A Review of Sublittoral Monitoring Methods in Temperate Waters: a Focus on Scale

doi:10.3723/ut.28.099 International Journal of the Society for Underwater Technology, Vol 28, No 3, pp 99–113, 2009

A review of sublittoral monitoring methods in temperate waters: a focus on scale

HB Van Rein, CJ Brown and R Quinn Technical Paper Centre for Coastal and Marine Research, School of Environmental Science, University of Ulster, Coleraine, Northern Ireland J Breen Northern Ireland Environment Agency, Belfast, Northern Ireland

Abstract the extent of compliance with a predetermined A plethora of methods to monitor shallow sublittoral standard or the degree of deviation from an benthic habitats and communities are available to expected norm’. Monitoring has also been defined the marine researcher today. The most widely used as: ‘sampling in time with adequate replication to methods are reviewed and evaluated, with reference detect variation over a temporal range from short to the spatial scale at which they operate. For ease and long time periods, done at more than one loca- of comparison, methods are categorised as operating tion’, (Kingsford and Battershill, 1998). Ecological over broad (>1km), meso (10m–1km) and fine scales monitoring programmes are specifically designed (<10m). A measure of efficiency and data resolution are to detect trends or changes from normal conditions provided by exploring the range of sampling techniques or a predetermined standard over time. Equally, and strategies at each of these spatial scales. they may monitor the progress of ecological change Recommendations are made regarding which methods and provide evidence of the efficacy of legislative are most effective at each scale: light detection and directives (Goldsmith, 1991). ranging (LIDAR) and multibeam sonar over broad Predetermined targets are, therefore, necessary scales; sidescan sonar, drop-down cameras, towed for the basis of a monitoring programme and will cameras and remotely operated vehicles (ROVs) over drive what needs to be monitored, where the mon- meso scales; and grab samplers, sediment corers for itoring will take place, when and in what manner soft, unconsolidated sediments and photoquadrats, the monitoring is to be conducted, and at what and video transects for hard, consolidated sediments frequency will samples be collected. The practical at fine scales. Emphasis is placed on the development issues related to what sampling equipment is best of standardised methodologies for sampling each scale suited to survey different sublittoral environments within a nested design, for the monitoring programmes and community assemblages, as well as at what of the future. sampling scales should these surveys be conducted, need to be appropriately addressed before the onset Keywords: marine, benthos, monitoring, scale, of any monitoring programme. temperate, resolution This review attempts to answer the methodological questions of scale, habitat and community by providing an account of current monitoring 1. Introduction methods available to marine researchers. In the The status of the seas and oceans is of increasing dynamic and growing field of marine habitat importance to conservation agencies, marine-based characterisation, varied sampling techniques are industries and government departments worldwide. employed by researchers. Rather than compile Evaluating status of the marine environment is an extensive list of methods and research equip- linked strongly with effective monitoring that may ment, which have been covered adequately in be employed for the accurate assessment of re- previous reviews (Kingsford and Battershill, 1998; sources (such as fish stocks, mineral deposits and Eleftheriou and McIntyre, 2005; Coggan et al., hydrocarbon reserves), marine habitats and pollu- 2007), this account consolidates current monitor- tant levels and for making reliable observations and ing research and makes recommendations for the informed predictions. monitoring programmes of the future based on The concept of monitoring is defined by current technological developments. Goldsmith (1991) as: ‘intermittent (regular or irreg- In Europe, recent international legislation, such ular) surveillance carried out in order to ascertain as the EU Habitats Directive (Council Directive

99 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

92/43/EEC on the conservation of natural habitats their associated environment; ‘community’ is most and of wild fauna and flora, 1992) and the Water closely related to the dynamic assemblage of species Framework Directive (WFD 2000/60/EC, 2000), living within a habitat; and ‘biotope’ is seen as a has spurred marine agencies and institutions into blend of the two, with both habitat and community developing a range of monitoring programmes to as one functional unit. suit a variety of environmental concerns. These programmes have to meet the challenges of 2. Communitymonitoring(fine-scalemethods) sampling scale, resolution and robustness over time, The biological component of any monitoring pro- yet be practical and cost-effective in a challenging gramme requires the collection of high resolution environment. However, marine monitoring of data from fine spatial scales (0.01–10m) to facili- temperate waters has historically developed slower tate accurate species identification. As species are than that in tropical waters (Davies et al., 2001; Hill present within a habitat at micro-, meio- and macro- and Wilkinson, 2004; Jokiel et al., 2005; Coggan faunal scales, it is also necessary to determine which et al., 2007). In the tropics, field survey conditions species are to be targeted and at what scale should are more amenable to all scales of marine research, the surveys operate. Once a species or assemblage and well established programmes conducted at has been targeted, it is important that sampling community, government and research institute equipment appropriate to the size and ecology of levels of expertise have been operating for some that species is selected for monitoring to avoid time (Hill and Wilkinson, 2004). Indeed, the better misrepresenting it in the data. Usually conspicuous developed areas of tropical marine research may macrofauna (0.01–1.00m scale), indicative of a be of great benefit to the contemporary areas of particular habitat or environmental condition, are temperate marine research programmes, an issue selected for monitoring. In this way the presence, which is addressed in this review. absence, abundance and percentage cover of these In contemplating these issues, this account biota can provide proxy indicators of the status of covers the most common methods used to monitor the environment (Goldsmith, 1991). shallow (0–40m) sublittoral benthic communities At the scale of centimetres to metres, soft and from temperate waters, incorporating tropical hard substrata present the researcher with very methods where appropriate. The benthos has been different conditions in which to monitor. At these regarded as a good indicator of environmental fine scales, the methods best employed within each condition and quality (Alden et al., 1997), and broad habitat type are very different as a direct the majority of conservation work and research result of the physical substratum. efforts are likely to occur in the shallow sublittoral zone (encompassing the infralittoral and shallow 2.1. Soft substratum community monitoring circalittoral zones). Limiting this review to shallow Unconsolidated sediments of soft substrata, con- water benthic environments will cover a large sisting of varying proportions of clay, mud, silt, degree of the current monitoring effort. sand and gravel, typically support rich infaunal The present account is divided into three broad communities of meio- and macro-fauna, along with sections: spatial monitoring, which reviews the motile epifaunal communities. Habitats within soft methodologies used to map and identify habitats substratum areas can cover vast regions of seabed at a range of different spatial scales; community (e.g. abyssal plains), but are considered to be monitoring, which reviews the high resolution relatively homogenous in terms of the community methods used within those habitats to qualify and assemblage within each habitat (Zajac, 2008). quantify fine-scale biological communities (from Methods used to sample these communities both soft and hard benthic substrata); and biotope at fine scales have changed little over the past monitoring, which reviews a newly emerging area of century, with the exception of sediment profile marine monitoring where habitat- and community- imagery, or SPI (Solan et al., 2003). Samples based methods are blended to study meso-scale from the seabed have been collected through changes in marine environments. These sections the physical removal of known areas of seabed are discussed in order of ascending spatial scales, brought to the surface, where they are usually from fine-scale community monitoring, through sieved (to remove larger particles of sediment) meso-scale biotope monitoring, to broad-scale and sorted to identify the biota. Sediment grab habitat monitoring methods (Table 1). samplers have proved effective for this task and are For the purposes of consistency, the concepts used widely today (Kingsford and Battershill, 1998; of habitat, community and biotope used in this Elías et al., 2005; Lu and Wu, 2007). A variety of paper are taken from Olenin and Ducrotoy (2006). grab samplers (such as Petersen, Campbell, Day, In brief, ‘habitat’ is related most to the physical van Veen, Shipek, IKU, Ponar, Ekman and Smith- and spatial structure of biological communities and McIntyre) are available to sample unconsolidated

100 Vol 28, No 3, 2009

Table 1: Broad evaluation of different monitoring methods and their application to monitoring marine environments at different scales: impact is defined as the level of disturbance to the monitored biota and cost refers to the financial cost of the monitoring method (based on table from Kingsford and Battershill, 1998) Scale Monitoring Method Monitoring Substratum Impact Cost Deployment Fine Sediment profile imager (SPI) Community Soft Mod High Ship Cores Community Soft Mod Mod Ship Grabs Community Soft Mod Mod Ship Quadrat Community Hard Low Low Scuba Photoquadrat Community Hard Low Mod Scuba Transect Community/Biotope Hard Low Low Scuba Transect – Video Community/Biotope Hard Low Mod Scuba

Meso Trawls Community/Biotope Soft High Mod Ship Dredges Community/Biotope Soft High Mod Ship Towed camera sled Community/Biotope/Habitat Soft Mod Mod Ship Dropdown camera Community/Biotope/Habitat All Low Mod Ship Remotely operated vehicle (ROV) Community/Biotope/Habitat All None High Ship Manta tow Community/Biotope/Habitat All None Low Boat Diver propulsion vehicle (DPV) Community/Biotope/Habitat All None Mod Scuba

