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Vol. 14: 135–140, 2011
Published online June 22
Endang Species Res
Killing for conservation: the need for alternatives
to lethal sampling of apex predatory sharks
Neil Hammerschlag1, 2, 3,*, James Sulikowski4
1Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami,
Florida 33149, USA
2Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, PO Box 248203, Coral Gables,
Florida 33124, USA
3RJ Dunlap Marine Conservation Program, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149, USA
4University of New England, Marine Sciences Department, Marine Science Center, 11 Hills Beach Road, Biddeford,
Maine 04005, USA
ABSTRACT: Top oceanic predators, especially large predatory sharks (TOPS), appear to be experi-encing varying degrees of population declines. Life history data (e.g. diet, reproductive status, ageand growth, mortality) are critical for developing effective conservation strategies for TOPS.
Presently, lethal sampling remains the most effective and accurate means of gathering these data. Tomeet such challenges, many scientists have utilized specimens obtained from recreational and com-mercial fisheries, but have needed to supplement those data with fishery-independent sampling.
However, there is growing public and scientific debate as to whether lethal sampling of TOPS is jus-tified for obtaining conservation data. Here we describe the development and use of non-lethal alter-natives for collecting data on (1) trophodynamics; (2) maturity state and fecundity; and (3) growth andmortality rates necessary to enact conservation measures for threatened or even data-deficient TOPS.
KEY WORDS: Conservation · Shark · Scientific sampling · Lethal sampling · Population status ·Life history · Fisheries Resale or republication not permitted without written consent of the publisher INTRODUCTION
Heupel & Simpfendorfer (2010). In their paper, the au-thors concluded that with respect to sharks: Through growing public awareness of the threats fac- …Although lethal sampling comes at a cost to a population, ing wildlife and the widespread exposure of ‘green’ is- especially for threatened species, the conservation benefits sues, the public, press, scientists, and politicians alike are from well-designed studies provide essential data that ‘jumping on the conservation bandwagon’ and arguing cannot be collected currently in any other way… (p. 1212) for protection of many threatened species. There are nu- Life history data (diet, reproductive status, age and merous lines of evidence that top oceanic predators, es- growth, mortality) are critical for developing effective pecially large predatory sharks (hereafter TOPS sensu conservation strategies for sharks, and Heupel & Jacques 2010), are experiencing varying degrees of pop- Simpfendorfer (2010) argued that lethal sampling ulation decline (Pauly et al. 1998, Baum et al. 2003, My- presently remains the most effective and accurate means ers & Worm 2003, Hampton et al. 2005, Sibert et al. 2006, of gathering these data. To meet such challenges, many Myers et al. 2007, Dulvy et al. 2008). Subsequently, there scientists have relied on fishery-derived specimens, but is mounting debate as to whether lethal sampling of have needed to supplement those data with fishery-in- TOPS is justified for obtaining scientific data. Recently, dependent sampling (e.g. Piercy et al. 2010). In many ter- this controversial issue was objectively tackled by restrial predators, marine mammals, and even some Inter-Research 2011 · fishes, accepted non-lethal alternatives exist for obtain- Regardless of technique employed, gut content ing life history and demographic data; however, at pre- analyses usually fail to identify prey items to species sent, comparable alternatives are not yet widely used to level due to differential digestive rates (Bowen 1996).
