Wearable sensors for monitoring marine environments and their inhabitants.

Human societies depend on marine ecosystems, but their degradation continues. Toward mitigating this decline, new and more effective ways to precisely measure the status and condition of marine environments are needed alongside existing rebuilding strategies. Here, we provide an overview of how sensors and wearable technology developed for humans could be adapted to improve marine monitoring. We describe barriers that have slowed the transition of this technology from land to sea, update on the developments in sensors to advance ocean observation and advocate for more widespread use of wearables on marine organisms in the wild and in aquaculture. We propose that large-scale use of wearables could facilitate the concept of an 'internet of marine life' that might contribute to a more robust and effective observation system for the oceans and commercial aquaculture operations. These observations may aid in rationalizing strategies toward conservation and restoration of marine communities and habitats.

The role of wingbeat frequency and amplitude in flight power.

Body-mounted accelerometers provide a new prospect for estimating power use in flying birds, as the signal varies with the two major kinematic determinants of aerodynamic power: wingbeat frequency and amplitude. Yet wingbeat frequency is sometimes used as a proxy for power output in isolation. There is, therefore, a need to understand which kinematic parameter birds vary and whether this is predicted by flight mode (e.g. accelerating, ascending/descending flight), speed or morphology. We investigate this using high-frequency acceleration data from (i) 14 species flying in the wild, (ii) two species flying in controlled conditions in a wind tunnel and (iii) a review of experimental and field studies. While wingbeat frequency and amplitude were positively correlated, R2 values were generally low, supporting the idea that parameters can vary independently. Indeed, birds were more likely to modulate wingbeat amplitude for more energy-demanding flight modes, including climbing and take-off. Nonetheless, the striking variability, even within species and flight types, highlights the complexity of describing the kinematic relationships, which appear sensitive to both the biological and physical context. Notwithstanding this, acceleration metrics that incorporate both kinematic parameters should be more robust proxies for power than wingbeat frequency alone.

Long walk home: Magellanic penguins have strategies that lead them to areas where they can navigate most efficiently.

Understanding how animals move in dense environments where vision is compromised is a major challenge. We used GPS and dead-reckoning to examine the movement of Magellanic penguins commuting through vegetation that precluded long-distance vision. Birds leaving the nest followed the shortest, quickest route to the sea (the 'ideal path', or 'I-path') but return tracks depended where the birds left the water. Penguins arriving at the beach departure spot mirrored the departure. Most of those landing at a distance from the departure spot travelled slowly, obliquely to the coast at a more acute angle than a beeline trajectory to the nest. On crossing their I-path, these birds then followed this route quickly to their nests. This movement strategy saves birds distance, time and energy compared to a route along the beach and the into the colony on the I-track and saves time and energy compared to a beeline trajectory which necessitates slow travel in unfamiliar areas. This suggests that some animals adopt tactics that take them to an area where their navigational capacities are enhanced for efficient travel in challenging environments.

Tracking the exposure of a pelagic seabird to marine plastic pollution.

We aimed to describe how debris originated from coastal cities and fisheries circulates and accumulates along the Argentine continental shelf and its potential interaction with southern giant petrels (SGP, Macronectes giganteus). We used tracking data of 31 SGPs (adults and juveniles) from Patagonian colonies. Lagrangian simulations of particles were released from coastal cities and fisheries. Oceanographic features together with plastic input generated a corridor of debris through the Argentine shelf with areas of high debris accumulation, exposing SGP to plastic consumption. During chick provisioning trips 93.9% of petrel's locations overlapped with areas of plastic accumulation. Although early developmental stages were more exposed to particles from cities, the exposure of petrels (all classes) to debris from fisheries was 10% higher than from cities. Measures to reduce debris from fisheries, would reduce plastic ingestion by giant petrels. Proper management of open sky dumpsters would reduce plastic consumption by chicks and juveniles.

How often should dead-reckoned animal movement paths be corrected for drift?

