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Camera technology for monitoring marine biodiversity and human impact Anthony WJ Bicknell1,2*, Brendan J Godley1,2, Emma V Sheehan3, Stephen C Votier2, and Matthew J Witt2 Human activities have fundamentally altered the marine environment, creating a need for effective management in one of Earth’s most challenging habitats. Remote camera imagery has emerged as an essential tool for monitoring at all scales, from individuals to populations and communities up to entire marine ecosystems. Here we review the use of remote cameras to monitor the marine environment in relation to human activity, and consider emerging and potential future applications. Rapid technological advances in equipment and analytical tools influence where, why, and how remote camera imagery can be applied. We encourage the inclusion of cameras within multi-method and multi-sensor approaches to improve our understanding of ecosystems and help manage human activities and minimize impacts. Front Ecol Environ 2016; 14(8): 424–432, doi: 10.1002/fee.1322

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rom the early days of televised programs devoted to marine natural history that informed the public about previously unrecognized species and unexplored habitats, video has sparked the human imagination. Cameras continue to play an important role in marine exploration and more recently have been used in environmental assessment (Figure 1; Bailey et al. 2007). Initially, camera equipment was complex, cumbersome, and expensive, but advances in the past two decades – including improvements in underwater housings, image quality, battery longevity, reduced cost, and data storage (Figure 1) – have driven a technological revolution. The potential for cameras to deliver highly repeatable sampling over broad temporal (hours to years) and spatial (meters to kilometers) scales means they are now regularly employed in applied and theoretical research, to study behavior, species interactions, ecosystem function, and resilience (detailed in WebTable 1; see also

In a nutshell: • Earth’s oceans are being transformed by the impacts of anthropogenic activities, which can be difficult to monitor effectively in the field • Camera imagery has become an important tool in understanding these impacts on individual animals, populations, and ecosystems • Technological advances in equipment and deployment methods are stimulating novel applications and wider use of cameras for impact assessment • As part of a multi-faceted monitoring approach, remote cameras can help to improve our understanding of anthropogenic impacts in marine ecosystems and the management of marine resources

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Centre for Ecology and Conservation, University of Exeter, Penryn, UK *([email protected]); 2Environment and Sustainability Institute, University of Exeter, Penryn, UK; 3Marine Institute, Plymouth University, Plymouth, UK www.frontiersinecology.org

Mallet and Pelletier 2014). Moreover, their relative ease of use and ever-decreasing cost have allowed a broader range of practitioners (eg government agencies, non-governmental organizations [NGOs], environmental consultants, universities) to utilize cameras for marine research. Here we assess the implementation of cameras for examining human influence on marine ecosystems and species – research that likely represents a catalyst for driving future innovation in technology, methods, and analytical techniques. We review how camera imagery can be applied to monitor ecosystems and populations, and examine individual responses to human activities. Key challenges to the successful use of videography are considered. Finally, we discuss potential future developments in the application of cameras and how multi- method and multi- sensor approaches will be vital in evaluating human impacts on marine ecosystems. JJ Ecosystem-and

population-level monitoring

Monitoring change in marine ecosystems is challenging. Water depth, pressure, and scale – at magnitudes typically not associated with other systems – restrict access to locations or sampling sites and increase instrumentation costs. Remote camera technologies are helping to overcome some of these issues and provide non-destructive methods for monitoring the effects and impact of human activities on habitats and species. These methods either complement or replace traditional sampling techniques used in the marine realm (eg benthic grabs, fishing trawls, box corers, diver surveys), many of which can be destructive or disturbing to marine life, unsuitable in certain habitats or locations, spatially restrictive, and/or prohibitively costly. Marine area protection and management of extractive activities are crucial to achieve healthy ecosystems and populations, and are enhanced by the use of camera technologies. © The Ecological Society of America

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Camera technology in marine monitoring

