A multiple instrument approach to quantifying the ... - Springer Link

Mar Biol (2010) 157:1857–1868 DOI 10.1007/s00227-010-1457-x

ORIGINAL PAPER

A multiple instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii Carl G. Meyer · Yannis P. Papastamatiou · Kim N. Holland

Received: 19 January 2010 / Accepted: 15 April 2010 / Published online: 5 May 2010 © Springer-Verlag 2010

Abstract We equipped individual tiger (Galeocerdo cuvier Péron and Lesueur, 1822) and Galapagos (Carcharhinus galapagensis Snodgrass and Heller, 1905) sharks with both acoustic and satellite transmitters to quantify their long-term movements in the Papahanaumokuakea Marine National Monument (Northwestern Hawaiian Islands). Tiger sharks exhibited two broad patterns of behavior. Some individuals were detected at French Frigate Shoals (FFS) year round, whereas others visited FFS atoll in summer to forage on Xedging albatross, then swam thousands of kilometers along the Hawaiian chain, or out into open ocean to the North PaciWc transition zone chlorophyll front, before returning to FFS in subsequent years. These patterns suggest tiger sharks may use cognitive maps to navigate between distant foraging areas. DiVerent patterns of spatial behavior may arise because cognitive maps are built up through individual exploration, and each tiger shark learns a unique combination of foraging sites. Galapagos shark detections were all associated with FFS, suggesting these sharks may be more resident around oceanic islands. Both Galapagos and tiger sharks primarily used the mixed layer (200–680 m and water temperatures as low as 7°C (Figs. 9, 10). Individuals from both species also showed evidence of depth ‘Xoors’ in their vertical movements. That is, periods of up to 3 days when their maximum depth remained continuously shallower than the thermocline, suggesting vertical movements were constrained by the presence of shallow habitat such as an atoll lagoon or submerged bank. For example, both GS1 and TS4 showed a clear switch from mixed layer swimming with deeper dives, to several days where maximum depth was 50 m or shallower (see arrows in Figs. 9, 10). In both cases, these depth Xoors appear to be associated with

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Fig. 5 Surface detection locations (shaded circles) of two tiger sharks (top panel TS1, bottom panel TS2) equipped with dorsal Wn mounted SPOT tags at French Frigate Shoals in May 2006. Lines connect successive detections. Shading indicates the quality of positional Wxes (3 = highest). Dashed line atoll barrier reef. Note that data for TS2 also include detections of implanted acoustic tags by stationary VR2 receivers (squares) and the PAT pop-up location (triangle)

slightly elevated sea surface temperatures (SSTs), suggesting sharks may have been swimming in warm, shallow waters, such as those found in atoll lagoons (Figs. 9, 10). Depth data also suggest that Galapagos sharks may be generally less surface-oriented than tiger sharks. Galapagos shark depth-temperature histograms contain multiple 6-h bins where sharks did not come to the surface, whereas tiger sharks came to the surface at least once during every 6-h period for which data were recovered (Figs. 9, 10). Eight of nine PATS were premature releases, resulting in tags drifting at the surface for 8–17 days before transmitting an initial position. The PAT deployed on TS2 popped up 25 km NE of FFS on 9/4/06 after a scheduled 100-day deployment (Fig. 5). This shark was also detected on an underwater receiver stationed on the FFS barrier reef (Rapture Reef) on 8/30 and 9/6/06 (Figs. 3, 5). Comparison of PAT retention times with detection data from SPOT and RCODE tags suggests PAT data were collected while sharks were associated with FFS.

