Determining the sex of bottlenose dolphins from Doubtful Sound using dorsal fin photographs

Sexing cetaceans usually requires time-consuming observation, or genetic sexing via biopsy sampling or skin swabbing. We developed a method to determine the sex of bottlenose dolphins ( Tursiops sp.) in Doubtful Sound, Fiordland, using laser-metric dorsal fin photographs. From dorsal fin photographs of 43 bottlenose dolphins of known sex (25 females, 18 males) we analyzed the shape, proportion of fin area covered in scarring and epidermal lesions, and the number of fin nicks. Males had significantly higher rates of scarring ( P < 0.001) and dorsal fin nicks ( P < 0.01) than females, whereas the severity of epidermal lesions was higher in females ( P < 0.05). A logistic regression applied to all measured variables, and measurements of dorsal fin size, indicated that the proportion of dorsal fin scarring ( P < 0.001), number of fin nicks ( P < 0.01), and dorsal fin surface area ( P < 0.01) were significant variables and together correctly predicted the sex of 93% (40/43) of the dolphins. The classification function may not be applicable to other populations due to geographic variation in bottlenose dolphin morphology and social structure. The method is quick and noninvasive to apply, and further increases the value of dorsal fin photo-identification pictures.     

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.     

ABUNDANCE OF BOTTLENOSE DOLPHINS IN THE BAYS, SOUNDS, AND ESTUARIES OF NORTH CAROLINA

We conducted a mark-recapture survey of bottlenose dolphins Tursiops truncatus in the bays, sounds, and estuaries of North Carolina during July 2000, using photographic identification techniques. During this survey we took 7,682 photographs of dolphins and, of these, 3,457 images were of sufficient quality for analysis. We identified 306 dolphins from distinctive nicks and notches on their dorsal fins. Eighry-six dolphins were photographed on more than one occasion during the course of the survey; one dolphin was photographed on four separate days. We then applied the results of our photographic analyses to several mark-recapture models and examined potential violations of the assumptions of these models, including an unexpected correlation between photo quality and mark distinctiveness. Our analysis suggests that our results are robusr to possible violations of these assumptions. The resulting estimates were then scaled to account for the proportion (0.46) of unmarked dolphins in the population. Our best estimate of the number of dolphins present in the inshore waters of North Carolina during July 2000 is 1,033 with a 95% Confidence Interval of 860–1,266 (CV = 0.099). Most dolphins were found in the northern part of the study area, which includes the second largest estuarine system in the United States.     

Evidence for Distinct Coastal and Offshore Communities of Bottlenose Dolphins in the North East Atlantic

Bottlenose dolphin stock structure in the northeast Atlantic remains poorly understood. However, fine scale photo-id data have shown that populations can comprise multiple overlapping social communities. These social communities form structural elements of bottlenose dolphin (Tursiops truncatus) populations, reflecting specific ecological and behavioural adaptations to local habitats. We investigated the social structure of bottlenose dolphins in the waters of northwest Ireland and present evidence for distinct inshore and offshore social communities. Individuals of the inshore community had a coastal distribution restricted to waters within 3 km from shore. These animals exhibited a cohesive, fission-fusion social organisation, with repeated resightings within the research area, within a larger coastal home range. The offshore community comprised one or more distinct groups, found significantly further offshore (>4 km) than the inshore animals. In addition, dorsal fin scarring patterns differed significantly between inshore and offshore communities with individuals of the offshore community having more distinctly marked dorsal fins. Specifically, almost half of the individuals in the offshore community (48%) had characteristic stereotyped damage to the tip of the dorsal fin, rarely recorded in the inshore community (7%). We propose that this characteristic is likely due to interactions with pelagic fisheries. Social segregation and scarring differences found here indicate that the distinct communities are likely to be spatially and behaviourally segregated. Together with recent genetic evidence of distinct offshore and coastal population structures, this provides evidence for bottlenose dolphin inshore/offshore community differentiation in the northeast Atlantic. We recommend that social communities should be considered as fundamental units for the management and conservation of bottlenose dolphins and their habitat specialisations.     