BACKGROUND: Understanding what animals do in time and space is important for a range of ecological questions, however accurate estimates of how animals use space is challenging. Within the use of animal-attached tags, radio telemetry (including the Global Positioning System, 'GPS') is typically used to verify an animal's location periodically. Straight lines are typically drawn between these 'Verified Positions' ('VPs') so the interpolation of space-use is limited by the temporal and spatial resolution of the system's measurement. As such, parameters such as route-taken and distance travelled can be poorly represented when using VP systems alone. Dead-reckoning has been suggested as a technique to improve the accuracy and resolution of reconstructed movement paths, whilst maximising battery life of VP systems. This typically involves deriving travel vectors from motion sensor systems and periodically correcting path dimensions for drift with simultaneously deployed VP systems. How often paths should be corrected for drift, however, has remained unclear. METHODS AND RESULTS: Here, we review the utility of dead-reckoning across four contrasting model species using different forms of locomotion (the African lion Panthera leo, the red-tailed tropicbird Phaethon rubricauda, the Magellanic penguin Spheniscus magellanicus, and the imperial cormorant Leucocarbo atriceps). Simulations were performed to examine the extent of dead-reckoning error, relative to VPs, as a function of Verified Position correction (VP correction) rate and the effect of this on estimates of distance moved. Dead-reckoning error was greatest for animals travelling within air and water. We demonstrate how sources of measurement error can arise within VP-corrected dead-reckoned tracks and propose advancements to this procedure to maximise dead-reckoning accuracy. CONCLUSIONS: We review the utility of VP-corrected dead-reckoning according to movement type and consider a range of ecological questions that would benefit from dead-reckoning, primarily concerning animal-barrier interactions and foraging strategies.

Estimates for energy expenditure in free-living animals using acceleration proxies: A reappraisal.

It is fundamentally important for many animal ecologists to quantify the costs of animal activities, although it is not straightforward to do so. The recording of triaxial acceleration by animal-attached devices has been proposed as a way forward for this, with the specific suggestion that dynamic body acceleration (DBA) be used as a proxy for movement-based power. Dynamic body acceleration has now been validated frequently, both in the laboratory and in the field, although the literature still shows that some aspects of DBA theory and practice are misunderstood. Here, we examine the theory behind DBA and employ modelling approaches to assess factors that affect the link between DBA and energy expenditure, from the deployment of the tag, through to the calibration of DBA with energy use in laboratory and field settings. Using data from a range of species and movement modes, we illustrate that vectorial and additive DBA metrics are proportional to each other. Either can be used as a proxy for energy and summed to estimate total energy expended over a given period, or divided by time to give a proxy for movement-related metabolic power. Nonetheless, we highlight how the ability of DBA to predict metabolic rate declines as the contribution of non-movement-related factors, such as heat production, increases. Overall, DBA seems to be a substantive proxy for movement-based power but consideration of other movement-related metrics, such as the static body acceleration and the rate of change of body pitch and roll, may enable researchers to refine movement-based metabolic costs, particularly in animals where movement is not characterized by marked changes in body acceleration.

Female-biased stranding in Magellanic penguins.

Magellanic penguins (Spheniscus magellanicus) have been reported to become stranded along the coasts of northern Argentina, Uruguay and southern Brazil during the austral winter [1-3]. This location is more than a thousand kilometers distant from their northernmost breeding colony in northern Patagonia. Curiously, females typically outnumber males at stranding sites (approximately three females per male) [2]. To date, no conspicuous sex differences have been reported in their migratory movements [3], although records are lacking during the peak stranding season. Consequently, the reason(s) for the female-biased stranding remain unknown, despite the growing necessity for understanding their behavior outside the breeding season [3]. We recorded at-sea distributions of Magellanic penguins throughout the non-breeding period using animal-borne data loggers and found that females reached more northern areas than males and did not dive as deep during winter (Figure 1). Such sexual differences in spatial domains might be driven by mechanisms related to sexual size dimorphism, such as the avoidance of intraspecific competition for food resources [4], differences in thermal habitat preference [5] or differences in the ability to withstand the northward-flowing ocean circulation [6]. Individual penguins that winter in northern areas are likely to be at greater risk of natural [7] and anthropogenic threats [8], and probably more so in females, as more females than males tend to frequent areas closer to the sites where penguins strand. Our results highlight the importance of understanding the spatial domains of each sex throughout the annual cycle that are associated with different mortality risks.

Towards informed metrics for examining the role of human-induced animal responses in tag studies on wild animals.

