Identifying Shark Mating Behaviour Using Three-Dimensional Acceleration Loggers
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Vol. 10: 71–82 ENDANGERED SPECIES RESEARCH Published online February 2, 2010 doi: 10.3354/esr00247 Endang Species Res Contribution to the Theme Section ‘Biologging technologies: new tools for conservation’ OPENPEN ACCESSCCESS Identifying shark mating behaviour using three-dimensional acceleration loggers Nicholas M. Whitney1,*, Harold L. Pratt Jr.2, Theo C. Pratt2, Jeffrey C. Carrier3 1Center for Shark Research, Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, Florida 34236, USA 2Center for Shark Research, Mote Tropical Marine Laboratory, 24244 Overseas Highway, Summerland Key, Florida 33042, USA 3Department of Biology, Albion College, Albion, Michigan 49224, USA ABSTRACT: Little is known about the reproductive strategies and mating behaviour of most sharks. Understanding mating behaviour is important as it can determine reproductive success and possibly rates of multiple paternity and fecundity. Additionally, some sharks appear to have specific habitat requirements for mating activities. We tested the utility of a 3-dimensional acceleration logger to identify mating events in free-living nurse sharks Ginglymostoma cirratum in an area where behav- iours can be observed directly, thus allowing corroboration of acceleration data. Loggers were attached to 4 adult females and were recovered after recording periods of 23.2 to 99.8 h (mean ± SD = 50.0 ± 35.1 h). We used acceleration data to classify several behaviours, including swimming, rest- ing, resting in a surge zone, and mating, with examples of each behaviour confirmed via direct obser- vation. Twenty-six mating events were inferred from acceleration data, ranging from 21 s to 20.1 min in duration (median = 2.22 min), with no events taking place during the nighttime hours between 23:00 and 07:00 h. Four events lasted longer than 9 min and took place during periods when logger- equipped sharks were not acoustically detected within the shallow study site. The similarity in mat- ing behaviours between this and some other species raises the possibility that accelerometry could be used to quantify mating in a variety of shark species. This is the first study to classify mating and other behaviours in free-living sharks from acceleration data. KEYWORDS: Ginglymostoma cirratum · Reproduction · Accelerometer · Mating · Behaviour Resale or republication not permitted without written consent of the publisher INTRODUCTION rates of genetic polyandry that vary widely between species (Saville et al. 2002, Chapman et al. 2004, Feld- Understanding reproductive strategies and mating heim et al. 2004) and between populations within the behaviour is crucial for proper management of marine same species (Daly-Engel et al. 2007, Portnoy et al. fish species (Rowe & Hutchings 2003). Shark popula- 2007). The underlying factors causing these differ- tions are particularly vulnerable to fishing pressure ences are poorly understood, but various aspects of due to their slow growth, late maturity, and low fecun- mating behaviour may be the most important determi- dity (Hoenig & Gruber 1990, Pratt & Casey 1990), and nants of the mating system exhibited by a species or some shark populations have been greatly reduced in population (Daly-Engel et al. 2007, Portnoy et al. 2007, recent decades (Musick et al. 2000, Cortés et al. 2002). DiBattista et al. 2008). Unfortunately, the mating pat- Despite renewed conservation and management terns of most sharks are unknown, as mating behav- efforts, very little is known about the mating systems of iour is difficult or impossible to observe. Thus there has most shark species (reviewed by Carrier et al. 2004). been no method to test behavioural hypotheses Molecular techniques have emerged to reveal complex regarding mating systems or to determine what physi- reproductive strategies for several sharks, including cal and biological factors may be required for shark *Email: [email protected] © Inter-Research 2010 · www.int-res.com 72 Endang Species Res 10: 71–82 species to mate successfully (Carrier & Pratt 1998, Pratt The goal of the present study was to determine & Carrier 2007). A device that can record shark mating whether acceleration loggers could be used to identify activities remotely would therefore be an invaluable mating behaviour in free-living nurse sharks during tool, both for understanding the frequency and diurnal their mating season in the Florida Keys. We present ac- periodicity of mating and for identifying essential mat- celeration signatures associated with swimming, rest- ing habitat and environmental conditions. ing, and mating behaviour, examples of which were Acceleration loggers have been applied to a wide confirmed through direct observations. We present a range of aquatic species to quantify fine-scale details hierarchical decision tree for classifying behaviours of swimming dynamics and various behaviours (e.g. based on their acceleration data (e.g. Gleiss et al. Yoda et al. 