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Fig. 6 Surface detection locations (shaded circles) of tiger shark #3 (TS3) equipped with a dorsal Wn mounted SPOT tag at French Frigate Shoals in May 2006. Lines connect successive detections. Shading indicates the quality of positional Wxes (3 = highest). Dashed lines indicate FFS atoll barrier reef and perimeters of submerged banks located 40–120 km NW of FFS

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Previous studies have shown tiger sharks alternate between wide-ranging behavior and more restricted movements and use a broad variety of habitats ranging from shallow coral reefs to open ocean (Polovina and Lau 1993; Holland et al. 1999; Meyer et al. 2009a). In this study, we used a multiple instrument approach to determine how these behaviors and habitats are linked for individual sharks over multi-year time scales. For example, distinctive clusters of acoustic detections at East Island indicate some tiger sharks (e.g. TS4 and TS5) visited FFS for several weeks in summer to forage on Xedging albatross and left when this prey resource ran out. A combination of satellite and acoustic telemetry revealed these sharks then swam thousands of kilometers along the Hawaiian chain, or out into open ocean, before returning to FFS in subsequent years. SPOT tracks suggest several tiger sharks navigated between distant patches of high resource availability. For example, TS3 and TS5 made highly directional movements between a succession of submerged banks and seamounts located between FFS and Pearl and Hermes Reef. This behavior indicates these sharks knew the locations of the bathymetric features from previous experience and were navigating between them. Tiger shark movements became more localized around these features, and although we do not know whether foraging occurred at these sites, seamounts are often hotspots of resource availability (e.g., Rogers 1993). Open ocean SPOT detections of TS4 in late fall 2006 were

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Fig. 7 Top Panel Overview of tiger shark #4 (TS4) SPOT track from French Frigate Shoals (FFS) to the North PaciWc transition zone chlorophyll front, 1,200 km NW of FFS in late October and early November 2006. Surface chlorophyll density estimated from SeaWiFS ocean color for the North PaciWc. Bottom Panel Detail of SPOT surface detection locations (shaded circles) and detections of implanted acoustic tags by stationary VR2 receivers (squares) while TS4 was associated with FFS. Lines connect successive detections. Shading indicates the quality of positional Wxes (3 = highest). Dashed line atoll barrier reef

associated with the transition zone chlorophyll front (TZCF), an area of high productivity and important oceanic foraging habitat for apex predators (Polovina et al. 2001). Long-term, reciprocal movements between distant locations suggest tiger sharks possess detailed cognitive maps of resource availability. The precise, seasonal arrival of certain tiger sharks at FFS in time for albatross Xedging indicates these sharks may also use internal clocks to guide their movements (Olding-Smee and Braithwaite 2003). Unlike mammalian apex predators such as bears (Gilbert 1999), there is no evidence of social transmission of foraging traditions in sharks, hence locations of good foraging areas must be uniquely learned by each individual. Tiger shark movements presumably include some element of exploration enabling them to discover new foraging locations (Meyer et al. 2009a). Sharks are long-lived animals which, over time, could build up detailed spatio-temporal maps of productive prey patches.

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Fig. 8 Inset Overview of tiger shark #5 (TS5) SPOT track (red line) from French Frigate Shoals (FFS) to Pearl and Hermes Reef (PHR) within the Papahanaumokuakea Marine National Monument (shaded area). Boxes indicate regions of track shown in detail in top and bottom panels. Top Panel Concentration of SPOT detections at FFS between 5/ 26/06 and 7/7/06, and route taken after departure from FFS on 7/8/06. Bottom Panel Detail of SPOT detections associated with submerged banks and seamounts surrounding Lisianski and Laysan islands

In contrast to tiger sharks TS3, TS4 and TS5 which were only present at FFS for short periods, tiger sharks TS1 and TS2 were detected at FFS at all times of the year and showed more extensive use of shallow lagoon habitats. Similar inter-individual variability in long-term movement patterns has been previously described in tiger sharks in the Main Hawaiian Islands (Meyer et al. 2009a). These diVerent patterns of behavior could result from unique individual learning experiences (i.e. each shark learns to exploit a diVerent combination of prey patches) and serve as a mechanism for intraspeciWc resource partitioning, giving rise to prey specialization. Albatross Xedgling predation at FFS provides strong evidence of prey specialization in tiger sharks. This directly observable phenomenon produces a characteristic cluster pattern of acoustic detections of tagged sharks at Xedging sites. Our results indicate a subset of tiger sharks present at FFS during summer intensively target these Xedging birds (e.g. TS4 and TS5), while others (e.g. TS1 and TS2) apparently do not. Thus, although overall this species has a very varied diet, this may be due to the contributions of many individuals each focusing on a narrower range of prey (e.g. Tinker et al. 2008).