Marine habitats and protected areas

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During the past half century, human impacts such as those related to overharvesting, pollution, and climate change have contributed to the global decline in areal coverage of tropical coral reefs (Bellwood et al. 2004). Consequently, research on reef mitigation and restoration has flourished, with underwater imagery as an important component. For example, by providing quantitative data on consumption rates of teleost fish on algae in coral reef systems (Vergés et al. 2012), in situ remote underwater cameras have demonstrated that reef resilience and recovery are dependent on herbivores, the populations of which can be directly affected by overfishing and climate change (Hughes et al. Figure 1. Timeline of important events in the development of camera imagery and its use 2007). Cameras have provided long- in studying and monitoring marine biodiversity (for full reference list, see WebPanel 1). term observational data in marine protected areas (MPAs) across habitats and depths to such as the deepwater coral Lophelia pertusa, as well as the detail reef change or recovery (eg McLean et al. 2010; ecological consequences (eg reduction in s pecies diversity, Stevens et al. 2014; Bouchet and Meeuwig 2015). These function, resilience) resulting from this damage (Fosså et al. approaches have contributed to an understanding of 2002). Establishing deepwater MPA networks to conserve both direct (eg target population) and indirect (eg these habitats and s pecies has now become a priority, leadtrophic cascades) effects of global change, as well as ing to further applications of camera systems (eg towed the timescales of these effects (Babcock et al. 2010). drop cameras) to capture imagery of deepwater epibenthic Static mounted cameras baited with dead fish, for assemblages, thereby assisting with habitat mapping and example, have revealed positive effects – related to site designation (Howell et al. 2010). abundance (Denny et al. 2004), density (Smith et al. 2014), size structure (Watson et al. 2009), and assem- Fish stocks and management blage structure (Malcolm et al. 2007) – of no- take reserves on target fish species in temperate and tropical Poorly managed capture fisheries – characterized by unsustainable stock depletion (Myers and Worm 2003), regions. Epibenthic communities and benthic habitats can be incidental mortality of non-target species (Lewison et al. assessed by non-destructive towed camera systems, which 2004), provision of unnatural food subsidies (Bicknell collect quantitative data over relatively large areas in a et al. 2013), and destruction of seabed habitat (Watling cost-effective manner (Sheehan et al. 2010). During a sur- and Norse 1998) – represent one of the most critical vey of an MPA, underwater video observations captured by threats to marine ecosystems. Nonetheless, fisheries are a benthic towed video camera provided the necessary a major source of livelihood and food for millions of replication and scale (spatial and temporal) to reveal that people worldwide and are therefore important in mainthe functional extent of the reef habitat (feature) under taining global food security (Smith et al. 2010). To achieve protection was larger than thought, raising important ques- sustainable fish stocks, resource managers need to consider tions on the reliability of feature-based protection for sites multiple biotic, abiotic, and socioeconomic components based fisheries management (EBFM) within a seafloor habitat mosaic (Sheehan et al. 2013a). under ecosystem- Similarly, deepwater benthic habitats are being assessed (Pikitch et al. 2004). To realize the healthy and productive and monitored by camera systems, partly in response to the marine ecosystems that are necessary to support sustainable recent growth in bottom trawl fisheries (Norse et al. 2012) fisheries, we argue that the cumulative impacts of fishing and the potential for extraction of deep-sea mineral depos- must be evaluated and managed, which can be supported its (Hoagland et al. 2010). Cameras on remotely operated through the deployment of camera technology. A combination of onboard video observations and vehicles (ROVs) have revealed the destructive effect of deep-sea fisheries on important habitat-building species, in-trawl video systems can improve bycatch estimates © The Ecological Society of America

