Shelf and deep-sea sedimentary environments and physical benthic disturbance regimes: A review and synthesis

Marine Geology 353 (2014) 169–184

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Review article

Shelf and deep-sea sedimentary environments and physical benthic disturbance regimes: A review and synthesis Peter T. Harris ⁎ Environmental Geoscience Division, Geoscience Australia, GPO Box 378, Canberra, ACT 2601, Australia

a r t i c l e

i n f o

Article history: Received 8 June 2013 Received in revised form 17 March 2014 Accepted 26 March 2014 Available online 15 April 2014 Communicated by D.J.W. Piper Keywords: disturbance regime physical sedimentology continental shelf continental slope abyssal seafloor benthic storm turbidity bottom currents intermediate disturbance hypothesis

a b s t r a c t Physical disturbances of the seafloor play a key role in ecosystem function and are postulated to exert control over spatial patterns of biodiversity. This review investigates the role of natural physical sedimentological processes that occur in shelf, slope and abyssal environments that also act as disturbances to benthic ecosystems and which, under certain circumstances, give rise to benthic disturbance regimes. Physical sedimentological processes can cause both press (process that causes a disturbance by acting over a timespan that is intolerable to benthos) and pulse (process that causes a disturbance by exceeding a threshold above which benthos are unable to remain attached to the seabed or are buried under rapidly deposited sediment) types of disturbance. On the continental shelf, pulse-type disturbances are due to temperate and tropical storm events, and press-type of disturbances identified here are due to the migration of bedforms and other sand bodies, and sustained periods of elevated turbidity caused by seasonally reversing wind patterns. On the continental slope and at abyssal depths, pulse-type disturbances are due to slumps, turbidity currents; benthic storms may cause either press or pulse type disturbances. A possible press-type of disturbance identified here is inter-annual changes in abyssal bottom current speed and/or direction. It is concluded that: 1) physical sedimentary disturbance regimes may characterize as much as 10% of the global ocean floor; 2) multidisciplinary research programs that integrate oceanography, sedimentology and benthic ecology to collect time series observational data sets are needed to study disturbance regimes; and 3) predictive habitat suitability modeling must include disturbance regime concepts, along with other biophysical variables that define the fundamental niches of marine species, in order to advance. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.

1. Introduction Research work conducted in shelf and deep-sea environments over the last decade has highlighted the importance of physical disturbances in understanding benthic ecosystem function and biodiversity. Kostylev (2012) notes that the “interaction of sediment and flow as a most common agent of natural disturbance, together with the effects of benthic organisms on this interaction, are at the core of benthos-sediment coupling”. Natural disturbances capable of removing, burying or killing the existing benthos create patches of clear space available for colonizing organisms. After such events, an ecological succession ensues with the early colonizers eventually replaced by a climax community consisting of more abundant and larger animals with higher bioturbation rates and deeper mixing depths than those which existed prior to the depositional event. The assemblage present at any one time is therefore governed by the rate of ecological succession and the spatial and temporal attributes of physical seafloor disturbances (e.g. Thistle, 1981, 2003).

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http://dx.doi.org/10.1016/j.margeo.2014.03.023 0025-3227/Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.

Disturbances of the seafloor are, of course, also caused by human activities and much research has been carried out to quantify the impact and the rates of recovery of marine life from anthropogenic disturbances. Examples include bottom trawling for fish (Collie et al., 2000; Thrush et al., 2005; Puig et al., 2012), aggregate and mineral seabed mining (Jewett et al., 1999; Hobbs, 2002), port construction and shipping channel maintenance, laying of pipelines, oil spills and oil and gas exploration and production (Gates and Jones, 2012). In the deep sea, the potential for future manganese nodule mining precipitated research into the possible impacts on, and responses of, the benthos (Jankowski et al., 1996; Morgan et al., 1999; Sharma, 2001). In general, these studies are based upon an artificial, deliberate disturbance of an area of seabed (or installing artificial surfaces representing the seafloor) and measuring the rates of colonization and regrowth of the original community. There are, however, differences between studies based on artificially manipulated environments versus the study of natural disturbances, and results from manipulated studies should be used with caution to infer natural rates and processes (Tyler, 2003). Examples of natural physical sedimentary processes that disturb benthic ecosystems include continental shelf sediment mobilization during extreme storm events (Williams, 1988; Preen et al., 1995;

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P.T. Harris / Marine Geology 353 (2014) 169–184

Halford et al., 2004), submarine canyons and fans subject to pulses of sediment influx from slope sediment failures (Young et al., 2001; Hess et al., 2005) and benthic storms that mobilize sediments at abyssal depths. However, there have been few studies published regarding recovery rates of the benthos from natural disturbances at shelf depths and even fewer published studies on the continental slope and at abyssal depths (Kostylev, 2012). The study of such dynamic sedimentary environments (and ecosystems) requires a multidisciplinary approach involving the collection of co-located marine geological and benthic ecology time-series data. Despite the clear linkages that exist between dynamic shelf and deepsea sedimentary environments and the benthic ecosystems that they support, there is surprisingly little known about their interdependencies or interactions. In order to be able to model and predict biological recovery of benthic habitats severely disturbed by human activity (such as fishing, waste disposal, seabed mining and anthropogenic global climate change), we must first understand and be able to quantify the natural disturbance processes with which the benthos are inextricably linked. 1.1. Scope and aims In this review, disturbance regime theory of dynamic sedimentary environments is considered in the context of benthic ecology. Examples of faunal succession rates documented for sedimentary continental shelf environments are compared with examples of shelf disturbance regimes driven by storms and other sediment suspension and transport processes. An overview of deep-sea disturbance regimes highlights the significance of benthic storms and the episodic, down-slope gravity flows characterizing submarine canyons and fan complexes. Finally the applications of disturbance regime theory to predictive habitat mapping (habitat suitability models) are considered. Only physical disturbance of the benthos related to dynamic sedimentary processes is addressed in this review; biotic (e.g. predation, nutrient availability), chemical (e.g. dissolved oxygen, salinity, pH), glacial or iceberg-related disturbances or any anthropogenic agents, among many others, are not included. It is acknowledged that, although we focus here on one set of physical sedimentological disturbance processes, many natural disturbance processes are contemporaneous and may interact with one another resulting in complex ecological responses (e.g. Levin and Dayton, 2009). The aim of this review is to highlight aspects of marine geoscience where further research could help to improve our understanding of marine sedimentary ecosystems in shelf, slope and abyssal environments. 2. Definition of “disturbance regimes” 2.1. Disturbances clear patches of habitat for recolonization A fundamental tenet of landscape ecology is that ecosystems and species evolve in response to a particular regime where environmental disturbance can play a significant role in controlling such things as life cycles, food and nutrient supply and habitat availability (Thistle, 1981). A definition of disturbance was provided by Pickett and White (1985) as “any discrete event in time that disrupts ecosystem, community or population structure and changes resources, substrate availability, or the physical environment” (i.e. alters niche opportunities for the species capable of living in a given setting). For the purposes of this discussion, emphasis is placed on substrate availability and a “disturbance” will be considered to create a patch of open space that is available for opportunistic species to colonize (see Sousa, 2001, for further discussion on the concept of “disturbance”). For landscape ecologists, storms causing a large tree to fall in the forest, fire destroying an area of forest or scrubland and a tree succumbing to drought are examples of important disturbances that create patches of open space. An ecological succession ensues, with different species arriving over time and competing for space, until the disturbed patch finally

