2006) and off the coast of California (Andrulewicz et al., 2003) showed few changes in the abundance or distribution of benthic fauna based on video observations (epifaunal) and sediment core samples (infauna). Overall the results indicate that the biological impacts of cables are minor at most. In the California study (Andrulewicz et al., 2003) it was found that Actiniarians (sea anemones) colonized the cable when it was exposed on the seafloor, and were therefore generally more abundant on the cable than in surrounding, sedimentdominated seafloor habitats. Some fishes were also more abundant near the cable, apparently due to the higher habitat complexity provided.

Shipping The impacts of shipping include the introduction of exotic species and ship-generated noise in the environment.

Introduction of exotic species The impact of shipping on the natural distribution of species has been locally dramatic. Some commercially valuable species have been deliberately transported to different locations for the production of food and ornaments (fish for aquaculture, aquarium 1

The literature on the effects of coastal pollution on the marine environment is vast; good reviews can be found in the volumes edited by Norse and Crowder (2005) and Nellemann et al (2008).

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specimens, pearls or pearl shell, etc.; Carlton and Ruiz, 2005). Most exotic species have, however, been accidentally introduced from one continent to another by ships that unwittingly carry plants and animals attached to their hulls or else contained in ballast water (Briggs, 2007). Mollusk species simply attach themselves to the hull, while planktonic algae, dinoflagellates, fish, spores, and larvae can be pumped aboard when the ship takes on ballast. When the ship arrives at a port, it discharges its ballast to take on cargo. Animals and plants that attached themselves to a ship’s hull in one port can be dislodged and dropped off in another. In these ways, an estimated 15,000 exotic species are carried around the world (Fig. 3.5) and dispersed between different ports every week (Carlton and Ruiz, 2005). In some cases the introduced species can outcompete and replace the native species occupying a similar ecological niche. Canal digging provides another pathway for exotic species to be introduced to new areas. When the Suez Canal was opened in 1869 the shipping route between Europe and Asia was shortened by about 4400 km, but a link was also formed between two previously separate bodies of water—the Red Sea and the Mediterranean Sea. Since the sea level in the Red Sea is slightly higher than the Mediterranean (due to evaporation exceeding precipitation in the Mediterranean), water flows in only one direction through the canal toward the Mediterranean. The water has carried some 300 species of plants and animals from the Red Sea that have begun to colonize the Mediterranean, including some deepwater species.

Figure 3.5 Global impact of invasive species. Source: From Nellemann, C., Hain, S., Alder, J., eds., 2008. In Dead Water—Merging of Climate Change With Pollution, Over-Harvest, and Infestations in the World’s Fishing Grounds. United Nations Environment Programme and GRID-Arendal, Arendal, Norway.

Anthropogenic threats to benthic habitats 49 The new arrivals, comprising the so-called Lessepsian migration (Por, 1978), have replaced many of the natives such that today 30% of fish caught in Israel are Red Sea migrants. The breach in the barrier at Suez has allowed a trans Indian-Mediterranean/Atlantic invasion to occur. In this context, the threat of breaching land bridges between seas in at least one other location, Panama, has major implications for the mixing of separate populations. The two sides of Panama have been separated for at least 3 million years and species once common to both sides have now evolved into different species. The present Panama Canal uses locks to lift vessels 25.9 m into a large freshwater lake, which is an effective barrier to marine species. Although the possible construction of a sea level canal in Panama is not presently on the agenda for the Panamanian government, the idea has been put forward in the past (McCullough, 1977).

Noise Anthropogenic noise in the oceans is another direct impact from shipping, but is also caused by commercial seismic surveys for oil and gas (see above), military sonar operations, and other human activities (e.g., jet skis, motor yachts, and wind turbines). However, noise from shipping is the largest and most widely dispersed source in the ocean. Anthropogenic ocean noise interferes with breeding and feeding, displaces animals from their habitat and may injure or even kill animals. Many species as disparate as fish, giant squid, dolphins, and whales are affected. Sound in the ocean travels as vibrations of water molecules that exert push pull pressure on objects in their path. Sound is heard by push pull of the ear or hearing mechanism of an animal and it similarly exerts pressure on the rest of the animal. Sound frequency is the rate of oscillation or vibration measured in cycles per second, known as Hertz (Hz). Ultrasonic frequencies are too high to be heard by humans (greater than 20,000 Hz) but may be heard by dolphins. Infrasound is too low to be heard by humans (less than 20 Hz) but can be heard by baleen whales (Richardson et al., 1995). Commercial container ships, tankers, and other large freighters generate noise in the frequency range of 10 1000 Hz, which coincides with frequencies used by marine mammals for communication and navigation. Sound energy dissipates as a function of the distance squared, so the impact of noise on benthic communities is greater for shallow water habitats closer to the sound source (at the sea surface) than for habitats in greater (off-shelf) water depths. It is not only large marine mammals that are affected; one recent study has documented a response of invertebrates to noise (Simpson et al., 2011). However, few papers have been published on the impacts of noise on benthic ecosystems (Inger et al., 2009).

