Issues and Options for Whale Shark Conservation in Gulf of Mexico

Transcription

Mote Marine Laboratory
Issues and Options for Whale Shark Conservation
in Gulf of Mexico and Western Caribbean Waters
of the U.S., Mexico and Cuba
Robert E. Hueter and John P. Tyminski
December 2012
Issues and Options for Whale Shark Conservation in the Gulf & Caribbean
Page 0
Issues and Options for Whale Shark Conservation
in Gulf of Mexico and Western Caribbean Waters
of the U.S., Mexico and Cuba
A Background Paper Prepared for Environmental Defense Fund
Robert E. Hueter and John P. Tyminski
The Center for Shark Research
Mote Marine Laboratory
Sarasota, Florida USA
December 2012
MOTE MARINE LABORATORY TECHNICAL REPORT NO. 1633
Page 1
Executive Summary
The whale shark is the world’s largest fish and a charismatic species for marine conservation. This filterfeeding shark poses no threat to humans and has become a favorite species for people to swim with in
ecotourism operations around the world. Its present status in the world’s oceans is poorly understood
and it is considered a vulnerable species with a potentially decreasing population trend. This paper
addresses issues and options facing the conservation of whale sharks in the Gulf of Mexico and western
Caribbean region. We summarize relevant aspects of whale shark biology and present information on
human utilization of this species and the risks, threats and vulnerabilities faced by whale sharks in the
region. We conclude with a list of recommendations and priorities to advance the conservation of
whale sharks in the Gulf and Caribbean, focusing on measures that can be taken in the U.S., Mexico and
Cuba and on an international scale.
Contents
Section 1 – Whale Shark Biology .......................................................................................................... 3
Section 2 – Human Uses of Whale Sharks .......................................................................................... 12
Section 3 – Risks, Threats and Vulnerabilities ..................................................................................... 17
Section 4 – Solutions and Opportunities for Whale Shark Conservation ............................................. 29
Section 5 – Recommendations and Priorities ..................................................................................... 34
References Cited ............................................................................................................................... 37
Acknowledgments
We thank our colleagues Rafael de la Parra, Paco Remolina and Jaime Gonzalez in Mexico for their many
collaborations through the years studying the whale sharks of Quintana Roo. Our gratitude is extended
to the ECOCEAN Whale Shark Photo-identification Library and all the contributors to this database. We
also thank the Georgia Aquarium for its generous support of our work and collaborations on whale
sharks, especially Al Dove and former staff members Bruce Carlson, Ray Davis and Jeff Swanagan. Now
deceased, Jeff taught that we must “touch the heart to teach the mind.” He knew that whale sharks
would touch a lot of hearts and help to advance the worldwide cause for marine conservation. We miss
Jeff’s leadership and wisdom but continue to carry on with his message.
Page 2
Section 1 – Whale Shark Biology
General Introduction to the Species
The whale shark, Rhincodon typus Smith, 1828, is the world’s largest extant fish and with its
unmistakable checkerboard pattern of spots and stripes is one of the most recognizable animals in the
sea (Fig. 1). It is a cosmopolitan species that inhabits tropical and subtropical coastal and oceanic
waters, forming aggregations in more than a dozen locations around the world (Fig. 2). On the Atlantic
side of the Americas, R. typus ranges from the Bay of Fundy to Florida, throughout the Gulf of Mexico
(GoM), in many parts of the Caribbean Sea including Belize, Honduras, Panama, Colombia, Venezuela,
Bahamas, Cuba, and Haiti, and as far south as central Brazil (Compagno 2001). Despite its wide range
and recognizability, our understanding of the life history and behavioral ecology of R. typus is
incomplete, as its enormous size – possibly to a maximum of 20 m (Chen et al. 1997) – and sporadic
distribution make the species a challenge to study. Over the past 15 years, due in part to discoveries of
previously unstudied aggregation sites and improvements in electronic tagging technology, our
understanding of many aspects of whale shark biology has advanced considerably.
Figure 1. Whale shark with snorkeler off the coast of Quintana Roo, Mexico. (Photo by Marj Awai).
Page 3
Figure 2. Whale shark worldwide distribution (red zone) and known aggregation sites (stars).
Feeding
Like the basking shark (Cetorhinus maximus) and megamouth shark (Megachasma pelagios), the whale
shark is a filter-feeder that specializes in various-sized planktonic prey (Compagno 2001). In R. typus,
unlike the other two shark species, the filtering apparatus is composed of 20 filtering pads in the
pharynx that strain food from the water using a process known as cross-flow filtration (Fig. 3; Motta et
al. 2010). Whale sharks can feed in two ways, by “ram-feeding” while swimming through the water and
by
“suction-feeding” while
hovering in the water column.
In studies from the GoM and
Caribbean Sea, common whale
shark prey items include
sergestid
shrimp,
calanoid
copepods, chaetognaths, crab
larvae, amphipods and fish eggs
(Heyman et al. 2001, Hoffmayer
et al. 2007, Motta et al. 2010, de
la Parra et al. 2011). In two
different whale shark feeding
aggregations, one in the
northern GoM and one in the
Figure 3. Open mouth of feeding whale shark showing filter pads in
south,
whale sharks have been
pharynx over the gills (dark structures deep inside mouth).
Page 4
observed feeding on dense patches of eggs from the little tunny, Euthynnus alletteratus (Hoffmayer et
al. 2007, de la Parra et al. 2011), suggesting that the spawning events of this fish might influence the
seasonal distribution patterns of whale sharks in the GoM. In other parts of the world, there is evidence
that whale sharks will ingest small fish. For example, in Indonesia whale sharks have learned to
congregate around fishing nets and suck small fish out of holes in the nets
(http://www.youtube.com/watch?v=71FLO_6JJVo). In general, the movements of whale sharks from
region to region appear to be timed with localized blooms in productivity and/or events that
concentrate their prey items, which allows for energy-efficient exploitation of food resources (Wilson et
al. 2001).
Life History
Many aspects of R. typus life history are poorly understood, particularly reproduction. The confirmation
that whale sharks are an aplacental, viviparous species did not come to light until 1995, with the capture
of a 10.6 m total length (TL) female off the coast of Taiwan. This female had uteri containing more than
300 embryos at varying stages of development and more than 50 empty egg cases (Joung et al. 1996). A
subsequent paternity analysis of a subsample of these embryos (n=29) revealed that they were full
siblings sired by the same male, suggesting that one male sired the entire litter (Schmidt et al. 2010),
which is not always the case with shark species. Given the range of developmental stages of the
embryos in this litter, Schmidt et al. (2010) suggested that female whale sharks store sperm, which is a
trait of some other shark species, facilitating a protracted period of fertilization and presumably birth of
the young. The duration of the whale shark’s reproductive cycle is not known but may be similar to that
of its relative the nurse shark (Ginglymostoma cirratum), which has a biennial cycle, with one litter
produced every other year (Fowler 2000, Castro 2011).
Growth rates and sizes at maturity for whale sharks are still being investigated. From captive studies, it
appears that newborn whale sharks grow very rapidly. One aquarium specimen grew from 60 cm TL to
139 cm TL in just 120 days (Chang et al. 1997). For wild populations, studies have reported widely
ranging growth rates for R. typus that are likely confounded by the measurement method utilized and
age of the specimens studied (Rowat and Brooks 2012). Using a maximum size of 20 m TL as input into a
calculation of life history parameters, Fowler (2000) estimated the theoretical age at first maturity for a
whale shark to be 21.4 years at 7.7 m TL. Field observations at Ningaloo Reef indicate that 95% of the
male whale sharks were mature at 9.1 m while 50% were mature at 8.1 m as indicated by clasper
condition (Norman and Stevens 2007). In an examination of stranded dead specimens off South Africa,
Beckley et al. (1997) reported that females up to 8.7 m TL were all sexually immature. Using vertebral
growth rings and back-calculations from von Bertalanffy Growth Equations, Hsu (2009) estimated ages
at maturity of 17.2 years for males and 19.2-22.6 years for females, a maximum longevity of more than
79 years, and an average annual growth rate over the whale shark’s lifespan of only 19.8 cm/year.
These parameters would be characteristic of a very long-lived, slow-growing species.
Whale shark mating has not been described in the scientific literature and the precise areas and times
where these events take place can only be speculated on. Although no direct evidence of mating has
Page 5
been observed off the northeast Yucatan Peninsula, mature males with roughed-up, reddish claspers,
suggesting recent copulation, have been observed regularly within the summer aggregations, as well as
occasional mature-sized females that appear pregnant (de la Parra et al. 2008). However, fine-scale
depth data from whale sharks tagged in this area have not to date revealed activity consistent with what
would be expected for mating behavior (Tyminski et al. unpublished data).
Population Structure
Two studies on the worldwide population genetics of whale sharks (Castro et al. 2007, Schmidt et al.
2009) have tentatively concluded the species comprises two populations, one inhabiting Atlantic Ocean
waters and the other inhabiting Pacific Ocean and Indian Ocean waters. More detailed population
structure within these broad areas is not clear, due perhaps to limited sample sizes but more likely to
significant gene flow across ocean basins. Both studies utilized samples from aggregation sites and it is
possible that segregation at these sites is masking some genetic relationships. More global samples
from other areas are needed to further substantiate these findings.
Both the Castro et al. (2007) and Schmidt et al. (2009) studies also attempted to estimate worldwide
population numbers for the species, based on genetic data. These estimates ranged between
approximately 27,000 and 476,000 whale sharks worldwide, numbers that should be taken only as a
starting point for determining how many whale sharks exist in the sea. Meaningful calculations of the
global population size are nearly impossible given the species’ cosmopolitan distribution and highly
migratory nature (Graham 2007). Most estimates of population size for this species are based on
localized sightings within individual aggregation areas (Meekan et al. 2006, Ramírez-Macías et al. 2012)
but are almost invariably biased by an uneven representation of the sexes. A distinct male bias has been
documented in a number of well-studied whale shark aggregations in the Seychelles (82% males, Rowat
et al. 2011), Ningaloo Reef off western Australia (83% males, Meekan et al. 2006), and Djibouti (85%
males, Rowat et al. 2011). Observations of whale shark aggregations from the western Atlantic also
have noted male-skewed populations. In the Caribbean waters off Belize, about 86% of the observed
sharks are immature males (Graham and Roberts 2007) while the aggregations off the northeast corner
of the Yucatan Peninsula comprise 71% males (de la Parra 2008). This bias makes estimates of
population size more difficult as it suggests we are observing only a subset of the population.
Pregnant females and very small whale sharks are rarely encountered within nearshore aggregation
areas (Colman 1997), suggesting that these population components usually remain in deeper offshore
waters. In the Gulf of California (GoC), large and apparently pregnant females (>9 m TL) have been
documented in offshore waters south of Banco Gorda, whereas only juveniles are found in the northern
and central parts of the GoC (Ramírez-Macías et al. 2007). The utilization of offshore habitat by large
females may reflect different dietary requirements, as stable isotope analyses have provided evidence
of a shift to larger prey with increasing size of whale sharks (Borrell et al. 2011). In a recent study using
both aerial and boat-based surveys in the southwest GoC, Ketchum et al. (2012) concluded that whale
shark segregation by size is related to behavioral strategies as opposed to oceanographic factors. These
authors found that the presence of juvenile whale sharks (<9 m TL) in shallow coastal waters of the GoC
Page 6
was correlated with a dietary preference, as these areas contain dense zooplankton patches which could
facilitate faster growth rates in these developing sharks. The adult whale sharks (>9 m TL), which remain
in deeper water in the GoC, prefer offshore habitat and feed opportunistically on the prey available
there. Records of free-swimming neonate whale sharks have come from tropical open-ocean habitats
(Wolfson 1983, Kukuyev 1996), which supports the possibility of deep offshore nursery areas for this
species. If this is the case, newborn whale sharks (55-64 cm TL, Castro 2011) might experience a high
predation rate in such an open, unprotected habitat, and hence the mother’s large litter size and
protracted period of parturition could be a means of compensating for this vulnerability.
Photo-identification of whale sharks has contributed to our understanding of the species’ population
structure. Photo-ID is a non-invasive means of identifying individual sharks using each animal’s unique
pattern of spots, stripes and scars on the skin. Its application has become increasingly popular among
whale shark researchers and non-researchers who come into contact with R. typus. Whale shark photos
capturing the skin pattern behind the gills can be submitted to the ECOCEAN Whale Shark PhotoIdentification Library (www.ecocean.org). This online, public database utilizes both the Interactive
Individual Identification System (I3S; Van Tienhoven et al. 2007) and Modified Groth (Arzoumanian et al.
2005) pattern recognition algorithms for computer-assisted identification of whale shark photographs.
As of December 2012, the ECOCEAN database had identified 4,065 individual whale sharks from various
locations around the world.
Distribution in the GoM and Caribbean
Some of the earliest literature on whale sharks came primarily in the form of short reports from E.W.
Gudger, an American Museum of Natural History ichthyologist who was practically obsessed with the
species. Over a 40-year period, Gudger published 47 articles on R. typus covering a number of topics
including natural history, feeding habits, collisions with vessels, and geographic range. In the GoM and
Caribbean Sea alone, his publications identified the presence of whale sharks off the coasts of Texas,
Florida, Mexico’s Yucatan Peninsula, Belize, Cuba, Haiti, Bahamas, and Trinidad (Gudger 1931, Gudger
1936, Gudger 1939a, Gudger 1939b). Relying on second-hand reports from ships and other sources,
Gudger himself never actually observed a live whale shark.