reverts to a mature, fully recovered, state (Connell, 1978; Huston, 1979). Hence, landscapes that are subject to disturbances exhibit a degree of patchiness that relates to past disturbances, their colonization by opportunists and gradual recovery. Hierarchies of patches coexist at multiple scales, created by a range of physical and biological processes (Wu and Loucks, 1995). Patchy landscapes, taken as a whole, contain a greater number of species (greater biodiversity) per unit area than either the disturbed or undisturbed habitat alone. Examples of physical disturbances involving seabed sediments include muddy seabeds of the continental shelf mobilized during extreme storm events (Swift et al., 1981; Morton, 1988); macrotidal estuarine sediment regimes subject to severe storm events (e.g. Yeo and Risk, 1979; Harris and Collins, 1988); the migration of large sedimentary bedforms burying benthos (e.g. Daniell et al., 2008); seasonal sediment pulses entering the heads of shelf-incising submarine canyons (Okey, 1997; Ogston et al., 2000; Mullenbach et al., 2004); and submarine fans subject to sediment influx from slope sediment failures (e.g. Posey et al., 1996). Such processes can exert a physical stress on organisms, tearing plants from their place of attachment (Thomsen et al., 2004), mobilizing sediment, burying plants and animals (Aller and Todorov, 1997), damaging organisms by abrasion (Cheroske et al., 2000), or by limiting light availability (Carruthers et al., 2002; see also reviews by Hall (1994), and Sousa (2001)). In each of these examples, a natural sedimentary process gives rise to a disturbance that disrupts the ecosystem, community or population structure and changes the availability of habitat or resources. Natural physical disturbance is the dominant effect structuring benthic communities (Hall, 1994; Sousa, 2001). However, there are also bioturbation effects of benthos on sediments. These include sediment stabilization, sediment mixing, biodeposition, compaction, and hydrodynamic effects (e.g. Murray et al., 2002). For example, Botto and Iribarne (2000) describe how the effects of different species of burrowing crabs may cause the same sediment type to be either more easily eroded or more difficult to erode; one species stabilizes the sediment by placing fine and cohesive sediment on the surface, while another disrupts the sediment by pelletizing it and making it more easily eroded. Although in this review we focus on physical disturbance of sedimentary environments, it is acknowledged that the sedimentary environments are, in turn, effected by the benthos. 2.2. The intermediate disturbance hypothesis The effects of disturbances on biodiversity have been conceptualized by the “intermediate disturbance hypothesis” (IDH; Connell, 1978; Huston, 1979). Where disturbances are too frequent, diversity is low because few species can thrive under such stressful conditions. Where disturbances are rare or infrequent, competitive exclusion takes its toll as weaker, less-well adapted species are eliminated. The IDH predicts that it is the intermediate zone of quasi-stable environments that allow for the greatest diversity of species to exist, as shown in coral reef studies by Connell (1978) and in a number of other studies of marine benthic communities (Sousa, 2001; see review by Hughes, 2012). If the IDH applies to complex communities such as coral reefs (Connell, 1978), then it seems reasonable that it should apply more broadly to other marine environments, as has been suggested by Field (2005). From his analysis of natural and anthropogenic shelf processes, Field (2005) concluded that “every habitat represents a time-averaged response to the dominant physical processes, which is as important in defining the habitat as geologic setting and community structure.” Kostylev and Hannah (2007) proposed that habitats are best understood within a “disturbance” – “scope for growth” stability diagram, which, according to ecological theory, defines traits of species and emergent properties of ecological communities such as species competition and biodiversity. Kostylev (2012) noted that, from a physical sedimentological perspective, the quadrants of the “disturbance” – “scope for growth” stability diagram can be plotted on a Hjulstrom (1935) diagram

P.T. Harris / Marine Geology 353 (2014) 169–184

(Fig. 1), thus illustrating the direction connection between sedimentology and ecology (see also Snelgrove and Butman, 1994). 2.3. What constitutes a “disturbance regime”? In this discussion, a “disturbance regime” is defined as existing when the disturbance process occurs at a frequency that is comparable to the rate of ecological succession (i.e. the criteria are met for an intermediate disturbance in the context of the IDH). The time required for an ecosystem to recover from a disturbance will depend on the spatial extent and intensity of the disturbance. A localized disturbance such as a few kelp holdfasts breaking free during a gale will require less time to recover than if an entire kelp forest is affected by a severe storm (Thomsen et al., 2004). With the advent of long-term oceanic monitoring stations, there is growing evidence of short-term (intra-annual) variability in benthic species composition at a given site, responding to subtle variations in food supply, water temperature and currents (Matabos et al., 2014). Such variations in benthic species composition do not constitute a disturbance, as defined here, since they do not give rise to a cleared patch of habitat available to colonizers. The climatic regime and water depth are factors too, since ecological processes are generally slower in cold-deep than warm-shallow ecosystems (Levinton, 2001); cold-deep ecosystems might generally be expected to take longer to recover from a disturbance than warm-shallow ecosystems (Fig. 2). Habitats characterized by larger, long-lived species will require more time to recover than habitats containing mostly smaller, short-lived species. Other factors might include proximity to source stock for larvae, availability of food and connectivity (Condie et al., 2005). To cause a disturbance that will create a patch of disturbed habitat and result in an ecological succession, the flow must achieve some critical threshold level compared with the capacity of the community to withstand the event and to recover from it. For example, Harris and Hughes (2012) proposed using Shields (1936) non-dimensional parameter θc: θc ¼

τc gðρs −ρÞd

ð1Þ

where τc is the critical bed shear stress required to initiate sediment motion, ρs is sediment density, ρ is water density and d is grain diameter. Disturbance of the benthos is likely to occur when the sedimentological

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conditions are met for the formation and migration of large bedforms (Harris and Hughes, 2012), which coincides with a Shield's parameter (non-dimensional bed shear stress) value of 0.25. This value is several times larger than that required to initiate traction bedload transport (~0.05) and falls in the middle of the ripple and dune bedform stability field. It is also important to distinguish between flows that have a frequent, repetitive, periodic nature and those that are rare and episodic. Processes that are at too high a frequency, like tidal currents or internal waves that are capable of generating strong, sediment transporting flows (Pomar et al., 2012), are semi-continuous over long (Nmonthly) time scales, such that the inhabiting benthos are adapted to the strong currents and high levels of turbidity. This is not to say that species that have evolved to exploit high-energy (e.g. macrotidal) habitats cannot be impacted by even higher energy storm events. In fact such an example has been documented in the Bay of Fundy, Canada (Yeo and Risk, 1979), which emphasizes the point that disturbance is not defined by any particular magnitude of current speed, but rather by periodic or episodic maxima that significantly exceed mean background values. In contrast, processes that are too infrequent (e.g. tsunamis, slumps and slope failures) will only create patches of disturbed/recovering habitat very rarely. For most of the time they support only the mature, fully recovered biological assemblage. A “disturbance regime” exists, therefore, when patches of disturbed habitat, coexist with patches of partly recovered habitat and other patches of fully recovered habitat; the surface area of disturbed, recovering and fully-recovered habitat are of comparable size within a defined spatial frame of reference. The disturbance process occurs at a great enough intensity to create a cleared patch of habitat at an intermediate frequency that is comparable to the rate of ecological succession (Sousa, 2001; Harris, 2012). In their modeling study of Australian shelf disturbance regimes, Harris and Hughes (2012) proposed a dimensionless ecological disturbance index (ED), given as: ED ¼ FA

ES RI

ð2Þ

where ES is the ecological succession rate for different substrates, RI is the recurrence interval of disturbance events and FA is the fraction of the frame of reference (surface area) disturbed.

Fig. 1. Comparison of: (A) quadrants of Kostylev and Hannah's (2007) habitat template where “disturbance” is defined as the ratio of the characteristic friction velocity to the critical shear stress required for initiation of sediment movement and scope for growth includes environmental factors that pose a cost for physiological functioning of organisms and limit somatic growth and reproduction (e.g. oxygen saturation, food availability, temperature); (B) dynamic zones of modified Hjulstrom (1935) diagram with the same four quadrants as in “A” (after Kostylev, 2012), demonstrating the direct linkages between sediment dynamics and benthic ecology. Hydraulically smooth flow of a fluid having a density (r) and viscosity (µ) occurs over flat beds comprised of sediment grain size (D) when the Reynolds number Re = rµ * D/µ b 3.5 and hydraulically rough flow occurs when Re N 100 (hydraulically transitional flow occurs for 3.5 b Re b 100).

P.T. Harris / Marine Geology 353 (2014) 169–184

Sa nd

Mu d

172

Equilibrium Community

el av Gr ef

Re

Transition Community Sa nd

ef

Re

1 - 10

Colonisation Community 100 - 1000

10 - 100 Time (Years)

20

Shelf

0 0.1

Abyss (polar)

De ep er

40

el av Gr

1.0

10

Co lde r-

60

DISTURBANCE

% Recovery

80

Mu d

100

Estuary (temperate-tropical)

Time (Years) Fig. 2. Rate of ecological succession: generalized relationship between elapsed time versus percentage of recovery for different benthic communities as a function of substrate type depth, and temperature (after Harris, 2012, based on references listed in Table 1).

Values of the disturbance index (ED) of between 0.2 and 1 are suggested by Harris and Hughes (2012) as ensuring the greatest likelihood of patches of disturbed habitat coexisting with patches of partly recovered habitat and other patches of fully recovered habitat, with all three types having a comparable areal extent. For a disturbance regime to exist, patches of disturbed habitat created by an event must be less than 100% of the frame of reference (FA must be fractionally less than 1). The spatial frame of reference for defining FA is determined, in turn, by the spatial footprint of the physical process. An individual disturbance event will have greater or lesser impact on one part of an area of seafloor over another for a number of different reasons related to inhomogeneity in seafloor composition (e.g. seafloor topography, degree of sediment bioturbation, sediment grain size) together with stochastic differences in the sedimentary process. By analogy with forest fires, the frame of reference is an area of forest where fires occur and FA in this context is the fraction of the area (sum of patches) of forest cleared by any random fire event. In the marine environment continental shelves subject to storm events or areas of continental slope subject to turbidity flows may be viewed in a similar way. If the disturbance recurs at the same or lesser time intervals as the rate of ecological succession then the effects of the disturbance are visible for 100% of the time and the conditions for a disturbance regime are not met. At increasing values of RI (decreasing values of ED) it can be seen that ED is asymptotic to the x-axis and the proportion of time that disturbed or recovering communities are present is very small compared with the amount of time that the equilibrium community is present. Eventually we reach a point where RI is too large to have any significant influence on the ‘normal’ state of the community; Harris and Hughes (2012) suggest an arbitrary lower limit of ED ≈ 0.2. 3. Disturbances and ecological succession in shelf sedimentary environments 3.1. Ecological succession rates in shelf sedimentary environments Several studies have documented the ecology of shelf sedimentary environments (e.g. Gray, 1981). Some notable recent examples are Torres Strait benthic habitats (Haywood et al., 2008), the sand-lance habitat in mobile dunes of British Columbia, Canada (Barrie et al., 2012) and mobile sediment habitats of other shelves (Beaman et al., 2012; James et al., 2012; Reynolds et al., 2012; Robinson et al., 2012; Todd and Valentine, 2012; van Dijk et al., 2012; Van Lancker et al., 2012). A number of studies have estimated the recovery times of benthic habitats from anthropogenic disturbances (Table 1). There are,