Broad Single beam sonar Biotope/Habitat All None High Ship Sidescan sonar Biotope/Habitat All None High Ship Multibeam sonar Biotope/Habitat All None High Ship Aerial photography Biotope/Habitat All None High Aircraft Light detection and ranging (LIDAR) Biotope/Habitat All None High Aircraft Satellite remote sensing Biotope/Habitat All None High Satellite soft substrata; each tool functions to overcome replication vary among studies: three samples per different sampling difficulties, substrata types or site (Mistri, 2002; Chainho et al., 2006), four per survey vessel constraints. Eleftheriou and McIntyre site (Elías et al., 2005; Aguado-Gimenez et al., 2007) (2005) and Coggan et al. (2007) provide an in- and five per site (Lu and Wu, 2007). In the UK, depth description and review of these various types soft substratum monitoring protocols have been of sampling tools. established at some sites for over 20 years and are Benthic corers operate to a greater sediment currently represented in the Green Book. Its sug- depth (>20cm) than grab samplers, thus collect gestion is to collect five replicates per site annually more infauna in each sample. With careful han- within a 50m radius of the site location (Natural dling, benthic corer samples can reveal additional Marine Monitoring Programme [NMMP], 2003). information regarding sediment stratification and Sampling design must also be considered in mon- depth of the Redox Potential Discontinuity (RPD) itoring studies. In a comparison, predetermined layer, as well as infaunal burrow structuring. As fixed sampling sites generated greater statistical with sediment grab samplers, a range of corers power than samples collected from random sites in (gravity, piston, pneumatic and vibracores) are the first year and re-sampled in subsequent years, available to researchers for use under different or random samples collected each consecutive substrata conditions. year (Van der Meer, 1997). In other comparative These methods collect samples from very fine studies, a random stratified approach to monitoring spatial scales with sampling footprints of ∼0.1m2, provided more accurate long-term data than ran- from which very high-resolution data may be dom, systematic or adaptive designs (Aschan, 1988; generated and particle size analysis (PSA), infaunal Cabral and Murta, 2004). In using this approach, community assemblages and contaminant infor- long-term trends in shallow macrobenthic commu- mation may be extracted. The drawbacks are the nity assemblages have been correlated to fluctua- time and skill required to analyse samples and tions in the North Atlantic Oscillation off the coast the simple fact that such fine-scale data must be of western Sweden (Tunberg and Nelson, 1998), extrapolated to represent potentially vast areas of climatic and anthropogenic factors in the North seabed. Therefore, replication is a major issue Sea (Clark and Frid, 2001) and anthropogenic with soft substratum community monitoring. It is thermal pollution in the Firth of Clyde, Scotland generally recommended that larger numbers of (Barnett and Watson, 1986). Short-term trends and small replicates yield greater statistical power than seasonality in shallow macrobenthic communities fewer large replicates (Aschan, 1988). Levels of are detected by sampling throughout the year and

101 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

infer effects ranging from sewage impacts and storm survey equipment (which must be practical), tidal activity (Elías et al., 2005), to seasonal oxygen forces, currents and surface weather conditions. deficiency in fjords (Nilsson and Rosenberg, 1997) The biota themselves must, on occasion, be and competition and nutrient availability in shallow factored into survey work, such as when surveys embayments (Lu and Wu, 2007). are conducted in kelp forest areas (limiting New technologies, such as SPI, may generate manoeuvrability) or over substrata with dense algal additional fine-scale community information relat- cover (obscuring understory biota) (Leonard and ing to infaunal species ecology and assemblage Clark, 1993). These factors limit the time allowed structure (Solan et al., 2003). Raw SPI data may to work under water, what survey equipment can be collected less invasively than that using cores be carried and manipulated, and where and when and may be stored as permanent digital records. In surveys can be conducted. In some cases, the use addition, the imagery may also be analysed faster, of remotely operated vehicles (ROVs) has been and infaunal ecology, with particular reference to explored as alternative to using divers (Lam et al., burrow structure, may be more accurately stud- 2007; Lirman et al., 2007), although they are more ied (Nilsson and Rosenberg, 1997; Solan et al., commonly used in deeper waters beyond diving 2003; Birchenough et al., 2006). However, the depths (Jerosch et al., 2007). advantages and disadvantages of using SPI should The monitoring methods most commonly used be carefully considered before its use in a mon- at fine scales on hard substrata employ a variety itoring programme (O’Connor, 2001). New sam- of quadrats and transects to collect community pling regimes, such as grid-based point-sampling data. Quadrats are typically used to collect high (replicates spread evenly throughout the habitat) resolution, quantitative community data across may be more appropriate to monitor large areas spatially heterogenous areas of hard substratum of soft substratum than the established regimes (Kingsford and Battershill, 1998), including Modi- (all replicates around one location). Additional olus sp. reefs growing on soft substrata (Sanderson research, such as that of Hewitt and Thrush (2007), et al., 2008). They are often deployed at intervals is required to determine if these new technologies along a transect line to provide more detailed and sampling regimes will be of benefit to the soft community information (Moore et al., 2006; Shears, substratum monitoring programmes of the future. 2007a,b; Carballo et al., 2008; Sanderson et al., 2.2. Hard substratum community monitoring 2008) and, as such, provide an excellent means of rapidly assessing sites for future monitoring. For Hard substrata, consisting of rock, boulders or consolidated sediments, do not support diverse monitoring programmes, the use of quadrats at infaunal communities, but instead provide surface permanent sites has been recommended as the best and structure that support varied and rich assem- means to assess changes to the smallest areas of blages of epifauna and epiflora. Space for coloni- seabed (Kingsford and Battershill, 1998; EK Brown sation is usually at a premium and is, therefore, et al., 2004). As such, fixed quadrats deployed at subject to considerable competition between biota. permanent sites are used for the study of individual Dynamic and heterogenous communities usually colonies of hard corals (EK Brown et al., 2004), or develop in these types of habitats with networks sponges (Duckworth and Battershill, 2001). of overgrowth, a high proportion of reef forming A transect may be deployed in many ways organisms and a patchy, complex collection of to collect high-resolution data; this is largely diverse communities (Wood, 1999). Monitoring dependent on the survey objectives (Sayer and communities on these substrata has proven to be Poonian, 2007). For example, when used in more difficult than the communities inhabiting short lengths along predetermined depth contours, unconsolidated soft substrata, thus standardised data from transects have characterised coral reef monitoring protocols vary considerably worldwide. community structure at the species level (EK Brown More research in standardising methodologies has et al., 2004; Leujak and Ormond, 2007), but when been conducted within tropical latitudes than in deployed perpendicular to the shore, descending temperate latitudes (EK Brown et al., 2004; Jokiel into the sublittoral, they have successfully recorded et al., 2005; Leujak and Ormond, 2007); although changes in community assemblages with depth at beyond the remit of this review, this accumulated the biotope level (Parsons et al., 2004; Moore et al., wealth of knowledge and experience can benefit 2006; Shears, 2007a,b). It is worth noting that when temperate monitoring programmes and in some collecting data at the species level, transects are cases is clearly transferable. much shorter (∼10m) than when acquiring data As the majority of hard substratum monitoring is at biotope level (∼200m). As with data generated conducted using scuba divers, any survey work must from using quadrats, when transects have been factor in dive tables (limiting time under water), deployed at permanent sites, they have detected

