Journal of Experimental and 448 (2013) 228–239

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Journal of Experimental Marine Biology and Ecology

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Impact of Costa Rican longline fishery on its bycatch of sharks, stingrays, bony fish and olive ridley turtles (Lepidochelys olivacea)

Derek Dapp a, Randall Arauz b, James R. Spotila a,⁎, Michael P. O'Connor a a Department of Biodiversity, Earth and Environmental Science, Drexel University, Philadelphia, PA 19104, USA b Programa Restauración de Tortugas Marinas (Pretoma), 1203-1100, Tibás, San José, article info abstract

Article history: We used data collected by an observer program to assess the impact of the Costa Rican longline fishery on Received 4 January 2013 numbers, capture locations, seasonality and body sizes of silky sharks (Carcharhinus falciformis), pelagic thresher Received in revised form 22 July 2013 sharks (Alopias pelagicus), olive ridley turtles (Lepidochelys olivacea) and other bycatch in the Central Accepted 24 July 2013 American Pacific. The longline fishery caught a large number of mahi-mahi (Coryphaena sp.) and silky sharks, Available online xxxx but also caught a large number of olive ridley turtles and pelagic stingrays (Pteroplatytrygon violacea). We esti- mated that longline fisheries caught 699,600 olive ridleys, including 92,300 adult females, from 1999 to 2010. Keywords: Geospatial analysis These captures were associated with a decline of nesting populations at nearby arribada beaches. There were sta- Longline fishery tistically significant size decreases from 1999 to 2010 in mature olive ridley turtles and from 2003 to 2010 in silky Marine conservation sharks. Average fork length of silky sharks in 2010 was 97.3 cm, which was far below observed fork length at Marine protected areas maturity, 144 cm. Pelagic thresher sharks were small and fluctuated in size over the study period. Capture of Observer program large numbers of juvenile blacktip sharks (Carcharhinus limbatus) indicated a nursery area near the Osa Peninsula. Populations Geospatial analysis indicated shifts in mahi-mahi abundance on a temporal scale but fishing efforts did not shift with the shift in mahi-mahi abundance. Yellowfintuna(Thunnus albacares), Indo-Pacific blue marlin (Makaira mazara) and Indo-Pacificsailfish (Istiophorus platypterus) catches varied seasonally and were most abundant out to sea and south of . Marine protected areas and/or time area closures are needed to reduce the impact of the Costa Rican longline fishery on sea turtles and sharks. © 2013 Elsevier B.V. All rights reserved.

1. Introduction boats reported over 55,000 turtles captured by longlines around the world. Therefore, bycatch may be a major problem for survival of sea Within the past few decades, there has been increasing interest turtle populations (Wallace et al., 2010). For olive ridley (Lepidochelys in the effects of longline fisheries on marine species (Lewison and olivacea), loggerhead (Caretta caretta) and leatherback (Dermochelys Crowder, 2007; Myers et al., 2007). In particular, species of sea turtles coriacea) turtles, mortality on fishing lines is highly variable, but is typ- and sharks display an intrinsic sensitivity to mortality from longline ically low (Koch et al., 2006; Lewison and Crowder, 2007). However, fisheries because they exhibit life history traits such as high adult survi- poor handling practices, retention of turtles for consumption and injury vorship, low fecundity and late age of maturity (Cope, 2006; Gilman caused after capture may contribute to increased mortality (Koch et al., et al., 2008; Lewison and Crowder, 2007) that limit their response to 2006; Watson et al., 2005). Overall, post-hooking mortality of sea turtles high rates of adult mortality. ranges from 4% to 27% in longline fisheries (Camiñas, 2004; Lewison and bycatch is a primary driver of population declines in elas- Crowder, 2007). In the olive ridley turtle, mortality caused by longlining mobranchs and sea turtles (Wallace et al., 2010). Shortfinmakosharks is typically low in Costa Rican longline fisheries and olive ridleys are (Isurus oxyrinchus) suffer high fishing mortality throughout their usually released alive, with minimal short-term post-capture mortality range (Dulvy et al., 2008)andfishing routinely depletes marine fish (Swimmer et al., 2006; Whoriskey et al., 2011). populations by 50 to 70% (Baum et al., 2003), with losses exceeding However, populations of olive ridleys at the two main nesting 90% becoming more common (Myers and Worm, 2005). From 1990 to beaches in Costa Rica have declined since the 1980s. Olive ridleys nest 2008 bycatch of sea turtles per unit effort was particularly high for long- in mass synchronous nesting aggregations, or arribadas, and two of lines in the Northwest Atlantic, Mediterranean, Southwest Atlantic and the six major arribada beaches in the world are in Costa Rica. The pop- Eastern Pacific and for gillnets in the Eastern Indian and trawls in ulation at Nancite beach declined precipitously in the 1980s and has the Eastern Pacific and Mediterranean. Observers on board b1%–5% of not recovered (Fonseca et al., 2009; Honarvar et al., 2008, 2011). The population at Ostional is very large (about 500,000) but also has ⁎ Corresponding author. Tel.: +1 6094405158; fax: +1 2158951273. declined in recent years (Valverde et al., 2012). Several arribada popula- E-mail address: [email protected] (J.R. Spotila). tions in have essentially disappeared (Koch et al., 2006;

0022-0981/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jembe.2013.07.014 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 229