study TOPS. Ethical, political, and emotional issues The use of a complementary measure, particularly sta- aside, lethal sampling does provide a variety of valuable ble isotope (SI) analysis, provides insights on an indi- biological and ecological data that cannot be otherwise vidual’s long-term diet, ontogenetic or seasonal diet achieved (Heupel & Simpfendorfer 2010). However, if shifts, as well as information on trophic position the goal is conser vation, we need to employ multi-disci- (Araújo & Gonzaga 2007). For SI analyses, only small plinary approaches to develop widely accepted alterna- samples of muscle, fin, or blood are needed, and these tives to traditional lethal techniques for generating data tissues can be easily, quickly and non-invasively necessary to enact conservation measures for threatened obtained in the field (Gallagher et al. 2010). Indeed, several recent studies have incorporated SI to examine Do researchers who study large terrestrial carnivores trophodynamics of TOPS (MacNeil et al. 2005, Estrada (e.g. lions Panthera leo, bald eagles Haliaeetus leuco- et al. 2006, Logan & Lutcavage 2010). However, SI cephalus, jaguars P. onca) even consider lethal sam- does not provide information on the identity of taxa pling as a viable option for obtaining demographic or actually being eaten. Thus, when designing a study on life history data for enacting conservation measures? feeding habits of TOPS, investigators should first con- We failed to find any evidence that this was the case sider whether SI could be used to address the ques- (e.g. Brown 1976, Lehmann et al. 2008, Ferreira & Fun- tions being investigated before adopting a lethal ston 2010). Do the inherent difficulties imposed by working in the ocean make lethal sampling of TOPS a Another promising non-lethal technique is employ- more necessary option for obtaining conservation ing stomach flushing (gastric lavage) in combination data? Working in the marine environment certainly with deoxyribonucleic acid (DNA) analysis of gut con- does present obstacles not encountered in terrestrial tents. Recently, Barnett et al. (2010) tested this method systems; however, studies of marine mammals and on subadult and adult broadnose sevengill sharks even fishes have found non-lethal alternatives for col- Notorynchus cepedianus up to ~3 m in total length. By lecting life history and demographic information undertaking molecular analysis of unidentifiable prey, (Weber & Innis 2007). Below we describe the use and the number of species-specific identifications of prey development of potential non-lethal alternatives for was double that which could be obtained without use collecting data on (1) trophodynamics; (2) maturity of DNA techniques. Further, after releasing sampled state and fecundity; and (3) growth and mortality rates.
sharks equipped with acoustic transmitters, subse-quent tracking demonstrated high survivorship post-fishing and stomach flushing (Barnett et al. 2010).
Studies of diets and feeding patterns can contribute MATURITY STATE AND FECUNDITY
to an understanding of ecological interactions andcommunity structure (e.g. Winemiller 1989, Krebs 1998, Data on maturity state, gestation period, and fecun- Hammerschlag et al. 2010). Such data are useful for dity are important for generating population models developing trophic models as tools for understanding used to estimate sustainable harvest levels. For TOPS, multi-species fisheries (Christensen & Pauly 1992, these parameters have traditionally been derived Walters et al. 1997). These data are traditionally through sacrificing of specimens. Such data have been obtained through gut content analysis. Several studies ob tained from dead specimens harvested in commer- have used non-lethal stomach eversion or gastric cial and recreational fisheries (Whitney & Crow 2007, lavage techniques (e.g. Cortés & Gruber 1990, Barnett Harry et al. 2010). Data collection could further be max- et al. 2010). Stomach contents can also be obtained imized by increased cooperation and coordination be- from TOPS already harvested in commercial and tween fishers and scientists. However, determination of recreational fisheries (e.g. Stillwell & Kohler 1982, reproductive timing and maturity requires sampling of Bowman et al. 2000, Maia et al. 2006). However, recre- all developmental stages and all months for both sexes.
ational and commercial fisheries sometimes only sam- Commercial and recreational fishery catches often re- ple a relatively narrow portion of the length-age distri- flect a small portion of the year (due to regulations or bution of a population; thus many studies have relied migratory patterns), only include a small span of the on supplementing these data with fishery-independent length and age distributions, and are often sex-biased.
surveys to obtain samples needed to investigate onto- Further, sacrificing animals in order to obtain reproduc- tive data can be problematic, especially for species that Hammerschlag & Sulikowski: Killing for conservation have been classified as Endangered or Threatened (e.g.
