MURDOCH RESEARCH REPOSITORY · shark mating behaviour at Ningaloo (Holmberg et al., 2008). The sea...

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The definitive version is available at http://dx.doi.org/10.1016/j.ecss.2014.05.023

Anderson, D.J., Kobryn, H.T., Norman, B.M., Bejder, L., Tyne, J.A. and Loneragan, N.R. (2014) Spatial and temporal patterns of

nature-based tourism interactions with whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Estuarine, Coastal and Shelf Science, 148 . pp. 109-119.

http://researchrepository.murdoch.edu.au/22932/

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Contents lists avai

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

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Spatial and temporal patterns of nature-based tourism interactionswith whale sharks (Rhincodon typus) at Ningaloo Reef, WesternAustralia

Douglas J. Anderson a, Halina T. Kobryn a, Brad M. Norman a, b, Lars Bejder a,Julian A. Tyne a, Neil R. Loneragan a, *

a Murdoch University Cetacean Research Unit, School of Veterinary and Life Sciences, Murdoch University, Murdoch, Western Australia 6150, Australiab ECOCEAN, 102/72 Marine Tce, Fremantle, Western Australia 6160, Australia

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a r t i c l e i n f o

Article history:Received 23 December 2013Accepted 25 May 2014Available online xxx

Keywords:reef passagessouthern oscillationLa Ni~naoceanic frontsecological distributionmanagement

* Corresponding author.E-mail address: [email protected] (N.R

http://dx.doi.org/10.1016/j.ecss.2014.05.0230272-7714/© 2014 Published by Elsevier Ltd.

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Please cite this article in press as: Anderson(Rhincodon typus) at Ningaloo Reef, Western

a b s t r a c t

As with other nature-based tourism ventures, whale shark tourism is expanding rapidly worldwide,which highlights the need to understand more about the nature of these activities. Records of in-teractions between tour operators and whale sharks at Ningaloo Reef, Western Australia (22.5�S, 113.5�E)were obtained from the Western Australian Department of Parks and Wildlife from 2006 to 2010 andevaluated to determine the scale of the tourism operations and the spatial and temporal distribution ofinteractions. The number of whale shark tours at Ningaloo increased by approx. 70% (520e886 tours peryear) and the number of interactions with whale sharks by 370% between 2006 (694) and 2010 (3254).The locations of whale shark interactions recorded in logbooks (2006e2009) and electronic monitoringsystems (2009 and 2010) were used to plot the smoothed densities of tour operator interactions withwhale sharks. Generalised linear models were used to investigate how the presence/absence and numberof whale shark interactions at North and South Ningaloo were influenced by the distance to the reefcrest, the distance to passages and their interaction terms for the aggregated five-year data set. Over thefive years, distance to the reef crest was the best predictor of the presence/absence of whale shark in-teractions at both North (interactions concentrated within 3 km of the reef crest) and South Ningaloo(interactions within 6 km of the reef crest) followed by distance to passages. The reef passages are verysignificant areas for tourism interactions with whale sharks at Ningaloo. The distribution of interactionsat North and South Ningaloo varied from year to year, particularly in the strong La Ni~na year of 2010,when average sea surface temperatures remained above 24 �C and whale sharks were observed muchlater in the year than previously (late August). This study demonstrates the value of the data collected bythe tour operators at Ningaloo Reef and managed by a government agency for the conservation andsustainable whale shark tourism.

© 2014 Published by Elsevier Ltd.

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1. Introduction

The whale shark, Rhincodon typus, is a migratory species thatinhabits tropical and warm temperate waters throughout theoceans (Meekan et al., 2006; Holmberg et al., 2009; Sequeira et al.,2013). They are sighted annually at many locations including Nin-galoo Reef, Western Australia in the Indian Ocean and Belize in theAtlantic Ocean, where they aggregate at times of peak food avail-ability brought about by coral and fish spawning (Heyman et al.,

. Loneragan).

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, D.J., et al., Spatial and tempoAustralia, Estuarine, Coastal

2001; Wilson et al., 2001). Whale shark aggregations have alsobeen identified at Donsol in the Philippines, the Seychelles and atMozambique (Quiros, 2007; Rowat et al., 2007; Pierce et al., 2010).The predictable nature of these aggregations provides the basis fora growing nature-based tourism industry that offers patrons theopportunity to swim with a whale shark (Holmberg et al., 2009).Investigating the spatial and temporal patterns of these aggrega-tions can help to better understand the factors influencing whaleshark movements and habitat use and as a consequence, identifyareas that may need higher levels of protection in order to helpconserve whale sharks.

