Manta Matcher: automated photographic identification of manta rays using keypoint features

For species which bear unique markings, such as natural spot patterning, field work has become increasingly more reliant on visual identification to recognize and catalog particular specimens or to monitor individuals within populations. While many species of interest exhibit characteristic markings that in principle allow individuals to be identified from photographs, scientists are often faced with the task of matching observations against databases of hundreds or thousands of images. We present a novel technique for automated identification of manta rays (Manta alfredi and Manta birostris) by means of a pattern‐matching algorithm applied to images of their ventral surface area. Automated visual identification has recently been developed for several species. However, such methods are typically limited to animals that can be photographed above water, or whose markings exhibit high contrast and appear in regular constellations. While manta rays bear natural patterning across their ventral surface, these patterns vary greatly in their size, shape, contrast, and spatial distribution. Our method is the first to have proven successful at achieving high matching accuracies on a large corpus of manta ray images taken under challenging underwater conditions. Our method is based on automated extraction and matching of keypoint features using the Scale‐Invariant Feature Transform (SIFT) algorithm. In order to cope with the considerable variation in quality of underwater photographs, we also incorporate preprocessing and image enhancement steps. Furthermore, we use a novel pattern‐matching approach that results in better accuracy than the standard SIFT approach and other alternative methods. We present quantitative evaluation results on a data set of 720 images of manta rays taken under widely different conditions. We describe a novel automated pattern representation and matching method that can be used to identify individual manta rays from photographs. The method has been incorporated into a website (mantamatcher.org) which will serve as a global resource for ecological and conservation research. It will allow researchers to manage and track sightings data to establish important life‐history parameters as well as determine other ecological data such as abundance, range, movement patterns, and structure of manta ray populations across the world.     

A newt does not change its spots: using pattern mapping for the identification of individuals in large populations of newt species

The correct identification of individuals is a requirement of capture-mark-recapture (CMR) methods, and it is commonly achieved by applying artificial marks or by mutilation of study-animals. An alternative, non-invasive method to identify individuals is to utilize the patterns of their natural body markings. However, the use of pattern mapping is not yet widespread, mainly because it is considered time consuming, particularly in large populations and/or long-term CMR studies. Here we explore the use of pattern mapping for the identification of adult individuals in the alpine (Ichthyosaura alpestris) and smooth (Lissotriton vulgaris) newts (Amphibia, Salamandridae), using the freely available, open-source software Wild-ID. Our photographic datasets comprised nearly 4000 captured animals’ images, taken during a 3-year period. The spot patterns of individual newts of both species did not change through time, and were sufficiently varied to allow their individual identification, even in the larger datasets. The pattern-recognition algorithm of Wild-ID was highly successful in identifying individual newts in both species. Our findings indicate that pattern mapping can be successfully employed for the identification of individuals in large populations of a broad range of animals that exhibit natural markings. The significance of pattern-mapping is accentuated in CMR studies that aim in obtaining long-term information on the demography and population dynamics of species of conservation interest, such as many amphibians facing population declines.     

The reliability of pigment pattern‐based identification of wild bottlenose dolphins

Long‐term studies often rely on natural markings for individual identification across time. The primary method for identification in small cetaceans relies on dorsal fin shape, scars, and other natural markings. However, dorsal fin markings can vary substantially over time and the dorsal fin can become unrecognizable after an encounter with a boat or shark. Although dorsal fins have the advantage in that they always break the water surface when the cetacean breathes, other physical features, such as body scars and pigmentation patterns can supplement. The goal of this study was to explore the use of dorso‐lateral pigment patterns to identify wild bottlenose dolphins. We employed photographic pigment matching tests to determine if pigmentation patterns showed (1) longitudinal consistency and (2) bilateral symmetry using a 30 yr photographic database of bottlenose dolphins (Tursiops aduncus). We compared experienced dolphin researchers and inexperienced undergraduate student subjects in their ability to accurately match images. Both experienced and inexperienced subjects correctly matched dolphin individuals at a rate significantly above chance, even though they only had 10 s to make the match. These results demonstrate that pigment patterns can be used to reliably identify individual wild bottlenose dolphins, and likely other small cetacean species at other sites.     