however, very few published studies that have documented both natural physical disturbances and rates of ecological succession in dynamic shelf sedimentary environments (Table 1). Newell et al. (1998, their Fig. 17) summarized the results of several studies and provided a conceptual summary of ecological succession rates (ES) typical of different substrates within temperate estuaries. Recovery periods increased from less than 1 yr (ES b 1 yr) for muddy substrates, to several years for sandy to gravely substrates and to around 10 yr for rocky, reef-type habitats (Fig. 2). These rates are comparable to those reported by other workers for similar substrate types in temperate and tropical shelf environments as summarized in Table 1. From these values we can see that disturbances in tropical and temperate estuaries and inner shelf habitats having a recurrence interval (RI) of from 1 to 10 yr are most likely to yield ED approximately equal to unity, depending on the fraction of area (FA) disturbed during an event. Ecological succession and recovery rates following a disturbance are as much as an order of magnitude longer in colder (polar) environments for comparable substrates and habitats (Newell et al., 1998). Similarly, at abyssal depths the available evidence suggests that rates of ES are generally much longer for comparable substrate types (Table 1; Fig. 2). 3.2. Press and pulse — Physical disturbances in shelf sedimentary environments Physical processes capable of causing a disturbance in shelf sedimentary environments include both “press” and “pulse” types of process, in the context of Bender et al. (1984). Pulse-type processes have their impact because, by attaining great intensity, they are able to remove the benthos over a short period of time to create clear patches of habitat (Table 2). In pulse-type disturbances, it is the combination of the frequency and intensity of the disturbance pressure, compared with the endurance and rate of ecological succession of the biota, which determines whether a process will create clear patches of habitat and thus constitute a disturbance regime. Examples of pulse-type processes in shelf sedimentary environments, that have an intermediate frequency, include the mobilization of bottom sediments by seasonal temperate and tropical storms (eg. Harris and Heap, 2009; Hughes et al., 2009) or by the episodic intrusion of ocean currents onto the shelf (Harris and Hughes, 2012; Fig. 3A). “Press” type disturbances have their impact because they cause the removal of benthos and clearing of patches by operating over a prolonged period of time. In shelf sedimentary environments, examples include the sustained period of elevated turbidity that follows a storm or flood event (eg. Ogston et al., 2000), the migration of bedforms

P.T. Harris / Marine Geology 353 (2014) 169–184

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Table 1 Examples of ecological succession rates (ES) for different biological communities on different substrate types. Studies are classified as natural or artificial in terms of the cause of disturbance. Community and type of disturbance Artificial disturbance studies Intertidal cockle beds harvested by hydraulic suction dredging Estuarine molluscs, tube worms and starfish following dredging operations Shelf crustaceans and infauna disturbed by fishing gear Artificial sediment mounds deployed at 1240 m depth to study macrofaunal succession Small mollusks, ophiuroids, and large polychaetes disturbed by fishing gear Estuarine molluscs, tube worms and starfish following dredging operations Sponge, anemones and corals at 380 m depth on the Norwegian shelf Estuarine molluscs, tube worms and starfish following dredging operations UK shelf community 316 taxa dominated by Polychaeta and Crustacea, with hydroids, Mollusca and Bryozoa disturbed by aggregate mining Benthic invertebrates disturbed by gold placer mining, 9–20 m depth Adult bivalves and encrusting fauna, adult large burrowing species disturbed by fishing gear UK continental shelf sand body benthic community disturbed by aggregate mining Motile, scavenging animals and hemisessile macrofauna at N4000 m depth in the Peru Basin Sponges and soft corals shelf depths disturbed by fishing gear Estuarine and shelf temperate rocky reef and complex bioherm structures disturbed by dredging operations Mature biogenic reef, shelf depths, disturbed by fishing gear Abyssal nematode assemblage within a 5000 m deep manganese nodule field, Clarion-Clipperton zone, North Pacific Natural disturbance studies Meio- and macrofauna at the HEBBLE sites disturbed by abyssal benthic storms Seagrass on the US Virgin Islands shelf disturbed by storms Benthic foraminifers in a submarine canyon in the Bay of Biscay Seagrass on the Great Barrier Reef shelf disturbed by tropical cyclones Antarctic ice shelf collapse and observed 2 to 3-fold increase in glass sponge abundance and biomass Tropical coral reefs disturbed by cyclone Garardia coral bioherms at 620 m depth on Little Bahama Bank, coral colony age Continental slope epifauna disturbed by the 1929 Grand Banks turbidity current Abyssal plain infauna disturbed by turbidites

(e.g. Daniell et al., 2008) or the seasonal onshore–offshore migration of inner-shelf sand bodies (e.g. Storlazzi et al., 2013). It is the combination of the intermediate frequency and persistence of the disturbance pressure, compared with the endurance and rate of ecological succession of the biota, which determines whether a process constitutes a disturbance regime (Fig. 3B; Table 2). 3.3. Pulse — Shelf-wide, storm-induced disturbance regimes Storms (both temperate and tropical) are clearly one of the most important disturbance processes that affect the creation of patches of disturbed habitat on continental shelves (Fig. 3A). The sediment transport effects of storms have been documented in tropical and temperate shelf environments (e.g. Rachor and Gerlach, 1978; Morton, 1988; Gagan

Substrate type

ES Yr

References

Muddy-gravelly sand Mud Sand and mud Mud Mud Sand Mud with small rocks Gravel Sand and gravel

0.2 1 b1 2 2+ 2+ N3 3 2 to 3

Hall and Harding (1997) Newell et al. (1998) Kaiser et al. (2006) Kukert and Smith (1992) Thrush et al. (2005) Newell et al. (1998) Gates and Jones (2012) Newell et al. (1998) Newell et al. (2004)

Sand on cobbles Mud and sand Sand and gravel Abyssal mud Sand Rocky reef

N4 6+ 3 to 7 N7 8 8–10

Jewett et al. (1999) Thrush et al. (2005) Boyd et al. (2004) Bluhm (2001) Kaiser et al. (2006) Newell et al. (1998)

Rocky reef Manganese nodules

15+ N27

Thrush et al. (2005) Miljutin et al. (2011)

Abyssal mud Bioturbated and rippled sand Muddy sand Bioturbated and rippled sand Muddy sand and gravel Reef limestone Reef Slope mud, sand and gravel Abyssal mud

0.05 0.5 to 0.7 0.5 to 0.7 2 4 10 N2000 N57 100's to 1000's

Aller (1997) Williams (1988) Hess et al. (2005) Preen et al. (1995) Fillinger et al. (2013) Halford et al. (2004) Druffel et al. (1995) Hughes Clarke et al. (1990) Young et al. (2001)

et al., 1990; Hubbard, 1992; Li et al., 2012) and there have been numerous studies of the effects of storms on shallow coral reefs (Done, 1992; Halford et al., 2004; Wantiez et al., 2006) and other shallow habitats (Van Blaricom, 1982; Dobbs and Vozarik, 1983; Newell et al., 1998; Dernie et al., 2003). Over a 3-yr period, large (storm-related) swell waves are estimated to be competent to mobilize fine sand on over 41.6% of the earth's continental shelves (Harris and Coleman, 1998). A recent modeling study carried out by Harris and Hughes (2012) estimated that about 10% of the Australian continental shelf, influenced by storm waves, tides and ocean currents, could theoretically be classified as a physical disturbance regime (Fig. 4). High-energy, patchclearing (pulse) events were defined as exceeding the Shields (bed shear stress) parameter value of 0.25 (Eq. (1)). Using known rates of ecological succession for different substrate types (gravel, sand and

Table 2 Examples of physical disturbances classified as press or pulse type and characteristic recurrence interval (where known). The fraction of area affected by disturbance (FA) is dependent upon the spatial scale of the physical process and size of the study area. Physical sedimentary process

Press or pulse? FA%

RI Yr

References

Seasonal movement of inner-shelf sand exposes underlying bedrock Seasonal tropical shelf turbidity maximum caused by seasonal wind-waves Seasonal Antarctic shelf turbidity maximum caused by bottom water formation

Pulse Press Press

1 1 1

Western Atlantic, deep sea benthic storms Greenland Sea, deep sea benthic storms Mediterranean Sea, deep sea benthic storms Deep sea slope failures Zone 1 Upper slope submarine canyon heads

? ? ? Pulse

Deep sea slope failures Zone 2 Lower slope Deep sea slope failures Zone 3 Proximal fan Deep sea slope failures Zone 4 Distal fan Changes in abyssal current speed and/or direction

