A Shark Attack Outbreak Off Recife, Pernambuco, Brazil: 1992ÂŒ2006

BULLETIN OF MARINE SCIENCE, 82(2): 199–212, 2008

A Shark Attack Outbreak off Recife, Pernambuco, Brazil: 1992–2006

Fábio H. V. Hazin, George H. Burgess, and Felipe C. Carvalho

Abstract An unprecedented series of shark attacks on humans off Recife, Pernambuco, Brazil within a 14-yr period from September 1992 to September 2006 resulted in 47 incidents, including 17 fatalities. A suite of biotic and abiotic factors was examined to determine commonality in the attacks. Surfers and body boarders were the group most affected with a majority of victims being young (< 20 yrs old) males. Attacks occurred predominantly in shallow water, close to shore at beaches lying on a narrow channel bordered by an adjacent reef. Attacks transpired year-round with peaks in July and were distributed daily from Thursday to Tuesday, with peak on Sundays and no attacks recorded on Wednesdays. The construction and growth of the Suape Port, located just to the south of Recife, has resulted in major environmental degra- dation and is likely to have played a role in the recent onset of shark attacks. Individ- uals of the species most often implicated in the attacks, the bull shark, Carcharhinus leucas (Müller and Henle, 1839), may have been displaced from preferred estuarine/ inshore habitats to the nearby Jaboatão River and the adjacent lagoon resulting in increased interaction with humans.

Shark attack on humans is not a recent phenomenon. The first writings on shark attacks date back to ancient Greece, about 500 yrs BC (Coppleson, 1958). In more recent years, despite the impact of fishing pressure on shark populations, the worldwide trend towards more intense recreational use of marine waters has increased the chances of shark-human interactions, resulting in an increase in the total number of attacks (Burgess, 1990). The gradual post-World War II increase in shark attacks, plus the military relevance of shark attacks as related to air and sea disasters during war- time, prompted the U.S. Office of Naval Research to establish the International Shark Attack File (ISAF), in 1958 (Baldridge, 1974). Presently, the ISAF is maintained at the Florida Museum of Natural History at the University of Florida, under the auspices of the American Elasmobranch Society. Recife is a rather large city located in northeastern Brazil. The capital of Pernam- buco State, it has a population of about 1.5 million and the tourism industry is one of its major economic activities. In 2005, Recife accounted for 5.15% of the total number of national and international tourists in Brazil (EMBRATUR, 2006). Recife has a coastline of about 20 km, with beautiful beaches and warm waters, which are several of its main attractions. Recife seawater temperatures range from about 24 °C during winter to 30 °C during summer (Hazin et al., 2000), fostering year-round bathing, surfing, and other aquatic recreational activities. Despite intense recreational use of Recife beaches since the early 1950s, except for a few unconfirmed anecdotal reports of shark attacks, there were virtually no records of such incidents in the area until 1992. However, within a period from June 1992 to September 2006, 47 attacks were recorded, including 17 fatalities. All attacks occurred along a 20 km stretch of shoreline, which included the beaches of Paiva, Candeias, Piedade, Boa Viagem, and Pina, all of which are under the influence of the Jaboatão River estuary (Fig. 1). This sudden outbreak of shark attacks was highly

Figure 1. Recife, Pernambuco, Brazil. The gray area represents the metropolitan region of Recife. publicized by local and national media, resulting in a negative economic impact on tourism, which, unfortunately, is difficult to fully assess (Gaiser, 1976). Shark attacks are relatively uncommon worldwide, annually averaging 50–75 un- provoked incidents and resulting in about 5–10 deaths (Burgess, 1990). Most attacks are recorded in waters of the United States (primarily in Florida and California), South Africa, and Australia (ISAF, 2006). Thus, this sudden outbreak of attacks in Brazil with more than one-third of the incidents resulting in fatalities, occurring within almost 14 yrs and along a narrow band of 20 km of shoreline, is quite unusual. In this study, we examine the characteristics of the recorded shark attacks in Recife, and consider several possible causes. HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 201

