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Are all sharks man-eaters?
If asked about the ecology of cartilaginous fish, most people would probably identify them as rapacious carnivores. Many sharks are predators on fish, squid, and marine mammals -- although comparatively few are dangerous to humans. However, other cartilaginous fishes, such as skates, rays, and chimaeras, live on crustaceans and molluscs; they lack the daggerlike teeth of predatory sharks, and their teeth take the form of heavy crushing plates. (Incidentally, the sting in a stingray's tail is not used for attack or predation; it is purely for defense.) It may come as a surprise that several large sharks, like the basking shark featured at the top of this page, have small teeth and feed on plankton. As they swim in the open ocean, water is taken in through the mouth and strained through the gill slits. The largest shark of all, the whale shark, is such a plankton feeder.

The picture of the basking shark was posted to the alt.binaries.pictures.animals newsgroup by an unknown person. Thanks.

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Are all sharks man-eaters? If asked about the ecology of cartilaginous fish, most people would probably identify them as rapacious carnivores. Many sharks are predators on fish, squid, and marine mammals -- although comparatively few are dangerous to humans.

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The earliest sharks (class Chondrichthyes) first appeared in the Early Devonian about 400 million years ago, became quite prominent by the end of the Devonian, and are still successful today.

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The earliest fossil remains of fishlike vertebrates are too fragmentary to permit tracing the modern fishes precisely to their origins.

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Sharks and their kin are sometimes described as "living fossils," and they are indeed part of an ancient clade of vertebrates. Very recently, fossil denticles (scale-like bony pieces embedded in or on the skin) that resemble chondrichthyan scales in minute detail have been found in the Late Ordovician of Colorado (Sansom et al. 1996). More fossil scales that probably belonged to unknown sharks have been found in the Silurian. Aside from these finds, the oldest known complete, identifiable cartilaginous fish date from the middle Devonian. Sharks and their relatives were diverse in the Paleozoic, but most of them were not directly related to living sharks, belonging instead to side groups that died out in the Permian or Triassic. Living sharks, rays, and skates belong to a group known as the Neoselachii. This group may have appeared in the Triassic or even as early as the Permian, but the oldest well-understood neoselachian fossils areJurassic in age. By the Cretaceous, modern-looking sharks, sawfish, and skates -- such as this beautifully preservedCyclobatis longicaudatus, from the Upper Cretaceous of Lebanon -- had appeared.
Shark and ray teeth, and sometimes calcified vertebrae, are common fossils in many Cretaceous and Cenozoic deposits. One of the more famous fossil sharks is the Miocene Carcharodon megalodon, with serrated, triangular teeth (pictured on the background of this page) ranging up to 17.5 cm (7 inches) in length. An early reconstruction of Carcharodon from its teeth suggested that this shark reached 30 meters (100 feet) in length. However, this reconstruction was made only from the largest single teeth found, without taking into account the fact that shark teeth taper in size from the center of the mouth to the edges. A revised estimate of the size of Carcharodon puts its length at "only" 12 meters (40 feet) -- about twice the size of the largest great white sharks of today. Click here to view an image of the reconstructed jaws of Carcharodon, courtesy of the Smithsonian Institution.

Various holocephalian fish (those with an upper jaw fused to the braincase) appeared about the same time the earliest sharks did, in the Devonian. They probably included the ancestors of the living chimaeras and ratfish, as well as some other groups that are now extinct (traditionally classified in the Iniopterygii), but their relationships are not well understood.
Got some shark teeth? You may be able to identify them using the Key to Common Genera of Neogene Shark Teeth, by Robert W. Purdy, available from thedepartment of Paleobiology of the National Museum of Natural History.
We have pictures of hybodontid fossils from Ethiopia.

One of the most famous places to find fossil teeth of Carcharodon and other sharks, dating from the Miocene, is Calvert County, Maryland, USA. Find out more about Calvert County sharks -- and other fossils -- from the Maryland Geological Survey.

Sources:
Carroll, R.L. 1988. Vertebrate Paleontology and Evolution. W.H. Freeman and Company, New York.

Sansom, I.J., Smith, M.M., and Smith, M.P. 1996. Scales of thelodont and shark-like fishes from the Ordovician of Colorado. Nature 379 (15 February 1996): 628-630.

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Sharks and their kin are sometimes described as "living fossils," and they are indeed part of an ancient clade of vertebrates. Very recently, fossil denticles (scale-like bony pieces embedded in or on the skin) that resemble chondrichthyan scales in minute detail have been found in the Late Ordovician of Colorado (Sansom et al.