Although whale sharks are often encountered singly and are not considered to be particularly social
animals, they form seasonal aggregations in a number of coastal areas in the GoM and Caribbean Sea
(Fig. 2), primarily to take advantage of localized food sources. In Cuba, whale sharks are observed off
the nation’s south coast in the Jardines de la Reina Archipelago (Graham 2007). The sharks reportedly
do not appear there in large numbers. After conducting interviews with commercial fishermen, fishing
guides, and scuba dive operators utilizing the Jardines de la Reina Archipelago, Pina et al. (2008)
reported that an average of about 13 whale sharks are sighted per year representing about 7% of the
respondent’s sea days. The whale shark sightings are reportedly most common between the months of
October and December. About 77% of the sightings comprise single whale sharks while the remaining
sightings are 2-3 individuals (Pina et al. 2008). The animals range in size from 3-15 m TL with about 8 m
TL being average (Pina et al. 2008). The whale sharks observed in this part of Cuba are often associated
Page 7
with schools of small sardines and small tunas (Pina et al. 2008). R. typus also is reportedly observed by
tuna fishermen off the northwest coast of Cuba, primarily near the continental shelf edge during the
months of October and November (G. González-Sansón pers. comm.).
Off the northeast corner of the Yucatan Peninsula, Mexico, whale sharks gather in great numbers near
Isla Holbox in the coastal waters between Cabo Catoche and Isla Contoy from May through September,
with peak abundance occurring between late July and mid-August (de la Parra et al. 2011) (Fig. 4).
During the spring and summer, cold nutrient-rich upwelled water of the Caribbean Current intrudes over
the Campeche Bank (Merino 1997, Zavala-Hidalgo et al. 2006), which leads to localized summer
plankton blooms (Pérez et al. 1999, Cárdenas-Palomo et al. 2010), providing the sharks with a rich and
dense food source. The Isla Holbox population of sharks has been estimated to range from 521 to 809
individuals (Ramírez-Macías et al. 2012). A second area of whale shark abundance east of Isla Contoy
and northeast of Isla Mujeres, dubbed the “Afuera” (Spanish for “outside”) aggregation, has been
described as the largest whale shark aggregation currently known anywhere in the world (de la Parra et
al. 2011). In 2009, during a single aerial survey of this area, 420 whale sharks were observed within an
AFUERA
Figure 4. Whale shark aggregation sites off northeast corner of Yucatan Peninsula, Mexico. The two
primary aggregation areas are shown as gray-shaded sections north of Cabo Catoche and east of Isla
Contoy (the latter is the site of the “Afuera” aggregation). The two large stippled polygons show the
limits of the Yum Balam federally protected natural area (terrestrial and inshore) and the Whale Shark
Biosphere Reserve (offshore). (Reproduced with permission from de la Parra et al. 2011.)
Page 8
elliptical patch of ocean measuring about 18 km2. These same surveys have revealed a great diversity of
other marine megafauna in the same area, with more than 80 giant mantas (Manta birostris) and
several hundred sea turtles recorded on a single day (de la Parra et al. 2008). Other species of rays as
well as flyingfishes, small tunas, billfishes, sea birds, and marine mammals also aggregate in this area
(Hueter 2012).
Off Honduras, primarily between the months of February and May, whale sharks aggregate off the north
shore of Utila, an area known for high primary and secondary productivity due its proximity to the
continental shelf break and a counter-clockwise gyre (Graham 2007). The whale sharks observed off
Utila are often associated with schools of blackfin tuna (Thunnus atlanticus) and to a lesser extent
skipjack tuna (Katsuwonus pelamis) and little tunny (Fox 2008). Along the Belize Barrier Reef, whale
sharks aggregate each year in April and May to feed primarily on the freshly released spawn of dog and
cubera snappers (Lutjanus jocu and L. cyanopterus) (Heyman et al. 2001). Whale shark presence in
Belize’s Gladden Spit is predictable and appears to be temporally linked to these April/May spawning
events, just after sunset each night for about seven consecutive days beginning with a full moon
(Heyman et al. 2001).
In the northern GoM, aggregations of R. typus have been documented in shelf edge waters during the
summer months (Hoffmayer et al. 2005, Burks et al. 2006). A recent study from this area utilizing a
presence-only dataset found that whale sharks sightings were most strongly correlated with proximity
to the continental shelf edge, distance to adjacent petroleum platforms, and chlorophyll a
concentrations (McKinney et al. 2012). Unpublished reports of more than 100 whale sharks seen south
of Louisiana appeared in 2010, concurrently with the Deepwater Horizon oil blowout occurring about 60
miles to the east (http://www.wlox.com/Global/story.asp?S=12741684). In the northwestern GoM,
Burks et al. (2006) documented aggregations as large as 23 sharks about 33 km west of the Flower
Garden Banks National Marine Sanctuary. This trio of coral reefs in the NW GoM lies about 170 km
south of Sabine Pass, Texas. The Flower Garden Banks have been thought to provide year-round habitat
to whale sharks (Pattengill-Semmens et al. 2000, Causey et al. 2002) though there are no published
peer-reviewed studies supporting that hypothesis.
All evidence to date indicates that whale shark aggregations as a whole, no matter where they occur in
the world, are more related to feeding than to any other behavioral or social function, including
reproduction. Whether or not male and female whale sharks come together in groups to mate in
certain areas is completely unknown. If such mating areas exist they are likely to be in the open sea or
even deep sea where they elude direct observation.
Movement and Migration within the GoM and Caribbean
Photo-identification results from the ECOCEAN database have revealed connectivity between Belize,
Honduras, Mexico’s Yucatan Peninsula, the northern and eastern GoM, and the east coast of Florida.
Results from the deployment of pop-up satellite archival tags (PSATs) on sharks aggregating off the NE
Yucatan Peninsula support these findings and have demonstrated movements of these animals
Page 9
throughout the GoM, through the Straits of Florida, and into the Caribbean Sea (Hueter et al. 2008).
Within the GoM, satellite tracking indicates that whale sharks departing their Quintana Roo summer
feeding grounds utilize the central, western, and northern parts of the GoM. To date we have no
evidence of these Yucatan Peninsula-tagged sharks utilizing the northeastern GoM (i.e. Florida’s west
coast waters) to any great extent, but a number of these animals have shown movements into the
Straits of Florida. In particular, an area north to northwest of Havana, Cuba appears to be an important
“hotspot” (Hueter et al. 2008). One of the Yucatan Peninsula-tagged sharks demonstrated movement
into the eastern Caribbean where it remained near Hispaniola for several weeks between October and
December. PSAT results have also demonstrated the movements of a mature and possibly pregnant
female from off the Yucatan Peninsula, through the northern and eastern Caribbean Sea, and into the
mid-Atlantic Ocean to an area just south of the equator – a journey of more than 7,700 km over five
months from August to January (Hueter et al. 2008). We speculate that this shark may have made this
extended journey to give birth to her pups and/or mate. This same shark has been observed back at the
Quintana Roo study site in more than one subsequent year, demonstrating true philopatric behavior (R.
Hueter et al. unpublished data).
The cues that trigger whale shark movement from one aggregation site to another are not well
understood. In Western Australia, biophysical drivers have been shown to affect whale shark
occurrence and abundance (Sleeman et al. 2010a, Sleeman et al. 2010b, Sequeira et al. 2011). For
example, correlations between whale shark movements and the retreat of warm sea surface
temperature (SST) isotherms toward the equator have been described for whale sharks at Ningaloo Reef
(Wilson et al. 2006). In the Indian Ocean, SST was similarly found to be the best predictor of whale shark
habitat while surface chlorophyll a concentrations were found to be less reliable (Sequeira et al. 2011).
Surface geostrophic currents do not appear to be utilized by whale sharks as an aid to migration in
animals tracked from Ningaloo Reef (Sleeman et al. 2010b). The Southern Oscillation Index, effectively a
measure of El Niño and La Niña climatic processes, along with wind shear were found to have the
greatest influence on whale shark abundance by affecting along-shelf currents that re-suspend
nutrients, resulting in pulses of productivity (Wilson et al. 2001, Sleeman et al. 2010a).
Vertical Movements and Deep Diving
Although whale sharks are normally observed at or near the surface, satellite tracking in recent years
using PSAT tags has revealed that these sharks exhibit variable patterns of vertical movement and spend
significant time in the mesopelagic and bathypelagic zones of the deep sea. Off the coast of
Mozambique, Brunnschweiler et al. (2009) found whale shark vertical movements down to 1,286 m and
suggested that deep dives most likely represented a search behavior for feeding opportunities. Graham
et al. (2006) reported that tagged whale sharks off Belize had diel and lunar patterns to their vertical
movements and these patterns were influenced by the timing of snapper (Lutjanus spp.) spawning. We
have found that whale sharks in the GoM and Caribbean are capable of dives to at least 1,928 m where
they can experience temperatures as low as 4.2°C (R. Hueter et al. unpublished data). High resolution
data from recovered satellite tags have shown that whale sharks in the Afuera aggregation also have a
distinct diel pattern of vertical movement, which can be characterized by surface feeding during the day
Page 10
followed by broader use of vertical habitat beginning in the later afternoon and continuing through the
night. These same tagging efforts off the Yucatan Peninsula have demonstrated a crepuscular pattern of
surface feeding, which is initiated each day precisely at sunrise, as well as deep dives that regularly occur
around sunrise and sunset (Tyminski et al. 2008). When in coastal waters, whale sharks can remain
continuously near the surface, feeding for many hours (an average of 7.5 hrs/d, Motta et al. 2010), after
which they begin more vertical movements and spend more time at depth. Through the use of multisensor ‘Daily-Diary’ data-loggers off Ningaloo Reef, Gleiss et al. (2010) presented evidence that whale
sharks utilize their negative buoyancy and glide at shallow angles during their descents, perhaps as a
means of reducing the energetic costs of horizontal movement. Although it remains to be scientifically
tested, it is possible that the deep dives (>1,000 m) of whale sharks in offshore waters provide a form of
metabolic rest during their slow, gliding descents, while continuing to move the shark in a horizontal
direction with great energy savings.
Page 11
Section 2 – Human Uses of Whale Sharks
Consumptive Uses: Fisheries
As the largest fish in the sea, whale sharks could conceivably provide a valuable, if not abundant, food
source for human consumption. In the GoM and Caribbean Sea, however, whale sharks are not
esteemed for their flesh, and so a fishery for the species has never been established in the region.
Occasionally Mexican fishermen have harpooned a whale shark in the past for human consumption, but
they found they did not care for the meat and so the practice never took hold (R. de la Parra pers.
comm.). There is no indication that a stable fishery ever existed in Cuba, although specimens have
occasionally been taken by Cuban fishermen in the past (Gudger 1936). The same is true in U.S. GoM
and Atlantic waters.
In other parts of the world, however, whale sharks have been, and in some cases still are, sought for
their meat and fins. Taiwan was particularly well known for its whale shark fishery, which capitalized on
the sharks traveling through coastal waters of the island nation. Prior to 1985, the demand and market
value for whale sharks in Taiwan was quite low (Chen et al. 1997). In the early 1990s, however, the
demand for whale shark meat, known locally as “tofu shark” due to its texture and taste, increased
dramatically and it became the most expensive shark meat available (Chen et al. 1997). Whale shark
landings grew accordingly in Taiwan with an estimated 272 individuals harvested annually, primarily
captured as bycatch in set net fisheries and opportunistically by harpoon (Chen et al. 1997). The
Taiwanese market value for the meat, which accounts for about 45% of the total body weight of a whale
shark, was reported as approximately US $11.80/kg at that time (Chen and Phipps 2002), and Taiwan
became the world’s largest consumer of whale shark meat. Due primarily to pressure from conservation
groups and concerns over sustainability of the fishery, Taiwan ended its whale shark fishery in 2007
(Norman and Catlin 2007).
India has also been the site of a whale shark fishery. Until the early 1980s, whale shark landings in India
comprised incidental catches that were not utilized (Pravin 2000). By the mid-1980s, however, a
directed fishery developed for whale shark meat, fins, liver, skin and cartilage. At the height of this
fishery in 1998, as many as 1,000 whale sharks were harvested in that one year alone (Pravin 2000).
Following concerns over the unregulated and likely unsustainable nature of this fishery, India’s Ministry
of Environment and Forests granted full legal protection to whale sharks in Indian territorial waters in
2001, by adding the species to Schedule I of the nation’s Wildlife Protection Act (Choudhary et al. 2008).
A similar story played out in the Philippines, where a once flourishing fishery for whale sharks and giant
mantas (M. birostris) (Alava et al. 1997) was ended with legal protection enacted in 1998, although, as
with elsewhere, occasional poaching still occurs (http://www.wildlifeextra.com/go/news/whale-sharkfin.html#cr).
Although whale shark meat constitutes its greatest consumable product by weight, the fins are also
quite valuable, primarily as display items and trophies, as their quality for shark fin soup is poor. Given
Page 12
their large size and relative rarity, single whale shark fins have been reportedly worth up to US $57,000
(Clark 2004) and they still are occasionally seen on display in markets and stores in Asia.
In summary, although individual whale sharks are still occasionally taken for food in some parts of the
world, no significant fishery directed at this species currently exists due to concerns over
unsustainability, pressure from conservation groups, and the existence of valuable non-consumptive
alternatives to fishing.