Materials and Methods

Information on the shark attacks was obtained from numerous sources, including pub- lished accounts in the local media, direct interview with witnesses, victims, and doctors that treated the wounds, and, in the case of fatalities, direct inspection of the remains of victims at the local Institute of Legal Medicine, in Recife. After the initial cases, the Universidade Feder- al Rural de Pernambuco (UFRPE) became a central clearinghouse for regional shark attacks. Whenever an attack occurred, members of the UFRPE staff were immediately contacted by local media, fire/rescue officials and/or physicians, the latter from emergency hospitals as well as from the Institute of Legal Medicine, facilitating the investigation of the incidents. Bodies bearing shark bites were considered the result of an attack incident only when the coroner’s report indicated that blood loss had been the causa mortis. All victims that died by drowning were thus excluded from the attack statistics. The total number of fatal drowning victims (those who disappeared at sea with the body subsequently recovered), including those bearing post-drowning shark-inflicted scavenge bites, occurring during the January 1990–April 1995 period were obtained from the archives of the Institute of Legal Medicine. Data from the 32-mo period prior the shark attack outbreak (January 1990–August 1992) were then compared to the 32-mo period after it began (September 1992–April 1995). As in Baldridge (1974) and McCosker and Lea (2006), the present study analyzed the attacks in relation to attack location, day of the week, time of the day, moon phase, and distance from shore. Information on distance from shore, however, must be interpreted with caution since it is based on the testimony of victims and eyewitnesses. Similarly, testimonies on the estimated depth of the attack site were, in many instances, very inaccurate and inconsistent with known bathymetry of the region and thus not considered in the present analysis. The possible influence of local bathymetry on shark behavior and attack occurrence was investigated by making a detailed bathymetric survey of Recife beaches to a distance of 8.0 km from shore (Fig. 2), with 500 m spacing between contours. The survey was conducted from a small boat equipped with a Furuno digital echosounder, with all depth data being reduced to level 0 for the Port of Recife using Brazilian Navy tidal tables (DHN, 2001). The activities of the victims were divided into two categories: (a) board riders (surfers or body boarders), and (b) bathers (swimmers and bodysurfers). Due to the increase in shark attacks, all board-riding activities in the attack area were banned by a Government decree on 1 January 1995. The prohibition was later reinforced by a new, stricter decree in May 1999. Therefore the activities of victims were analyzed for two periods bounded by the initial decree. The first period is prior to surfing prohibition, from September 1992 to December 1994, and the second period ranges from January 1995 to September 2006, during the surfing ban period. The severity of injuries was defined as either fatal or non-fatal, and the injured body part was classified as legs (calf, knee, and thigh), arms (hand, forearm, elbow, and upper arm), torso, and multiple body regions, noting that in some instances more than one body part was injured (e.g., torso and leg). Based on bite patterns, tooth fragments and description of the shark by victims and eyewitnesses, it was possible to identify the responsible species in only seven of the 47 attacks. In the early 1980s, construction began on a new port facility, the Suape Port, located just to the south of the attack area (Fig. 1). During this construction, major changes to the local marine ecosystem were noted; therefore, we investigated the possible contributing role of the port construction in the increased frequency of shark attacks. Since sharks are known to follow ships (Baldridge, 1974; Schultz, 1975) and port areas are recognized as having a higher risk of shark attacks (Coppleson, 1958), data on the monthly frequency of incoming ships were obtained and compared to the monthly frequency of shark attacks. The number of drowning victims bearing shark scavenge bites was also examined to determine whether they exhibited a similar increase as the confirmed attacks, which could mean a higher number of scavenging sharks in the area or perhaps an increase in unreported attacks. 202 BULLETIN OF MARINE SCIENCE, VOL. 82, NO. 2, 2008

