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Mar Biol (2016) 163:214 DOI 10.1007/s00227-016-2991-y

ORIGINAL PAPER

Adult female whale sharks make long‑distance movements past Darwin Island (Galapagos, Ecuador) in the Eastern Tropical Pacific

Alex R. Hearn1,2,7 · J. Green3 · M. H. Román4 · D. Acuña‑Marrero5 · E. Espinoza6 · A. P. Klimley7

Received: 20 August 2015 / Accepted: 15 September 2016 © Springer-Verlag Berlin Heidelberg 2016

by photo-identification (n = 2) or satellite track (n = 3). Tracks that lasted through December ended along the conti-nental shelf break of northern Peru. We show return move-ments of individuals through Darwin after moving large distances into the open ocean and establish connectivity with mainland Ecuador and Peru.

Introduction

Whale sharks Rhincodon typus Smith 1828 have been observed globally in tropical and subtropical waters (Com-pagno 2001). They have been seen occasionally in the Mediterranean Sea (Jaffa and Taher 2007) and sometimes as far north as 40°N (Tomita et al. 2014) and as far south as New Zealand (Duffy 2002). It is the world’s largest fish, reaching a total length of up to 20 m (Chen et al. 1997). There appears to be some gene flow among the Pacific, Atlantic and Indian Oceans although whale sharks in the Atlantic Ocean appear to be more genetically isolated from the other two ocean basins (Castro et al. 2007; Viganud et al. 2014). Although they are mainly solitary and pelagic, whale sharks do appear together at the surface some times of year in many locations around the world, often to feed on plankton blooms (e.g., Heyman et al. 2001; Kumari and Raman 2010; Ketchum et al. 2013). Except in the Red Sea (Berumen et al. 2014), most sharks seen have been imma-ture males (e.g., Eckert and Stewart 2001; Riley et al. 2010; Norman and Stevens 2007; Ramirez-Macias et al. 2012a). A single pregnant female with 304 embryos was landed Taiwan in 1995 (Joung et al. 1996), while large females with distended abdomens have been seen near Espiritu Santo Island and Gorda Banks at the tip of Baja California (Eckert and Stewart 2001; Ramirez-Macias et al. 2012b; Ketchum et al. 2013). Ramirez-Macias et al.

Abstract Most previous studies on whale shark move-ments have been on immature sharks. Here, we pre-sent tracking data for large females that we tagged at the Galapagos Islands, where they occur seasonally. We con-ducted fieldwork at Darwin Island (1.67, 92.0°W) from July to October in 2011 and in 2012. We often saw indi-vidual sharks several times on a particular day, but rarely saw them again more than 2 days later after they were first sighted. We tagged 39 female whale sharks, 36 of which were between 8 and 12 m long. We tracked 27 sharks for 9–176 days (median = 47 day). Sharks tagged in July moved west into the open ocean, whereas those tagged in September and October moved toward the coast of South America. They travelled between 49 and 2747 km from Darwin (median = 1296 km), at about 38 km day−1 (median rate). We observed five of those sharks later at various times at Darwin Island after >1 month absence,

Responsible Editor: B. Stewart.

Reviewed by R. Hueter and an undisclosed expert.

* Alex R. Hearn ahearn@usfq.edu.ec

1 Universidad San Francisco de Quito USFQ, Quito, Ecuador2 Turtle Island Restoration Network, Olema, CA, USA3 Marine Megafauna Foundation Ecuador, Quito, Ecuador4 Inter-American Tropical Tuna Commission, La Jolla, CA,

USA5 Charles Darwin Foundation, Puerto Ayora, Galapagos

Islands, Ecuador6 Galapagos National Park Directorate, Puerto Ayora,

Galapagos Islands, Ecuador7 University of California Davis, Davis, CA, USA

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(2012b) suggested that those females might have been pregnant.

Baja California was the only location in the Eastern Pacific where whale sharks have been studied, though they are also reported to appear near Coiba, Panama (Hector Guzman, Smithsonian Tropical Research Institute, pers. comm.) and around the oceanic islands of Cocos and Mal-pelo (Sibaja-Cordero 2008; Sandra Bessudo, Fundacion Malpelo, pers. Comm.). Farther south, whale sharks occur off the coast of northern Peru from January through March (Ramirez 1995), when surface water temperatures are greatest (23–25 °C). In the Galapagos Islands, the seasonal presence of whale sharks from late June through December at the northernmost island of Darwin has generated a grow-ing dive tourism industry (Zarate 2002; Acuña-Marrero et al. 2014; Hearn et al. 2014).