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Climate change Predicting the impacts on benthic habitats caused by global climate change is difficult because ocean ecosystems themselves are complex and poorly understood. Humans have increased the concentration of greenhouse gases in the global atmosphere, particularly carbon dioxide, through the combustion of fossil fuels, cement production, agriculture, and deforestation. The concentration of CO2 in the atmosphere has been increasing from its preindustrial level of about 280 parts per million (ppm) to over 400 ppm today. Increased greenhouse gas concentrations are expected to cause acidification and warming of the ocean, changes to ocean circulation patterns, sea level rise, changed evaporation and precipitation patterns, and changes to ocean wave patterns, among a range of other effects. Climate change impacts will combine with other pressures, exacerbating their effects in many cases (Rahmstorf, 1997; Caldeira and Wickett, 2003; Hughes et al., 2003; Pandolfi et al., 2003; Feely et al., 2004; Hoegh-Guldberg, 2005; Coleman and Koenig, 2010).

Acidification The increasing amount of dissolved CO2 in the oceans has the effect of lowering the pH, making seawater more corrosive to calcium carbonate (Doney et al., 2009). This causes stress to any organism that builds shells because the lower pH increases the energy needed to build shells out of calcium carbonate. The surface waters of the oceans are slightly alkaline, with an average pH of about 8.2, although this varies across the oceans by 6 0.3 pH units because of local, regional, and seasonal variations. When CO2 dissolves in seawater it forms a weak acid, called carbonic acid. Part of this acidity is neutralized by the buffering effect of seawater, but the overall impact is to increase the acidity (lower the pH). The dissolution of CO2 has already lowered the average pH of the oceans by about 0.1 unit from preindustrial levels (Caldeira and Wickett, 2003). These small changes in ocean chemistry could have major impacts on some pelagic calcifying organisms. For example, ocean acidification is likely to affect calcification of foraminifera, a group of calcite-producing protists. As ocean pH declines, it might be expected that calcifying organisms in near-polar areas, where pH is the lowest, will be affected first. The other frontline area for ocean acidification is the benthic community living at the depth where the calcium carbonate compensation depth (CCD) intersects the seafloor. Below this depth calcium carbonate dissolves, but ocean acidification is causing the CCD to rise at a rate of 1 or 2 m year21; by the year 2100 it will have risen around 100 200 m. Owing to the higher solubility of aragonite, corals, and pteropods, that produce CaCO3 in its aragonite form, will be more strongly affected than the coccolithophores and foraminifera which produce the calcite form (Feely et al., 2004). It has been predicted that

Anthropogenic threats to benthic habitats 51 if CO2 emissions continue on current trends the aragonite saturation horizon will rise to the surface of the oceans before the end of this century, making aragonite skeletons unstable throughout the water column of the entire ocean (Caldeira and Wickett, 2003; Hughes et al., 2003; Pandolfi et al., 2003; Feely et al., 2004; Hoegh-Guldberg, 2005).

Ocean warming and coral bleaching The most obvious effect of the rising CO2 concentrations in the atmosphere is an overall warming of the oceans (attendant with greenhouse warming of the atmosphere). In the 2015 northern hemisphere and 2015 16 southern hemisphere summers, the third global coral bleaching event commenced, following similar events in 1998 and 2010. The third event, which is ongoing at the time of this writing (December 2018), is the longest and most damaging ever recorded. To date it has affected 70% of the world’s reefs, with reefs in some areas experiencing annual bleaching since 2015. Australia’s Great Barrier Reef has been particularly hard hit, with more than 50% of the reef impacted since 2016 (GRMPA, 2017). O’Neill et al. (2017) concluded that there “is robust evidence (from recent coral bleaching) of early warning signals that a biophysical regime shift already may be underway.” Veron et al. (2009) predicted the coral reef bleaching tipping point (an abrupt change in state that occurs when a threshold value is exceeded) would occur once global atmospheric CO2 reached 350 ppm. This value was reached in about 1988, but because ocean warming lags behind global atmospheric CO2 levels (Hansen et al., 2004) it has taken almost 30 years for the impact of this level of CO2 to be revealed. In effect the ocean is currently responding to CO2 levels of decades ago and the balance of evidence indicates that a tipping point for coral bleaching has now been passed (Hoegh-Guldberg et al., 2007; Frieler et al., 2013; Hughes et al., 2017). The combination of thermal stress and acidification of the oceans will affect most coral reefs and experts agree that the coral reefs that survive to the end of the 21st century, will bear little resemblance to those we are familiar with (Hughes et al., 2017). Coastal and shelf species will also have to adjust to the gradual poleward shift of climatic belts as global warming proceeds. Human land uses often create “islands” of habitat surrounded by developed land, which precludes species from migrating as climate changes, thus causing local extinctions. Local variations in the response to global warming will mean that the generalized pattern of poleward migrating ecosystems may not occur everywhere; some habitats may disappear locally with different habitats being created in their place. Warming may not affect locations that have strong buffering processes (e.g., where ocean temperature is governed by upwelling of cold ocean water masses). A poleward retreat path is not available to coastal or shelf species at the southern ends of

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South Africa, South America, or Tasmania (to name a few locations) owing to geography. The response to warming is therefore complex and difficult to predict at local, regional, and global levels.