102 Vol 28, No 3, 2009

temporal community changes better than randomly usually repulsed by the presence of divers (Sayer located transects (EK Brown et al., 2004). and Poonian, 2007). Stereo-video data can provide The size of sample and number of replicates greater depth perception of epifaunal and epifloral conducted depends upon the objectives, location communities than a single video camera, leading and resources of the monitoring programme (Sayer to more accurate species identification (Lundalv and Poonian, 2007). Quadrats of 1m2 have been and Christie, 1986; Lundalv et al., 1986). Video employed by many researchers (Parsons et al., transects can be used to detect changes in coral reef 2004; Leujak and Ormond, 2007), although smaller communities (EK Brown et al., 2004; Jokiel et al., quadrats of 0.25m2 (Kingsford and Battershill, 2005; Leujak and Ormond, 2007) and in temperate 1998) and even 0.0625m2 (Moore et al., 2006) have rocky communites (Parsons et al., 2004). been used to target specific fauna in some surveys. Fixed photoquadrat monitoring has been When replication is considered, many studies employed to detect the growth and recruitment of have resulted in different recommendations: 5–10 tropical corals over a 12-year period (Nybakken, quadrats per discrete area (Moore and Gilliland, 1997). Method comparison studies have explored 1999), 8–12 per discrete area (Kingsford and which of these methods and sampling designs per- Battershill, 1998), 27 per 50m transect (Leujak and form best at detecting changes in the community Ormond, 2007). For transects, the same problems assemblages of hard substrata. In the development are clear. EK Brown et al. (2004) found that of Hawaii’s Coral Reef Assessment and Monitoring in areas of high habitat heterogeneity (such as Program–Rapid Assessment Technique (CRAMP- coral reefs), shorter transects (10m) were more RAT) survey methodology, high-precision sampling statistically reliable than longer transects (25–50m), using a stratified random approach, as well as using yet Houk and Van Woesik (2006) found that longer permanent stations for transects and quadrats alike, transects (50m) with less replication yielded better was found to generate higher statistical robustness estimates of coral cover and diversity than shorter in a monitoring programme (EK Brown et al., 2004; transects (15m and 35m) with more replication. Jokiel et al., 2005). Although potentially a site-specific issue, it is clear There appears to be a range of different rec- that more research needs to be conducted with ommendations among researchers as to the most reference to the optimum quadrat and transect appropriate method of data collection and analysis size, as well as levels of replication, required across to be used in hard substratum environments. In a a range of differing sites before a more general comparison between different coral reef monitor- standardised protocol is agreed upon. ing methods – diver hand-mapping; point intercept The use of digital imagery has greatly facilitated methods of analysis from a video camera, stills scuba survey work, allowing faster and greater levels camera and diver observations; percentage cover of data collection than traditional manual observa- analysis from a stills camera and line intercept from tions on dive slates (Cabaitan et al., 2007; Leujak diver observations – along a 50m transect, the over- and Ormond, 2007). Indeed, when given the time all conclusion was that video-based methodology constraints of scuba, underwater photography and performed the best overall in terms of accuracy, videography provide the only practical means to cost and time taken to survey and process the data sample large areas under water (Aronson et al., in the study (Leujak and Ormond, 2007). This 1994). The quality of imagery, however, is affected view is shared in a number of other similar studies by underwater visibility and turbidity, therefore (EK Brown et al., 2004; Jokiel et al., 2005). limiting the efficacy of surveys based solely on A more recent comparison between stills and digital imagery. Despite this, advances in image video imagery showed, however, that although resolution (object discrimination possible at scales both media yielded similar results, analysis of of <1cm) have led to digital imagery becoming the video data required significantly more time the preferred medium of data collection from hard and was therefore less cost-effective than using substratum environments. With digital imagery also stills media for data collection (Cabaitan et al., comes the ability to generate permanent records 2007). Alternatively, the physical removal of the so that image classifications can be conferred sample for analysis in the lab has been shown among different researchers, thus generating fur- to be more accurate in determining abundance, ther survey accuracy. frequency counts and biomass of epifauna than The versatility of underwater video and stills using either imagery-based or in situ observation imagery in hard substratum surveys is still being methods (Beaumont et al., 2007). It is unlikely realised. Video used in free-swimming surveys that labour- and time-intensive laboratory-based captures cryptic species that quantitative methods monitoring methods will be used widely in the tend to miss (Breen et al., 2006); the use of infrared future because of cost implications. It is more video can record life stages of animals that are likely that future monitoring programmes will

103 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

be conducted using a combination of in situ will also increase the statistical power of monitor- stills- and video-based methodologies, for despite ing data (EK Brown et al., 2004). Advances in greater acquisition costs, the long-term efficiency underwater site location technologies, such as radio and benefit of using these mediums will prove acoustic positioning telemetry (RAPT), Shallow valuable (Aronson et al., 1994; EK Brown et al., Water Positioning System (SWaPS) and ultra-short 2004; Jokiel et al., 2005; Leujak and Ormond, 2007). baseline system (USBL), will undoubtedly increase More recently, the benefits of mosaicing images the accuracy and sensitivity of future hard substra- together to reconstruct entire survey sites have tum monitoring programmes (Parsons et al., 2004; been explored (Burton et al., 2007; Lirman et al., Whittington et al., 2006; Lirman et al., 2008). 2007). The technology is not new with previous applications in maritime archaeology (Ballard et al., 3. Biotope monitoring (meso-scale methods) 2000; Martin and Martin, 2002) and seafloor By sampling over meso scales (10m–1km), the mapping (Rzhanov and Mayer, 2004), although condition of many habitats may be assessed in less until recently, it has not been applied or explored time and at less expense than conducting numerous in any great depth to fine-scale benthic community independent fine-scale surveys within each habitat. monitoring (Burton et al., 2007). Image processing, In addition, motile benthic fauna that are usually with the emphasis on the generation of automated not detected in fine-scale surveys may also be mosaicing software (Gracias and Santos-Victor, sampled. The emphasis of this type of monitoring 1998, 2000; Smolic and Wiegand, 2001; Jerosch is to detect coarse assemblages of biota and habitats et al., 2007), automated image recognition (Marcos termed commonly as ‘biotopes’ across large areas of et al., 2005) and geo-referencing of mosaics seabed. (Vincent et al., 2003; Zhu et al., 2005; Rzhanov et al., In recent years, biotope maps have been pre- 2006), is where the majority of past research was sented in many public reports (Jones et al., 2000; conducted. Bates et al., 2004; Moore et al., 2006) as a blend It is worth noting that automated image mosaic- of broad-scale mapping surveys together with fine- ing software available today tends to be more appli- scale biological surveys. Presenting these different cable to panoramic videography (e.g. Photoshop) data collectively in the meso scale has proved an or designed for military use (e.g. Terrasight) and adequate method for detecting gross habitat and thus very expensive. Despite a lack of specifically community changes in monitoring programmes developed, automated mosaicing software, image (Parsons et al., 2004). It should be noted that no mosaicing will be of great benefit to monitoring strict meso-scale monitoring programmes exist at programmes in the future, when high resolution present without the incorporation of fine-scale and data may be collected at fine scales over large areas broad-scale methods. of seabed. Larger samples can be collected and Meso-scale methods are either qualitative or replication reduced without compromising data semi-quantitative, with no practical fully quantita- resolution. Although successful in tropical waters tive methods available at present. Most of the equip- 2 over an area of 400m (Lirman et al., 2007), it is ment used – such as underwater cameras, sledges, more likely that image mosaics will be significantly trawls or dredges – are deployed from survey vessels. smaller in turbid, temperate waters. Traditional destructive methods, such as trawls and It is evident that monitoring at fine scales dredges, are still in some cases employed today, (1m2–0.1m2) must utilise precise methods to collect as they allow the physical removal of a sample for species information from the communities of both sorting in the laboratory (CJ Brown et al., 2001, soft and hard substrata. With this high-resolution 2002; Beaman and Harris, 2005; Lathrop et al., data, changes in community structure are more 2006). These methods provide a means of collecting effectively detected (Hewitt et al., 1998). How- semi-quantitative data of both sessile and motile ever, accurate positional data must accompany forms of benthic fauna and, as such, remain the only the biological data, and replication must not way of monitoring crustacean populations (Viscido only be adequate, but also spatially spread out et al., 1997). Many types of trawl exist, such as to increase the confidence of broad-scale habitat Agassiz, beam, otter and Jackson Rockhopper trawls characterisations. It appears that across different (Greenstreet et al., 1997; Kingsford and Battershill, substratum types, a random stratified approach 1998), and each type generally consists of a wide- to sampling yields more robust data and should mouthed net towed through the water. Dredges, be considered for all monitoring programmes at such as the naturalist’s, anchor, hydraulic, bucket this scale (Aschan, 1988; EK Brown et al., 2004; or rock dredges, generally consist of large, towed Cabral and Murta, 2004; Jokiel et al., 2005). Precise metal frames with a mesh bag to collect the sample location, particularly at sites on hard substrata, (Kingsford and Battershill, 1998). The efficiency