In this paper, we report on our tagging of large female whale sharks at Darwin Island in the Galapagos Archipel-ago. This site is one of the few known offshore, mid-ocean locations where adult whale sharks have been seen regu-larly. Consequently, it offers a unique opportunity to record the movements of these sharks from oceanic areas in con-trast to most previous studies near mainland coasts.

Methods and materials

Ethics statement

The work undertaken for the preparation of this manuscript was approved by the University of California Davis Insti-tutional Animal Care and Use Committee (IACUC) Proto-col # 16022 and authorized by the Galapagos National Park Directorate research permit PC-37-11.

Study area and fieldwork

The Galapagos Archipelago straddles the equator about 1000 km west of mainland Ecuador. It consists of thir-teen major islands and over 100 islets and emergent rocks (Snell et al. 1996), all volcanic in origin. In 1998, the Gov-ernment of Ecuador created a 138,000-km2 marine reserve around the islands, extending to a distance of 40 nm off-shore. The Galapagos Marine Reserve (GMR) became a UNESCO World Heritage Site in 2001. The GMR lies at the confluence of three major ocean currents: the Panama Current, bringing warm water from the north; the Hum-boldt Current, bringing cool water from the south; and the upwelling Equatorial Undercurrent or Cromwell Cur-rent (EUC), bringing deep, cold, productive waters to the surface in the western region (Palacios 2004; Lavin et al. 2006; Sweet et al. 2007). The influence of the EUC is strongest in the first half of the year. Farther to the north,

the Equatorial Front (EF) runs from the coast of South America along the equator westwards to the international dateline, crossing the GMR at 1–2 °N. The EF separates the warm, eastward flowing North Equatorial Counter Cur-rent (NECC) to the north from the cool, westward flow-ing South Equatorial Current (SEC) to the south (Palacios 2004). The SEC is strongest in the latter part of the year (Johnson et al. 2002).

The complex nature of the currents surrounding the islands effectively structures the GMR into four biogeo-graphic regions, based on the composition of its reef fish and macro-invertebrate communities surrounding each island (Edgar et al. 2004). Although whale sharks have occasionally been seen throughout the Galapagos archi-pelago (Hearn et al. 2014), they occur regularly at certain times of year in the northern bioregion near Wolf Island and especially Darwin Island, both strongly influenced by the Panama Current (Edgar et al. 2004; Palacios 2004). Darwin (106 Ha) and Wolf (134 Ha) are the smallest of the islands. These remote islands are separated from each other by 36 km and are about 140 km north of the rest of the archipelago (Snell et al. 1996). Both islands have a steep rocky coast which drops rapidly to depths greater than 100 m within 400 m of the islands (Peñaherrera et al. 2013). The islands are separated from the main Galapa-gos platform to the south by a channel of approximately 1000 m deep (Wooster and Hedgpeth 1966). Sea surface temperature at Darwin and Wolf ranges from 22.5 °C in August to 27 °C in March in normal years (Banks 2002). However, the entire marine reserve is a highly dynamic system and is strongly influenced by periodic warming dur-ing El Niño events (Glynn and Ault 2000), which greatly affects the ecology of the terrestrial and marine ecosystem in the islands (Edgar et al. 2010).

Satellite tags

We tagged whale sharks near Darwin Island, Galapagos, at a location known as Darwin’s Arch (1.6725°, −91.989°). A rocky platform there at a depth of approximately 7 m drops almost vertically to over 30 m along a 300-m stretch. Dar-win’s Arch has become an important site for dive tourism, partly due to the predictable occurrence of whale sharks from June through December each year (Acuña-Marrero et al. 2014, Hearn et al. 2014). Our research cruises were timed to coincide with the start, middle and end of the whale shark season. We spent 7–10 days at Darwin Island each month in July, September and October 2011 and in August and October 2012.

