- Email: [email protected]
Identification Methods
503
I IDENTIFICATION METHODS Randall S. Wells Individual identification is an important tool for studies of animal behavior, ecology, and population biology. Much can be learned from recognition of individuals within a population or social unit, or from tracking individuals through time. Repeated observations of a recognizable individual can help to define its ranging patterns, or to quantify habitat use. Individual identification is essential to understanding group compositions, especially when the individual’s sex, age, genetic relationships, and reproductive conditions are known. Similarly, interpretation of social interactions requires the ability to distinguish among the players. Behavioral descriptions often involve measuring rates of occurrence of behaviors. These rates are measured most accurately when a selected individual is followed through time, or when its behaviors are recorded at predetermined intervals, as with focal animal behavioral observations. Descriptions of life history patterns and empirical measures of population dynamics benefit from individual identification. By following individuals through time it is possible to determine age at sexual maturity, calving intervals, calf survivorship, and lifespan, providing measures of reproductive success. Combined, such individual measures can provide population-level vital rates, including birth rates, mortality rates, and recruitment. Mark-recapture techniques use individual identification to arrive at abundance estimates. Individual identification provides one of the best tools for documenting exchanges of individuals between populations, allowing estimation of immigration and emigration rates. Identification technique selection depends on the research questions being addressed and the species under study. Frequent monitoring of individuals may require identification from a distance, whereas other studies may only need to recognize an animal when it is handled subsequently, alive or at the end of its life. Some species exhibit individually specific natural markings. Other species lack such markings and require the attachment of artificial marks, or tags. Some species are visible on land at times, whereas others are entirely aquatic. Morphological, behavioral, and ecological features guide tag and attachment selection, relative to safety for the animal and effectiveness for the research. It is now possible to collect small tissue samples that allow the identification of individuals genetically. Individual identification techniques have been summarized for cetaceans, pinnipeds, and sirenians (Hammond et al., 1990; Scott et al., 1990; Würsig and Jefferson, 1990; Erickson et al., 1993; Wells et al., 1999; Loughlin et al., 2010). Walker et al. (2012) reviewed the effects of marking and tagging on marine mammals. They noted that while some marking techniques were reported to cause pain and to change swimming and haulout behavior, maternal attendance, and duration of foraging Encyclopedia of Marine Mammals. DOI: http://dx.doi.org/10.1016/B978-0-12-804327-1.00009-1 © 2018 Elsevier Inc. All rights reserved.
trips, marking typically does not affect survival. They further noted that more evaluation is needed of the possible acute effects of marking, including the potential for pain and distress, and to better understand the potential for long-term effects on health and disease, growth, and reproduction.
I. Cetaceans A. Natural Markings Cetaceans exhibit a variety of individually distinctive natural features. Typically, features appearing above the surface during breaths are most useful. In particular, heads, backs, dorsal fins, and flukes offer variations in color patterns, skin patches, body scarring, and/or nicks and notches. Some individuals of most species acquire distinctive scars from wounds or injuries. Perhaps the most unique cetacean identification features are the callosities of right whales, Eubalaena spp. (Payne et al., 1983). These individually distinctive raised patches of roughened skin are present on the rostrum anterior to the blowholes in a pattern referred to as the bonnet, on the chin, lower lips, above the eyes, and near the blowholes. Whale lice (Cyamus spp.), cyamid crustaceans that live on the callosities, give them a white, orange, yellow, or pink appearance. Callosities have provided reliable recognition of individuals over decades. Color variations, where they exist among cetacean species, have been used with much success for individual identification, especially among the mysticetes. Blue whales (Balaenoptera musculus) and gray whales (Eschrichtius robustus) exhibit individually distinctive dorsal mottling (Fig. 1). Pigmentation on sperm whale flanks (Physeter macrocephalus) has proved to be a reliable identification feature. Bowhead whales (Balaena mysticetus) often have a distinctive white pigmentation on the chin and/or peduncle. Fin whales (Balaenoptera physalus) exhibit strongly asymmetrical pigmentation, with both lips and the first third of the baleen on the right side appearing white or pale gray. A light-colored “blaze” sweeps back on the right side, and a V-shaped light-colored “chevron” occurs on both sides behind the blowhole. Minke whales (Balaenoptera spp.) exhibit a pattern of pale lateral pigmentation on the body, often in three distinct swaths, with the relative brightness varying consistently between Northern and Southern Hemispheres. The distinctive dark and white patterns of the flippers and ventral surface of the flukes are familiar identification features for humpback whales (Megaptera novaeangliae) (Katona et al., 1979). Some of the smaller cetaceans also exhibit individually distinctive color variations. Most notable are the light-colored saddle patches behind the dorsal fin of the killer whale (Orcinus orca), which differ in size and shape. The saddle marks of pilot whales (Globicephala spp.) are less distinct. Dorsal fin and/or back pigmentation variation has proven effective with a variety of dolphins and porpoises, and facial color patterns were used to identify the now-extinct baiji (Lipotes vexillifer). Extensive speckling develops with age in spotted dolphins, facilitating individual identification from both above and below the surface in behavioral studies of Stenella frontalis.
I
504
Identification Methods
Figure 1 Distinctive color patterns of a blue whale (Balaenoptera musculus) (Photo by R.S. Wells).
I
Figure 2 Killer whale dorsal fins and saddle patches provide reliable identification cues (Photo by RS. Wells). Scarring can create useful pigment variations. Risso’s dolphins acquire distinctive long-term white scars on their otherwise brown or gray bodies, and belugas (Delphinapterus leucas) acquire dark scars on their otherwise white bodies. In the Mediterranean sea, 71% of Cuvier’s beaked whale males (Ziphius cavirostris) are reliably marked, with males acquiring significantly more marks than females, through conspecific interactions. Bottlenose dolphin (Tursiops spp.) scars on the dorsal fin often are white, in contrast to their general gray coloration. Cookie cutter shark (Isistius spp.) bite wounds leave permanent small diameter oval-shaped scars which are often depressed and pigmented differently from the rest of many pelagic cetaceans’ bodies; these have been used to identify individuals of a variety of species. Dorsal fins are visible to researchers during most surfacings. In many species, dorsal fins develop distinctive shapes or acquire nicks and notches, often through intra- or interspecific interactions that allow for individual identification. For example, male dusky dolphins (Lagenorhynchus obscurus) had significantly more conspecific-acquired dorsal fin markings than females. Among the larger whales, fin, sei (Balaenoptera borealis), Bryde’s (B. edeni), minke, humpback, and sperm whale dorsal fins serve as useful identification features. Building on the pioneering work of Bigg (1982) with killer whales (Fig. 2) and Würsig and Würsig (1977) with bottlenose dolphins, studies based on dorsal fin identifications of various small cetaceans have blossomed (Hammond et al., 1990; Scott et al., 1990; Würsig and Jefferson, 1990; Wells et al., 1999). The
Figure 3 Distinctive dark and light patterns on the ventral surface of a humpback whale’s (Megaptera novaeangliae) fluke (Photo by R.S. Wells).