104 Vol 28, No 3, 2009

of these methods depends largely on the survey Fish stock assessment surveys represent one of conditions, substratum type and the mobility of the more active areas of meso-scale research. epifauna. For Norway lobster (Nephrops norvegicus) stock Where trawls and dredges cannot operate over assessments, there is a trend towards developing hard substrata, optical methods must be used. methodologies based on towed optical systems as The immediate advantages are that permanent opposed to more destructive traditional methods records are generated and large areas of seabed such as bottom trawling (Ball et al., 2000; Smith may be surveyed (Kingsford and Battershill, 1998). et al., 2003; Morello et al., 2007). Similar work Three main types of optical systems are used over employing towed optical systems has been used to meso scales, each differing in the control the develop stock assessment models of scallop popu- researcher has over the image: drop-down systems, lations (Adams et al., 2008). Few of these studies, towed systems and ROVs. All three systems can use however, have conducted temporal assessments of video/stills photography, often employing a combi- stocks in the form of regular monitoring (Smith and nation of both (Gilkinson et al., 2003). Drop-down Papadopoulou, 2003). As more emphasis and im- systems are used frequently to validate acoustic portance is placed on the monitoring of sublittoral surveys (Beaman and Harris, 2005; Hutin et al., biotopes, the necessary interest to develop robust, 2005; Roberts et al., 2005), representing a cheap and ideally quantitative, meso-scale methods for and effective method for surveying large areas at future monitoring programmes will be created. acceptable resolution (Brown and Coggan, 2007). As they are usually deployed close to, but not touch- 4. Spatial monitoring (broad-scale methods) ing, the seabed, accurate scaling of benthic features is not usually possible. The alternatives have been Remote-sensing methods operate over a range to use laser dots for scale (Bax et al., 1999) or of spatial scales, with the ability to image fine- 2 stereo-cameras (Kingsford and Battershill, 1998). scale (boulders <1m ), meso-scale (biogenic reefs 2 2 Towed optical systems, consisting of a protective >100m ), and broad-scale (banks >10000km ; 2 sled that houses the camera and light systems, shelves >100000km ) areas (Anderson et al., 2008). overcome the problem of scaling, as they are This collective operational range across the scales dragged across the seabed, thus enabling the is particularly useful over the larger areas of seabed image dimensions to be calculated. Like drop-down for which no standard monitoring procedures exist. cameras, camera sleds can collect data from large As with a range of spatial scales, the resolution areas of seabed and may be used to validate acoustic of remote-sensing data can be equally variable, surveys (Birchenough et al., 2006; Ehrhold et al., ranging from low-resolution satellite-borne systems, 2006), or identify fish habitat over meso scales such as medium-spectral resolution, imaging spec- 2 (Shucksmith et al., 2006). Towed systems are not trometer, or MERIS (300m grid), to systems that usually used over hard substrata because of deploy- offer higher resolution, such as aerial photography, ment constraints and the inherent difficulties of light detection and ranging (LIDAR), sidescan and towing over very rough ground; therefore, they are multibeam sonars (1m2 grid); see Table 2. only effective while operating over soft substrata. Clear monitoring objectives are needed before ROVs offer the greatest control to the researcher the employment of a remote-sensing system, as well among remote optical systems and can be actively as determining the required scale and resolution piloted to specific sites while also being capable needed for the duration of the programme. of surveying large areas (Jerosch et al., 2007). In many cases, the acquisition costs and data Powered by propellers and thrusters, ROVs can processing times are as important as the sensitivity be manoeuvred carefully into sensitive areas, such and range of the system. The many remote-sensing as cold water coral reefs, where they can be used systems differ in their basic function, as well as to carry out inspections across areas ranging from where they collect the data from. They are broadly hundreds of metres to a several kilometres (Fossa divided according to their data acquisition systems, et al., 2002). The versatility of ROVs means that they with all above-water systems using optical/laser- have also been used to validate areas in acoustic based methods and below-water systems typically surveys (Wildish et al., 1998; Hovland et al., 2002). utilising acoustic-based methods. The limiting factors of the high acquisition costs of From space, satellite-based systems such as ROVs, coupled with their inability to work in strong IKONOS, LandSat, ALI, Quickbird and MERIS, currents, mean that dropdown cameras appear to collect optical data from the surface of the planet be a method of choice over hard substrata at meso across the electromagnetic spectrum on sensors scales (Brown and Coggan, 2007). operating over predefined spectral ranges, or Monitoring of marine substrata in shallow tem- bands. A range of different spatial resolutions are perate waters over meso scale areas is not common. achievable across these systems (Table 2). Although

105 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

Table 2: Overview of operational capabilities of a range of remote sensing technologies with respect to marine habitat mapping (based on table from Kenny et al., 2003) Horizontal Operational resolution resolution Method System Scale range (m) (m) Reference Satellite Envisat MERIS Broad >300–300 300 Kutser et al., 2006 LandSat Broad 90–30 30 Mumby and Edwards, 2002, Weiers et al. 2004; Zharikov et al., 2005; Kutser et al., 2006 SPOT Broad >20–20 20 Zharikov et al., 2005 IKONOS Broad 4–1 4 Mumby and Edwards, 2002; Zharikov et al., 2005; Kutser et al., 2006 Quickbird Broad >2.4–2.4 2.4 Kutser et al., 2006

Aerial photos CASI imagery Broad >10–1 1 Mumby and Edwards, 2002; Gagnon et al., 2008 GEOSCAPE imagery Broad >10–2.5 2.5 Zharikov et al., 2005

LIDAR LIDAR Broad–Meso 1–25 1 Brock et al., 2006; Intelmann, 2006; Wedding et al., 2008

Sonar Multibeam Broad–Meso 100–0.1 1 Kenny et al., 2003; Anderson et al., 2007 Sidescan Broad–Meso 100–0.01 0.1 Kenny et al., 2003; Anderson et al., 2007 Single beam Broad–Meso 100–0.01 1 Kenny et al., 2003; Anderson et al., 2007

these technologies are more applicable to the map- that of aircraft-based systems, with resolution in the ping of terrestrial habitats (Weiers et al., 2004), order of 1m2 (Table 2). With these capabilities, system comparison studies have been conducted this remote-sensing method is likely to be used for in tropical waters (Mumby and Edwards, 2002) future shallow intertidal and subtidal habitat clas- and habitat characterisation studies have been sification surveys, and possibly even in monitoring conducted in temperate waters (Karpouzli and programmes (Gesch and Wilson, 2002). Malthus, 2003; Kutser et al., 2006). Critically, the These above-water methods do share a common sensors fail to detect seabed features deeper than a drawback, regardless of image resolution and spa- few metres in temperate waters because of the high tial range of survey: their entire sensory system relies absorption of electromagnetic energy by seawater on detecting light reflected up from the ground. (Kutser et al., 2006). In shallow sublittoral environments, particularly From the skies, aircraft based systems (such as in turbid temperate waters, above-water remote Center for Aircraft and Systems/Support sensing methods lack sufficient depth penetration Infrastructure, or CASI) collect optical data in a to be able to successfully image the seabed. similar process to the multispectral sensors onboard It is from ships that the best seabed mapping the satellites, but to higher resolutions of 1m2 data is collected across a range of depths from a grids (Table 2). The optical sensors on aircraft range of seas, through the use of sound naviga- systems are capable of detecting greater radiance tion and ranging (sonar). Hull-mounted systems, contrast from the seabed than those on satellites, such as single-beam echo-sounders (SBES) and thus significantly improving image classifications multibeam echo-sounders (MBES); towed systems, (Mumby and Edwards, 2002). Issues pertaining such as sidescan sonar; and pre-programmed to adequate depth penetration in turbid waters autonomous underwater vehicles (AUVs) utilise highlight the limitations for these optical sensors in sonar technology by emitting pulses of sound from temperate waters (Theriault et al., 2006). transducers and detect the reflected echoes from Perhaps the most successful above-water optical the seabed on receivers. By their emission and methods to date have been the LIDAR systems, detection of sound pulses, sonar systems differ which have been demonstrated to identify seabed because of their beam forming and reception features in temperate seas to depths of 22.2m properties. A brief description of the effects that (Intelmann, 2006) and, under ideal conditions, different angles of incidence, frequency, foot- are rated to 40m depths (Wedding et al., 2008). print size and multiple beams have on sonar Achievable spatial resolution for data is similar to systems is provided with respect to acoustic seabed

106 Vol 28, No 3, 2009

classification (Kenny et al., 2003; Anderson et al., the employment of two acoustic systems becomes 2007; 2008). important. Firstly, a method is needed to map large areas at a broad scale; MBES are able to 4.1. Angle of incidence insonify large areas of seabed relatively quickly, Systems with a normal angle of incidence, such as from which high-resolution and spatially accurate SBES (and MBES in part), are typically used to bathymetric maps can be produced through an ob- measure seabed bathymetry, whereas systems with jective, statistically based classification. These maps an oblique angle of incidence, like sidescan sonars form ideal base maps from which future areas of (and MBES in part) are typically used to measure interest/monitoring can be identified and targeted. seabed texture and roughness, determined by Secondly, a method is needed to collect more analysis of the backscatter. detailed data from these targeted areas, preferably with habitat information; sidescan sonar produces 4.2. Frequency high-resolution, spatially accurate backscatter maps Acoustic beams of higher frequencies are able to at broad and meso scales, usually produced through resolve smaller features on the seabed, achieving subjective, validation-based classification (CJ Brown horizontal resolution of up to 0.1m (sidescan et al., 2001, 2002, 2004a,b). Although a third system sonar) and 1m (MBES) (Reid, 2007), whereas lower is available to researchers in the form of SBES frequencies have poorer spatial resolution but are acoustic ground discriminating systems (AGDS), able to penetrate the seabed, thereby detecting the research has demonstrated that this system is underlying geological features. largely obsolete when operated over broad scales in 4.3. Footprint size comparison with sidescan sonar and MBES (Brown The size of the acoustic ‘footprint’ is important, as et al., 2005). it determines the area over which the sound energy All remote-sensing systems require data valida- is dispersed. A characteristic of acoustic beams is tion (ground-truthing) for habitat classification that they fan out with increasing water depth, so purposes, producing what is referred to as a at greater depths the footprint is larger than when supervised classification (Simard and Stepnowski, in shallower water. In shallow sublittoral habitats, 2007). Too few studies have been conducted smaller footprints increase the resolution of the in automated seabed classifications without data beams, but also increase the surveying effort. validation (Brown and Coggan, 2007) – referred to as unsupervised classifications to negate the need 4.4. Swath systems versus single track for adequate validation surveys. Therefore, seabed When SBES operate in shallow water, data is habitat classifications achieved from remotely collected from the area of seabed that is the size sensed data sources are only as accurate as the of the beam’s acoustic footprint. By surveying in validation survey carried out post-classification tightly spaced lines, the majority of the seabed can (McGonigle et al., 2009). be insonified to a high level of detail, though for As previously discussed, validation surveys are full 100% seabed coverage, complex and inaccurate normally conducted using other sampling appa- interpolation of all the track data is required to ratus designed for operation in specific habitats, fill in the blank areas. With the multiple beams of such as grabs, dredges and cores for soft substratum a swath system (MBES), over 100 beam footprints areas, and dropdown optical systems to collect fan out under the survey vessel, and by surveying stills and video for hard substratum areas. Scuba in similarly tightly spaced lines, 100% of the divers and ROVs offer a more flexible alternative seabed may be insonified and the tracks mosaiced to these methods and increase researcher con- together, requiring little or no interpolation. The trol over the data validation survey. There is an overlap in the beams adds further detail to the obvious mismatch between finer scale validation classification and can generate very high resolution methods and the broader scale remotely sensed seabed classifications (McGonigle et al., 2009). classifications. When fine- and meso-scale data Towed sidescan sonar systems are also regarded as is extrapolated to larger areas based on remote swath systems, on account that the acoustic beams classifications, it is imperative that the validation have an oblique angle of incidence (high-grazing survey should be carefully researched, robust and angle) either side of the towfish. This results in the spatially accurate for successful, remotely sensed insonification of wide tracks of the seabed that are seabed classifications (Anderson et al., 2008). usually mosaiced together in a similar fashion to There are few studies that have concluded MBES data, to create seabed classifications based on remote-sensing methods for shallow sublittoral 100% coverage. habitat monitoring; surveys based on change de- When the above factors are applied to sur- tection over time are focused largely on geological veying shallow sublittoral benthic environments, features (Diesing et al., 2006; McDowell et al.,