Two prime issues can detrimentally affect animals that have been equipped with tags: (i) the effect of the capture and restraint process; and (ii) the effect of the tag itself. This work examines some of the issues surrounding quantification of tag effects on wild animals for both restrained and free-living animals. A new method to quantify stress effects based on monitoring ventilation rates in relation to activity is suggested for restrained animals which may help improve the practice of handling animals. It is also suggested that various metrics, many derived from accelerometers, can be examined in tagged wild animals to examine the change in behaviors over time with a view to having a better understanding of welfare issues, assuring the quality of recorded data and informing best practice.

Corrigendum to "Lousy chicks: Chewing lice from the imperial shag, Leucocarbo atriceps" [Int. J. Parasitol. Parasites Wildl. 6 (2017) 229-232].

[This corrects the article DOI: 10.1016/j.ijppaw.2017.08.002.].

Long necks enhance and constrain foraging capacity in aquatic vertebrates.

Highly specialized diving birds display substantial dichotomy in neck length with, for example, cormorants and anhingas having extreme necks, while penguins and auks have minimized necks. We attached acceleration loggers to Imperial cormorants Phalacrocorax atriceps and Magellanic penguins Spheniscus magellanicus, both foraging in waters over the Patagonian Shelf, to examine the difference in movement between their respective heads and bodies in an attempt to explain this dichotomy. The penguins had head and body attitudes and movements that broadly concurred throughout all phases of their dives. By contrast, although the cormorants followed this pattern during the descent and ascent phases of dives, during the bottom (foraging) phase of the dive, the head angle differed widely from that of the body and its dynamism (measured using vectorial dynamic acceleration) was over four times greater. A simple model indicated that having the head on an extended neck would allow these cormorants to half the energy expenditure that they would expend if their body moved in the way their heads did. This apparently energy-saving solution is likely to lead to greater heat loss though and would seem tenable in slow-swimming species because the loss of streamlining that it engenders would make it detrimental for fast-swimming taxa such as penguins.

Lousy chicks: Chewing lice from the Imperial Shag, Leucocarbo atriceps.

Forty-one imperial shag chicks were sampled for lice during the breeding season of 2014 in Punta León, Argentina. We found 2 lice species, Pectinopygus turbinatus infesting the body and Piagetiella caputincisum present in the oral cavity of the birds. This constitutes the first host record for P. turbinatus and the first record for the continental Argentina for P. caputincisum. Ninety-three percent of the chicks were infested by at least one lice species. P. turbinatus was present in all of the lousy chicks, while P. caputincisum infested 84.2% of them. The mean intensity was 29.5 and the range 1-129. There was no difference in prevalence, mean intensity or mean abundance between louse species. However, we found differences among the pattern of infestation of each species. Imperial shag chicks were infested by their parents during their first days of life by P. turbinatus, mainly in nymphal stage and by P. caputincisum as adult lice. Our results showed differences among lice species that could be related to the restrictions that lice from seabirds faced during their life cycle.

Identification of animal movement patterns using tri-axial magnetometry.

BACKGROUND: Accelerometers are powerful sensors in many bio-logging devices, and are increasingly allowing researchers to investigate the performance, behaviour, energy expenditure and even state, of free-living animals. Another sensor commonly used in animal-attached loggers is the magnetometer, which has been primarily used in dead-reckoning or inertial measurement tags, but little outside that. We examine the potential of magnetometers for helping elucidate the behaviour of animals in a manner analogous to, but very different from, accelerometers. The particular responses of magnetometers to movement means that there are instances when they can resolve behaviours that are not easily perceived using accelerometers. METHODS: We calibrated the tri-axial magnetometer to rotations in each axis of movement and constructed 3-dimensional plots to inspect these stylised movements. Using the tri-axial data of Daily Diary tags, attached to individuals of number of animal species as they perform different behaviours, we used these 3-d plots to develop a framework with which tri-axial magnetometry data can be examined and introduce metrics that should help quantify movement and behaviour.. RESULTS: Tri-axial magnetometry data reveal patterns in movement at various scales of rotation that are not always evident in acceleration data. Some of these patterns may be obscure until visualised in 3D space as tri-axial spherical plots (m-spheres). A tag-fitted animal that rotates in heading while adopting a constant body attitude produces a ring of data around the pole of the m-sphere that we define as its Normal Operational Plane (NOP). Data that do not lie on this ring are created by postural rotations of the animal as it pitches and/or rolls. Consequently, stereotyped behaviours appear as specific trajectories on the sphere (m-prints), reflecting conserved sequences of postural changes (and/or angular velocities), which result from the precise relationship between body attitude and heading. This novel approach shows promise for helping researchers to identify and quantify behaviours in terms of animal body posture, including heading. CONCLUSION: Magnetometer-based techniques and metrics can enhance our capacity to identify and examine animal behaviour, either as a technique used alone, or one that is complementary to tri-axial accelerometry.