A new model study species: high accuracy of discrimination between individual freckled hawkfish (Paracirrhites forsteri) using natural markings

Variations between distinct natural markings of freckled hawkfish (Paracirrhites forsteri) could allow in situ identification of individuals from underwater photography. Receiver operating characteristic analysis was used to assess the ability of the Interactive Individual Identification System (I³S) software to assist in discriminating between images of P. forsteri individuals. This study's results show the high discriminant ability of I³S to differentiate between unlike individuals and identify images of the same individual. The ability to use automatic computer-aided assistance in the study of this species will enable future research to explore behaviour and movements of individuals in the wild.     

Validating the use of colouration patterns for individual recognition in the worm pipefish using a novel set of microsatellite markers

In studies of behaviour, ecology and evolution, identification of individual organisms can be an invaluable tool, capable of unravelling otherwise cryptic information regarding group structure, movement patterns, population size and mating strategies. The use of natural markings is arguably the least invasive method for identification. However, to be truly useful natural markings must be sufficiently variable to allow for unique identification, while being stable enough to permit long‐term studies. Non‐invasive marking techniques are especially important in fishes of the Family Syngnathidae (pipefishes, seahorses and seadragons), as many of these taxa are of conservation concern or used extensively in studies of sexual selection. Here, we assessed the reliability of natural markings as a character for individual identification in a wild population of Nerophis lumbriciformis by comparing results from natural markings to individual genetic assignments based on eight novel microsatellite loci. We also established a minimally invasive method based on epithelial cell swabbing to sample DNA. All pipefish used in the validation of natural markings, independently of sex or time between recaptures, were individually recognized through facial colouration patterns. Their identities were verified by the observation of the same multilocus genotype at every sampling event for each individual that was identified on the basis of natural markings. Successful recaptures of previously swabbed pipefish indicated that this process probably did not induce an elevated rate of mortality. Also, the recapture of newly pregnant males showed that swabbing did not affect reproductive behaviour.     

Size‐dependent predation risk partly explains the sex‐related marking polymorphism in the sexually size‐dimorphic pygmy grasshopper Tetrix japonica

The sexually size‐dimorphic grasshopper Tetrix japonica exhibits variation in body‐color markings on the pronotum even within a single local population. Such markings have been suggested to reduce the visual detectability of grasshoppers. However, some grasshoppers have no markings. In the present study, we examined the effect of the sex‐related difference in body size and the spotted markings on the degree of camouflage. We hypothesized that: (i) large individuals (females) are potentially more readily detectable than small individuals; (ii) large individuals (females) with spotted markings would realize a moderate degree of the camouflage effect, whereas large individuals (females) without spotted markings would be quite poorly camouflaged; (iii) small individuals (males) would be sufficiently less detectable, with or without markings; and (iv) large individuals (females) would tend to have spotted markings in the wild. To test this hypothesis, we conducted a morph‐frequency field survey and laboratory experiments on the body‐size dependency of the spotted markings. The field survey confirmed that all females exhibited spotted markings and that the majority of males were non‐spotted morphs. Next, to determine whether body size and the spotted markings affected crypsis, we conducted detection task experiments using humans as dummy predators by manipulating the body size, presence/absence of spotted markings, or both, of printed grasshoppers. The absence of spotted markings increased the detection risk in large and small grasshoppers, particularly in large‐sized females. These results suggest that female‐biased selective predation could have eliminated non‐spotted female morphs because they were too conspicuous.     

Novel Acoustic Technology for Studying Free-Ranging Shark Social Behaviour by Recording Individuals' Interactions

Group behaviours are widespread among fish but comparatively little is known about the interactions between free-ranging individuals and how these might change across different spatio-temporal scales. This is largely due to the difficulty of observing wild fish groups directly underwater over long enough time periods to quantify group structure and individual associations. Here we describe the use of a novel technology, an animal-borne acoustic proximity receiver that records close-spatial associations between free-ranging fish by detection of acoustic signals emitted from transmitters on other individuals. Validation trials, held within enclosures in the natural environment, on juvenile lemon sharks Negaprion brevirostris fitted with external receivers and transmitters, showed receivers logged interactions between individuals regularly when sharks were within 4 m (∼4 body lengths) of each other, but rarely when at 10 m distance. A field trial lasting 17 days with 5 juvenile lemon sharks implanted with proximity receivers showed one receiver successfully recorded association data, demonstrating this shark associated with 9 other juvenile lemon sharks on 128 occasions. This study describes the use of acoustic underwater proximity receivers to quantify interactions among wild sharks, setting the scene for new advances in understanding the social behaviours of marine animals.     