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(Jaiteh et al. 2014), thereby providing crucial information toward effective management, although this is complicated in part by unseen underwater gear-related injury and death to fish. Trawl fisheries in particular also discard large quantities of undesirable (or unlandable) catch, which not only has direct negative consequences for target and non-target stocks but may also have ecosystem- level effects (Bicknell et al. 2013). Discards are now being strictly managed by authorities in the US (www.nmfs. noaa.gov/by_catch/index.htm) and Europe (http://ec. europa.eu/fisheries/reform/index_en.htm), necessitating the monitoring of fishing activity to ensure compliance. Recently, video-based electronic surveillance has been piloted and implemented for compliance purposes in fisheries in the US, New Zealand, Australia, and Europe (eg McElderry 2008), in place of more traditional onboard observer programs. Installation of a remote-sensing system – including closed- circuit cameras, a Global Positioning System (GPS) receiver, and sensors – on fishing vessels can effectively monitor catch and discards, providing a permanent data record (an improvement as compared with traditional logbooks) and allowing the industry to engage in self- reporting. The latter is of increasing importance if fisheries want to be certified as sustainable by eco-labelling organizations (eg the Marine Stewardship Council; www.msc.org/about-us/standards), where responsible management and minimization of negative environmental impact are part of the certification criteria. In the Greenland shrimp fishery, drop cameras are being deployed to assess gear-related impacts on benthic habitats and communities, potentially encouraging the fishery to consider more sustainable extraction methods and to minimize habitat degradation (Kemp and Yesson 2013). Independent of fisheries certification, imagery in coastal waters around the Isle of Man (UK) have increased our understanding of potential recovery rates and the resilience of epibenthic communities to towed bottom-trawl fishing gear; there, estimated recovery rates (12 years) and identification of potential recovery drivers provide further insight into how destructive fishing methods might be better managed (Lambert et al. 2014). Because fish behavior can introduce uncertainty or bias in catch estimates derived from fishery-independent surveys, photographic evidence obtained from cameras may help to improve the accuracy of stock assessments by providing behavioral information on fish in the vicinity of gear. For instance, cameras attached to a trawl net in the Northeast Pacific revealed flatfish herding behavior associated with this gear type, which, if not considered during stock assessments, would lead to overestimation of stock biomass (Bryan et al. 2014). When affixed to the entrance of nets, camera systems also offer the potential to gather in-trawl information on target and non-target species during surveys, allowing for a more detailed description of the catch, species distribution in the water column, and method efficiency (Rosen and Holst 2013). www.frontiersinecology.org

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The impact of trawl methods on non-target fishery stocks is another consideration, with implications for management. In Newfoundland and Labrador, Canada, Nguyen et al. (2014) relied on net cameras to reveal the behavioral responses of commercially important snow crabs (Chionoecetes opilio) when encountering shrimp trawl fishing gear; this evidence helps to explain how the gear could be modified to mitigate future impacts. Renewable and extractive energy industries

As fossil-fuel reserves decline and the need to reduce global atmospheric emissions of carbon dioxide intensifies, the marine renewable energy (MRE) industry is likely to become more important in meeting future global energy demands. Tidal, wave, and wind energy project sites in marine habitats will be associated with increased at- sea activities (eg shipping, construction) and the introduction of man-made structures into the marine environment (eg monopiles, cables, turbines, lagoon walls). Cameras can provide long-term baseline and impact- related data for development sites and energy converters (Broadhurst and Orme 2014). As part of ongoing monitoring of a MRE test facility site off the north Cornwall coast in the UK, benthic towed (Figure 2) and static (Figure 3) remote underwater imagery systems have been used to assess epibenthic communities and habitats. The differences in benthic assemblage composition and an increase in cuckoo wrasse (Labrus mixtus) abundance observed around the seabed cable’s protective rock armoring (Sheehan et al. 2013b) revealed how structures act as artificial reefs or fish aggregation devices (FADs; Langhamer 2012), with potential positive effects for local fisheries. Cameras mounted below or above the water can also monitor the effect of operational energy convertors on fish, mammal, and bird behavior (eg Broadhurst et al. 2014). In contrast to the MRE industry, extractive natural resource industries have a long and complicated history with video imagery systems. Although initially developed in association with first-generation ROVs for the offshore petroleum sector, these systems are now employed to not only discover new seabed areas suitable for underwater mining (Birney et al. 2006) but also to help understand and/or predict the impact of extracting natural resources from the marine environment (Jones et al. 2007). Such activities are coming under closer scrutiny over their direct and indirect environmental impacts (Ramirez- Llodra et al. 2011), which has led to the development of long-term, multi-sensor, observatory systems (including imagery capture systems) to assess the effect on deepwater ecosystems (Vardaro et al. 2013). JJ Individual-level

monitoring

Animal- borne remote sensors have revolutionized the study of free-living, mobile species, providing insights © The Ecological Society of America

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into their physiology and behavior (Moll et al. 2007). For mobile and/or elusive marine species, they are the only available method to collect reliable data on individual movement and foraging, in addition to their encountered environment (Ropert-Coudert and Wilson 2005). Studying animal behavior in submarine systems poses unique challenges (eg high pressure and low light environments), which drove much of the early innovation in animal-borne equipment. The combined size and weight of cameras, batteries, and data storage capacity initially limited applications, but these technological barriers are being overcome. The first- described animal- borne video camera was attached to loggerhead (Caretta caretta) and leatherback (Dermochelys coriacea) sea turtles (early National Geographic CRITTERCAM; Marshall 1990). Field applications soon extended to a wide range of marine vertebrates and invertebrates, not only to study foraging behavior, social interactions, and habitat preference, but also to gather empirical data to test the validity of activities and behavior that have previously been indirectly inferred from tracking or accelerometry data (WebTable 2). Foraging behavior and habitat use