Non-Consumptive Uses: Ecotourism
Wildlife tourism, or ecotourism, is a growing industry that can provide a means of transitioning local
economies from unsustainable consumptive uses of environmental resources to more sustainable nonconsumptive uses (Ziegler et al. 2012). Whale shark ecotourism has grown dramatically in the past two
decades as scientific and popular articles, television reports and video documentaries, websites,
Facebook, YouTube, and other sources have brought the subject of swimming with whale sharks to the
masses. (A search for “whale shark diving” on YouTube.com yields about 18,100 results.) Although the
practice may be conducted differently in different regions, it always comes down to the same concept:
swimming in the open sea alongside the largest species of shark that has ever existed. The fact that
whale sharks are docile, surface-feeding on plankton, and slow-moving make them ideal for shark
encounter tourism (Graham 2004). In fact, because whale sharks are planktivores with no known
aggressive behavior, they are arguably the largest animal on earth that people can approach in the
natural environment and not be in any real danger. Unlike most other types of shark dives, whale shark
ecotourism encounters usually do not involve baiting or feeding and hence are closer to a “wild”
experience for tourists (Graham 2004). Being so close to such a large wild animal, not to mention a
shark, provides ecotourists with the thrill of a lifetime. The animal’s polka-dot coloration and its benign,
“gentle giant” nature add an esthetic quality to the experience that touches many people. This charisma
provides a powerful tool for driving public education and conservation efforts for the species worldwide.
Ecotourism operations for whale sharks have sprung up in a number of places around the world where
whale sharks aggregate to feed (Fig. 2). The Ningaloo Marine Park on the mid-northern coast of
Western Australia is reported to be home of the longest-running whale shark ecotourism industry.
Originating in 1989, the Ningaloo case exemplifies a well-managed and sustainable approach to use of
the resource (Catlin and Jones 2010). In other areas of the world, individual boats and tour guides have
been taking customers to see whale sharks for decades; for example, dive boat operators in Mexico’s
Gulf of California (Sea of Cortez) have been incorporating whale sharks into their dive tours since at least
1980 (E. Clark, pers. comm.).
On the Atlantic side of North America, whale shark ecotourism industries have become well-established
in three major locations: Quintana Roo, Mexico; Gladden Spit, Belize; and Utila, Honduras (Gallagher
and Hammerschlag 2011). Two main sites for whale shark ecotourism on Mexico’s northeastern
Yucatan Peninsula, Isla Holbox and Isla Mujeres in the state of Quintana Roo, appear to represent the
largest and fastest developing whale shark watching industries in the world (Dearden et al. 2008 as cited
Page 13
by Ziegler et al. 2012). Comparing whale shark ecotourism industries in Ningaloo, Belize, and Isla
Holbox/Isla Mujeres, Mexico (Table 1), it is evident that the Mexican site has significantly more permit
holders/operators (208 permits in 2009) than the others. The Mexican site also contains a greater
estimated number of sharks. Overall, there are more similarities than differences when comparing
these three areas of whale shark ecotourism (Table 1).
Whale shark ecotourism is worth millions of dollars in revenue to local economies. In Australia, the
industry was valued at between AU $3.2 million and AU $6.2 million in 2007 (Norman and Catlin 2007).
Given the number of whale sharks at this site and the longevity of each animal’s contribution to
ecotourism, a value of AU $282,000 has been estimated for each living whale shark at Ningaloo (Norman
and Catlin 2007). In Belize in 2002, whale shark encounter tourism contributed US $1.35 million to the
Gladden Spit and Silk Cayes Marine Reserve communities during its six-week season (Graham 2003).
Using the 2002 numbers for Belize, Graham (2004) estimated that each whale shark is worth at least US
$34,906 annually in local ecotourism revenues and an estimated US $3.7 million annually to the national
economy of Belize. Such revenues are particularly significant for developing countries and provide a
strong incentive to conserve the living animals for non-consumptive ecotourism uses (Graham 2004). It
is possible that current revenues from whale shark ecotourism at the Mexico site have eclipsed the
other two, but current figures are not yet available.
To help manage their whale shark ecotourism industries, Ningaloo, Belize and Mexico have adopted
codes of conduct for participating boats, guides and tourists (Table 1). The codes are fairly similar in the
three areas, prohibiting touching the sharks and limiting the number of people and boats near an animal
at any one time, but each has adopted different strategies and rules tailored for their own situation. For
example, Ningaloo uses a 250 m radius around each whale shark in which only one vessel at a time can
be within that exclusive contact zone. A second nearby vessel must remain outside of the 250 m zone
and a third vessel in the area must maintain a distance of at least 400 m between it and the shark as
long as the two other vessels are present (Department of Environment and Conservation 2012). To
reduce potential impact of boats and divers on the sharks, Belize authorities have divided the day into
three time slots for engaging with whale sharks, with no more than six vessels (max 14 divers/vessel)
utilizing a given time slot (Carne 2008). In Mexico, a Whale Shark Biosphere Reserve was created in
2009 that encompasses most of the aggregation areas as an aid to conservation and management of the
animals and their habitat (de la Parra et al. 2011).
Page 14
Table 1. A comparison of whale shark ecotourism operations in Ningaloo (Australia), Gladden Spit (Belize), and Isla Holbox/Isla Mujeres (Mexico).
Characteristic
Ningaloo
Gladden Spit
1
Isla Holbox/Isla Mujeres
1989, licensing in 1993
1997
20023
April - June1
March - June2
May - Sept4
151
26 (2004)5
140 (2008)4
15 (2007)5
208 (2009)6
AU $3.2 - 6.2 M7
US $3.7 M (2002)8
US $1 M2
8,000 - 10,000 annually1
2,110 (2006)5; 1,963 (2007)5
17,600 (2008)4
Snorkel (scuba to lesser extent)1
Scuba (snorkel to lesser extent)5
Snorkel only4
Estimated Carrying Capacity
?
?
~160 boats9
Estimated Value of Each WS
AU $282,000 (over 24 yrs)7
US $34,906/yr (2002)8
Inception
Months of Primary Operation
No. of Permits/Operators
Value ($) of Industry Nationally
No. of Tourists/Participants
Scuba or Snorkel?
2
US $2.1 M over lifetime
10
Estimated No. of Sharks in Area
Min. of 1068
320 – 440
Agency Responsible for WS
The Western Australian Dept.
521 – 8096
Co-managed by Friends of Nature
1
Management
8
11
of Environment and Conservation
and the government of Belize
Natural Areas (CONANP)4
· No touching or riding sharks1
· No touching or harassing sharks
· No touching, chasing or harassing
5
· No approaching head/body closer
Key Points in Code of
(US $5,000 fine)
sharks4
· Min. distance from shark is 15 ft
· Min. distance of swimmer to shark
1
5
is 2 m (lowered due to poor vis.)4
than 3 m, and 4 m from tail region
or 4.6 m
· No flash photography1
· No more than 10 people in water
· Tourist/Guide ratio is 8:15
· Only 2 tourists and 1 guide at a time
Conduct
1
permitted to be in water with WS4
at any time around WS
Unique Regulations
1
National Commission of Protected
· "Contact vessel" can go no
· Boat must remain at least 50 ft or
· Boat must remain at least 10 m
closer than 30 m to WS12
15.2 m from sharks5
from shark4
Employ an exclusive contact zone
Day divided into 3 time slots with
A Whale Shark Biosphere Reserve
of 250 m from shark. Only 1
6 boats (max 14 divers/boat)
was created in 2009 to assist WS
vessel at a time can be within zone
2
3
12
5
4
allowed per time slot
5
6
conservation and management13
7
References: Catlin and Jones (2010), Ziegler et al. (2008), Ziegler et al. (2012), de la Parra (2008), Carne (2008), Ramírez-Macías et al. (2012), Norman and Catlin (2007),
9
10
11
12
13
Graham (2004), J.F.Remolina pers. comm., Meekan et al. (2006), Quiros (2005), Department of Environment and Conservation (2012), de la Parra et al. (2011)
8
Page 15
Non-Consumptive Uses: Aquarium Display
A very limited but highly visible use for individual whale sharks has emerged with their capture for
display in public aquaria. Because these living specimens can potentially be released back into the wild
and are not used for any type of seafood product, we include this under the non-consumptive category
of human use. At the present time a total of thirteen individual whale sharks in six aquaria in three
countries (one shark in Taiwan, eight sharks in Japan in four aquaria, and four sharks in the U.S. in the
Georgia Aquarium in Atlanta) are believed to be on display. (Japan and Taiwan may maintain a few
additional individuals in sea pens for future display.) Other aquaria have displayed whale sharks for
temporary periods, for example the Atlantis Aquarium in Dubai, but the massive size of the animals
requires tanks of such enormous volume and life support system capacity that the practice is limited to
only a handful of facilities around the world. The thirteen sharks currently on display have been viewed
by millions of aquarium visitors, inspiring those people to care about whale sharks and support
conservation of the species. Viewing a whale shark behind a glass window may not be as exhilarating
and inspiring as swimming with them in the sea, but for various reasons not all people have access to
ecotourism sites, and in any case, there is clearly no capacity for those sites to accommodate the
millions of people who get to experience whale sharks first-hand at public aquaria.
Page 16
Section 3 – Risks, Threats and Vulnerabilities
Whale sharks face a number of risks to their survival, some of which are common to most marine fishes
and others that are somewhat special to this species. In this section we discuss the major risks, threats
and vulnerabilities that whale sharks face in today’s oceans, including the GoM and Caribbean Sea.
Directed Fishing/Finning
Although significant directed fisheries for whale sharks have existed in Taiwan (Chen et al. 1997), the
Philippines (Alava et al. 1997) and India (Hanfee 2001), protection afforded to whale sharks in recent
years has brought most large-scale directed fisheries for this shark to an end. However, illegal,
unregulated, and unreported (IUU) fishing of whale sharks on a smaller, mostly artisanal scale remains a
concern. Part of the reason for this is the value of their fins remains high, providing strong monetary
incentive for poaching. In addition, a single whale shark can be a significant source of protein for a small
fishing village in a developing nation. A recent report of illegal exploitation of whale sharks came from
the Maldives where one specimen was impaled with a spear while another had its first dorsal fin nearly
severed (Riley et al. 2009). Recent reports of the finning of whale sharks in the Philippines
(http://seychelles-whale-sharks.blogspot.com/2010/02/whale-shark-finned.html) have appeared online
as have other reports indicating that the hunting of whale sharks continues to be practiced to some
extent in China (http://english.cri.cn/3100/2007/09/17/[email protected]).
In North American waters, however, whale shark landings and/or the practice of finning whale sharks
appears to be very rare. We could find no recent published reports for the GoM/Caribbean. Several
decades ago newspaper reports appeared of two whale sharks harvested off Quintana Roo, Mexico. The
harvesting of at least one of these sharks was reportedly directed by the Secretaria de Pesca as an
experiment, presumably to see if a market could be developed for this resource (R. de la Parra pers.
comm.), but the fish were barely utilized because the meat was so disagreeable to Mexican consumers.
To date, there are no confirmed reports of finned whale sharks seen in the Quintana Roo feeding
aggregation (R. de la Parra pers. comm.). In summary, there appears to be no significant directed fishing
and/or finning threat to whale sharks in the GoM/Caribbean region.
Indirect or Non-Target Fishing Activities
As large slow-swimming fish, whale sharks can act as natural aggregation devices for other species, such
as tunas in tropical seas, and tuna purse seine fisheries take advantage of this. When tunas school
around whale sharks and purse seiners set on the school, the sharks can be vulnerable to encirclement
by the tuna nets. Australia has expressed serious concern over the potential impact of purse seine
fishing on populations of whale sharks. In the western and central Pacific purse seine fishery, the
mortality rate of whale shark interactions was estimated (based on observer data) at 12% for 2007-2009
and 5% in 2010. The observed interaction and mortality rates imply the total whale shark mortalities in
the purse seine fishery was approximately 56 animals in 2009 and 19 animals in 2010 (SPC-OFP, 2011)
Page 17
(Fig. 5). A 2010 proposal to the Western and Central
Pacific Fisheries Commission to ban the setting of nets
around whale sharks was not supported (Rowat and
Brooks 2012). For the GoM/Caribbean, no data have
been found on the magnitude of whale shark
mortalities in purse seine fisheries, but it is unlikely to
be a significant threat in this region.
Entanglement of whale sharks in other types of fishing
nets, lines or other gear types is a potential threat.
Reports are scarce and not well documented in the
Figure 5. Purse seine vessel with a young
published literature. A recent video of divers cutting a whale shark taken as bycatch in the Pacific.
large, encrusted rope encircling a whale shark
(http://www.cbsnews.com/video/watch/?id=50136512n) is attributed to Mexico, but the exact location
is unclear. Any type of fishing gear set on the surface or in the water column of whale sharks – e.g. drift
gill nets, pelagic longlines, fish aggregating devices (FADs) – poses some risk. Off Quintana Roo we have
observed a whale shark that was impaled with a spear from a diver’s speargun, apparently when the
diver was attempting to capture other fish (e.g. cobia, Rachycentron canadum) swimming around the
shark. According to local sources, this was not an isolated incident (R. de la Parra pers. comm.).
Unchecked commercial exploitation of key species such as the little tunny in the GoM could present an
indirect threat to whale sharks, because of the sharks’ preference for feeding on the spawn of these
fishes in various areas. The dietary importance of little tunny eggs to whale sharks is unknown, but
there is no question that whale sharks feed heavily on these eggs at times (Hoffmayer et al. 2007, de la
Parra et al. 2011). At present, the status of little tunny stocks in the GoM is unclear but appears to be
healthy. If this species were to be depleted by overfishing or other factors, the ramifications for the
feeding ecology of whale sharks in the GoM could be profound. Fortunately the little tunny is not
presently a highly sought fish in GoM fisheries. On the other hand, the same relationship exists between
whale sharks and certain reef fishes in the western Caribbean, notably snappers (Lutjanus sp.) on whose
spawn whale sharks feed off Belize (Heyman et al. 2001), and those reef fishes are a highly sought food
source for Caribbean nations. Without consideration of the need for whale shark food in the
management of these reef fishes, the sharks could be vulnerable to the indirect effects of overfishing
these other species.