Nature-based tourism operations that observe and interact withmarine megafauna (e.g. whales, dolphins, pinnipeds and sharks)

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ral patterns of nature-based tourism interactions with whale sharksand Shelf Science (2014), http://dx.doi.org/10.1016/j.ecss.2014.05.023

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have increased greatly worldwide in recent times (O'Connor et al.,2009; Brunnschweiler, 2010; Vianna et al., 2012; O'Malley et al.,2013; Tyne et al., 2014). For example, in 2009 the cetacean-watchtourism industry exceeded an annual turnover of US $2 billion,with 13 million passengers paying to observe whales and dolphinsin their natural environment (O’Connor et al., 2009). Concerns havearisen that the scale, and lack of appropriate management of thisindustry, may be having detrimental effects on the targeted pop-ulations; through repeated disturbance (Lusseau, 2004; Bejderet al., 2006; Williams et al., 2006). This concern was documentedin 2006, when the International Whaling Commission (IWC) notedthat “there is compelling evidence that the fitness of individualodontocetes (toothed whales) repeatedly exposed to whalewatching vessel traffic can be compromised and that this can leadto population-level effects” (IWC, 2009). This highlights the need tobetter understand the nature and extent of interactions with thesefauna. Other groups of marine megafauna have also been nega-tively affected by increasing nature-based tourism. For example,feeding stingrays in the Cayman Islands decreased the health andincreased the parasite loads of stingrays inside the tourism areacompared with stingrays outside this area (Semeniuk et al., 2009).In a recent review of the biology, fisheries and conservation of thewhale sharks, Rowat and Brooks (2012) summarised trends inwhale shark tourism from around the world. Expanding whaleshark tourism industries have led to declines in the number ofwhale sharks sighted in Belize and effects on the behaviour ofsharks in Donsol, Philippines. Concerns have been raised about thepossible impacts of tourism on whale sharks off the YucatanPeninsula in Mexico, where large numbers of vessels operate(z140) (see Rowat and Brooks, 2012).

Whale sharks aggregate annually at Ningaloo Reef betweenMarch and July (Mau and Wilson, 2007; Holmberg et al., 2008;Sleeman et al., 2010a) but the number of sharks observed variesfrom year to year (Wilson et al., 2001). The timing of the sharkarrival coincides with the annual mass coral spawning (Taylor,1996), which generally occurs after the full moon in March andApril (Simpson, 1991; Taylor, 1996; Rosser and Gilmour, 2008). Themass coral spawning produces elevated levels of zooplankton,which provides abundant food for the whale sharks (Taylor, 1996).Sharks are often observed feeding at Ningaloo (Gunn et al., 1999;Taylor, 2007), where they appear to target mainly high densitysurface assemblages of the krill Pseudeuphausia latifrons (Jarmanand Wilson, 2004). To date, there has been no evidence of whaleshark mating behaviour at Ningaloo (Holmberg et al., 2008).

The sea surface temperature (SST) also appears to influence themovement of whale sharks at Ningaloo, with most sharks seen inwarmer waters of between 27 and 31 �C (Sleeman et al., 2007). TheSST along the coast of Western Australia is influenced by thestrength of the Leeuwin Current, a warm water, nutrient poor,southward flowing current that originates in tropical waters to thenorth of Australia (Cresswell and Golding,1980;Wilson et al., 2001;Feng et al., 2009). In La Ni~na years, the current is stronger andtransports more warm water further south, which increases watertemperatures at Ningaloo Reef (Wilson et al., 2001; Feng et al.,2009). The concentration of chlorophyll-a may also influence themovement of whale sharks, as most are sighted in regions withhigher chlorophyll-a concentrations (Sleeman et al., 2007).

The whale shark tourism industry at Ningaloo Reef began in1989 (Catlin et al., 2010) and has prospered since then, with touristnumbers increasing from 1000 in 1993 to over 17,000 in 2011(DPaW, 2013). In 2006, the estimated value of the whale sharktourism industry to the local economy was AUD $6 million (Catlinet al., 2010), a value which has subsequently increased, withparticipant numbers continuing to grow every year (DPaW, 2013).The Western Australian Department of Parks and Wildlife (DPaW,

Please cite this article in press as: Anderson, D.J., et al., Spatial and tempo(Rhincodon typus) at Ningaloo Reef, Western Australia, Estuarine, Coastal

formally known as the Department of Environment and Conser-vation) manages the whale shark tourism industry in the NingalooMarine Park and has allocated a restricted number of licences since1993 (Catlin et al., 2011). Under the conditions of their licences, touroperators are required to record information on each tour,including the location of interactions with whale sharks (Mau andWilson, 2007). The data collected by tour operators provide aunique source of information to investigate the sighting patterns ofwhale sharks in this region (Wilson et al., 2001).

The objectives of this study were to 1) describe the pattern oftour operator effort at Ningaloo Reef between 2006 and 2010 todetermine how the intensity of operations has changed over thisfive-year period; 2) investigate the inter-annual variation in thedistribution of whale shark tourism interactions at Ningaloo Reefbetween 2006 and 2010, and 3) determine whether the patterns ofwhale shark interactions differed between the northern andsouthern regions of the Ningaloo Marine Park.