Figure 2. Bathymetry of Recife, Pernambuco, Brazil. The arrow indicates nearshore channel lying adjacent to popular beaches and surfing locations. We also evaluated a possible relationship between the rise in shark attacks and an increase in the number of people living in Recife. As data on the actual number of people living in coastal areas, as well as the census of people frequenting Recife beaches by year or days of week were not available, the analysis was done by using Recife population data from 1980 to 2005 (IBGE, 2006) as a proxy for human utilization of nearshore waters. Fluctuating environmental variables could also be important in understanding the dynamics of the ecosystem and its influence in shark attacks. Data of rainfall at latitude 08°36´00˝S and longitude 34°55´12˝W were obtained from CPTEC (Center for Weather Forecasting and Climatic Studies), located near Cidade Universitária, Recife. A survey was completed by UFRPE that documented the quantity of untreated waste dumped directly into the Jaboatão River estuary from both the Muribeca Waste Landfill, a 62-ha garbage dump, and the Ja- boatão Public Slaughterhouse.

Results

The bathymetric survey indicated the presence of a deep channel located approximately 500 m offshore, having a maximum depth of about 6 m during low tide, run- ning roughly parallel to the beaches of Boa Viagem and Piedade. Farther seaward, at about 2 km offshore, a bank of calcareous algae occurs at depths < 2 m (Fig. 2). Most shark attacks victims (52.6%) were < 20 yrs of age (Table 1) and their primary activity was riding a surfboard or a body board (55.3%, Table 2). The activity of vic- HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 203

Table 1. Age of the victims involved in shark attacks off Recife, Pernambuco, Brazil.

Age Number of attacks % of Attacks 11–15 3 6.4 16–20 17 36.2 21–25 11 23.4 26–30 2 4.3 31–35 4 8.5 36–40 1 2.1 Unknown 9 19.1

tims was almost identical prior to and after the first government decree prohibiting the use of surf or body boards in the area of risk (1 January 1995), indicating that this user group largely ignored the prohibition. However, after the second decree (May 1999), the situation changed, as bathers were involved in the majority of the incidents. The fatality rate was much higher among bathers than board riders, but dropped for both groups after the second decree (Table 3). Surfers were mainly attacked on the legs (71.0%), while the majority of bathers were bitten on the torso (50.0%, Table 4). The mean yearly number of attacks for the 1992–2006 period was 3.2. From 1992 to 2006, the number of attacks per year was close to the overall mean, except for 1994, when 10 incidents were recorded (Table 2). Following the second governmental decree in 1999, the attack frequency initially dropped and then increased; 2000 (no attacks recorded), 2001 (one attack), 2002 (six attacks), and 2004 (seven cases). The number of attacks was particularly high in the month of July (Kruskal-Wallis, F = 3.21; P = 0.028) (Fig. 3). Attacks on surfers were much more common during new and full moons than during first and last quarters K( ruskal-Wallis, F = 2.90; P = 0.011); however, for bathers, attacks were significantly higher only during the new moon (Kruskal-Wallis, F = 1.77; P = 0.006) (Fig. 4). Most of the attacks took place at Boa Viagem and Piedade Beaches (Kruskal-Wallis, F = 3.10; P = 0.017) (Fig. 5). Approximately 62% of the incidents occurred within 100 Table 2. Activity of 47 victims involved in shark attacks off Recife, Pernambuco, Brazil.

Number of attacks Number of attacks Total number Year on surfers (%) on bathers (%) of attacks 1992 1 (33.3) 2 (66.7) 3 1993 2 (66.7) 1 (33.3) 3 1994 9 (90.0) 1 (10.0) 10 1995 3 (100) 0 (0.0) 3 1996 2 (66.7) 1 (33.3) 3 1997 2 (66.7) 1 (33.3) 3 1998 3 (75.0) 1 (25.0) 4 1999 1 (50.0) 1 (50.0) 2 2000 0 (0.0) 0 (0.0) 0 2001 0 (0.0) 1 (100) 1 2002 2 (33.3) 4 (67.7) 6 2003 0 (0.0) 0 (0.0) 0 2004 1 (14.3) 6 (85.7) 7 2005 0 (0.0) 0 (0.0) 0 2006* 0 (0.0) 2 (100) 2 Total 26 (55.3) 21 (44.7) 47 * Jan–Sept. 204 BULLETIN OF MARINE SCIENCE, VOL. 82, NO. 2, 2008

Table 3. Activity of 47 shark attack victims in periods prior to and after first governmental decree, and after second governmental decree banning all board-riding activities.

