From Microsatellite DNA Profiling to Satellite Telemetry: Integrating Behavioral Ecology Into Shark Conservation.

Chapter 1 The mating systems of two annually-reproducing hammerhead sharks (scalloped hammerhead Sphyrna lewini, bonnethead Sphyrna tiburo) were investigated by genetically-profiling 82 litters (902 embryos). Unlike three biennially-reproducing shark species previously studied that are polygynandrous, genetic monogamy was common in females of both of these hammerheads (S. lewini [70.6 % of litters], S.tiburo [85.4-62.5%]), suggesting a polygynous mating system overall. These mating system characteristics suggest that hammerheads may have lower ratios of effective to census population sizes than polygynandrous sharks, adding to conservation concerns for these species. Results suggest that female mating behavior may play a more limited role in determining the population-level of multiple paternity than currently envisioned in sharks, with the interplay between male mating tactics and female reproductive periodicity (biennial or annual) perhaps being more influential. Two lines of evidence infer that multiple paternity is associated with larger females in S. tiburo: mothers of multi-sired litters are significantly larger than mothers of single paternity litters in West Florida and the frequency of multiple paternity is significantly higher in South Carolina, where females are larger. Large females may therefore produce larger, more genetically-diverse litters in some shark species and could contribute disproportionately to recruitment and population genetic diversity, increasing their importance from a conservation perspective. Chapter 2 Although most shark species have relatively small body-sizes as adults (\u3c100 cm total length), little is known about the genetic population structure and lineage diversification of small sharks. Mitochondrial control region and nuclear internal transcribed spacer 2 sequences combined with three independent microsatellite loci all concordantly show that the diminutive hammerhead shark Sphyrna tiburo (bonnethead) consists of two highly divergent lineages from South Carolina, U.S.A. to Belize, a coastal distance of less than 6000 km. One lineage was restricted to Belize, while the other was almost completely restricted to five North American sampling sites (pairwise CR ΦST = 0.891-0.915, microsatellite Fst=0.277-0.319). This represents the highest degree of population structure recorded concordantly at both mitochondrial and nuclear loci in a shark along a continuous coastline. Regional measures of population structure and genetic divergence in this diminutive hammerhead shark mirror but exceed values obtained for larger shark species over the same sampling range and are comparable to those observed in a larger congener on a global scale. Direct evidence of interbreeding between these lineages indicates that speciation has not yet occurred. Gene-flow was generally high among North American populations, but there was evidence that female-mediated gene flow is moderately restricted between subtropical Florida Bay and higher latitude populations, suggesting that changes in latitude and climate regime may help drive population genetic differentiation in this species. This study is the second to reveal unexpectedly high lineage diversification within Atlantic hammerhead sharks, which suggests that further genetic surveys are required to fully understand and conserve hammerhead shark biodiversity in this region. Chapter 3 Dried fins from the scalloped hammerhead shark (Sphyrna lewini) are highly-valued for utilization in the Asian delicacy shark-fin soup. While global landings of this species annually measure in the millions to supply this market, Western Atlantic populations have collapsed and are now considered to be endangered. This study reveals that Western Atlantic S. lewini comprise at least three distinct management units that will be reliant on intrinsic reproduction rather than immigration for rebuilding (MU’s: U.S.A., Central American Caribbean and Brazil; overall ΦST=0.64). These MU’s are sufficiently differentiated from each other, eastern Atlantic and Indo-Pacific stocks to use mixed-stock analysis (MSA) to better understand the impact of the fin trade on sharks of this region. Stock of origin was determined for 57 Hong Kong market-derived S. lewini dried fins, revealing that contemporary trade is globally-sourced with a substantial presence of fins from imperiled Western Atlantic stocks. Results are used to formulate regional management recommendations and to develop monitoring strategies for the Asian fin trade that could dramatically improve global conservation of S. lewini and serve as a template for other sharks impacted by this trade. Chapter 4 Longline sampling (83 sets) supplemented with 6 pop-off archival tag (PAT) deployments were used to characterize vertical habitat use by Caribbean reef sharks, Carcharhinus perezi, at Glover’s reef atoll, Belize. Longline CPUE in two shallow reef habitats (lagoon \u3c 18m depth, fore-reef \u3c 40 m depth) underwent significant nocturnal increases for sharks larger than 110 cm total length (TL) but not for smaller sharks. Nocturnal CPUE of small sharks increased in the lagoon and decreased on the fore-reef, suggesting movements to avoid larger conspecifics. PAT deployments (7-20 days) indicate that large C. perezi generally increased the amount of time they spent in the upper 40 m of the water column during the night and have a much wider depth and temperature range than previously thought (0 to 356 m, 31-12.4oC). The wide vertical range of this top-predator reveals ecological coupling of deep and shallow reef habitats and has implications for place-based conservation. Chapter 5 Marine Protected Areas (MPAs) are increasingly advocated for the restoration and conservation of coral reef ecosystems, yet given the typically small size of most no-take MPAs it remains unknown how effective this strategy will be for roving, top-level predators such as sharks. Movement patterns of Caribbean reef sharks, Carcharhinus perezi, tagged with coded acoustic transmitters were monitored with an array of up to 22 underwater receivers from May 2004 to October 2006 at Glover’s Reef Marine Reserve, a zoned MPA in Belize. Thirty one tagged sharks ranged in size from 80-215 cm total length [TL], spanning young-of-the-year to mature specimens of both genders. Twenty five of these sharks provided data for more than one week after tagging. Individual sharks were detected within the array on from 5 to 464 days and all but four were predominantly detected on the receiver(s) nearest their original capture. Although daily movements of up to 20-50 km were documented by large sharks (\u3e110 cm TL), most individuals were detected at Glover’s Reef on an almost daily basis throughout the year and appear to be residents of this reef system. Small sharks were documented to be residents for at least six months. The daily dispersal ranges and distribution of sharks tracked in this study suggest that typically small-sized no-take zones will be of limited value for reef shark conservation. However, the long-term residency and site-fidelity of large and small C. perezi to this reef system in its entirety indicates that nesting this no-take zone within a broader ocean zoning plan tailored to protect large roving predators achieves the scale necessary to provide meaningful protection for these ecologically important, threatened predators