2. Materials and methods

2.1. Study area and environmental data

The NingalooMarine Park extends fromPointMurat (21�50’S) inthe north, around the North West Cape and continues south to RedBluff, extending along approximately 300 km of coastline (Fig. 1).The marine park has been divided into recreation, sanctuary andgeneral use zones in order to control human activities(Commonwealth of Australia, 2002).

Monthly values of the Southern Oscillation Index (SOI), which isused as a measure of the strength of the El Nin~o Southern Oscil-lation (ENSO), were retrieved from the Bureau of Meteorology(BOM) for the years from 1990 to 2011 (BOM, 2013a). Prolongedperiods of negative SOI values < �8 generally indicate El Nin~oconditions, whereas prolonged periods of positive SOI values >8generally indicate La Ni~na conditions (BOM, 2013b). The rainfalldata recorded at Learmonth Airport (35 km south of Exmouth),between 2006 and 2010 were retrieved from the BOM. The averagemonthly sea surface temperature data were calculated from dailyvalues retrieved from the Ningaloo Atlas for North and SouthNingaloo over the same period (NOAA Coral Reef Watch, 2013).

2.2. Tourism operations and data

The number of whale shark licences issued at Ningaloo hasvaried between 13 and15 since 1993, with 14 licenses operatingcurrently. Three operators are located at Coral Bay in the south and11 are in the north (Catlin et al., 2011). An average of five to sevenvessels take whale shark tours on any given day during the peakwhale shark season at North Ningaloo (i.e. departing from Tanta-biddi), with a maximum of 10 vessels.

Three vessels operate from Coral Bay in South Ningaloo. From1995 to 1999, it was common for each vessel to engage their ownspotter plane at North Ningaloo but since then, some operatorshave shared spotter planes. From 2006 until 2010, one shared planeoperated from South Ningaloo and two or three planes haveoperated from North Ningaloo (one shared, and one or two singleoperator planes).

The tours leave themoorings at about 08:00 andwhen a shark islocated early in the day (i.e., before midday), finish by about 14:00.If whale sharks take time to locate, spotter planes continuesearching and boats remain on the water until 15:30 at the latest, toallow the tour to return to shore by 16:00. If a whale shark is notfound, operators guarantee that the participants will be able to goon another tour.


Fig. 1. Map of the Ningaloo Reef study site showing the North and South Ningaloo regions and the Ningaloo Marine Park (State waters). Red Bluff at the southern extent of the park,is about 110 km south of Coral Bay.

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Whale shark operators tend to minimise the amount of fuelconsumed on any given day and in the north (departing Tantabiddi)decide whether they go out through North Passage or South Pas-sage. They often instruct the pilots to begin their search byconcentrating between these two points on the reef and to focus onopenings in the reef where whale sharks often surface. If no sharksare found after an hour of searching, pilots are instructed to expandtheir search up to 30 km further south, increasing the transit timeand fuel costs significantly. The northernmost extent of each searchby the spotter planes is North Passage along the reef front, some-times out to ~5 km off the reef.

Tour operators will pass, or ‘hand-ball’, a shark to anotheroperator in close proximity. This practise ensures that all touristshave the opportunity to swimwith awhale shark at least once. Dataon “hand-balling” are complete only for 2010, when it was esti-mated that 46% of the total of 3254 recorded interactions werehandballed to another operator. Each vessel records the interaction


separately and thus the number of interactions includes data onrepeat interactions with the same individual on the same day.Wilson et al. (2001) note that if the numbers of interactions is usedas an index of abundance, the index is over-inflated when whalesharks are scarce and proportionally more sharks are hand-balledthan when whale sharks are abundant.

Data on interactions between whale sharks and tour operators(hereafter referred to as “interactions”) were obtained from DPaWfor the years between 2006 and 2010; this information was recor-ded in logbooks from 2006 to 2008 and for a small proportion ofinteractions in 2009. The remainder of the interactions in 2009 andall those in 2010 were recorded in the Electronic Monitoring Sys-tems (EMS). Data on the number of tours were also provided byDPaW.

In 1995, logbooks were introduced for recording data on whaleshark tour operations by DPaW (Mau and Wilson, 2007). Sincethen, whale shark tour operators have been required to record data


Table 1Pearson correlation values to test the relationship between different variables forinclusion in generalised linear model analyses to predict the presence/absence andnumbers of whale shark interactions. Long. ¼ longitude; Lat. ¼ Latitude.Dis. ¼ Distance, Cr. ¼ Crest. N ¼ number of grid cells. All correlations significant atP < 0.001.