Number of Number of attacks Number of attacks on Number of Total number Period on surfers (%) fatalities (%) bathers (%) fatalities (%) of attacks Pre-Decree I Sep. 1992–Dec. 1994 12 (75.0) 1 (8.3) 4 (25.0) 4 (100.0) 16 Post-Decree I Jan. 1995–Apr. 1999 10 (76.9) 2 (20.0) 3 (23.1) 3 (100.0) 13 Post-Decree II May. 1999–Sep. 2006 4 (22.2) 0 (0.0) 14 (77.8) 7 (50.0) 18 All Periods 26 (55.3) 3 (11.5) 21 (44.7) 14 (66.7) 47

m of shore (Table 5). Review of the daily frequency of attacks during the 14-yr period revealed a pattern of increasing number of attacks from Thursday to a peak on Sun- day then declining through Wednesdays, when no attacks were recorded. The number of attacks on Sunday was significantly different from the number of attacks that occurred on other days of week (Kruskal-Wallis, F = 2.08; P = 0.014; Fig. 6). Although quantified data on the actual number of people at the beaches by weekday are un- available, according to lifeguard Cel. Ricardo Santana. (Corpo de Bombeiros Militar de Pernambuco, pers. comm.), the number is low from Monday through Wednesday, begins to increase on Thursday, and peaks on Sunday. Attacks were most frequent early in the morning (0600–0800) and later in the day (1600–1800) (χ2 = 9.41; df = 2; P < 0.001; Fig. 7). Of 172 people that died from drowning during the initial 32-mo period (January 1990–August 1992) before the shark attack outbreak, 12 had shark scavenge bites, a frequency of 7.0% (Table 6). During the first 32 mo after the attacks began (September 1992–April 1995), 258 persons died by drowning. Sixteen of the victims had shark scavenge bites, a frequency of 6.2%, nearly equal to that of the previous period. Examination of the number of shark attacks and drowning cases with shark scavenge bites in conjunction with the number of ships entering Suape Port by month, during the period September 1992–December 1994 (28 mo) indicated that the number of scavenged drowning victims was not significantly different for the three ranges (χ2 = 042; df = 2; P > 0.10), but shark attacks occurred in a much higher frequency in months where the number of ships entering the Suape Port in a month was > 30 (χ2 = 12. 38; df = 2; P < 0.001; Table 7). The shark species responsible for attack was confidently identified in seven cases; six being attributed to the bull shark, Carcharhinus leucas (Valenciennes, 1839) and one to the tiger shark, Galeocerdo cuvier (Perón and Lesueur, 1822) (Gadig and Saz- ima, 2003). The size of the attacking sharks ranged from about 1.0–3.0 m, based on

Table 4. Body locations subjected to traumatic injury in 44 shark attack victims from Recife, Brazil.

Number of Number of Total number of Body locations affected surfers affected bathers affected victims Legs 17 6 23 Arms 3 2 5 Torso 1 10 11 Multiple body regions 3 2 5 Total 24 20 44 HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 205

Figure 3. Mean number (± SE) of shark attacks per month. Numbers above the bars are total number of shark attacks.