Assortative mating among animals of captive and wild origin following experimental conservation releases

Captive breeding is a high profile management tool used for conserving threatened species. However, the inevitable consequence of generations in captivity is broad scale and often-rapid phenotypic divergence between captive and wild individuals, through environmental differences and genetic processes. Although poorly understood, mate choice preference is one of the changes that may occur in captivity that could have important implications for the reintroduction success of captive-bred animals. We bred wild-caught house mice for three generations to examine mating patterns and reproductive outcomes when these animals were simultaneously released into multiple outdoor enclosures with wild conspecifics. At release, there were significant differences in phenotypic (e.g. body mass) and genetic measures (e.g. G_st and F) between captive-bred and wild adult mice. Furthermore, 83% of offspring produced post-release were of same source parentage, inferring pronounced assortative mating. Our findings suggest that captive breeding may affect mating preferences, with potentially adverse implications for the success of threatened species reintroduction programmes.     

Differences in mortality rates, dispersal distances and breeding success of commercially reared and wild grey partridges in the Czech agricultural landscape

The aim of this study was to evaluate the efficiency of releasing commercially reared individuals of the grey partridge (Perdix perdix) as a method for species recovery. This study compares the mortality risk of grey partridges depending on origin, sex and body condition, controlling for age, infection risk and release method. In total, 110 locally caught wild individuals and 75 commercially reared game-farm partridges were released and radio tracked within the same study area in the Czech Republic between 2009 and 2011. To exclude a possible effect of age on survival, only individuals in the second calendar year of life were chosen for the analysis. Commercially reared partridges had significantly higher mortality risk than wild ones. None of the commercially reared birds survived in the wild until the end of the nesting period, and none produced a fledged brood. Females from game farms showed significantly better survival than males and preferred to mate with wild males, whereas wild females avoided mating with commercially reared males. Predation was the main cause of mortality, and proportion of birds killed by raptors and mammals did not differ between wild and commercially reared birds. These results highlight the uselessness of releasing adult commercially reared partridges in an effort to establish viable populations of this species in the wild and stress the need for a change from intensive rearing methods aimed predominantly at quantity towards a more conservation breeding-oriented approach aimed at quality.     

The ethology of Labroides dimidiatus (cuv. & val.) (Labridae,Pisces) on Aldabra

A small group of Labroides dimidiatus were studied over a period of 4 months in the shallow reef environment of Aldabra. It was found necessary to redefine the concept of a cleaning station. Different sizes of Labroides occupied different types of area and it was found the smallest individuals do not have fixed ranges, but move about beneath available crevices. Larger individuals occupied more open situations and the adults usually lived in pairs. The areas occupied appeared to reflect the fishes' ability to maintain position against strong water movements and tidal currents. Labroides dimidiatus shows territorial, intraspecific aggression and model presentation experiments indicate that body pigmentation acts as the releaser for this aggression. This aggression serves as a dispersal mechanism for young fish. Interspecific aggression occurred against fish with similar body markings to Labroides or which constituted a threat. The cleaning behaviour was studied and it was found that different species of host fish are cleaned in a highly specific manner, and certain hosts are preferred to others. There is evidence that this may be learned as a result of early experience with the host fish. Measurements are made of the cleaning intensity in the area. Some host fish were shown to be attracted to the cleaning range and may adopt invitation postures in the absence of the cleaner. The results are discussed in relation to the recent literature on Labroides dimidiatus and their importance to reef fish populations.     

Testing Thayer's hypothesis: can camouflage work by distraction?

One of the oldest theories of animal camouflage predicts that apparently conspicuous markings enhance concealment. Such 'distraction' marks are hypothesized to work by drawing the viewer's attention away from salient features, such as the body outline, that would otherwise reveal the animal. If distraction marks enhance concealment, then they offer a route for animals to combine camouflage markings with conspicuous signalling strategies, such as warning signals. However, the theory has never been tested and remains controversial. By using camouflaged artificial prey presented to wild avian predators, we test whether distractive markings enhance concealment. In contrast to predictions, we find that markings, both circular and irregular shapes, increase predation compared with unmarked targets. Markings became increasingly costly as their contrast against the prey increased. Our experiments failed to find any empirical support for the hypothesis that distraction markings are an important aspect of camouflage in animals.     