Variable Long. Lat. Depth Distance to passage

South North Nearest

a) North (N ¼ 4915)Latitude 0.49Depth 0.66 �0.26Dis. South �0.33 �0.32 �0.21Dis. North �0.78 �0.89 �0.15 0.53Dis. Nearest �0.74 �0.59 �0.36 0.82 0.84Dis. Reef Cr. �0.59 0.38 �0.95 0.23 0.05 0.31

Main Passage 1 Nearestb) South (N ¼ 15,209)Latitude �0.07Depth 0.63 �0.43Dis. Main �0.68 0.21 �0.60Dis. Passage 1 �0.18 �0.91 0.10 0.12Dis. Nearest �0.65 �0.55 �0.28 0.58 0.78Dis. Reef Cr. �0.91 �0.27 �0.40 0.47 0.42 0.78


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on the daily operations of the tour, any interactions with whalesharks and details of individual sharks. The following details arerecorded for each trip: the number of paying passengers and thestart and finish times of the tour. The time the shark was observedis recorded as well as the GPS coordinates of the sighting location,depth, length estimate, sex and whether or not the shark waspassed on to another operator (‘handballed’) (Mau and Wilson,2007).

The EMS records similar information to the logbooks, with moredetail on the interactions with the sharks. The start and end of theinteraction are recorded and the GPS coordinates are logged auto-matically when the start contact button is pressed. Informationrecorded about the shark includes sex (where possible), length andswimming direction and whether it is a new shark for that day andif the shark was handballed to another operator.

In 2009, 17% of the interactions were recorded in logbooks andthe rest in the EMS, while in 2010; all data were recorded in theEMS. Data on the number of tours were investigated for the wholeof Ningaloo Reef. The number of interactions and the number ofdays in which interactions took place were calculated for eachmonth of the main whale shark season (March to July, inclusive)between 2006 and 2010. The average number of tour boats oper-ating on days when interactions with sharks were recorded wasalso calculated for each season between 2006 and 2010.

2.3. Spatial analyses

The logbook and EMS interaction data were analysed in ArcGIS10. Spatial analyses were performed using plots of the interactionlocations (x, y coordinates), which were filtered to remove anyoutliers. At North Ningaloo, all interactions south of 22�30’S, northof 21�45’S, on the landward side of the reef crest and beyond 8 kmseaward of the reef crest were excluded. At South Ningaloo, allinteractions north of 22�30’S, south of 23�30’S, on the landwardside of the reef crest (except those in the main passage just to thenorth of Coral Bay) and >18 km seaward of the reef crest wereexcluded. These criteria for filtering were based on knowledge ofwherewhale sharks are sighted and where tour boats are willing totravel (B. Norman, ECOCEAN, unpublished data). Once the data havebeen filtered, two study areas were mapped out, one at NorthNingaloo and one at South Ningaloo (Fig. 1), which represent thetwo regions where all whale shark interactions were recorded.

Kernel densities of the number of interactions per km2 werecalculated in ArcGIS 10, using cell sizes of 500 m � 500 m and asearch radius of 1000 m (taken from the centre of the cell). Maps ofkernel density were produced for all years combined and each yearfrom 2006 to 2010 for North and South Ningaloo separately. A gridwith 500 m � 500 m cells was overlaid on to the North Ningaloostudy area and intersected with the interaction locations from 2006to 2010, providing a measure of the number of interactions per gridcell (interaction grid). The interaction grid was intersected withfactors including bathymetry and Euclidean (straight-line) distanceto the north passage, south passage and the reef crest. Points werecreated at the centre of the north and south passage (Fig. 1) tocalculate the distance from each passage to the mid-point of eachgrid cell. The interaction data and the factors investigated at SouthNingaloo were processed in the same way as North Ningaloo,except that two different passages (passage 1 and main passage)were used (Fig. 1).

2.4. Data analyses

Pearson correlation analyses were used to examine the re-lationships between the following factors; distance to reef crest,distance to passages (north and south passage at North Ningaloo,


passage 1 and main passage at South Ningaloo and nearest passageat both sites), latitude, longitude and bathymetry. The results fromthese analyses were used to select factors for inclusion (Pearsoncut-off ¼ 0.50) in generalised linear models (GLMs), to investigatethe presence/absence (binary logistic model) and the number ofwhale shark interactions (negative binomial with log link model) atNorth and South Ningaloo separately. The negative binomial withlog link functionwas used to investigate the number of interactionsas this approach takes into account the over-dispersion generallypresent in count data (Blundell et al., 1995).

At North and South Ningaloo, correlation analyses indicated thatlongitude, latitude and depth were highly correlated with the dis-tance to passages or the reef crest andwere therefore not entered inthe GLM analyses (Table 1). At North Ningaloo, the distances tonorth and south passage were highly correlated with the distanceto the nearest passage and were excluded. At South Ningaloo thedistance to the nearest passage was highly correlated with thedistance to the reef crest so it was excluded for this site (Table 1).Distance to reef crest and distance to nearest passage at NorthNingaloo and distance to reef crest, passage 1 and main passage atSouth Ningaloo were then fitted to GLMs to determine how wellthey could predict the presence/absence and number of in-teractions with whale sharks.