Gauging the Threat: The First Population Estimate for White Sharks in South Africa Using Photo Identification and Automated Software

South Africa is reputed to host the world’s largest remaining population of white sharks, yet no studies have accurately determined a population estimate based on mark-recapture of live individuals. We used dorsal fin photographs (fin IDs) to identify white sharks in Gansbaai, South Africa, from January 2007 – December 2011. We used the computer programme DARWIN to catalogue and match fin IDs of individuals; this is the first study to successfully use the software for white shark identification. The programme performed well despite a number of individual fins showing drastic changes in dorsal fin shape over time. Of 1682 fin IDs used, 532 unique individuals were identified. We estimated population size using the open-population POPAN parameterisation in Program MARK, which estimated the superpopulation size at 908 (95% confidence interval 808–1008). This estimated population size is considerably larger than those described at other aggregation areas of the species and is comparable to a previous South African population estimate conducted 16 years prior. Our assessment suggests the species has not made a marked recovery since being nationally protected in 1991. As such, additional international protection may prove vital for the long-term conservation of this threatened species.     

Nicks and notches of the dorsal ridge: Promising mark types for the photo-identification of narwhals

The narwhal is a hunted species for which we have many knowledge gaps. Photo-identification, which uses photographs of natural markings to identify individuals, is widely used in cetacean studies and can address a broad range of biological questions. However, it has not been developed for narwhals. The marks used for other cetaceans are inappropriate for this species either because narwhals lack the body part on which these marks are found or because the marks are known to change with time. We investigated the marks apparent in photographs of narwhals. Nicks and notches on the dorsal ridge are the mark types most promising for photo-identification. They are found on 91%–98% of the individuals, thus allowing the identification of a large part of the population. They can be used to differentiate between individuals, in part because they are variable in their location, numbers, shape, and size. Although our results suggest that nicks and notches are relatively stable over time, rates of change should be formally measured to assess the probability of photographic matches over multiple years. However, we are confident that these marks can be used in studies spanning at least a field season.     

Microhabitat use of Pseudocharopinus markewitschi (Gusev, 1951) (Copepoda: Lernaeopodidae) on the mottled skate,Beringraja pulchra (Liu, 1932): Does biased occurrence on the dorsal side of the pelvic fin imply a safety zone?

The mottled skate Beringraja pulchra is a coastal fish caught by gillnet and bottom trawl fisheries in Hokkaido, Japan. We recently found a parasitic copepod identical to Pseudocharopinus markewitschi (Gusev, 1951) on this commercially important fish. A total of 109 host individuals caught off the coast of northern Hokkaido, Japan, were examined for adult females of this copepod, and 67 cases (61.5%) of infection comprised with 31 cases (67.4%) of 46 males and 36 cases (57.1%) of 63 females were found. The parasite specimens (n = 229) were recovered mainly from the dorsal side of the pelvic fin (n = 168, 73.4%), followed by the claspers (n = 32, 14.0%). The mottled skate is thought to spend most of its lifetime lying in sand or crawling on the seafloor. Therefore, the biased infection to the dorsal side of the pelvic fin may imply that site selection favors less susceptible for disturbances resulting from such host-specific behavior.     

SOCIAL ECOLOGY OF BOTTLENOSE DOLPHINS IN THE KVARNERIĆ (NORTHERN ADRIATIC SEA)

A bottlenose dolphin community was studied from small inflatable craft from 1987 to 1994 in a relatively large area (about 800 km²) east of the islands of Loˇsinj and Cres, northern Adriatic Sea. A total of 106 individuals were photoidentified based on natural permanent marks on their dorsal fins. Most of the dolphins were resighted on a regular basis, indicating a high level of year-round site fidelity, although their range was evidently greater than the chosen study area. Dolphin density was highly variable and considerably lower than for most well-known bottlenose dolphin communities. Groups averaged seven individuals, with a mode of two. Groups entirely composed of adults were the smallest, groups with calves the largest. Group fluidity was high, seasonal and yearly changes in mean group size being also considerable. Summer was the peak calving season, with a striking variation in the number of births on alternate years. Poor evidence of shark predation was found. The social organization of this dolphin community seemed to be highly flexible, possibly as an adaptation to cope with environmental changes as well as with a limited and variable availability of prey.     