Pulse Pulse Pulse Press

Storlazzi et al. (2013) Saint-Cast (2008) Beaman and Harris (2003), Harris and Beaman (2003) Hollister (1993) Woodgate and Fahrbach (1999) Guidi-Guilvard (2002) Piper and Normark (1983), Mienert (2004), Talling (in press) Piper and Normark (1983) Piper and Normark (1983) Piper and Normark (1983) Shaffer et al. (2004)

33% of study area 50% of Torres Strait shelf 25% of study area

~0.1 0.25 0.25 b0.1–100

20% of Antarctic continental rise

10–1000 100–N1000 N1000 Seasonal and at El Nino frequency

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P.T. Harris / Marine Geology 353 (2014) 169–184

Fig. 3. Conceptual diagrams showing the typical frequency and magnitude of current types at a typical mid-shelf setting in relation to those capable of causing a benthic disturbance regime A) as a pulse-type process where the current intensity exceeding a critical level of shear stress (Cr) (after Harris and Hughes, 2012); and B) as a press-type process where the persistence (duration) of turbidity or sediment burial events exceeds a critical time threshold beyond which plants and animals cannot survive. In order for the process to comprise a disturbance regime, the return interval must fall within the frequency of ecological succession (i.e. approximately 1–10 yr; see Eq. (2) and text for further explanation).

mud; Fig. 2), predictions were made of the spatial distribution of the dimensionless ecological disturbance index (ED in Eq. (2); see Fig. 4). 3.4. Press — Shelf bedform and sand body migration Sedimentary bedform movement on continental shelves represents one category of press-type disturbance processes. Bedform migration leads to burial of the lag deposit (or bedrock surfaces) exposed in bedform troughs, together with any biota that may occur there (Daniell et al., 2008; James et al., 2012). Depending on the period and depth of burial, such bedform movements will be lethal to any immobile biota that is unable to escape from the advancing bedform, whereby a cleared patch of habitat is revealed once the bedform passes and the trough surface is eventually re-exposed. The frequency of bedform migration is

thus equal to the disturbance recurrence interval, given as the ratio of bedform celerity (C) and wavelength (L): RI = C/L, which varies greatly in nature (eg. Ashley et al., 1990; van Dijk and Kleinhans, 2005; Daniell et al., 2008). Biota located in dune troughs are commonly more biodiverse than that inhabiting dune crests and includes both epifauna and infauna communities (Beaman et al., 2012; James et al., 2012; Reynolds et al., 2012; Robinson et al., 2012; Todd and Valentine, 2012; van Dijk et al., 2012; Van Lancker et al., 2012). Other regular movements of shelf sand bodies have been described in the literature in relation to seasonal winter/summer wave patterns. In their recently published study, Storlazzi et al. (2013) monitored the substrate and communities on the California inner continental shelf over an 8-month period comparing locations that experience sand inundation with adjacent areas that do not. In the study area, seasonal movement of sand exposes underlying bedrock and sand buries other rocky areas (e.g. in Eq. (2), RI = 1 yr). The study area is about 70% rocky habitat and 30% sand, with the total area of exhumed and buried seabed equal to about 33% (e.g. FA = 33%). Storlazzi et al. (2013) found that diatom films colonize early and grow quickly and were approximately twice as abundant in dynamic areas as stable areas. Sponges and tubeworms were more abundant in dynamic areas. In contrast, coralline algae, bryozoans, strawberry anemones (Corynactis californica), cup corals, and hydroids were less abundant or did not occur in dynamic areas that underwent burial and/or exhumation (Storlazzi et al., 2013). In this latter area, the rate of ecological succession appears to be much greater than 1 yr (e.g. ES N 1 yr). Therefore, the dimensionless disturbance index ED = FA(ES/RI) = 0.33(N1/1) = N0.33 would meet the criterion for the existence of a disturbance regime, provided the rate of ecological succession does not exceed 3 yr. 3.5. Press — Seasonal, shelf-wide turbidity events

Fig. 4. Dimensionless ecological disturbance index (ED) calculated for the Australian shelf (after Harris and Hughes, 2012). Note FA = 1 was used in the calculation (see Eq. (2)). The index is shown for values up to 10, thus allowing for FA to vary between 0.1 and 1. White areas apply to values of ED greater than 10 and less than 0.2. Example areas are: (a) wavedominated shelf, (b) tide-dominated shelf, and (c) cyclone-influenced shelf.

Shelf-wide turbidity events are normally attributed to storms, during which large swell waves and currents mobilize the seabed sediments. Buoyant, turbid-water river plumes are commonly generated in association with storm events and may also cover extensive areas of the shelf adjacent to the mouths of major rivers (Nittrouer and Wright, 1994; Dagg et al., 2004). A less well known phenomenon is the occurrence of turbidity maxima associated with seasonal changes in wind regime, as occurs in Torres Strait in northern Australia (Table 2). A shelf-wide, turbidity maximum zone was first described in Torres Strait by Harris and Baker (1991). Sediment modeling work published

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by Saint-Cast (2008) found that water turbidity in the Torres Strait is expected to peak at the end of the monsoon season, while it is likely to be at a low at the end of the SE trade wind season (RI = 1 yr). Light levels are of critical importance to seagrass species found in Torres Strait (Campbell et al., 2008) and hence monsoon-related, low-light levels constitutes a severe risk of seagrass dieback. A number of benthic species coexist with seagrasses (Haywood et al., 2008) such that disturbances that effect seagrass abundance will also affect other species. Laboratory experiments have shown that some seagrasses can survive in light intensities below their minimum requirements for periods ranging from a few weeks to several months (Erftemeijer and Lewis, 2006; Fig. 3B). Sublethal and lethal effects of turbidity have been noted for a number of organisms and may cause decreased disease resistance, hatching success, growth and egg development, as well as reduced immune function, physiological condition, and tissue and cellular structure of organisms (Coen, 1995). In the Torres Strait, the effects of the seasonal variation in turbidity and light levels on seagrasses and associated benthos have not been measured. Seagrass meadows in the Torres Strait coexist with mobile, subtidal sand dunes, whereby the seagrass areas are located in troughs between dunes (Daniell et al., 2008). The 4–6 m amplitude subtidal dunes are comprised wholly of carbonate sediments, derived mainly from benthic foraminifera supplemented with various percentages of molluscs, bryozoans and corals (Cole et al., 1995). However, based on repeat measurements of dune migration and seagrass coverage in an area of Torres Strait, Daniell et al. (2008) concluded that dieback of seagrasses is not caused by dune migration. Another example of press-type processes is related to seasonal density currents affecting sediment drift deposits on the Antarctic continental shelf (Table 2). Sediment drifts are known from deep-sea settings (Faugeres et al., 2000), but have only recently been discovered on the Antarctic continental shelf (Harris et al., 1999; Harris and Beaman, 2003; Leventer et al., 2006). Drift sedimentation is distinguished from simple drape or fill styles by its mounded, depositional architecture resulting from sediment transporting bottom currents which are, in turn, associated with elevated bottom water turbidity. On the East Antarctic continental shelf, in the trough incised by the Mertz Glacier during the Pleistocene, Holocene deposits are N6 m thick on the 400 km2 Mertz Drift but are thin or absent in adjacent shallower and steeper sea-floor areas of the wider Mertz Basin. This pattern of sedimentation implies that sediments are winnowed from (or not deposited on) the surrounding continental shelf and deposition is focussed on the drift (Harris and Beaman, 2003). A likely oceanographic mechanism causing the observed sedimentation pattern is related to the seasonal formation of High Salinity Shelf Water (HSSW) within a coastal polynya by brine-rejection during sea ice formation (RI = 1 yr). This water exits the shelf during the winter via the shelf trough to the deep sea where it contributes about 1.5 × 106 m3 s− 1 (1.5 Sverdrups) of Antarctic bottom water (Rintoul, 1998; Williams and Bindoff, 2003). The drift appears to have accumulated at the center of a current gyre, where lower velocities have facilitated the local accumulation of sediments (Harris and Beaman, 2003). Beaman and Harris (2005) described the faunal assemblage characterizing the Mertz Drift as a ‘deposit-feeder basin’ Biotope, comprised of a high proportion of infaunal, deposit-feeding polychaete and nonpolychaete worms; this assemblage is distinct from the surrounding shelf that has a diverse macrofauna with significant epifauna (Beaman and Harris, 2005). Other Mertz Drift macrofauna are sponges, typically as sponge spicule matting, and underwater photos also reveal stalked sponges concentrated on or near ice-rafted-debris (IRD) cobbles, that presumably provide a stable and hard surface to settle and grow upon. Seafloor photographs show the presence of seapens upright in the soft mud (Beaman and Harris, 2005). Photography was negatively affected by high levels of suspended sediments, even though this survey was carried out in late summer when bottom water density currents would be at their seasonally weakest speeds (Brancolini et al., 2000).