Unregulated/Excessive Whale Shark Ecotourism
Tourism has not proven to be the ideal substitute for shark fishing in many communities, where sociocultural, educational, language, infrastructural, and economic barriers prevent many fishers from
entering into and profiting from shark ecotourism and thereby valuing live vs. dead sharks (Kyne et al.
2012). In addition, for whale sharks, tourism pressure could have a detrimental impact on the sharks
themselves (Colman 1997). In short, it would be naïve to consider the non-consumptive practice of
ecotourism to be a panacea in replacing consumptive, unsustainable fishing for sharks in all cases.
Page 18
In Isla Holbox and Isla Mujeres near the huge resort city of Cancun, Mexico, the whale shark ecotourism
industry began development around 2002. This area now has one of the largest and fastest growing
whale shark watching industries in the world (Dearden et al. 2008 as cited by Ziegler et al. 2012). From
perhaps an occasional boat taking people to view whale sharks before 2002, to about 240 permitted
ecotourism boats in 2012 (J.F. Remolina pers. comm.) plus unknown numbers of non-permitted boats
that enter the area to view the sharks, development of whale shark ecotourism off Quintana Roo is
unprecedented. The problem with such fast growth is that it could be damaging the resource before
obvious signs come to light, causing potentially catastrophic and perhaps irreparable damage to the very
asset on which the industry depends.
With the feeding aggregations of whale sharks just a short boat ride from Cancun and the other major
resort area of Playa del Carmen not much farther south, there is great potential for an increase in the
demand for whale shark ecotourism in Quintana Roo. In a recent study evaluating the shark tourism
industry in Isla Holbox, clear recommendations were made to limit the number of boats to sustainable
levels (Ziegler et al. 2012). Recent estimates of carrying capacity for this practice indicate that a
maximum of 160 boats should be authorized, rather than the current permitted number of about 240
(J.F. Remolina pers. comm.). In August of 2012, as many as 115 vessels were observed at one time
within the dense “Afuera” feeding aggregation (R. de la Parra pers. comm.) of whale sharks east of Isla
Contoy. These vessels comprised permitted ecotourism operators, non-permitted tour operators
(“pirates”), and private yachts (R. de la Parra pers. comm.). Enforcement of the rules for whale shark
ecotourism, as with other fishery and wildlife issues in Mexico, has ongoing challenges due to the lack of
resources. It is difficult to ignore a growing sense that control of the situation is slipping away from
Comisión Nacional de Áreas Naturales Protegidas (CONANP), the primary government agency charged
with overseeing this industry and its use of marine wildlife resources.
To help combat this, ecotourism managers in Isla Holbox and Isla Mujeres have tried a type of selfregulation whereby the permitted operators, as industry stakeholders, help police the activities by
reporting any observed violations to the code of conduct. During whale shark conferences and
workshops held in Isla Holbox and Isla Mujeres, tour operators have been invited to share their
observations with scientists as well as gain firsthand insight into whale shark research being conducted
in their area and other places around the world. These operators have provided important information
on the latest locations of the whale sharks as an aid to the industry and research efforts, and as a
symbol of cooperation with government and academia. In return, researchers have assisted the
industry in several ways. For example, daily information received from satellite-tagged whale sharks has
been shared with ecotourism operators so they can steer their vessels straight to aggregation areas and
save on fuel and time, making the industry more efficient and profitable. Research results on whale
shark behavior also have been provided as educational information for tour operators to share with
their customers.
Nevertheless, an excessive number of boats and swimmers could directly affect whale shark feeding
behavior and ultimately disrupt their ability to forage. The sharks’ surface-swimming behavior during
Page 19
morning hours off Quintana Roo, as revealed through Mote Marine Laboratory high resolution satellite
tag data, lends itself perfectly to the local ecotourism cycle where morning (half-day) trips have become
the norm. This also means that placing hundreds of boats and swimmers in the water at this time could
be disrupting a critical feeding period for the sharks. An examination of the short-term behavioral
responses of sharks to tourists and boats at Ningaloo Reef (Norman 1999) and Donsol in the Philippines
(Quiros 2007) demonstrated that sharks routinely display avoidance behaviors including banking, eyerolling, fast swimming and diving in response to close approaches by swimmers or boats. In the
Philippines, Quiros (2007) identified specific human behaviors that significantly affected whale shark
behavior. This author highlighted the essential need for whale shark ecotourism managers to monitor
the impacts of tourists and utilize adaptive management strategies to minimize these impacts.
Long-term effects of such interactions are poorly understood but could include disruption of normal
feeding cycles, avoidance of or displacement from critical feeding areas, physiological stress, and injury
or even mortality due to boat strikes. A continuous, decade-long study of whale sharks at Ningaloo Reef
concluded that mean shark length declined by nearly 2 m and relative abundance from ecotourism
sightings fell by about 40% during the study (Bradshaw et al. 2008). These declines were attributed to
overfishing of whale sharks in other parts of their range, rather than long-term abiotic or biotic shifts in
the local environment, but effects of the growing ecotourism trade itself could not be ruled out.
However, the reported declines have been debated and questioned by other investigators (Holmberg et
al. 2009). In addition to direct impacts on the sharks, increased boat traffic and numbers of visitors
could directly and deleteriously affect other associated species at the whale shark viewing site. For
example, an increase in ecotourism at the Gladden Spit Marine Reserve in Belize coincided with
alterations in the spawning behavior of aggregating snappers, which consequently changed the patterns
of visitation by whale sharks (Graham 2003).
In summary, although responsible ecotourism focused on whale sharks provides many benefits for the
species, including an alternative to harvesting and a greater public awareness of whale shark behavior,
ecology and conservation, the practice has its own limits of sustainability. Excessive or unregulated
ecotourism has the potential of inflicting significant damage on whale sharks both as individuals and as
populations. Left unchecked, we could end up “loving them to death.”
Ship and Boat Strikes
Because whale sharks are large and spend considerable periods of time at or close to the surface, they
are highly vulnerable to being struck by boats and ships. Commercial shipping activity introduces a
number of environmental risks into the sea, including noise pollution, ship groundings or sinkings, and
ship strikes on large animals (Halpern et al. 2008). Stevens (2007) stated that whale shark mortality
related to human activity, aside from directed fishing, occurs mainly through boat strikes. In the first
half of the 20th century, Gudger (1940) documented collisions between whale sharks and large vessels in
the Atlantic Ocean, Caribbean Sea, Pacific Ocean, Indian Ocean, and the Red Sea. Among reports
compiled by Gudger were those of a whale shark impaled on the bow of a ship in the south Pacific
(Gudger 1937a) and another shark literally cut in half after collision with an ocean liner in the Caribbean
Page 20
Sea (Gudger 1937b). Gudger (1938) further reported on four whale sharks that collided with large ships
in the Red Sea between 1933 and 1937; two of these sharks were killed while the other two were
described as having wounds that were likely fatal.
In the last 50 years, the world’s commercial shipping
fleet has approximately tripled while the gross tonnage
of commercial ships has increased by a factor of more
than six, according to Lloyd’s Register of Shipping
(Hildebrand 2009) (Fig. 6). In the GoM, the Port of
South Louisiana and Port of Houston are two of the 10
busiest ports in the world by cargo volume. Seven of
the top 10 seaports in the U.S. are located on the GoM
coast (http://www.epa.gov/gmpo/about/facts.html). In
describing the threats to mantas off the Yucatan
Peninsula, Graham et al. (2012) noted some of the
Caribbean’s busiest shipping lanes (citing Halpern et al.
2008) coincide with locations where mantas aggregate.
Figure 6. Number of vessels (dashed line) and
gross tonnage of vessels (solid line) in the
world’s commercial shipping fleet. Data from
Lloyd’s register of shipping for self-propelled,
merchant fleet vessels of 100 gross tons or
more (figure from Hildebrand 2009).
Figure 7. Commercial shipping activity in the
Gulf of Mexico and western Caribbean Sea.
Red lines are large shipping routes, gray
clusters are areas where mantas aggregate
to feed (very similar to whale shark feeding
sites) and black crosses are major tourism
locations. Data from World Meteorological
Organization Voluntary Observing Ship
Scheme (figure from Graham et al. 2012).
These same locations off of Quintana Roo
(Fig. 7) are where whale sharks come to
feed May through September (Fig. 8). No
studies have been published that document whale shark mortalities by ship strikes in the Gulf and
Caribbean, but reports occasionally surface in the popular media online that suggest they do occur (see,
for example, http://www.nova.edu/ocean/forms/sunsentinel-18-foot-whale-shark-found-dead-off-porteverglades.pdf). Speed et al. (2008b) recommended that mortalities by large vessel strikes need to be
accounted for in management of whale sharks. Quantifying these strikes poses significant challenges,
however, as such collisions probably occur offshore and dead whale sharks would normally sink due to
their negative buoyancy. However, it is reasonable to assume the rate of large vessel strikes on whale
shark has increased over the last half century. Not only has the commercial fleet at least tripled since
Gudger’s reports of the 1930s and 40s, but ships today are larger, have more powerful engines and
travel at higher rates of speed.
Page 21
Figure 8. Whale sharks in
the “Afuera” aggregation
off Isla Contoy, Mexico in
the immediate vicinity of a
large ocean-going vessel.
Strikes by small boats on whale sharks (Fig. 9) is a growing
concern, especially with the growth of boat-based ecotourism.
For example, of the whale sharks observed in Bahia de los
Angeles in the Gulf of California, Mexico between 2001–2004,
Figure 9. Whale shark observed off
more than 50% had fresh injuries or scars caused by boat the northeast Yucatan Peninsula
strikes, most of which occurred when boats ran at high speeds with damage from a boat propeller
through whale shark feeding areas (Cárdenas-Torres-Torres et (photo courtesy of R. de la Parra).
al. 2007). Evidence of boat strikes has been found in other
whale shark aggregation areas including Ningaloo Reef (Meekan et al. 2006), the Gulf of Tadjourna,
Djibouti (Rowat et al. 2007) and Belize (Graham and Roberts 2007). Off the northeast Yucatan
Peninsula, whale sharks commonly show scars and wounds from boat propellers and/or boat hulls.
Ramírez-Macías et al. (2012) reported 25% of the whale sharks observed off Isla Holbox between 2005
and 2008 displayed evidence of collisions with boats. More recently, in the summer of 2012, an
ecotourism operator reported about half the whale sharks off Isla Mujeres had either fresh propeller
injuries or scarring from old injuries (A. Murch pers. comm.).
As with other shark species, whale sharks have a remarkable capacity to heal from wounds to the body
surface and fins. We have observed many whale sharks with sliced or even missing fins that have healed
over a period of months and the sharks have continued to swim and feed. Speed et al. (2008b)
concluded that scarring from natural predators and small vessels appears to not affect whale shark
survival, but it is difficult to verify this. We cannot rule out that sublethal effects on whale shark health
might compromise the animals’ immune systems, cause swimming and feeding abnormalities, or even
affect reproduction.
Page 22
Strandings
Whale shark strandings onshore have been reported infrequently in various parts of the world. In May
1977, one of the authors (REH) observed an approximately 9 m TL female whale shark stranded in
shallow water of the GoM in the Florida Keys. The shark rested for short periods on the bottom at a 2-3
m depth, oriented into the current, and occasionally swam for a short distance to a new position where
it settled on the bottom again. This animal had no external marks or scars on it, and it died a day or two
later, cause unknown (R. Hueter unpublished data). Beckley et al. (1997) presented data from 36 whale
sharks that stranded along the South African coast between 1984 and 1995. The sharks were mostly
immature but ranged in size from 3 to 11 m TL and had an even sex ratio. The strandings occurred with
no known pattern but one year (1991) ten sharks were observed in three separate events that occurred
in the same area. This study posed two hypotheses to explain the strandings: 1) sudden changes in
water temperature had reduced the sharks’ metabolic rates; and/or 2) a combination of strong wave
action and a steeply sloping continental shelf had pushed the sharks ashore. In a subsequent case from
Australia, two whale sharks were reported to have stranded, one from the west coast in 2006 and the
other from the east coast in 2007 (Speed et al. 2008a). There was no obvious reason for these
strandings as neither animal showed evidence of wounds, scarring, or entanglement. In this case, the
authors ruled out the two hypotheses proposed by Beckley et al. (1997) for the South African strandings.
In a recent stranding in the Philippines, the popular media reported a 4.6 m TL whale shark was found
floating in the sea by local fishermen, who towed the shark to shore and cut it up for food
(http://voxbikol.com/article/frequent-whale-shark-strandings-san-miguel-bay-alarm-experts).
On a global scale, whale sharks appear to strand only rarely, suggesting that such events are not likely to
represent a major threat to the species. Although most whale shark stranding reports claim that no
wounds or other external trauma were apparent on the animal, it is likely that at least some of these
mortalities resulted from ship/boat strikes, directed fishing or fishing gear entanglement.