We used three types of satellite tags with Argos trans-mitters. Towed SPOT-5 and SPLASH tags, with torpedo-shaped housings (Wildlife Computers Inc., WA, USA), use the Doppler effect to provide positions through the Argos

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satellite network when at the surface. SeaTags (Desert Star LLC, CA, USA) were originally designed as pop-up archi-val (PSAT) tags, but can also be programmed to provide near real-time positions when at the surface. In contrast with commonly used PSAT tags, SeaTags estimate latitude by use of a magnetometer, which measures the earth’s mag-netic field, rather than using light curves. Error ranges are reported by the manufacturer to be 30–40 nm.

All tags were attached to sharks by SCUBA divers. The tags had on 1.2- to 2-m stainless steel tethers with stainless steel barbs which were inserted beneath the skin using a pneumatic spear gun or a heavy-duty pole spear just off the midline in front of or immediately behind the base of the first dorsal fin. Tags were painted with a nonmetal-based antifouling paint prior to attachment. Dive teams photo-graphed each shark, estimated the length (see below) and noted whether the shark had a distended abdomen (Ram-irez-Macias et al. 2012b). We determined the sex of each shark by the presence or absence of claspers.

Data analysis

Estimation of length

Where possible, we measured the length of whale sharks which was measured using laser photogrammetry (Rohner et al. 2011). This method relates the total length of a whale shark to the distance between the fifth gill slit and a perpen-dicular line from the start of the first dorsal fin (r2 = 0.93). Two underwater laser pointers (APINEX, Montreal) were set 25 cm apart in parallel on each side of an underwa-ter digital camera (Nikon D80). Parallel alignment of the lasers was verified before and after each dive by measur-ing the distance between the two projected laser dots on a parallel surface approximately 5 m away. Only photographs taken on the same plane as the whale shark were used for this measurement (N = 20).

For those sharks for which photos were not available or valid for analysis (N = 27), we relied on gross estimates by the divers. Based on a comparison of 20 sharks with both estimates and measurements, we found that 14 sharks had been under-estimated by 0.2–4.4 m, three sharks had been

over-estimated by 0.4–0.8 m and three estimations were correct (r2 = 0.6).

Satellite tracks

The tag location estimates are assigned a quality depend-ing on the associated error of the position and number of messages received per pass. When at least four messages are received, a numerical quality class is assigned from 0 (>1500 m error) to 3 (<250 m error). For fewer messages, the estimate is assigned a letter, either A, B or Z, in decreas-ing quality, and no error is provided. We calculated the dis-tance between each successive point using the Vincenty’s formula to calculate the distance between two points on a spheroid in the geosphere package in R (Hijmans et al. 2012; R Core Team 2013). We then applied an iterative for-ward/backward averaging filter (McConnell et al. 1992) to remove locations with large error, using a maximum veloc-ity of 2 ms−1 (Gunn et al. 1999; Gleiss et al. 2011). For the resulting tracks, we determined when the tag had released from the shark based on timing and quality of message cri-teria presented by Hearn et al. (2013). We selected a single point for each day based on quality (2 and 3 were preferred over A and B) and proximity to midday. Movement rated and distances travelled were calculated using the resulting daily positions.

Results

Satellite tracking

We had 184 encounters with whale sharks during 44 days (40 at Darwin Island, 4 at Wolf Island) in 2011 and 2012 (Table 1). We estimated that these encounters represented 80 different sharks, 67 identified with photo-identification software. All of them were females except for one male (7.2 m long). None of the sharks had been previously identified elsewhere in the global whale shark photo-iden-tification database, Wildbook for Whale Sharks (www.whaleshark.org). We had 1–4 encounters with whale sharks during each dive (mean = 1.29 encounters).

Table 1 Encounter rates and probable number of individual sharks identified per trip 2011–2012

Date # Days # Dives # Encounters Probable # individuals Encounters per dive Satellite tags deployed

July 11 7 24 34 20 1.60 14

September 11 10 30 10 7 0.33 7

October 11 9 26 17 6 0.70 3

September 12 8 33 73 26 2.21 8

October 12 10 30 50 21 1.67 8

Total/mean 44 143 184 80 1.29 40

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The tagged females ranged from 4 to 14 m long. All were longer than 8 m (mean = 10.4 m) except for 3 juve-niles. That size range was consistent with the non-tagged females encountered and contrasts with most other stud-ies of whale sharks elsewhere where most sharks observed have been estimated at between 3 and 8 meters long (Fig. 1). All but two of the large (>8 m) females had dis-tended abdomens.