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A key point is that the modern deposit-feeder biotope assemblage on the Mertz Drift is associated in sediment cores with a 10–80 cm thick, massively-bedded, bioturbated, sandy unit that overlies a laminated, opal-rich unit, interpreted as representing a transition from the modern, strong bottom current regime to a period of weaker bottom currents in the mid- to late-Holocene (Harris and Beaman, 2003). Laminated sedimentation implies an absence of deposit-feeding bioturbators during that phase of (mid- to late-Holocene) deposition. In February, 2010, a large iceberg collided with the 3000 km2 Mertz Glacier tongue, breaking it off from its point of attachment to the mainland. The Mertz Glacier tongue formed a persistent polynya on its western, down-drift side, the site of HSSW production described above, which was reduced by an estimated 23% following the breakage event (Kusahara et al., 2011). If the reduced formation of HSSW heralds a return to the deposition of laminated, opal-rich sediments (as in the mid- to late-Holocene), we might also expect a faunal succession to occur as the habitat becomes unsuited to the present, deposit-feederdominated, assemblage. 4. Deep-sea sedimentary environments — Disturbance and ecological succession Human perceptions of the deep ocean environment have changed dramatically in recent decades. As aptly summarized by Levin et al. (2001) “once considered to be constant, spatially uniform, and isolated, deep-sea sediments are now recognized as a dynamic, richly textured environment that is inextricably linked to the global biosphere”. Snelgrove and Smith (2002) conclude that “small-scale habitat variability and patchy disturbance, as well as global and regional variability, may play roles in maintaining deep-sea diversity”. Of particular relevance to the present discussion is the recognition of the episodic disturbance of the benthos by bottom currents and slope-sourced turbidites. The effects of such disturbances range from “pulse” intensified flows capable of mobilizing and transporting sediment, causing turbidity events and dislodging benthic organisms, to “press” subtle variations in current strength and attendant variation in sediment (and food) supply. 4.1. Benthic storms — Press, pulse or both? Current meters and other instruments, deployed beneath large eddies shed by the Gulf Stream Current in the North Atlantic Ocean as part of the High Energy Benthic Boundary Layer Experiment (HEBBLE), showed that, in certain areas, seabed sediments are mobilized during “benthic storm” events (Hollister and McCave, 1984; Gross et al., 1988; Gross and Williams, 1991). Such storms last from 2 to 22 days (mostly from 3 to 5 days) and have a return frequency of 8–10 storms per year (Hollister, 1993; i.e. RI = 0.1 to 0.13 yr). During benthic storms, near-bed currents attain speeds of up to 0.73 m s−1 and suspended sediment concentrations may be as much as 12,000 μg/l. Benthic storms attaining near-bed speeds of 0.2 m s− 1 are comparable to a 9 m s− 1 (Beaufort 5) windstorm (Cronin et al., 2013). During benthic storms, surficial organic matter, micro-organisms, larvae and juveniles are transported out of the area of erosion (Aller, 1989). Benthic storms typically occur where the kinetic energy of ocean surface currents is large, in particular, beneath eddies shed by major western boundary currents like the Gulf Stream (where bottom currents reach more than 0.4 m s−1; Savidge and Bane, 1999). At abyssal depths beneath the Circumpolar Current in Drake Passage, bottom currents of more than 0.7 m s−1 were sustained for up to 70 days (Chereskin et al., 2009). Near-bed turbidity is greater beneath the Circumpolar Current than in surrounding areas, attributed to resuspension of bottom sediments (Kolla et al., 1976; McCave, 1986). Bottom currents exceed 0.2 m s−1 more than 50% of the time in narrow regions beneath the Agulhas Current (Cronin et al., 2013) and in the central Greenland Sea (3340 m water depth) current meters placed ~50 m above the sea floor recorded currents of up to 0.43 m s−1, occurring about

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4 times a year and lasting about a week (Woodgate and Fahrbach, 1999). At the DYFAMED site in the Mediterranean Sea, four benthic storms with peak velocities between 0.13 and 0.21 m s−1 were identified over a 28-month period between 1995 and 1997 (Guidi-Guilvard, 2002). These results (Table 2) confirm that benthic storms occur in all oceans, but also raise the question as to whether benthic storms should be classed as press, pulse or both? A key point is that bedforms observed at abyssal depths (a proxy for benthic storms) correlate with sea surface elevation derived from satellite altimetry data (Hollister, 1993). It is now possible to model bottom currents globally at a resolution of 1/12th of a degree using the ORCA12 global model configuration developed by the DRAKKAR consortium (Barnier et al., 2011; Deshayes et al., 2013; Fig. 6). From this model we can infer that there is an intensification of benthic storm occurrence beneath the Circumpolar Current and associated with western boundary currents (Fig. 6). In a transect normal to the margin, bottom current speeds under western boundary currents reach a maximum speed before decreasing away from the margins towards the mid-ocean (Figs. 6 and 7). The region having the greatest areal extent of maximum bottom currents is predicted to occur in the mid-Southern Ocean, encircling the Antarctic continent (Fig. 6). In this region, benthic storms occur towards the center of the ocean basin as well as adjacent to continental margins, in contrast with western boundary currents where storms occur mainly adjacent to continental margins (Figs. 6 ad 7). Based on this map (Fig. 6) the area of the global ocean affected by benthic storms (i.e. abyssal areas where near-bottom current speeds exceeded 0.2 m s−1 at some time over a 2-yr period) is estimated to be approximately 26.9 million km2 (equal to about 8% of the area of the world ocean). We may here define this broad area as a zone of potential benthic storm disturbance regime, which will vary spatially (stochastically) as a function of storm intensity, duration and recurrence interval (RI) and that will contain different communities inhabiting different substrate types and potentially having different rates of ecological succession. Seabed photographs taken at the HEBBLE site showed the sediment surface to be tracked and worked by benthic biota, with mounds and burrows clearly visible (Gross et al., 1988). Benthic storms caused smoothing of the seabed, with some tracks and burrows being obliterated. However, 3 weeks later, after a “normal” quiet period when nearbed currents were less than 0.1 m s−1 and suspended sediment concentrations were typically b500 μg/l, photographs showed the tracks and burrows had returned to their pre-storm state (ES = 3 weeks = 0.058 yr). Aller (1997) reported that recovery time to disturbance events is relatively short for meio- and macrofaunal abundances at the HEBBLE sites (ES = days to weeks = 0.005 to 0.05 yr). These results suggest that disturbances at the HEBBLE site occur at a frequency that is comparable to the ecological succession rate: from Eq. (2), ED = FA (ES/RI) = FA (0.05 to 0.005/0.1 to 0.125) = FA (0.5 to 0.05). Although the fraction of area (FA) disturbed during a benthic storm is unknown, the calculated values of ED suggest the occurrence of a disturbance regime. However, it must also be asked what intensity (and/or duration) must be attained by a benthic storm before it causes a patch-clearing disturbance? Those rapid recovery times for meio- and macrofaunal abundances at the HEBBLE sites reported by Aller (1997) could be interpreted as indicating that the habitat was not actually “disturbed” in the sense of patch-clearing processes, thus explaining the rapid rate of “recovery”. From the perspective of IDH, the available data suggest that the HEBBLE site is not within a benthic disturbance regime. Levin et al. (2001) reported that a range of macrofaunal species exhibited lower diversity at the stronger current sites (including the HEBBLE site) than at lower energy sites. Bivalves, foraminifera and ploychaetes were all affected in this way; however, in the case of meiofaunal taxa, Levin et al. (2001) found that diversity was not significantly different between high-energy and low-energy sites. Lambshead et al. (2001) reported that nematode diversity at the HEBBLE site was statistically, and significantly, lower than at reference sites. This observation is consistent with