frequency of occurrence of distinctive fin features varies across species, and sometimes across populations. Off Florida, 60%–80% of bottlenose dolphins have distinctive dorsal fins. Unlike color patterns that vary from one side to the other, dorsal fin nicks and notches are equally visible from both sides and are distinctive under a broad range of lighting conditions. As suggested by Bamford and Robinson (2016) for short-beaked common dolphins (Delphinus delphis), dorsal edge markings and/or injuries may provide an indication of the nature of fisheries interactions affecting specific populations. Some species regularly lift their flukes from the water prior to a dive, providing predictable opportunities to record the occurrence of nicks, notches, and other features on the trailing edge of the flukes. Humpback whales offer both distinctive color patterns and trailing edge features (Fig. 3). Humpback whale flukes were among the first natural markings on cetaceans to be recognized for their individual specificity, and the technique is now used worldwide in studies of population size and structure (Smith et al., 1999). Sperm whales also demonstrate much individual-specific variability in fluke edge features. Many identification features are visible only during surfacings, or are too subtle for real-time identification. Most individual identification research involves the collection of photographs for subsequent analysis, a process known as photo-identification. New imaging platforms, such as unmanned aerial systems, provide additional perspectives for individual identification and associated data. A hexacopter has been used to collect individual identification and photogrammetric data for killer whales (Durban et al., 2015) (Fig. 4). Photo-identification involves obtaining high-quality, highresolution, full-frame images of identifying features (Würsig and Jefferson, 1990). Photo-identification typically involves scientists in vessels or aircraft attempting to position themselves such that their lens is perpendicular to the feature of interest. Video or multiple images taken in quick succession optimize capturing fins, backs, or flukes at their greatest perpendicularity and height. Time, date, and geographic data associated with each image facilitate matching images and data records. Image storage, retrieval, and analysis techniques vary greatly across research situations, but the development of digital photography has greatly increased efficiency and decreased costs for image manipulation and storage. Historically, slides, prints, or negatives were labeled and stored chronologically, then examined under magnification through a handheld lupe or dissecting microscope. Digital
Identification Methods
505
Figure 4 (A) Overhead image of a killer whale (Orcinus orca) group taken from a hexacopter more than 30 m above the whales, with (B) a magnified inset showing the distinct pigmentation pattern of a whale's saddle patch that can be used to identify distinct individuals. This example displays the distinctive saddle patch of an adult female from the Northern resident killer whale population (Photo by Durban et al. (2015)). images increase capacity for manipulation, including cropping and enlarging identifying features, electronic storage, or transmission over the internet. Photographic quality and fin distinctiveness must be carefully controlled for the technique to be most effective (Urian et al., 2015). Digital images also facilitate computer-assisted automated analysis. Previously, photographic matches were made through the laborious process of individual comparison by eye of an image to all possible matches in a catalog of distinctive individuals. Software can now search thousands of images in a very short time to produce a limited set of potential matches. The research team can make the final match using the exceptional resolving capabilities of the human eye. Computer-assisted matching is becoming increasingly important as catalogs are now incorporating thousands of individuals, and as contributions to centralized regional catalogs are being made by numerous collaborating researchers (Hillman et al., 2003; Bas et al., 2005; Adams et al., 2006). Genetic markers from skin biopsy samples provide another kind of “natural marking.” Analyses of small samples allow determination of sex and individual identification from genotypes provided by microsatellite loci. This technique was developed for large-scale use during an ocean-basin-wide study of humpback whales, in which photographs were used to identify 2998 individual whales, and microsatellite loci were used to identify 2015 whales (Smith et al., 1999). Subsequent work with humpback whales has found that sloughed skin can provide larger samples than those from biopsy darts, the samples can be reliably assigned to individuals, the DNA is of high quality, and samples can be readily obtained from calves or others for which biopsy sampling is not allowed.
B. Temporary Markings Natural temporary markings include skin lesions and soft-bodied barnacles attached to dorsal fins. Temporary markings can distinguish among otherwise unmarked animals within a group, but their changeable nature make them less reliable for the long term. Skin lesions may take months to heal and disappear, but their characteristics change during healing. Soft-bodied barnacles favor fin tips, leading to low position variability, thus minimizing their value. Anthropogenic temporary markings are of limited utility (Scott et al., 1990). Remotely applied paint and tattoos tested with small cetaceans either did not yield reidentifications or they disappeared within 24 hr, from skin sloughing. Zinc oxide-based, brightly
I
Figure 5 A 12-year-old freeze brands (48) in the center of the dorsal fin and on the back of a 41-year-old bottlenose dolphin (Tursiops truncatus). The healed notch near the base of the fin is from a rototag applied 16 years before (Photo by Sarasota Dolphin Research Program).
colored sun protection ointments applied to dolphins’ dorsal fins have facilitated short-term identification.
C. Scarring and Branding Dorsal fin notching has been used with killer whales and smaller delphinids. Notching requires capture, providing opportunities to learn sex, age, and other biological information. Freeze branding, using metal numerals 5–8 cm high applied to the animals’ body or dorsal fin for 10–20 sec, has been used with a variety of small cetaceans. Application typically results in little or no reaction by dolphins, but minor skin lesions may occur if brands are applied for too long. Readable white marks usually appear within a few days (Fig. 5). Freeze brands may fade over time, but the marks can often still be identified for many years in good quality photographs even if they are not readily visible in the field (Irvine et al., 1982; Scott et al., 1990).
D. Attachment Tags The use of attachment tags for identification purposes (rather than telemetry, covered elsewhere in this volume) has been reviewed
506
I
Identification Methods
by Scott et al. (1990) and Loughlin et al. (2010). Discovery tags are numbered metal cylinders shot into the blubber, used primarily with baleen and sperm whales, and recovered when the whales were captured and rendered, yielding two points within the animals’ range. More than 20,000 discovery tags were deployed during 1932–85, with low return rates (<15%). Smaller versions have been used with small whales without notable success, and use with cetaceans less than 4.6-m long has been discouraged because of risk of serious injury. Streamer or spaghetti tags, originally developed for fish tagging, are colored vinyl-covered strands of wire cable of variable length with metal dart tips that are applied with either a crossbow or a jab stick, with the intent of anchoring the tip between blubber and muscle. Thousands of spaghetti tags were applied to dolphins, porpoises, and belugas, especially in association with the tuna seine net fishery in the eastern tropical Pacific Ocean. Because of poor retention and high risk of injury, spaghetti tag use has been discouraged (Irvine et al., 1982). Dorsal fins or ridges are commonly used for tag attachment because of their structure, prominence, and regularity of appearance above the water’s surface. Button tags, numbered and colored fiberglass or plastic disks or rectangular plates designed after the Peterson disk fish tags, have been applied during capture-release to several species of small cetaceans (Evans et al., 1972; Scott et al., 1990). Button tags are attached through the dorsal fin by one or more plastic (especially delrin) or stainless steel bolts or pins that connect the tag halves on each side of the fin. Although some button tags have lasted for several years on pelagic dolphins, inshore animals often lose the tags within weeks or months. Use of button tags has been largely discontinued due to poor tag retention and the potential for injury (Irvine et al., 1982). Small plastic livestock ear tags, or rototags, clipped through the trailing edges of dorsal fins have proved successful for identifying small cetaceans (Fig. 5; Scott et al., 1990). Typically, a small hole is made in the thin tissue of the trailing edge using sterile technique, and the tag is clipped through the fin with special pliers. Though the written markings are too small to be read at a distance, number of tags, color, and position on the fin provide a useful degree of variation. Rototags have remained in position for years, although often they are lost within months. Rototag halves may separate, leaving a healed hole in the fin, or they migrate through the trailing edge of the fin, leaving a small, healed notch; both pose minimal risks to the animals but offer continuing identification features. Barnacle and algae fouling, and pressure necrosis are infrequent problems. Tethers or plastic-coated wires, or polypropylene or soft rubber tubing, have proved ineffective and injurious when attached to the peduncle. Tag loss rates have been high, and abrasions were frequently noted.
II. Pinnipeds A. Natural Markings Natural body markings have been used in a variety of studies of pinnipeds. Yochem et al. (1990) examined pelage patterns of harbor (Phoca vitulina) and largha (P. largha) seals to distinguish between populations and individuals. Using black and white photographs they scored the presence or absence of spots, clarity of spots, relative density of spots, complexity of spots, presence of rings, and spacing of rings in selected body areas (especially sides of the head, neck, and chest). Computer-aided matching systems have been developed for screening digitized photographs of gray seals (Halichoerus grypus) (Hiby and Lovell, 1990), and pattern cells
or combinations of pattern cells from photographs of the ventrum, flank, shoulder, and/or head of harbor seals (Cunningham, 2009). The systems created a three-dimensional model to locate features on the seal’s body, especially using the side of the neck. Harting et al. (2004) devised a computer-assisted system for photo-identification of Hawaiian monk seals (Monachus schauinslandi). The use of whisker spot patterns for identifying pinnipeds, similar to the approach for computer-aided matching of polar bears (Ursus maritimus, Anderson et al., 2010), has not yet proved reliable. Studies using natural markings of many pinnipeds are hampered by a lack of distinctive markings, large numbers of individuals, or pack ice distributions.
B. Temporary Markings Temporary marking of pinnipeds involves paints, dyes, bleaches, and pelage clippings (Erickson et al., 1993). These can be used without having to restrain the animals and permit remote identification without disturbance. However, these marks are typically lost upon molting. A variety of paints have been used to mark seals and sea lions, applied from brushes or rollers on poles, and from plastic bags thrown at the animals. Quick-drying paint has proved relatively effective, with a useful lifespan of about 1 month. Northern fur seals (Callorhinus ursinus) have been marked for 2–12 months with a fluorescent plastic resin, naptha-based paint, matting guard hairs which then break off leaving an outline of the mark. Highgloss marine enamel applied from aerosol cans to mark Hooker’s sea lions (Phocarctas hookeri) has lasted for 3 months, even after trips to sea. CO2 powered paint guns firing small capsules have not been effective for marking elephant seals due to reliability problems and small mark size. Dyes have been used with success, especially with light-colored species (Erickson et al., 1993). Successful dying usually occurs with permanent dyes used when the animals are dry and remain so following application. Colored dyes and black Nyanzol D have lasted for 3–4 months on several species. Alcohol added to Nyanzol D leaves a more distinct marker because it dissolves fur oils, and also prevents dye solution freezing. Yellow picric acid in a saturated alcohol solution has been used with gray seals, lasting through pup molting, and appearing on the adults as well. This can be applied from a back-pack tree sprayer to wet or dry seals. Fluorescent dye mixed with small quantities of epoxy resin has also been used with success. In some cases, such as southern elephant seals (Mirounga leonina), dyes have been less successful. Bleach offers a very effective and sometimes longer-lasting alternative to paints and dyes (Erickson et al., 1993). Many of the bleach solutions can be applied to sleeping animals via a squeeze bottle, thus minimizing risk, effort, and disturbance. Commercially available products, such as Lady Clairol Ultra Blue dye in combination with various chemicals, have been used most often, leaving a white or cream-colored mark that is most visible on dark pelages. Bleach marks on elephant seals last until molt, and have lasted for two seasons on fur seals. Combinations of bleaches and dyes have also been used in some cases such as northern elephant seals (Fig. 6). Hair clipping is somewhat more difficult than the previous techniques, but effective when the underfur is a different color from the guard hairs (Erickson et al., 1993). This involves clipping or singeing the pelage to create a distinctive mark.