Animal-borne cameras can be combined with movement sensors (eg GPS receivers, time depth recorders, accelerometers) to gain novel perspectives on behavior and habitat use (reviewed in Moll et al. 2007). For example, imagery combined with time depth recorders and satellite tags revealed previously unknown omnivory in green sea turtles (Chelonia mydas) (reviewed in Hochscheid 2014), which has led to the identification of new foraging habitats and consequently a change in the approach to conservation of key areas. Moreover, images and GPS data from bird-borne devices revealed that while northern gannets (Morus bassanus) followed fishing vessels more than was previous thought (Figure 4), they also switched between scavenging and natural foraging (Votier et al. 2013). These findings are important as they provide a more thorough understanding of the way in which birds exploit fisheries discards, which may change in the face of global fisheries management reform (Bicknell et al. 2013). Inter-and intra-specific interactions

Individual interactions with man-made objects or with human activities in the marine environment (eg fishing boats/gear, renewable energy converters, oil rigs) are currently inferred through observations (eg bycatch rates, boat-based surveys) or tracking devices. Gathering evidence of how different individuals, sexes, and age classes respond during these encounters may help improve predictions of where, when, and how impacts will manifest in populations. It is logistically difficult, © The Ecological Society of America


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Figure 2. (a–c) Still frame grabs from benthic towed video imagery systems at a marine renewable energy test facility site in north Cornwall, UK. (a) Two red gurnard and a lesser octopus, (b) Ross coral, and (c) a high resolution frame grab to enable identification of smaller organisms.

for example, to monitor seabird mortality from collisions with offshore wind turbines, and birdstrike vulnerability has been assessed or modeled mainly through known flight heights (Cleasby et al. 2015). Capturing imagery to quantify intraspecific (eg individual, sex, age) and interspecific variation in behavior during encounters with wind turbines (eg avoidance, reduction of flight height, use for resting or foraging) would greatly improve not only predictions regarding species’ collision risks and potential population- level impacts but also evaluation of future turbine sites and mitigation efforts. A similar rationale could be applied to monitoring bycatch in fishing gear (eg sea turtles in gillnets), since little is currently known about entrapment rates in www.frontiersinecology.org


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applications and future developments

As technologies have become more sophisticated (eg inertial navigation systems, Fastloc™ GPS receivers, wireless network transmission) and as equipment costs have decreased, there are more opportunities to apply and expand the capacity of camera-based methods to ecological research. Aerial, surface, and sub-surface vehicles (b)

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Figure 3. (a–c) Still frame grabs from benthic baited (static) video imagery systems at a marine renewable energy test facility site in north Cornwall, UK. (a) Reef structure with encrusting organisms and sea urchin, (b) large- and small-spotted cat sharks, and (c) a European lobster.

relation to encounters. For instance, important turtle nesting beaches close to high- density gillnet fisheries could be targeted and pop- off cameras (that detach automatically after a set period) deployed on females (on the beaches) and males (caught offshore) to detail intra-and interspecific differences in behavior when encountering nets, and the ratio of encounters to entrapment. Technological advances are still required to enable extended periods of animal- borne video capture, but cameras have greatly improved our view of animal behavior and interactions with human activities. The integration of tracking technologies that allow remote downloading between individual animals (including proximity data), and to base stations, will provide further insights. www.frontiersinecology.org