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Studies found that because Chondrichthyes live on water, they underwent less structural evolution. Chondrichthyes however developed a more cartilaginous composition.

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According to the fossil record, modern white sharks evolved sometime between 10 million and 4 million years ago, from the middle of the Miocene Epoch (23 million to 5.3 million years ago) through the first half of the Pliocene Epoch (5.3 million to 2.6 million years ago)

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White shark, ( Carcharodon carcharias), also called great white shark or white pointer, any member of the largest living species of the mackerel sharks (Lamnidae) and one of the most powerful and dangerous predatory sharks in the world. Starring as the villain of movies such as Jaws (1975), the white shark is much maligned and publicly feared. However, surprisingly little is understood of its life and behaviour.

Distribution

White shark populations are frequently centred in highly productive temperate coastal waters (that is, waters characterized by an abundance of fishes and marine mammals), such as off the coasts of the northeastern and western United States, Chile, northern Japan, southern Australia, New Zealand, southern Africa, and the Mediterranean. Some individual white sharks may travel far out to sea or into tropical waters, but field studies show that most return to these temperate feeding areas each year.

Body structure

White sharks are large bulky fishes with a body shaped like a blunt torpedo. They have a sharply pointed conical snout, large pectoral and dorsal fins, and a strong crescent-shaped tail. Only the belly of white sharks is whitish. They have a contrasting pattern of dark blue, gray, or brown on their back and sides. They are amazing hunters armed with strong muscles, good eyesight, and a keen sense of smell. In addition, their massive jaws are armed with large sharply pointed, coarsely serrated teeth. Each tooth is designed to cut flesh and can easily puncture and shatter bone. The largest fully grown white sharks do not exceed 6.4 metres (21 feet) in length. Most weigh between 680 and 1,800 kg (1,500 and 4,000 pounds), but some weighing more than 2,270 kg (about 5,000 pounds) have been documented.

Most fish are ectothermic, or cold-blooded, but white sharks have a complex circulatory system that conserves heat generated through the contraction of swimming muscles. This heat is distributed throughout the body to warm its critical regions, giving the white shark a body temperature higher than the temperature of the surrounding water. This adaptation, called regional endothermy (which is a type of warm-bloodedness), allows the animal to be active in water that may be too cold for other species of predatory sharks.

Behaviour

Feeding habits

Newborn white sharks feed on fishes and other sharks. As they reach adulthood, their prey includes sea turtles, seals, sea lions, porpoises, dolphins, and small whales. Prey is usually hunted by ambush, where the shark will attempt to rush the animal by surprise and inflict a sudden and massive fatal bite. Often this initial rush is so strong that the intense impact may send the prey out of the water or will send the shark into the air if it misses the target. The sharks will retire and wait for the prey to quickly die, giving rise to the terms bite and spit or bite and wait for this method of attack. White sharks are also opportunistic scavengers and will feed on the carcasses of whales and basking sharks; however, they are not indiscriminate.

Attacks on humans

In the areas where they are most common, white sharks are responsible for numerous unprovoked, and sometimes fatal, attacks on swimmers, divers, surfers, kayakers, and even small boats. A white shark tends to inflict a single bite on its human victim and then retreat. In many instances, however, the shark does not return for a second bite. If the victim suffers a moderate bite, he or she may have time to seek safety. In situations where a large bite occurs, however, serious tissue and organ damage may result in death. A review of white shark attacks off the western United States showed that about 7 percent of attacks were fatal, but data from other localities, such as South Africa, show fatality rates of more than 20 percent. Fatality rates as high as 60 percent have been recorded from attacks in the waters off Australia.

Many researchers maintain that attacks on humans stem from the shark's curiosity. In contrast, other authorities contend that these attacks may be the result of the shark mistaking humans for its natural prey, such as seals and sea lions. It is also possible that white sharks intend to attack humans where their normal prey may be scarce.

Social behaviour

Little is known about the social behaviour and natural history of the white shark. There appears to be no apparent social structure; however, there is evidence that some sharks may be territorial and assume dominance hierarchies around feeding areas. White sharks are largely solitary, but some pairs have been seen to travel together and associate for long periods of time. Some individuals may reside within feeding areas throughout the year, whereas other individuals may leave the feeding area and migrate widely. For example, some white sharks off California have been tracked to Hawaii, and some South African white sharks have been tracked to southern Australia and back.