Marquez et al., 1996). Although Plotkin et al. (2012) report that popula- sharks (Carcharhinus limbatus), a species considered to be globally tions are recovering in Mexico and that similar trends are occurring in near threatened. Costa Rica, the most recent and complete data (Valverde et al., 2012) demonstrate that the olive ridley population at Ostional has actually de- 2. Methods creased and the population at Nancite is still very low (Fonseca et al., 2009). Despite the seemingly low rates of mortality caused by longlines 2.1. Observer program in the Costa Rican fishery, it is essential to monitor the potential impacts fi of the shery on olive ridleys because even slight decreases in adult The program began in 1999 and longline monitoring was continuous survivorship have substantial impacts on sea turtle populations (Koch until 2010, with the exception of 2001, when no observations were fi et al., 2006; Wallace et al., 2010)and sheries in areas that have large conducted. Efforts of the program varied between years, with a mini- numbers of mature olive ridleys could be extremely detrimental to mum of 15 longlines observed in 2000 and maximum of 88 longlines turtle populations. observed in 2008. Observer effort also varied by month. Most observa- While considerable effort has been made to reduce sea turtle tions took place in May, which had 14.3% of the total observed lines. bycatch on longlines, comparatively few efforts have been made to Observations were conducted onboard six medium scale (10–15 ton eliminate shark bycatch on longlines (Gilman et al., 2008; Swimmer capacity with iced holds) vessels out of a Costa Rican fleet of 350 vessels. et al., 2011). Shark and sea turtle bycatch varies greatly depending Boats were owned by Papagayo Seafood S.A. vessels and sailed from upon spatial location and methods utilized (Gilman et al., 2006, 2008). Playa del Coco. fi Mahi-mahi (Coryphaena hippurus and Coryphaena equiselis) sheries Observers were trained to identify and record species, sex, reproduc- fi in the Central American Eastern Paci c may be particularly prone to tive state and dimensions of all captured onboard longline fish- catching sea turtles and sharks due to their shallow set depth, which ing trips. Prior to 2003 silky sharks and blacktip sharks were recorded as typically has a higher catch rate of sharks and sea turtles (Lewison and Carcharhinus spp. so we could not analyze individual species, and sizes of Crowder, 2007; Whiting et al., 2007a; Whoriskey et al., 2011). Unlike fish were not recorded. Observers also recorded information pertaining sea turtles, shark bycatch on longlines in Costa Rica typically results in to individual longlines, such as location, set and haul back times, hook fi mortality, because shermen retain sharks, removing and selling their type, hook number, bait used, target species and total number of hooks. fi ns for export and selling their meat for domestic consumption All hooks used were circle hooks (#14, 15, 16) with and without 10° (Arauz, pers. obs.). Capture stress can cause high rates of immediate or offset (Swimmer et al., 2011). Set specific data on bait used were incom- delayed mortality in sharks (Frick et al., 2010). Shark populations are plete. Observers remained on fishing vessels throughout a voyage and fi very sensitive to over shing as indicated by substantial decreases in recorded all data from each line set. Trips typically lasted about two fi many shark populations worldwide following heavy shing pressure weeks and vessels set approximately 18-mile longlines with wire leaders (Baum et al., 2003; Clarke et al., 2006; Heithaus et al., 2008; Myers and 650 hooks per set. et al., 2007; Robbins et al., 2006). In Costa Rica, silky shark, Carcharhinus falciformis, and pelagic thresher shark, Alopias pelagicus, populations are fi declining (Whoriskey et al., 2011). 2.2. Examining shing effort and catch rates Sharks regulate marine communities and provide stability to each ecosystem they inhabit, both through direct (Bascompte Using the total number of hooks on the longline, and number of et al., 2005; Myers et al., 2007) and by altering the habits of various spe- individuals caught of each species we calculated the rate of catch per cies in their presence (Heithaus and Dill, 2006; Heithaus et al., 2007, 1000 hooks set. We used ArcGIS to plot locations of each longline onto 2008; Preisser et al., 2005). Decline or absence of sharks in many areas a base map with the corresponding catch data of the main targeted has caused substantial problems in ecosystems because mesopredators species and bycatch species, mahi-mahi, olive ridley turtles, silky fi fi increase following a decrease in localized shark abundances, which can sharks, pelagic stingrays (Pteroplatytrygon violacea), Indo-Paci c sail sh fi have a cascading effect, reducing populations of species that inhabit (Istiophorus platypterus), yellow ntuna(Thunnus albacares), pelagic fi lower trophic levels (Agardy, 2000; Baum and Worm, 2009; Myers thresher sharks, Indo-Paci cbluemarlin(Makaira mazara), skipjack et al., 2007). However, fisheries-induced trophic cascades are not uni- tuna (Katsuwonus lepamis), striped marlin (Retrapturus audux)and versal in the world's . Jensen et al. (2012) review the concept of blacktip sharks (C. limbatus). Rasters were created with a size of marine fisheries as ecological experiments and point out that while 50 km by 50 km and, if multiple longlines were in a single raster, values fishery-induced trophic cascades are reported for several ocean food of catch rates were averaged together. webs, other studies report that there is little effect of fishing on non- target species, especially on coral reefs. The complexity of top–down 2.3. Estimation of size changes effectsisseenina15yearstudyoftigersharks(Galeocerdo cuvier)in Australia in which the sharks have widespread risk effects on both The curved carapace length of olive ridley turtles was measured large-bodied herbivores and mesopredators that may affect community from 1999 to 2010. Because the location of the most intense longline dynamics (Heithaus et al., 2012). Large sharks are top predators fishing was near arribada beaches, we analyzed the sizes of mature (Ferretti et al., 2010), but under severe exploitation the average body olive ridleys to determine if they changed through time. To date, there size of shark species declines, diminishing their effectiveness as top has only been one study that has noted the size of olive ridleys at predators (Baum and Myers, 2004; Hilborn and Walters, 1992; Myers maturity (IUCN, 2012; Zug et al., 2006) and it used the straight carapace et al., 2007). length. Conversions for straight carapace length to curved carapace Data from observers indicated that there were increases in catch length are available for other sea turtle species (Byrd et al., 2005), but rates of olive ridley turtles and decreases in catch rates of mahi-mahi are not currently available for olive ridleys. The curved carapace length and silky sharks from 1999 to 2008 in the Costa Rican mahi-mahi of nesting female olive ridleys ranges between 65 and 75.2 cm (Whiting longline fishery (Whoriskey et al., 2011). We analyzed a larger data et al., 2007b). For this study, we used 65 cm as the minimum curved set from the Costa Rican longline fishery to determine the spatiotempo- carapace length of maturity for both male and female olive ridleys. ral relationships of that fishery for mahi-mahi, other targeted fish and We analyzed changes in fork length of silky sharks (n = 2556) from three bycatch species of global conservation concern, the olive ridley 2003 to 2010. We excluded 2005 from the analysis for silky sharks, since turtle, silky shark and pelagic thresher shark. We also examined the only five specimens were caught during that year. We analyzed data on effects of the fishery on the body sizes of those three species from pelagic thresher sharks (n = 285) from 1999 to 2010. We analyzed 1999 to 2010. Finally, we identified a nursery ground for blacktip changes in size between for all three species with a One Way ANOVA 230 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 231 and Tukey's post hoc tests. All analyses were conducted by using the R in October, December and January. From April to September there were software package (R Development Core Team, 2012). 194 longline sets with 133,136 hooks and fishing effort was greatest off shore (Fig. 2E). From October to February there were 232 longlines sets 3. Results with 158,835 hooks and fishing effort was greatest near the Guanacaste and off the Osa Peninsula of Costa Rica (Fig. 2F). From April to 3.1. Fishing effort and catch rates September catch rates of mahi-mahi were lower near the coast and highest far off shore, where fishing effort was lowest (Fig. 2G). From Observer data only encompassed a small proportion of the effort of October to February catch rates of mahi-mahi were highest near the the Costa Rican longline fishery with a total of 483 longlines and over coast of Guanacaste (Fig. 2H). Silky shark catch was highest in October 320,000 hooks observed. The average number of hooks set per line and November while thresher shark catch rate was highest from April (for 471 lines with hook data) was 688 ± 184 (SD). We examined to September. Indo-Pacific sailfish catch was highest in August and spatial–temporal data on 466 lines with 320,426 hooks for which September, Indo-Pacific blue marlin catch was highest in June and there were good GPS data. Longline sets were concentrated near the July, and striped marlin catch was highest in October and November. northwestern coast of Costa Rica, with many of the sets located in Yellowfin tuna catch was highest in August and September. close proximity to arribada nesting beaches (Fig. 1A). The most frequent target catch was mahi-mahi, which was the sole target of 51% of 3.3. Changes in size the longlines set and a targeted catch in at least 70% of the observed sets (Table 1). Other species that were targeted were tuna, marlins There was a small, statistically significant decrease in size of mature and sharks. In the data set, the target catch was not recorded for 27 olive ridleys from 1999 to 2010 (F = 6.983, df = 10, 741, p b 0.0001) longlines. There were 62 types of fish caught, along with three species (Fig. 3A). Olive ridleys caught in 1999 were significantly larger than of sea turtles and some unidentified dolphin (mammal) species olive ridleys caught from 2005 to 2008 and in 2010 (Tukey test (Table 2). Mahi-mahi was the most common species caught (10,142 p b 0.05). The change in size observed during the period went from a or 31.34/1000 hooks), but olive ridley turtle was the second most com- mean curved carapace length of 68.5 cm in 1999 to 66.6 cm in 2010. mon species caught (2864 or 8.85/1000 hooks), of which 739 were The smallest mature silky sharks had a total length of 171 to 176 cm, adults (377 female, 362 male). The next most common fishes caught which corresponded to a fork length of 144 to 148 cm. Of the 2562 silky were silky sharks (2613 or 8.08/1000), pelagic stingrays (1416 or sharks examined, only 375 silky sharks had a fork length greater than 4.38/1000), Indo-Pacificsailfish (669 or 2.07/1000), unidentified rays 144 cm. There were statistically significant decreases in size of silky (566 or 1.75/1000) and yellowfin tuna (522 or 1.61/1000). There were sharks (F = 9.684, df = 7, 2554, p b 0.0001) (Fig. 3B). In both 2004 more green turtles (Chelonia mydas) (96) caught than most species of and 2007, fork lengths were significantly longer than in 2008, 2009 fish. The catch rate of sharks was low in areas near the arribada beaches and 2010 (Tukey test, p b 0.05). The longest mean observed fork length where catch rates of mahi-mahi and olive ridleys were high. occurred in 2007 (mean = 110.2 cm). Fork length decreased to a mean The primary mahi-mahi species caught was C. hippurus but catches of 97.3 cm in 2010. of C. equiselis were also recorded (Table 2). Most mahi-mahi were Female pelagic thresher sharks matured at a fork length of approxi- caught off of Guanacaste province (Fig. 1B). Olive ridleys were caught mately 140 cm and total length of approximately 230 cm. There was off the nesting beaches and out to sea (Fig. 1C and D). Indo-Pacificsail- asignificant difference in the size of this species between years fish (Fig. 1E) were caught south of the Osa Peninsula, off Guanacaste, (F = 10.1, df = 7, 277, p b 0.0001). Pelagic thresher sharks fluctuated south of Panama and farther out to sea and yellowfintuna(Fig. 1F) in size between years (Fig. 3C) but there was no clear trend. This may were caught primarily out to sea. Marlin catches were highly variable have been due to small sample sizes. The smallest pelagic thresher in time and space, with Indo-pacific blue marlin (171) the most com- sharks were caught in 2004 (mean fork length = 132 cm) and 2009 mon species with a hotspot south of Panama (Fig. 1G), followed by (mean fork length = 133 cm) and were significantly shorter than striped marlin (152) that were caught out to sea (Fig. 1I) and black mar- those caught in 2003, 2007, 2008 and 2010 (Tukey test, p b 0.05). The lin, Makaira indica (53), for which no pattern was apparent. Skipjack largest mean fork length was in 2010 (159 cm). Overall mean fork tuna (167) were caught near nesting beaches and out to sea off Panama length was 146.4 cm. There were insufficient data to assess changes in (Fig. 1H). sizes of other fish species. Fishermen caught 25 species of elasmobranchs (sharks and rays), of which the most common species was the silky shark, followed by 4. Discussion the pelagic stingray, other unidentified rays (566), requiem sharks, Carcharhinus sp. (307), pelagic thresher sharks (304) and blacktip The Costa Rican longline fishery caught a large number of mahi- sharks (131) (Table 2). Catches of silky sharks increased with distance mahi and silky sharks, as well as a large number of olive ridley turtles from shore and were most common off Panama (Fig. 2A). Catches of and pelagic stingrays. The olive ridley turtle was the second most abun- pelagic thresher shark were highly spatially variable (Fig. 2B). From dant species captured. The catch rates in this study were similar to those 2003 to 2010, catches of blacktip sharks (n = 128) were almost all con- reported by Whoriskey et al. (2011),whoexaminedasubsetofthedata fined to a single area off the Osa Peninsula of Costa Rica (Fig. 2C). Pelagic base used in our study. It was not surprising that they reported a higher stingrays were caught out to sea (Fig. 2D). catch rate for mahi-mahi because they only examined data for longlines targeting mahi-mahi. Their catch rate per 1000 hooks for olive ridley 3.2. Seasonality and catch rates turtles (9.05), pelagic stingrays (4.77), Indo-Pacificsailfish (2.52), pelagic thresher sharks (1.12) and green turtles (0.35) was similar to Seasonality affected catch rates of mahi-mahi, olive ridley turtles, those in this study. Catch rates for other species varied in that study as silky sharks, thresher sharks, Indo-Pacific sailfish, yellowfintuna,Indo- they did here. Swimmer et al. (2011) reported higher catch rates of Pacific blue marlin and striped marlin. There were insufficient data to sea turtles (14.03 for olive ridleys and 0.54 for green turtles) in a examine seasonality for the other species. Mahi-mahi catches were small-scale study of circle hooks (54 lines) in the Costa Rican longline highest from October to February and olive ridley catches were highest fishery. The rate of bycatch for turtles is higher in the Costa Rican