C. Scarring and Branding Punch marks and amputations have been used extensively with fur seals, with poor success and concerns about injury (Erickson
Identification Methods
Figure 6 Bleach markings on a northern elephant seal (Mirounga angustirostris). “Bilbo” is marked in black dye for identification through the summer molt and in bleach for the winter breeding season (Photo by C.J. Deutsch).
et al., 1993). Initial efforts to mark northern and Antarctic fur seals by punching holes in flippers in unique combinations of numbers and positions found this to be unreliable due to healing and occlusion. Hair on the flippers of phocid seals precludes utility with these species. Flipper notching was also found to be unreliable due to tissue regrowth. Although ear notching was used for cohort marking in northern fur seals, it is no longer used because of concerns regarding interference with diving abilities. Both hot and freeze branding have been used (Erickson et al., 1993). Hot brands have been used since 1912 with thousands of seals, with some marks remaining readable for up to 20 years. The technique seems best suited to colonial seals due to the bulky nature of the branding tools and heat source. Typically, brands are heated to red hot, and applied, ideally with gas anesthesia, with firm, even pressure for 2–7 sec, depending on whether the hair has been clipped. Correctly applied, hot brands on the fur and skin cause second-degree burns that kill the hair follicles and melanocytes, creating a permanent, bald, unpigmented mark, which may take years to heal completely (Loughlin et al., 2010). Brands are applied to the upper saddle, middle back, or upper shoulder to optimize sightability. Studies of Steller sea lions (Eumetopias jubatus) found that, after about 2 months, changes in health parameters following branding were consistent with minor tissue trauma and were indistinguishable from baseline levels (Mellish et al., 2007). Research on southern elephant seals and New Zealand sea lions (Phocarctos hookeri) found that neither short- nor long-term survival was adversely influenced by branding (McMahon et al., 2006; Wilkinson et al., 2011). Freeze branding selectively kills pigment-producing cells through contact with a super-cooled metal numeral or symbol (typically 5-cm high) (Erickson et al., 1993). Brands are cooled with liquid nitrogen or a dry ice and alcohol mixture and applied for about 20 sec to an area where hair has been removed. Correct freeze brand application leaves a nonpigmented pelage mark. Readable brands have been documented for elephant seals (up to a year), California sea lions (readable for 1.5 years), walrus (readable for many years), and Australian sea lions (Neophoca cinerea) (legible on flippers for 7 years, on flanks for 4 years). Many freeze brands have been found to repigment within 1–2 years, perhaps as a result of excessive branding.
507
Figure 7 Flipper tag on a northern elephant seal (Mirounga angustirostris) (Photo by B.J. LeBoeuf).
D. Attachment Tags Plastic or metal attachment tags are used more than any other kind of individual identification system with pinnipeds (Erickson et al., 1993). Monel or stainless steel tags, such as those used to mark livestock, are the most common metal tags. These metal strap tags are self-piercing and are attached by means of special pliers to the trailing edge of the foreflippers of otariids, and to the interdigital web of the hindflippers of phocids. Typically, the tags are stamped with an address and serial number. Thousands of metal tags have been attached to phocids, with poor retention rates and with tears and cuts sometimes becoming infected. Hundreds of thousands of metal tags have been attached to otariids, with similar poor results. The use of plastic tags is now much more common than metal tags (Fig. 7). Plastic livestock ear tags are commonly used. These consist of self-piercing male and female elements that are applied with special pliers. Plastic tags are available in a variety of colors, leading to hundreds of unique color combination possibilities. The visibility of both metal and plastic attachment tags can be enhanced using streamer markers such as nylon cloth strips reinforced with vinyl, which may last for a year or more. Utility of these techniques varies by species and age. Tagging success with both metal and plastic tags is less than desired. Loss rates of the two kinds of plastic tags are variable, but tend to be lower than for metal tags, about 10% annually. However, the long-term durability of metal tags is better than plastic. Wounds from metal tags are more common than from plastic; little evidence of plastic-tagging-related infections was found in a study with gray seal pups. Passive integrated transponder (PIT) tags, radiofrequency identification tags or implantable transponder tags, are small low-frequency computer chips encased in biocompatible material that can be injected under the skin, incorporated into external tags, or implanted into the body cavity. Each tag is programmed with an identification number that can be read by a scanner up to 1 m away. Subcutaneous PIT tags have been used with fur seals and sea lions; they are easy to apply, inexpensive, and can last the duration of an animal’s life (Loughlin et al., 2010).
III. Sirenians A. Natural Markings The process of developing new techniques and applying existing technology to studies of sirenians was reviewed in Wells et al.
I
508
Identification Methods chafing, break away if it should become snagged, and carry a floating very high frequency (VHF) or satellite-linked transmitter at the end of a tether. Transmitter floats are color coded for individual identification. The tethers can be replaced by swimmers. PIT tags, glass-encapsulated microchips, are about the size of a rice grain, have been implanted in many Florida manatees subcutaneously 3.5 cm deep, dorsal and caudal to the ear, and medial to the scapula. The tag is inserted in a small incision via a 12 gauge needle. Each is programmed with a unique identification code that is activated by a handheld scanner when it passes within 15 cm. PIT tags last for a long time, are reusable, rarely infect the animals, have an unlimited number of potential codes, and allow for easy data recording and transfer.
See Also the Following Articles Behavior, Overview Mark–Recapture
■
History of Marine Mammal Research
■
References Figure 8 Identifying scars from boat collisions on a Florida manatee (Trichechus manatus) (Photo by J.K. Koelsch).
I
(1999). Natural marks, including deformities and scars, have been used to identify individual Florida manatees (Trichechus manatus latirostris) since the 1950s. Images of scar patterns can be saved, cataloged, and searched with the assistance of computers.
B. Temporary Markings No widely accepted techniques currently exist for temporarily marking sirenians. Paint, flipper bands, and harnesses have been tested, but were not effective (Irvine and Scott, 1984). “Paintstiks,” oil-based crayon-like markers, have remained visible for 3–7 days, though rubbing eventually smears or removes them. Aerosol paint was short-lived, and application startled the animals and polluted the water.
C. Scarring and Branding Among the marks that have proven most useful are the scars from collisions with boats, especially propeller scars. Most manatees in Florida waters bear scars from boat collisions, often from more than one event. Boat scars mostly occur on the dorsal surface and paddle (Fig. 8). Scientists also can cut small notches in the paddles, with the positions around the paddle providing information on cohorts. Freeze branding has been used with catured or rehabilitated manatees with some success (Irvine and Scott, 1984). Though most brands fade with time, some have remained readable for up to 4 years. Success may vary with whether the manatees are shedding, as well as season, water temperature, and salinity.
