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Transcript
REVIEWS REVIEWS REVIEWS
424
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
F
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
1
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
AWJ Bicknell et al.
Camera technology in marine monitoring
Marine habitats and protected
areas
425
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
www.frontiersinecology.org
Camera technology in marine monitoring
426
(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 (<1 to >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
AWJ Bicknell et al.
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
AWJ Bicknell et al.
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
Camera technology in marine monitoring
427
(a)
(b)
(c)
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
Camera technology in marine monitoring
428
(a)
AWJ Bicknell et al.
JJ Emerging
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)
(c)
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
AWJ Bicknell et al.
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.
Camera technology in marine monitoring
429
(a)
(b)
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
(c)
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
Camera technology in marine monitoring
430
AWJ Bicknell et al.
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 multi-­
spectral 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
AWJ Bicknell et al.
Camera technology in marine monitoring
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.
Dayoub F, Dunbabin M, and Corke P. 2015. Robotic detection and
tracking of crown-of-thorns starfish. IEEE/RSJ International
Conference on Intelligent Robots and Systems; 28 Sep–2 Oct
2015. Hamburg, Germany. http://bit.ly/2aeq9Zr. Viewed 25 Jul
2016.
Denny CM, Willis TJ, and Babcock RC. 2004. Rapid recolonisation of snapper Pagrus auratus: Sparidae within an offshore
island marine reserve after implementation of no-­take status.
Mar Ecol-­Prog Ser 272: 183–90.
Dickinson JL, Shirk J, Bonter D, et al. 2012. The current state of
citizen science as a tool for ecological research and public
JJ Acknowledgements
engagement. Front Ecol Environ 10: 291–97.
Edgington DR, Cline DE, Davis D, et al. 2006. Detecting, tracking
and classifying animals in underwater video. Proceedings of
This work was funded by a Natural Environment
OCEANS 2006; 18–21 Sep 2006; Boston, MA. IEEE.
Research Grant (NE/J012319/1).
doi:10.1109/OCEANS.2006.306878.
Fosså JH, Mortensen PB, and Furevik DM. 2002. The deep-­water
JJ References
coral Lophelia pertusa in Norwegian waters: distribution and
Anderson K and Gaston KJ. 2013. Lightweight unmanned aerial
fishery impacts. Hydrobiologia 471: 1–12.
vehicles will revolutionize spatial ecology. Front Ecol Environ
Friberg N, Bonada N, Bradley DC, et al. 2011. Biomonitoring of
11: 138–46.
human impacts in freshwater ecosystems: the good, the bad and
Babcock RC, Shears NT, Alcala AC, et al. 2010. Decadal trends in
the ugly. Adv Ecol Res 44: 1–68.
marine reserves reveal differential rates of change in direct and
Gleason ACR, Reid RP, and Voss KJ. 2007. Automated ­classification
indirect effects. P Natl Acad Sci USA 107: 18256–61.
of underwater multispectral imagery for coral reef monitoring.
Bailey DM, King NJ, and Priede IG. 2007. Cameras and carcasses:
Proceedings of OCEANS 2007; 29 Sep–4 Oct 2007; Vancouver,
historical and current methods for using artificial food falls to
Canada. IEEE. doi:10.1109/OCEANS.2007.4449394.
study deep-­water animals. Mar Ecol-­Prog Ser 350: 179–91.
Hoagland P, Beaulieu S, Tivey MA, et al. 2010. Deep-­sea mining of
Bellwood DR, Hughes TP, Folke C, et al. 2004. Confronting the
seafloor massive sulfides. Mar Policy 34: 728–32.
coral reef crisis. Nature 429: 827–33.
Hochscheid S. 2014. Why we mind sea turtles’ underwater busiBicknell AWJ, Oro D, Camphuysen K, et al. 2013. Potential conseness: a review on the study of diving behavior. J Exp Mar Biol
quences of discard reform for seabird communities. J Appl Ecol
Ecol 450: 118–36.
50: 649–58.
Hodgson A, Kelly N, and Peel D. 2013. Unmanned aerial vehicles
Birney K, Griffin A, Gwiazda J, et al. 2006. Potential deep-sea min(UAVs) for surveying marine fauna: a dugong case study. PLoS
ing of seafloor massive sulfides: a case study in Papua New
ONE 8: e79556.
Guinea. Santa Barbara, CA: University of California–Santa
Howell KL, Davies JS, and Narayanaswamy BE. 2010. Identifying
Barbara. Technical report. http://bit.ly/2a8n0Ge. Viewed 25
deep-­sea megafaunal epibenthic assemblages for use in habitat
Jul 2016.
mapping and marine protected area network design. J Mar Biol
Bonney R, Ballard H, Jordan R, et al. 2009. Public participation in
Assoc UK 90: 33–68.
scientific research: defining the field and assessing its potential
Hughes TP, Rodrigues MJ, Bellwood DR, et al. 2007. Phase shifts,
for informal science education. A CAISE Inquiry Group
herbivory, and the resilience of coral reefs to climate change.