A spherical-plot solution to linking acceleration metrics with animal performance, state, behaviour and lifestyle.

BACKGROUND: We are increasingly using recording devices with multiple sensors operating at high frequencies to produce large volumes of data which are problematic to interpret. A particularly challenging example comes from studies on animals and humans where researchers use animal-attached accelerometers on moving subjects to attempt to quantify behaviour, energy expenditure and condition. RESULTS: The approach taken effectively concatinated three complex lines of acceleration into one visualization that highlighted patterns that were otherwise not obvious. The summation of data points within sphere facets and presentation into histograms on the sphere surface effectively dealt with data occlusion. Further frequency binning of data within facets and representation of these bins as discs on spines radiating from the sphere allowed patterns in dynamic body accelerations (DBA) associated with different postures to become obvious. METHOD: We examine the extent to which novel, gravity-based spherical plots can produce revealing visualizations to incorporate the complexity of such multidimensional acceleration data using a suite of different acceleration-derived metrics with a view to highlighting patterns that are not obvious using current approaches. The basis for the visualisation involved three-dimensional plots of the smoothed acceleration values, which then occupied points on the surface of a sphere. This sphere was divided into facets and point density within each facet expressed as a histogram. Within each facet-dependent histogram, data were also grouped into frequency bins of any desirable parameters, most particularly dynamic body acceleration (DBA), which were then presented as discs on a central spine radiating from the facet. Greater radial distances from the sphere surface indicated greater DBA values while greater disc diameter indicated larger numbers of data points with that particular value. CONCLUSIONS: We indicate how this approach links behaviour and proxies for energetics and can inform our identification and understanding of movement-related processes, highlighting subtle differences in movement and its associated energetics. This approach has ramifications that should expand to areas as disparate as disease identification, lifestyle, sports practice and wild animal ecology. UCT Science Faculty Animal Ethics 2014/V10/PR (valid until 2017).

Selfies of Imperial Cormorants (Phalacrocorax atriceps): What Is Happening Underwater?

During the last few years, the development of animal-borne still cameras and video recorders has enabled researchers to observe what a wild animal sees in the field. In the present study, we deployed miniaturized video recorders to investigate the underwater foraging behavior of Imperial cormorants (Phalacrocorax atriceps). Video footage was obtained from 12 animals and 49 dives comprising a total of 8.1 h of foraging data. Video information revealed that Imperial cormorants are almost exclusively benthic feeders. While foraging along the seafloor, animals did not necessarily keep their body horizontal but inclined it downwards. The head of the instrumented animal was always visible in the videos and in the majority of the dives it was moved constantly forward and backward by extending and contracting the neck while travelling on the seafloor. Animals detected prey at very short distances, performed quick capture attempts and spent the majority of their time on the seafloor searching for prey. Cormorants foraged at three different sea bottom habitats and the way in which they searched for food differed between habitats. Dives were frequently performed under low luminosity levels suggesting that cormorants would locate prey with other sensory systems in addition to sight. Our video data support the idea that Imperial cormorants' efficient hunting involves the use of specialized foraging techniques to compensate for their poor underwater vision.

Love thy neighbour: automatic animal behavioural classification of acceleration data using the K-nearest neighbour algorithm.