the comparative analysis of residual tooth fragments and the size of the bites on the surfboards (Kohler et al., 1996). According to the Environmental Monitoring Plan for Water Resources—Jaboatão River Basin, provided by EMLURB (Urban Maintenance and Sanitation Company), in the year 2000 the Jaboatão Public slaughterhouse dumped its untreated effluents directly into the Jaboatão River at an average volume of 345 m3 d–1, including blood, entrails, and associated water. The BOD (Biochemical Oxygen Demand, a measure of the quantity of dissolved oxygen necessary for the decomposition of organic matter by microorganisms, such as bacteria) for this type of waste, estimated at 7400 mg L, was the highest among all industrial waste sources identified in the region, surpassing the volume of the second highest pollution source (Pernambuco Chemi- cal, with 394 mg L) by nearly 20 times. The EMLURB plan also stated that the flow of untreated liquid waste from the Muribeca Waste Landfill into the Jaboatão River was at an average of 60 L min–1, with an increase of around 20% during the rainy season.

Figure 4. Mean number (± SE) of shark attacks per lunar phase. Numbers above the bars are to total number of shark attacks. 206 BULLETIN OF MARINE SCIENCE, VOL. 82, NO. 2, 2008

Figure 5. Mean number (± SE) of shark attacks as a function of the different beaches. Numbers above the bars are to total number of shark attacks.

Discussion

The population of Recife increased from about 1,150,000 people in 1980 to 1,300.000 in 1990. In 2004, the year of the last demographic census, the Recife population reached 1,511,000 people (IBGE, 2006). It is clear, therefore, that although the population grew about 13% from the 1980s to the 1990s, with a likely similar increase in the number of people in Recife beaches, this rise is by no means sufficient to -ex plain the sharp increase in shark attacks. As observed in other areas of the world, most of the shark attack victims were young male surfers, a trend explained by the observation that at Recife beaches male surfers greatly outnumber female surfers (Geraldo Carvalho, ASPE, pers. comm.). Additionally, males tend to be much more recreationally active than women at Rec- ife beaches, and advance into deeper waters. The high incidence of attacks on board riders can be explained by the nature of the sport. Surfing and body boarding are highly provocative activities. The splashing of arms and legs while paddling could be an attractant to sharks (ISAF, 2006). In contrast to swimmers, board riders spend longer periods in the water and venture greater distances from the shore. These hab- its render them more vulnerable to an encounter with a shark (Cliff, 1991). This is particularly true in the case of Recife beaches, because of their peculiar topography. Due to the presence of a deep channel close to shore, the surfers spend most of their time waiting for appropriate waves, which form exactly where the depth gradient is highest, i.e., on the edge of the channel. A deep channel located near a beach, sandbar or reef is an excellent place from which a shark can initiate an attack (Schultz, 1975). The submarine topography may also explain why Boa Viagem and Piedade Beaches accounted for almost 80% of the attacks, since these are the sections of the shoreline

Table 5. Distance from shore at which 21 shark attacks occurred. Distance from shore data could not be obtained for other victims.

Distance from shore Number of attacks on surfers Number of attacks on bathers 0–50 m 2 4 51–100 m 3 4 101–150 m 1 1 151–200 m 1 1 201–250 m 1 0 251–300 m 2 1 HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 207

Figure 6. Mean number (± SE) of shark attacks per day of the week. Numbers above the bars refer to total of shark attacks. where the channel lies closest to the beach. This feature may also explain why most of the attacks happened within 100 m of the shore, although this is a general worldwide trend since the majority of swimmers are found within 30 m from shore (Baldridge, 1974). At the time of the attack, most of the surfers were sitting on the board waiting for a “good” wave, which explains why most victims were bitten on the legs, while a majority of bathers were attacked on the torso. It is also reasonable to assume that a surfer’s leg hanging from the board and moving in deeper water is more attractive to a shark than a bather standing in the shallow water. The differences in location of bites on the bodies of bathers (torso) and surfers (legs) likely contributed to markedly higher fatality rate in bathers. In addition, injured surfers also have the resource of the board to lie upon during the swim back to the beach and are commonly accom- panied by colleagues that may help them to get safely ashore. The nearly equal proportion of surfers and bathers attacked before and after the first decree prohibiting board riding activities in the affected beaches demonstrates that the initial decree did little to discourage surfers from continuing their practice (although over a 100 surfboards were seized and burned by beach safety personnel). The second decree, however, apparently was more effective since there was a significant reduction in the number of surfers attacked.