D. Attachment Tags Sirenians provide few opportunities for tag attachment. Spaghetti tags have been tested, with 20-cm-long plastic streamer tags attached to a metal dart applied with either a lance or a crossbow, attempting to anchor the tag about 2 cm below the skin. These demonstrated poor retention, and caused abscesses on some manatees (Irvine and Scott, 1984). The most effective tag attachment involves a breakaway “belt” looped around the peduncle. This belt is designed to minimize
Adams, J.D., Speakman, T., Zolman, E., and Schwacke, L.H. (2006). “Automating image matching, cataloging, and analysis for photo-identification research.” Aquat. Mamm. 32, 374–384. Anderson, C.J.R., Da Vitoria Lobo, N., Roth, J.D., and Waterman, J.M. (2010). Computer-aided photo-identification system with an application to polar bears based on whisker spot patterns. J. Mammal. 91, 1350–1359. Bamford, C.C.G., and Robinson, K.P. (2016). An analysis of dorsal edge markings in short-beaked common dolphins (Delphinus delphis) from the Bay of Gibraltar and the Moray Firth. J. Mar. Biol. Assoc. UK. 96, 999–1004. Bas, W., Beekmans, P.M., Whitehead, H., Huele, R., Steiner, L., and Steenbeek, A.G. (2005). Comparison of two computer-assisted photo-identification methods applied to sperm whales (Physeter macrocephalus). Aquat. Mamm. 31, 243–247. Bigg, M. (1982). An assessment of killer whale (Orcinus orca) stocks off Vancouver Island, British Columbia. Rep. Int. Whal. Comm. 32, 655–666. Cunningham, L. (2009). Using computer-assisted photo-identification and capture-recapture techniques to monitor the conservation status of harbour seals (Phoca vitulina). Aquat. Mamm. 35, 319–329. Durban, J.W., Fearnbach, H., Barrett-Lennard, L.G., Perryman, W.L., and Leroi, D.J. (2015). Photogrammetry of killer whales using a small hexacopter launched at sea. J. Unmanned Veh. Syst. 3, 131–135. Erickson, A.W., Bester, M.N., and Laws, R.M. (1993). Marking techniques. In “Antarctic Seals” (R.M. Laws, Ed.), pp. 89–118. Cambridge University Press, Cambridge. Evans, W.E., Hall, J.D., Irvine, A.B., and Leatherwood, J.S. (1972). Methods for tagging small cetaceans. Fish. Bull. 70, 61–65. Hammond, P.S., Mizroch, S.A., and Donovan, G.P. (1990). Report of the workshop on individual recognition and the estimation of cetacean population parameters. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 3–17. Report of the International Whaling Commission, Cambridge, Special Issue 12. Harting, A., Baker, J., and Becker, B. (2004). Non-metrical digital photo-identification system for the Hawaiian monk seal. Mar. Mamm. Sci. 20, 886–895. Hillman, G.R., Wursig, B., Gailey, G., and Weller, D.W. (2003). Computer-assisted photo-identification of individual marine vertebrates: A multi-species system. Aquat. Mamm. 29, 117–123. Hiby, L., and Lovell, P. (1990). Computer aided matching of natural markings: A prototype system for grey seals. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond,
Indo-Pacific Beaked Whale S.A. Mizroch, and G.P. Donovan, Eds), pp. 57–61. Report of the International Whaling Commission, Cambridge, Special Issue 12. Irvine, A.B., and Scott, M.D. (1984). Development and use of marking techniques to study manatees in Florida. Fla Sci. 47, 12–26. Irvine, A.B., Wells, R.S., and Scott, M.D. (1982). An evaluation of techniques for tagging small odontocete cetaceans. Fish. Bull. 80, 135–143. Katona, S., Baxter, B., Brazer, O., Kraus, S., Perkins, J., and Whitehead, H. (1979). Identification of humpback whales from fluke photographs. In “Behavior of Marine Mammals—Current Perspectives in Research” (H.E. Winn, and B. Olla, Eds), pp. 33–44. Plenum Press, New York. Loughlin, T., Cunningham, L., Gales, N., Wells, R.S., and Boyd, I. (2010). Marking and capturing. In “Marine Mammal Ecology and Conservation: A Handbook of Techniques” (I. Boyd, D. Bowen, and S. Iverson, Eds), pp. 16-41. Oxford University Press, Oxford, UK. McMahon, C.R., Burton, H.R., van den Hoff, J., Woods, R., and Bradshaw, C.J.A. (2006). Assessing hot-iron and cryo-branding for permanently marking southern elephant seals. J. Wildlife Manage. 70, 1484–1489. Mellish, J.-A., Thornton, J., and Horning, M. (2007). Physiological and behavioral response to intra-abdominal transmitter implantation in Stellar sea lions. J. Exp. Mar. Biol. Ecol. 351, 283–293. Payne, R., Brazier, O., Dorsey, E.M., Perkins, J.S., Rowntree, V.J., and Titus, A. (1983). External features in southern right whales (Eubalaena australis) and their use in identifying individuals. In “Communication and Behavior of Whales” (R. Payne, Ed.), pp. 371–445. Westview Press, Boulder. Scott, M.D., Wells, R.S., Irvine, A.B., and Mate, B.R. (1990). Tagging and marking studies on small cetaceans. In “The Bottlenose Dolphin” (S. Leatherwood, and R.R. Reeves, Eds), pp. 489–514. Academic Press, San Diego. Smith, T.D., Allen, J., Clapham, P.J., Hammond, P.S., Katona, S., Larsen, F., et al. (1999). An ocean-basin-wide mark-recapture study of the North Atlantic humpback whale (Megaptera novaeangliae). Mar. Mamm. Sci. 15, 10–32. Urian, K., Read, A., Gorgone, A., Balmer, B., Wells, R., Berggren, P., and et al. (2015). Recommendations for photo-identification methods used in capture-recapture models with cetaceans. Mar. Mamm. Sci. 31, 298–321. Walker, K.A., Trites, A.W., Haulena, M., and Weary, D.M. (2012). A review of the effects of different marking and tagging techniques on marine mammals. Wildlife Res. 39, 15–30. Wells, R.S., Boness, D.J., and Rathbun, G.B. (1999). Behavior. In “Biology of Marine Mammals”, (J.E. Reynolds III, and S.A. Rommel, Eds) pp. 324–422. Smithsonian Institution Press, Washington, DC. Wilkinson, I.S., Chilvers, B.L., Duignan, P.J., and Pistorius, P.A. (2011). An evaluation of hot-iron branding as a permanent marking method for adult New Zealand sea lions, Phocarctos hookeri. Wildlife Res. 38, 51–60. Würsig, B., and Jefferson, T.A. (1990). Methods of photo-identification for small cetaceans. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 43–55. Report of the International Whaling Commission, Cambridge, Special Issue 12. Würsig, B., and Würsig, M. (1977). The photographic determination of group size, composition, and stability of coastal porpoises (Tursiops truncatus). Science. 198, 755–756. Yochem, P.K., Stewart, B.S., Mina, M., Zorin, A., Sadavov, V., and Tablakov, A. (1990). Non-metrical analyses of pelage patterns in demographic studies of harbor seals. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 87–90. Report of the International Whaling Commission, Cambridge, Special Issue 12.
509
INDO-PACIFIC BEAKED WHALE Indopacetus pacificus Robert Pitman The Indo-Pacific beaked whale is also called Longman’s beaked whale or the tropical bottlenose whale; it pertains to the Order Cetartiodactyla and the family Ziphiidae (Fig. 1). It is an uncommon ziphiid that lives in the tropical Indo-Pacific region (Fig. 2). Until recently, it was one of the least-known extant cetaceans.
I. Characteristics and Taxonomy Indopacetus pacificus was originally described by Longman (1926) as Mesoplodon pacificus from a beach-worn skull collected in Queensland, Australia, in 1882. The validity of the species was initially challenged by researchers who variously suggested that it was a subspecies of True’s beaked whale (Mesoplodon mirus) or an adult female southern bottlenose whale (Hyperoodon planifrons). These claims were refuted and the validity of the species confirmed by the discovery of a second skull from the coast of Somalia in 1955 (Azzaroli, 1968). After further study, Moore (1968) found it sufficiently distinct to warrant establishing a new genus: Indopacetus. These two skulls were the only evidence that this species existed until a series of at-sea sightings of an unidentified bottlenose whale from the tropical Indian and Pacific Oceans was compiled and analyzed. These sightings had previously been tentatively identified as southern bottlenose whales, but color pattern differences ruled out that identification and the suggestion was made that they could be I. pacificus (Pitman et al., 1999). This identification was subsequently confirmed by genetically matching stranded animals (that had previously been identified as H. planifrons) with the holotype of I. pacificus (Dalebout et al., 2003). This clarification has led to the identification of scores of at-sea sightings, and the distinctive I. pacificus has now become one of the more frequently identified beaked whales. Longman’s beaked whale is identified in the field as a relatively large (6–6.5 m) ziphiid with a prominent melon, a moderately long beak, a relatively large dorsal fin, and a subtle but distinctive color pattern (Fig. 1). Younger animals, including calves, are dark gray with a conspicuously pale head. The light color of the melon extends only as far back as the blowhole (this is important because in the otherwise similar-looking southern bottlenose whale the paleness on the melon extends 10 cm or so behind the blowhole). Much of the face, lower jaw and throat are also pale. Immediately posterior to the blowhole, the dark gray dorsal coloration extends ventrally to form a dark patch around the eye. This darkness continues ventrally and backward to the insertion of the flipper, forming a broad band. There is a small, white “ear spot” embedded in the dark area behind the eye. Immediately posterior to the dark flipper band, and setting it off, is a large white area formed by the white from the ventrum extending high up on the sides of the animal. Calves are similar to adults except that the paleness of the melon, ventrum, and thoracic area is more pronounced; the head of the adults appears to darken with age. Adults also have a relatively longer beak and they are often heavily scarred. Adult females appear gray-brown in good light; males are similarly colored but often appear lighter than females due, at least in part, to an accumulation of scars from tooth rake marks by other males. Females have few or none of the linear (tooth rake) scars found on adult males,
I
I IDENTIFICATION METHODS Randall S. Wells Individual identification is an important tool for studies of animal behavior, ecology, and population biology. Much can be learned from recognition of individuals within a population or social unit, or from tracking individuals through time. Repeated observations of a recognizable individual can help to define its ranging patterns, or to quantify habitat use. Individual identification is essential to understanding group compositions, especially when the individual’s sex, age, genetic relationships, and reproductive conditions are known. Similarly, interpretation of social interactions requires the ability to distinguish among the players. Behavioral descriptions often involve measuring rates of occurrence of behaviors. These rates are measured most accurately when a selected individual is followed through time, or when its behaviors are recorded at predetermined intervals, as with focal animal behavioral observations. Descriptions of life history patterns and empirical measures of population dynamics benefit from individual identification. By following individuals through time it is possible to determine age at sexual maturity, calving intervals, calf survivorship, and lifespan, providing measures of reproductive success. Combined, such individual measures can provide population-level vital rates, including birth rates, mortality rates, and recruitment. Mark-recapture techniques use individual identification to arrive at abundance estimates. Individual identification provides one of the best tools for documenting exchanges of individuals between populations, allowing estimation of immigration and emigration rates. Identification technique selection depends on the research questions being addressed and the species under study. Frequent monitoring of individuals may require identification from a distance, whereas other studies may only need to recognize an animal when it is handled subsequently, alive or at the end of its life. Some species exhibit individually specific natural markings. Other species lack such markings and require the attachment of artificial marks, or tags. Some species are visible on land at times, whereas others are entirely aquatic. Morphological, behavioral, and ecological features guide tag and attachment selection, relative to safety for the animal and effectiveness for the research. It is now possible to collect small tissue samples that allow the identification of individuals genetically. Individual identification techniques have been summarized for cetaceans, pinnipeds, and sirenians (Hammond et al., 1990; Scott et al., 1990; Würsig and Jefferson, 1990; Erickson et al., 1993; Wells et al., 1999; Loughlin et al., 2010). Walker et al. (2012) reviewed the effects of marking and tagging on marine mammals. They noted that while some marking techniques were reported to cause pain and to change swimming and haulout behavior, maternal attendance, and duration of foraging Encyclopedia of Marine Mammals. DOI: http://dx.doi.org/10.1016/B978-0-12-804327-1.00009-1 © 2018 Elsevier Inc. All rights reserved.