Fig. 1. (A) Observed longline fishing effort based upon the number of hooks set per 50 km by 50 km raster. Catch per 1000 hooks of: (B) mahi-mahi, (C) mature male olive ridley turtles, (D) mature female olive ridley turtles, (E) Indo-PacificSailfish, (F) yellowfin tuna, (G) blue marlin, (H) skipjack tuna, and (I) striped marlin. Blue circles with turtles represent, going from north to south, Playa Chacocente, Playa La Flor, Playa Nancite, and Playa Ostional, which are four major olive ridley arribada nesting beaches. 232 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 longline fishery than in other longline fisheries for which data are avail- Fishermen in small artisanal fishing boats typically catch both olive rid- able. Sea turtle bycatch in 19 different countries is typically less than 2 ley and green turtles (Blanco et al., 2012). Assuming that small artisanal per 1000 hooks (Lewison and Crowder, 2007), for instance 0.098 in vessels caught an average of only 10 turtles each per year, a minimum India (Varghese et al., 2010) and 0.38 in the Gulf of Guinea off West Af- estimate based on the observations of Blanco et al. (2012), then they rica (Carranza et al., 2006). Worldwide it ranges from 0.004 to 0.59 per captured about 290,500 olive ridleys. Based on our observer data, of (Wallace et al., 2010). these 699,600 turtles, 25.8% were adults and 13.2% were mature fe- males. Therefore, we estimate that the Costa Rican longline fishery caught at least 92,300 adult female olive ridley turtles during the 4.1. Olive ridley turtles study period. While a large number of olive ridleys were caught in this fishery it is We estimated the impact of the Costa Rica longline fleet on olive rid- not easy to project the impact of those captures on the turtle population. ley turtles based on data on numbers of vessels, capture rates from this Sea turtles that are lightly hooked apparently survive and behave study and observations of the small scale artisanal fishery by Blanco normally for at least a few weeks (Swimmer et al., 2006), although et al. (2012). The six vessels on which observers were present repre- long term survival is unknown and survival of turtles injured more seri- sented a small portion (1.7%) of the 350 medium scale longline vessels ously or captured on boats without observers is difficult to project. We in the Costa Rican fishery. There were also 316 advanced longline do know that the population of olive ridleys nesting on Nancite beach vessels and 22 large-scale industrial size vessels in the fleet. There declined precipitously in the 1980s and has not recovered. This decrease were 2421 small artisanal vessels (pangas) that fished within a few is due in part to a lowering of hatching success brought about by a vari- km of shore (Arauz, 1999; Mug Villanueva, 2002; INCOPESCA, Costa ety of biotic and abiotic factors (Fonseca et al., 2009; Honarvar et al., Rican fisheries agency, records). Therefore, if we assume that medium 2008, 2011). At Ostional the operation of an harvest system is scale longline fishing boats from Costa Rica caught olive ridleys at the thought to reduce the impact of density dependent effects on hatching same rate as our six vessels with observers, then they caught 167,100 success. While the population at Ostional is very large (500,000) it olive ridley turtles from 1999 to 2010. If we assume that advanced also has declined in recent years (Valverde et al., 2012). The large num- and large scale longline vessels caught 1 1/2 times as many turtles per ber of olive ridleys caught on longlines is associated with the declines in boat as the medium scale vessels (probably an underestimate given numbers of nesting turtles at those beaches. Much of the longline fish- numbers of hooks set per longline, numbers of longlines per trip and ing effort is near the nesting beaches (Fig. 1A) and many turtles are length of trips) then they caught at least another 242,000 olive ridleys. caught near those beaches as well as out to sea. The near shore artisanal fishery is active near and off the nesting beaches and may have a larger fi Table 1 impact than we estimated above. The industrial longline shery of other Characteristics of Costa Rican longline fishery as recorded by observers on medium sized countries may also have a large impact. Thus, applying the precaution- vessels from 1999 to 2010. ary principle, the impact of the Costa Rican longline fishing on olive ridley turtles should be greatly reduced. Given the large number of im- Year Number of lines set Year percentage of total mature turtles captured we may find that the population will suffer a 1999 62 12.8 greater decline in the next few years due to a reduction in recruitment 2000 15 3.1 2002 17 3.5 of adults. 2003 85 17.6 Olive ridleys are known to forage along major oceanic currents 2004 42 8.7 (Polovina et al., 2004). Leatherback turtles in Costa Rica are known to 2005 24 5 travel along the Pacific coast of Central America, following currents, 2006 29 6 2007 69 14.2 into the equatorial region (Shillinger et al., 2008, 2010). The equatorial 2008 88 18.2 counter current runs along the western coast of Central America, creat- 2009 28 5.8 ing a biological hotspot of increased productivity in the Pacific Ocean off 2010 24 5 Costa Rica (Palacios et al., 2006) and may be a prime location for forag- ing olive ridley turtles. Longlines are catching olive ridley turtles near Month Number of lines set Month percentage of total the arribada beaches and out to sea in the area of the Costa Rican January 63 13 Dome (Shillinger et al., 2008, 2012) and along convergent zones. Efforts February 45 9.3 March 51 10.6 to reduce turtle bycatch should be focused in those areas. April 61 12.6 There were small decreases in body size of adult olive ridley turtles May 69 14.3 caught in the longline fishery (Fig. 3A). That decrease could be due to in- June 34 7 creased recruitment of young individuals to the population, as occurred July 3 0.6 in Mexico (Koch et al., 2006). In green turtles, there is an inverse corre- August 8 1.7 September 20 4.1 lation between growth rates and population density (Bjorndal et al., October 33 6.9 2000). However, another plausible explanation for the decrease in size November 38 7.9 is a lack of resources. Once sea turtles mature, their growth rates slow December 58 12 down substantially and their body size remains fairly stable. When

Target species Number of lines set Target percent total resources are limited turtles mature at a smaller size and generally stay small as adults (Price et al., 2004; Reina et al., 2009). In the Eastern Mahi-mahi 247 51.1 Pacific Ocean, El Niño events are associated with a period of reduced Shark 90 18.6 Mahi-mahi, shark 41 8.5 primary productivity when compared with La Niña events. Reduced pri- No data 27 5.6 mary productivity leads to longer interesting intervals in leatherback Tuna 19 3.9 turtles (Reina et al., 2009; Saba et al., 2007) and smaller leatherback tur- Mahi-mahi, tuna, marlin 17 3.5 tles in the Pacific as compared to the (Saba et al., 2008; Mahi-mahi, tuna, marlin, shark 17 3.5 Mahi-mahi, marlin, shark 10 2.1 Wallace et al., 2006a, 2006b). Lack of nutrients contributes to decreases Tuna, marlin 9 1.9 in body sizes and growth rates of other sea turtle populations as well Mahi-mahi, tuna 3 0.6 (Bjorndal, 1985; Tiwari and Bjorndal, 2000). Therefore, increased El Mahi-mahi, marlin 2 0.4 Niño events in recent years probably resulted in a reduced resource Mahi-mahi, tuna, shark 1 0.2 base for olive ridleys and thus a decrease in adult body size. D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 233

Table 2 The total catch for each species of fish and bycatch recorded by observers on Costa Rican longline vessels from 1999 to 2010. In the final two rows, mean catch rate per 1000 hooks and the 2012 IUCN Red List global status are shown (LC = least concern, DD = data deficient, NT = near threatened, VU = vulnerable, EN = endangered, CR = critically endangered).