Report. Washington, DC: Center for Advancement of Informal
Curr Biol 17: 360–65.
Science Education (CAISE).
Jaiteh VF, Allen SJ, Meeuwig JJ, et al. 2014. Combining in-­trawl
Bouchet PJ and Meeuwig JJ. 2015. Drifting baited stereo-­
video with observer coverage improves understanding of provideography: a novel sampling tool for surveying pelagic wildtected and vulnerable species by-­catch in trawl fisheries. Mar
life in offshore marine reserves. Ecosphere 6: art137.
Freshwater Res 65: 830–37.
Broadhurst M and Orme CDL. 2014. Spatial and temporal benJones DOB, Wigham BD, Hudson IR, et al. 2007. Anthropogenic
thic species assemblage responses with a deployed marine tidal
disturbance of deep-­sea megabenthic assemblages: a study with
energy device: a small scaled study. Mar Environ Res 99:
remotely operated vehicles in the Faroe-­Shetland Channel, NE
76–84.
Atlantic. Mar Biol 151: 1731–41.
Broadhurst M, Barr S, and Orme CDL. 2014. In-­situ ecological
Kemp K and Yesson C. 2013. Greenland benthic assessment, 2nd
interactions with a deployed tidal energy device: an observaannual report. London, UK: Institute of Zoology, Zoological
tional pilot study. Ocean Coast Manage 99: 31–38.
Society of London.
Bryan DR, Bosley KL, Hicks AC, et al. 2014. Quantitative video
Lambert GI, Jennings S, Kaiser MJ, et al. 2014. Quantifying recovanalysis of flatfish herding behavior and impact on effective
ery rates and resilience of seabed habitats impacted by bottom
area swept of a survey trawl. Fish Res 154: 120–26.
fishing. J Appl Ecol 51: 1326–36.
Buckland ST, Burt ML, Rexstad EA, et al. 2012. Aerial surveys of
Langhamer O. 2012. Artificial reef effect in relation to offshore
seabirds: the advent of digital methods. J Appl Ecol 49: 960–
renewable energy conversion: state of the art. Sci World J 2012:
67.
art386713.
Burton AC, Neilson E, Moreira D, et al. 2015. Wildlife camera
Lathrop RG, Montesano P, and Haag S. 2006. A multi-­
scale
trapping: a review and recommendations for linking surveys to
segmentation approach to mapping seagrass habitats using
­
ecological processes. J Appl Ecol 52: 675–85.
­airborne digital camera imagery. Photogramm Eng Rem S 72:
Butler DA and Meek P. 2013. Camera trapping and invasions
665–75.
of privacy: an Australian legal perspective. Torts Law J 20:
Lewison RL, Crowder LB, Read AJ, et al. 2004. Understanding
235–64.
impacts of fisheries bycatch on marine megafauna. Trends Ecol
Cleasby IR, Wakefield ED, Bearhop S, et al. 2015. Three-­
Evol 19: 598–604.
dimensional tracking of a wide-­ranging marine predator: flight
Lukeman R, Li Y-X, and Edelstein-Keshet L. 2010. Inferring indiheights and vulnerability to offshore wind farms. J Appl Ecol 52:
vidual rules from collective behavior. P Natl Acad Sci USA 107:
1474–82.
12576–80.
© The Ecological Society of America
www.frontiersinecology.org
431
Camera technology in marine monitoring
432
Malcolm HA, Gladstone W, Lindfield S, et al. 2007. Spatial and
temporal variation in reef fish assemblages of marine parks in
New South Wales, Australia: baited video observations. Mar
Ecol-­Prog Ser 350: 277–90.
Mallet D and Pelletier D. 2014. Underwater video techniques for
observing coastal marine biodiversity: a review of sixty years of
publications (1952–2012). Fish Res 154: 44–62.
Marshall G. 1990. A video-collar to study aquatic fauna: a view
from the animal’s back. In: Reed D (Ed). Spirit of Enterprise:
The 1990 Rolex Awards. Bern, Switzerland: Buri International.
McElderry H. 2008. At-sea observing using video-based electronic
monitoring. Electronic Monitoring Workshop; Seattle, WA;
29–30 Jul 2008. Victoria, Canada: Archipelago Marine Rese­
arch Ltd.
McLean DL, Harvey ES, Fairclough DV, et al. 2010. Large decline
in the abundance of a targeted tropical lethrinid in areas open
and closed to fishing. Mar Ecol-­Prog Ser 418: 189–99.
McShea WJ, Forrester T, Costello R, et al. 2015. Volunteer-­run
cameras as distributed sensors for macrosystem mammal
research. Landscape Ecol 31: 55–66.
Moll RJ, Millspaugh JJ, Beringer J, et al. 2007. A new ‘view’ of ecology and conservation through animal-­
borne video systems.
Trends Ecol Evol 22: 660–68.
Monson DH, Udevitz MS, and Jay CV. 2013. Estimating age ratios
and size of Pacific walrus herds on coastal haulouts using video
imaging. PLoS ONE 8: e69806.