1999, Tanaka et al. 2001, Kawabe et al. 2009a), and we discuss the implications of these find- 2003, Kato et al. 2006) and, more recently, have been ings for future studies of shark reproductive behaviour. used to calculate metabolic rates based on an animal’s We believe that our findings represent the first step to- overall dynamic body acceleration (ODBA; Wilson et ward a broader goal of quantifying mating behaviour in al. 2006). In sharks, acceleration loggers have been shark species for which it cannot be directly observed. used to quantify activity patterns over several days to weeks in captive whitetip reef sharks Triaenodon obe- sus (Whitney et al. 2007) and measure swimming MATERIALS AND METHODS behaviour and ODBA for periods of several hours in free-living whale sharks Rhincodon typus (Gleiss et al. Study site and mating behaviour. The Dry Tortugas 2009b) and captive lemon sharks Negaprion brevi- study site (described in Pratt & Carrier 2007) is a shal- rostris (Gleiss et al. 2009a). Since both static and low (0 to 1.8 m) marine flat partially surrounded by dynamic acceleration can be derived from the total islands comprising the Dry Tortugas group, Florida, acceleration measured by these devices, they can be USA. Adult female nurse sharks aggregate in the shal- used to determine both the body orientation and move- lows each year, often shoaling in 1 m of water or less ments of a logger-equipped subject (Yoda et al. 1999). for several weeks during the mating season, with inter- Such data can provide clear indication of the occur- mittent forays out of the area for hours or days at a rence and characteristics of several behaviours that time. Males patrol the deeper boundaries of the site, may be rare or difficult to observe directly (e.g. Watan- occasionally moving into the shallows to investigate or abe et al. 2005, Wilson et al. 2008, Shepard et al. 2008, attempt to mate with a given female (Carrier et al. this Theme Section). For example, Tsuda et al. (2006) 1994). Mating typically occurs in the shallows or used accelerometers to classify 8 behaviours as- nearby in slightly deeper (2 to 3 m) water into which sociated with spawning in female chum salmon males will often attempt to carry a female to improve Oncorhynchus keta and showed that the occurrence of their chance of successful copulation, which only these behaviours was substantially affected by turbid happens in ~8% of events (Pratt & Carrier 2001). The water runoff after a storm. annual occurrence of this mating aggregation and the Mating behaviour in nurse sharks Ginglymostoma animals’ use of shallow, clear water make the Dry Tor- cirratum, and some other shark species for which it tugas site ideal for capturing and tagging animals and has been observed, typically consists of a male grasp- monitoring their behaviour for prolonged periods. ing a female’s pectoral fin and attempting to insert Tag package design and attachment technique. We one of his paired claspers into the female cloaca (see applied 3-dimensional acceleration data loggers (16 × Pratt & Carrier 2001 for a review). Once a pectoral 108 mm, 35 g, Vemco) to 6 adult nurse sharks (5 fe- grasp is attained, the female will often adopt a variety male, 1 male) during their mating season in June 2008, of positions and behaviours to avoid copulating with and recovered loggers from 4 of the 6 (see Table 1). the male (Carrier et al. 1994, Whitney et al. 2004), or Loggers were set to record at 5 Hz; other details of log- in some cases she will seemingly cooperate and allow ger function are described in Whitney et al. (2007). copulation to take place (Carrier et al. 1994, Pratt & Each tag package consisted of an acceleration logger, Carrier 2001). Mating events can last from a few sec- a V16 continuous acoustic pinger tag (Vemco) trans- onds to several minutes and involve behaviours such mitting once per second, and a timed galvanic release as rolling, grasping, erratic tailbeats, and arching in (International Fishing Devices) designed to corrode af- unusual postures, including ventral-side-up positions ter a 3 or 7 d period in tropical seawater (Fig. 1). Eye- and vertical headstands (reviewed in Pratt & Carrier loops on both ends of the galvanic releases were 2001). For the purposes of the present study, the term ground down to nubs (and new holes drilled through ‘mating event’ is used to refer to all of these activities, them) so they were small enough to pass through the regardless of whether or not copulation was holes in the fin and to be shed after the body of the re- achieved. lease had corroded. Tags were held together with elec- Whitney et al.: Identifying shark mating with accelerometry 73 noted whenever possible, with particular attention given to changes in behaviour likely to be obvious in acceleration data, such as the beginning and cessation of swimming behaviour or the onset of mating events. Logger-equipped animals that could not be seen were occasionally detected by hydrophone, which allowed us to approach them by kayak or snorkeling and note their behaviour.