We tagged 39 whale sharks at the Darwin Arch dive site at Darwin Island with satellite transmitters. We used 29 SPOT5 tags (which provided 21 tracks), four SPLASH tags (which provided 2 tracks), six SeaTags (which provided 3 tracks) and one pop-up tag with depth records (WS-36, Table 2). Two SeaTags did not report, while all the other SPOT5 and SPLASH tags detached from the sharks the same day and transmitted while floating at the surface. Tracks ranged from 9 to 176 days (median = 47 days), with sharks detected on average 44 % of the track dura-tion (every 2 days). The tags transmitted from a broad geographic area ranging over 800 km in latitude from −12.9° to −5.4° and almost 4000 km in longitude from −80.4° to −116.8°, including national waters of Peru, Ecuador, Colombia, Costa Rica and the high seas. All of sharks appeared to move away from Darwin Island within 1–2 days of tagging. The straight-line distance between tagging and detachment ranged from 49 km over a 9-day period to 2553 km over a period of 55 days. Overall speeds (from first to last position) ranged from 5 to 113 km day−1 (average 27 km day−1). These are conservative values, however, as movements were probably not in a straight line.

Five of the adult females were tracked for less than 2 weeks (Fig. 2), though three of them (WS-21, WS-25

and WS-29) moved out of the GMR during that period. In particular, WS-21 travelled at least 880 km over 12 days. WS-31 moved 40 km, almost to the boundary of the GMR in 10 days. WS-6 moved 10.7 km to the north during the 14 h that the tag transmitted.

Five of the adult females that were tracked longer were tagged in July 2011. All of them made long-distance movements of >1000 km west along the South Equatorial Current (SEC) into the open ocean and then apparently returned along a similar path. The longest of those tracks (WS-9) was 170 days; it showed moved almost 2000 km west in 46 days before returning to within 75 km of Dar-win Island 100 days after it was tagged there and then turned south in mid-October and then east toward the coast of Peru. The tag detached off the shelf break of northern Peru, 1430 km from Darwin Island, although the greatest distance between two points on this track was 2770 km, while covering about of 6536 km, at an average speed of 60 km day−1 (Fig. 3).

None of the sharks identified by the dive teams were seen again later in the year or the next year. One female tagged in July 2011 (WS-7; Table 2) was photographed (Dr. Andrea Marshall, Marine Megafauna Foundation, pers. comm) in October 2011 at Darwin Island, although the tag had stopped transmitting a month earlier about 800 km west of the island (Fig. 3).

Only one of the sharks tagged later in 2011 moved west (WS-16). WS-20 moved 100 km to the north then returned to within 30 km of Darwin Island a week later. The remain-ing five sharks moved toward the east, initially in the area of ocean between the Galapagos Islands and the shelf break of mainland Ecuador. One of those (WS-14) came as close to shore as the entry to the Gulf of Guayaquil before

Fig. 1 Length–frequency distribution of whale sharks fitted with satellite tags from the Galapagos Marine Reserve (this study) in comparison with the rest of the world (data from Berumen et al. 2014; Hueter et al. 2013 and cf. Sequeira et al. 2013, where sizes were grossly estimated)

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Tabl

e 2

Tag

ging

dat

a an

d tr

ack

leng

th in

form

atio

n fo

r w

hale

sha

rks

used

in th

is s

tudy

IDTo

tal l

engt

h (m

)aD

ate

tagg

edTa

g ty

peL

ast d

etec

tion

Tra

ck le

ngth

(d

ay)

# D

ays

dete

cted

Prop

ortio

n da

ys

dete

cted

Dis

tanc

e D

arw

in–l

ast

posi

tion

(km

)

Max

dis

t fro

m

Dar

win

(km

)M

ax d

ist 2

po

ints

(km

)C

umul

ativ

e di

stan

ce (

km)

WS-

14.

27/

8/11

SPO

T5

8/22

/11

4736

0.77

1799

1799

1799

2517

WS-

28.

07/

12/1

1SP

OT

58/

10/1

130

50.