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Fig. 9 Pop-up satellite archival tag (PAT) depth-temperature histograms (6 h bins) and sea surface temperature (SST) plots for three Galapagos sharks captured at French Frigate Shoals (FFS) in May 2006. Note 3-day period spent swimming shallower than 30-m depth by GS1 (arrow)

The multiple tag method also provided additional insight into Galapagos shark behavior. Although sample size was low (N = 3), and acoustic and SPOT detections were sparse (perhaps because of their preference for non-surface waters as disclosed by the PAT data), there was no evidence of tagged Galapagos sharks moving >30 km away from FFS. This is consistent with limited conventional identiWcation tagging results from Bermuda (Kohler et al. 1998) suggesting most Galapagos sharks are fairly resident around oceanic islands. The lower number of Galapagos shark acoustic detections in comparison with tiger sharks may reXect interspeciWc diVerences in habitat use at FFS because acoustic monitoring coverage at FFS was heavily skewed toward shallow lagoon habitats (N = 6 receivers), with low coverage outside the barrier reef (N = 2 receivers), and no coverage in deeper areas of the lagoon. The only acoustic detections of Galapagos sharks were on a receiver stationed outside the barrier reef, and PAT data show these sharks spend most time swimming within the mixed layer (0–100 m) with periodic deeper dives (maximum 680 m). Although Galapagos PAT data contained depth ‘Xoors’, consistent with moving into shallower habitat for several days, the maximum depths recorded during these periods were equivalent to deeper areas of the FFS lagoon. Visual observations, Wshing surveys and previous acoustic tagging

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studies (Antonelis et al. 2006; Lowe et al. 2006; C. Meyer unpublished data) indicate large Galapagos sharks do use shallow lagoon habitats at FFS, but only in low numbers. Overall observations suggest large Galapagos sharks prefer deeper habitats around FFS, which is consistent with recent observations from the Main Hawaiian Islands (C. Meyer unpublished data). Comparison with previous studies also indicates possible ontogenetic habitat shifts by Galapagos sharks, with juvenile sharks regularly utilizing shallow lagoon habitats (Lowe et al. 2006; C. Meyer unpublished data), while adults prefer deeper fore-reef habitats (this study; Wetherbee et al. 1996). Although results of this and previous studies (e.g. Papastamatiou et al. 2006) indicate broad overlap in habitat use between tiger and Galapagos sharks, there is also evidence of habitat partitioning between these species. For example, although active tracking (Holland et al. 1999) and PAT data show both tiger and Galapagos sharks primarily utilize the mixed layer (0–100 m), the current PAT and SPOT data suggest tiger sharks spend more time at the surface than Galapagos sharks. Tiger sharks also appear to use shallow lagoon habitats far more frequently than large Galapagos sharks. DiVerences in habitat use patterns may indicate resource partitioning between these species which have high dietary overlap (Papastamatiou et al. 2006). The purpose of occasional deep dives below the thermocline by

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Fig. 10 Pop-up satellite archival tag (PAT) depth-temperature histograms (6 h bins) and sea surface temperature (SST) plots for Wve tiger sharks captured at French Frigate Shoals (FFS) in May 2006. Note periods spent swimming shallower than 50-m depth by TS4 (arrows). Gaps in TS2 depth temperature plot are due to incomplete data recovery

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Galapagos and tiger sharks is unknown, but this behavior appears to be common in other reef sharks, and marine predators as a whole (e.g. Chapman et al. 2007; Sims et al. 2008). Collectively, these studies show reef-associated sharks utilize a wide variety of habitats ranging from shallow atoll lagoons to deep reefs and open ocean and may provide important trophic links between these habitats. With one exception, PAT retention times during our study were all less than one-third of the programmed 100day deployment time (median retention time 14.5 days). Previous studies reveal premature PAT shedding to be a common problem (see Stevens et al. 2010). Premature PAT shedding can occur through failure of either the leader materials (wire, sleeves), the anchor (failure to physically hold or through tissue rejection), or the PAT burn pin (due to physical damage or premature burn). A software problem prevented us from determining whether leader or pin failure was responsible for premature PAT releases in our study. Nor can we determine whether premature shedding resulted from gradual deterioration of the PAT attachment, or from a sudden event. However, the latter seems to be a strong possibility because tiger and Galapagos sharks are both highly reef associated and could dislodge externally attached tags by rubbing against the substrate. Predator strikes may be another cause of premature PAT release. PATs are similar in shape and size to potential prey Wshes,