Autonomous and unmanned vehicles are being used for remote sensing in both sea and air (Williams et al. 2012; Anderson and Gaston 2013). Miniaturized and lightweight cameras installed on unmanned aerial vehicles (UAVs) have been deployed to survey marine vertebrates on land (Pacific walrus [Odobenus rosmarus divergens]; Monson et al. 2013) and in water (dugongs [Dugong dugon]; Hodgson et al. 2013). Aerial imagery techniques have previously been utilized for population estimates (see Buckland et al. 2012), Environmental Impact Assessments (Thaxter and Burton 2009), and coastal habitat mapping (Lathrop et al. 2006), but the improved spatial and temporal resolution provided by UAVs offer many other applications in marine systems (Anderson and Gaston 2013). Autonomous underwater vehicles (AUVs) and unmanned surface vehicles are not constrained by weather or sea state, and can gather high- resolution imagery and environmental data from previously inaccessible habitats (eg deep- sea benthos) (Singh et al. 2004). By affixing cameras to AUVs to monitor the health of benthic habitats and communities, Smale et al. (2012) captured information directly relevant to EBFM. A more recent technique to control the invasive crown-of-thorns sea star (Acanthaster planci) in reef systems uses AUVs to visually identify individuals and subsequently administer a lethal injection of bile salts (Dayoub et al. 2015). Despite their high purchase costs (circa £30k–300k, €37k–370k, $50k–500k), AUVs offer great potential for combining multiple sensors, data streams (eg hydrography and environmental monitoring), and physical equipment. Underwater camera-traps

For decades, camera-traps (ie remotely triggered cameras that automatically take images of subjects passing in front of them) have been successfully deployed in terrestrial systems to measure abundance, species diversity, and behavior, as well as to observe rare species (see Burton et al. 2015), but only recently has the concept been developed for marine systems. Williams et al.’s (2014) TrigCam is a low-cost, low-power, motion-triggered underwater system that employs far red illumination and stereo images to reveal the number, size, position, and orientation of animals that activate the camera. By using novel hardware and open- source software, the authors © The Ecological Society of America

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have enabled further, independent system development by individuals or research groups to help expand its use in various marine environments. The rapid adoption of camera-traps within terrestrial research provided valuable new data and insightful images but also highlighted inherent challenges associated with many remote camera systems (eg imperfect detection, effective sampling area, multispecies inference; Burton et al. 2015). To enable robust ecological inquiry using camera systems, those who develop survey methods/designs need to explicitly focus on the ecological processes (eg abundance, movement) they intend to measure and the assumptions necessary to relate camera detections to those processes. Heeding the lessons learned from camera-trap usage in terrestrial systems will help facilitate a successful transition of this method to the marine environment.


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Accessibility and capacity

The production of quality, mass-produced, high-definition (HD) cameras (eg GoPro©) is changing how imagery can be applied to study marine biodiversity. Because of their greater affordability (circa £100–£400, €150–490, $250–660), reduced size, and improved underwater housing, cameras can now be deployed in places that were previously unfeasible and by a much wider group of investigators (eg students, NGOs, citizen scientists). Research and monitoring involving these types of cameras will undoubtedly increase, especially with innovations in extending battery longevity and expanding the storage capacity for captured images. Fisheries interactions (eg post-catch behavior on longlines, habitat impact of potting), effects of MRE devices (eg FAD effects, seabird feeding), and monitoring marinas or commercial ports for introduced species are examples where this equipment could provide invaluable data to help understand potential anthropogenic impacts. While logistically and scientifically challenging (Bonney et al. 2009), conducting relatively low-cost and long-term research incorporating networks of cameras with multiple stakeholders is a promising prospect in both marine and terrestrial systems (Dickinson et al. 2012; McShea et al. 2015). With suitable support, training and management of stakeholders/volunteers, and development of e- technologies to overcome data management and storage issues, these projects could substantially change how cameras are utilized in ecological monitoring (eg McShea et al. 2015; Wild.Id software, www.teamnetwork.org/solution). Automated classification, visual recognition, and image enhancement

Despite advances in imagery collection, the development of methods to extract biological or ecologically important information from photographs or video lags behind. The conversion of imagery into quantitative data can still be painstakingly slow, and streamlining and automating © The Ecological Society of America

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Figure 4. (a–c) Gannet-borne camera images of interactions with fishing vessels in the Celtic Sea.

the process remains a major challenge. To this end, motion detection software for video files has been written, which can identify moving objects and therefore help categorize useful and redundant sections of video for analysis (Weinstein 2015). Edgington et al. (2006) have also developed a visual recognition system to identify a suite of fish and echinoderms independently (without human observers), and Lukeman et al. (2010) used digitized images to study collective behavior in seaducks. www.frontiersinecology.org