Genetic markers validate using the natural phenotypic characteristics of shed feathers to identify individual northern goshawks Accipiter gentilis

The recognition of individual animals is essential for many types of ecological research, as it enables estimates of demographic parameters such as population size, survival and reproductive rates. A popular method of visually identifying individuals uses natural variations in spot, stripe or scar markings. Although several studies have assessed the accuracy of these methods in mammals, crustaceans and fish, there have been few attempts to determine whether phenotypic characteristics are accurate when used for birds. Furthermore, even less is known about whether shed or moulted body parts can be reliably used to visually identify individuals. Here we assessed the accuracy of using phenotypic characteristics to identify avian individuals using a double‐marking experiment, whereby nine microsatellite genetic markers and natural markings on shed feathers were used to independently identify northern goshawks Accipiter gentilis. Phenotypic and genetic identification of individuals was consistent in 94.4% (51/54) comparisons. Our results suggest that the phenotypic characteristics of shed feathers can be reliably used as a non‐invasive and relatively inexpensive technique to monitor populations of an elusive species, the northern goshawk, without having to physically re‐capture or re‐sight individuals. We posit that using natural markings on shed feathers will also be a reliable method of identifying individuals in avian species with similar phenotypic characteristics, such as other Accipiter species.     

Mate recognition in members of the Drosophila nasuta complex

An examination of the courtship patterns of species belonging to the Drosophila nasuta complex shows that markings which are characteristic of males are almost certainly involved in their recognition as conspecifics by females. In each species the males perform a courtship sequence in such a way as to expose these markings to the female. A phylogeny of the species based on both male courtship patterns and the associated male markings is constructed. This phylogeny is compared to previously published phylogenies of the same group which were based on fixed and floating chromosomal differences between the species. Finally, the evidence which the complex provides for the utility and general significance of a new species concept, the Recognition Concept, is evaluated.     

Nautilus pompilius life history and demographics at the Osprey Reef Seamount, Coral Sea, Australia

Nautiloids are the subject of speculation as to their threatened status arising from the impacts of targeted fishing for the ornamental shell market. Life history knowledge is essential to understand the susceptibility of this group to overfishing and to the instigation of management frameworks. This study provides a comprehensive insight into the life of Nautilus in the wild. At Osprey Reef from 1998–2008, trapping for Nautilus was conducted on 354 occasions, with 2460 individuals of one species, Nautilus pompilius, captured and 247 individuals recaptured. Baited remote underwater video systems (BRUVS) were deployed on 15 occasions and six remotely operated vehicle (ROV) dives from 100–800 m were conducted to record Nautilus presence and behavior. Maturity, sex and size data were recorded, while measurements of recaptured individuals allowed estimation of growth rates to maturity, and longevity beyond maturity. We found sexual dimorphism in size at maturity (males: 131.9±SD = 2.6 mm; females: 118.9±7.5 mm shell diameter) in a population dominated by mature individuals (58%). Mean growth rates of 15 immature recaptured animals were 0.061±0.023 mm day⁻¹ resulting in an estimate of around 15.5 years to maturation. Recaptures of mature animals after five years provide evidence of a lifespan exceeding 20 years. Juvenile Nautilus pompilius feeding behavior was recorded for the first time within the same depth range (200–610 m) as adults. Our results provide strong evidence of a K-selected life history for Nautilus from a detailed study of a ‘closed’ wild population. In conjunction with population size and density estimates established for the Osprey Reef Nautilus, this work allows calculations for sustainable catch and provides mechanisms to extrapolate these findings to other extant nautiloid populations (Nautilus and Allonautilus spp.) throughout the Indo-Pacific.     