Total hooks set: 323,578 Total lines examined: 483 Total caught Catch rate IUCN status

Average hooks per line: 688 ± 184

Species name Common name

Coryphaena sp. Mahi-mahi 10,142 31.34 LC Lepidochelys olivacea Olive ridley turtle 2864 8.85 VU Carcharhinus falciformis Silky shark 2613 8.08 NT Pteroplatytrygon violacea Pelagic stingray 1416 4.38 LC Istiophorus platypterus Indo-Pacific sailfish 669 2.07 LC Unid. ray speciesa Unid. ray species 566 1.75 – Thunnus albacares Yellowfin tuna 522 1.61 NT Carcharhinus sp. Unid. requiem shark species 307 0.949 – Alopias pelagicus Pelagic thresher shark 304 0.939 VU Makaira mazara Indo-Pacific blue marlin 171 0.528 – Katsuwonus pelamis Skipjack tuna 167 0.516 LC Tetrapturus audax Striped marlin 152 0.470 – Carcharhinus limbatus Blacktip shark 131 0.405 NT Chelonia mydas Green turtle 96 0.297 EN Euthynnus lineatus Black skipjack tuna 95 0.294 LC Sphyrna lewini Scalloped hammerhead 83 0.256 EN Thunnus orientalis Pacific bluefintuna 70 0.216 LC Acanthocybium solandri Wahoo 63 0.195 LC Mustelus henleib Brown smooth-hound 60 0.185 LC Prionace glauca Blue shark 56 0.173 NT Makaira indica Black marlin 53 0.164 – Rhizoprionodon longuriob Pacific sharpnose shark 47 0.145 DD Bagre sp.b Unid. sea catfish species 45 0.139 – Dasiatys longa Longtail stingray 35 0.108 – Pseudocarcharias kamoharai Crocodile shark 31 0.096 NT Alopias vulpinus Common thresher shark 23 0.071 VU Xiphias gladius Swordfish 23 0.071 LC Nasolamia velox Whitenose shark 20 0.062 DD Manta sp. Unid. manta species 18 0.056 – Dasyatis brevis Whiptail stingray 17 0.052 – Sphyrna zygaena Smooth Hammerhead 17 0.052 VU Makaira sp. Unid. marlin species 15 0.046 – Ginglymostoma cirratumb Nurse shark 14 0.043 DD Mola mola Ocean sunfish 13 0.040 – Lutjanus guttatusb Spotted rose snapper 12 0.037 LC Aetobatus narinarib Spotted eagle ray 11 0.034 NT Carcharhinus longimanus Oceanic whitetip shark 10 0.031 VU Gempylus serpens Snake mackerel 8 0.025 – Mobula thurstoni Bentfin devil ray 7 0.022 NT Unid. dolphin sp. Unid. dolphin species 7 0.022 – Lutjanus argentiventrisb Yellow snapper 7 0.022 LC Lutjanus coloradob Colorado snapper 7 0.022 LC conicepsb Red pike-conger 5 0.015 DD Mustelus lunulatusb Sicklefin smooth-hound 4 0.012 LC Unid. thresher shark sp. Unid. thresher shark species 3 0.009 – Sarda orientalis Striped bonito 3 0.009 LC Lutjanus novemfasciatusb Pacific dog snapper 3 0.009 LC Thunnus obesus Bigeye tuna 3 0.009 VU Sphyraena ensis Mexican barracuda 2 0.006 LC Murenidae sp.b Unid. moray species 2 0.006 – Galeocerdo cuvier Tiger shark 2 0.006 NT Sphyrna coronab Scalloped bonnethead shark 2 0.006 NT Echiophis brunneusb Pacific spoon-nose eel 2 0.006 LC sexfasciatusb Bigeye trevally 2 0.006 LC Caranx caninusb Pacific 2 0.006 LC Carcharhinus leucas Bull shark 1 0.003 NT Mobula tarapacana Spiny mobula 1 0.003 DD Mobula japanica Spinetail mobula 1 0.003 NT Haemulidae sp.b Unid. grunt species 1 0.003 – Diodontidae sp. Unid. porcupinefish species 1 0.003 – Trachinotus kennedyib Blackbotch pompano 1 0.003 LC Anguilla sp.b Unid. eel species 1 0.003 – Ariidae sp.b Unid. catfish species 1 0.003 – sp. Unid. jack or pompano species 1 0.003 – Sphyrna tiburob Bonnethead shark 1 0.003 LC Dermochelys coriacea Leatherback sea turtle 1 0.003 CR

a Accurate recording of ray species did not occur until 2003 and most ray species were listed as unidentified (unid.) b Thesecoastalspecieswerecaughtonafishing trip that lasted for 8 sets which was closer in proximity to the shore than earlier and subsequent sets. 234 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239

Fig. 2. Catch per 1000 hooks on longlines of (A) silky sharks, (B) pelagic thresher sharks, (C) blacktip sharks, and (D) pelagic stingrays. Hooks set per 50 km by 50 km raster in (E) April through September and (F) October through February. Mahi-mahi caught per 1000 hooks in (G) April through September and (H) October through February.

Observed sex ratio of adult olive ridleys in our study was 1:1 4.2. Bony fishes (n = 752). Hatchling olive ridleys in the northeastern Pacifichavea skewed sex ratio of 55% females (Hernández-Echeagaray et al., 2012; Sailfish, tuna and marlin were the most common bony fishes caught Sandoval -Espinoza, 2011). Therefore, there must be a small differential in the Costa Rican longline fisheries after mahi-mahi. Most of those fish survival of male and female juveniles in the population. Curved cara- were caught out to sea away from turtle nesting beaches. Although pace length of adult male olive ridleys, mean = 67.7 cm (n = 373), sailfish and marlin are considered bycatch by longline fishermen, they was nearly identical to that of adult female olive ridleys, mean = are retained for local consumption and export and are highly prized 67.6 cm (n = 379). This differs from previous studies that noted that by sports fishermen, who generally release them after capture (personal adult females are typically larger than adult males (National Marine observation). Catch rates were highest during the rainy season and loca- Fisheries Service, 1998, 2003). tion of capture probably related to movements of off shore currents and D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 235