Leduc and Pilditch (2013), who found that nematode communities respond in different ways to sediment disturbance, with some species avoiding impacts by burrowing into the sediment, while others are less tolerant and may perish. A lower species richness at the HEBBLE sites is not what would be predicted by the IDH if the sites were within a disturbance regime. Taken together, these results suggest that benthic storms occur at too high a frequency for them to be a disturbance (ED ≪ 0.2). Since benthic storms are stochastic in nature, the possibility exists that disturbance regimes may exist along the periphery of the zone of frequent benthic storms (i.e. the areas bordering hot spots shown in Fig. 6). Finding such areas subject to infrequent (decadal or longer?) benthic storms could be accomplished by using a long-term (century?) run of a hydrodynamic model like ORCA12. In general terms, there is very little information available on the rates of ecological succession for abyssal sediment communities (Table 1). In their review of the potential environmental effects of manganese nodule mining, Morgan et al. (1999) found that none of the studies completed up to that time had been able to establish quantitative relationships between burial depth and faunal succession; a more recent study by Miljutin et al. (2011) reported that an abyssal nematode assemblage had not returned to its initial state 26 yr after experimental dredging carried out in one Clarion-Clipperton manganese nodule mining lease area. In a study of an artificially disturbed site in the 4160 m deep Peru Basin, Bluhm (2001) found that the repopulation of the disturbed areas by highly motile and scavenging animals started shortly after the area was plowed; 7 yr later hemisessile animals had returned to the disturbed areas, but the total abundance of soft-bottom taxa was still low compared to control sites. Young et al. (2001) postulate that the recovery of sites where turbidites have occurred may take hundreds to thousands of years (see below). Thus, whereas the rates of ecological succession of meiofauna may be annual to sub-annual, the rates of ecological succession for deep-sea macrofauna are measured in decades if not centuries or longer. Thus, while benthic storms are potential agents for meiofauna disturbance regimes, unless we can identify areas where their return frequency is measured in years or decades, they are not likely to be agents for macrofauna disturbance regimes (Fig. 7). 4.2. Pulse — Slope failures, slumps and turbidity currents Perhaps one of the most spectacular, albeit destructive, processes occurring in the deep sea is catastrophic slope failure that causes largevolume submarine slides, massive sediment slumps, debris flows and turbidity flows (Piper and Normark, 2009; Covault, 2011). Slope failures are commonly ascribed to continental slopes even at gradients N 0.5°, but they occur also on the steep (5 to 10°) volcanic flanks of seamounts, ocean trench walls, ocean ridges and on other steep-sided geomorphic features of the ocean floor (Hughes Clarke et al., 1990; McAdoo et al., 2000; Skene and Piper, 2006). The scale of the largest submarine slides and slumps can attain gigantic proportions: an individual slide off Hawaii may have exceeded 5000 km3 in volume of volcanic rocks and sediment, and cumulatively slides, slumps and debris flows cover more than 5 times the surface area of the islands themselves (Moore et al., 1989). Blocks of basalt 1.2 km across and 200 m high were imaged in 4000 m water depth using TOBI sidescan sonar in a debris flow generated by the collapse of a submerged flank of Hierro Island in the Canaries (Masson, 1996). Globally, the area of seafloor characterized by submarine fans is estimated at 8.3 million km2, or 2.3% of the ocean floor (Harris et al., in press). The slump that flowed onto the Venezuelan Abyssal Plain some 2000 yr ago, smothered the fauna beneath a N14 cm thick layer and the recolonization of the sedimentary surface is yet to attain the climax community (Young and Richardson, 1998; Young et al., 2001). In that area, the turbidite province exhibits lower species diversity, dominated by sponges and holothurians, compared with mollusks, decapods and fishes found to dominate in adjacent pelagic and hemipelagic provinces

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(Young et al., 2001). Similarly, 57 yr after the widespread 1929 Grand Banks turbidity current at 4000 m depth, there was essentially no recolonization by visible (hemisessile) benthic organisms (Hughes Clarke et al., 1990). The inability of the original fauna to become reestablished may be explained in part because the properties (grain size, organic content, etc.) of the sediment deposited by the slump differs from that which was originally present. Fauna are often particularly suited to specific sediment properties (Snelgrove and Butman, 1994). In general terms, Young et al. (2001) conclude that the time needed for the recovery of benthic fauna from slumps and turbidites (ES) will vary according to the characteristics of the slumped material, the thickness and spatial extent, the composition of the original benthic community and the frequency of events (RI), but that complete ecological succession rates are measured in 100's to 1000's of years. The immediate effect of a slope failure on the abyssal benthos is of course death by dislodgement and burial. The kill zone may extend beyond the immediate path of the moving sediments because of the increased levels of turbidity carried down-slope by bottom turbidity currents. Animals that have evolved to filter minute quantities of detritus from very clear ocean water would be overwhelmed by a sudden influx of highly turbid water and be unable to withstand the impact (e.g. Lambshead et al., 2001). Turbidity levels would probably affect benthic life over a wide area for some time period (days to weeks?) following a large-scale, submarine slope failure. Depending on the characteristics of the surfaces involved, the effects of burial are suggested by some workers to be more important than erosion processes (Miller et al., 2002). Burial of a rocky substrate would mean a transformation from rocky to sediment-covered habitat that would likely be catastrophic for the original community (e.g. deep sea corals); burial of soft-sediment habitat would only be a disturbance if the burial rate and thickness of the deposit significantly exceeds background sedimentation rates. Defining appropriate spatial scales (FA) is of critical importance to understand turbidite-related disturbances. For example, Kukert and Smith (1992) built 10 cm high by 35 cm wide artificial mounds of essentially macrofauna-free sediment on the Santa Catalina Basin seafloor (1240 m depth) and found that macrofauna reached background levels of abundance after 11 months although community succession proceeded for at least 23 months (ES = 2 yr) when maximum biodiversity was achieved (Kukert and Smith, 1992). These results may be contrasted with natural turbidite events, described above, that affect 100's of km2 and where rates of community succession are measured in 100's to 1000's of years (Young et al., 2001). Conceptually, slope failure disturbance regimes may be divided into the following depth zones, in a transect from the shelf break to abyssal plain (Table 2; Fig. 7): Zone 1) regimes affected by frequent but localized slope failures, found mainly on upper to mid-slope, areas characterized by submarine canyons; Zone 2) regimes affected by occasional large failures and turbidity flows, scaled to the length of submarine canyons and submarine fan complexes and found mainly in mid- to lower-slope areas; Zone 3) regimes affected by rare but catastrophic slope failures that might extend across the slope and onto the continental rise, culminating in lower slope to basin-wide turbidity flows; and Zone 4) distal continental rise to abyssal regimes rarely affected by any slope failures or turbidity currents. 4.2.1. Zone 1 — Upper to mid-slope, areas characterized by submarine canyons In this zone, frequent but localized slope failures occur where a significant sediment supply to the upper slope is occurring at the present time. The zone is characterized by the upper part of submarine canyons that have heads that extend onto the continental shelf. Because turbidity flows may occur once or more every year within such zones, and may be semi-continuous in some locations, they are among the best-studied slope sediment transport systems (e.g. the European COSTA project; Mienert, 2004). Examples of canyons that experience intra-annual and/or seasonal turbidity current events include the Monterey Canyon

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in California (Shepard, 1963; Okey, 1997), the Sepic River in Papua New Guinea (Walsh and Nittrouer, 2003), the canyons in the Gulf of Lyons (Canals et al., 2006) and the Fraser Island slope off eastern Australia (Boyd et al., 2008). This zone may be highly energetic, being influenced by tides and internal waves, seasonal density cascades (Ivanov et al., 2004; Canals et al., 2006;) and less frequent turbidity flows, slumps and very infrequent tsunami or debris-flow events. In such areas, turbidity flows cause frequent disturbances to benthic communities and examples of communities may be found at different stages of recolonization and recovery. For example, Hess et al. (2005) studied benthic foraminifers in a submarine canyon in the Bay of Biscay, sampled at different times after a down-slope turbidity flow event. These authors found that the recovery of foraminiferal faunas was achieved in about 6–9 months. Samples taken down-core in successive turbidite sequences contained nearly the same faunal elements as the surface assemblages, suggesting that the community structure is confined to an early stage of ecosystem recolonization, attesting to the relatively high frequency (sub-annual?) of turbidity currents (ED ≪ 0.2). In the Nazare ́ Canyon, Spain, Paterson et al. (2011) found that frequent physical disturbance in the middle and upper sections of the canyon axis had a dramatic impact on Foraminifera with only certain species able to colonize and survive in these habitats (i.e. ED b 0.2). 4.2.2. Zone 2 — Mid- to lower-slope canyon and submarine fan complexes This zone is characterized by occasional slope failures and turbidity flows, extending along the length of submarine canyons and from the canyon mouth to the upper portions of submarine fan complexes. This zone experiences debris flows and/or turbidity flows typically on decadal to century timescales and is found mainly in mid- to lowerslope areas, but may include headless canyons and other non-canyon slopes, seamount flanks and other steep slopes. For example, in the Cascadia Subduction Zone off the western coast of the United States, Guitierrez-Pastor et al. (2009) measured turbidite frequencies from 12 piston cores located at different points along the margin. Average turbidite frequencies of 200 to 550 yr, and maximum frequencies of around 1200 yr were reported. Further north, on the glaciated margin of British Columbia, Canada, Knudson and Hendy (2009) measured turbidite frequencies of 75 to 130 yr on the Nitinat Fan at Ocean Drilling Program Hole 888B in 2000 m water depth. Disturbances to benthic communities are infrequent and few examples of communities can be found at the earliest stages of recolonization and recovery. However for some long-lived species and slowto-recover communities (ES equal to decades or longer; see Glover et al., 2010, for example), the occurrence of disturbance regimes is possible (i.e. 0.2 b ED b 1.0). It is important to recognize that submarine canyon fauna occupy different depth-related biomes (e.g. Last et al., 2010); for example, some species of cold-water corals that occur within the shelf-incising heads of canyons off Newfoundland are absent at greater depths (Baker et al., 2012), even though corals were found at all depths surveyed between 350 and 2245 m. 4.2.3. Zone 3 — Lower slope and continental rise, submarine fan complexes In this zone, sediment input is related to rare but catastrophic slope failures that might extend across the slope and beyond, culminating in lower slope turbidity flows that extend to the distal limits of submarine fan deposition. In their review of 68 slope failures exceeding 1 km2 in volume located mainly in the North Atlantic Ocean and b 30 kyr in age, Urlaub et al. (2013) found that the frequency of submarine landslides during the last glacial cycle was 0.4 to 2 failures per thousand years (Table 1). These events may therefore occur at century to millennial intervals, and although disturbances to benthic communities are rare, their impact is widespread and catastrophic when they do occur. Indirect effects of turbidites are related to the higher TOC content carried by the turbidite as compared with the pelagic sediments. Turbidites, therefore, can be a comparatively rich food source for abyssal benthic communities. Levin et al. (2001) cite an example from the

