key: cord-0325778-yw24ppxh authors: Véronique, Sarano; François, Sarano; Justine, Girardet; Axel, Preud’homme; Hugues, Vitry; René, Heuzey; Marion, Sarano; Fabienne, Delfour; Hervé, Glotin; Olivier, Adam; Bénédicte, Madon; Jean-Luc, Jung title: Underwater photo-identification of marine megafauna: an identity card catalogue of sperm whales (Physeter macrocephalus) off Mauritius Island date: 2021-03-09 journal: bioRxiv DOI: 10.1101/2021.03.08.433909 sha: 9a90daaf556af51d45430f1dd4db230ff88cba97 doc_id: 325778 cord_uid: yw24ppxh The long-term monitoring of long-lived animal populations often requires individual identification. For cetacean populations, this identification is mostly based on morphological characters observable from a boat such as shape, spots and cuts of the back, caudal and dorsal fins. This is well suited for species easily displaying their caudal fins, such as the humpback whales Megaptera novaeangliae, or those whose skin pigmentation patterns enable individual identification. However, for elusive or shier species such as the sperm whales Physeter macrocephalus, this approach may be more challenging as individuals display a rather uniform skin pigmentation. They also do not show very often their caudal fin that must be photographed perpendicularly to the water surface, vertically and fully emerged, uneasing the individual identification from a boat. Immature sperm whales that usually have a caudal fin without any distinctive marks may sometimes be excluded from photo-identification catalogues. Within the framework of the Maubydick project, focusing on the long-term monitoring of sperm whales in Mauritius, passive underwater observation and video recording were used to identify long-lasting body markers (e.g., sex, ventral white markings, cut outs of fins) to improve individual identification. A catalogue of individual identity cards was developed and 38 individuals were recorded (six adult males, 18 adult females and 14 immatures). This catalogue was used in the field and enabled observers to record some nearly-daily and yearly recaptures. Advantages and disadvantages of this method are presented here. Such catalogues represent a robust baseline for conducting behavioural, genetic and acoustic studies in marine megafauna social species. Benefits of such newly acquired knowledge are of first importance to implement relevant conservation plans in the marine realm. The long-term study of long-lived animal population often requires individual identification, e.g. 92 for abundance estimation in mark-recapture surveys, social behaviour understanding and for 93 conservation purposes (Hammond et al. 1990 fin barely distinctive (Van der Linde & Eriksson 2020) and as sperm whales have a caudal fin of 127 uniform color unlike humpback whales for example Underwater observations 186 187 The observation protocol was described in Sarano et al. (2021) . Briefly, when a group of sperm 188 whales was spotted from the boat, the animals were approached no closer than 100m and a small 189 group of swimming observers, generally a scuba diver and 4 snorkelers, immerged themselves, 190 upstream considering the movement direction of the sperm whale group. Observers were as 191 passive as possible, typically not swimming towards the whales but waiting for the sperm whales 192 to approach to film them. When sperm whales were static (e.g., socializing or sleeping), 193 observers slowly and quietly approached. The scuba diver recorded videos and observations at a 194 maximum diving depth of 40m, while the snorkelers performed observations from the surface 195 and filmed the sperm whales at a maximum 20m depth. 196 The duration of observation varied between 20s to 10min when the animals were sleeping or 197 socializing near the observers. The boat always stayed away and picked up the observers once 198 the sperm whale group had moved away. 199 200 201 Video processing 202 203 The identification of morphological markers to create the catalogue of ID-cards was based on 204 meticulous analyses of the videos using VLC player (VideoLAN Organization, France). Slow 205 motion mode was used to get the best screenshot for each of the body marks. These pictures 206 were then used to illustrate the morphological markers on the catalogue. 207 208 209 Morphological markers 210 211 The morphological markers retained for the ID-cards are illustrated in Figure 1 . They include: 212 sex, white spots, cuts with removal of material, scars from teeth marks (i.e. rake marks), shape of 213 the fluke. Some of these marks can be observed from a boat (e.g., cuts on the caudal fin, cuts / 214 callus on the dorsal fin), but the majority are visible only underwater (e.g., sex, cutting of the 215 pectoral fins, clear spots of depigmentation on the ventral side, on the mandibular area and the 216 cheeks, shape of the jaw, size of the teeth). 217 218 Cutting Pattern of the fins 219 Types of cutting pattern of the fins (small nicks, distinct nicks, waves, scallops, missing portions, 220 holes, tooth mark scars and calluses) have already been defined (Arnbom & Whitehead 1989, 221 Whitehead 1990). 