Novel method for identifying individual cetaceans using facial features and symmetry: A test case using dolphins

Individual identification plays a major role in our understanding of the biology, ecology and behavior in cetaceans. Being able to tell individuals apart can provide invaluable insight into basic biological and scientific questions, but is also highly relevant to science‐based conservation. Given the importance of individual identification, it appears vital to improve existing identification methods and find new ones. Here, we present a novel identification method of using facial information, with common bottlenose dolphins (Tursiops truncatus) as a case study. In dolphins, dorsal fins are typically used for identification, but not all individuals or species are sufficiently marked. We show that facial features in bottlenose dolphins are long‐term and consistent across the left and right sides, and may enable calves (which tend to have unmarked fins) to be re‐identified after weaning, thus increasing cross‐generational knowledge. This novel method can complement dorsal fin identification by helping document mark changes over time and reduce false negative or positive errors. It also shows that current identification methods can still be improved. With increasing prevalence of digital photography and computer‐aided matching, it may become more viable to use ‘unconventional’ means of identification. We encourage other researchers to explore their photographic records for similar discoveries.     

multimark: an R package for analysis of capture–recapture data consisting of multiple “noninvasive” marks

I describe an open‐source R package, multimark , for estimation of survival and abundance from capture–mark–recapture data consisting of multiple “noninvasive” marks. Noninvasive marks include natural pelt or skin patterns, scars, and genetic markers that enable individual identification in lieu of physical capture. multimark provides a means for combining and jointly analyzing encounter histories from multiple noninvasive sources that otherwise cannot be reliably matched (e.g., left‐ and right‐sided photographs of bilaterally asymmetrical individuals). The package is currently capable of fitting open population Cormack–Jolly–Seber (CJS) and closed population abundance models with up to two mark types using Bayesian Markov chain Monte Carlo (MCMC) methods. multimark can also be used for Bayesian analyses of conventional capture–recapture data consisting of a single‐mark type. Some package features include (1) general model specification using formulas already familiar to most R users, (2) ability to include temporal, behavioral, age, cohort, and individual heterogeneity effects in detection and survival probabilities, (3) improved MCMC algorithm that is computationally faster and more efficient than previously proposed methods, (4) Bayesian multimodel inference using reversible jump MCMC, and (5) data simulation capabilities for power analyses and assessing model performance. I demonstrate use of multimark using left‐ and right‐sided encounter histories for bobcats (Lynx rufus) collected from remote single‐camera stations in southern California. In this example, there is evidence of a behavioral effect (i.e., trap “happy” response) that is otherwise indiscernible using conventional single‐sided analyses. The package will be most useful to ecologists seeking stronger inferences by combining different sources of mark–recapture data that are difficult (or impossible) to reliably reconcile, particularly with the sparse datasets typical of rare or elusive species for which noninvasive sampling techniques are most commonly employed. Addressing deficiencies in currently available software, multimark also provides a user‐friendly interface for performing Bayesian multimodel inference using capture–recapture data consisting of a single conventional mark or multiple noninvasive marks.     