Prey selection and dietary response by wolves in a high-density multi-species ungulate community

Studies on predation by the wolf (Canis lupus) have often reported contradictory results about the role of prey density and vulnerability on wolf prey use. We investigated dietary response and prey selection by wolves in a high-density and multi-species ungulate community, analysing scats collected over a period of 11 years in the Casentinesi Forests, Italy. The second most abundant species, wild boar (Sus scrofa), was found to be the main wolf prey, and we did not observe any dietary response of wolves to variations in the density of either primary or secondary prey species. Selection patterns were uniform throughout the study period. Wolves strongly selected for wild boar piglets, while roe deer (Capreolus capreolus) fawns and adults, red deer (Cervus elaphus) adults and fallow deer (Dama dama) adults were avoided. Wolf preference for wild boar was inversely density dependent. Within each species, juveniles were preferred to adults. Medium-sized, young individuals of both wild boar and roe deer were optimal prey, although with different selection patterns related to the different anti-predator strategies adopted by each prey species. The results of this study suggest that in productive ecosystems with high density and high renewal rates of prey, selection patterns by wolves are determined by prey vulnerability, which is connected to prey age and body size. The different patterns of wild boar versus cervids use by wolf across Europe seems to be related to their relative abundances, while the strong selection of wild boar in Italian Apennines with respect to the more frequent avoidance in central-eastern Europe is better explained by higher piglet productivity and smaller body size of adults boar in Mediterranean temperate forests.     

Plasticity and genetic effects contribute to different axes of neural divergence in a community of mimetic Heliconius butterflies

Changes in ecological preference, often driven by spatial and temporal variation in resource distribution, can expose populations to environments with divergent information content. This can lead to adaptive changes in the degree to which individuals invest in sensory systems and downstream processes, to optimize behavioural performance in different contexts. At the same time, environmental conditions can produce plastic responses in nervous system development and maturation, providing an alternative route to integrating neural and ecological variation. Here, we explore how these two processes play out across a community of Heliconius butterflies. Heliconius communities exhibit multiple Mullerian mimicry rings, associated with habitat partitioning across environmental gradients. These environmental differences have previously been linked to heritable divergence in brain morphology in parapatric species pairs. They also exhibit a unique dietary adaptation, known as pollen feeding, that relies heavily on learning foraging routes, or trap-lines, between resources, which implies an important environmental influence on behavioural development. By comparing brain morphology across 133 wild-caught and insectary-reared individuals from seven Heliconius species, we find strong evidence for interspecific variation in patterns of neural investment. These largely fall into two distinct patterns of variation; first, we find consistent patterns of divergence in the size of visual brain components across both wild and insectary-reared individuals, suggesting genetically encoded divergence in the visual pathway. Second, we find interspecific differences in mushroom body size, a central component of learning and memory systems, but only among wild caught individuals. The lack of this effect in common-garden individuals suggests an extensive role for developmental plasticity in interspecific variation in the wild. Finally, we illustrate the impact of relatively small-scale spatial effects on mushroom body plasticity by performing experiments altering the cage size and structure experienced by individual H. hecale. Our data provide a comprehensive survey of community level variation in brain structure, and demonstrate that genetic effects and developmental plasticity contribute to different axes of interspecific neural variation.     

Identification of individual adult female Javan lutungs (Trachypithecus auratus sondaicus) by using patterns of dark pigmentation in the pubic area

In a series of field surveys of wild Javan lutungs (Trachypithecus auratus sondaicus) conducted at Pangandaran Nature Reserve in West Java, Indonesia, from 2011 to 2012, we tried to use a method of individual identification by using individual-specific patterns of dark pigmentation in the pubic area. During the 2011 dry season, we used a digital SLR camera with a 400-mm telephoto lens to photograph the pubic area of each individual of a habituated group. These photographs were the basis for identifying 14 different adult females. During the rainy season of 2011 and the dry season of 2012, we checked the presence/absence of each of the identified individuals and found that these patterns were stable, at least during our study period. We found that two adult females and one adult female disappeared from the subject group between the first and second and between the second and third surveys, respectively, and that one adult female gave birth between the first and second surveys, but the infant had disappeared from the group between the second and third surveys. We could not confirm the validity of the method for juvenile females because of the dense white hair in their pubic areas and the fact that few individuals had clear patterns. Furthermore, we could not use this method for males because of the lack of pigmentation in the pubic area. As patterns of pigmentation in the pubic area are known to be present in other Trachypithecus species, our method can be useful for identification of individual adult females of these species, on which few individual-based behavioral studies have been conducted. Collecting individual-based behavioral data would enable us to track the presence of individuals in groups or movements between groups; determine the effects of social rank and age on within-group competition and copulation; and examine population data.     