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white shark | Size, Diet, Habitat, Teeth, Attacks, & Facts

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White shark, any member of the largest species of the mackerel sharks (Lamnidae) and one of the most powerful and dangerous predatory sharks in the world. Despite being much maligned and publicly feared, surprisingly little is understood of the white shark's life and behavior.

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Dr. Samuel H. Gruber broke new ground in the study of sensory physiology in sharks and over the course of a career lasting more than 50 years he published over 190 peer-reviewed papers on shark biology, ecology and behaviour, greatly advancing our understanding of these enigmatic creatures.

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Dr Samuel ('Sonny') Harvey Gruber passed away at his home with his family by his side on Thursday, 18 April 2019 at the age of 80. A true pioneer and one of the most influential figures in shark science, Dr Gruber made contributions to elasmobranch research that cannot be overstated. Called simply 'Doc' by most who knew him, he broke new ground in the study of sensory physiology in sharks and over the course of a career lasting more than 50 years he published over 190 peer-reviewed papers on shark biology, ecology and behaviour, greatly advancing our understanding of these enigmatic creatures.

One of his greatest contributions to the field was the co-founding of the American Elasmobranch Society (AES) in 1983, along with California State University Long Beach professor Dr Don Nelson. The AES has become the largest professional society of elasmobranch scientists on the planet. Another major achievement, and the one that Doc was most proud of, was the establishment of the Bimini Biological Field Station (aka the 'Shark Lab') in 1990, which moved shark research forward through novel scientific findings and by serving as a conveyor belt of competent and passionate shark researchers.

Doc was born in 1938 in Brooklyn, New York, to Claire and Sidney Gruber. His love for the ocean and sense of connection to it emerged strongly when the family moved to South Beach in Miami, Florida, shortly after the end of the Second World War. He quickly became an avid swimmer and high board diver, feeling very at home in and under the water. Doc would have the family driver take him to the shore as often as possible, where he would spend hours at the beach or fishing docks, fascinated by the weird and wonderful creatures the boats would bring in at the end of the day. On one such day he was so enthralled by his surroundings that he left a brand-new pair of shoes on the dock. This was the final straw for his parents, whose patience was already strained by frequent instances of misbehaviour. They decided that enough was enough and in 1953 they sent him to military school.

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Eulogy of Dr Samuel H Gruber | Save Our Seas Magazine

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Dr Samuel ('Sonny') Harvey Gruber passed away at his home with his family by his side on Thursday, 18 April 2019 at the age of 80. A true pioneer and one of the most influential figures in shark science, Dr Gruber made contributions to elasmobranch research that cannot be overstated.

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The earliest fossil evidence for sharks or their ancestors are a few scales dating to 450 million years ago, during the Late Ordovician Period.

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Shark evolution: a 450 million year timeline

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Evolving before trees and weathering five mass extinctions, sharks are true survivors.

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Dr. Eugenie Clark was a scientific pioneer who greatly contributed to people's knowledge of sharks and other fish, and who worked tirelessly to improve sharks' reputation in the public eye.

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The 'Shark Lady'

Dr. Eugenie Clark was a scientific pioneer who greatly contributed to people's knowledge of sharks and other fish, and who worked tirelessly to improve sharks' reputation in the public eye. Image courtesy of Mote Marine Laboratory and Aquarium.

Few women, let alone those of Japanese American descent, were working in the male-dominated field of marine biology shortly after World War II. Dr. Eugenie Clark changed all that. A scientific pioneer who greatly contributed to people's knowledge of sharks and other fish, Clark worked to improve sharks' reputation in the public eye. Perhaps more importantly, she challenged the stereotypes surrounding women in science by proving that women had much to contribute to the scientific community.

Early Life and Education

Born in New York City on May 4, 1922, Clark learned to swim before the age of two. She often credited her childhood visits to the New York Aquarium as fostering her passion for the aquatic world, together with her Japanese heritage and the central role of the sea in Japanese culture.

Working to pay her way through Hunter College in the early 1940s, Clark studied ichthyology, the branch of biology devoted to the study of fish. Following graduate research in the South Pacific, she took a job at the Scripps Institution of Oceanography in San Diego, California. Scripps is where she learned to scuba dive, a skill that Clark used continuously throughout her career in ocean research.