222 The features used in this study are (for those previously defined, descriptions are those of 223 Arnbom & Whitehead 1989 when indicated; in the other cases, descriptions have been 224 generalized to fit to underwater observations, Figure 1 and Temporary scratches and peeling spots were used only to help with daily recapture over a field 252 season. These non-permanent markers were therefore, not retained in the catalog. 253 254 255 Catalogue of ID-card creation 256 257 The catalogue developed through the underwater observation protocol consists of a series of 258 individual ID cards for each sperm whale ( Supplementary Information 1 and 2 ). For better 259 recognition of individuals in the field and easier use of the catalogue, the ID-cards were designed 260 using simplified standards (see Supplementary Information 1 and 2) . For each individual, the 261 distinctive markers were indicated on the ID-card (e.g., on the caudal), and/or detailed on 262 dedicated zoomed photos (of pectoral, spots, mouth, ...). Additional information was listed at the 263 top of the card such as date of first observation, date of last observation, and years of successive 264 observations. Each individual was given a name in an alphanumeric reference system to ease its 265 identification in the field. Additional information, such as the availability of DNA samples, or 266 information of kinship relations when known are enriched the ID-cards. (Table 1 ). In 2020, the 283 fieldwork season was shortened due to bad weather and the Covid19 pandemic. 284 285 The ID-cards were created from about 250 hours of underwater video recording between 2015 286 and 2020, for a total number of 317 days of observation (see Table 1 ). Sperm whales were 287 observed in 83.9% of the fieldtrips. 288 289 290 Catalogue of individual ID-cards 291 292 A total of 38 ID-cards corresponding to 38 identified individuals are presented in this study: 18 293 adult females, 14 immatures (9 males, 5 females) and 6 adult males (Table 2 and Supplementary 294 Information 1 and 2). Table 2 presents all morphological markers identified for each of these 38 295 individuals. They are described according to their position on the body (e.g., sex, caudal, 296 pectoral, dorsal, back, head) and, for white marks, according to their location on the ventral parts 297 of the animal. 298 299 Gender was the first identification criterion used in the field to identify the individuals. Then the 300 individual-specific body markers were used to narrow down the identification at the individual 301 level. The number of body marks typically increased with age, young individuals displaying very 302 few (e.g., Ali, Alexander, Daren, Lana) to more than 10 marks in older individuals (e.g., up to 14 303 marks for the adult male Anjhin, Table 2 ). Some of these body markers were unique enough to 304 enable direct identification of the individuals: e.g., distinct missing portions on the fluke (e.g., 305 Arthur, Chesna, Miss Tautou, Agatha) or on the pectoral fin (e.g., Germine), white markers (e.g., 306 Adélie, Tache blanche, Issa, Joue Blanche) or arched-shaped jaw (e.g., Irène's twisted jaw). For 307 other individuals, the observation of several body markers was required to make the 308 identification. Overall, the body marks presented in Table 2 enabled field observers to 309 unambiguously identify these 38 individuals. Recapture rate of females and immatures 330 331 The primary aim of the ID-card catalogue was to enable underwater field identification of 332 individual whales from 2015 to 2020. The ID-cards were also used to analyze field videos 333 recorded between 2011 and 2014, as well as some older underwater photographs taken in 2007 334 and 2009, in order to identify the individuals. The observation effort was therefore divided in 2 335 periods, one until 2014 and the second starting in 2015 (Tables 1 and 3). 336 337 Over the period 2011-2020, 17 adult females identified were recaptured 1,542 times with an 338 average rate of 91 recaptures per individual (min=23, max=177). One adult female, Joue 339 Blanche, was seen only 8 times, and no more since 2015 (Table 3) . Among the adult females, 2 340 had few recaptures (Déline n = 31 and Swastee n = 23) although they were easily identified 341 thanks to their distinct markers (for Swastee, a huge bulge on the nape; for Déline, a big cut on 342 the caudal fin -see Supplementary Information 1 and 2) . The most recaptured females were 343 Germine (n = 177) and Irène (n=156), observed during more than 50% of the days of field work. 344 Immatures were more often recaptured, even those presenting limited distinctive markers such as 345 Roméo, Ali or Daren (between 39% to 68% of the days of observation depending on the 346 individual, 55% on average) than adult females (between 22% to 39%, 30% of the days of 347 observation on average). The most recaptured immature was Arthur (n=184). 348 During the 2015-2020 period, some individuals disappeared. They have been collated at the 349 bottom of Table 3 , i.e., 2 immature males (Maurice, 5 years-old and Baptiste, 3 weeks-old), 350 probably dead, and a immature female (Agatha, 1 year-old) with her assigned mother Joue 351 Blanche ( Whitehead 1989), skin biopsies and molecular sexing are therefore necessary to determine the 371 genders (Gero et al. 2008 (Gero et al. , 2009 (Gero et al. , 2014 . Underwater observation allows to observe the genital 372 slit, and thus to distinguish between males and females, even before they reach sexual maturity. 