TEMPORAL VARIABILITY IN FEATURES USED TO PHOTO-IDENTIFY HUMPBACK WHALES (MEGAPTERA NOVAEANGLIAE)

Photographs of 99 humpback whales of known age were analyzed to assess the temporal variability and recognizability of individually distinctive fluke and dorsal fin features used for photo-identification. Stable features tended to be morphological in nature (dorsal fin shape and edges, the trailing edge of the fluke, and the raised bumps on the caudal peduncle termed "knobs"). Transitory features typically were superficial marks (scarring, scratching, and pigmentation). The variability of several features was found to be age-dependent as well. Young animals sometimes experienced substantial change to their fluke coloration patterns, though this feature stabilized with age. Dorsal fin edges and fluke serration peaks tended to undergo more change in males than in females, with most changes occurring following sexual maturation. Peduncle knobs were the most stable feature, with no documented change in any age interval. Given the extreme stability (and hence recognizability) of dorsal fin shape and peduncle knobs, we suggest that photographs combining the dorsal fin and the caudal peduncle provide the most consistent way to reidentify humpback whales, particularly calves following weaning.     

POPULATION ANALYSIS OF NORTHERN BOTTLENOSE WHALES IN THE GULLY, NOVA SCOTIA

Northern bottlenose whales ( Hyperoodon ampullatus ) are consistently found through the year in the Gully, a prominent submarine canyon on the edge of the Scotian Shelf. Individuals were photographically identified during field studies between 1988 and 1995. About 70% of the population is identifiable, and 29% have markings which persist reliably over periods of years. A mark-recapture analysis of photographic individual identifications collected between 1988 and 1995 indicates that the population using the Gully numbers about 230 animals (approximate 95% confidence interval 160-360). The rate of mortality plus emigration plus mark change (in animals with reliable long-term marks) is about 12% per year, although this estimate has wide and uncertain confidence limits. Members of the Gully population, which includes calves and mature males, are shorter than animals caught off Labrador. The small size of the Gully population and its persistent use of a very small, bathy-metrically unique ocean area make it vulnerable to human disturbance.     

CETACEANS OF THE NORTHERN GULF OF CALIFORNIA: DISTRIBUTION, OCCURRENCE, and RELATIVE ABUNDANCE

A total of 1,715 km of boat-based surveys and 1,521 km of aircraft-based surveys was conducted from 1986–1989 to assess the distribution, relative abundance, and ecological relationships of cetaceans in the northern Gulf of California. Seven cetacean species were seen; in decreasing frequency of groups encountered they were: bottlenose dolphins, Tursiops truncatus ; vaquitas, Phocoena sinus ; common dolphins, Delphinus delphis ; fin whales, Balaenoptera physalus ; Bryde's whales, B. edeni ; gray whales, Eschrichtius robustus , and killer whales, Orcinus orca. Common dolphins were numerically dominant and bottlenose dolphins were seen most often. Bryde's whales and vaquitas had the smallest group sizes. In general, the odontocete cetaceans were separated spatially, whereas the distribution of Bryde's and fin whales overlapped considerably.     

THE USE OF NATURAL MARKINGS IN STUDIES OF LONG-FINNED PILOT WHALES (GLOBICEPHALA MELAS)

Photo-identification using natural markings has been used for pilot whale ( Globicephala melas ) studies. However, none of these studies investigated the reliability of the marks used. To identify which mark types are reliable and which could improve the method, fifteen mark types, and their distribution within the population, were described. The rates of gain and loss of each mark type were calculated and the variability in visibility was investigated. Although the mark types associated with the current photo-identification method, the notch and the protruding piece, appear to be permanent, they allowed us to identify only 33% of our sample. The prevalence of all but two mark types is independent of the identifiability of a photograph. One of these is already used in the current photo-identification method. This independence indicates that the proportion of the population that is currently identifiable does not differ from the rest of the population in its susceptibility to factors causing marks, such as predation, and thus appears to be representative of the whole population. Using saddle patches in combination with the current photo-identification method would double the percentage of the identifiable individuals. However, due to limitations of matching software, the current method is easier to use.     