From 'Dr. Clark' to 'The Shark Lady'

In 1950, Clark earned her PhD from New York University with research on the live-bearing reproduction of platys and swordtail fish. Later that year, as a Fulbright Scholar, Clark conducted research in the virtually unexplored waters of the Red Sea from the Al-Ghardaqah Marine Biological Station in Egypt. Her memoir of her time there, Lady with a Spear (1953), was an international bestseller.

Clark discovered several fish species, among them Trichonotus nikii, a Red Sea sand diver named after her son Nikolas, and the Red Sea Moses sole ( Pardachirus marmoratus), which produces a natural shark repellent. Her passion, however, was studying sharks and dispelling myths and fears about them through education. It was Clark who discovered that some shark species do not have to swim continuously to breathe. Her work with "sleeping sharks" in Mexico was a tremendous advancement in the understanding of shark behavior and biology. Her efforts earned her the unofficial but widely used name of "the Shark Lady".

Clark's career, which spanned half a century, included work with the New York Zoological Society (now the Wildlife Conservation Society), the American Museum of Natural History in New York, and Woods Hole Oceanographic Institution in Massachusetts. In 1955, she founded the Cape Haze Marine Laboratory in Sarasota, Florida. Known today as Mote Marine Laboratory, its focus has expanded from shark research to include wild fisheries, coral reef restoration, marine mammals, marine biomedical research, and related fields.

In 1968, Dr. Clark joined the faculty of the University of Maryland, where she taught marine biology until her retirement in 1992. Clark lectured across the globe to promote greater understanding of sharks and the marine environment, and also wrote extensively for National Geographic and other publications.

A Lasting Legacy

Eugenie Clark made her last dive in June 2014. She died on February 25, 2015, at the age of 92. She leaves a legacy that will inform her fellow scientists and ocean lovers for generations to come. On March 16, 2015, the U.S. Congress posthumously honored and recognized Dr. Clark for her efforts to understand and preserve the ocean realm.

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Dr. Clark received numerous honors and awards during her long career, including a 1996 Emmy Award for her underwater films. In 1989, she was inducted into the Maryland Women's Hall of Fame.

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american museum of natural history in new york

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national oceanic and atmospheric administration

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Few women, let alone those of Japanese American descent, were working in the male-dominated field of marine biology shortly after World War II. Dr. Eugenie Clark changed all that. A scientific pioneer who greatly contributed to people's knowledge of sharks and other fish, Clark worked to improve sharks' reputation in the public eye.

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Chondrichthyes Population in the Present

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Chondrichthyes Population in the Present

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Some chondrichthyans have life-history traits (slow growth rates, late maturities, low fecundities, and long gestation periods) which make them less resilient to fishing, even at low levels of exploitation (Frisk et al., 2001). Recent assessments, for example, estimated that one-quarter of the world's chondrichthyans were threatened with extinction as a result of overfishing

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Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San José, Costa Rica

Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica

Escuela de Ciencias Exactas y Naturales, Universidad Estatal a Distancia, San José, Costa Rica

Museo de Zoología, Universidad de Costa Rica, San José, Costa Rica

Laboratório de Ictiologia, Departamento de Zoologia e Botânica, UNESP, Universidade Estadual Paulista "Júlio de Mesquita Filho", São José do Rio Preto, Brazil

Biomolecular Laboratory, Center for International Programs, Universidad VERITAS, San José, Costa Rica

Sala de Colecciones Biologicas, Facultad de Ciencias del Mar, Universidad Catolica del Norte, Antofagasta, Chile

Changing Ocean Research Unit, Institute for the Oceans and Fisheries, The University of British Columbia, Vancouver, BC, Canada

Understanding key aspects of the biology and ecology of chondrichthyan fishes (sharks, rays, and chimeras), as well as the range of threats affecting their populations is crucial given the rapid rate at which some species are declining. In the Eastern Tropical Pacific (ETP), the lack of knowledge, unreliable (or non-existent) landing statistics, and limited enforcement of existing fisheries regulations has hindered management and conservation efforts for chondrichthyan species. This review evaluated our current understanding of Costa Rican chondrichthyans and their conservation status. Specifically, we (1) provide an updated checklist on the species richness, habitat use, and distribution patterns, (2) summarize the most relevant chondrichthyan studies (scientific publications, theses, and official technical reports), (3) identify knowledge gaps, (4) discuss fisheries-related threats, and (5) highlight the management challenges and research needs to effectively protect their populations. A total of 99 chondrichthyan species are formally recorded in Costa Rican waters, from which 15% are threatened with extinction and 41% are "Data Deficient" based on the IUCN (International Union for Conservation of Nature) Red List. A total of 121 studies were published between 1891 and 2017; 82% in the Pacific (24% from Isla del Coco) and only 18% from the Caribbean Sea. These results highlight the need to redirect research efforts on specific taxonomic groups and geographic regions (i.e., Caribbean). Based on our review, improving the quality and quantity of fisheries landing statistics, as well as determining the degree of overlap between chondrichthyans and Costa Rican fisheries remains a priority. We proposed an adaptive management framework for chondrichthyan fisheries in data-poor countries where management goals/targets are clearly defined. This framework could strengthen the conservation of chondrichthyan populations in Costa Rica and the region.