Figure 7. Shark attacks on 23 surfers and 14 bathers as a function of time of day. Numbers above the bars are total number of shark attacks. Time of attack could not be ascertained for other victims. 208 BULLETIN OF MARINE SCIENCE, VOL. 82, NO. 2, 2008

Table 6. Total number of drowning victims and those recovered with post-mortem shark bites for the 32 mo period (Jan. 1990–Aug. 1992) prior to onset of shark attack outbreak and the 32 mo period following (Sept. 1992–April 1995) the onset of shark attacks.

Total number of Drowning victims bearing % Victims bearing post- Period drowning victims post-mortem shark bites mortem shark bites Pre-onset 172 12 7.0 Post-onset 258 16 6.2 Total 430 28 7.0

The significantly higher frequency of attacks on surfers during new moon and full moon, and on bathers during new moon may be related to the higher tides occurring during these moon phases, which could facilitate the immigration of larger sharks into the nearshore areas. It is also noteworthy that during these moon phases, the high tides at Recife beaches always occur early in the morning or late in the afternoon, times of the day when the attacks were more frequent. In 2005, for in- stance, the maximum high tide during new moon occurred at ~ 0405 (ranging from 0324–0454); and 1617 (ranging from 1538–1651). During full moon, maximum high tide occurred at 0353 (0321–0409) and 1619 (1555–1651) (DHN, 2005). High tides also are the most suitable times for surfing, since the waves are much higher on these tides. In addition, surfers tend to surf in the early morning (prior to 0600–1000) and late afternoon (after 1600–1800) when lifeguards are off–duty and the surf prohibition is not enforced. Prevailing onshore winds also disrupt the swells, making them less attractive to surfers, so the early morning hours, before the wind picks up, as well as the late afternoon, after the winds drop, are usually better conditions for surfing. The distribution of shark attacks by day of the week shows an expected peak on Sundays, but also exhibits an unusually high frequency on Mondays and Tuesdays. This differs from the general worldwide trend of the highest number of attacks during weekends, when beaches are most highly utilized. This apparent anomaly might be because most of the victims were young, often unemployed surfers who may prefer to surf early in the week when the beaches are much emptier, thus “extending” the weekend. The highest numbers of attacks were recorded in July. This may be explained based on a combination of the dynamics of local human and shark populations. In Brazil there are four months of school vacation each year: July (winter), and December–February (summer). Although actual statistics are not available, the number of bathers at Recife beaches is considerably higher during the summer vacation period, peaking in Janu- ary, than during the winter vacation. The region’s rainy season is typically from May through July, which is immediately followed by the windy season which favors the for- mation of bigger waves, and thus more surfing activity. In addition, the aforementioned increase in river runoff in May–July plus the stronger winds during July–September make July–August the time of the year when the water is murkiest. The bull shark was the species implicated in most attacks (six of seven cases in which the shark species was identified). This species is particularly aggressive and has been linked to numerous attacks around the world, particularly in South Africa (Cliff and Dudley, 1992), the United States, and Australia (Burgess, ISAF data). All beaches where the attacks occurred are under the influence of the Jaboatão River discharge, which always runs northward along the Recife coast. Reduced salinity waters are favorite haunts of bull sharks, and both pregnant females bearing full term embryos and juvenile bull sharks have been caught with gillnets in the Jaboatão River HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 209

Table 7. Number of shark attacks and drowning victims bearing shark scavenges bites as related to the number of ships entering Suape Port per month.