107 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

a BROAD-SCALE MONITORING METHODS (Spatial Mapping) 10000m

LIDAR

Sidescan SONAR

Multibeam SONAR

b MESO-SCALE MONITORING METHODS (Biotope Monitoring)

Beam Trawl Drop-down Camera 1000m

Camera Sled ROV

c FINE-SCALE MONITORING METHODS (Community Monitoring)

Grab Sampler Box Corer 10m

Video Transect Photoquadrat

Fig 1: Monitoring methods over different sampling scales: (a) mosaiced LIDAR and mulitbeam sonar bathymetric data, with targeted sidescan sonar survey area (white box); (b) mosaiced sidescan sonar data from (a), with targeted community monitoring area (white box); and (c) image showing boundary between a hard-substrate reef and medium sand habitat

2007; Du Four and Van Lancker, 2008). Of the habitats indicate that remote monitoring of shallow few studies focused on change detection in benthic benthic habitats is possible and could, therefore, be habitats, the majority of successes appear to be in attempted using a combination of remote-sensing tropical and sub-tropical waters in which remote technologies, particularly where habitat maps are to methods have successfully monitored the status of be included in monitoring programmes. coral reefs and seagrass beds (Ardizzone et al., 2006; Collier and Humber, 2007). Large biological 5. Monitoring recommendations structures, such as beds of the giant kelp (Macrocystis pyrifera), have been monitored in temperate waters A number a key issues have been identified (Grove et al., 2002), and a whole range of other throughout this review. When considering the temperate sublittoral habitats have been remotely most appropriate monitoring strategy, the scale at identified and mapped: scallop grounds (Kostylev which surveys are conducted is as important as et al., 2003); Lophelia sp. reefs (Roberts et al., 2005); the sampling equipment selected for the survey. Modiolus sp. reefs (Wildish et al., 1998; Lindenbaum At each of the three spatial scales (fine, meso et al., 2008); Lanice conchilega reefs (Degraer et al., and broad) selected for this review, a diversity of 2008); and numerous soft sediment habitats (Sager different sampling devices and strategies have been et al., 2003; CJ Brown et al., 2004a,b; Ehrhold et al., discussed and evaluated through method compar- 2006; Lathrop et al., 2006). Although no repeat ison studies (Aschan, 1988; Mumby and Edwards, surveys were conducted in any of these studies, the 2002; EK Brown et al., 2004; Cabral and Murta, successful mapping and characterisation of those 2004; Jokiel et al., 2005; Leujak and Ormond, 2007).

108 Vol 28, No 3, 2009

A broad overview of the most widely used monitor- methodologies also represents an area for further ing methods, and the spatial scales at which they research because, among the sampling scales, they best operate at, is provided in Fig 1. may be of use to future biotope monitoring. Overall, it is clear that to monitor biological Exciting and new developments in the field communities and their associated habitats success- of temperate marine monitoring lie with the in- fully, with the aims of detecting variation over short creased use of AUVs. When fitted with underwater and long time scales (Kingsford and Battershill, cameras, sonar instruments and physical sampling 1998), survey methods must be employed at a equipment, these robots are capable of collecting variety of different spatial scales and must sample high-resolution data across all spatial scales. Should within a nested strategy. As such, a combination of this technology become more cost-effective and different remote methods such as LIDAR, SBES, robust in the future, it will provide researchers MBES and sidescan sonar is recommended for with an opportunity to sample across all scales with broad-scale habitat mapping surveys (Gesch and just the one sampling platform. AUVs may yet play Wilson, 2002; Gilkinson et al., 2003; Leriche et al., a major role in the future of marine monitoring 2006; Walker et al., 2008). methods in shallow temperate waters. Over the meso scale, a range of acoustic validation techniques, such as drop-down cameras, Acknowledgements video sleds and ROVs, are necessary for classifying The authors would like to thank Alex Callaway, the biotopes within the facies/habitats identified Annika Clements and Chris McGonigle for their through remote-sensing methods (Fossa et al., valued input in methodological discussions. Equally 2002; Hovland et al., 2002; Kostylev et al., 2003). so, the authors are appreciative of the com- This facilitates the targeting of all subsequent survey ments from the reviewers, which added to and work at fine scales, at which the status of biological refined the review text. The work was funded communities is assessed through different optical by Northern Ireland Environment Agency project and physical sampling methods, such as video entitled: ‘Investigating monitoring methods for transects, image mosaics, photoquadrats, grabs and assessing change in seabed habitats’ (University of cores (Hewitt et al., 1998; Parsons et al., 2004; Ulster grant: 1203-R-0187). Birchenough et al., 2006; Lathrop et al., 2006). There is scope for improvement of technical methods by increasing the efficiency of sampling, References the speed at which samples are processed and the Adams CF, Harris BP and Stokesbury KDE. (2008). Geostatistical comparison of two independent video objectiveness of any classifications generated. This surveys of sea scallop abundance in the Elephant Trunk may be achieved by greater automation in data Closed Area, USA. ICES Journal of Marine Science 65: processing of acoustic data (Collier and Brown, 995–1003. 2005; Anderson et al., 2008; Brown and Collier, Aguado-Gimenez F, Marin A, Montoya S, Marin-Guirao L, 2008; McGonigle et al., 2009) and further research Piedecausa A and Garcia-Garcia B. (2007). Comparison into developing automated image mosaicing and between some procedures for monitoring offshore cage culture in western Mediterranean Sea: sampling methods recognition software for optical data (Jerosch et al., and impact indicators in soft substrata. Aquaculture 271: 2007; Lirman et al., 2007). In addition, the need 357–370. for greater precision in the relocation of permanent Alden RW, Weisberg SB, Ranasinghe JA and Dauer DM. monitoring sites for subsequent surveys should be (1997). Optimizing temporal sampling strategies for viewed as a priority for future monitoring (Parsons benthic environmental monitoring programs. Marine et al., 2004), as this is seen to greatly improve the Pollution Bulletin 34: 913–922. Anderson JT, Holliday V, Kloser R, Reid D and Simard Y. accuracy and sensitivity of any monitoring work (2007). Acoustic seabed classification of marine physical previously carried out (EK Brown et al., 2004; Jokiel and biological landscapes. ICES Co-operative Research et al., 2005). Report 286. Copenhagen: International Council for the Further research is needed in the standardisation Exploration of the Sea (ICES), 195pp. of hard substratum monitoring techniques and Anderson JT, Van Holliday D, Kloser R, Reid G and Simard Y. (2008). Acoustic seabed classification: current methodologies in temperate waters where, at practice and future directions. ICES Journal of Marine present, there is significant variation in how similar Science 65: 1004–1011. methodologies are applied and interpreted (Davies Ardizzone G, Belluscio A and Maiorano L. (2006). Long- et al., 2001; Whittington et al., 2006; Shears, 2007b). term change in the structure of a Posidonia oceanica The utility of current guides, such as the Marine landscape and its reference for a monitoring plan. Marine Monitoring Handbook (Davies et al., 2001), which can Ecology: An Evolutionary Perspective 27(4): 299–309. Aronson RB, Edmunds PJ, Precht WF, Swanson DW and be updated online as new methodologies emerge, Levitan DR. (1994). Large-scale, long-term monitoring will perform an important role in this process. The of Caribbean coral reefs: simple, quick, and inexpensive development of quantitative meso-scale monitoring techniques. Atoll Research Bulletin 451: 1–19.