Fig. 3. (A) Observed curved carapace lengths of mature olive ridley turtles from 1999 to 2010. Observed fork lengths of: (B) silky sharks from 2003 to 2010 and (C) pelagic thresher sharks from 1999 to 2010. The cross symbol represents the mean size for each year. The box plots display the median as a thick black line, extreme lower whisker, lower hinge (median of the lower half of the numbers), upper hinge (median of the larger half of the numbers) and extreme upper whisker. The extreme upper and lower whiskers are defined as the most extreme data points within 1.5* the interquartile range of the first and third quartiles. Circles represent outliers in the data. shifting of location and size of the Costa Rican Dome (Palacios and per obs). Hotspots for silky sharks and thresher sharks were out at Bograd, 2005; Shillinger et al., 2008, 2012). sea, except for an area at the tip of the Nicoya Peninsula where thresher sharks were abundant (Fig. 2A and B). High catch rates of blacktip 4.3. Sharks and rays sharks near the Osa Peninsula (Fig. 2C) indicated that that area was a nursery ground since most sharks were juveniles. Juvenile blacktip Large numbers of sharks and rays were caught in the longline fisher- sharks utilize near shore and bay nursery areas during the spring and y. Pelagic stingrays were caught out to sea. Rays were discarded but summer months (Baremore et al., 2012). In our study, almost all sharks were retained for their fins, meat or as bait. Fins were removed blacktip sharks were caught in April to June, except for four caught in from sharks on board ship, sometimes while they were still alive October. Mean fork length of blacktip sharks caught in the study was (personal observation), for which fishermen were paid $10/kg for 62 cm. Although different populations of blacktip shark mature at dif- small fins (Whoriskey et al., 2011)and$70/kgforlargefins (Arauz, ferent sizes, 62 cm is considerably less than the reported size of 236 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 maturity for blacktip sharks, which ranges between 117.6 and 126.6 cm depleted fish stocks. While the Costa Rican fishery still catches large for females and 103.4 and 116.7 cm for males (Carlson et al., 2006). Ju- numbers of mahi-mahi, the small size of adult sharks and large numbers venile sharks may use the Gulf of Dulce and the area near the Osa Pen- of juveniles captured suggest that development of a sustainable fishery insula as an important nursery habitat. will require both immediate steps to reduce the impact of the fishery Decreases in fork length in silky sharks (Fig. 3 B) indicated a reduc- and long term scientific studies and stock assessments of the fish popu- tion in relative numbers of adults in the population. Although decreases lations to more accurately determine the best strategies to restore and in silky shark size were small, average fork length in 2010 was only maintain them (Branch et al., 2011). 97.3 cm. There was a 91.2% decrease in silky shark abundance in the Historical overfishing has caused more disturbance to coastal eco- Gulf of Mexico from the 1950s to 1990s (Baum and Myers, 2004). Aver- systems than any other source of human degradation (Jackson et al., age body size of silky sharks plummeted from 102.3 kg to 16.7 kg. 2001). Historical abundance of large consumer species was so large Converted from mass to fork lengths, average fork length for silky sharks that humans can scarcely imagine it in the 21st century (Nadon et al., in the Gulf of Mexico was around 97 cm in the 1990s, nearly exactly the 2012). Books such as “Sea of Slaughter” (Mowat, 1996), which details size we found for Costa Rica in 2010. Silky sharks along Baja Mexico the loss of life in the North Atlantic, and “Fisheries of Raritan mature at a total length of 180 cm (Sánchez-de Ita et al., 2010). Lengths Bay” (MacKenzie, 1992), which describes the incredible abundance of at maturity were similar to those in our study. There is a large propor- shell fish and finfish when Europeans first settled in New Jersey, then tion of juvenile silky sharks in the northeastern Pacific above 5° latitude a British colony, provide a vivid picture of the abundance of marine compared to adults, which could indicate a spawning or parturition animals before exploitation by modern humans. Place names such as ground (Watson et al., 2009). However, the reduction in sizes of silky Pearl River and turtle cove remain ghosts of populations long since sharks over time in this study and the small sizes of sharks also indicated lost. Time lags of decades to centuries took place between the onset of that adults were becoming less abundant in the population. overfishing and the collapse of marine ecosystems (Jackson et al., Mean fork length of pelagic thresher sharks in this study was small 2001). Therefore, the implications of current overfishing by the Costa and fluctuated between years with no clear trend (Fig. 3C). Mean fork Rican longline fleets may not be clear for many years to come. Will length was only slightly longer (146.2 cm) than the length at maturity there be a trophic cascade, in which removal of a top predator has (140 cm). There were only a few large sharks in the population. Female effects far down a food web (Borer et al., 2005), due to the decline of sharks matured at a smaller total length (230 cm) than the size at shark populations? Will mahi-mahi populations remain abundant or maturity in the northwestern Pacific, total length of 267–276 cm for will they decline, and will a decline affect species lower down the males and 282–292 for females (Liu et al., 1999). Fishing pressure on food web? Are those populations controlled by fishing or by productiv- adults may be selecting for maturation at a smaller size in thresher ity regime changes in the area of the Costa Rican Dome as described for sharks in the Costa Rican fishery. Few studies have been conducted other populations (Vert-pre et al., 2013)? Historically, catches of fish examining the ecology of pelagic thresher sharks (IUCN, 2012). In the have remained high in populations that then suddenly declined over a Northwest Pacific, pelagic thresher shark stocks are likely overexploited few years. Patterns of vulnerability to population collapse are very dif- (Liu et al., 2006). In contrast, in the Northwest Atlantic populations of all ferent in the ocean than on land, such that both small and large fishes thresher sharks species combined have begun to stabilize (Baum and arevulnerabletocollapse(Pinsky et al., 2011). Thus, our data suggest Blanchard, 2010). This population is likely largely comprised of com- that the populations of fish affected by the Costa Rican longline fishery mon thresher sharks, which are considerably more resilient to fishing may be in danger of collapse and that there are insufficient scientific pressures than pelagic thresher sharks (IUCN, 2012). It is difficult to dis- data to predict whether and when such a collapse will occur, and in cern the magnitude of impact fisheries have had on pelagic thresher which species. sharks in the Northeast Pacific. With fishing pressure increasing in the Northeast Pacific and few assessments having been made on pelagic 4.5. Management recommendations thresher sharks, it is imperative that further studies be done to deter- mine the level of exploitation that is occurring. Area and seasonal closures would be effective in reducing the by- Although many studies demonstrate a decreasing body size in shark catch of olive ridley turtles. Establishment and effective enforcement species in response to fishing pressures (Baum and Myers, 2004; of a no-take marine protected area along the Guanacaste coast as pro- Hilborn and Walters, 1992; Myers et al., 2007), the smaller sizes of posed by Whoriskey et al. (2011) would greatly reduce bycatch not sharks at maturation in the Eastern Pacific may also be due to the re- only of olive ridleys but also of leatherback turtles, since the largest duced primary productivity of this area and the influence of El Nino nesting population remaining in the eastern Pacific nests at Parque (Saba et al., 2008; Wallace et al., 2006a, 2006b). Additional testing is Nacional Marino Las Baulas in Guanacaste (Shillinger et al., 2010), and needed to determine the effect of bottom–up and climate forcing on of green turtles that nest in the area (Blanco et al., 2012). Another ap- pelagic thresher sharks and silky sharks. proach would be to enforce a time-area closure of the fishing season during the turtle nesting seasons. The greatest interactions with olive 4.4. Implications for bony fishes and sharks ridleys near the arribada beaches occurred from October to February, the same period during which leatherbacks nest. Closing the area to There are serious negative implications of continuing the current fishing during that period would greatly reduce bycatch of sea turtles. rates of Costa Rican longline fishing for populations of bony fish, sharks This approach would also control the large unregulated artisanal and rays. Our data indicated that several species were being fishery. overexploited. This is not an unfamiliar situation. Hutchings et al. Pelagic sharks and rays are subject to high and often unrestricted (2010) reported that marine fishes declined by 38% between 1970 levels of mortality from bycatch and targeted fisheries throughout the and 2007, and that the rate of decline increased among several top oceans (Baum et al., 2003). We found that the Costa Rican longline fish- predators since 1992. Meaningful progress in restoring depleted fish ery affected the three species of sharks that we examined (reduced sizes populations will require population-specific recovery targets and time of silky sharks, capture of small blacktip sharks from nursery grounds lines for achieving those targets. On a worldwide