Researchers hoping to elucidate the behaviour of species that aren't readily observed are able to do so using biotelemetry methods. Accelerometers in particular are proving particularly effective and have been used on terrestrial, aquatic and volant species with success. In the past, behavioural modes were detected in accelerometer data through manual inspection, but with developments in technology, modern accelerometers now record at frequencies that make this impractical. In light of this, some researchers have suggested the use of various machine learning approaches as a means to classify accelerometer data automatically. We feel uptake of this approach by the scientific community is inhibited for two reasons; 1) Most machine learning algorithms require selection of summary statistics which obscure the decision mechanisms by which classifications are arrived, and 2) they are difficult to implement without appreciable computational skill. We present a method which allows researchers to classify accelerometer data into behavioural classes automatically using a primitive machine learning algorithm, k-nearest neighbour (KNN). Raw acceleration data may be used in KNN without selection of summary statistics, and it is easily implemented using the freeware program R. The method is evaluated by detecting 5 behavioural modes in 8 species, with examples of quadrupedal, bipedal and volant species. Accuracy and Precision were found to be comparable with other, more complex methods. In order to assist in the application of this method, the script required to run KNN analysis in R is provided. We envisage that the KNN method may be coupled with methods for investigating animal position, such as GPS telemetry or dead-reckoning, in order to implement an integrated approach to movement ecology research.

Phylogeography and genetic structure of two Patagonian shag species (Aves: Phalacrocoracidae).

We compared the phylogeographic and genetic structure of two sympatric shag species, Phalacrocorax magellanicus (rock shag) and Phalacrocorax atriceps (imperial shag), from Patagonia (southern South America). We used multilocus genotypes of nuclear DNA (microsatellite loci) from 324 individuals and mitochondrial DNA sequences (ATPase) from 177 individuals, to evaluate hypotheses related to the effect of physical and non-physical barriers on seabird evolution. Despite sharing many ecological traits, the focal species strongly differ in two key aspects: P. magellanicus has a strong tendency to remain at/near their breeding colonies during foraging trips and the non-breeding season, while P. atriceps exhibits the converse pattern. Both species showed similar mtDNA genetic structure, where colonies from the Atlantic Coast, Pacific Coast and Fuegian region were genetically divergent. We also found similarities in the results of Bayesian clustering analysis of microsatellites, with both species having four clusters. However population differentiation (e.g. Fst, Φst) was higher in P. magellanicus compared to P. atriceps, and average membership probabilities of individuals to specific clusters (Q-values) were also higher in the former. Phalacrocorax magellanicus has strong phylogeographic structure, consistent with the impact of Pleistocene glaciations, with diagnostic haplotypes associated with each of the three mentioned regions. The same pattern was not as evident for P. atriceps. Migration rate estimators were higher for P. atriceps than for P. magellanicus; however both species followed an n-island-like model of gene flow, this implies that dispersal occurs across the continental land mass that separates Atlantic and Pacific Oceans. Our results supported the hypothesis that non-physical barriers are important drivers of the genetic and phylogeographic structure in seabirds, and also that physical barriers constitute effective but not absolute impediments to gene flow.

Serosurvey for selected infectious agents in two sympatric species of cormorants (Phalacrocorax atriceps and Phalacrocorax magellanicus) from coastal Patagonia, Argentina.

We conducted a serologic survey for selected infectious agents on two sympatric cormorants, the Imperial Cormorant (Phalacrocorax atriceps) and the Rock Shag (Phalacrocorax magellanicus). Blood was collected from 267 Imperial Cormorants and 106 Rock Shags at 17 colonies along the Patagonia Atlantic shore during nine breeding seasons (1994, 1999-2001-2005-2008-2010). Antibodies to four pathogens were common to both species and frequently observed: avian paramyxovirus type 1 (56% of Imperial Cormorants and 56% of Rock Shags); avian adenovirus (67% of Imperial Cormorants and 40% of Rock Shags); infectious bronchitis virus serotypes IBV-41, IBV-46, IBV-99, and IBV-JMK (53% of Imperial Cormorants and 64% of Rock Shags); and Salmonella pullorum (18% of Imperial Cormorants and 7% of Rock Shags). Antibody prevalence for these pathogens varied significantly between species, except for avian paramyxovirus type 1. Exposure to avian paramyxovirus type 1 and all serotypes of infectious bronchitis virus varied significantly among seasons in both species. In contrast, the sporadic occurrence of positive titers suggest that cormorants had occasional exposure to Aspergillus spp. (3% of Rock Shags, only in 2000), avian paramyxovirus type 3 (5% of Rock Shags, only in 2008), Chlamydophila spp. (1% of Imperial Cormorants, only in 2010), and avian reovirus (1% of Rock Shags, only in 1999; 29% of Imperial Cormorants, in 2008 and 2010). Both species were antibody negative for avian encephalomyelitis virus, avian influenza virus, avian laryngotracheitis virus, avian paramyxovirus type 2, and infectious bursal disease virus. We provide the first information on pathogen exposure, indicated by detection of antibody in blood samples, for two sympatric species of South Atlantic cormorants. To determine major causes of morbidity and mortality in these birds future efforts should focus on necropsy surveys in cormorant colonies.