1713

1713

1713

1713

28

WS-

34.

07/

10/1

1SP

OT

57/

29/1

121

200.

9722

4222

4222

4223

18

WS-

49.

57/

11/1

1SP

OT

57/

11/1

1

WS-

510

.07/

14/1

1SP

OT

57/

14/1

1

WS-

610

.27/

15/1

1SP

OT

57/

15/1

1

WS-

711

.07/

14/1

1SP

OT

59/

4/11

5311

0.21

602

602

783

1315

WS-

810

.07/

9/11

SPO

T5

7/9/

11

WS‑

911

.57/

8/11

SPO

T5

12/2

4/11

170

370.

2214

3214

3228

8365

36

WS-

109.

67/

11/1

1SP

OT

57/

11/1

1

WS-

1111

.17/

13/1

1SP

OT

57/

13/1

1

WS-

129.

07/

13/1

1SP

OT

511

/2/1

111

312

0.11

2026

2026

2026

2133

WS-

1310

.07/

14/1

1SP

OT

511

/21/

1113

234

0.26

940

2724

2724

5634

WS-

1411

.49/

10/1

1SP

OT

53/

2/12

176

134

0.76

1357

1408

1371

7323

WS-

1512

.79/

1/11

SPO

T5

11/7

/11

685

0.07

1212

1212

1212

1626

WS-

1612

.49/

10/1

1SP

OT

510

/4/1

126

30.

1212

8712

8712

8713

37

WS-

1711

.09/

9/11

SPO

T5

9/9/

11

WS-

1812

.09/

10/1

1SP

OT

51/

6/12

119

290.

2412

9612

9612

9638

69

WS-

1911

.09/

1/11

SPO

T5

10/1

/11

315

0.16

142

142

142

173

WS‑

2010

.89/

8/11

SPO

T5

10/1

5/11

3827

0.71

297

571

571

1801

WS-

2111

.010

/23/

11SP

OT

511

/3/1

112

20.

1688

888

888

888

7

WS-

2210

.010

/27/

11SP

OT

51/

15/1

281

130.

1615

6015

6015

6022

43

WS-

238.

010

/28/

11SP

OT

510

/28/

11

WS-

249.

09/

3/12

SPL

ASH

9/3/

12

WS-

259.

09/

4/12

SPL

ASH

9/15

/12

128

0.67

346

346

446

631

WS-

2613

.19/

4/12

SPO

T5

9/20

/12

172

0.12

349

349

349

349

WS‑

275.

69/

5/12

SPO

T5

10/6

/12

3231

0.96

1738

1738

1887

2224

WS‑

2811

.29/

6/12

SPL

ASH

10/2

4/12

5040

0.80

656

656

1265

2952

WS-

2912

.59/

6/12

SPO

T5

9/12

/12

77

1.00

221

221

221

234

WS-

3011

.09/

6/12

SPO

T5

1/25

/13

142

160.

1118

9419

7219

7223

31

WS-

3112

.59/

7/12

SPO

T5

9/16

/12

103

0.29

4949

4950

WS-

3210

.910

/13/

12SP

OT

510

/13/

12

WS-

3312

.010

/13/

12Se

aTag

10/1

3/12

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moving offshore again (Fig. 4). By December 2011, the four sharks that still retained their tags were off the shelf break of northern Peru, in a similar location to WS-9 described above.

The whale sharks tagged in 2012 provided tracks rang-ing from 7 to 142 days (Table 2). Of the seven adults tracked longer than 14 day (Fig. 5), two remained within the GMR. WS-26 was located just once when 350 SE of Darwin Island 17 days after it was tagged. WS-36 was observed by the dive team at Darwin Island nine times over 7 days but was tracked it appeared in the center of the archipelago 273 km south of Darwin Island 45 days after tagging. It was then photographed at Darwin Island in October 2013 and again in August 2014. WS-28 moved eastward and made large loops extending up to 620 km from Darwin for 3 weeks, before returning to within 50 km of the island. It then continued west another 600 km at about 98 km day−1. WS-35 and WS-38 also moved to the west, the former for over 2700 km before detaching as it reversed direction. WS-30 was first detected 18 days after it was tagged when 500 km east of Darwin. It was next detected 10 weeks later, in December, off the shelf break of Peru, where it might have stayed for about 2 weeks until the tag detached. WS-37 moved northeast to within 80 km of the Cocos Island MPA (Costa Rica) before veering east and eventually before the tag detached on January 18, 2013, within the Malpelo MPA (Colombia), an overall dis-tance of at least 1400 km in 95 days.