Climate Change
The effects of climate change on the biology and conservation of marine organisms is a major global
concern. Few papers have addressed this issue in sharks. Chin et al. (2010) conducted a risk assessment
of climate change effects on sharks and rays of the Great Barrier Reef. These authors identified ten
factors potentially affecting sharks, split into direct factors (temperature, ocean acidification, and
freshwater input) and indirect factors (ocean circulation, temperature, sea level rise, severe weather,
freshwater input, light, and ocean acidification). Their results indicated that the vulnerability of pelagic
sharks and rays to climate change would be manifested primarily through changes in ocean circulation
and temperature. Of these pelagic species, the whale shark (along with the manta ray) would be the
most vulnerable species in this group because they are plankton-feeding specialists and are relatively
rare. Specialization and rarity are recognized as factors increasing the risk of extinction (Davies et al.
2004 as cited by Chin et al. 2010).
Page 23
Whale sharks are highly migratory and are known to travel between ocean basins to exploit seasonal
productivity events. In pelagic systems, productivity events are typically linked to current and nutrientrich upwellings, which are greatly affected by climatic processes such as El Niño and La Niña. Alterations
to these processes through climate change could have significant effects on biological production and
hence prey availability for whale sharks. Zooplankton, a primary food for whale sharks, is essential to
the functioning of marine food webs given its abundance, diversity, and pivotal roles in ocean
ecosystems (Richardson 2008). One of the plausible repercussions of global warming is a change in the
abundance, size composition, diversity, and trophic efficiency of zooplankton (Richardson 2008). We
already have evidence of large-scale changes in the biogeography of calanoid copepods in the eastern
North Atlantic Ocean and European shelf seas in response to both the increasing trend in northern
hemisphere temperature and the North Atlantic Oscillation (Beaugrand et al. 2002). As zooplankton
specialists, whale sharks may be particularly vulnerable to these types of changes as they undergo
migrations to seek pulses of secondary productivity. In the United Kingdom, changes in the distribution
of the filter-feeding basking shark off southwest England into more northerly Scottish waters have led to
speculation that climate change may be responsible for these changes in distribution pattern (e.g. see
http://www.dailymail.co.uk/news/article-352618/Climate-change-forcing-basking-sharks-north.html).
The acidification of the ocean, as a result of rising atmospheric carbon dioxide, could also have an
indirect impact on filter-feeding megafauna. Acidification can lower calcium carbonate saturation states
which can impact shell-forming marine organisms from plankton to benthic molluscs, echinoderms, and
corals (Doney et al. 2009). Another consequence is a change in ocean chemistry that would limit the
bioavailability of iron (Fe), a limiting nutrient in large oceanic regions, and deleteriously affect
phytoplankton populations in some areas (Shi et al. 2010). Subsequent alterations in the patterns of
primary productivity could affect the availability of predictable food sources for whale sharks.
Marine Pollution
Little is known of the effects of pollution on the biology and health of whale sharks. Because whale
sharks are not apex predators but feed primarily on zooplankton, they probably do not contain high
levels of bioaccumulated contaminants such as heavy metals like mercury, which accumulate in many
species of predatory sharks. However, as surface filter feeders they are highly vulnerable to
contaminants floating on or contained in seawater. This would include petroleum compounds and
dispersant chemicals used on oil spills.
With nearly 4,000 oil and gas platforms in the U.S. GoM alone, the threat of spills on the whale sharks of
the region is very real. Although oil industry operations have traditionally been conducted in relatively
shallow water on the continental shelf, the trend in recent years has been to explore in deeper waters
(>500 m) along the continental slope (Hildebrand 2009). Over the past decade, the U.S. GoM had an
average of about 25 offshore oil exploration crews in operation every month (Hildebrand 2009; Fig. 10).
Such areas in the northern Gulf are prime habitat for whale sharks (Hoffmayer et al. 2005, Burks et al
2006, Hoffmayer et al. 2007). Oil and gas rigs also are found in the southern GoM in Mexican waters
from Campeche west to Veracruz, where whale sharks also migrate. There are about 100 oil platforms
Page 24
operating in the Bay of Campeche, Mexico’s main oil-producing region in the Gulf. On June 3, 1979,
Ixtoc I, an exploratory oil well located in the bay, suffered a blowout that caused an explosion, resulting
in one of the largest oil spills in history. As Mexico’s inshore oil reserves are running low, Mexican oil
interests are beginning to conduct deepwater drilling operations for offshore rigs. This is a concern
because Mexico has limited experience in deepwater drilling, and their standards for worker health,
inspections, and industrial safety are already considered some of the weakest in the industry (see e.g.
the following two sites: http://edition.cnn.com/2012/09/25/business/mexico-deep-water-oil/index.html
and http://www.mcclatchydc.com/2012/04/03/144004/mexican-plan-for-gulf-deepwater.html).
Figure 10. Potential threat of oil
spills on whale sharks. (Top) Areas
of offshore oil exploration from
1994 to 2005. Size of star denotes
relative level of activity. Compare
with map of whale shark
distribution and aggregation sites
in Fig. 2.
(Bottom) Average
number of offshore oil exploration
crews working per month for
different regions from 1994 to
2005.
Data from World
Geophysical News (figures from
Hildebrand 2009).
The surface-feeding behavior of whale sharks puts them at risk from both oil and the dispersants used
on spills (Campagna et al. 2011). Whale sharks coming into direct contact with oil could be severely
impaired as a result of having their gills and filter pads clogged, interfering with breathing and feeding.
In addition, their planktonic prey can become contaminated with oil pollutants (Graham et al. 2010).
Over the long term, exposure to oil and associated chemical dispersants could compromise the animals’
endocrine and immune systems. The April 2010 Deepwater Horizon (DWH) oil rig explosion and
subsequent spill of more than 200 million gallons of oil into the northeastern GoM posed a direct threat
to whale sharks, which aggregate in the region of the DWH spill in significant numbers (Hoffmayer et al.
2005, Burks et al 2006, Hoffmayer et al. 2007). The death of some whale sharks was suspected as a
direct result of the DWH spill (http://news.nationalgeographic.com/news/2010/09/100924-whaleIssues and Options for Whale Shark Conservation in the Gulf & Caribbean
Page 25
sharks-gulf-oil-spill-science-environment/) but could not be verified. About 2 million gallons of Corexit®
dispersant were applied to break up the DWH oil and the effects of that chemical on whale sharks are
unknown. But this dispersant is by definition a surfactant, a class of compounds that is one of the few
effective chemical shark repellents, irritating sharks’ gills (Sisneros and Nelson 2001). In the late spring
and early summer months during the DWH spill, Mote scientists received a number of reports of large
pelagic animals in inshore waters within 12 nautical miles of the coast. These species included Atlantic
sailfish (Istiophorus albicans) and blackfin tuna that are normally found in much deeper offshore waters.
The reports also included frequent sightings of whale sharks, including a group of ten sharks that were
located and studied by Mote scientists. Several of these animals were tagged with satellite tags and
some showed movements that could indicate avoidance of the area around the oil spill (Fig. 11). We
speculated these sharks and other pelagic animals may have been displaced by the oil and perhaps
dispersant and had shifted their normal migration routes to the east to find more suitable conditions.
Figure 11. Track of whale shark Gilbert in relation to the Deepwater Horizon oil spill of 2010. The area
in green represents the NOAA/NESDIS satellite-derived analysis for the spread of oil at the surface on
July 20, 2010. Gilbert was tagged on June 18, 2010 (green pin) as part of a group of ten sharks that were
found less than 20 nautical miles from the southwest Florida coast. Gilbert’s tag popped up on August
10, 2010 (red pin). The tag’s premature release was caused by the activation of its tether’s depth
failsafe device, as a result of the shark diving to an extreme depth of 1,928 m on that day.
With respect to marine pollution originating from land masses, Graham (2007) provided some details on
watershed-based pollutants in the vicinity of the western Caribbean’s major whale shark aggregations,
referring to a study by Burke and Sugg (2006). In a watershed analysis for the Mesoamerican Reef
(MAR), Burke and Sugg (2006) reported most of the sediment and nutrients delivered by watersheds
along the MAR originate in Honduras. They estimated more than 80% of sediment loads and more than
half of all nutrients (both nitrogen and phosphorous) originate in Honduras. Guatemala was identified
Page 26
as a source of about one-sixth of all sediments and about one-quarter of all nitrogen and phosphorous
entering coastal waters along the MAR. The modeling suggests that compared to the other countries,
relatively minor percentages of the regional sediment load come from Belize and Mexico. Belize
contributes 10-15% and Mexico about 5% of the nutrients from all modeled watersheds. Burke and
Sugg (2006) noted that Mexico’s contributions may be underestimated because the analysis did not
include underground rivers. How these various pollutants directly or indirectly affect the whale sharks
of the MAR region is subject to speculation and requires further study.
Coastal Development
Coastal development in warm temperate and tropical regions often results in the disturbance or
destruction of wetlands, salt marshes, mangroves, and other habitats essential to countless species of
marine wildlife. Excessive coastal development can negatively impact coastal marine animals through a
number of channels, both direct and indirect. When whale sharks aggregate in continental shelf waters,
they become essentially coastal animals vulnerable to these sorts of impacts.
On the northeast Yucatan Peninsula, there are at least two mega-developments in the works that could
pose a risk to whale sharks in the area. The first is a large development planned for Isla Holbox and
adjacent areas. This project targets the luxury market and will include hotels, a golf course, a marina,
and an airstrip. According to media reports, the company Bepensa is heading up this project. Despite
Isla Holbox being part of a federally protected natural area, plans for this development have proceeded.
There has been a great deal of controversy over the apparent paradox between the co-existence of
natural protected area and mega-development, with insinuations of corruption among the politicians
and bureaucrats involved. See, for example, the following online reports on this issue:
http://articles.latimes.com/2012/oct/18/world/la-fg-mexico-isla-holbox-20121018
http://www.quintanarooaldia.com/noticia/desarrollo-hotelero-en-holbox-sin-control/15334
A second mega-development in the area is planned for Isla Blanca, which lies north of Cancun. This area
is about the same size as Cancun’s Hotel Zone but is in a relatively virgin state at the present time. A 12year project to develop a major tourist area called Soto Lindo is planned, including 9,600 hotel rooms
covering 221 hectares, two marinas, a golf course, casinos and exclusive residences. Mangrove swamps
in the region will be seriously compromised by this development. Mangroves are fundamental to the
equilibrium of marine coastal ecosystems, as they provide food and habitat for many species, function
as a natural flood control system, and provide protection against hurricanes. The area where Soto Lindo
is to be built is home to 15 species of vertebrates that have protected status and nine endemic and
migratory species. Online reports of this proposed development can be found at the following sites:
http://www.reporteindigo.com/lodehoy/negocios-negros-en-isla-blanca
http://www.proceso.com.mx/?p=294986
http://www.mexicohazalgo.org/2012/04/salvemos-isla-blanca-firmando-la-peticion-para-detener-laconstruccion-de-soto-lindo/
http://lasrealidadesdequintanaroo.blogspot.com/2012/06/semarnat-endorse-illegal-political.html
Page 27
The close proximity of these two proposed mega-developments to whale shark feeding grounds and one
of the most important whale shark ecotourism areas in the world poses a significant concern. The
destruction of coastal mangroves and wetlands could result in reduced water quality of the run-off into
the nearshore marine environment, due to increased sedimentation and the lack of filtering that these
habitats provide. With the development of hotels, roads, and golf courses, the water quality of the
surrounding ecosystem could also be compromised by run-off containing pesticides, septic system
discharges, and petroleum products. Collectively, these changes could adversely affect the delicate
balance of the adjacent marine ecosystem, the food supply of whale sharks and other species, and the
health of the sharks themselves.
Effects could be unpredictable, surprising, and devastating, as exemplified in the following case. The
decision to replace native forests with coconut palms (Cocos nucifera) in the Palmyra Atoll of the tropical
central Pacific led to a series of cascading ecological alterations that ultimately led to decreased
zooplankton biomass. As a result, an obligate plankton consumer, the giant manta ray, stopped coming
to the atoll’s adjacent coastal zone (McCauley et al. 2012; Fig. 12). Although the whale sharks of
Quintana Roo are found farther offshore than the mantas of Palmyra Atoll, they are not so far away that
onshore development cannot affect them. The increased number of boats that would come with these
mega-developments in Quintana Roo also could multiply the risk factors of water quality degradation,
boat strikes, and excessive ecotourism pressure on whale sharks in the region.
Figure 12. Illustration of the interactive chain linking forests to manta rays on the Palmyra Atoll, south
central Pacific Ocean (figure from McCauley et al. 2012). The bar graphs demonstrate how replacement
of native forests (N) with palm trees (P) led to a cascading effect resulting in reduced seabird abundance,
less terrestrial nutrients, an impairment of nutrient movement to the marine environment, a reduction in
zooplankton abundance, and ultimately an absence of manta rays utilizing the coastal zone.
Page 28
Section 4 – Solutions and Opportunities for Whale Shark Conservation
Whale sharks have become a keystone species in conservation, not just because they are the world’s
largest fish and vulnerable to exploitation, but because of their public charisma. The benign, polkadotted giants have come to serve as a flagship species for conservation of the greater marine
environment (Norman and Catlin 2007). Whether justified or not, they attract world attention and in
that fact lies the opportunity to save the species for future generations.