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Madeira Abyssal Plain, in which turbidite associated fauna are characterized by a lower species richness but greater abundance of polychaetes and Nematodes than found on non-turbidite sites. Benthic storms and contour currents may result in concomitant disturbance regimes in this zone (Fig. 7). The frequency of turbidite deposition varies, from annual to decadal frequency at proximal (upper slope) locations to millennial frequency at distal (abyssal depth) locations (Piper and Normark, 1983, their Fig. 9), although switching of depocenters across the fan complex may cause sediment sources to switch on and off over millennial timescales (Covault et al., 2007). 4.2.4. Zone 4 — Distal continental rise to abyssal plain This zone is rarely affected by slope failures and includes the distal portions of continental rise that are at the limits of influence of even the largest of turbidites and debris flows. Gentle continental slopes, plateaus and terraces draped with thick layers of hemipelgic sediments are included in this zone. Benthic storms and contour currents may result in concomitant disturbance regimes in this zone, but slope-failure and turbidite related processes are extremely rare. The summary of information shown in Fig. 7 illustrates how different groups of organisms (e.g. cold water corals, marofauna and meiofauna) have different post-disturbance recovery rates. This means that different disturbance processes (benthic storms, turbidity currents, slumps, etc.) may result in a disturbance regime for one community of organisms, but not for others. Thus there are multiple, contemporaneous, overlapping disturbance regimes defined on the bases of the physical disturbance process and the effected benthic communities (Fig. 7). From the above analysis, the available information suggests that the low-frequency end of turbidite disturbance (RI of 1000's of years) may equal rates of macrofanua ecological succession (ES also 1000's of years), which implies the possibility of disturbance regimes (0.2 N ED N 1). For example, the area of continental rise surrounding Antarctica is estimated to be 6.7 million km2, of which about 1.16 million km2 is submarine fan (Harris et al., in press), thus FA = 1.2/6.7 = 0.2 and by Eq. (2), ED = 0.2(1 kyr/1 kyr) = 0.2. Thus taken as an entity, the Antarctic continental rise may be classified as a turbidite disturbance regime for macrofauna (Fig. 7). 4.3. Press — Inter-annual changes in abyssal bottom currents In abyssal environments subject to regular benthic storm events, animals exploit the pulses of allochthonous sediment input as events when fresh food is transported into their habitat. Based on observations of deposit feeders at the HEBBLE site, Thistle et al. (1991) noted that “abundances of polychaetes, bivalves, tanaids, and nematodes were consistent over time and appeared to be unaffected by the periods of strong near-bottom flow that characterized the site”. Thus it is intriguing to speculate that it may be the absence of storms (prolonged periods without storms), causing starvation that is in fact the disturbance for some abyssal communities. This idea leads to the more general questions: What effects do long-term (scaled to the life histories of benthic fauna) changes in abyssal bottom currents have on benthos? What evidence exists as to the spatial–temporal stability (or instability) of sediment-transporting abyssal bottom currents? Taking the last question first, direct observations from moored current meters or deep-drifting floats are difficult to make at abyssal depths and there are consequently few, long-term (e.g. 1 yr or longer), direct measurements of near-bed, deep ocean currents. In general, mean current speeds of around 0.02 m s−1 are typical and maximum currents flowing near the abyssal seabed rarely exceed 0.1 m s− 1 (Tyler, 1995). Deep ocean currents do, however, exhibit significant spatial variability (Fig. 6) and temporal variations are known to occur over seasonal and intra-annual time scales as described from the above discussion on benthic storms (see also Bonnin et al., 2006). However, a very few studies have also presented records of inter-annual changes in abyssal currents.

For example, Shaffer et al. (2004) reported the results of current meter deployments at 3750 m depth in the Chile Basin (Southeastern Pacific Ocean) over a 7-yr observation period. The current meters were moored close to the continental margin (150 km off the coast of Chile) and recorded hourly measurements. Mean speeds were only 0.003 ± 0.001 m s− 1 but peak current speeds of up to 0.078 m s−1 were recorded and there were seasonal reversals in current direction, modulated by El Nino events. Thus, inter-annual variations in abyssal flow regime do occur, but what ecological impact would they be expected to have? Filterfeeding organisms rely on currents to carry food (phytodetritus) to them, so a 50% increase or decrease in current speed implies a proportionate increase or decrease in food supply (Nowell et al., 1984). Epibenthic, sessile and mobile macrofauna seek out elevated habitat to access stronger currents and induce localized flow effects by their height and shape to optimize their food intake (Jumars and Nowell, 1984; Muschenheim, 1987; Thistle, 2003). At a fixed reference point, any spatial heterogeneity in the near-bottom concentration of suspended sediments (including organic matter) translates into temporal fluctuations in food supply under a steady, unidirectional current. Hollister and McCave (1984) consider that much of the sediment passing through the HEBBLE region originated from the Laurentian Fan on the upper Nova Scotia Rise. Changes in current direction could, therefore, also result in an organism receiving suspended matter from different source areas, containing food in greater or lesser quantities. It follows that abyssal benthic filter feeders must be able to withstand variability in food supply, with individuals located at the margins of suitable habitat most vulnerable to even small changes in bottom currents. That there are seasons in the deep sea is now an established fact. Detrital-feeding fauna and suspension feeding organisms have evolved to exploit the seasonal, vertical flux of surface matter sinking to the seabed. Seasons are recorded by moored sediment traps (e.g. Juniper et al., 2013) and in thick versus thin growth rings in the shells of small abyssal molluscs, (Gage and Tyler, 1991). In addition to seasonal changes, there is now biological evidence that there are other (longer) frequencies of variability in abyssal food supply. Monitoring of megafaunal community structure in both the North Atlantic and North Pacific over 10–15 yr demonstrates that abrupt shifts occur in the species composition of deposit-feeding echinoderms, with time lags as short as 6–23 months, that appear to be related to changes in the quantity and quality of POC flux to the abyssal seafloor (Smith et al., 2008). This time scale (6–23 months) provides a guide to the critical length of time (persistence in change to sediment transport patterns) required to cause a disturbance (Fig. 5). The food available to suspended-detritus-feeding abyssal fauna is thus a function of the seasonal vertical flux of organic matter modulated by horizontal transport by bottom currents. The available evidence indicates that even small changes in ocean circulation could potentially have a significant ecological impact on abyssal fauna (e.g. Thistle, 2003; Ramirez-Llodra et al., 2011). It is possible that changes in near-bottom ocean currents could lead to widespread starvation and leave devastated patches of cleared habitat available for colonization by other species. For these reasons, inter-annual changes in the speed and/or direction of bottom currents are included here as a potential cause of disturbance regimes. 5. Disturbance regimes and predictive habitat mapping Spatial information on the distribution of the benthos is needed to support government spatial marine planning, management, and decision-making. However, the collection of data on benthic ecosystems by directly observing and mapping flora and fauna is expensive, timeconsuming and impractical in most shelf and deep-sea situations. A solution that has gained broad acceptance around the world is to apply benthic habitat mapping techniques that are based on exploiting the relationships that exist between the occurrence of particular benthic

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Benthic Disturbance Regimes - Slope and Abyssal HIGH

Tidal Currents Internal Waves

Bottom shear stress

Turbidity Currents: SeasonalEpisodic

Tsunami, Slumps and Debris Flows

Benthic Storms

Cr

LOW 0.01

0.1

1

10

100

1000 years

Disturbance frequency Fig. 5. Conceptual diagram showing the characteristic frequency and magnitude of current types at a typical abyssal setting in relation to those capable of causing a physical benthic disturbance regime as a pulse-type process that exceeds a critical level of bed shear stress (Cr). In order for the process to comprise a disturbance regime, the return interval must fall within the frequency of ecological succession (i.e. approximately 1–100 yr; see Eq. (2) and text for further explanation). Benthic storms, turbidity currents and slumps and debris flows occur at frequencies that potentially coincide with rates of ecological succession for some faunal groups.

species and communities with the biophysical (including marine geological) aspects of the seafloor (Roff and Taylor, 2000; Harris and Baker, 2012). Biophysical aspects of the environment are generally faster and less expensive to map than the occurrence of biota mapped by direct observations, and lend themselves to an approach known as predictive habitat modeling (PHM; also habitat suitability modeling). Niche theory implies that by measuring the environmental parameters coinciding with the occurrence of a species and the relative strengths of the different relationships, one should be able to predict the species' fundamental niche. This is the principle behind PHM (Kostylev, 2012). Optimizing the use of existing data, many studies use biophysical parameters such as bathymetry, seafloor sediment properties, oceanographic data, satellite remotely-sensed variables (primary production, coastal habitats, etc.) and particularly multibeam sonar data (depth and acoustic backscatter) to produce benthic habitat maps. The theory and limitations of PHM are well summarized by Brown et al. (2011; Fig. 8). In its simplest form PHM is applied to predict the fundamental niche of a single species. The known distribution of the species is correlated with existing spatial data using a range of empirical statistical methods (supervised or unsupervised multivariate techniques) to find the most informative predictors (Huang et al., 2011). Different species generally have different sets of most informative predictors (Fig. 8) so there is no single, most-useful, biophysical variable (McArthur et al., 2010). Brown et al. (2011) note that the single species mapping approach “works well for sessile species such as corals, attached epifaunal organisms, or slow moving infaunal or epifaunal species, where there is likely a close correlation between substratum characteristics and the geographical distribution of the organisms.” The occurrence of particular benthic communities (biomes) may be predicted by combining the fundamental niches of a number of its component species and selecting the area of overlap, or alternatively the known distribution of the community may be correlated with existing spatial data. The PHM approach has the inherent flaw that it only predicts the fundamental niches of species; other biological processes like competition, recruitment, diseases and predation will reduce the usable habitat for a species to its realized niche (Fig. 8). Firm boundaries are exceptions