373 Here gender assignment was possible for 14 immatures, some of them from the day they were 374 born. 375 Identification of immatures without any distinctive markers on the fluke 378 Underwater observation provides access to a range of body markers that a platform-based 379 observer can only occasionally see but whose utility on sperm whale individual identification has 380 been proved (Van der Linde & Eriksson 2020). These markers are, in particular, relevant for 381 individuals without any distinctive markers on the fluke (Figure 3 ) and for the very young 382 individuals that seldom fluke. These markers are, for instance, the indentations on the pectoral 383 fins, the shape of the jaw or the pigmentation patterns on the ventral side, the flanks and the 384 mandibular area. The presence / pattern of colored markings is often used for humpback whales 385 (Glockner-Ferrari & Ferrari 1990) or for dolphins (Herzing 1997) . Three immatures with an 386 intact caudal fin and therefore impossible to identify from a boat were identified this way: Zoé, 387 Tache blanche and Eliot (Figure 3) . Underwater, the observer can notice that Zoé has a distinct 388 nick on each pectoral and is a female, Eliot, a male, has a white ventral escutcheon and Tache 389 blanche, another male, has a white spot on the belly as well as a small nick on the right pectoral 390 (Figure 3 ). 391 392 393 Zoé has a nick on each pectoral and is a female. This underwater method provided additional information on the immatures and could therefore 398 improve the knowledge on this cohort, e.g., by allowing to determine mortality rates including 399 calves ). 400 401 Recapture rate 403 The recapture rate is increased by underwater observation as compared to boat-based studies. 404 Over a period of 9 years, the method presented here has resulted in numerous recaptures for all 405 the individuals identified (mean rate for adult females = 91, Water conditions 463 In this study, the underwater visibility (around 20m) enabled to easily identify morphological 464 markers and white spot patterns on the body. But in terms of logistics linked to climatic 465 conditions, it is clear that this underwater method cannot be implemented everywhere, e.g., it is 466 much more complicated to perform underwater observations in polar waters for example, which 467 are relatively dark and where the temperature may be near 0°C. Additional equipment adapted to 468 these conditions would then be necessary. High turbidity can also reduce the visibility to a few 469 meters (due to high primary production or turbid rainwater coming from inland particularly important, as only their precise count allows to determine the real rate of increase of 518 the population (e.g. Gero and Whitehead 2016). Local trends of sperm whale populations will be 519 more precisely determined, which will be of first importance to define conservation concerns, 520 priorities, and to measure the benefits of newly implemented protection plans. Other cetaceans 521 could obviously strongly benefit of such careful individual specific studies, in particular when 522 local groups of small size are known, whose trends can vary depending on impact of local 523 anthropogenic activities (e.g. Louis et al. 2017 The protocol based on underwater videos has already proven to be highly robust and widely-used 531 for other marine megafauna species (e.g., Glockner-Ferrari & Ferrari 1990, Herzing 1997, 532 Marshall & Holmberg 2018, Pierce et al. 2018 ). It has been applied here for the identification of 533 sperm whales in Mauritius, based on underwater observations. The relevance of this approach is 534 evidenced by quasi-daily recaptures of females and immatures, over the field seasons and from 535 one year to another. These recaptures were carried based on markers that can hardly be observed 536 from the sea surface. The markers used proved to be stable and reliable over the 9 years of the 537 study. This underwater observation approach using video recordings enables to identify 538 individuals with intact caudal fins and to sex the entire group, including young and newborns, 539 without using biopsies and molecular sexing. Like any catalogue, it requires annual updates of 540 the ID-cards to take into account the possible evolution of morphological markers. It will also 541 soon be extended by the ID-cards of around sixty more individuals observed off the coast of 542 Mauritius. Impact assessment research: use and misuse of 603 habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli Multi-state open robust design 606 applied to opportunistic data reveals dynamics of wide-ranging taxa: the sperm whale case SPLASH: 609 Structure of populations, levels of abundance and status of humpback whales in the North Pacific Cultural turnover among Galápagos sperm whales Ethology and Behavioral Ecology of Odontocetes, in Ethology and Behavioral Ecology of Marine 615 Assessing sperm whale (Physeter macrocephalus) movements within the 618 western Mediterranean