IUCN / CITES Listings and Federal Regulations
Globally, the whale shark is listed in the IUCN Red List of Threatened Species as Vulnerable with a
decreasing population trend (IUCN 2012, Norman 2005). This downward trend pertains primarily to
populations in Southeast Asia and there are no data indicating a decline in numbers in the GoM and
Caribbean. On the contrary, sightings data in the region suggest the population is relatively healthy at
the present time. The whale shark is one of only three shark species, along with basking and white
sharks, listed in Appendix II of the Convention on International Trade in Endangered Species of Wild
Fauna and Flora (CITES; Stewart and Wilson 2005). The CITES listing provides the framework to monitor
and regulate international trade in whale shark products (Graham 2007). Since consumptive uses of
whale sharks do not currently exist in the GoM and Caribbean, no known trade in whale shark products
occurs in the region.
Regulatory measures concerning whale sharks vary among the countries bordering the GoM and
northwestern Caribbean, but generally involve some amount of protection or, at the very least, a benign
“live-and-let-live” attitude. In other words, there is relatively little regional controversy about the value
of conserving whale sharks. In the U.S., the retention or possession of whale sharks in both commercial
and recreational fisheries has been prohibited since 1997 (Kyne et al. 2012). Some states, such as
Florida, also have harvesting and possession bans that apply to state waters. There are no federal or
state regulations prohibiting “harassing” or “molesting” whale sharks in U.S. waters, only a ban on
harvesting. In Mexico, the federal government finalized the Official Standard Rules (NOM-029-PESC2006) for shark and ray fisheries in 2006, and adopted the measures in 2007. These regulations ban the
take of whale sharks as well as basking sharks and white sharks in Mexican waters (Kyne et al. 2012). In
Cuba, no laws presently exist that specifically protect whale sharks (Graham 2007). In Belize and
Honduras, the whale shark has been federally protected since 2003 and 1998, respectively, but in
Guatemala there are no laws protecting the species (Kyne et al. 2012).
Marine Protected Areas
The use of marine protected areas (MPAs) for conservation of marine habitats and species can be found
in a number of countries bordering the GoM and western Caribbean. In most cases these MPAs are not
specifically designed or designated for whale sharks but may afford them some protection. In U.S.
waters, the Flower Garden Banks National Marine Sanctuary is an MPA providing some sanctuary for
Page 29
whale sharks in the northwestern GoM. This trio of coral reefs where whale sharks visit in summer
months lies about 170 km south of Sabine Pass, Texas. In Belize, the Gladden Spit and Silk Cayes Marine
Reserve encompasses the primary whale shark feeding area in those waters (Graham 2007). Off
Honduras, Roatan Marine Park and the Bay Islands Conservation Association co-manage a nationally
recognized marine reserve along the northwest coast of Roatan (http://www.roatanmarinepark.com/).
This protected area at least partially encompasses the whale shark feeding site off the northeast coast of
Utila. On the Caribbean coast of Cuba, where whale sharks sometimes visit, Jardines de la Reina is one
of Cuba’s largest MPAs. However, the primary whale shark aggregation sites appear to lie outside of this
MPA’s boundaries (Graham 2007). There is no protected area for whale sharks along Cuba’s northwest
coast, which Mote tagging data show to be an important area for migrating whale sharks and which has
been identified as a distinct biodiversity “hotspot” (Worm et al. 2003).
Mexico has taken the most progressive approach to designating a spatial area for whale shark
conservation. The islands of Isla Holbox, Isla Contoy, and Isla Mujeres and adjacent waters off the
northeast Yucatan Peninsula comprise several areas under the CONANP’s jurisdiction. The largest of
these is the Yum Balam Area de Protección de Flora y Fauna (“Lord Jaguar Protection Area of Flora and
Fauna”), which includes Isla Holbox, adjacent coastal and terrestrial areas, and an offshore zone that
slightly overlaps with a major whale shark feeding area (Fig. 4). According to CONANP, Mexican natural
protected areas such as Yum Balam are defined and designated as follows:
The instrument of environmental policy with greater legal definition for the conservation of
biodiversity is protected areas. These are portions of land or water in the country representing
various ecosystems, where the original environment has not been essentially altered and which
produce environmental benefits increasingly recognized and valued. They are created by
presidential decree and the activities that can be performed on them are set in accordance with
the General Act of Ecological Equilibrium and Environmental Protection, its regulations, the
management program and the programs of land-use planning in an ecological way. They are
subject to special protection, conservation, restoration and development, according to
categories defined in the Act. (http://www.conanp.gob.mx/english.php)
The real extent of CONANP’s authority to manage resources and development within these designated
areas is unclear. For example, the mega-development proposed for the eastern end of Isla Holbox falls
within the Yum Balam protected area, and yet development plans have proceeded. However, CONANP
has been the authoritative agency to oversee whale shark issues in Quintana Roo and has led a number
of important actions. These include licensing and regulation of the ecotourism industry (Table 1) and a
research and conservation program entitled “Proyecto Domino” (http://www.domino.conanp.gob.mx).
As research in the mid-2000s by Proyecto Domino, Mote Marine Laboratory, Georgia Aquarium and
others revealed the spatial extent of the whale shark feeding areas off Quintana Roo (Fig. 4), it became
clear these were mostly outside of the CONANP protected areas in place at that time. To address this,
the area of protection was expanded in June of 2009, with the Mexican federal government’s
establishment of the Whale Shark Biosphere Reserve, also administered by CONANP. This reserve was
Page 30
designed to encompass all of the primary locations where whale sharks had been reported between Isla
Holbox and the northern tip of Isla Contoy (de la Parra et al. 2011). The reserve was the first of its kind
in the world, specifically designated for whale sharks, and marked a major step forward in whale shark
conservation. Three years later, however, the actual authority of the reserve to manage and control
activities involving whale sharks, including ecotourism and boat/ship traffic, remains unclear.
Furthermore, with the more recent discovery of the “Afuera” aggregation east of Isla Contoy and
northeast of Isla Mujeres (Fig. 4), we now know that an extremely important feeding area for whale
sharks—perhaps one of the most important in the world—is not contained within the boundaries of the
present Whale Shark Biosphere Reserve.
In general MPAs presently provide some protection to whale sharks in the GoM and western Caribbean,
but these protected areas cover only a fraction of the habitat utilized by the highly mobile and migratory
sharks. Furthermore, MPAs can only be effective if regulatory powers are clear, if authority matches
responsibility, and if proper levels of enforcement are in place. On all three counts there is much work
left to do to protect whale sharks in the region.
One option to consider is elevating the protected area status for whale sharks to a higher level of
visibility, such as a UNESCO World Heritage Site. This would focus world attention on the special nature
of whale sharks and their habitats and could attract funding for conservation and management,
enforcement of regulations, and research. Currently there are 188 natural areas in the world designated
as World Heritage Sites, including five in Mexico and two in Cuba (http://whc.unesco.org). The U.S. has
none in the GoM. The Ningaloo Coast in Western Australia was declared a World Heritage Site in 2011,
largely because of the whale shark population there. The Belize Barrier Reef System is also on UNESCO’s
list of World Heritage in Danger.
The best candidate in the GoM and western Caribbean for new designation as a whale shark-rich World
Heritage Site, or other similar recognition, is the area off the northeast Yucatan Peninsula in Quintana
Roo, Mexico. The tremendous numbers of whale sharks feeding there from May to September, its
biodiversity of other large marine animals that aggregate there, its burgeoning ecotourism industry, and
its established network of federally protected areas provide the basis for establishing international
recognition of the entire region. Whether or not Mexico would embrace such an approach must be
explored, but only about 100 miles down the coast of Quintana Roo is the Sian Ka’an Biosphere Reserve,
also a UNESCO World Heritage Site.
Commercial Shipping Lanes
A whale shark MPA approach should include regulations on commercial shipping traffic through the
area. One effort already is underway in Quintana Roo. With hundreds of whale sharks and giant mantas
aggregating in the vicinity of major ship traffic (Figs. 7-9), concern has grown over the potential for
collisions between these animals and large ocean-going vessels. In 2011, Proyecto Domino initiated
plans to deploy three demarcation buoys near Isla Contoy and Isla Mujeres to protect the whale sharks,
other marine life, and ecotourism operators and tourists. These beacon buoys transmit alert messages,
Page 31
locations, and recommendations to nearby ships so they can avoid sensitive areas and proceed with
caution. In collaboration with the Instituto de Ciencias del Mar y Limnologia from the Universidad
Nacional Autonoma de Mexico (UNAM), the first mooring assembly was deployed in June 2012. The
remaining two moorings and their three associated buoys are scheduled to be deployed in 2013. Much
of this work is now being done by former CONANP/Proyecto Domino staffer Rafael de la Parra, who has
established a new NGO called “Ch’ooj Ajuail” to continue his research, conservation and education work
with whale sharks.
Information Exchanges, Meetings, and Partnerships
There is great potential for uniting entities in the GoM and Caribbean in a common cause to increase the
level of international protection for whale sharks in the region. There already is much overlap and
collaboration among U.S., Mexican and Cuban researchers working on the species, but the focus has
been primarily on individual research projects. The whale shark scientific community is relatively closeknit although some territorial friction exists with certain factions. That is not a trait unique to whale
sharks and can be overcome.
The use of meetings and information exchanges to advance the cause of whale shark conservation in the
GoM and Caribbean has been successfully used in the past. In April 2003, Mexican officials organized a
small meeting in Holbox to assess knowledge on the local whale shark population, which was just
beginning to be exploited by ecotourism operators. At that meeting a research program was designed
by two officials from CONANP (Jose Francisco Remolina Suarez and Dr. Jaime Gonzalez Cano) and Dr.
Robert Hueter from Mote Marine Laboratory. That framework led to a decade of discovery and
successful research on the whale sharks of Quintana Roo. In July 2008, the 2nd International Whale
Shark Conference was held in Holbox (http://www.domino.conanp.gob.mx/conferencia08.html). (The
first international conference was held in Perth, Australia in May 2005). The Holbox meeting brought
together researchers, conservationists, ecotourism operators, government officials and others from 21
countries including Mexico, Cuba and the U.S. A third international conference is planned for October
2013, at the Georgia Aquarium in Atlanta * (Dr. Hueter is on the organizing committee). These meetings
are very effective tools for exchanging information on whale sharks and designing and promoting new
advances in whale shark conservation.
Public Outreach
Public outreach and education play a powerful role in whale shark conservation. Major broadcast and
print media outlets are fond of whale shark stories and the media can be re-engaged in an effort to
increase whale shark protection in the GoM and western Caribbean. Websites are effective in providing
_____________________________________________________________________________
* One controversial issue in the whale shark conservation community is the capture and holding of whale shark specimens in
captivity for public display. Some individuals vehemently object to the practice as a tool to engage millions of people in the
cause for whale shark conservation. Because the Georgia Aquarium has four whale sharks on display, some of those individuals
might elect not to participate in the 2013 conference.
Page 32
public information on whale shark biology, sightings reports, conservation issues, and ecotourism
operations. Public lectures by experts on the subject are also popular in many countries. School
curriculum material on whale sharks for children in the U.S., Mexico and elsewhere is a widely applied
educational tool for reaching new audiences of younger generations. Aquarium displays of whale
sharks, as exemplified by the Georgia Aquarium in the U.S. and the Churaumi Aquarium in Okinawa,
Japan, are extremely popular. The Georgia Aquarium draws up to 4 million visitors per year and the
whale sharks are a marquee attraction. Incorporated into the exhibit is information on whale shark
biology, conservation and the research that the Aquarium has sponsored.
Public events and festivals celebrating whale sharks in local communities are another effective outreach
tool. In coastal towns in India where whale sharks have been harvested, public festivities promoting
whale shark conservation have included a colorful, life-sized inflatable model of a whale shark, used to
engage the admiration of both children and adults (Choudhary et al. 2008). Festivals in Western
Australia at Ningaloo celebrate their bounty of whale sharks. In Mexico, a whale shark festival has been
held on Isla Mujeres every summer beginning in 2008. This multi-day event includes parades with lifesize shark models, public lectures, workshops, puppet shows for children, contests, music and dance,
and other activities to promote the awareness of whale sharks among residents and tourists.
Page 33
Section 5 – Recommendations and Priorities
Based on the compiled information on whale shark biology, human uses, risks and vulnerabilities, and
solutions and opportunities, we recommend the following strategies and steps be considered to improve
whale shark conservation in the GoM and western Caribbean:
Regional Strategies
• Establish and/or expand national/international protected areas for whale sharks, associated
species, and their habitats in the region
• Create an international advisory body of scientists and conservation policy experts to study and
advise on whale shark issues in the GoM and Caribbean
• Use a multinational approach (trinational within the GoM) to develop a coordinated
international network of MPAs for the whale shark following the guidelines of Nash and
McLaughlin (2012):
o Use bottom-up coordination through data-sharing portals for whale shark information in
the region
o Cultivate local support for top-down governance strategies for the MPA network
o Develop international funding opportunities to encourage investment of national
resources into international whale shark conservation
o Create a multinational commission charged with implementation and management of
the international whale shark MPA network
• Strengthen regulations and enforcement of measures already in place protecting whale sharks
• Conduct further research on whale shark abundance, behavior, ecology, population genetics,
health, and risk assessment in the GoM and Caribbean, especially in ecotourism areas
• Modify shipping lanes as needed during critical periods of whale shark migration, feeding and
other aspects of their life history in the GoM and Caribbean
• Obtain international agreement on a standard code of conduct for the whale shark ecotourism
industry in the region
• Determine “carrying capacity” for whale shark ecotourism operations in the region
• Improve public communications in whale shark photo-identification, tag reporting, and other
data-generating functions
• Conduct public outreach and education in whale shark conservation for all of the countries of
the region
Steps in the U.S.