basis, recovery of and small sizes of pelagic thresher sharks). In addition to the usual overexploited marine populations has been slow (Neubauer et al., need for more data, there is a clear need for more effective management 2013). Resilience of stocks subjected to moderate levels of overfishing of the Costa Rican longline fishery. Effective management plans to- is enhanced, but prolonged intense overexploitation delays recovery protect sharks have had success in the in recent years and increases the uncertainty in recovery times. Current harvest and (Carlson et al., 2012). In the United States, fork lengths from 1994 to low biomass levels mean that recovery is unlikely for the majority of 2009 for four species of coastal shark remained relatively stable D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 237 following a management plan for shark populations introduced in 1993 caught in that fishery and the high rate of bycatch of non-target species. (Carlson et al., 2012; National Marine Fisheries Service, 1993). However, Therefore, there is no sustainable fishery to protect. Currently, reduction fishing pressure is increasing in Costa Rica with particular emphasis on of fishing effort through creation of marine protected areas or time area catching mahi-mahi, billfish and sharks (Alpizar, 2006). In 2005, Costa closures is the only true option to reduce sea turtle and shark bycatch. Rica passed a fisheries law, which prohibits the landing of sharks with- It appears that neither fisheries biologists nor regulators have out their fins attached (Ley de Pesca y Acuicultura #8436). As of the learned any lessons from the implementation of turtle excluder device writing of this manuscript, this law has had very limited effects on the regulations in the US shrimp fishery. A turtle excluder device allows shark fishery due to lax enforcement by INCOPESCA (Alpizar, 2006; sea turtles to escape from a shrimp or other trawl by swimming out of Pretoma, 2012; Whoriskey et al., 2011) and it does not address shark a hole before it reaches the bag end of the net. That technology was overfishing (whether sharks are finned or not). A protected area or invented in the 1970s but not fully required on fishing trawls in the time area closure approach is needed for sharks as well as for sea turtles. US until 2003. It took almost 30 years for the US federal government Protection is needed for the nursery area of blacktip sharks. That in to finally require use of this effective technology by all shrimp trawlers turn would also protect green turtles and olive ridley turtles that nest because fishery biologists and regulators were waiting for fishermen to on the Osa Peninsula (Drake, 1996; Govan, 1998). In the case of silky accept the technology (Spotila, 2011). Tens of thousands of adult logger- sharks, spatial closures of the eastern Pacifictunafishery would mini- head turtles (Caretta carreta) drowned in shrimp trawls during that mize catch of juvenile silky sharks (Watson et al., 2009). It is unknown period and the population continued to decline. what effect this would have on other bycatch species such as pelagic In Costa Rica, INCOPESCA, the national fisheries agency has defied thresher sharks and olive ridley turtles, but it would reduce silky national law and failed to enforce rules against the landing of shark shark bycatch by 33% and tuna bycatch by only 12%. Another approach fins. The agency is reluctant to enforce laws that inconvenience fisher- would be to enact seasonal closures of the mahi-mahi fishery, closing men due to conflicts of interest on the part of Board members of the the fishery when mahi-mahi are not in season and when shark catch agency who are fishermen (Presidencia de la República, 2012). It also is greatest. Finally, decreasing soak times of longlines proved to de- either does not have data or does not make those data public on fishing crease catch rate of olive ridley turtles, silky sharks and thresher sharks effort and catches for much of the fishery. Therefore, it will be that much in the northeastern Pacific and had little impact on the number of mahi- harder for fishery biologists to begin finding solutions acceptable to the mahi caught (Whoriskey et al., 2011). With strengthened management industry because they remain at the data collection stage of the process. and protection of shark species in Costa Rican waters, it should be pos- sible to ameliorate the stresses caused to shark populations by fisheries. 5. Conclusion fi 4.6. The sheries conundrum: regulators and promoters In the face of delay and obfuscation on the part of the fishing indus- try and INCOPESCA the only solution to reduce bycatch of sea turtles fi Unfortunately, it is dif cult to implement methods to minimize and affected species of fish in Costa Rica is to set aside protected areas catch of bycatch species such as sea turtles because of limitations im- where both turtles and fish are safe from longlines and other fishing fi fi posed by both sheries biologists and regulators. Many sheries biolo- gear. At the same time observers should be placed on at least 50% of me- gists believe that the only acceptable methods of reducing bycatch are dium and larger fishing vessels so that data can be acquired on fishing fi those that do not inconvenience shermen or reduce their target methods and bycatch and fishermen can be educated to improve their fi catch more than a minimal amount. Regulators nd themselves in the fishing techniques and to release bycatch species alive. This approach situation of promoting the industry that they are required to regulate. has been effective in reducing bycatch in the Chilean longline fishery fi In a recent study, non-target species in the Costa Rica longline shery (Donoso and Dutton, 2010). Educational efforts with artisanal fisher- comprised more than half of the total catch when compared to market- men may be effective in improving their fishing techniques so that able catch (Swimmer et al., 2011). Yet the authors conclude that they can catch fish and not turtles, or at least release the turtles “ strategies to reduce sea turtle interactions must meet strict criteria if unharmed. fi they are to be adopted. Speci cally, they must be effective at reducing Waiting 30 years for fishery biologists to do more tests and for fish- bycatch and commercially viable in maintaining target species catch ermen to get comfortable with regulations, assuming regulators actually ” rates. Although experimental appendage hooks were effective in re- enforce them, is not a viable solution for sea turtles and for many species ducing sea turtle interactions in the Costa Rica shallow set mahi-mahi of fish. All countries have regulations about not robbing banks. Society fi “ shery, the authors concluded that the hooks would not be acceptable does not wait for robbers to agree to those regulations before it enforces ” to the industry because of reductions in target species capture rates. them. The same should be true for enforcing regulations on fishermen fi The authors are continuing their search for a modi cation that better who are effectively robbing the oceans of their biodiversity. [SS] serves both industry and conservation. Despite all of the data already available on the effect of longline and gill net fisheries on sea turtles (Lewison and Crowder, 2007; Spotila References et al., 2000; Wallace et al., 2010; Whoriskey et al., 2011), Hall et al. Agardy, T., 2000. Effects of fisheries on marine ecosystems: a conservationist's perspec- (2012) state that it is still necessary to gather more detailed data to tive. J. Mar. Sci. 57, 761–765. pinpoint seasonality, geographic range, fishing techniques and species Alpizar, M., 2006. Participation and fisheries management in Costa Rica: from theory to practice. Mar. Policy 30, 641–650. most associated with sea turtle bycatch. Once the problem has been Arauz, R., 1999. Description of the eastern Pacific high-seas longline and coastal gillnet identified they state that a research program is needed to identify a swordfish fisheries of South America, including sea turtle interactions, and manage- technological fix. Whatever the fix, it must operate so that fishermen ment recommendations. Unpublished report, Sea Turtle Restoration Project and Tur- can continue to practice a sustainable fishery. Solutions will have to be tle Island Restoration Network Report. Available from www.pretoma.org/downloads/ pdf/Spotila%20report.pdf [accessed 27 June 2012]. “effective and practical to increase the chances of adoption by the fish- Baremore, I.E., Bathea, D.M., Andrews, K.I., 2012. Gillnet selectivity for juvenile blacktip ers themselves, reducing problems of rejection or noncompliance.” sharks. . Bull.-NOAA 110, 230–241. Bascompte, J., Melián, C.J., Sala, E., 2005. Interaction strength combinations and the Thus, it appears that bycatch will continue unabated for many years fi – fi fi over shing of a marine food web. Proc. Natl. Acad. Sci.-Biol. 102, 5443 5447. while shery biologists collect more data and shermen become com- Baum, J.K., Blanchard, W., 2010. Inferring shark population trends from generalized linear fortable with whatever solutions fishery biologists come up with to mixed models of pelagic longline catch and effort data. Fish. Res. 102, 229–239. save sea turtles and other vulnerable species from extinction. The idea Baum, J.K., Myers, R.A., 2004. Shifting baselines and the decline of pelagic sharks in the – fi “ ” fi Gulf of Mexico. Ecol. Lett. 7, 135 145. that the Costa Rican longline shery is sustainable is falsi ed by the Baum, J.K., Worm, B., 2009. Cascading top–down effects of changing oceanic predator data that indicate the decrease in size or small size of the sharks being abundances. J. Anim. Ecol. 78, 699–714. 238 D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239