109 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

Aschan M. (1988). Soft bottom macrobenthos in a Baltic Brown CJ, Hewer AJ, Limpenny DS, Cooper KM, archipelago: Spatial variation and optimal sampling Rees HL and Meadows WJ. (2004b). Mapping strategy. Annales Zoologici Fennici 25: 153–164. seabed biotopes using sidescan sonar in regions of Ball BJ, Fox G and Munday BW. (2000). Long- and short- heterogeneous substrata: Case study east of the Isle of term consequences of a Nephrops trawl fishery on the Wight, English Channel. Underwater Technology 26(1): benthos and environment of the Irish Sea. ICES Journal 27–36. of Marine Science 57: 1315–1320. Brown CJ, Mitchell A, Limpenny DS, Robertson MR, Ballard RD, McCann AM, Yoerger D, Whitcomb L, Service M and Golding N. (2005). Mapping seabed Mindell D, Oleson J, Singh H, Foley B, Adams J, habitats in the Firth of Lorn off the west coast Piechota D and Giangrande C. (2000). The discovery of Scotland: evaluation and comparison of habitat of ancient history in the deep sea using advanced maps produced using the acoustic ground-discrimination deep submergence technology. Deep-Sea Research, Part I: system, RoxAnn, and sidescan sonar. ICES Journal of Oceanographic Research Papers 47(9): 1591–1620. Marine Science 62: 790–802. Barnett PRO and Watson J. (1986). Long-term changes in Brown CJ and Coggan R. (2007). Verification of acoustic some benthic species in the Firth of Clyde, with particular classes. In: Anderson JT, Holliday V, Kloser R, Reid D and reference to Tellina tenuis (da Costa). Proceedings of the Simard Y. (eds.). Acoustic seabed classification of marine Royal Society of Edinburgh: B 90: 287–302. physical and biological landscapes. ICES Co-operative Bates CR, Moore CG, Malthus T, Harries DB, Austin W, Research Report 286. Copenhagen: ICES, 127–144. Mair JM and Karpouzli E. (2004). Broad scale mapping Brown CJ and Collier JS. (2008). Mapping benthic habitat of sublittoral habitats in the Sound of Barra, Scotland. in regions of gradational substrata: An automated Scottish Natural Heritage Report: 005, 147pp. approach utilising geophysical, geological, and biological Bax N, Kloser R, Williams A, Gowlett-Holmes K and relationships. Estuarine Coastal and Shelf Science 78(1): Ryan T. (1999). Seafloor habitat definition for spatial 203–214. management in fisheries: a case study on the continental Brown EK, Cox E, Jokiel PL, Rodgers KS, Smith WR, shelf of southeast Australia. In: Oceanologica acta: Marine Tissot BN, Coles SL and Hultquist J. (2004). Development Benthic Habitats and their Living Resources: monitoring, of Benthic Sampling Methods for the Coral Reef management and applications to Pacific Island countries, Assessment and Monitoring Program (CRAMP) in Hawai’i. Pacific Science 58: 145–158. Vol. 22. Paris: Elsevier, 705–720. Burton M, Lock K, Gibbs R and Newman P. (2007). Beaman RJ and Harris PT. (2005). Bioregionalization of the Skomer Marine Nature Reserve project status report George V Shelf, East Antarctica. Continental Shelf Research 2006/2007. Countryside Council for Wales regional 25(14): 1657–1691. report: CCW/WW/07/4. Bangor, Wales: Countryside Beaumont JC, Brown CJ and Sayer MDJ. (2007). Evaluation Council, 79pp. Available at http://www.wwmc.org.uk/ of techniques used in the assessment of subtidal epibiotic SkomerMNR_PSR_2006.pdf, accessed on 5 May 2009. assemblage structure. Biofouling 23: 343–356. Cabaitan PC, Licuanan WY and Gomez ED. (2007). Birchenough SNR, Boyd SE, Coggan RA, Limpenny DS, Comparison between Videographic and Photographic Meadows WJ and Rees HL. (2006). Lights, camera Methods in Assessing Coral Reef Benthic Communities. and acoustics: Assessing macrobenthic communities at a Science Diliman 19: 7–13. dredged material disposal site off the North East coast of Cabral HN and Murta AG. (2004). Effect of sampling design the UK. Journal of Marine Systems 62: 204–216. on abundance estimates of benthic invertebrates in Breen J, Hanna J and Harrison T. (2006). A survey of environmental monitoring studies. Marine Ecology Progress the marine environment of Rathlin Island. Environment Series 276: 19–24. and Heritage Service Report. Belfast: Environment and Carballo JL, Vega C, Cruz-Barraza JA, Yanez B, Nava H, Heritage Service, 82pp. Avila E and Wilson M. (2008). Short- and long-term Brock JC, Wright CW, Kuffner IB, Hernandez R and patterns of sponge diversity on a rocky tropical coast: Thompson P. (2006). Airborne lidar sensing of massive evidence of large-scale structuring factors. Marine Ecology: stony coral colonies on patch reefs in the northern An Evolutionary Perspective 29(2): 216–236. Florida reef tract. Remote Sensing of Environment 104: Chainho P, Costa JL, Chaves ML, Lane MF, Dauer DM and 31–42. Costa MJ. (2006). Seasonal and spatial patterns of Brown CJ, Hewer AJ, Meadows WJ, Limpenny DS, distribution of subtidal benthic invertebrate communities Cooper KM, Rees HL and Vivian CMG. (2001). in the Mondego River, Portugal – a poikilohaline estuary. Mapping gravel biotopes and an examination of the Hydrobiologia 555: 59–74. factors controlling the distribution, type and diversity Clark RA and Frid CLJ. (2001). Long-term changes in the of their biological communities. CEFAS Science Series North Sea ecosystem. Environmental Reviews 9: 131–187. Technical Report No. 114. Lowestoft, England: Centre Coggan R, Populus J, White J, Sheehan K, Fitzpatrick F and for Environment, Fisheries and Aquaculture Science, Piel S. (2007). Review of Standards and Protocols for Seabed 43pp. Habitat Mapping. Peterborough, UK: Mapping European Brown CJ, Cooper KM, Meadows WJ, Limpenny DS and Seabed Habitats (MESH), 210pp. Rees HL. (2002). Small-scale mapping of sea-bed assem- Collier JS and Brown CJ. (2005). Correlation of sidescan blages in the eastern English Channel using sidescan backscatter with grain size distribution of surficial seabed sonar and remote sampling techniques. Estuarine Coastal sediments. Marine Geology 214: 431–449. and Shelf Science 54(3): 263–278. Collier JS and Humber SR. (2007). Time-lapse side-scan Brown CJ, Hewer AJ, Meadows WJ, Limpenny DS, sonar imaging of bleached coral reefs: A case study Cooper KM and Rees HL. (2004a). Mapping seabed from the Seychelles. Remote Sensing of Environment 108: biotopes at Hastings Shingle Bank, Eastern English 339–356. Channel. Part 1. Assessment using sidescan sonar. Journal Davies J, Baxter J, Bradley M, Connor D, Khan J, Murray E, of the Marine Biological Association of the UK 84: 481–488. Sanderson W, Turnbull C and Vincent M. (2001). Marine