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rather than the rule in ecosystems, and most environmental changes occur over temporally-varying spatial gradients that are not easily represented in a map (Lucieer and Lucieer, 2009). The PHM approach is challenged by mobile species that interact with the seafloor for one or more different life history activities (e.g. feeding, refuge, reproduction); different aspects of the seabed environment are exploited at different life stages, confounding species-niche relationships. Another flaw is that the starting set of possible biophysical correlates (e.g. depth, temperature, bottom current speed, sediment grain size; Fig. 8) are often selected based on what is readily available, rather than what is most relevant to defining the fundamental niche for a particular species. This approach potentially renders derived habitat maps useless for predicting species distributions (Kostylev, 2012). An often missing, first-step in such studies is to first acquire an in-depth understanding of the life habits of the focal species before selecting niche characteristics to then produce a potential habitat map. The net result is that predictive habitat maps are generally not applicable beyond the immediate area for which they were developed (Pitcher et al., 2012). There is no question that disturbance has a major influence on the occurrence of many benthic species (e.g. Sousa, 2001; Guisan and Thuiller, 2005; Kostylev and Hannah, 2007). However, to date most PHMs do not include seafloor dynamic aspects or disturbances in their models (Harris and Baker, 2012). This is probably because of the large cost associated with collecting data over the range of spatial and temporal scales needed to quantify the rates of ecological succession of species and biotopes, and which is impossible in deep-sea environments having millennial-scale rates of ecological succession. Nevertheless, simply recognizing that an area of seafloor may be influenced by turbidites (for example) while an adjacent area is not, could help to explain differences in the composition of assemblages characterizing them. The assessment of deep sea benthic disturbance regimes presented above points to the need to consider both disturbance processes and ecological responses over near-geologic time scales. Disturbance regimes governed by turbidites, where rates of ecological succession range from centuries to millennia, will require the inclusion of sedimentological indicators of turbidite frequency and spatial extent, for successful PHM. Recognition that different communities have different rates of succession that may respond to different disturbance processes (Fig. 7) is also needed. Researchers applying the PHM approach have contributed to a better understanding of benthic ecosystems and the differences between biophysical variables that define the fundamental niches of marine species. The inclusion of disturbance concepts is necessary to make progress in applying PHM theory for many benthic species. 6. Conclusions: The significance of benthic disturbance regimes This review has focused on physical sedimentological processes that occur in shelf and abyssal environments that also act as patch-clearing disturbances to benthic ecosystems and which, under certain circumstances, give rise to disturbance regimes. Physical sedimentological processes can cause both press and pulse types of ecological disturbance. On the continental shelf, pulse-type disturbances are due to temperate and tropical storm events, and press-type of disturbances identified here are sediment body migration and sustained periods of elevated turbidity caused by seasonally reversing wind patterns and by seasonal Antarctic bottom water production. On the slope and at abyssal depths, pulse-type disturbances are due to slumps and turbidity currents; benthic storms, that attain N0.70 ms−1 sustained for periods of over 70 days under parts of the Circumpolar Current (Chereskin et al., 2009), may be either press or pulse and it is unclear at present which type is most responsible for causing disturbances. Another possible press-type of disturbance identified here is inter-annual changes in abyssal bottom current speed and/or direction. Disturbance regimes are important ecologically because they may harbor the most biodiverse benthic environments in the oceans,

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Fig. 6. Maximum bottom current speed for the 2 yr period 2008–2009 from the ORCA12 model (Barnier et al., 2011), a 1/12° eddy resolving model (resolution is 9 km at the equator and 4 km in the Arctic and around Antarctic). The model has 46 to 75 vertical levels and the level nearest to the seabed is shown here. Bottom velocities are extracted from a 30-yr ORCA12 model simulation, stored as 5-day averages (i.e. maximum speeds are 5-day averages). Map provided courtesy of Dr. B. Barnier, Grenoble University, France. The area of abyssal ocean where near-bottom current speeds are predicted to exceed 0.2 m s−1 over the 2-yr period (excluding the continental shelf) is estimated to be about 26.9 million km2.

according to the intermediate disturbance hypothesis. They are significant at the very least since they are likely to characterize a significant area of the ocean floor. Around 10% of the Australian continental shelf

is predicted to be characterized by disturbance regimes caused by storms and currents (Fig. 4). Variability in the production of bottom water, with associated shelf-basin turbidity events, may cause disturbances to

Frequency (years) (RI) Shelf Break

Increasing Water Depth

1000 idi

b

ur

dt

DR

tes

Cold Water Corals

100

n sa

p

um Sl

Macrofauna 10

? ur Conto Internal Waves

WBC benthic storms

? CC benthic storms

nts

Curre

1

DR

Conti

l Rise

Tidal currents

Zone 1 Zone 2 (Upper Canyon) (L ower Slope)

Meiofauna

0.1

nenta

0.01 Zone 3 (Lower Fan)

Distance

Zone 4 (Abyss)

Characteristic Rates of Abyssal Ecological Succession (ES)

Fig. 7. Idealized profile normal to the continental margin, illustrating the spatial variation in characteristic return-frequencies of slumps, turbidites, contour currents, benthic storms, tidal currents and internal waves (Zones 1–4 are described in the text). The return frequencies for slumps and turbidites increase in a seaward direction (Piper and Normark, 1983). Eddies that induce benthic storms form annually to semi-annually, most commonly proximal to the base of slope under western boundary currents (WBC) and are less common in the centre of ocean basin; in contrast benthic storms appear to be more common beneath the mid-ocean, Circumpolar Current (CC), decreasing towards the continents (Fig. 6). The return frequency of benthic storms measured by 1–2 yr moorings is typically 1–3 months (Table 2) although it is postulated here that longer (decadal?) return frequencies may occur locally (illustrated by dashed lines for benthic storm occurrence fields). Contour currents are most common adjacent to the continental margin of the western North and South Atlantic (Hollister, 1993) and could possibly cause disturbance regimes (DR) for meiofauna. Tidal currents and internal waves occur at a high-frequency, the latter having their greatest impact on the upper slope. Also shown are characteristic succession rates for three benthic groups: cold water corals, soft-sediment macrofauna and meiofauna (see Table 1 and text for references). The dashed green lines indicate areas where the return frequency of the disturbance corresponds with the approximate rate of ecological succession for different communities, conditions necessary to produce a disturbance regime. Thus slumps and turbidites may produce disturbance regimes (DR) for macofaunal communities and cold-water coral communities whereas only benthic storms occur at a high enough return frequency to cause a disturbance regime for meiofauna.

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benthic fauna on the Antarctic shelf. Benthic storms occur over ~8% of the abyssal ocean (Fig. 6) and may give rise to disturbance regimes for meiofaua; they may also act as an agent for macrofauna disturbance regimes (Fig. 7) which could be elucidated by long-term (century-scale) computer model runs of bottom currents. The Antarctic continental rise could meet the criteria for a turbidite-dominated disturbance regime for macrofauna, operating over geologic time scales (Fig. 7). Combining the areas of seafloor characterized by one or more physical sedimentary disturbance processes is likely to yield a figure approaching 10% globally for the oceans. Based on this review, three general conclusions may be drawn:

2. Disturbance regimes cannot be studied or understood by conventional marine survey techniques that take a single “snap-shot” of the benthos and associated environmental parameters. Instead, multidisciplinary research programs that integrate oceanography, sedimentology and benthic ecology to collect time series observational data sets are needed. 3. Predictive habitat mapping has made rapid advances in recent years through new technologies and analytical techniques. Inclusion of disturbance regime concepts with other biophysical variables that define the fundamental niches of marine species is needed for predictive habitat modeling to advance.

1. Natural physical sediment disturbances are an important ecological process for benthic ecosystems and may be a key factor controlling the spatial distribution of many species in the marine environment. The available evidence indicates that a significant portion of ocean area is characterized by physical sedimentary disturbance regimes.

Acknowledgments This work was produced with the support of funding from the Australian Government's National Environmental Research Program (NERP) and is a contribution of the NERP Marine Biodiversity Hub.

Fig. 8. Diagram illustrating the predictive habitat mapping concept (after Brown et al., 2011). Species evolve to fit a certain ecological niche as defined by specific abiotic gradients. The geographical distributions for each species in the community represent the realized niche of each type of organism, taking account of biotic interactions (Guisan and Thuiller, 2005). Offshore, ecosystems are mostly characterized by gradational changes in environmental characteristics, making community patterns difficult to predict.

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