Baum, J.K., Myers, R.A., Kehler, D.G., Worm, B., Harley, S.J., Doherty, P.A., 2003. Collapse Honarvar, S., Spotila, J.R., O'Connor, M.P., 2011. Microbial community structure in sand on and conservation of shark populations in the Northwest Atlantic. Science 299, two olive ridley arribada nesting beaches, Playa La Flor, and Playa Nancite, 389–392. Costa Rica. J. Exp. Mar. Biol. Ecol. 409, 339–344. Bjorndal, K.A., 1985. Nutritional ecology of sea turtles. Copeia 1985, 736–751. Hutchings, J.A., Minto, C., Ricard, D., Baum, J.K., Jensen, O.P., 2010. Trends in the abundance Bjorndal, K.A., Bolten, A.B., Chaloupka, M.Y., 2000. Green turtle somatic growth model: ev- of marine fishes. Can. J. Fish. Aquat. Sci. 67, 1205–1210. idence for density dependence. Ecol. Appl. 10, 269–282. IUCN, 2012. IUCN Red List of threatened species. Version 2012.1 www.iucnredlist.org Blanco, G.S., Morreale, S.J., Seminoff, J.A., Paladino, F.V., Piedra, R., Spotila, J.R., 2012. (downloaded on 8/6/2012). Movements and diving behavior of internesting green turtles (Chelonia mydas, Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J., Linnaeus 1758) along Pacific Costa Rica. Integr. Zool. http://dx.doi.org/10.1111/ Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S., Lange, j.1749-4877.2012.00298 (14 NOV 2012). C.A., Lenihan, H.S., Pandolfi, J.M., Peterson, C.H., Steneck, R.S., Tegner, M.J., Warner, Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B., R.R., 2001. Historical overfishing and the recent collapse of coastal ecosystems. Cooper, S.D., Halpern, B.S., 2005. What determines the strength of a trophic cascade? Science 293, 629–638. Ecology 86, 528–537. Jensen, O.P., Branch, T.A., Hilborn, R., 2012. Marine fisheries as ecological experiments. Branch, T.A., Jensen, O.P., Ricard, D., Ye, Y., Hilborn, R., 2011. Contrasting global trends in Theor. Ecol. 5, 3–22. marine fishery status obtained from catches and from stock assessments. Conserv. Koch, V., Nichols, W., Peckham, H., Delatoba, V., 2006. Estimates of sea turtle mortality Biol. 25, 777–786. from poaching and bycatch in Bahía Magdalena, Baja Sur, Mexico. Biol. Byrd, J., Murphy, S., Von Harten, A., 2005. Morphometric analysis of the northern Conserv. 128, 327–334. subpopulation of Caretta caretta in South Carolina, USA. Mar. Turtle Newslett. Lewison, R.L., Crowder, L.B., 2007. Putting longline bycatch of sea turtles into perspective. 107, 1–4. Conserv. Biol. 21 (1), 79–86. Camiñas, J.A., 2004. Sea turtles of the Mediterranean Sea: population dynamics, sources Liu, K., Chen, C., Liao, T., Joung, S., 1999. Age, growth, and reproduction of the pelagic of mortality and relative importance of fisheries impacts. Expert Consultation on thresher shark, Alopias pelagicus, in the Northwestern Pacific. Copeia 1999, 68–74. Interactions between Sea Turtles and Fisheries within an Ecosystem Context. Food Liu, K., Chang, Y., Hsun Ni, I., Jin, C., 2006. Spawning per recruit analysis of the pelagic and Agriculture Organization Fisheries Report 738, Supplement. FAO, Rome. thresher shark, Alopias pelagicus, in the eastern Taiwan waters. Fish. Res. 82 (1-3), Carlson, J.K., Sulikowski, J.R., Baremore, I.E., 2006. Do differences in life history exist for 56–64. blacktip sharks, Carcharhinus limbatus, from the United States South Atlantic Bight Mackenzie Jr., C.L., 1992. The fisheries of Raritan Bay. Rutgers University Press, New and Eastern Gulf of Mexico? Environ. Biol. Fish. 77, 279–292. Brunswick, New Jersey. Carlson, J.K., Hale, L.F., Morgan, A., Burgess, G., 2012. Relative abundance and size of Marquez, R.M., Peñaflores, C., Vasconcelos, J., 1996. Olive ridley turtles (Lepidochelys coastal sharks derived from commercial shark longline catch and effort data. J. Fish olivacea) show signs of recovery at La Escobilla, Oaxaca. Mar. Turtle Newslett. 73, 5–7. Biol. 80, 1749–1764. Mowat, F., 1996. Sea of Slaughter. Chapters, Shelburne, Vermont. Carranza, A., Domingo, A., Estrades, A., 2006. Pelagic longlines: A threat to sea turtles in Mug Villanueva, M., 2002. Octavo informe sobre el estado de la Nación en desarrollo the Equatorial Eastern Atlantic. Biol. Conserv. 131, 52–57. humano sostenible. Análisis de las tendencias del comportamiento y desempeño Clarke, S.C., McAllister, M.K., Milner-Gulland, E.J., Kirkwood, G.P., Michielsens, C.G.J., del sector pesquero en Costa Rica. Estado de la Nación, Costa Rica. Agnew, D.J., Pikitch, E.K., Nakano, H., Shivji, M.S., 2006. Global estimates of shark Myers, R.A., Worm, B., 2005. Extinction, survival, or recovery of large predatory fishes. catches using trade records from commercial markets. Ecol. Lett. 9, 1115–1126. Philos.Trans.R.Soc.Lond.BBiol.Sci.360,13–20. Cope, J.M., 2006. Exploring intraspecific life history patterns in sharks. Fish. Bull.-NOAA Myers, R.A., Baum, J.K., Shepherd, T.D., Powers, S.P., Peterson, C.H., 2007. Cascading effects 104, 311–320. of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850. Development Core Team, 2012. www.r-project.org. Nadon, M.O., Baum, J.K., Williams, I.D., McPherson, J.M., Zgliczynski, B.J., Richards, B.L., Donoso, M., Dutton, P.H., 2010. Sea turtle bycatch in the Chilean pelagic longline Schroeder, R.E., Brainard, R.E., 2012. Re-creating missing population baselines for fishery in the southeastern Pacific: opportunities for conservation. Biol. Conserv. Pacific reef sharks. Conserv. Biol. 26, 493–503. 143, 2672–2684. National Marine Fisheries Service, 1993. management plan for sharks of the At- Drake, D.L., 1996. Marine turtle nesting, nest predation, hatch frequency, and nesting lantic Ocean. Available at http://www.nmfs.noaa.gov/sfa/hms/hmsdocument_files/ seasonality on the Osa Peninsula, Costa Rica. Chelonian Conserv. Biol. 2, 89–92. FMPs.htm/. Dulvy, N.K., Baum, J.K., Clarke, S., Compagno, L.J.V., Cortes, E., Domingo, A., Fordham, S., National Marine Fisheries Service, 1998. Recovery plan for U.S. Pacific populations of the Fowler, S., Francis, M.P., Gibson, C., Martinez, J., Musick, J.A., Soldo, A., Stevens, J.D., olive ridley turtle. Available at http://www.nmfs.noaa.gov/pr/pdfs/recovery/ Valenti, S., 2008. You can swim but you can't hide: the global status and conservation turtle_oliveridley.pdf. of oceanic pelagic sharks and rays. Aquat. Conserv. 18, 459–482. National Marine Fisheries Service, 2003. Final amendment 1 to the fishery management Ferretti, F., Worm, B., Britten, G.L., Heithaus, M.R., Lotze, H.K., 2010. Patterns and ecosystem plan for Atlantic tunas, swordfish and sharks. Available at http://www.nmfs.noaa. consequences of shark declines in the ocean. Ecol. Lett. 13, 1055–1071. gov/sfa/hms/hmsdocument_files/FMPs.htm/. Fonseca, L.G., Murillo, G.A., Guadamúz, L., Spínola, R.M., Valverde, R.A., 2009. Downward Neubauer, P., Jensen, O.P., Hutchings, J.A., Baum, J.K., 2013. Resilience and recovery of but stable trend in the abundance of arribada olive ridley sea turtles (Lepidochelys overexploited marine populations. Science 340, 347–349. olivacea) at Nancite Beach, Costa Rica (1971–2007). Chelonian Conserv. Biol. 8, Palacios, D.M., Bograd, S.J., 2005. A census of Tehuantepec and Papagayo eddies in the 19–27. northeastern tropical Pacific. Geophys. Res. Lett. 32 http://dx.doi.org/10.1029/ Frick, L.H., Reina, R.D., Walker, T.I., 2010. Stress related physiological changes and post- 2005GL024324 L23606. release survival of Port Jackson sharks (Heterodontus portusjacksoni) and gummy Palacios, D., Bograd, S., Foley, D., Schwing, F., 2006. Oceanographic characteristics of bio- sharks (Mustelus antarcticus) following gill-net and longline capture in captivity. logical hot spots in the North Pacific: a remote sensing perspective. Deep Sea Res. II J. Exp. Mar. Biol. Ecol. 385, 29–37. Top. Stud. Ocean 53, 250–269. Gilman, E., Zollett, E., Beverly, S., Nakano, H., Davis, K., Shiode, D., Dalzell, P., Kinan, I., 2006. Pinsky, M.L., Jensen, O.P., Ricard, D., Palumbi, S.R., 2011. Unexpected patterns of fisheries Reducing sea turtle by-catch in pelagic longline fisheries. Fish Fish. 7, 2–23. collapse in the world's oceans. Proc. Natl. Acad. Sci. U. S. A. 108, 8317–8322. Gilman, E., Clarke, S., Brothers, N., Alfaroshigueto, J., Mandelman, J., Mangel, J., Petersen, S., Plotkin, P.T., Briseno-Duenas, R., Abreu-Grobois, F.A., 2012. Interpreting signs of olive Piovano, S., Thomson, N., Dalzell, P., 2008. Shark interactions in pelagic longline ridley recovery in the eastern Pacific. In: Seminoff, J.A., Wallace, B.P. (Eds.), Sea Turtles fisheries. Mar. Policy 32, 1–18. of the Eastern Pacific. Advances in Research and Conservation. University of Arizona Govan, H., 1998. Community turtle conservation at Rio Oro on the Pacific coast of Costa Press, Tucson, Arizona, pp. 302–335. Rica. Mar. Turtle Newslett. 80, 10–11. Polovina, J.J., Balazs, G.H., Howell, E.A., Parker, D.M., Seki, M.P., Dutton, P.H., 2004. Forage Hall, M., Swimmer, Y., Parga, M., 2012. No “silver bullets” but plenty of options. In: and migration habitat of loggerhead (Caretta caretta) and olive ridley (Lepidochelys Seminoff, J.A., Wallace, B.P. (Eds.), Sea Turtles of the Eastern Pacific. Advances olivacea) sea turtles in the central North Pacific Ocean. Fish. Oceanogr. 13, 36–51. in Research and Conservation. University of Arizona Press, Tucson, Arizona, Preisser, E.L., Bolnick, D.I., Benard, M.F., 2005. Scared to death? The effects of intimidation pp. 136–153. and consumption in predator-prey interactions. Ecology 86, 501–509. Heithaus, M.R., Dill, L.M., 2006. Does tiger shark predation risk influence foraging habitat Presidencia de la República, 2012. INFORME: Comisión Presidencial Para la Gobernanza use by bottlenose dolphins at multiple spatial scales? Oikos 114, 257–264. Marina. Presidencia de la República de Costa Rica (14 de junio, 2012). Heithaus, M.R., Frid, A., Wirsing, A.J., Dill, L.M., Fourqurean, J.W., Burkholder, D., Thomson, Pretoma, 2012. Programa restauración de Tortugas marinas. www.pretoma.org. J., Bejder, L., 2007. State-dependent risk-taking by green sea turtles mediates top– Price, E.R., Wallace, B.P., Reina, R.D., Spotila, J.R., Paladino, F.V., Piedra, R., Velez, E., down effects of tiger shark intimidationinamarineecosystem.J.Anim.Ecol. 2004. Size, growth and reproductive output of adult female leatherback turtles 76, 837–844. (Dermochelys coriacea). Endanger. Species Res. 5, 1–8. Heithaus, M.R., Frid, A., Wirsing, A.J., Worm, B., 2008. Predicting ecological consequences Reina, R.D., Spotila, J.R., Paladino, F.V., Dunham, A.E., 2009. Changed reproductive sched- of marine top predator declines. Trends Ecol. Evol. 4, 202–210. ule of eastern Pacific leatherback turtles Dermochelys coriacea following the Heithaus, M.R., Wirsing, A.J., Dill, L.M., 2012. The ecological importance of intact top- 1997–98 El Niño to La Niña transition. Endang. Species Res. 7, 155–161. predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Robbins, W.D., Hisano, M., Connolly, S.R., Choat, H., 2006. Ongoing collapse of coral-reef Mar.Freshw.Res.63,1039–1050. shark populations. Curr. Biol. 16, 2314–2319. Hernández-Echeagaray, O.E., Hernández-Cornejo, R., Harfush-Meléndez, M., García- Saba, V.S., Santidrian-Tomillo, P., Reina, R.D., Spotila, J.R., Musick, J.A., Evans, D.A., Paladino, Gasca, A., 2012. Evaluation of sex ratios of the olive ridley sea turtle (Lepidochelys F.V., 2007. The effect of El Niño Southern Oscillation on the reproductive frequency of olivacea) on the arribada nesting beach, La Escobilla, Mexico. Mar. Turtle Newslett. eastern Pacific leatherback turtles. J. Appl. Ecol. 44, 395–404. 133, 12–16. Saba, V.S., Spotila, J.R., Chavez, F.P., Musick, J.A., 2008. Bottom-up and climatic forcing on Hilborn, R., Walters, C.J., 1992. Quantitative Fisheries Stock Assessment. Chapman & Hall, the worldwide population of leatherback turtles. Ecology 89, 1414–1427. New York, NY, USA. Sánchez-de Ita, J.A., Quiñónez-Velázquez, C., Galván-Magaña, F., Bocanegra-Castillo, N., Honarvar, S., O'Connor, M.P., Spotila, J.R., 2008. Density-dependent effects on hatching Félix-Uraga, R., 2010. Age and growth of the silky shark Carcharhinus falciformis success of the olive ridley turtle, Lepidochelys olivacea. Oecologia 157, 221–230. from the West Coast of Baja California Sur, Mexico. J. Appl. Ichthyol. 27, 20–24. D. Dapp et al. / Journal of Experimental Marine Biology and Ecology 448 (2013) 228–239 239