Hematology and blood chemistry values in free-living imperial cormorants (Phalacrocorax atriceps).

As part of an on-going, long-term study on the reproductive ecology and health status of imperial cormorants (Phalacrocorax atriceps), blood samples were collected to establish baseline values for hematologic parameters (hematocrit, red and white blood cell counts, leukocyte profile, heterophil:lymphocyte ratio, total solids) and serum chemistries (glucose, uric acid, urea, total protein, triglycerides, cholesterol, albumin:globulin ratio, alkaline phosphatase, lactate dehydrogenase, creatine phosphokinase, aspartate aminotransferase, alanine aminotransferase, calcium, phosphorus). One hundred and eighty-four male adults from the Punta Le6n breeding colony in Patagonia Argentina were captured during the chick-rearing period of four breeding seasons, 2004 (n = 48), 2005 (n = 29), 2010 (n = 43), and 2011 (n = 64). All birds appeared to be in good body condition and no abnormalities were noted during physical examination. In general, values for the parameters reported in this study were similar to those previously described for other cormorant species. Significant interannual differences were observed in most health parameters analyzed. This study defines baseline health parameters for imperial cormorants and, coupled with previous reports on pathogen exposure, contributes to our knowledge of the overall health status of the species.

How much is too much? Assessment of prey consumption by Magellanic penguins in Patagonian colonies.

Penguins are major consumers in the southern oceans although quantification of this has been problematic. One suggestion proposes the use of points of inflection in diving profiles ('wiggles') for this, a method that has been validated for the estimation of prey consumption by Magellanic penguins (Spheniscus magellanicus) by Simeone and Wilson (2003). Following them, we used wiggles from 31 depth logger-equipped Magellanic penguins foraging from four Patagonian colonies; Punta Norte (PN), Bahía Bustamente (BB), Puerto Deseado (PD) and Puerto San Julián (PSJ), all located in Argentina between 42-49° S, to estimate the prey captured and calculate the catch per unit time (CPUT) for birds foraging during the early chick-rearing period. Numbers of prey caught and CPUT were significantly different between colonies. Birds from PD caught the highest number of prey per foraging trip, with CPUT values of 68±19 prey per hour underwater (almost two times greater than for the three remaining colonies). We modeled consumption from these data and calculate that the world Magellanic penguin population consumes about 2 million tons of prey per year. Possible errors in this calculation are discussed. Despite this, the analysis of wiggles seems a powerful and simple tool to begin to quantify prey consumption by Magellanic penguins, allowing comparison between different breeding sites. The total number of wiggles and/or CPUT do not reflect, by themselves, the availability of food for each colony, as the number of prey consumed by foraging trip is strongly associated with the energy content and wet mass of each colony-specific 'prey type'. Individuals consuming more profitable prey could be optimizing the time spent underwater, thereby optimizing the energy expenditure associated with the dives.

The need for speed: testing acceleration for estimating animal travel rates in terrestrial dead-reckoning systems.

Numerous methods are currently available to track animal movements. However, only one of these, dead-reckoning, has the capacity to provide continuous data for animal movements over fine scales. Dead-reckoning has been applied almost exclusively in the study of marine species, in part due to the difficulty of accurately measuring the speed of terrestrial species. In the present study we evaluate the use of accelerometers and a metric known as overall dynamic body acceleration (ODBA) as a proxy for the measurement of speed for use in dead-reckoning. Data were collated from previous studies, for 10 species locomoting on a treadmill and their ODBA measured by an attached data logger. All species except one showed a highly significant linear relationship between speed and ODBA; however, there was appreciable inter- and intra-specific variance in this relationship. ODBA was then used to estimate speed in a simple trial run of a dead-reckoning track. Estimating distance travelled using speed derived from prior calibration for ODBA resulted in appreciable errors. We describe a method by which these errors can be minimised, by periodic ground-truthing (e.g., by GPS or VHF telemetry) of the dead-reckoned track and adjusting the relationship between speed and ODBA until actual known positions and dead-reckoned positions accord.