• Establish MPAs that protect aggregations of whale sharks and their key prey in the U.S. GoM,
e.g. in the northeastern GoM off the Mississippi River and the northwestern GoM in the Flower
Garden Banks area
• Include whale sharks in assessments of environmental impacts in the GoM, including the
impacts of oil/gas operations, marine pollution, shipping traffic, and coastal development
Page 34
•
•
•
Develop regulations prohibiting the harassment or molestation of whale sharks in federal and
state waters – e.g. no touching, minimum swimming/boating distances, etc. – and ensure that
all GoM state waters are covered by no harvest/possession/harassment regulations for whale
sharks
Continue research on whale shark hotspots in the U.S. Gulf, the importance of “prey” species,
such as the little tunny, in whale shark feeding ecology, and the environmental cues that whale
sharks use to navigate to these hotspots
Utilize the 3rd International Whale Shark Conference in Atlanta, Georgia in October 2013, as a
platform to plan, promote and advance the cause of whale shark conservation in the GoM and
western Caribbean
Steps in Mexico
• Increase the protected area of the Quintana Roo Whale Shark Biosphere Reserve to include the
Afuera zone and any other adjacent important areas for whale sharks
• Establish a higher level of protection of this aggregation area with World Heritage Site or similar
designation to conserve not just whale sharks but the special habitats and other faunal
aggregations off the northeast Yucatan Peninsula
• Determine “carrying capacity” for the burgeoning Quintana Roo whale shark ecotourism
industry and develop new regulations/permitting procedures to limit the industry to that
capacity
• Evaluate current code of conduct for the Mexican whale shark ecotourism industry to determine
if changes need to be made, by studying experiences in other areas (e.g. Western Australia)
• Incorporate higher standards for education of ecotourists in whale shark biology and
conservation and improve guide-training programs
• Obtain buy-in from the Mexican whale shark ecotourism industry by having its representatives
at the table for policy decisions and recognize/reward ecotourism operators who consistently
abide by the industry’s regulations and exemplify the proper code of conduct
• Work towards ensuring an equitable distribution of the economic benefits within the
ecotourism industry as a means of reducing negatives like competition and false advertising
(Ziegler et al. 2012)
• Include whale sharks in environmental impact assessments (oil/gas, pollution, shipping,
development)
Steps in Cuba
• Formalize full legal and regulatory protection for whale sharks in Cuban waters
• Establish MPAs for whale sharks at hotspots such as the northwest coast and the Jardines de la
Reina areas
• Research whale sharks in Cuba to better identify and delineate hotspots of abundance and
scope out areas for potential ecotourism operations
• Develop a standard code of conduct and carrying capacities for whale shark ecotourism
operations in Cuba
Page 35
•
Include whale sharks in environmental impact assessments (oil/gas, pollution, shipping,
development)
Beyond the GoM and Western Caribbean
• Coordinate whale shark conservation policy with other nations in the western Atlantic where
whale sharks are found, as the chances are good these are “shared” sharks with the GoM and
western Caribbean
• Establish full protection for whale sharks throughout the Americas and western Atlantic
• Conduct and coordinate research to discover migratory routes, population structure, feeding
areas, and mating and pupping grounds for whale sharks in the Atlantic, to protect the sharks in
those areas as needed
• Include whale sharks in environmental impact assessments (oil/gas, pollution, shipping,
development, other impacts) throughout their range in the western Atlantic
From these strategies and steps we recommend the following five priorities for near-term action items
for whale shark conservation in the GoM and western Caribbean:
Priorities
1. Expand the scope of the Quintana Roo, Mexico whale shark reserve into a broader MPA that
includes the aggregation zones and critical habitat for other megafauna (little tunny, rays,
billfish, marine turtles and mammals, etc.)
2. Establish carrying capacity for Quintana Roo whale shark ecotourism operations, institute those
limits through necessary regulation, improve codes of conduct as necessary (e.g. consider
reducing the hours and/or days of contact to decrease interference with whale shark feeding
behavior), and enforce those regulations
3. Engage the shipping industry and agencies overseeing marine navigation to determine needed
changes in shipping lanes to protect whale sharks, mantas and other surface-swimming
megafauna, as well as ecotourists enjoying these species, in the GoM and western Caribbean
4. Conduct research to further our knowledge of important whale shark biology and ecology in the
region and elsewhere where the sharks migrate
5. Establish international commissions to advise and oversee coordinated management for whale
shark protection and conservation in the GoM and western Caribbean
Page 36
References Cited
Alava MNR, Dolumbaló ERZ, Yaptinchay AA, Trono RB (1997) Fishery and trade of whale sharks and manta rays in
the Bohol Sea, Philippines. In Elasmobranch Biodiversity, Conservation, and Management (Fowler SL, Reed TM,
Dipper FA, eds.) p. 260. Sabah:IUCN.
Arzoumanian Z, Holmberg J, Norman B (2005) An astronomical pattern-matching algorithm for computer-aided
identification of whale sharks Rhincodon typus. J Appl Ecol 42: 999-1011.
Beaugrand G, Reid PC, Ibañez F, Lindley JA, Edwards M (2002) Reorganisation of North Atlantic marine copepod
biodiversity and climate. Science 296: 1692–1694.
Beckley LE, Cliff G, Smale MJ, Compagno LJV (1997) Recent strandings and sightings of whale sharks in South Africa.
Environ Biol Fish 50: 343-348.
Borrell A, Aguillar A, Gazo M, Kumarran RP, Cordona L (2011) Stable isotope profiles in whale shark (Rhincodon
typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environ Biol Fish 92: 559-567.
Bradshaw CJA, Fitzpatrick BM, Steinberg CC, Brook BW, Meekan MG (2008) Decline in whale shark size and
abundance at Ningaloo Reef over the past decade: the world’s largest fish is getting smaller. Biol Conserv 141(7):
1894-1905.
Brunnschweiler JM, Baensch H, Pierce SJ, Sims DW (2009) Deep-diving behaviour of a whale shark Rhincodon typus
during long-distance movement in the western Indian Ocean. J Fish Biol 74: 706-714.
Burke L, Sugg Z (2006) Watershed analysis for the Mesoamerican Reef. World Resources Institute, Washington DC,
USA, p. 40.
Burks CM, Driggers WB, Mullin KD (2006) Abundance and distribution of whale sharks (Rhincodon typus) in the
northern Gulf of Mexico. Fish Bull 104: 579-584.
Campagna C, Short FT, Polidoro BA, McManus R, Collette BB, et al. (2011) Gulf of Mexico oil blowout increases
risks to globally threateneed species. BioScience 61: 393-397.
Cárdenas-Palomo N, Herrera-Silveira J, Reyes Ó (2010) Distribución espacio-temporal de variables fisicoquímicas y
biológicas en el hábitat del tiburón ballena Rhincodon typus (Orectolobiformes: Rhincodontidae) al norte del
Caribe Mexicano. Rev Biol Trop 58(1): 399-412.
Cárdenas-Torres-Torres N, Enríquez-Andrade R, Rodríguez-Dowdell N (2007) Community-based management
through ecotourism in Bahia de los Angeles, Mexico. Fish Res 84: 114-118.
Carne L (2008) Monitoring and management of whale shark tourism at Gladden Spit and the Silk Cayes Marine
Reserve, Belize 2003-2007. In Second International Whale Shark Conference. Holbox, Mexico. Available at
http://www.domino.conanp.gob.mx/presentaciones.html (last accessed 11 December 2012).
Castro JI (2011) The Sharks of North America. Oxford University Press, Inc. New York, NY.
Castro ALF, Stewart BS, Wilson SG, Hueter RE, Meekan MG, et al. (2007) Population structure of Earth’s largest fish,
the whale shark (Rhincodon typus). Mol Ecol 16: 5183-5192.
Catlin J, Jones R (2010) Whale shark tourism at Ningaloo Marine Park: a longitudinal study of wildlife tourism.
Tourism Manage 21: 386-394.
Page 37
Causey B, Delaney J, Diaz E, Dodge D, Garcia J et al. (2002) Status of coral reefs in the US Caribbean and Gulf of
Mexico: Florida, Texas, Puerto Rico, U.S. Virgin Islands and Navassa. In Status of Coral Reefs of the World: 2000 (ed.
Wilkinson C), pp. 239–259. Australian Institute of Marine Science, Townsville, Australia.
Chang WB, Leu MY, Fang LS (1997) Embryos of the whale shark, Rhincodon typus, early growth and size
distribution. Copeia 1997(2): 444-446.
Chen, CT, Liu, KM, and Joung, SJ (1997) Preliminary report on Taiwan’s whale shark fishery. TRAFFIC Bulletin 17(1):
53-57.
Chen VY, Phipps MJ (2002) Management and trade of whale sharks in Taiwan. TRAFFIC East Asia-Taipei.
Chin A, Kyne PM, Walker TI, McAuley RB (2010) An integrated risk assessment for climate change: analysing the
vulnerability of sharks and rays on Australia’s Great Barrier Reef. Glob Change Biol 16: 1936-1953.
Choudhary RG, Joshi D, Mookerjee A, Talwar V, Menon V (2008) Turning the tide - the campaign to save Vhali, the
whale shark in Gujarat. Wildlife Trust of India 1-88. Available at:
http://www.wildlifetrustofindia.org/publications/reports.htm (last accessed 11 December 2012).
Clarke S (2004) Shark product trade in Hong Kong and mainland China and implementation of the CITES Shark
Listings. TRAFFIC East Asia, Hong Kong, China.
Colman JG (1997) A review of the biology and ecology of the whale shark. J Fish Biol 51: 1219-1234.
Compagno LJV (2001) Sharks of the world: an annotated and illustrated catalogue of shark species known to date.
Volume 2: bullhead, mackerel, and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes), FAO
Species Catalogue for Fishery Purposes No. 1, Rome. 269 pp.
Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of
extinction. Ecology 85: 265-271.
de la Parra R (2008) Domino Project Technical Report 2003-2008. CONANP. October 2008. Available at
de la Parra R, Remolina F, Tyminski J, Hueter R, González J, et al. (2008) Resultados Proyecto Dominó 2003-2007.
CONANP. October 2008. Available at http://www.domino.conanp.gob.mx/presentaciones.html (last accessed 11
December 2012).
de la Parra Venegas R, Hueter R, González Cano J, Tyminski J, Gregorio Remolina J, et al. (2011) An unprecedented
aggregation of whale sharks, Rhincodon typus, in Mexican coastal waters of the Caribbean Sea. PLoS ONE 6(4):
e18994. DOI:10.1371/journal.pone.0018994.
Dearden P, Topelko K, Ziegler J (2008) Tourist interactions with sharks. In J. Higham and M. Lück (Eds.). Marine
Wildlife and Tourism Management (pp. 66-90). Cambridge, MA: CAB International.
Department of Environment and Conservation (2012) Swimming with whale sharks.
Available at
http://www.dec.wa.gov.au/parks-and-recreation/key-attractions/whale-sharks.html?showall=&start=6
(last
accessed 11 December 2012).
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Marine Sci 1:
169-192.
Page 38
Fowler S (2000) Whale shark, Rhincodon typus, policy and research scoping study. Nature Conservation Bureau.
Available at http://www.whalesharkproject.org/do_download.asp?did=28155 (last accessed 11 December 2012).
Fox S (2008) Whale sharks of Utila – a study using the ECOCEAN photo ID database. In Second International Whale
Shark Conference. Holbox, Mexico. Available at http://www.domino.conanp.gob.mx/presentaciones.html (last
accessed 11 December 2012).
Gallagher AJ, Hammerschlag N (2011) Global shark currency: the distribution, frequency, and economic value of
shark ecotourism. Curr Issues Tourism 1: 1-16.
Gleiss AC, Norman B, and Wilson RP (2010) Moved by that sinking feeling: variable diving geometry underlies
movement strategies in whale sharks. Funct Ecol 25(3): 595-607.
Graham RT (2003) Behaviour and conservation of whale sharks on the Belize Barrier Reef. Ph. D, University of
York, York, UK. 408pp.
Graham RT (2004) Global whale shark tourism: a “golden goose” of sustainable and lucrative income. Shark News
16: 8-9.
Graham RT (2007) Whale sharks of the western Caribbean: an overview of current research and conservation
efforts and future needs for effective management of the species. Gulf Caribb Res 19(2): 149-159.
Graham RT, Roberts CM, Smart JCR (2006) Diving behaviour of whale sharks in relation to a predictable food pulse.
J R Soc Interface 3(6): 109–116.
Graham R, Roberts C (2007) Assessing the size, growth rate and structure of a seasonal population of whale sharks
(Rhincodon typus Smith 1828) using conventional tagging and photo identification. Fish Res 84: 71-80.
Graham RT, Witt MJ, Castellanos DW, Remolina F, Maxwell S et al. (2012) Satellite tracking of manta rays highlights
challenges to their conservation. PLoS ONE 7(5): 1-6.
Graham WM, Condon RH, Carmichael RH, D'Ambra I, Patterson HK et al. (2010) Oil carbon entered the coastal
planktonic food web during the Deepwater Horizon oil spill. Environ Res Lett 5(4): 1-6.
Gudger EW (1931) The fourth Florida whale shark, Rhineodon typus, and the American Museum model based on it.
Bull Amer Mus Nat Hist 61: 613-637.
Gudger EW (1936) The whale shark off Havana. Sci Monthly 42: 84-85.
Gudger EW (1937a) A whale shark impaled on the bow of a steamer near the Tuamotus, south seas. Science 85:
314.
Gudger EW (1937b) A whale shark speared on the bow of a steamer in the Caribbean Sea. Copeia 1: 60.