110 Vol 28, No 3, 2009

Monitoring Handbook. Peterborough, UK: Joint Nature Gracias N and Santos-Victor J. (2000). Underwater video Conservation Committee, 405pp. Available at http:// mosaics as visual navigation maps. Computer Vision and www.jncc.gov.uk/page-2430, accessed on 5 May 2009. Image Understanding 79: 66–91. Degraer S, Moerkerke G, Rabaut M, Van Hoey G, Du Greenstreet SPR, Tuck ID, Grewar GN, Armstrong E, Four I, Vincx M, Henriet J and Van Lancker V. (2008). Reid DG and Wright PJ. (1997). An assessment of Very-high resolution side-scan sonar mapping of biogenic the acoustic survey technique, RoxAnn, as a means of reefs of the tube-worm Lanice conchilega. Remote Sensing of mapping seabed habitat. ICES Journal of Marine Science Environment 112: 3323–3328. 54(5): 939–959. Diesing M, Kubicki A, Winter C and Schwarzer K. (2006). Grove RS, Zabloudil K, Norall T and Deysher L. (2002). Decadal scale stability of sorted bedforms, German Bight, Effects of El Nino events on natural kelp beds and southeastern North Sea. Continental Shelf Research 26(8): artificial reefs in southern California. ICES Journal of 902–916. Marine Science 59(suppl): S330–S337. Duckworth AR and Battershill CN. (2001). Population Hewitt JE, Thrush SF, Cummings VJ and Turner SJ. (1998). dynamics and chemical ecology of New Zealand The effect of changing sampling scales on our ability to Demospongiae Latrunculia sp. nov. and Polymastia detect effects of large-scale processes on communities. croceus (Poecilosclerida: Latrunculiidae: Polymastiidae). New Journal of Experimental Marine Biology and Ecology 227(2): Zealand Journal of Marine and Freshwater Research 35(5): 251–264. 935–949. Hewitt JE and Thrush SF. (2007). Effective long-term Du Four I and Van Lancker V. (2008). Changes of ecological monitoring using spatially and temporally sedimentological patterns and morphological features nested sampling. Environmental Monitoring and Assessment due to the disposal of dredge spoil and the regeneration 133: 295–307. after cessation of the disposal activities. Marine Geology Hill J and Wilkinson C. (2004). Methods for ecological 255: 15–29. monitoring of coral reefs. Townsville, AU: Australian Institute Ehrhold A, Hamon D and Guillaumont B. (2006). The of Marine Science, 117pp. REBENT monitoring network, a spatially integrated, Houk P and Van Woesik R. (2006). Coral Reef Benthic acoustic approach to surveying nearshore macrobenthic Video Surveys Facilitate Long-Term Monitoring in habitats: application to the Bay of Concarneau (South the Commonwealth of the Northern Mariana Islands: Brittany, France). ICES Journal of Marine Science 63(9): Toward an Optimal Sampling Strategy. Pacific Science 1604–1615. 60(2): 177–189. Eleftheriou AT and McIntyre A (eds.). (2005). Methods for Hovland M, Vasshus S, Indreeide A, Austdal L and Nilsen O. the study of marine benthos, 3rd edition. Oxford: Blackwell (2002). Mapping and imaging deep-sea coral reefs off Publishing, 418pp. Norway, 1982–2000. Hydrobiologia 471: 13–17. Elías R, Palacios JR, Rivero MS and Vallarino EA. (2005). Hutin E, Simard Y and Archambault P. (2005). Acoustic de- Short-term responses to sewage discharge and storms of tection of a scallop bed from a single-beam echosounder subtidal sand-bottom macrozoobenthic assemblages off in the St. Lawrence. ICES Journal of Marine Science 62(5): Mar del Plata City, Argentina (SW Atlantic). Journal of Sea 966–983. Research 53(4): 231– 242. Intelmann SS. (2006). Comments on hydrographic and to- European Union. (2000). Water Framework Directive. pographic LIDAR acquisition and merging with multibeam WFD 2000/60/EC. Available at http://www.euwfd.com, sounding data acquired in the Olympic Coast National Ma- accessed on 9 March 2009. rine Sanctuary. Marine Sanctuaries Conservation Series: European Union Habitats Directive. (1992). Council Direc- ONMS-06-05. Silver Spring, MD: US Dept. of Commerce, tive 92/43/EEC on the conservation of natural habitats National Oceanic and Atmospheric Administration, Na- and of wild fauna and flora. tional Ocean Service, Office of Ocean and Coastal Fossa JH, Mortensen PB and Furevik DM. (2002). The Resource Management, National Marine Sanctuary Pro- deep-water coral Lophelia pertusa in Norwegian waters: gram USA, 19pp. distribution and fishery impacts. Hydrobiologia 471: 1–12. Jerosch K, Luedtke A, Schlueter M and Ioannidis GT. Gagnon P, Scheibling RE, Jones W and Tully D. (2008). (2007). Automatic content-based analysis of georefer- The role of digital bathymetry in mapping shallow marine enced image data: Detection of Beggiatoa mats in seafloor vegetation from hyperspectral image data. International video mosaics from the Håkon Mosby Mud Volcano. Journal of Remote Sensing 29(3): 879–904. Computers and Geosciences 33(2): 202–218. Gesch D and Wilson R. (2002). Development of a seamless Jokiel PL, Rodgers KS, Brown EK, Kenyon JC, Aeby G, multisource topographic/bathymetric elevation model of Smith WR and Farell F. (2005). Comparison of Methods Tampa Bay. Marine Technology Society Journal 35(4): 58–64. Used to Estimate Coral Cover in the Hawaiian Islands. Gilkinson KD, Fader GBJ, Gordon DC, Charron R, NOAA/NOS NWHI Coral Reef Ecosystem Reserve McKeown D, Roddick D, Kenchington ELR, MacIsaac K, Report. Honolulu: NOAA/NOS NWHI Coral Reef Bourbonnais C, Vass P and Liu Q. (2003). Immediate Ecosystem Reserve, 22pp. and longer-term impacts of hydraulic clam dredging on Jones LA, Hiscock K and Connor DW. (2000). Marine an offshore sandy seabed: effects on physical habitat habitat reviews. A summary of ecological requirements and processes of recovery. Continental Shelf Research 23: and sensitivity characteristics for the conservation and 1315–1336. management of marine SACs. Joint Nature Conservation Goldsmith FB. (ed.). (1991). Monitoring for conservation and Committee Report. Peterborough, UK: JNCC, 178pp. ecology. Conservation Biology Series. London: Chapman Karpouzli E and Malthus T. (2003). The empirical line and Hall, 275pp. method for the atmospheric correction of IKONOS Gracias N and Santos-Victor J. (1998). Automatic mosaic imagery. International Journal of Remote Sensing 24(5): creation of the ocean floor. In: Proceedings IEEE 1143–1150. Oceans ’98, 28 September–1 October, Nice, France, Kenny AJ, Cato I, Desprez M, Fader G, Vol. 1, 257–262. Schuttenhelm RTE and Side J. (2003). An overview

111 Van Rein et al. A review of sublittoral monitoring methods in temperate waters: a focus on scale

of seabed-mapping technologies in the context of Martin CJM and Martin EA. (2002). An underwater pho- marine habitat classification. ICES Journal of Marine tomosaic technique using Adobe PhotoshopTM. Interna- Science 60(2): 411–418. tional Journal of Nautical Archaeology 31(1): 137–147. Kingsford M and Battershill C. (eds.). (1998). Studying McDowell JL, Knight J and Quinn R. (2007). Mesoscale Temperate Marine Environments: A Handbook for Ecologists. changes in present-day nearshore surface sediments and Christchurch, NZ: Canterbury University Press, 335pp. bedform dynamics off the north coast of Ireland. In: Kostylev VE, Courtney RC, Robert G and Todd BJ. (2003). Balson PS and Collins MB (eds.). Coastal shelf and trans- Stock evaluation of giant scallop (Placopecten magellanicus) port. Geological Society of London, Special Publication using high-resolution acoustics for seabed mapping. 274. London: The Geological Society, 103–116. Fisheries Research 60: 479–492. McGonigle C, Brown C, Quinn R and Grabowski J. (2009). Kutser T, Vahtmae E and Martin G. (2006). Assessing Evaluation of image-based multibeam sonar backscatter suitability of multispectral satellites for mapping benthic classification for benthic habitat discrimination and macroalgal cover in turbid coastal waters by means of mapping at Stanton Banks, UK. Estuarine Coastal and Shelf model simulations. Estuarine Coastal and Shelf Science Science 81(3): 423–437. 67(3): 521–529. Mistri M. (2002). Persistence of benthic communities: a case Lam K, Shin PKS, Bradbeer R, Ku K, Hodgson P and study from the Valli di Comacchio, a northern Adriatic Cheung SG. (2007). Baseline data of subtropical coral lagoonal ecosystem (Italy). ICES Journal of Marine Science communities in Hoi Ha Wan Marine Park, Hong Kong, 59: 314–322. obtained by an underwater remote operated vehicle Moore CG, Saunders G, Mair JM and Lyndon AR. (2006). (ROV). Marine Pollution Bulletin 54: 107–112. The inauguration of site condition monitoring of marine Lathrop RG, Cole M, Senyk N and Butman B. (2006). features of Loch Maddy Special Area of Conservation. Seafloor habitat mapping of the New York Bight Scottish Natural Heritage Report 152 (ROAME No. incorporating sidescan sonar data. Estuarine Coastal and F02AA409). Edinburgh: Scottish Natural Heritage, 55pp. Shelf Science 68: 221–230. Moore JJ and Gilliland P. (1999). Development of a Leonard GH and Clark RP. (1993). Point quadrat versus monitoring programme and methods in Plymouth video transect estimates of the cover of benthic red algae. Sound cSAC: Application of diver techniques and ROV Marine Ecology Progress Series 101: 203–208. techniques. Unpublished report by Cordah Limited to Leriche A, Pasqualini V, Boudouresque CF, Bernard G, English Nature, 79pp. Morello EB, Froglia C and Atkinson RJA. (2007). Under- Bonhomme P, Clabaut P and Denis J. (2006). Spatial, water television as a fishery-independent method for temporal and structural variations of a Posidonia oceanica stock assessment of Norway lobster (Nephrops norvegicus) seagrass meadow facing human activities. Aquatic Botany in the central Adriatic sea (Italy). ICES Journal of Marine 84(4): 287–293. Science 64: 1116–1123. Leujak W and Ormond RFG. (2007). Comparative accuracy Mumby PJ and Edwards AJ. (2002). Mapping marine and efficiency of six coral community survey methods. environments with IKONOS imagery: enhanced spatial Journal of Experimental Marine Biology and Ecology 351: resolution can deliver greater thematic accuracy. Remote 168–187. Sensing of Environment 82: 248–257. Lindenbaum C, Bennell JD, Rees ELS, Mcclean D, Cook W, National Marine Monitoring Programme (NMMP). (2003). Wheeler AJ and Sanderson WG. (2008). Small-scale Green Book v12. Available at http://www.monae.org/ variation within a Modiolus modiolus (Mollusca: Bivalvia) documents/UK%20monitoring%20GBMain%20Text% reef in the Irish Sea: I. Seabed mapping and reef 201103.pdf, accessed on 8 May 2009. morphology. Journal of the Marine Biological Association of Nilsson HC and Rosenberg R. (1997). Benthic habitat the UK 88(1): 133–141. quality assessment of an oxygen stressed fjord by surface Lirman D, Gracias NR, Gintert BE, Gleason ACR, Reid RP, and sediment profile images. Journal of Marine Systems 11: Negahdaripour S and Kramer P. (2007). Development 249–264. and application of a video-mosaic survey technology Nybakken JW. (ed.). (1997). Marine Biology: An Ecological to document the status of coral reef communities. Approach. Reading, PA: Addison-Wesley Educational Environmental Monitoring and Assessment 125: 59–73. Publishers, 481pp. Lirman D, Deangelo G, Serafy JE, Hazra A, Hazra DS and O’Connor B. (2001). Procedural guideline no. 2.2 – Brown A. (2008). Geospatial video monitoring of sediment profile imagery. In: Davies J, Baxter J, Bradley nearshore benthic habitats of western Biscayne Bay M, Connor D, Khan J, Murray E, Sanderson W, (Florida) using the shallow-water positioning system Turnbull C and Vincent M. (eds.). Marine Monitoring (SWaPS). Journal of Coastal Research 24(1): 135–145. Handbook. Peterborough, UK: Joint Nature Conservation Lu L and Wu RSS. (2007). Seasonal effects on recolonization Committee, 211–215. Available at http://www.jncc.gov. of macrobenthos in defaunated sediment: a series of field uk/page-2430, accessed on 5 May 2009. experiments. Journal of Experimental Marine Biology and Olenin S and Ducrotoy JP. (2006). The concept of biotope in Ecology 351: 199–210. marine ecology and coastal management. Marine Pollution Lundalv T and Christie H. (1986). Comparative trends Bulletin 53: 20–29. and ecological patterns of rocky subtidal communities in Parsons DM, Shears NT, Babcock RC and Haggitt TR. the Swedish and Norwegian Skagerrak area. Hydrobiologia (2004). Fine-scale habitat change in a marine reserve, 142: 71–80. mapped using radio-acoustically positioned video tran- Lundalv T, Larsson CS and Axelsson L. (1986). Long-term sects. Marine and Freshwater Research 55: 257–265. trends in algal-dominated rocky subtidal communities Reid D. (2007). Accounting for spatial and temporal on the Swedish west coast – a transitional system? scales and interpolation in acoustic seabed classification Hydrobiologia 142: 81–95. surveys. In: Anderson JT, Holliday V, Kloser R, Reid D and Marcos SA, Soriano M and Saloma C. (2005). Classification Simard Y. (2007). Acoustic seabed classification of marine of coral reef images from underwater video using neural physical and biological landscapes. ICES Co-operative networks. Optical Express 13: 8766–8771. Research Report 286. Copenhagen: ICES, 73–93.