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and the PMNM is a predator-rich environment with abundant large, aggressive piscivores (e.g. Caranx spp.) that may attack these tags. SPOT performance during our study was broadly comparable to results of previous studies with equivalent sample sizes (N < 10) of similar dorsal Wn tags. SPOT transmission times during our study (22–161 days) exceeded those previously reported for tiger sharks (n = 5, 12– 99 days; Heithaus et al. 2007) and blue sharks (Prionace glauca, n = 7, 0–159 days; Stevens et al. 2010) but fell short of those reported for white sharks (Carcharodon carcharias, n = 4, 49–221 days; Bruce et al. 2006) and salmon sharks (Lamna dipterus, n = 68, 6–1,335 days; Weng et al. 2008). Hays et al. (2007) identify a number of possible causes for satellite tag transmission loss including exhaustion of batteries, salt-water switch failure, antenna breakage, animal mortality and premature detachment of tags. They note biofouling of the saltwater switch may be particularly problematic in tropical waters. Rapid fouling of underwater receivers did occur in the PMNM (C. Meyer personal observation) and may have contributed to the demise of SPOTs deployed on Galapagos and tiger sharks during this study. SPOTs may also have been physically damaged or dislodged by sharks rubbing against the substrate. We also documented unexpected gaps in SPOT transmissions during periods when acoustic detections revealed a tiger shark was present daily for 2 weeks in a shallow lagoon where tiger sharks feed on albatross Xedglings and are frequently observed cruising at the surface with dorsal Wns exposed. The lack of SPOT detections from this shark is diYcult to explain but may have resulted from poor satellite coverage during those periods, or infrequent surface Wnning behavior by this particular individual. However, this result underscores the utility of a multi-tagging approach because, without the acoustic transmitter, this sharks’ frequent presence at a foraging location would have gone undetected. Equipping individual sharks with both satellite and acoustic tags provided a more comprehensive picture of their behavior than would have been obtained from single tag deployments. Here, we used a combination of devices that provided new insights into long-term movement and habitat use patterns of reef-associated sharks. However, to better interpret these patterns we need to determine why sharks use these areas. The ability to directly observe tiger sharks feeding on albatross Xedglings at FFS enabled us to interpret the tight clusters of tiger shark detections recorded at albatross nesting habitats during Xedging season. In most other cases, direct observations of foraging are not possible, but determining when and where sharks are feeding is essential for advancing our understanding of their ecology. The timing and location of other ecologically important behaviors such as mating are also completely unknown for

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most shark species. Future studies could shed light on shark feeding and mating by combining instruments which tell us about spatial behavior with other devices which directly measure feeding or inter-animal interactions (e.g. Papastamatiou et al. 2008; Holland et al. 2009). Acknowledgments We thank the crew of the NOAA ship Hi’ialakai especially coxswains S. Jones, J. Kehn and G. Maurizio for scientiWc mission support. We thank R. Kosaki, B. Bowen, M. Craig, J. Zamzow and P. Santos for their assistance in the Weld. We are grateful to Lucas Moxey (NOAA) for providing WiFS ocean color satellite imagery. This study was funded by an award to Hawaii Institute of Marine Biology from the National Marine Sanctuary Program (MOA 2005-008/ 6882). This work was carried out in accordance with the animal use protocols of the University of Hawaii (protocol #05-053). This work was conducted under U.S. Fish and Wildlife Special Use Permit #12521-06048, State of Hawaii Department of Land and Natural Resources permits # DLNR.NWHI06R019, NOAA-NWHIMNM-permit #2006-012, and Papahanaumokuakea Marine National Monument permits # PMNM-2007-031, #PMNM-2008-027 and # PMNM-2009-037. The experiments carried out during this study complied with the current laws of the United States of America.

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