Gudger EW (1938) Four whale sharks rammed by steamers in the Red Sea region. Copeia 4: 170-173.
Gudger EW (1939a) The whale shark in the Caribbean Sea and the Gulf of Mexico. Sci Monthly 48: 261-264.
Gudger EW (1939b) A school of whale sharks in the Bahamá Islands. Nature 143: 79-80.
Gudger EW (1940) Whale sharks rammed by ocean vessels: how these sluggish leviathans aid in their own
destruction. New England Naturalist 7: 1-10.
Page 39
Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F et al. (2008) A global map of human impact on marine
ecosystems. Science 319: 948-952.
Hanfee F (2001) Gentle giants of the sea. Traffic-India /WWF-India.
Heyman WD, Graham RT, Kjerfve B, Johannes RE (2001) Whale sharks Rhincodon typus aggregate to feed on fish
spawn in Belize. Mar Ecol Prog Ser 215: 275-282.
Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395: 520.
Hoffmayer ER, Franks JS, Shelley JP (2005) Recent observations on whale sharks, Rhincodon typus, in the
northcentral Gulf of Mexico. Gulf Caribb Res 17: 117-120.
Hoffmayer ER, Franks JS, Driggers WB, Oswald KJ, Quattro JM (2007) Observations of a feeding aggregation of
whale sharks, Rhincodon typus, in the north central Gulf of Mexico. Gulf Caribb Res 19(2): 69-73.
Holmberg J, Norman B, Arzoumanian Z (2009) Estimating population size, structure, and residency time for whale
sharks Rhincodon typus through collaborative photo-identification. Endangered Sp Res 7: 39-53.
Hsu HH (2009) Age, growth, and migration of the whale shark, Rhincodon typus, in the Northwestern Pacific.
Unpub. Ph.D. diss., 189 pp. National Taiwan Ocean University, Keelung, Taiwan.
Hueter B (2012) Whale shark aggregation areas. In Beyond the Horizon: A Forum to Discuss a Potential Network of
Special Ocean Places to Strengthen the Ecology and Culture of the Gulf of Mexico (KB Ritchie and WE Kiene, eds), p
40-41. Proceedings of the Forum: May 11-13, 2011, Mote Marine Laboratory, Sarasota, Florida. Available at
http://www.mote.org/clientuploads/4nadine/beyondhorizon/BTH%20Forum%20Proceedings%20Final.pdf and at
http://issuu.com/lawsonmitchell/docs/bth_forum_proceedings_final/3 (last accessed 11 December 2012).
Hueter RE, Tyminski JP, de la Parra R (2008) The geographical movements of whale sharks tagged with pop-up
archival satellite tags off Quintana Roo, Mexico. In Second International Whale Shark Conference. Holbox, Mexico.
Available at http://www.domino.conanp.gob.mx/presentaciones.html (last accessed 11 December 2012).
IUCN (2012) IUCN Red List of Threatened Species. Version 2012.2. <www.iucnredlist.org>. Downloaded on 07
December 2012.
Joung SJ, Chen CT, Clark E, Uchida S, Huang WYP (1996) The whale shark, Rhincodon typus, is a livebearer: 300
embryos found in one ‘megamamma’ supreme. Environ Biol Fish 46: 219-223.
Ketchum JT, Galván-Magaña F, Klimley AP (2012) Segregation and foraging ecology of whale sharks, Rhincodon
typus, in the southwestern Gulf of California. Environ Biol Fish DOI 10.1007/s10641-012-0071-9.
Kukuyev EI (1996) The new finds in recently born individuals of the whale shark Rhiniodon typus (Rhiniodontidae)
in the Atlantic Ocean. J Ichthyol 36: 203-205.
Kyne PM, Carlson JK, Ebert DA, Fordham SV, Bizzarro JJ, Graham RT, Kulka DW, Tewes EE, Harrison LR, Dulvy NK
(eds) (2012) In The Conservation Status of North American, Central American, and Caribbean Chondrichthyans.
IUCN Species Survival Commission Shark Specialist Group, Vancouver, Canada.
McCauley DJ, DeSalles PA, Young HS, Dunbar RB, Dirzo R et al. (2012) From wing to wing: the persistence of long
ecological interaction chains in less-disturbed ecosystems. Sci Rep 2(409): 1-5.
Page 40
McKinney JA, Hoffmayer ER, Wu W, Fulford R, Hendon JM (2012) Feeding habitat of the whale shark Rhincodon
typus in the northern Gulf of Mexico determined using species distribution modeling. Mar Ecol Prog Ser 458: 199211.
Meekan MG, Bradshaw CJA, Press M, McLean C, Richards A, et al. (2006) Population size and structure of whale
sharks Rhincodon typus at Ningaloo Reef, Western Australia. Mar Ecol Prog Ser 319: 275-285.
Merino M (1997) Upwelling on the Yucatan Shelf: hydrographic evidence. J Marine Syst 13: 101–121.
Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R, et al. (2010) Feeding anatomy, filter-feeding rate, and
diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology
113: 199-212.
Nash HL, McLaughlin RJ (2012) Opportunities for trinational governance of ecologically connected habitat sites in
the Gulf of Mexico. KMI International Journal of Maritime Affairs and Fisheries 4(1): 1-32.
Norman B (1999) Aspects of the biology and ecotourism industry of the whale shark Rhincodon typus in northwestern Australia. Masters Thesis. Perth. Western Australia: Murdoch University.
Norman B (2005) Rhincodon typus. In: IUCN 2010. IUCN red list of threatened species. Version 2010.1. Available:
http://www.iucnredlist.org. Downloaded on 7 December 2012.
Norman B, Catlin J (2007) Economic importance of conserving whale sharks. Report for the International Fund for
Animal Welfare (IFAW), Australia.
Norman B, Stevens JD (2007) Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in
Western Australia. Fish Res 84: 81-86.
Pattengill-Semmens C, Gittings SR, Shyka T (2000) Flower Garden Banks National Marine Sanctuary: a rapid
assessment of coral, fish, and algae using the AGRRA protocol. Marine Sanctuaries Conservation Series MSD-00-3.
U.S. Department of Commerce, National Oceanic and Atmospheric Administration, Marine Sanctuaries Division,
Silver Spring, MD. 15 pp.
Pérez R, Muller-Karger FE, Victoria I, Melo N, Cerdeira S (1999) Cuban, Mexican, U.S. researchers probing mysteries
of Yucatan current. EOS Trans AGU 80, 153-158.
Pina F, Figueredo T, González G (2008) Dameros (Rhincodon typus) en Jardines de la Reina, Cuba. In Second Intl.
Whale Shark Conference., Holbox, Mexico. Available at http://www.domino.conanp.gob.mx/presentaciones.html
(last accessed 11 December 2012).
Pravin P (2000) Whale shark in the Indian coast – need for conservation. Curr Sci India 79(3): 310-315.
Quiros A (2005) Whale shark “ecotourism” in the Philippines and Belize: evaluating conservation and community
benefits. Trop Res Bull 24: 42-48.
Quiros AL (2007) Tourist compliance to a code of conduct and the resulting effects on whale shark (Rhincodon
typus) behavior in Donsol, Philippines. Fish Res 84: 102-108.
Ramírez-Macías D, Vázquez-Juárez R, Galván-Magaña F, Munguía-Vega A (2007) Variations of the mitochondrial
control region sequence in whale sharks (Rhincodon typus) from the Gulf of California, Mexico. Fish Res 84: 87-95.
Page 41
Ramírez-Macías D, Meekan M, de la Parra-Venegas R, Remolina-Suárez, Trigo-Mendoza M, et al. (2012) Patterns in
composition, abundance and scarring of whale sharks Rhincodon typus near Holbox Island, Mexcio. J Fish Biol 80:
1401-1416.
Richardson AJ (2008) In hot water: zooplankton and climate change. ICES J Mar Sci 65:279-295.
Riley MJ, Harman A, Rees RG (2009) Evidence of continued hunting of whale sharks Rhincodon typus in the
Maldives. Environ Biol Fish 86: 371-374.
Rowat D, Meekan MG, Engelhardt U, Pardigon B, Vely M (2007) Aggregations of juvenile whale sharks (Rhincodon
typus) in the Gulf of Tadjoura, Djibouti. Environ Biol Fish 80: 465-472.
Rowat D, Brooks K, March A, McCarten C, Jouannet D et al. (2011) Long-term membership of whale sharks
(Rhincodon typus) in coastal aggregations in Seychelles and Djibouti. Mar Freshwater Res 62: 621-627.
Rowat D, Brooks KS (2012) A review of the biology, fisheries and conservations of the whale shark Rhincodon
typus. J Fish Biol 80: 1019-1056.
Schmidt JV, Schmidt CL, Ozer F, Ernst RE, Feldheim KA, et al. (2009) Low genetic differentiation across three major
ocean populations of the whale shark, Rhincodon typus. PLoS ONE 4(4): e4988. doi:10.1371/journal.pone.0004988.
Schmidt JV, Chen CC, Sheikh SI, Meekan MG, Norman BM, et al. (2010) Paternity analysis in a litter of whale shark
embryos. Endang Species Res 12: 117-124.
Sequeira A, Mellin C, Rowat D, Meekan MG, Bradshaw CJA (2011) Ocean-scale prediction of whale shark
distribution. Diversity Distrib 1-15. DOI: 10.1111/j.1472-4642.2011.00853.x.
Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine
phytoplankton. Science 327: 676-679.
Sisneros JA, Nelson DR (2001) Surfactants as chemical shark repellents: past, present, and future. Environ Biol
Fishes 60:117-130.
Sleeman JC, Meekan MG, Fitzpatrick BJ, Steinberg CR, Ancel R, et al. (2010a) Oceanographic and atmospheric
phenomena influence the abundance of whale sharks at Ningaloo Reef, Western Australia. J Exp Mar Biol Ecol
382(2): 77-81.
Sleeman JC, Meekan MG, Wilson SG, Polovina JJ, Stevens JD, et al. (2010b) To go or not to go with the flow:
environmental influences on whale shark movement patterns. J Exp Mar Biol Ecol 390: 84-98.
SPC-OFP (2011) Summary information on whale shark and cetacean interactions in the tropical WCPFC purse seine
fishery. Eighth Regular Session of WCPFC, Information paper WCPFC8 ‐2011‐IP‐01. Tumon, Guam, USA. Available at
http://www.wcpfc.int/node/4476 (last accessed 11 December 2012).
Speed CW, Meekan MG, Russel BC, Bradshaw CJA (2008a) Recent whale shark (Rhincodon typus) beach strandings
in Australia. Marine Biodiversity Records 2: 1-3.
Speed CW, Meekan MG, Rowat D, Pierce SJ, Marshall AD, et al. (2008b) Scarring patterns and relative mortality
rates of Indian Ocean whale sharks. J Fish Biol 72(6): 1488-1503.
Stevens JD (2007) Whale shark (Rhincodon typus) biology and ecology: a review of the primary literature. Fish Res
84: 4-9.
Page 42
Stewart BS, Wilson SG (2005) Threatened fishes of the world: Rhincodon typus (Smith 1828) (Rhinodontidae).
Environ Biol Fish 74: 184-185.
Tyminski J, Hueter R, de la Parra R (2008) The vertical movements of whale sharks tagged with pop-up archival
satellite tags off Quintana Roo, Mexico. In Second International Whale Shark Conference. Holbox, Mexico.
Available at http://www.domino.conanp.gob.mx/presentaciones.html (last accessed 11 December 2012).
Van Tienhoven AM, Den Hartog JE, Reijns RA, Peddemors VM (2007) A computer-aided program for patternmatching of natural marks on the spotted raggedtooth shark Carcharias taurus. J Appl Ecol 44: 273-280.
Wilson SG, Taylor JG, Pearce AF (2001) The seasonal aggregation of whale sharks at Ningaloo Reef, Western
Australia: currents, migrations and the El Niño/Southern Oscilliation. Environ Biol Fish 61: 1-11.
Wilson SG, Polovina JJ, Stewart BS, Meekan MG (2006) Movement of whale sharks (Rhincodon typus) tagged at
Ningaloo Reef, Western Australia. Mar Biol 148: 1157-1166.
Wolfson FH (1983) Records of seven juveniles of the whale shark, Rhiniodon typus. J Fish Biol 22: 647-655.
Worm B, Lotze HK, Myers RA (2003) Predator diversity hotspots in the blue ocean. Proc Natl Acad Sci USA 100:
9884-9888.
Zavala-Hidalgo J, Gallegos-García A, Martínez-López B, Morey SL, O'Brien JJ (2006) Seasonal upwelling on the
western and southern shelves of the Gulf of Mexico. Ocean Dynam 56: 333-338.
Ziegler J, Dearden P, Catlin J, Norman B (2008) Assessing the sustainability of whale shark tourism: a global
perspective. In Second International Whale Shark Conference. Holbox, Mexico. Available at
Ziegler J, Dearden P, Rollins R (2012) But are tourists satisfied? Importance-performance analysis of the whale
shark industry on Isla Holbox, Mexico. Tourism Manage 33: 692-701.
Page 43

Issues and Options for Whale Shark Conservation in Gulf of Mexico

Transcription

Similar documents

What Are The Odds Of A Shark Attack?

April 16-23, 2011 Deep Blue Resort

whale tail

Sharks have a skeleton that is made out of cartilage and connective

The SILENCE OF THE SHARKS project is

Fungalland and the Stranded Mother Whale

Truth About Shark Attack

Events December 2014 - Comox Valley Aquatic Club

long-finned pilot whale