The three juvenile females tagged in July 2011 (WS-1, WS-3) and September 2012 (WS-27) were tracked for 31–47 day (Fig. 6). All moved rapidly west, but while WS-3 moved in a constant direction along the SEC at an overall speed of 213 km day−1 before the tag detached 2215 km west of Darwin, WS-1 and WS-27 moved to the southwest and both tags detached in the same general area along the East Pacific Rise, approximately 1800 km from Darwin.

Discussion

Whale sharks appear to be detectable at Darwin Island in the northern region of the Galapagos Marine Reserve occurs mostly from July through November. Virtually all seem to be large females (Hearn et al. 2014). Because there have been few observations of large females anywhere, size at sexual maturity for females is uncertain. All seven females ranging from 4.8 to 8.7 m stranded on beaches in South Africa were immature (Beckley et al. 1997). The pregnant female landed in Taiwan in 1995 was 10.6 m (Joung et al. 1996), while Ramirez-Macias et al. (2012b) suggested that all 23 females (9–13 m TL) observed at two offshore sites in the Gulf of California were pregnant, ID

s in

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fer

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lase

r ph

otog

ram

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her

size

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sual

est

imat

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y di

vers

Tabl

e 2

con

tinue

d

IDTo

tal l

engt

h (m

)aD

ate

tagg

edTa

g ty

peL

ast d

etec

tion

Tra

ck le

ngth

(d

ay)

# D

ays

dete

cted

Prop

ortio

n da

ys

dete

cted

Dis

tanc

e D

arw

in–l

ast

posi

tion

(km

)

Max

dis

t fro

m

Dar

win

(km

)M

ax d

ist 2

po

ints

(km

)C

umul

ativ

e di

stan

ce (

km)

WS-

3410

.010

/15/

12SP

LA

SH10

/15/

12

WS-

3511

.810

/15/

12Se

aTag

12/9

/12

5653

0.95

2553

2747

2747

4694

WS-

3612

.510

/15/

12Se

aTag

11/2

8/12

452

0.04

270

270

270

270

WS-

3712

.810

/16/

12Se

aTag

1/18

/13

9576

0.80

1227

1335

1335

2581

WS-

3811

.410

/19/

12Se

aTag

12/3

/12

4631

0.67

1519

1526

1526

1747

WS-

3912

.010

/20/

12Se

aTag

10/2

0/12

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based solely on their distended abdomens. Most females that we observed were >8 m long and had distended abdo-mens so they might have been pregnant.

Throughout this study, and in the three decades of dive tourism preceding it, we know of only a single report of a feeding episode. If whale shark aggregations occur for

feeding and as a response to local plankton blooms and spawning events (Riley et al. 2010; Ketchum et al. 2013), then we might expect whale sharks to be more common in the western and southwestern part of the Galapagos Marine Reserve given the influence of the highly produc-tive upwelling Equatorial Undercurrent (EUC) (Palacios

Fig. 2 Short-term tracks (<2 weeks) from 2011 and 2012

Fig. 3 Long-term (>2 week) tracks from whale sharks tagged in July 2011

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2002, 2004). This region of the GMR is remote and vis-ited only rarely by fishers or tourists, although the first record for a whale shark in Galapagos was in this region—a large female reported to the north of Fernandina Island in June 1925 (Beebe 1926; Gudger 1927). A second small individual was reported at Isabela Island in spring of

1933 (Gudger 1933). In March and April 1985, four large females were observed south of the island of Isabela (Arn-bom and Papastavrou 1988), coinciding with the period of greatest primary productivity in this region.