Introduction

In many regions, chondrichthyan populations (sharks, rays, and chimeras) have been reduced to unsustainable levels ( Ward-Paige et al., 2010; Davidson et al., 2016; Spaet et al., 2016), raising global concern over their conservation status ( Dulvy et al., 2014, 2017). Some chondrichthyans have life-history traits (slow growth rates, late maturities, low fecundities, and long gestation periods) which make them less resilient to fishing, even at low levels of exploitation ( Frisk et al., 2001). Recent assessments, for example, estimated that one-quarter of the world's chondrichthyans were threatened with extinction as a result of overfishing ( Dulvy et al., 2014; Davidson et al., 2016). Moreover, Dulvy et al. (2014) highlighted the current lack of information on many chondrichthyans, particularly batoids (rays and skates), as almost half of the species assessed were listed as "Data Deficient."

While overfishing has been identified as the main driver of chondrichthyan population declines, habitat loss/degradation, and climate change can also play significant roles ( García et al., 2008; Chin et al., 2010; Dulvy et al., 2014). Sawfishes (Pristidae) and freshwater stingrays (Potamotrygonidae), for instance, have a greater affinity for freshwater and estuarine habitats ( Carrier et al., 2010; Norton et al., 2012), all of which are largely affected by human practices (e.g., agriculture, aquaculture, hydroelectric power stations), and/or rapid and unplanned coastal/riverine development ( Peverell, 2009; Hossain et al., 2015). Moreover, many coastal elasmobranchs (sharks and rays) utilize a wide range of inshore habitats during their early stages as feeding, reproduction, and/or nursery grounds ( Heupel et al., 2007; Jirik and Lowe, 2012; Tobin et al., 2014; Chapman et al., 2015). In addition, climate-driven changes in the physical, chemical, and biological conditions of chondrichthyan habitats have the potential to affect their distribution, movement, feeding ecology, reproduction, and growth ( Chin et al., 2010; Dulvy et al., 2014; Pistevos et al., 2015). Therefore, understanding the range of anthropogenic and environmental drivers that influence (directly or indirectly) chondrichthyan populations is crucial to designing more effective management approaches to improve their conservation.

In many countries from the Eastern Tropical Pacific (ETP), the current status of chondrichthyans is unclear ( Rojas et al., 2000; Dapp et al., 2013; Clarke et al., 2017). Moreover, the lack of biological and ecological data, unreliable (or non-existent) landing statistics, and limited enforcement of existing management regulations has hindered conservation efforts for sharks, rays, and chimeras that are currently threatened in this region. In Costa Rica, for example, reconstructed shark catches were estimated to be 83% higher than FAO statistics, while national landing statistics were 60% lower than FAO landing statistics ( Trujillo et al., 2015). Moreover, illegal fishing activities, even in remote Marine Protected Areas (MPAs) and UNESCO World Heritage Sites such as Cocos ( Arias et al., 2014; White et al., 2015; López-Garro et al., 2016) and Galapagos Islands ( Sills, 2017) are threatening the future of migratory shark stocks within the ETP.

Over the past decades, marine research in Costa Rica has grown considerably ( Wehrtmann and Cortés, 2009), yet chondrichthyan science continues to be overlooked. Given the rapid rate at which some species are declining, their vulnerability to increasing market demands (especially for their fins) and the uncertainty about the distribution and status of the ETP chondrichthyan stocks ( Dent and Clarke, 2015; Davidson et al., 2016), it is essential to (i) identify knowledge gaps and establish research priorities at a regional scale, (ii) assess non-listed and data-deficient species, and (iii) bridge the gap between science and policy. This review evaluated the current knowledge and conservation status of Costa Rican chondrichthyans. Specifically, we (1) provide an updated checklist on the species richness, habitat use and distribution patterns, (2) summarize the most relevant chondrichthyan studies (scientific publications, theses, and official technical reports), (3) identify knowledge gaps, (4) discuss fisheries-related threats, and (5) highlight the management challenges and research needs to effectively protect their populations. Moreover, we proposed an adaptive management framework for chondrichthyan fisheries in Costa Rica, which may be applicable to other data-poor countries from the ETP.