Mortazavi H, Oakley JP, and Barkat B. 2013. Mitigating the effect
of optical back-­scatter in multispectral underwater imaging.
Meas Sci Technol 24: 074025.
Myers RA and Worm B. 2003. Rapid worldwide depletion of predatory fish communities. Nature 423: 280–83.
Nguyen TX, Winger PD, Legge G, et al. 2014. Underwater observations of the behaviour of snow crab (Chionoecetes opilio)
encountering a shrimp trawl off northeast Newfoundland. Fish
Res 156: 9–13.
Norse EA, Brooke S, Cheung WW, et al. 2012. Sustainability of
deep-­sea fisheries. Mar Policy 36: 307–20.
Pikitch EK, Santora C, Babcock EA, et al. 2004. Ecosystem-­based
fishery management. Science 305: 346–47.
Ramirez-Llodra E, Tyler PA, Baker MC, et al. 2011. Man and the
last great wilderness: human impact on the deep sea. PLoS
ONE 6: e22588.
Ropert-Coudert Y and Wilson R. 2005. Trends and perspectives
in animal-­
attached remote sensing. Front Ecol Environ 3:
437–44.
Rosen S and Holst JC. 2013. DeepVision in-­trawl imaging: sampling the water column in four dimensions. Fish Res 148:
64–73.
Sheehan EV, Stevens TF, and Attrill MJ. 2010. A quantitative,
non-­destructive methodology for habitat characterisation and
benthic monitoring at offshore renewable energy developments. PLoS ONE 5: e14461.
Sheehan EV, Cousens SL, Nancollas SJ, et al. 2013a. Drawing lines
at the sand: evidence for functional vs visual reef boundaries in
temperate Marine Protected Areas. Mar Pollut Bull 76:
194–202.
www.frontiersinecology.org
AWJ Bicknell et al.
Sheehan EV, Witt MJ, Cousens SL, et al. 2013b. Benthic interactions with renewable energy installations in a temperate
ecosystem. Proceedings of the Twenty-third International
­
Offshore and Polar Engineering Conference; Anchorage, AK;
30 Jun–5 Jul 2013. International Society of Offshore and Polar
Engineers. ISOPE-I-13-159.
Singh H, Can A, Eustice R, et al. 2004. Seabed AUV offers new
platform for high-­resolution imaging. Eos T Am Geophys Un
85: 289–96.
Smale DA, Kendrick GA, Harvey ES, et al. 2012. Regional-­scale
benthic monitoring for ecosystem-­based fisheries management
(EBFM) using an autonomous underwater vehicle (AUV).
ICES J Mar Sci 69: 1108–18.
Smith ANH, Anderson MJ, Millar RB, et al. 2014. Effects of
marine reserves in the context of spatial and temporal variation: an analysis using Bayesian zero-­inflated mixed models.
Mar Ecol-­Prog Ser 499: 203–16.
Smith MD, Roheim CA, Crowder LB, et al. 2010. Sustainability
and global seafood. Science 327: 784–86.
Stevens TF, Sheehan EV, Gall SC, et al. 2014. Monitoring benthic
biodiversity restoration in Lyme Bay marine protected area:
design, sampling and analysis. Mar Policy 45: 310–17.
Thaxter CB and Burton NHK. 2009. High definition imagery for
surveying seabirds and marine mammals: a review of recent
trials and development of protocols. Thetford, UK: BTO.
Vardaro MF, Bagley PM, Bailey DM, et al. 2013. A Southeast
Atlantic deep-­ocean observatory: first experiences and results.
Limnol Oceanogr-­Meth 11: 304–15.
Vergés A, Bennett S, and Bellwood DR. 2012. Diversity among
macroalgae-­consuming fishes on coral reefs: a transcontinental
comparison. PLoS ONE 7: e45543.
Votier SC, Bicknell A, Cox SL, et al. 2013. A bird’s eye view of
discard reforms: bird-­borne cameras reveal seabird/fishery interactions. PLoS ONE 8: e57376.
Watling L and Norse EA. 1998. Disturbance of the seabed by
mobile fishing gear: a comparison to forest clearcutting.
Conserv Biol 12: 1180–97.
Watson DL, Anderson MJ, Kendrick GA, et al. 2009. Effects of
protection from fishing on the lengths of targeted and non-­
targeted fish species at the Houtman Abrolhos Islands, Western
Australia. Mar Ecol-­Prog Ser 384: 241–49.
Weinstein BG. 2015. MotionMeerkat: integrating motion video
detection and ecological monitoring. Methods Ecol Evol 6:
357–62.
Williams K, De Robertis A, Berkowitz Z, et al. 2014. An underwater stereo-­camera trap. Methods Oceanogr 11: 1–12.
Williams SB, Pizarro OR, Jakuba MV, et al. 2012. Monitoring of
benthic reference sites: using an autonomous underwater vehicle. IEEE Robot Autom Mag 19: 73–84.
JJ Supporting
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