Number of ships entering Suape Port 11–20 21–30 31–40 Number of months having numerical ship total 1 17 10 Number of attacks (mean attacks per month) 0 (0.0) 4 (0.2) 13 (1.3) Number of drowning victims with shark scavenge bites 1 (1.0) 9 (52.9) 5 (50.0) (mean scavenges per month) estuary (Hazin, unpubl. data). The lagoon region of Cananeia in southeastern Brazil hosts adult female bull sharks only during the short parturition period that extends from November to February. In the nearshore waters outside the Cananeia lagoon, subadults as well as adults of both sexes occur more frequently during the spring and summer months (Sadowsky, 1971). From December 1994 to August 1995, ten botton longline fishing cruises were made off Recife beaches H( azin et al., 2000). Sampling ranged from very close to shore to depths of about 60 m. In total 18,606 hooks were set, resulting in a catch of 196 fishes. Of the fish caught, 73 were sharks, which included three bull sharks and three tiger sharks, both potentially dangerous shark species. The evidence that submarine topography and oceanographic conditions favor the occurrence of shark attacks, that shark species known to attack humans are present in the area, and that there is intense recreational use of Recife beaches does not explain why the attacks did not occur more frequently before 1992. Why, in a stretch of about 20 km of beach where virtually no shark attacks had been recorded, suddenly, have almost 50 cases occurred over a 14-yr period? Although an observed increase in the number of Recife surfers over time likely resulted in an increased risk of shark attack, this trend in aquatic recreation certainly began almost 50 yrs ago, not just since 1992. Furthermore, although many continued to surf in the area, the number of regional surfers likely declined after the initiation of attacks as many became frightened and ceased surfing in waters off Recife beaches (Geraldo Carvalho, ASPE, pers. comm.). One possible contributor to the shark attack outbreak may have been the construction of a port facility, the Suape Port, situated to the south of Recife and the Jaboatão River estuary. Port areas are generally recognized as having a higher risk of shark attacks (Coppleson, 1958). Before port construction, four rivers, the Massangana, Tat- uoca, Ipojuca, and Merepe, converged in Suape Bay. After the port was completed, the Ipojuca and Merepe rivers had their connection to the bay interrupted by sub- stantial embankments, which resulted in periodic flooding of the surrounding agri- cultural fields. To solve this problem, the government elected to demolish part of the reef line (Neumann-Leitão and Matsumura-Tundisi, 1998). This measure alleviated the flooding resulting from the blocking of Ipojuca and Merepe Rivers, but had little effect on the accessibility for sharks, as the opening was too shallow and narrow to allow sharks to move from the sea into these two rivers. Although the Port construction began in the early 1980s, the first large influx of ships only began in 1989–1991. In the past 10 yrs, the number of incoming vessels has almost tripled. The intensifica- tion of maritime traffic may have influenced the occurrence of shark attacks, since sharks are known to follow ships (Baldridge, 1974; Schultz, 1975). Thirteen attacks occurred in the 10 mo when the monthly number of ships was > 30, while only four 210 BULLETIN OF MARINE SCIENCE, VOL. 82, NO. 2, 2008