Changes to ocean circulation The oceanic responses to global warming include the possible slowdown of ocean thermohaline circulation (Fig. 3.6), deduced mainly from studies of coupled oceanatmospheric computer models. Observations of the extent of winter sea ice cover in both the northern and southern hemispheres show significant reductions over the past 50 years, and some model results suggest that this might reduce, or even shut down, thermohaline circulation in the ocean over the next century (Rahmstorf, 1997; Wu and Budd, 1999; Bi et al., 2001). Such changes could profoundly affect surface ocean productivity, the strength of major ocean surface currents like the Gulf Stream and the ventilation of the deep oceans, leading to less food and oxygen for deep-sea benthic communities (Joos et al., 2003; Broecker, 2005; Shaffer et al., 2009; IPCC, 2018). Limits in the ability of models to accurately predict ocean response to climate change mean that such scenarios are speculative. However, the consequences of a slowing or shutdown of thermohaline circulation are potentially catastrophic for oceanic benthic ecosystems.

Figure 3.6 The global ocean “conveyor” thermohaline circulation (Wu and Budd, 1999; Bi et al., 2001; IPCC, 2018). Bottom water is formed in the polar seas via sea ice formation in winter, which rejects cold, salty (dense) water. This sinks to the ocean floor and flows into the Indian and North Pacific Oceans before returning to complete the loop in the North Atlantic. Numbers indicate estimated volumes of bottom water production in “Sverdrups” (1 Sverdrup 5 1 million m3 per second), which may be reduced by global warming because less sea ice will be formed during winter.

Anthropogenic threats to benthic habitats 53

Global sea level rise Global warming is predicted to cause a rise in mean sea level by as much as 1 m by the year 2100 (Hansen et al., 2016). Sea level has risen about 19 cm in the last 100 years and the rate is getting faster; it was rising about 1.7 mm year21 at the end of the 20th century and is now rising at around 3.4 mm year21; the absolute magnitude of sea level rise by the year 2100 is strongly dependent upon whether or not the East Antarctic ice sheet collapses (Hulbe, 2017). Rising sea level will change the configuration and habitat composition of the coastline by inundating wetlands and other low-lying coasts, inducing erosion to beaches, and increasing the salinity of estuaries, bays, and groundwater tables. As sea level rises, low-lying areas that are not directly inundated will experience more frequent and higher storm surges. The human response to sea level rise will include armoring coastlines to protect real estate, thus cutting off the natural (landward) retreat path of coastal and intertidal organisms. Coastal development that has occurred on low-gradient, sandy coastlines is the most vulnerable, since the natural response of such systems is to retreat landward as sea level rises. Although a positive net sediment supply will ensure many atolls will maintain their freeboard and possibly continue to expand in spite of rising sea levels (Webb and Kench, 2010), the demise of coral reefs from bleaching (caused by warmer ocean surface temperatures) and acidification will counteract natural reef-growth processes. The result is that many inhabited coral atolls, that have only a few meters of freeboard, are under direct threat of becoming uninhabitable when their water tables disappear or they become submerged when sea level rises.

Changes to evaporation/precipitation patterns Changes in rainfall obviously impact terrestrial ecosystems but there are consequences for the estuarine and coastal ecosystems as well. Habitats within estuaries and river deltas are intimately related to fluvial systems and their delivery of water, nutrients, and sediment to the coastal zone. Primary production is often related to freshwater (and nutrient) discharge, for example. Animals and plants that have evolved to tolerate a certain salinity range may be unable to survive in coastal areas impacted by severe changes in precipitation and evaporation patterns (Baldwin and Mendelssohn, 1998). For example, climate change is expected to cause increases in Arctic river discharge (Bring et al., 2017), which will in turn cause spatiotemporal changes in coastal and estuarine salinity patterns, thus affecting the dependent ecosystems. In arid locations, such as Australia, reduced rainfall has been linked to reduced coastal primary production (Auricht et al., 2018).