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Panel 1. Limitations and challenges when using camera imagery in ecological monitoring Technology • Battery life for cameras and/or lights, as well as data storage, have advanced but are still major limitations to long-term m onitoring involving remote camera systems or animal-borne devices. • Size, mass, and hydrodynamic shape currently limit the use of animal-borne cameras to larger species. Device effects • Necessary attention/assessment is required to avoid device effects on individual animals that might harm them and/or alter their “natural” behavior. • Species or individuals may show avoidance behavior to underwater camera systems. Visibility • Reduced water clarity or reduced light can prevent species identification and abundance estimates, in some cases rendering underwater footage unusable. Attractants and olfactory plume • For baited camera systems, the type of bait and the range of the olfactory plume need to be considered.

Automated classification of benthic habitats is improving through advances in multispectral underwater image processing and segmentation algorithms, which have been employed to discriminate coral and algal cover in reef systems (Gleason et al. 2007), not possible with standard color imagery. This method (and others) will be further enhanced in many ecosystems by the inclusion of optical back-scatter filters to improve image clarity (Mortazavi et al. 2013). Such methods are unlikely to entirely exclude the need for human analysis, especially in low-contrast underwater environments, but it is hoped that the developing techniques will substantially decrease observer time in the future and therefore further propel the utility of videography. JJ Welfare

and environmental ethics

Widespread application of cameras to study marine ecosystems and/or organisms raises some ethical and legal questions. Animal welfare is a primary concern for animal-borne systems, and in many countries is currently regulated and managed by national agencies. Elsewhere, however, such regulations are limited or absent, and the increased accessibility of small, low-cost, HD cameras could lead to unnecessary and/or harmful applications. A potential but often overlooked issue with the use of any equipment in the marine environment is littering and pollution. Cumulatively, numerous sources of waste (eg shipping, discharges) have already contributed to extensive pollution in the oceans. Privacy issues for citizens are already a growing concern with respect to cameras in terrestrial systems (Butler and Meek 2013). Although unlikely to be problematic in underwater settings, such concerns may be valid to people in developed coastal areas. Proper understanding and consideration of www.frontiersinecology.org

• Species, individuals, sexes, and age classes may respond differently to attractants. • Species or individuals may become habituated to attractants. • Attractants may increase the chance of predation for target species. Video or stills analysis • Automation of video or photo analysis is challenging in marine systems, and human intervention will always be required, making it a time-consuming process. Experimental design and sampling • There may be imperfect detection of species and/or individuals by camera systems. • Reasonable levels of redundancy in the experimental design are required to account for device failure or unusable footage, particularly required in dynamic environments (eg temperate marine systems) • Typically, animal-borne camera studies have small sample sizes.

ethical and legal issues is needed before conducting research or regulatory agencies permitting activities. JJ Conclusions

By offering access to previously inaccessible marine habitats and novel perspectives on animal behavior, remote camera systems can help provide a better u nderstanding of how animals and habitats are affected by human activities. However, imagery has limita tions (Panel 1) and requires complementary sensor data and/or direct sampling to realize its full potential. For example, animal- borne images have limited value in the absence of other data such as location (eg latitude and longitude) and behavior (eg Votier et al. 2013). Similarly, although remote underwater images allow mobile species to be seen in context of habitats and sessile organisms, identifying small and cryptic species can be challenging and requires direct physical sampling. Accurately assessing marine ecosystem health requires information on both biotic and abiotic components, including animal behavior, species diversity, genetic structure, bathymetry, and water chemistry. It also relies on a detailed understanding of the underlying ecological perturbations, which may not be available for many aquatic systems (Friberg et al. 2011). A prerequisite to monitor change is the compilation of baseline data of these components, which requires a multi-method and sensor approach over relevant spatial and temporal scales. Robust experimental design, survey methods, and sampling are also essential for detecting changes caused by human activities. Through the use of cameras, passive and active a coustic systems, oceanographic sensors (eg those measuring temperature, salinity, fluorescence, and conductivity), tracking technology, next- generation genetic sequencing, © The Ecological Society of America

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remote sensing, and direct sampling, there is the potential to construct a comprehensive, multi-level depiction of a marine ecosystem. This is an imposing task, but monitoring aspects in isolation will not provide the details required to truly understand the component interactions and associations that can ultimately influence the health and productivity of a marine system, and the marked or subtle effects of human activities.

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