Experimental evaluation of calcein and alizarin red S for immersion marking of silver carp Hypophthalmichthys molitrix (Valenciennes, 1844)

Calcein (CAL) and alizarin red S (ARS) at concentrations of 50–200 and 150–300 mg/L, respectively, were used for immersion marking of juvenile silver carp Hypophthalmichthys molitrix (79.65 ± 2.11 mm total length, mean ± SD). The marked fish were kept in separate tanks (0.012 individuals per litre, rearing temperature 18.4–25.7°C) for 360 days. Each experimental treatment group consisted of three replicates (16 individuals per replicate). Immersion for 24 h produced detectable marks in the sagittae, lateral line and non‐lateral line scales, and fin rays (dorsal, pectoral, ventral, anal, and caudal) at 360 days post‐marking. Acceptable marks in the sagittae were observed for CAL at concentrations of 150–200 mg/L and for ARS at concentrations of 200–300 mg/L. Fluorescent marks were poorly visible in all non‐lateral line scales from both the CAL‐ and ARS‐treated groups. Acceptable fluorescent marks in the lateral line scales and fin rays were detected for CAL at concentrations of 150–200 and 100–200 mg/L, respectively, and for ARS at concentrations of 200–300 and 150–300 mg/L, respectively. In particular, optimal marks were observed at the highest concentrations investigated in lateral line scales (200 mg/L CAL, 300 mg/L ARS) and fin rays (200 mg/L CAL, 200–300 mg/L ARS). There was no significant difference in the survival or growth of marked fish compared to controls throughout the experiment (P > 0.05).     

Validation of photo‐identification as a mark–recapture method in the spotted eagle ray Aetobatus narinari

The spotted eagle ray Aetobatus narinari is characterized by pigmentation patterns that are retained for up to 3·5 years. These pigmentations can be used to identify individuals through photo‐identification. Only one study has validated this technique, but no study has estimated the percentage of correct identification of the rays using this technique. In order to carry out demographic research, a reliable photographic identification technique is needed. To achieve this validation for A. narinari, a double‐mark system was established over 11 months and photographs of the dorsal surface of 191 rays were taken. Three body parts with distinctive natural patterns were analysed (dorsal surface of the cephalic region, dorsal surface of the pectoral fins and dorsal surface of the pelvic fins) in order to determine the body part that could be used to give the highest percentage of correct identification. The dorsal surface of the pectoral fins of A. narinari provides the most accurate photo‐identification to distinguish individuals (88·2%).     

Experimental evaluation of using calcein and alizarin red S for immersion marking of bighead carp Aristichthys nobilis (Richardson, 1845) to assess growth and identification of marks in otoliths,scales and fin rays

In order to evaluate the effects of immersion marking with calcein (CAL) and alizarin red S (ARS) on growth and mortality of juvenile bighead carp Aristichthys nobilis, and assess mark quality in otoliths, scales, and fin rays, CAL from 50 to 200 mg L^?1 and ARS from 150 to 300 mg L^?1 concentrations were used. With the exception of non‐lateral line scales from 50 mg L^?1 CAL treatments, immersion for 24 h produced detectable marks in sagittae, lateral line and non‐lateral line scales, and fin rays (dorsal, pectoral, ventral, anal, and caudal) at 100 days post‐marking. Detectable fluorescent marks in sagittae were readily observed at concentrations of 150–200 mg L^?1 CAL or 150–300 mg L^?1 ARS. Marks were poorly visible in all non‐lateral line scales from both CAL‐ and ARS‐treated groups. Fluorescent marks were readily detected in lateral line scales at 100–200 mg L^?1 CAL or 150–300 mg L^?1 ARS, and in fin rays at 150–200 mg L^?1 CAL or 150–300 mg L^?1 ARS. In particular, optimal marks were observed at the highest concentrations investigated in sagittae (300 mg L^?1 ARS), lateral line scales (150–200 mg L^?1 CAL or 250–300 mg L^?1 ARS), and fin rays (200 mg L^?1 CAL or 250–300 mg L^?1 ARS). However, fluorescent marks visible to the naked eye were not produced by any of the CAL or ARS treatments in sagittae, scales, or fin rays during this experiment. In addition, there was no significant difference on survival and growth of marked fish compared to controls throughout the experiment (P > 0.05).     