trips, marking typically does not affect survival. They further noted that more evaluation is needed of the possible acute effects of marking, including the potential for pain and distress, and to better understand the potential for long-term effects on health and disease, growth, and reproduction.
I. Cetaceans A. Natural Markings Cetaceans exhibit a variety of individually distinctive natural features. Typically, features appearing above the surface during breaths are most useful. In particular, heads, backs, dorsal fins, and flukes offer variations in color patterns, skin patches, body scarring, and/or nicks and notches. Some individuals of most species acquire distinctive scars from wounds or injuries. Perhaps the most unique cetacean identification features are the callosities of right whales, Eubalaena spp. (Payne et al., 1983). These individually distinctive raised patches of roughened skin are present on the rostrum anterior to the blowholes in a pattern referred to as the bonnet, on the chin, lower lips, above the eyes, and near the blowholes. Whale lice (Cyamus spp.), cyamid crustaceans that live on the callosities, give them a white, orange, yellow, or pink appearance. Callosities have provided reliable recognition of individuals over decades. Color variations, where they exist among cetacean species, have been used with much success for individual identification, especially among the mysticetes. Blue whales (Balaenoptera musculus) and gray whales (Eschrichtius robustus) exhibit individually distinctive dorsal mottling (Fig. 1). Pigmentation on sperm whale flanks (Physeter macrocephalus) has proved to be a reliable identification feature. Bowhead whales (Balaena mysticetus) often have a distinctive white pigmentation on the chin and/or peduncle. Fin whales (Balaenoptera physalus) exhibit strongly asymmetrical pigmentation, with both lips and the first third of the baleen on the right side appearing white or pale gray. A light-colored “blaze” sweeps back on the right side, and a V-shaped light-colored “chevron” occurs on both sides behind the blowhole. Minke whales (Balaenoptera spp.) exhibit a pattern of pale lateral pigmentation on the body, often in three distinct swaths, with the relative brightness varying consistently between Northern and Southern Hemispheres. The distinctive dark and white patterns of the flippers and ventral surface of the flukes are familiar identification features for humpback whales (Megaptera novaeangliae) (Katona et al., 1979). Some of the smaller cetaceans also exhibit individually distinctive color variations. Most notable are the light-colored saddle patches behind the dorsal fin of the killer whale (Orcinus orca), which differ in size and shape. The saddle marks of pilot whales (Globicephala spp.) are less distinct. Dorsal fin and/or back pigmentation variation has proven effective with a variety of dolphins and porpoises, and facial color patterns were used to identify the now-extinct baiji (Lipotes vexillifer). Extensive speckling develops with age in spotted dolphins, facilitating individual identification from both above and below the surface in behavioral studies of Stenella frontalis.
I
504
Identification Methods
Figure 1 Distinctive color patterns of a blue whale (Balaenoptera musculus) (Photo by R.S. Wells).
I
Figure 2 Killer whale dorsal fins and saddle patches provide reliable identification cues (Photo by RS. Wells). Scarring can create useful pigment variations. Risso’s dolphins acquire distinctive long-term white scars on their otherwise brown or gray bodies, and belugas (Delphinapterus leucas) acquire dark scars on their otherwise white bodies. In the Mediterranean sea, 71% of Cuvier’s beaked whale males (Ziphius cavirostris) are reliably marked, with males acquiring significantly more marks than females, through conspecific interactions. Bottlenose dolphin (Tursiops spp.) scars on the dorsal fin often are white, in contrast to their general gray coloration. Cookie cutter shark (Isistius spp.) bite wounds leave permanent small diameter oval-shaped scars which are often depressed and pigmented differently from the rest of many pelagic cetaceans’ bodies; these have been used to identify individuals of a variety of species. Dorsal fins are visible to researchers during most surfacings. In many species, dorsal fins develop distinctive shapes or acquire nicks and notches, often through intra- or interspecific interactions that allow for individual identification. For example, male dusky dolphins (Lagenorhynchus obscurus) had significantly more conspecific-acquired dorsal fin markings than females. Among the larger whales, fin, sei (Balaenoptera borealis), Bryde’s (B. edeni), minke, humpback, and sperm whale dorsal fins serve as useful identification features. Building on the pioneering work of Bigg (1982) with killer whales (Fig. 2) and Würsig and Würsig (1977) with bottlenose dolphins, studies based on dorsal fin identifications of various small cetaceans have blossomed (Hammond et al., 1990; Scott et al., 1990; Würsig and Jefferson, 1990; Wells et al., 1999). The
Figure 3 Distinctive dark and light patterns on the ventral surface of a humpback whale’s (Megaptera novaeangliae) fluke (Photo by R.S. Wells).
frequency of occurrence of distinctive fin features varies across species, and sometimes across populations. Off Florida, 60%–80% of bottlenose dolphins have distinctive dorsal fins. Unlike color patterns that vary from one side to the other, dorsal fin nicks and notches are equally visible from both sides and are distinctive under a broad range of lighting conditions. As suggested by Bamford and Robinson (2016) for short-beaked common dolphins (Delphinus delphis), dorsal edge markings and/or injuries may provide an indication of the nature of fisheries interactions affecting specific populations. Some species regularly lift their flukes from the water prior to a dive, providing predictable opportunities to record the occurrence of nicks, notches, and other features on the trailing edge of the flukes. Humpback whales offer both distinctive color patterns and trailing edge features (Fig. 3). Humpback whale flukes were among the first natural markings on cetaceans to be recognized for their individual specificity, and the technique is now used worldwide in studies of population size and structure (Smith et al., 1999). Sperm whales also demonstrate much individual-specific variability in fluke edge features. Many identification features are visible only during surfacings, or are too subtle for real-time identification. Most individual identification research involves the collection of photographs for subsequent analysis, a process known as photo-identification. New imaging platforms, such as unmanned aerial systems, provide additional perspectives for individual identification and associated data. A hexacopter has been used to collect individual identification and photogrammetric data for killer whales (Durban et al., 2015) (Fig. 4). Photo-identification involves obtaining high-quality, highresolution, full-frame images of identifying features (Würsig and Jefferson, 1990). Photo-identification typically involves scientists in vessels or aircraft attempting to position themselves such that their lens is perpendicular to the feature of interest. Video or multiple images taken in quick succession optimize capturing fins, backs, or flukes at their greatest perpendicularity and height. Time, date, and geographic data associated with each image facilitate matching images and data records. Image storage, retrieval, and analysis techniques vary greatly across research situations, but the development of digital photography has greatly increased efficiency and decreased costs for image manipulation and storage. Historically, slides, prints, or negatives were labeled and stored chronologically, then examined under magnification through a handheld lupe or dissecting microscope. Digital
Identification Methods
505
Figure 4 (A) Overhead image of a killer whale (Orcinus orca) group taken from a hexacopter more than 30 m above the whales, with (B) a magnified inset showing the distinct pigmentation pattern of a whale's saddle patch that can be used to identify distinct individuals. This example displays the distinctive saddle patch of an adult female from the Northern resident killer whale population (Photo by Durban et al. (2015)). images increase capacity for manipulation, including cropping and enlarging identifying features, electronic storage, or transmission over the internet. Photographic quality and fin distinctiveness must be carefully controlled for the technique to be most effective (Urian et al., 2015). Digital images also facilitate computer-assisted automated analysis. Previously, photographic matches were made through the laborious process of individual comparison by eye of an image to all possible matches in a catalog of distinctive individuals. Software can now search thousands of images in a very short time to produce a limited set of potential matches. The research team can make the final match using the exceptional resolving capabilities of the human eye. Computer-assisted matching is becoming increasingly important as catalogs are now incorporating thousands of individuals, and as contributions to centralized regional catalogs are being made by numerous collaborating researchers (Hillman et al., 2003; Bas et al., 2005; Adams et al., 2006). Genetic markers from skin biopsy samples provide another kind of “natural marking.” Analyses of small samples allow determination of sex and individual identification from genotypes provided by microsatellite loci. This technique was developed for large-scale use during an ocean-basin-wide study of humpback whales, in which photographs were used to identify 2998 individual whales, and microsatellite loci were used to identify 2015 whales (Smith et al., 1999). Subsequent work with humpback whales has found that sloughed skin can provide larger samples than those from biopsy darts, the samples can be reliably assigned to individuals, the DNA is of high quality, and samples can be readily obtained from calves or others for which biopsy sampling is not allowed.