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Changes to storm intensity and ocean swell waves Another apparent response to the warming of the Earth’s atmosphere is a change in the ocean wave climate, manifested as increased wave heights associated with more intense storm events (Hemer et al., 2013). Changes in wave regime may affect the stability of sandy shorelines and potentially dramatic changes in coastal geomorphology may occur locally. For example, the transformation from tide-dominated to wave-dominated coastal systems is possible in some locations (Harris et al., 2002). On the continental shelf increased wave height and period translates into an increase in the water depth at which sediments may be mobilized, thereby fundamentally changing the character of the seabed habitat. For example, areas of sandy seafloor previously stable under the prevailing wave and current regime may become transformed into a different habitat type, subject to mobilizing forces of episodic storms (Harris and Hughes, 2012).

Changes to sea ice Satellite observations since 1979 have documented a 38% decline in the area of Arctic sea ice cover at the end of summer. Arctic Ocean ecosystems have responded dramatically to the loss in sea ice cover. Warmer ocean conditions coupled with changes in ocean circulation and ecological processes are already causing profound changes to the ranges and ecology of Arctic fish (Hollowed et al., 2013a,b; Christiansen et al., 2014), benthos (Kortsch et al., 2012), birds, and mammals (Wassmann et al., 2011; Descamps et al., 2017). It is estimated that in a seasonally ice-free Arctic, the prolonged period of open water conditions could result in a threefold increase in primary productivity (Arrigo et al., 2008). The reduced sea ice cover makes a range of benthic habitats accessible to ships and therefore to industrial pressures for the first time in human history, in areas that have little or no protection within MPAs (Harris et al., 2018). Melting permafrost, coupled with increased coastal swell waves (resulting from more frequent and extensive open water conditions) are causing rapid erosion of the Arctic coastline (Benjamin et al., 2018), thus destabilizing many dependent coastal habitats and probably impacting adjacent inner-shelf habitats. While Arctic sea ice is clearly reducing in area due to anthropogenic climate change, the trend in the Antarctic appears less clear, with evidence for local increases in sea ice area; the most likely explanation is linked to oceanic responses to changing atmospheric circulation patterns (Serreze and Meier, 2018).

Wind farms Inger et al. (2009) reviewed the positive and negative ecological effects of offshore renewable energy installations, including wind turbines. The negative aspects include the displacement of animals from their habitat, noise generated by the machinery, and

Anthropogenic threats to benthic habitats 55 electromagnetic fields generated along the cables that join the turbine to the onshore electricity grid. Positive aspects are that the structures may form artificial reefs and fish aggregation points and they act as small marine protected areas because of the exclusion zones needed around each installation. From a habitat perspective, wind turbines are preferentially built on hard substrates to provide for a secure foundation. Multibeam sonar mapping work is commonly undertaken to find suitable rocky substrate for installation sites. This may mean that rocky habitats are preferentially targeted for wind farm construction. Rocky habitat types are by far the smallest in proportional area (compared with soft sediment habitat) in most bioregions. They provide critical habitat for many species which increases their conservation value, while at the same time they are targeted for other human uses, such as fishing and tourism (scuba diving).

Concluding remarks Anthropogenic threats to benthic habitats are a key driver underpinning the need for building accurate and comprehensive habitat maps. Habitat mapping provides condition assessments and establishes baselines against which changes can be measured. Repeated mapping and sampling are essential for quantifying change, measuring impacts, and tracking recovery of impacted and degraded habitats. Habitat mapping is viewed by many government agencies as an essential component of ecosystem-based management. Destructive fishing practices are viewed by GeoHab scientists and many other experts as the greatest single threat to the marine environment (an order of magnitude greater than the total extent of all other activities according to Benn et al., 2010). However, it is important to recognize that human impacts are cumulative. Destructive fishing, pollution, mining, climate change, etc. often affect the same habitats and the benthos are simultaneously affected by more than one stressor. One final theme that emerges from the literature (and from the case studies) is that the responses of benthic habitats to anthropogenic pressures (singly or cumulatively) are poorly understood. It is therefore often difficult to give reliable, scientifically defensible answers to questions as to how a habitat or ecosystem will respond to any particular pressure (or combination of pressures). This situation is exacerbated by the ocean floor being out of sight from public view so that we are not aware of the full extent of the impacts and damage we cause. The greatest threat to the oceans from humans may simply be ignorance.

Acknowledgments This chapter is updated from the version published in the 2012 volume with minor additions to references and text as needed. The authors acknowledge the financial assistance of UN Environment/GRID-Arendal.

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Further reading MAR-ECO Expedition, Deep sea search finds species surprises. ,http://www.msnbc.msn.com/id/5610557/.. PARLOC, 2001. The Update of Loss of Containment Data for Offshore Pipelines—Prepared by Mott MacDonald Ltd. for: The Health and Safety Executive, The UK Offshore Operators Association and The Institute of Petroleum. Mott MacDonald Ltd., Croydon, p. 161.