112 Vol 28, No 3, 2009

Roberts JM, Brown CJ, Long D and Bates CR. (2005). and process in marine benthic systems: a picture is worth Acoustic mapping using a multibeam echosounder a thousand worms. Journal of Experimental Marine Biology reveals cold-water coral reefs and surrounding habitats. and Ecology 285: 313–338. Coral Reefs 24: 654–669. Theriault C, Scheibling R, Hatcher B and Jones W. (2006). Rzhanov Y and Mayer L. (2004). Deep-sea image processing. Mapping the distribution of an invasive marine alga In: Oceans ’04 MTS/IEEE Techno-Ocean ’04, Vols. 1–2, (Codium fragile s tomentosoides) in optically shallow coastal 647–652. waters using the compact airborne spectrographic imager Rzhanov Y, Mayer L, Beaulieu S, Shank T, Soule SA and (CASI). Canadian Journal of Remote Sensing 32: 315–329. Fornari DJ. (2006). Deep-sea Geo-referenced Video Tunberg BG and Nelson WG. (1998). Do climatic os- Mosaics. In: Proceedings, IEEE Oceans ’06, 18–21 cillations influence cyclical patterns of soft bottom September, Boston, MA, 1–6. macrobenthic communities on the Swedish west coast? Sager WW, MacDonald IR and Hou RS. (2003). Geophysical Marine Ecology Progress Series 170: 85–94. signatures of mud mounds at hydrocarbon seeps on the Van der Meer J. (1997). Sampling design of monitoring Louisiana continental slope, northern Gulf of Mexico. programmes for marine benthos: a comparison between Marine Geology 198: 97–132. the use of fixed versus randomly selected stations. Journal Sanderson WG, Holt RHF, Kay L, Ramsay K, Perrins J, of Sea Research 37: 167–179. Mcmath AJ and Rees EIS. (2008). Small-scale variation Vincent AG, Pessel N, Borgetto M, Jouffroy J, within a Modiolus modiolus (Mollusca: Bivalvia) reef in the Opderbecke J and Rigaud V. (2003). Real-time Irish Sea. II. Epifauna recorded by divers and cameras. geo-referenced video mosaicking with the MATISSE Journal of the Marine Biological Association of the UK 88: system. In: Proceedings, IEEE Oceans ’03, 22–26 143–149. September, San Diego, CA, Vol. 4, 2319–2324. Sayer MDJ and Poonian C. (2007). The influences of Viscido SV, Stearns DE and Able KW. (1997). Seasonal census technique on estimating indices of macrofaunal and spatial patterns of an epibenthic decapod crustacean population density in the temperate rocky subtidal zone. assemblage in north-west Atlantic continental shelf Underwater Technology 27(3): 119–139. waters. Estuarine Coastal and Shelf Science 45(3): 377–392. Shears NT. (2007a). Biogeography, community structure Walker BK, Riegl B and Dodge RE. (2008). Mapping coral and biological habitat types of subtidal reefs on the reef habitats in southeast Florida using a combined South Island West Coast, New Zealand. Science for technique approach. Journal of Coastal Research 24(5): Conservation Report 281. Wellington, NZ: Department of 1138–1150. Conservation, Northland Conservancy, 53pp. Wedding LM, Friedlander AM, McGranaghan M, Shears NT. (2007b). Shallow subtidal reef communities Yost RS and Monaco ME. (2008). Using bathymetric at the Poor Knights Islands Marine Reserve after eight lidar to define nearshore benthic habitat complexity: years of no-take protection. Department of Conservation, implications for management of reef fish assemblages in Northland Conservancy Report. Wellington, NZ: Depart- Hawaii. Remote Sensing of Environment 112(11): 4159–4165. ment of Conservation, Northland Conservancy, 48pp. Weiers S, Bock M, Wissen M and Rossner G. (2004). Shucksmith R, Hinz H, Bergmann M and Kaiser MJ. (2006). Mapping and indicator approaches for the assessment of Evaluation of habitat use by adult plaice (Pleuronectes habitats at different scales using remote sensing and GIS platessa L.) using underwater video survey techniques. methods. Landscape and Urban Planning 67: 43–65. Journal of Sea Research 56: 317–328. Whittington MW, Holt R, Irving R, Northen K and Stanwell- Simard Y and Stepnowski A. (2007). Classification methods Smith D. (2006). Across-Wales Diving Monitoring Project and criteria. In: Anderson JT, Holliday V, Kloser R, Reid Volume 2: Standard Operating Procedures. Countryside D and Simard Y. (2007). Acoustic seabed classification Council for Wales Report 25b. Bangor, Wales: Country- of marine physical and biological landscapes. ICES side Council for Wales, 76pp. Co-operative Research Report 286. Copenhagen: ICES, Wildish DJ, Fader GBJ, Lawton P and MacDonald AJ. (1998). 61–72. The acoustic detection and characteristics of sublittoral Smith CJ and Papadopoulou KN. (2003). Burrow density bivalve reefs in the Bay of Fundy. Continental Shelf Research and stock size fluctuations of Nephrops norvegicus in a 18(1): 105–113. semi-enclosed bay. ICES Journal of Marine Science 60(4): Wood R. (1999). Reef evolution. New York: Oxford University 798–805. Press, 432pp. Smith CJ, Marrs SJ, Atkinson RJA, Papadopoulou KN and Zajac RN. (2008). Macrobenthic biodiversity and sea floor Hills JM. (2003). Underwater television for fisheries- landscape structure. Journal of Experimental Marine Biology independent stock assessment of Nephrops norvegicus from and Ecology 366: 198–203. the Aegean (eastern Mediterranean) Sea. Marine Ecology Zharikov Y, Skilleter GA, Loneragan NR, Taranto T and Progress Series 256: 161–170. Cameron BE. (2005). Mapping and characterising sub- Smolic A and Wiegand T. (2001). High-resolution video tropical estuarine landscapes using aerial photography mosaicing. IEEE International Conference on Image and GIS for potential application in wildlife conser- Processing, 7–10 October, Thessaloniki, Greece, Vol. 3, vation and management. Biological Conservation 125(1): 872–875. 87–100. Solan M, Germano JD, Rhoads DC, Smith C, Michaud E, Zhu ZG, Riseman EM, Hanson AR and Schultz H. Parry D, Wenzhofer F, Kennedy B, Henriques C, Battle E, (2005). An efficient method for geo-referenced video Carey D, Iocco L, Valente R, Watson J and Rosenberg R. mosaicing for environmental monitoring. Machine Vision (2003). Towards a greater understanding of pattern, scale and Applications 16(4): 203–216.

113