B. Temporary Markings Natural temporary markings include skin lesions and soft-bodied barnacles attached to dorsal fins. Temporary markings can distinguish among otherwise unmarked animals within a group, but their changeable nature make them less reliable for the long term. Skin lesions may take months to heal and disappear, but their characteristics change during healing. Soft-bodied barnacles favor fin tips, leading to low position variability, thus minimizing their value. Anthropogenic temporary markings are of limited utility (Scott et al., 1990). Remotely applied paint and tattoos tested with small cetaceans either did not yield reidentifications or they disappeared within 24 hr, from skin sloughing. Zinc oxide-based, brightly
I
Figure 5 A 12-year-old freeze brands (48) in the center of the dorsal fin and on the back of a 41-year-old bottlenose dolphin (Tursiops truncatus). The healed notch near the base of the fin is from a rototag applied 16 years before (Photo by Sarasota Dolphin Research Program).
colored sun protection ointments applied to dolphins’ dorsal fins have facilitated short-term identification.
C. Scarring and Branding Dorsal fin notching has been used with killer whales and smaller delphinids. Notching requires capture, providing opportunities to learn sex, age, and other biological information. Freeze branding, using metal numerals 5–8 cm high applied to the animals’ body or dorsal fin for 10–20 sec, has been used with a variety of small cetaceans. Application typically results in little or no reaction by dolphins, but minor skin lesions may occur if brands are applied for too long. Readable white marks usually appear within a few days (Fig. 5). Freeze brands may fade over time, but the marks can often still be identified for many years in good quality photographs even if they are not readily visible in the field (Irvine et al., 1982; Scott et al., 1990).
D. Attachment Tags The use of attachment tags for identification purposes (rather than telemetry, covered elsewhere in this volume) has been reviewed
506
I
Identification Methods
by Scott et al. (1990) and Loughlin et al. (2010). Discovery tags are numbered metal cylinders shot into the blubber, used primarily with baleen and sperm whales, and recovered when the whales were captured and rendered, yielding two points within the animals’ range. More than 20,000 discovery tags were deployed during 1932–85, with low return rates (<15%). Smaller versions have been used with small whales without notable success, and use with cetaceans less than 4.6-m long has been discouraged because of risk of serious injury. Streamer or spaghetti tags, originally developed for fish tagging, are colored vinyl-covered strands of wire cable of variable length with metal dart tips that are applied with either a crossbow or a jab stick, with the intent of anchoring the tip between blubber and muscle. Thousands of spaghetti tags were applied to dolphins, porpoises, and belugas, especially in association with the tuna seine net fishery in the eastern tropical Pacific Ocean. Because of poor retention and high risk of injury, spaghetti tag use has been discouraged (Irvine et al., 1982). Dorsal fins or ridges are commonly used for tag attachment because of their structure, prominence, and regularity of appearance above the water’s surface. Button tags, numbered and colored fiberglass or plastic disks or rectangular plates designed after the Peterson disk fish tags, have been applied during capture-release to several species of small cetaceans (Evans et al., 1972; Scott et al., 1990). Button tags are attached through the dorsal fin by one or more plastic (especially delrin) or stainless steel bolts or pins that connect the tag halves on each side of the fin. Although some button tags have lasted for several years on pelagic dolphins, inshore animals often lose the tags within weeks or months. Use of button tags has been largely discontinued due to poor tag retention and the potential for injury (Irvine et al., 1982). Small plastic livestock ear tags, or rototags, clipped through the trailing edges of dorsal fins have proved successful for identifying small cetaceans (Fig. 5; Scott et al., 1990). Typically, a small hole is made in the thin tissue of the trailing edge using sterile technique, and the tag is clipped through the fin with special pliers. Though the written markings are too small to be read at a distance, number of tags, color, and position on the fin provide a useful degree of variation. Rototags have remained in position for years, although often they are lost within months. Rototag halves may separate, leaving a healed hole in the fin, or they migrate through the trailing edge of the fin, leaving a small, healed notch; both pose minimal risks to the animals but offer continuing identification features. Barnacle and algae fouling, and pressure necrosis are infrequent problems. Tethers or plastic-coated wires, or polypropylene or soft rubber tubing, have proved ineffective and injurious when attached to the peduncle. Tag loss rates have been high, and abrasions were frequently noted.
II. Pinnipeds A. Natural Markings Natural body markings have been used in a variety of studies of pinnipeds. Yochem et al. (1990) examined pelage patterns of harbor (Phoca vitulina) and largha (P. largha) seals to distinguish between populations and individuals. Using black and white photographs they scored the presence or absence of spots, clarity of spots, relative density of spots, complexity of spots, presence of rings, and spacing of rings in selected body areas (especially sides of the head, neck, and chest). Computer-aided matching systems have been developed for screening digitized photographs of gray seals (Halichoerus grypus) (Hiby and Lovell, 1990), and pattern cells
or combinations of pattern cells from photographs of the ventrum, flank, shoulder, and/or head of harbor seals (Cunningham, 2009). The systems created a three-dimensional model to locate features on the seal’s body, especially using the side of the neck. Harting et al. (2004) devised a computer-assisted system for photo-identification of Hawaiian monk seals (Monachus schauinslandi). The use of whisker spot patterns for identifying pinnipeds, similar to the approach for computer-aided matching of polar bears (Ursus maritimus, Anderson et al., 2010), has not yet proved reliable. Studies using natural markings of many pinnipeds are hampered by a lack of distinctive markings, large numbers of individuals, or pack ice distributions.
B. Temporary Markings Temporary marking of pinnipeds involves paints, dyes, bleaches, and pelage clippings (Erickson et al., 1993). These can be used without having to restrain the animals and permit remote identification without disturbance. However, these marks are typically lost upon molting. A variety of paints have been used to mark seals and sea lions, applied from brushes or rollers on poles, and from plastic bags thrown at the animals. Quick-drying paint has proved relatively effective, with a useful lifespan of about 1 month. Northern fur seals (Callorhinus ursinus) have been marked for 2–12 months with a fluorescent plastic resin, naptha-based paint, matting guard hairs which then break off leaving an outline of the mark. Highgloss marine enamel applied from aerosol cans to mark Hooker’s sea lions (Phocarctas hookeri) has lasted for 3 months, even after trips to sea. CO2 powered paint guns firing small capsules have not been effective for marking elephant seals due to reliability problems and small mark size. Dyes have been used with success, especially with light-colored species (Erickson et al., 1993). Successful dying usually occurs with permanent dyes used when the animals are dry and remain so following application. Colored dyes and black Nyanzol D have lasted for 3–4 months on several species. Alcohol added to Nyanzol D leaves a more distinct marker because it dissolves fur oils, and also prevents dye solution freezing. Yellow picric acid in a saturated alcohol solution has been used with gray seals, lasting through pup molting, and appearing on the adults as well. This can be applied from a back-pack tree sprayer to wet or dry seals. Fluorescent dye mixed with small quantities of epoxy resin has also been used with success. In some cases, such as southern elephant seals (Mirounga leonina), dyes have been less successful. Bleach offers a very effective and sometimes longer-lasting alternative to paints and dyes (Erickson et al., 1993). Many of the bleach solutions can be applied to sleeping animals via a squeeze bottle, thus minimizing risk, effort, and disturbance. Commercially available products, such as Lady Clairol Ultra Blue dye in combination with various chemicals, have been used most often, leaving a white or cream-colored mark that is most visible on dark pelages. Bleach marks on elephant seals last until molt, and have lasted for two seasons on fur seals. Combinations of bleaches and dyes have also been used in some cases such as northern elephant seals (Fig. 6). Hair clipping is somewhat more difficult than the previous techniques, but effective when the underfur is a different color from the guard hairs (Erickson et al., 1993). This involves clipping or singeing the pelage to create a distinctive mark.