Sandoval -Espinoza, S., 2011. Proporción sexual en crías de tortuga Lepidochelys olivacea en Varghese, S.P., Varghese, S., Somvanshi, V.S., 2010. Impact of tuna longline fishery on the corrales de incubación del Pacífico Mexicano. Doctoral Thesis Centro Interdisciplinario sea turtles of Indian seas. Curr. Sci. India 98, 1378–1384. de Ciencias Marinas, Mexico 80 (In Spanish). Vert-pre, K.A., Amoroso, R.O., Jensen, O.P., Hilborn, R., 2013. Frequency and intensity of Shillinger, G.L., Palacios, D.M., Bailey, H., Bograd, S.J., Swithenbank, A.M., Gaspar, P., productivity regime shifts in marine fish stocks. Proc. Acad. Natl. Sci. U. S. A. 110, Wallace, B.P., Spotila, J.R., Paladino, F.V., Piedra, R., Eckert, S.A., Block, B.A., 2008. 1779–1784. Persistent leatherback turtle migrations present opportunities for conservation. Wallace, B.P., Kilham, S., Paladino, F.V., Spotila, J.R., 2006a. Energy budget calculations re- PLoS Biol. 6 (7), E171. veal resource limitation in eastern Pacific leatherback turtles. Mar. Ecol. Prog. Ser. Shillinger, G.L., Swithenbank, A.M., Bograd, S.J., Bailey, H., Castelton, M.R., Wallace, B.P., 318, 263–270. Spotila, J.R., Paladino, F.V., Piedra, R., Block, B.A., 2010. Identification of high-use Wallace, B.P., Seminoff, J.A., Kilham, S.S., Spotila, J.R., Dutton, P.H., 2006b. Leatherback tur- internesting habitats for eastern Pacific leatherback turtles: role of the environment tles as oceanographic indicators: stable isotope analyses reveal a trophic dichotomy and implications for conservation. Endang. Species Res. 10, 215–232. between ocean basins. Mar. Biol. 149, 953–960. Shillinger, G.L., Di Lorenzo, E., Luo, H., Bograd, S.J., Hazen, E.L., Bailey, H., Spotila, J.R., 2012. Wallace, B.P., Lewison, R.L., McDonald, S.L., McDonald, R.K., Kot, C.Y., Kelez, S., Bjorkland, On the dispersal of leatherback turtle hatchlings from Mesoamerican nesting R.K., Finkbeiner, E.M., Helmbrecht, S., Crowder, L.B., 2010. Global patterns of marine beaches. Proc. R. Soc. B 279, 2391–2395. turtle bycatch. Conserv. Lett. 3, 131–142. Spotila, J.R., 2011. Saving Sea Turtles, Extraordinary Stories from the Battle Against Watson, J.W., Epperly, S.P., Shah, A.K., Foster, D.G., 2005. Fishing methods to reduce Extinction. Johns Hopkins Press, Baltimore MD, USA. sea turtle mortality associated with pelagic longlines. Can. J. Fish. Aquat. Sci. 62, Spotila, J.R., Reina, R.R., Steyermark, A.C., Plotkin, P.T., Paladino, F.V., 2000. Pacificleather- 965–981. back turtles face extinction. Nature 405, 529–530. Watson, J.T., Essington, T.E., Lennert-Cody, C.E., Hall, M.A., 2009. Trade-offs in the design of Swimmer, Y., Arauz, R., McCracken, M., Ballestero, J., Musyl, M., Bigelow, K., Brill, R., 2006. fishery closures: management of silky shark bycatch in the Eastern PacificOceantuna Diving behavior and delayed mortality of olive ridley sea turtles Lepidochelys olivacea fishery. Conserv. Biol. 23, 626–635. after their release from longline fishing gear. Mar. Ecol. Prog. Ser. 323, 253–261. Whiting, S.D., Long, J.L., Coyne, M., 2007a. Migration routes and foraging behaviour of Swimmer, Y., Suter, J., Arauz, R., Bigelow, K., Lopez, A., Zanela, I., Bolanos, J., Suarez, R., olive ridley turtles Lepidochelys olivacea in Northern Australia. Endang. Species Res. Wang, J., Boggs, C., 2011. Sustainable fishing gear: the case of modified circle hooks 3, 1–9. in a Costa Rican fishery. Mar. Biol. 158, 757–767. Whiting, S.D., Long, J.L., Hadden, K.M., Lauder, A.D.K., Koch, A.U., 2007b. Insights into size, Tiwari, M., Bjorndal, K.A., 2000. Variation in morphology and reproduction in loggerheads, seasonality and biology of a nesting population of the olive ridley turtle in Northern Caretta caretta, nesting in the United States, Brazil, and Greece. Herpetologica 56, Australia. Wildl. Res. 34, 200–210. 343–356. Whoriskey, S., Arauz, R., Baum, J.K., 2011. Potential impacts of emerging mahi-mahi fisheries Valverde, R.A., Orrego, C.M., Tordoir, M.T., Gómez, F.M., Solís, D.S., Hernández, R.A., Gómez, on sea turtle and elasmobranch bycatch species. Biol. Conserv. 144, 1841–1849. G.B., Brenes, L.S., Baltodano, J.P., Fonseca, L.G., Spotila, J.R., 2012. Olive ridley mass Zug, G.R., Chaloupka, M., Balazs, G.H., 2006. Age and growth in olive ridley sea turtles nesting ecology and egg harvest at Ostional beach, Costa Rica. Chelonian Conserv. (Lepidochelys olivacea) from the north-central Pacific: a skeletochronological analysis. Biol. 11, 1–11. Mar. Ecol. 27, 263–270.