The GLM analyses were completed using the full five year dataset. Single factor models were fitted first to examine the variationexplained by each main factor, followed by fitting models withother factors and interaction terms. The Akaike Information Crite-rion (AIC) was used to identify the most parsimonious model(Akaike, 1974).

3. Results

3.1. Environmental data

The SOI values were very high from April 2010 until the end of2011, indicating a strong La Ni~na weather pattern (Fig. 2a). Theaverage sea surface temperatures at North and South Ningaloofollowed a similar pattern of seasonal variation but were about 1 �Chigher in the north than the south (Fig. 2b). In 2010, 2011, theaverage SST at North Ningaloo did not fall below 23.9 �C (Fig. 2b).The SSTs were also high at South Ningaloo in 2011 (Fig. 2b). Theannual rainfall in 2006, 2007 and 2009 (134.4e166.4 mm) was


Fig. 3. The number of a) whale shark tours, b) days that whale shark interactions wererecorded between March and July and c) whale shark interactions, from 2006 to 2010.

Fig. 2. Monthly (a) Southern Oscillation Index (SOI) (negative SOI values < �8 indicateEl Nin~o conditions; SOI values > 8 indicate La Ni~na) from the Bureau of Meterology,Western Australia; and (b) average monthly sea surface temperatures at North Nin-galoo and South Ningaloo (NOAA Coral Reef Watch, 2013) from 2006 to 2011.


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much lower than the long-term average rainfall of 253.8 mm (BOM,2013c). The annual rainfall was particularly high in 2008(451.8 mm) and was just above average in 2010 (265.8 mm).

3.2. Tourism interactions with whale sharks

The number of whale shark tours at Ningaloo Reef increasedfrom 520 in 2006 to 886 in 2010 (Fig. 3a). The number of days thatwhale shark interactions were recorded between March and Julyincreased by 68% between 2006 (82) and 2010 (138) (Fig. 3b). Thetotal number of whale shark interactions recorded from March toJuly increased by over 350% between 2006 (694) and 2010 (3254)(Fig. 3c). The highest number of interactions was recorded inMay ineach year except 2007, where it was June (Fig. 4). In 2010, thenumber of interactions recorded in July was higher than the peakmonths of interactions in 2006 and 2007 (Fig. 4) and interactionswith whale sharks were recorded until late August. The averagenumber of interactions per tour has increased nearly three-foldfrom 1.33 interactions per tour in 2006 to 3.67 interactions pertour in 2010. The average number of tour boats operating on daysthat shark interactions were recorded, increased from 4.8 ± 0.3 in2006 to 6.2 ± 0.2 in 2010.

3.3. Spatial and temporal patterns of whale shark interactions

At North Ningaloo, the number of tour vessel interactions withwhale sharks for the five years between 2006 and 2010 showedthat the interactions were concentrated around South Passage,extending from Mangrove Bay (21.95�S) to 22.09�S (Fig. 6). In


contrast, the interactions at South Ningaloo over the whole studyperiod were more widely dispersed, with a concentration outsidepassage 1 and several small concentrations between BruboodjooPoint (22.97�S) and Coral Bay (23.15�S) (Fig. 6). The highest con-centrations of interactions were within 3 km and 6 km of the reef


Fig. 4. The number of whale shark interactions recorded in each month from March toJuly between 2006 and 2010 at Ningaloo Reef.


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crest at North Ningaloo and South Ningaloo, respectively. In-teractions were more widely dispersed away from the reef crest atSouth than North Ningaloo (Figs. 5 and 6).

The kernel density plots for the whale shark interactions in in-dividual years showed some differences in the distribution of in-teractions among years (Figs. 5 and 6). In 2006, 2007 and 2009 themain concentration of interactions at North Ningaloo were southand west of south passage (21.94e22.08�S), with higher concen-trations to the south of this passage (Fig. 5). In 2008, the in-teractions at North Ningalooweremorewidely dispersed (Fig. 5). In2010, interactions at North Ningaloo were generally concentratedfurther north than in the previous four years, particularly comparedwith the high interaction year of 2009 (Fig. 5).

At South Ningaloo, interactions were very patchy in 2006 and2007, apart from a small concentration adjacent to the main pas-sage in 2006 (22.99e23.06�S) (Fig. 6). In 2008, the main concen-tration of interactions at South Ningaloo extended betweenpassage1 and passage 2 (22.76e22.87�S) (Fig. 6). Interactions were evenlydistributed fromPoint Cloates to Coral Bay (22.71e23.19�S) in 2009.In 2010, interactions were concentrated between Bruboodjoo Pointand Coral Bay (22.97e23.15�S), with a large proportion of these inor around the main passage (Fig. 6). Interactions were concentratedmuch further south in 2010 than in the previous four years at SouthNingaloo, with very few interactions occurring north of BruboodjooPoint (Fig. 6).