C. Scarring and Branding Punch marks and amputations have been used extensively with fur seals, with poor success and concerns about injury (Erickson
Identification Methods
Figure 6 Bleach markings on a northern elephant seal (Mirounga angustirostris). “Bilbo” is marked in black dye for identification through the summer molt and in bleach for the winter breeding season (Photo by C.J. Deutsch).
et al., 1993). Initial efforts to mark northern and Antarctic fur seals by punching holes in flippers in unique combinations of numbers and positions found this to be unreliable due to healing and occlusion. Hair on the flippers of phocid seals precludes utility with these species. Flipper notching was also found to be unreliable due to tissue regrowth. Although ear notching was used for cohort marking in northern fur seals, it is no longer used because of concerns regarding interference with diving abilities. Both hot and freeze branding have been used (Erickson et al., 1993). Hot brands have been used since 1912 with thousands of seals, with some marks remaining readable for up to 20 years. The technique seems best suited to colonial seals due to the bulky nature of the branding tools and heat source. Typically, brands are heated to red hot, and applied, ideally with gas anesthesia, with firm, even pressure for 2–7 sec, depending on whether the hair has been clipped. Correctly applied, hot brands on the fur and skin cause second-degree burns that kill the hair follicles and melanocytes, creating a permanent, bald, unpigmented mark, which may take years to heal completely (Loughlin et al., 2010). Brands are applied to the upper saddle, middle back, or upper shoulder to optimize sightability. Studies of Steller sea lions (Eumetopias jubatus) found that, after about 2 months, changes in health parameters following branding were consistent with minor tissue trauma and were indistinguishable from baseline levels (Mellish et al., 2007). Research on southern elephant seals and New Zealand sea lions (Phocarctos hookeri) found that neither short- nor long-term survival was adversely influenced by branding (McMahon et al., 2006; Wilkinson et al., 2011). Freeze branding selectively kills pigment-producing cells through contact with a super-cooled metal numeral or symbol (typically 5-cm high) (Erickson et al., 1993). Brands are cooled with liquid nitrogen or a dry ice and alcohol mixture and applied for about 20 sec to an area where hair has been removed. Correct freeze brand application leaves a nonpigmented pelage mark. Readable brands have been documented for elephant seals (up to a year), California sea lions (readable for 1.5 years), walrus (readable for many years), and Australian sea lions (Neophoca cinerea) (legible on flippers for 7 years, on flanks for 4 years). Many freeze brands have been found to repigment within 1–2 years, perhaps as a result of excessive branding.
507
Figure 7 Flipper tag on a northern elephant seal (Mirounga angustirostris) (Photo by B.J. LeBoeuf).
D. Attachment Tags Plastic or metal attachment tags are used more than any other kind of individual identification system with pinnipeds (Erickson et al., 1993). Monel or stainless steel tags, such as those used to mark livestock, are the most common metal tags. These metal strap tags are self-piercing and are attached by means of special pliers to the trailing edge of the foreflippers of otariids, and to the interdigital web of the hindflippers of phocids. Typically, the tags are stamped with an address and serial number. Thousands of metal tags have been attached to phocids, with poor retention rates and with tears and cuts sometimes becoming infected. Hundreds of thousands of metal tags have been attached to otariids, with similar poor results. The use of plastic tags is now much more common than metal tags (Fig. 7). Plastic livestock ear tags are commonly used. These consist of self-piercing male and female elements that are applied with special pliers. Plastic tags are available in a variety of colors, leading to hundreds of unique color combination possibilities. The visibility of both metal and plastic attachment tags can be enhanced using streamer markers such as nylon cloth strips reinforced with vinyl, which may last for a year or more. Utility of these techniques varies by species and age. Tagging success with both metal and plastic tags is less than desired. Loss rates of the two kinds of plastic tags are variable, but tend to be lower than for metal tags, about 10% annually. However, the long-term durability of metal tags is better than plastic. Wounds from metal tags are more common than from plastic; little evidence of plastic-tagging-related infections was found in a study with gray seal pups. Passive integrated transponder (PIT) tags, radiofrequency identification tags or implantable transponder tags, are small low-frequency computer chips encased in biocompatible material that can be injected under the skin, incorporated into external tags, or implanted into the body cavity. Each tag is programmed with an identification number that can be read by a scanner up to 1 m away. Subcutaneous PIT tags have been used with fur seals and sea lions; they are easy to apply, inexpensive, and can last the duration of an animal’s life (Loughlin et al., 2010).
III. Sirenians A. Natural Markings The process of developing new techniques and applying existing technology to studies of sirenians was reviewed in Wells et al.
I
508
Identification Methods chafing, break away if it should become snagged, and carry a floating very high frequency (VHF) or satellite-linked transmitter at the end of a tether. Transmitter floats are color coded for individual identification. The tethers can be replaced by swimmers. PIT tags, glass-encapsulated microchips, are about the size of a rice grain, have been implanted in many Florida manatees subcutaneously 3.5 cm deep, dorsal and caudal to the ear, and medial to the scapula. The tag is inserted in a small incision via a 12 gauge needle. Each is programmed with a unique identification code that is activated by a handheld scanner when it passes within 15 cm. PIT tags last for a long time, are reusable, rarely infect the animals, have an unlimited number of potential codes, and allow for easy data recording and transfer.
See Also the Following Articles Behavior, Overview Mark–Recapture
■
History of Marine Mammal Research
■
References Figure 8 Identifying scars from boat collisions on a Florida manatee (Trichechus manatus) (Photo by J.K. Koelsch).
I
(1999). Natural marks, including deformities and scars, have been used to identify individual Florida manatees (Trichechus manatus latirostris) since the 1950s. Images of scar patterns can be saved, cataloged, and searched with the assistance of computers.
B. Temporary Markings No widely accepted techniques currently exist for temporarily marking sirenians. Paint, flipper bands, and harnesses have been tested, but were not effective (Irvine and Scott, 1984). “Paintstiks,” oil-based crayon-like markers, have remained visible for 3–7 days, though rubbing eventually smears or removes them. Aerosol paint was short-lived, and application startled the animals and polluted the water.
C. Scarring and Branding Among the marks that have proven most useful are the scars from collisions with boats, especially propeller scars. Most manatees in Florida waters bear scars from boat collisions, often from more than one event. Boat scars mostly occur on the dorsal surface and paddle (Fig. 8). Scientists also can cut small notches in the paddles, with the positions around the paddle providing information on cohorts. Freeze branding has been used with catured or rehabilitated manatees with some success (Irvine and Scott, 1984). Though most brands fade with time, some have remained readable for up to 4 years. Success may vary with whether the manatees are shedding, as well as season, water temperature, and salinity.