A simple laser photogrammetry technique for measuring Hector's dolphins (Cephalorhynchus hectori) in the field

The ability to measure and age individuals within a population has many important applications, for example, for examining growth and determining size class. We developed a simple photogrammetric system using two parallel lasers and a digital camera, in order to measure dorsal fin dimensions of free-ranging Hector's dolphins. Laser dots were projected onto the fin, providing scale, thus allowing measurement as well as simultaneous photo-ID of 34 individuals from fin nicks and other marks. Multiple measurements (≥5) were available for six individuals; these resulted in mean CVs of 3.71% for fin length and 3.76% for fin height. Errors due to variations in angle and measurement were quantified via photography of a fiberglass Hector's dolphin model. Allometric measurements and age data were collated from 233 autopsied Hector's dolphins. Using these data, fin length was found to be a better predictor of total length (females r²= 0.732, males r²= 0.678) than fin height. Gompertz age/length growth curves were fitted to these individuals. Linear regressions were used to estimate total length for 34 individuals from laser-metrically estimated fin base length. Individuals were then assigned one of three age categories. This system shows promise as a noninvasive way of measuring individuals, while allowing simultaneous photographic identification.     

AN ASSESSMENT OF CHANGES WITH TIME IN THE MARKING PATTERNS USED FOR PHOTOIDENTIFICATION OF INDIVIDUAL SPERM WHALES, PHYSETER MACROCEPHALUS

We observed changes with time in the patterns of characteristic fluke markings used to identify sperm whales. Changes were categorized as minor, moderate, or major based on their severity. These change types were found to occur at rates of 0.9%, 11.8%, and 1.3% per individual per year, respectively. Gain and loss rates for each of seven different mark types were also calculated. The highest estimated rate was the gain of small nicks at 0.08 per individual per year. Most individuals identified by us possess at least a few characteristic marks and, therefore, changes of the type observed in this study are unlikely to severely affect their recognizability. For all but one mark type, gain rates were higher than loss rates, indicating that individuals may be accumulating marks with age. Over long periods this could eventually make individuals unrecognizable, with the result that population sizes calculated from these data may be overestimated. As long as photoidentification studies are conducted sufficiently often, and these changes are as gradual as they appear to be, this problem should be minimal.     

Decline in abundance and apparent survival rates of fin whales (Balaenoptera physalus) in the northern Gulf of St. Lawrence

Estimates of abundance and survivorship provide quantifiable measures to monitor populations and to define and understand their conservation status. This study investigated changes in abundance and survival rates of fin whales (Balaenoptera physalus) in the northern Gulf of St. Lawrence in the context of anthropogenic pressures and changing environmental conditions. A long‐term data set, consisting of 35 years of photo‐identification surveys and comprising more than 5,000 identifications of 507 individuals, formed the basis of this mark–recapture study. Based on model selection using corrected Akaike Information Criterion, the most parsimonious Cormack–Jolly–Seber model included a linear temporal trend in noncalf apparent survival rates with a sharp decline in the last 5 years of the study and a median survival rate of 0.946 (95% confidence interval (CI) 0.910–0.967). To account for capture heterogeneity due to divergent patterns of site fidelity, agglomerative hierarchical cluster analysis was employed to categorize individuals based on their annual and survey site fidelity indices. However, the negative trend in survivorship remained and was corroborated by a significant decline in the estimated super‐population size from 335 (95% CI 321–348) individuals in 2004–2010 to 291 (95% CI 270–312) individuals in 2010–2016. Concurrently, a negative trend was estimated in recruitment to the population, supported by a sharp decrease in the number of observed calves. Ship strikes and changes in prey availability are potential drivers of the observed decline in fin whale abundance. The combination of clustering methods with mark–recapture represents a flexible way to investigate the effects of site fidelity on demographic variables and is broadly applicable to other individual‐based studies.