3.4. Predictors of whale shark interactions

Over the five years from 2006 to 2010, the best single factor forpredicting the presence/absence of whale shark interactions wasthe distance to the reef crest at North and South Ningaloo. Thechange in AIC (D AIC) at North Ningaloo from distance to thenearest passage to distance to the reef crest was about 550, while atSouth Ningaloo, the D AIC between the distance to main passageand the distance to the reef crest was 1514. Distance to reef crestwas also the best single factor predictor for the number of in-teractions at North and South Ningaloo. The multifactor models forthe presence/absence of interactions did not improve the fit overthe single factor models. In contrast, the most parsimonious modelfor predicting the number of whale shark interactions at NorthNingaloo included a combination of distance to reef crest and dis-tance to nearest passage (AIC ¼ 8146.0), compared with the singlefactor model for distance to reef crest (AIC ¼ 8868.6). At SouthNingaloo three factors were fitted to the most parsimonious model


for the number of interactions; distance to reef crest, distance topassage 1 and distance to main passage (AIC ¼ 6208.5), a D AIC of1009 compared with the model for distance to reef crest only.

4. Discussion

4.1. Tourism interactions with whale sharks

The results from the current study show that whale sharktourism at Ningaloo has increased markedly between 2006 and2010, with increases in both the number of tours (70%) and thenumber of days with a recorded interaction (68%). The number oftours increased by a further 12% in 2011 (E. Wilson, DPaW, un-published data). Most of this growth has been at North Ningaloo,where the number of tours increased from 398 to 712 between2006 and 2010. Interactions with whale sharks were recorded onmost days between April and July but in 2010, several tours tookplace in August and September, increasing the number of days thattour operators interacted with whale sharks.

The number of interactions made by tour operators during thewhale shark season has increased by a much greater extent (4.7times) than the number of tours and days with interactions, withthe total number of interactions increasing from 694 in 2006 to3254 in 2010. With tours continuing to operate in August andSeptember, the number of interactions has the potential to increasefurther. Although the possible impact of an increasing number ofinteractions with whale sharks at Ningaloo is unknown, Norman(2002) observed short term responses of whale sharks to in-teractions with tour operators, such as sharks diving or banking. Hesuggested that long-term impacts, such as changes to feedingpatterns, or stress and injury as a result of boat strikes, are possiblewith high interaction rates. Previous studies that have investigatedthe impact of nature-based tourism on dolphin populations havefound that increases in the number of interactions between vesselsand dolphins have had negative impacts on the resident population(Bejder et al., 2006).

The average number of tour boats operating on days when in-teractions with whale sharks were recorded increased by nearly30% between 2006 (4.8 tour boats per day) and 2010 (6.2 tour boatsper day). In the peak months of April andMay, up to 14 boats can beoperating on a single day at Ningaloo. In Belize, the number ofwhale shark tour operators increased rapidly from one in 1996 to26 in 2005, and even with adjustments to management practices,the number of whale sharks aggregating there decreased, as well asthe likelihood of seeing a whale shark (Carne, 2007). Whale sharktourism started in 2002 off the Yucatan Peninsula in the Caribbeanand grew very rapidly over the next five years to a total of 140operators. This led to concerns about the possible impacts on thesharks as compliance with the codes of conduct was still a problem(Rowat and Brooks, 2012). The whale shark tourism industry thatoperates at Ningaloo Reef is aworld leader in terms of managementand the adoption of a code of best practise for tour operators. Thenumber of tour operators has been controlled through the use oflicensing since 1993 (Catlin et al., 2010; Rowat and Brooks, 2012)and the number of vessels operating at Ningaloo has never excee-ded 15 (Catlin et al., 2010), which is much lower than the number ofvessels operating in Belize and the Yucatan Peninsula. These ex-amples demonstrate the importance of regulating the number ofboats that operate in the industry and strictly enforcing the codes ofconduct, in order to maintain the sustainability of whale sharktourism.

The number of tourists taking part in whale shark tours atNingaloo has increased greatly from 1000 in 1993 to over 17,000 in2011 (DPaW, 2013). Similar large increases in whale shark tourismhave been reported at other locations (for review see Rowat and


Fig. 5. Kernel density plots of the number of whale shark interactions km�2 at North Ningaloo for all five years and each year between 2006 and 2010. Data from the Department ofParks and Wildlife, W.A.