D. Attachment Tags Sirenians provide few opportunities for tag attachment. Spaghetti tags have been tested, with 20-cm-long plastic streamer tags attached to a metal dart applied with either a lance or a crossbow, attempting to anchor the tag about 2 cm below the skin. These demonstrated poor retention, and caused abscesses on some manatees (Irvine and Scott, 1984). The most effective tag attachment involves a breakaway “belt” looped around the peduncle. This belt is designed to minimize
Adams, J.D., Speakman, T., Zolman, E., and Schwacke, L.H. (2006). “Automating image matching, cataloging, and analysis for photo-identification research.” Aquat. Mamm. 32, 374–384. Anderson, C.J.R., Da Vitoria Lobo, N., Roth, J.D., and Waterman, J.M. (2010). Computer-aided photo-identification system with an application to polar bears based on whisker spot patterns. J. Mammal. 91, 1350–1359. Bamford, C.C.G., and Robinson, K.P. (2016). An analysis of dorsal edge markings in short-beaked common dolphins (Delphinus delphis) from the Bay of Gibraltar and the Moray Firth. J. Mar. Biol. Assoc. UK. 96, 999–1004. Bas, W., Beekmans, P.M., Whitehead, H., Huele, R., Steiner, L., and Steenbeek, A.G. (2005). Comparison of two computer-assisted photo-identification methods applied to sperm whales (Physeter macrocephalus). Aquat. Mamm. 31, 243–247. Bigg, M. (1982). An assessment of killer whale (Orcinus orca) stocks off Vancouver Island, British Columbia. Rep. Int. Whal. Comm. 32, 655–666. Cunningham, L. (2009). Using computer-assisted photo-identification and capture-recapture techniques to monitor the conservation status of harbour seals (Phoca vitulina). Aquat. Mamm. 35, 319–329. Durban, J.W., Fearnbach, H., Barrett-Lennard, L.G., Perryman, W.L., and Leroi, D.J. (2015). Photogrammetry of killer whales using a small hexacopter launched at sea. J. Unmanned Veh. Syst. 3, 131–135. Erickson, A.W., Bester, M.N., and Laws, R.M. (1993). Marking techniques. In “Antarctic Seals” (R.M. Laws, Ed.), pp. 89–118. Cambridge University Press, Cambridge. Evans, W.E., Hall, J.D., Irvine, A.B., and Leatherwood, J.S. (1972). Methods for tagging small cetaceans. Fish. Bull. 70, 61–65. Hammond, P.S., Mizroch, S.A., and Donovan, G.P. (1990). Report of the workshop on individual recognition and the estimation of cetacean population parameters. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 3–17. Report of the International Whaling Commission, Cambridge, Special Issue 12. Harting, A., Baker, J., and Becker, B. (2004). Non-metrical digital photo-identification system for the Hawaiian monk seal. Mar. Mamm. Sci. 20, 886–895. Hillman, G.R., Wursig, B., Gailey, G., and Weller, D.W. (2003). Computer-assisted photo-identification of individual marine vertebrates: A multi-species system. Aquat. Mamm. 29, 117–123. Hiby, L., and Lovell, P. (1990). Computer aided matching of natural markings: A prototype system for grey seals. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond,
Indo-Pacific Beaked Whale S.A. Mizroch, and G.P. Donovan, Eds), pp. 57–61. Report of the International Whaling Commission, Cambridge, Special Issue 12. Irvine, A.B., and Scott, M.D. (1984). Development and use of marking techniques to study manatees in Florida. Fla Sci. 47, 12–26. Irvine, A.B., Wells, R.S., and Scott, M.D. (1982). An evaluation of techniques for tagging small odontocete cetaceans. Fish. Bull. 80, 135–143. Katona, S., Baxter, B., Brazer, O., Kraus, S., Perkins, J., and Whitehead, H. (1979). Identification of humpback whales from fluke photographs. In “Behavior of Marine Mammals—Current Perspectives in Research” (H.E. Winn, and B. Olla, Eds), pp. 33–44. Plenum Press, New York. Loughlin, T., Cunningham, L., Gales, N., Wells, R.S., and Boyd, I. (2010). Marking and capturing. In “Marine Mammal Ecology and Conservation: A Handbook of Techniques” (I. Boyd, D. Bowen, and S. Iverson, Eds), pp. 16-41. Oxford University Press, Oxford, UK. McMahon, C.R., Burton, H.R., van den Hoff, J., Woods, R., and Bradshaw, C.J.A. (2006). Assessing hot-iron and cryo-branding for permanently marking southern elephant seals. J. Wildlife Manage. 70, 1484–1489. Mellish, J.-A., Thornton, J., and Horning, M. (2007). Physiological and behavioral response to intra-abdominal transmitter implantation in Stellar sea lions. J. Exp. Mar. Biol. Ecol. 351, 283–293. Payne, R., Brazier, O., Dorsey, E.M., Perkins, J.S., Rowntree, V.J., and Titus, A. (1983). External features in southern right whales (Eubalaena australis) and their use in identifying individuals. In “Communication and Behavior of Whales” (R. Payne, Ed.), pp. 371–445. Westview Press, Boulder. Scott, M.D., Wells, R.S., Irvine, A.B., and Mate, B.R. (1990). Tagging and marking studies on small cetaceans. In “The Bottlenose Dolphin” (S. Leatherwood, and R.R. Reeves, Eds), pp. 489–514. Academic Press, San Diego. Smith, T.D., Allen, J., Clapham, P.J., Hammond, P.S., Katona, S., Larsen, F., et al. (1999). An ocean-basin-wide mark-recapture study of the North Atlantic humpback whale (Megaptera novaeangliae). Mar. Mamm. Sci. 15, 10–32. Urian, K., Read, A., Gorgone, A., Balmer, B., Wells, R., Berggren, P., and et al. (2015). Recommendations for photo-identification methods used in capture-recapture models with cetaceans. Mar. Mamm. Sci. 31, 298–321. Walker, K.A., Trites, A.W., Haulena, M., and Weary, D.M. (2012). A review of the effects of different marking and tagging techniques on marine mammals. Wildlife Res. 39, 15–30. Wells, R.S., Boness, D.J., and Rathbun, G.B. (1999). Behavior. In “Biology of Marine Mammals”, (J.E. Reynolds III, and S.A. Rommel, Eds) pp. 324–422. Smithsonian Institution Press, Washington, DC. Wilkinson, I.S., Chilvers, B.L., Duignan, P.J., and Pistorius, P.A. (2011). An evaluation of hot-iron branding as a permanent marking method for adult New Zealand sea lions, Phocarctos hookeri. Wildlife Res. 38, 51–60. Würsig, B., and Jefferson, T.A. (1990). Methods of photo-identification for small cetaceans. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 43–55. Report of the International Whaling Commission, Cambridge, Special Issue 12. Würsig, B., and Würsig, M. (1977). The photographic determination of group size, composition, and stability of coastal porpoises (Tursiops truncatus). Science. 198, 755–756. Yochem, P.K., Stewart, B.S., Mina, M., Zorin, A., Sadavov, V., and Tablakov, A. (1990). Non-metrical analyses of pelage patterns in demographic studies of harbor seals. In “Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters” (P.S. Hammond, S.A. Mizroch, and G.P. Donovan, Eds), pp. 87–90. Report of the International Whaling Commission, Cambridge, Special Issue 12.
509
INDO-PACIFIC BEAKED WHALE Indopacetus pacificus Robert Pitman The Indo-Pacific beaked whale is also called Longman’s beaked whale or the tropical bottlenose whale; it pertains to the Order Cetartiodactyla and the family Ziphiidae (Fig. 1). It is an uncommon ziphiid that lives in the tropical Indo-Pacific region (Fig. 2). Until recently, it was one of the least-known extant cetaceans.
I. Characteristics and Taxonomy Indopacetus pacificus was originally described by Longman (1926) as Mesoplodon pacificus from a beach-worn skull collected in Queensland, Australia, in 1882. The validity of the species was initially challenged by researchers who variously suggested that it was a subspecies of True’s beaked whale (Mesoplodon mirus) or an adult female southern bottlenose whale (Hyperoodon planifrons). These claims were refuted and the validity of the species confirmed by the discovery of a second skull from the coast of Somalia in 1955 (Azzaroli, 1968). After further study, Moore (1968) found it sufficiently distinct to warrant establishing a new genus: Indopacetus. These two skulls were the only evidence that this species existed until a series of at-sea sightings of an unidentified bottlenose whale from the tropical Indian and Pacific Oceans was compiled and analyzed. These sightings had previously been tentatively identified as southern bottlenose whales, but color pattern differences ruled out that identification and the suggestion was made that they could be I. pacificus (Pitman et al., 1999). This identification was subsequently confirmed by genetically matching stranded animals (that had previously been identified as H. planifrons) with the holotype of I. pacificus (Dalebout et al., 2003). This clarification has led to the identification of scores of at-sea sightings, and the distinctive I. pacificus has now become one of the more frequently identified beaked whales. Longman’s beaked whale is identified in the field as a relatively large (6–6.5 m) ziphiid with a prominent melon, a moderately long beak, a relatively large dorsal fin, and a subtle but distinctive color pattern (Fig. 1). Younger animals, including calves, are dark gray with a conspicuously pale head. The light color of the melon extends only as far back as the blowhole (this is important because in the otherwise similar-looking southern bottlenose whale the paleness on the melon extends 10 cm or so behind the blowhole). Much of the face, lower jaw and throat are also pale. Immediately posterior to the blowhole, the dark gray dorsal coloration extends ventrally to form a dark patch around the eye. This darkness continues ventrally and backward to the insertion of the flipper, forming a broad band. There is a small, white “ear spot” embedded in the dark area behind the eye. Immediately posterior to the dark flipper band, and setting it off, is a large white area formed by the white from the ventrum extending high up on the sides of the animal. Calves are similar to adults except that the paleness of the melon, ventrum, and thoracic area is more pronounced; the head of the adults appears to darken with age. Adults also have a relatively longer beak and they are often heavily scarred. Adult females appear gray-brown in good light; males are similarly colored but often appear lighter than females due, at least in part, to an accumulation of scars from tooth rake marks by other males. Females have few or none of the linear (tooth rake) scars found on adult males,
I