Darwin and Wolf Island share similar oceanographic set-tings, with a predominantly northwesterly current splitting

Fig. 4 Long-term (>2 week) tracks from whale sharks tagged in September and October 2011

Fig. 5 Long-term (>2 week) tracks from whale sharks tagged in 2012

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around each island. Where the current impinges upon each island and splits, large aggregations of marine life are often found, like hammerhead sharks, Galapagos sharks and sev-eral species of jack that interact with the reef environment by sometimes preying on reef fish and at other times being cleaned by them (Hearn et al. 2010; Ketchum et al. 2014). Large groups of hammerhead sharks are also very socially active there (Klimley 1987). Whale sharks occur there at times too, particularly near Darwin Island (Acuña-Marrero et al. 2014). However, interactions with reef cleaner fish here have not been reported, and the only observed inter-action between two whale sharks occurred when a larger female swam into the path of a smaller female and knocked her flank with her pectoral fin. Interspecific interactions were limited to remoras attached to the sharks, and to an observation by the authors of a small group of bottlenose dolphins bow-riding, similar to that reported by Latusek-Nabholz et al. (2014) and to Galapagos and silky sharks and jacks swimming alongside the whale sharks, occasion-ally rubbing against their flanks.

Other oceanic islands where whale sharks may be found include St. Helena Island in the South Atlantic, where adult males and females are often seen, along with occasional smaller animals, where they apparently feed (A Dove. Georgia Aquarium, pers comm). At St. Peter and St. Paul Archipelago in the Central Atlantic, whale sharks rang-ing from an estimated length of 1.8 m to 14 m have been reported (Hazin et al. 2008). Feeding behavior has not been reported there, and Hazin et al. (2008) suggested that whale sharks might be giving birth there instead. Hueter

et al. (2013) also suggested that too after tracking an large (7.5 m), and possibly female from the Gulf of Mexico to a mid-Atlantic location 543 km southeast of St. Peter & St. Paul over a period of 150 days. Whale shark neonates have not yet been reported, however, at St. Peter & St. Paul or at Darwin Island, and the distended abdomens of large females seen there might not necessarily imply pregnancy (Ramirez-Macias et al. 2012b, Hearn et al. 2013).

While coastal aggregations are related to feeding, oce-anic movements suggest influence of prevailing geos-trophic currents (Rowat and Gore 2007), boundary currents and local bathymetry (Hsu et al. 2007). The July–August oceanic movements of whale sharks at Darwin Island cor-related with the westward flowing South Equatorial Cur-rent (SEC) and close to the Equatorial Front (EF), which separates the SEC from the eastwards flowing North Equa-torial Counter Current (NECC) and is biologically pro-ductive area that evidently attracts planktivorous seabirds (e.g., Wyrtki 1966; Spear et al. 2001). The EF extends from south of the equator off the coast of Ecuador to 1°–3°N to the west of Galapagos and is most pronounced from May through November (Wyrtki 1966). That might be an area where the females are feeding. Motta et al. (2010) sug-gested that the filtering structures of whale sharks are una-ble to cope with high rates of water flow through them, but with average sustained surface ram filter feeding veloci-ties of 0.3–1.5 ms−1 (Motta et al. 2010) the general daily movement rates of the sharks tracked in this study do fall within that range. Similarly, the final locations of some of the sharks we tracked were just seaward of the continental

Fig. 6 Track from 3 immature female whale sharks (WS#1, WS#3 and WS#27)

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shelf of mainland Ecuador and northern Peru in December and January. That area is the near-equatorial subsystem of the Humboldt Current (Bakun and Weeks 2008). It is warmer than water farther south and primary production peaks there from December through March (Thomas et al. 1994) which coincides with the presence of at least a few whale sharks. It also often generates the major proportion of the entire Humboldt system’s fish production (Bakun and Weeks 2008).