Sea through photo-identification. Aquatic Conservation: Marine and Freshwater 619 Ecosystems No evidence for recovery in the population of 621 sperm whale bulls off Western Australia, 30 years post-whaling A first assessment of operator compliance and 624 dolphin behavioural responses during swim-with-dolphin programs for three species of Delphinids in the Azores 625 Life and Marine Sciences Baleen whales: conservation issues and the status of the most 627 endangered populations. Mammal Review, 29, 37−62 Increased avoidance of swimmers by wild bottlenose dolphins (Tursiops truncatus) due to 629 long term exposure to swim with dolphin tourism Hawaiian spinner dolphins and the growing dolphin watching activity in Oahu Behavior and social structure of 657 the sperm whales of Dominica, West Indies Critical decline of the Eastern Caribbean sperm whale population Reproduction in the humpback whale Hawaiian waters, 1975-1988: the life history, reproductive rates, and behaviour of known individuals identified 663 through surface and underwater photography Photo-identification; a reliable and non-invasive tool for 666 studying pink river dolphins (Inia geoffrensis) Aquatic Mammals Photographic identification of northern bottlenose whales (Hyperoodon 669 ampullatus): Sources of heterogeneity from natural marks Individual recognition of cetaceans: Use of photo-672 identification and other techniques to estimate population parameters Underwater observations of benthic-feeding bottlenose dolphins Computer-678 assisted photo-identification of individual marine vertebrates: A multi-species system Identification of individual sperm whales by wavelet transform of the trailing 681 edge of the flukes Using wavelet transforms to match photographs of individual sperm whales 683 identified by the contour of the trailing edge of the fluke Information and Information Systems. VISUAL 1999 Vocal repertoires 687 and insights into social structure of sperm whales Fatal ingestion of floating net debris by two sperm whales 690 (Physeter macrocephalus) Evidence that sperm 692 whale (Physeter macrocephalus) calves suckle through their mouth Protection des mammifères marins face aux activités humaines et nouvelles 694 connaissances issues des études de l'ADN, in Actes du colloque « Le transport maritime et la protection de la 695 biodiversité Revised abundance indices for sperm whales off Albany Reports to the International Whaling Commission Long-term associations among male sperm whales (Physeter 700 macrocephalus) Collisions between ships and whales Significant plastic accumulation on the Cocos (Keeling) Flukebook: a cloud-based photo-identification analysis 706 tools for marine mammal research Strong bonds and small home 708 range in a resident bottlenose dolphin community in a marine protected area Marine Mammal Science MantaMatcher Photo-identification Library Available Mark-recapture analysis of sperm whale (Physeter macrocephalus) 713 photo-id data from the Azores (1987-1995) Computer assisted photo-identification of humpback whales. Reports 715 to the International Whaling Commission Indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia Improved abundance and trends estimates for sperm whales in the eastern North 720 Pacific from Bayesian hierarchical modelling Swim encounters with killer whales (Orcinus orca) off Northern 723 Norway: interactive behaviours directed towards human divers and snorkelers obtained from opportunistic 724 underwater video recordings First insights into the effects of swim-with-dolphin 726 tourism on the behavior, response and group structure of southern Australian bottlenose dolphins Photographic identification of sharks The status and distribution of cetaceans in the Black Sea and 732 IUCN Centre for Mediterranean Cooperation Impacts of commercial whale watching on male sperm whales at 734 Patterns of kinship in groups of free-living sperm 736 whales (Physeter macrocephalus) revealed by multiple molecular genetic analyses Cultural transmission 739 of fine-scale fidelity to feeding sites may shape humpback whale genetic diversity in Russian Pacific waters Kin relationships in cultural species of the marine realm: 743 case study of a matrilineal social group of sperm whales off Mauritius island Bottlenose dolphins, (Tursiops truncatus), 746 increase whistling in the presence of "swim-with-dolphin" tour operators Photographic identification 749 of the blue whale (Balaenoptera musculus) in the Gulf of St. Lawrence, Canada. Report of the International 750 Whaling Commission Physeter macrocephalus 752 (amended version of 2008 assessment). The IUCN Red List of Threatened Species Manta Matcher: automated photographic identification of manta 755 rays using keypoint features Deaville, unmanned vehicles for the detection and monitoring of marine Fauna Automated image acquisition and morphometric description Computer assisted individual identification of sperm whale flukes Estimates of the current global population size and historical trajectory for sperm whales Direct estimation of within group heterogeneity in photo identification of sperm whales Methods of photo-identification for small cetaceans. Reports of the 774 International Whaling Commission