& Goldman 2004, Goldman 2005). The ability to per- Sulikowski et al. in press). Thus, unless non-lethal form age determinations based on the examination of sampling techniques are developed or those currently hard anatomical parts is of fundamental importance in in use are fine-tuned, information regarding reproduc- fisheries research (Goldman 2005). In most chon- tive biology for prohibited species will be difficult or drichthyans, enumeration of growth zones deposited in vertebral centra provides the most reliable method of Despite these difficulties, a wide range of potential estimating age-at-length (Cailliet & Goldman 2004, solutions do exist. Intrauterine endoscopy has shown Goldman 2005). This entails post-mortem extraction of promise as a non-lethal technique as it can directly vertebrae which can be obtained from ‘already-dead’ visualize the progress of gestation (Carrier et al.
animals, but usually requires supplementing with fish- 2003). However, despite its non-lethal nature, use of ery-independent surveys. Tag and release experi- this technique has the potential to produce detrimen- ments can also be designed in combination with post- tal side effects, including spontaneous abortion and mortem vertebrae studies to examine growth rates and accelerated gestation (Carrier et al. 2003). In recent age-validation in TOPS (Kohler & Turner 2001). This years, circulating concentrations of plasma steroid has been achieved, for example, in lemon sharks hormones, such as 17-β-estradiol (E2), progesterone Negaprion brevirostris (Gruber & Stout 1983), tiger (P4), and testosterone (T), have been used in combina- sharks Geleocerdo cuvier (Natanson et al. 1999), blue tion with an examination of gross morphological sharks Prionace glauca (Skomal 1990), and sandbar changes to evaluate events associated with reproduc- sharks Carcharhinus plumbeus (Casey & Natanson tive cycles and sexual maturity in a number of elas- 1992). The use of external hard parts, such as spines mobranchs (Manire et al. 1995, Heupel et al. 1999, and thorns, to non-lethally age chondrichthyans has Carrier et al. 2003, Sulikowski et al. 2006, 2007, generally yielded less than satisfactory results and is Awruch et al. 2008, Hoffmayer et al. 2010, Sulikowski typically associated with high inter-reader bias and et al. in press). While the results from these studies low repeatability (e.g. Davis et al. 2007, Barnett et al.
indicate that morphological changes in reproductive 2009). In addition, the general usefulness of these tracts and gonadal steroid hormone biosynthesis are structures appears to be species-specific and limited to intimately linked in elasmobranch reproduction, this chondrichthyans possessing those structures (e.g. Gal- technique requires further validation across all repro- lagher & Nolan 1999, Irvine et al. 2006). ductive modes. Another methodology that has the More recently, non-invasive estimates of growth and potential to be used as a non-lethal technique is ultra- mortality rates of fishes have been generated by ana- sound imaging, especially since this technology has lyzing nucleic acid levels and RNA:DNA ratios from become small and portable (e.g. 3.0–7.5 EC 7.5 MHz tissue biopsies (Buckley et al. 1999, Vinagre et al.
2008). To date, these methods have been mainly used While studies of TOPS using ultrasound have been to estimate condition-based growth rates over short limited, this technique has successfully been used to time scales in small fishes. However, further research visually monitor the reproductive status of broadnose and development is needed to determine if and how sevengill sharks (Daly et al. 2007) and maturity in the RNA:DNA ratios from tissue biopsies could be applied thornback ray Raja clavata and small-spotted catshark to sharks for estimating growth rates over many years, Scyliorhinus canicula (Whittamore et al. 2010). Al as required for demographic modeling.
though ultrasound studies have experienced difficul-ties in distinguishing between reproductive featureswithin an elasmobranch, coupling the use of ultra- CONCLUSION
sound with steroid hormone analysis can provide ameans to biochemically and visually assess reproduc- In the case of TOPS which are highly protected, tive biology, leading to a more accurate, and truly non- lethal sampling is not an option. As such, scientists have invasive, determination of this life history parameter.
generated innovative non-lethal alternatives for obtain-ing data on trophodynamics, age-growth, maturity, andreproductive status. This is best exemplified in the AGE, GROWTH, AND MORTALITY RATES
white shark Carcharodon carcharias, which is desig-nated as Vulnerable to Extinction by The International Age information forms the basis for the calculations Union for Conservation of Nature (IUCN; Fergusson et of growth rate, mortality rate, and productivity, making al. 2005), listed on Appendix II of the Convention on In- it one of the most important variables for estimating a ternational Trade in Endangered Species (CITES), and population’s status and assessing the risks associated fully protected in South Africa, Namibia, the USA, Aus- with its exploitation (Ricker 1975, Cortés 1998, Cailliet tralia, Israel, Italy, and Malta (Fergusson et al. 2005).
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