Rowat and Brooks (2012) remarked that despite the growing number of whale shark tracking studies, true migration, in the form of a long-distance movement fol-lowed by a return movement to the same location, has yet to be detected using tagging data alone. In Hearn et al. (2013), we reported the first such movements of all three large females that were tagged at Darwin, moved away for distances of several hundred kilometers, then returned to within 75 km of the island several weeks later (these sharks correspond to WS#9, 20 and 38 in this study). Two whale sharks fitted with acoustic devices returned to Darwin and Wolf Islands after being out of range of the receivers from more than a month (Hearn, unpublished data), while another two sharks were identified from pho-tographs at Darwin Island after their tags had detached. We tracked one shark (WS#7) over a distance of 800 km to the west of Darwin Island, and another shark (WS#36) was first detected when the pop-up tag detached 273 km to the south of Darwin in the central region of the Galapagos Islands 45 days after it was attached. In all those cases, the recorded presence of these sharks for a second time was brief similar to their previous visit. Long-distance return movements are only one component of migration, which is a biological phenomenon that includes important behav-ioral and physiological aspects (Dingle 1996; Dingle and Drake 2007). These include persistent, straightened out locomotory activity, and relocation that is likely on a much greater scale than that arising from normal daily activities. Although our dataset may appear to show this, the time intervals between detections do not persuasively demon-strate migration. A second component of migration implies the movement from one habitat to another. The sharks did move between habitats, from an oceanic islet, reef-associ-ated habitat (Acuña-Marrero et al. 2014) to the Equatorial Front and then to the shelf break of the continental land-mass of South America. However, migration also implies that the organisms are undistracted by stimuli that would otherwise trigger a response under non-migratory condi-tions, that there are distinct behaviors associated with leav-ing and arriving and that migrants reallocate energy specifi-cally to support movement (Kennedy 1985; Dingle 1996). Evidently, these characteristics cannot be inferred from our dataset and in any case are difficult to detect in a marine

system. It is possible that the movements we describe are part of a seasonal migration carried out by large females within the region, but further study is required to determine whether these movements fulfill the biological definition of migration.

Globally, excluding this current study, only 189 whale shark tracks using satellite tags are described in the scien-tific literature (cf., Eckert and Stewart 2001; Wilson et al. 2006; Sequeira et al. 2013; Hueter et al. 2013; Berumen et al. 2014). Of those sharks, only three were longer than 10 m, and all three were female. Two were from the Gulf of California (Eckert and Stewart 2001), and one was from Ningaloo Reef, Western Australia (Wilson et al. 2006). Most other tracks were of immature males, reflecting the size and sex structure of most areas where whale sharks are seen. Although many of the tracks in the literature are short (median reported duration = 70 days), the median distance travelled by whale sharks was 379 km, which indicates that whale sharks are present for long at any site. Once they leave those areas, the sharks appeared to disperse widely with no consistent pattern (Eckert and Stewart 2001; Eck-ert et al. 2002; Hsu et al. 2007; Hueter et al. 2013; Beru-men et al. 2014), though six sharks tagged at Ningaloo Reef moved northeast into the Indian Ocean (Wilson et al. 2006). Long-distance movements of several thousand kilometers have been reported, notably a 7.5-m female whale shark tagged in the Gulf of Mexico which was tracked over a dis-tance of 7213 km to the mid-Atlantic St. Peter and St. Paul Archipelago in 2007 (Hueter et al. 2013), and was subse-quently identified back in the Gulf of Mexico in 2011 (De la Parra, Proyecto Domino, Comision Nacional de Areas Natu-rales Protegidas Quintana Roo, Mexico pers. Comm.).

Most information about whale sharks comes from coastal mainland or island sites where they appear at the surface briefly at some seasons. Most sharks that are seen there are immature males, some that have been observed feeding. Other observations from fishing industries sug-gest that at least some sharks live alone in pelagic habitats at times. The results from our study provide insight into a segment of the population that we know little about, in a geographic region and environmental context that we think could be key to better understanding their biology.

Acknowledgments Our study was funded by a grant from the George, Blake and Kimberly Rapier Foundation to the Galapagos Whale Shark Project (through Conservation International and the Galapagos Conservancy) and by the Galapagos Conservation Trust. Fieldwork was carried out under permits (PC-37-11 and MAE-PNG/CDS-2012-0020) issued by the Galapagos National Park Directorate. We thank the Captain and Crew of the MV Queen Mabel, and to the staff and volunteers from the Charles Darwin Foundation and Galapa-gos National Park Directorate who participated in the fieldwork, espe-cially Cesar Peñaherrera, Yasmania Llerena, Inti Keith, Jules Paredes and Gabriel Vazquez.

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Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

Ethical approval All procedures performed in studies involving ani-mals were in accordance with the ethical standards of the University of California Davis, under IACUC Protocol #16022, and with permission from the authority of the Galapagos Marine Reserve in the figure of Permit PC-37-11 from the Galapagos National Park Directorate.

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