Estimating body mass of wild pigs (Sus scrofa) using body morphometrics

Wild pigs (Sus scrofa) are invading many areas globally and impacting biodiversity and economies in their non‐native range. Thus, wild pigs are often targeted for eradication efforts. Age‐ and sex‐specific body measurements are important for informing these eradication efforts because they reflect body condition, resource availability, and fecundity, which are common indicators of population trajectory. However, body mass is often difficult to collect, especially on large individuals that require specialized equipment or multiple people to weigh. Measurements that can be rapidly taken by a single land or wildlife manager on any size wild pig without aid from specialized equipment would be beneficial if they accurately infer wild pig body mass. Our goals were to assess whether morphometric measurements could accurately predict wild pig body mass, and to provide tools to directly input these measures and estimate wild pig body mass. Using linear models, we quantified the relationship between body mass and morphometric measurements (i.e., body length, chest girth, ear length, eye to snout length, hindfoot length, shoulder length, and tail length) from a subset (n = 102) of wild pigs culled at the Mississippi Alluvial Valley, Mississippi, USA. We evaluated separate models for each individual morphometric measurement. We then used the model coefficients to develop equations to predict wild pig body mass. We validated these equations predicting body mass of 1592 individuals collected across eight areas in Australia, Guam, and the USA for cross‐validation. Each developed equation remained accurate when cross‐validated across regions. Body length, chest girth, and shoulder length were the morphometrics that best predicted wild pig body mass. Our analyses indicated it is possible to use the presented equations to infer wild pig body mass from simple metrics.     

Inferring the Provenance of an Alien Species with DNA Barcodes: The Neotropical Butterfly Dryas iulia in Thailand

The Neotropical butterfly Dryas iulia has been collected from several locations in Thailand and Malaysia since 2007, and has been observed breeding in the wild, using introduced Passiflora foetida as a larval host plant. The butterfly is bred by a butterfly house in Phuket, Thailand, for release at weddings and Buddhist ceremonies, and we hypothesized that this butterfly house was the source of wild, Thai individuals. We compared wing patterns and COI barcodes from two, wild Thai populations with individuals obtained from this butterfly house. All Thai individuals resemble the subspecies D. iulia modesta, and barcodes from wild and captive Thai specimens were identical. This unique, Thai barcode was not found in any of the 30 specimens sampled from the wild in the species'' native range, but is most similar to specimens from Costa Rica, where many exporting butterfly farms are located. These data implicate the butterfly house as the source of Thailand''s wild D. iulia populations, which are currently so widespread that eradication efforts are unlikely to be successful.     

Effects of Sand Dune Stabilization on the Spatial Pattern of Artemisia ordosica Population in Mu Us Desert,Northwest China

Vegetation patterns are strongly influenced by sand mobility in desert ecosystems. However, little is known about the spatial patterns of Artemisia ordosica, a dominant shrub in the Mu Us desert of Northwest China, in relation to sand fixation. The aim of this study was to investigate and contrast the effects of sand dune stabilization on the population and spatial distribution of this desert shrub. Spatial autocorrelation, semi-variance analysis, and point-pattern analysis were used jointly in this study to investigate the spatial patterns of A. ordosica populations on dunes in Yanchi County of Ningxia, China. The results showed that the spatial autocorrelation and spatial heterogeneity declined gradually, and the distance between the clustered individuals shortened following sand dune fixation. Seedlings were more aggregated than adults in all stage of dune stabilization, and both were more aggregated on shifting sand dunes separately. Spatial associations of the seedlings with the adults were mostly positive at distances of 0–5 m in shifting sand dunes, and the spatial association changed from positive to neutral in semi-fixed sand dunes. The seedlings were spaced in an almost random pattern around the adults, and their distances from the adults did not seem to affect their locations in semi-fixed sand dunes. Furthermore, spatial associations of the seedlings with the adults were negative in the fixed sand dune. These findings demonstrate that sand stabilization is an important factor affecting the spatial patterns of A. ordosica populations in the Mu Us desert. These findings suggest that, strong association between individuals may be the mechanism to explain the spatial pattern formation at preliminary stage of dune fixation. Sand dune stabilization can change the spatial pattern of shrub population by weakening the spatial association between native shrub individuals, which may affect the development direction of desert shrubs.