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Brooks, 2012): e.g., the number of tourists swimming with whalesharks in Donsol in the Philippines increased from 850 in 1998(Pine et al., 2007) to 7100 in 2005 (Quiros, 2007) and over 16,000tourists swam with whale sharks off the Yucatan Peninsula in theCaribbean in 2007 (Remolina Su�arez et al., 2007). The behaviours of


whale sharks at both of these locations are thought to have beenimpacted by these large numbers of tourists, mainly as a result oftour operators not following the codes of conduct (Rowat andBrooks, 2012). Quiros (2007) observed that when whale sharkswere touched or their swimming path was obstructed by divers,


Fig. 6. Kernel density plots of the number of whale shark interactions km�2 at South Ningaloo for all five years and each year between 2006 and 2010, BP ¼ Bruboodjoo Point. Datafrom the Department of Parks and Wildlife, W.A.


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sharks modified their behaviour by diving, banking, changing di-rection and even shuddering.

Following the growth in tourism in Belize, management changeswere introduced and tourism increased to >2000 visitors in 2006(see Rowat and Brooks, 2012). Whale shark tourism has been well


regulated at Ningaloo since its inception in 1993 and the numbersof whale shark interactions in 2010 were the highest on record. Thenumber of whale sharks present has been debated. Bradshaw et al.(2008) reported a decline in mean length and whale shark numbersat Ningaloo, while Holmberg et al. (2009), concluded that the


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reduction in length was due to the recruitment of new, smallerindividuals into the aggregation and that the whale shark numbersmay have been increasing.

4.2. Spatial patterns of whale shark interactions

The concentration of tour vessel interactions with whale sharksadjacent to south passage at North Ningaloo is consistent withobservations from spotter planeswhich show that large numbers ofwhale sharks are sighted off reef passages (Wilson et al., 2002).Wilson et al. (2002) used hydro-acoustic surveys to investigate thedistribution of zooplankton during the whale shark season atNingaloo Reef and often observed whale sharks associated withfrontal zones out from south passage and to the south of this pas-sage. At Ningaloo Reef, oceanographic fronts form adjacent topassages as dense lagoon water meets fresher shelf water, creatingintense mixing which is often associated with dense plankton as-semblages (Wilson et al., 2002). Wilson et al. (2002) observed thehighest productivity, determined from acoustic mean volumebackscatter data collected using an echosounder, out from northpassage and south passage, which suggests that dense planktonassemblages are found in these areas. Whale sharks target highconcentrations of plankton when feeding at Ningaloo (Jarman andWilson, 2004) and as a consequence, these areas are likely to attractlarge numbers of whale sharks, and therefore, interactions withtour operators. Whale sharks have also been observed feeding inwaters adjacent to passages at the Great Barrier Reef (Wolanski andHamner, 1988). Studies on the planktivorous basking shark havemade similar observations, finding that frontal features, like thoseobserved adjacent to passages at Ningaloo, are important feedinghabitats for these sharks (Sims et al., 2003).

Whale shark interactions at South Ningaloo were also concen-trated adjacent to passages, probably for similar reasons to thoseoutlined for North Ningaloo. The two passages located just south ofPoint Cloates are zones of mixing of different water masses as aresult of outflow from these passages and also due to the NingalooCurrent, which begins to turn in a westerly direction as it ap-proaches Point Cloates (Woo et al., 2006). Hanson et al. (2005)recorded high primary productivities in the Ningaloo Current wa-ters just south of Point Cloates. Therefore, it is likely that denseplankton assemblages would arise here as a result, particularly inyears when the Ningaloo Current is flowing at a reasonablestrength (El Nin~o years), which would help to explain the highdensities of interactions with whale sharks in these areas. In thestrong La Ni~na year of 2010, very few interactions were observedadjacent to these passages just south of Point Cloates and wereinstead concentrated much further south, lending some support tothis theory.

Distance to the reef crest and the passages in the reef were thebest predictors of whale shark interactions. This finding is consis-tent with the close association of whale sharks with the reef atNingaloo, which has been reported in several other studies (Taylor,1996; Gunn et al., 1999; Gleiss et al., 2011). In the north, tour op-erators use these passages to gain access to the outer reef and directthe spotter planes to begin their search in these areas. Therefore, ifwhale sharks are sighted in these areas, tour operators will interactwith these sharks rather than those located further away to reduceoperating costs. However, tour operators will travel longer dis-tances if whale sharks are not sighted near passages, as customersare offered a repeat trip if no interaction occurs.

Our results based on the reported tour vessel interactions withwhale sharks provide some indications of the distribution of whalesharks at Ningaloo but cannot be regarded as providing an unbiasedrepresentation of their pattern of distribution and relative abun-dance. In attempting to minimise costs, tour operators concentrate


the searching time of spotter planes on areas known for whalesharks that are close to starting points of the tours to allowcompletion of the tour within one day. The patterns of reportedinteractions are likely to under-represent the number of whalesharks found further from the reef crest and the tour starting pointsof Tantabiddi in the north and Coral Bay in the south. In our study,no interactions were recorded in the area between North and SouthNingaloo, about 50 km from Tantabiddi and Coral Bay, and furtherthan it is possible for tour operators to travel and interact withwhale sharks in a single day. Whale sharks have been sightedduring independent whale shark aerial surveys in this area distantfrom the tour starting points (Taylor, 1996), although in lowernumbers than further north (Taylor, 1996). Whale sharks tagged atNingaloo have also been recorded moving through this region(Sleeman et al., 2010b).