incidents were recorded during the 18 mo when the monthly number of vessels was < 30. The number of drowning victims with shark scavenge bites, however, was not significantly different in the three ship frequency periods. The nearly identical percent- ages of drowning victims that were recovered with shark scavenge bites during the 32-mo period prior to (7.0%) and immediately after (6.2%) the shark attack outbreak likely reflect the natural abundance levels of shark species not directly linked to the human attacks. Possibly many of these scavenge bites were inflicted by normally non- attacking species such as the blacknose shark [Carcharhinus acronotus (Poey, 1860)], a common nearshore species taken in longline surveys (Hazin et al., 2000). It is also possible that the negative environmental impact caused by the construction of Suape Port resulted in the displacement of a number of bull sharks from the areas formerly available as a parturition ground and nearshore feeding area. Fol- lowing prevailing northerly currents, they may have been displaced to the nearest estuary to the north, the Jaboatão River, and adjacent lagoonal channels frequented by humans. The Port construction caused significant changes in the plankton community, leading to a strong quantitative decrease in plankton abundance (Neumann et al., 1998). A key factor contributing to these changes was a large increase in sus- pended matter, mainly in the rainy season. The disrupted link between the Ipojuca River and the sea also resulted in a decline in zooplankton abundance by inhibiting marine fishes and crustaceans from immigration into the estuary for breeding. From the above-mentioned evidence, it is reasonable to suppose that discharg- ing blood and entrails into the Jaboatão River, which flows into the stretch of beach where 47 attacks were recorded, constitutes an important potential for attracting sharks to the area, thereby contributing the aggravation of the problem of attacks. The FAO (Food and Agriculture Organization of the United Nations) manual on animal health in developing countries establishes a direct link between the attrac- tion potential of this type of waste and predators in general, indicating that when discharged into the ocean, such waste can increase the number of sharks in the area (FAO, 1991). Such a direct link between the discharge waste from a slaughterhouse, and an outbreak in shark attacks was reported on at least one previous occasion. In Mogadishu on the coast of Somalia, from 1978 to 1987, a total of 30 shark attacks, 28 of which were fatal, occurred along a small stretch of beach about 1.5 km long (Lido Beach), resulting in an average of 4.5 shark attacks per year, 36% greater than 3.3 attacks yr–1 in Metropolitan Recife from 1992 to 2006. According to Stevens (1987), the main cause of this outbreak of attacks was the beginning of a slaughterhouse operation in the area. Curiously, in a manner similar to the problem in the state of Pernambuco, a new port structure had also been constructed in the region before the outbreak of shark attacks. The species identified in the Mogadishu incidents were the bull and tiger sharks. Attacks in Mogadishu seem to be more frequent when bull sharks are abundant in the area, which occurs during the monsoon season in the southeast, when intense rains diminish salinity and temperatures in the area and increase turbidity (McPherson, 1994). Increasing river discharge to the south of the area where the attacks occurred was associated with these oceanographic conditions in a manner identical to the situation we observed in Metropolitan Recife. Sharks also tend to be abundant in areas near garbage dumps, and a nearby dump facility was identified in nearly one-quarter of the locations in which shark attacks occurred throughout the world prior to 1974 (Baldridge, 1974). As the Muribecca Waste landfill also discharges waste into the same river, it is impossible to distin- HAZIN ET AL.: BRAZILIAN SHARK ATTACKS 211 guish the role of the landfill from the slaughterhouse, but is likely that sharks are attracted or excited by the waste emanating from this landfill. If construction of the Suape Port and the pollution of the Jaboatão River estuary were indeed a primary contributing factor to the shark attack outbreak, there are two important lessons to be learned: (1) how difficult it is to anticipate the response of marine ecosystems to human interference; and (2) that the shark attack outbreak is certainly only the visible tip of a much bigger iceberg of ecosystem impact resulting from this habitat alteration, the scope of which may be never understood.

Acknowledgments

The authors are grateful to the Government of Pernambuco, which provided the necessary funds for this research, through the Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco and Secretaria de Indústria, Comércio e Turismo. We are also thankful to the Florida Program for Shark Research Internship Program, at the Florida Museum of Natural History, the two anonymous referees and M. Burgess for making helpful comments on earlier drafts of this paper, and the many students of the Fisheries Department of Universidade Fed- eral Rural de Pernambuco who helped us, especially to P. Oliveira, P. Pinheiro, A. Fischer, D. Véras, C. Wor, and M. Coxey.

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Date Submitted: 28 March, 2007. Date Accepted: 5 December, 2007.

Addresses: (F.H.V.H.) Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Bra- zil. (G.H.B.) International Shark Attack File, Florida Program for Shark Research, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611. (F.C.C.) Depart- ment of Fisheries and Aquatic Sciences/Florida Program for Shark Research, University of Florida, Gainesville, Florida 32653. Corresponding Author: (F.H.V.H.) E-mail: fhvhazin@ terra.com.br.