4.3. Interannual variation in interactions

The distribution of whale shark interactions at north and southNingaloo (Figs. 6 and 7) varied between years, particularly in thestrong La Ni~na year of 2010. Rohner et al. (2013) also found thatwhale shark numbers varied between years and reported a declinein sightings at Mozambique over time. They attributed this declineto a variety of potential factors such as bycatch in a purse-seinefishery, net entanglement, anthropogenic disturbance, and varia-tion in large-scale oceanographic processes that may influencewhale shark food.

At North Ningaloo, the main concentration of whale shark in-teractions was adjacent to south passage between 2006 and 2009.At South Ningaloo, interactions werewell spread out between 2006and 2009, with some of the larger concentrations occurring adja-cent to the passages just south of Point Cloates. The distribution ofinteractions at North and South Ningaloo in the strong La Ni~na yearof 2010 (Fig. 2, Pearce and Feng, 2012) differedmarkedly from thoseof the previous four years, possibly due to changes in the distri-bution of their zooplankton prey in response to the alteredoceanographic conditions (see also Richardson, 2008; Rohner et al.,2013).

In 2010, interactions were generally concentrated further northat North Ningaloo and further south at South Ningaloo. The con-centration of interactions further north at North Ningaloo in 2010 isnot what would be predicted based on observations made by pre-vious studies. The southerly flowing Leeuwin Current is strongerunder La Ni~na conditions, and as a result, it was predicted that preyare likely to be transported further south in strong La Ni~na years(Wilson et al., 2001; see also; Woo et al., 2006). The interactions atSouth Ningaloo, which had been wide spread in 2008 and 2009,were concentrated in the southern parts of this region in 2010. Thissuggests that the stronger southerly flowing Leeuwin Current mayhave been more influential at South Ningaloo than at North Nin-galoo in 2010. Wilson et al. (2001) also suggest that the northerlyflowing Ningaloo Current could be weaker under La Ni~na condi-tions, which could explainwhy interactions at South Ningaloowereconcentrated further south.

Since 2010, whale sharks have been observed in August and evenin September (B. Norman, Murdoch University, personal communi-cation). The minimum average sea surface temperatures at NorthNingaloo in 2010 were higher than in the previous four years, anindication that suitable conditions may have lasted longer in 2010,allowing thewhale sharks to stay at Ningaloo until later in the year. Asimilar pattern was observed in 2011, when the minimum averageSST were again higher than usual (Fig. 3). Whale sharks at Ningaloohave been found to favour the warmer waters and have beenobserved in waters between 24 and 32 �C (Sleeman et al., 2007;Sequeira et al., 2012). In 2010, 2011, the average monthly sea


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surface temperatures at North Ningaloo remained close to or above24 �C throughout the year. If the La Ni~na weather pattern continuesand sea surface temperatures remain higher for longer, whale sharksare likely to remain at Ningaloo until later in the year.

5. Conclusions

The whale shark tourism industry at Ningaloo increased mark-edly between 2006 and 2010. The tour vessel interactions withwhale sharks at North and South Ningaloo were concentratedwithin 3 km of the reef crest in the North and 6 km in the South andwere also close to reef passages in both regions. High densities ofplankton and whale shark interactions have been observed aroundpassages, indicating that these areas are potentially importantfeeding sites for whale sharks at Ningaloo, and therefore, importantareas for the conservation of whale sharks. The distribution of in-teractions with whale sharks varied among years at North andSouth Ningaloo, particularly in the strong La Ni~na year of 2010. Thehigher sea surface temperatures that have been recorded in the LaNi~na years appear to allowwhale sharks to stay longer than usual atNingaloo, with whale sharks being sighted in August andSeptember. Further research is required to investigate the responseof whale sharks to consecutive interactions from multiple touroperators and the number of interactions that individual whalesharks are experiencing per year in order to determine how manyinteractions are believed to be sustainable. This study demonstratesthe value of the data collected by the Department of Parks andWildlife and the tourism operators at Ningaloo Reef for the con-servation of whale sharks.

Acknowledgements

Special thanks to the staff at the Exmouth District office of theDepartment of Parks and Wildlife for arranging access to the whaleshark interaction data and their guidance on its use. We would liketo thank Hugh Finn for his helpful feedback during the productionof this paper and Claire Smallwood for providing the digitised reefcrest used in our analyses. We thank the anonymous reviewers andthe handling editor for their constructive comments on themanuscript. This research formed part of the Honours Thesis byDouglas Anderson at Murdoch University and was funded by theThyne Reid Foundation and Murdoch University.

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