Methods

Updated Checklist: Species Richness and Distribution Patterns

Diversity and distribution data for chondrichthyans in Costa Rican waters were obtained from a detailed review of available scientific data, species occurrence records, and fish collections (e.g., Bussing and López, 2009; Robertson and Allen, 2015; Robertson and Van Tassell, 2015). Species occurrence records were obtained by querying the database FishNet2 ( http://www.fishnet2.net/aboutFishNet.html) and the digital catalog of the fish collection of the Museo de Zoología of the Universidad de Costa Rica (UCR). Specimens from UCR were revised and re-identified. Our search resulted in a checklist of chondrichthyan species with confirmed occurrence records (i.e., species formally recorded in the literature and/or with voucher specimens collected in Costa Rica) as well as those expected to occur in Costa Rica (based on known or postulated distributions; i.e., species with wide distribution ranges that may include Costa Rican waters, but for which there are still no formal records). This checklist was arranged by order and family following Eschmeyer and Fong (2017), and is provided in Appendix I in Supplementary Material. The following information for each species is provided: valid scientific name with author(s) and year of description, following Eschmeyer et al. (2017); popular, technical, and/or vernacular names in English (En) and Spanish (Sp), following Robertson and Allen (2015), Robertson and Van Tassell (2015), and Froese and Pauly (2017); current known geographical distribution, depth range and habitat use following Robertson and Allen (2015), Robertson and Van Tassell (2015), Weigmann (2016), and Froese and Pauly (2017); conservation status, according to the International Union for Conservation of Nature (IUCN) Red List criteria ( IUCN, 2017); and relevant literature [relatively recent references arbitrarily considered by us to have taxonomic and/or distributional value by providing short diagnosis, identification keys, illustrations, and/or distribution (geographical and depth) information, not mere usage of the specific names].

Literature Search of Chondrichthyan Studies in Costa Rica

Detailed searches for scientific publications, theses, technical reports, and books related to chondrichthyans in Costa Rican waters were conducted until November 2017, using Google Scholar, SIDUNA (Documentary Information System of the National University), Shark-References ( http://shark-references.com/), and SIBDI (System of Libraries, Documentation, and Information from Universidad de Costa Rica). The online search was based on the following keyword combinations: "[(sharks or shark) AND (rays or ray) AND (chimera or chimeras) AND (elasmobranch or elasmobranchs) AND (chondrichthyans or chondrichthyes) AND Costa Rica]." This search identified 526 studies that contained any of the keyword combinations. We filtered the resulting publication list to exclude studies that were not conducted in Costa Rica and did not include at least one chondrichthyan species, for a final publication list of 121 studies. To determine the current state of knowledge and general information gaps, chondrichthyan studies were classified in one of the following topics: (i) fisheries and management, (ii) taxonomy and identification, (iii) distribution and abundance patterns, (iv) parasites, (v) life-history, (vi) feeding ecology, (vii), genetic connectivity (viii) paleontology, (ix) climate change, (x) contaminants, (xi) spatial ecology, and (xii) tourism. To examine spatial and temporal trends in chondrichthyan studies, we analyzed the location of the study (Pacific and Caribbean coast; Cocos Island) and the frequency of publications per year (year/topic). For each study, we also determined the conservation status of target species based on the IUCN Red List criteria ( IUCN, 2017).

Results and Discussion

Chondrichthyan Diversity

There are 99 chondrichthyan species formally recorded in the literature and/or with voucher specimens collected within Costa Rican waters (see Table 1 and Appendix I in Supplementary Material). These species are grouped in 2 subclasses (Holocephali and Elasmobranchii), 12 orders, 34 families, and 50 genera. The subclass Holocephali (chimeras) is represented by six species and there are 93 species included in the subclass Elasmobranchii (sharks and rays). Two orders of elasmobranchs, Carcharhiniformes (ground sharks), and Myliobatiformes (stingrays), have the largest number of species within Costa Rican waters, with 27 species each (see Table 1). From these, Carcharhinidae (requiem sharks) and Urotrygonidae (round rays) are the most diverse families, with 16 and 7 species, respectively. A complete list of the formally recorded chondrichthyan species from Costa Rica, as well as additional information on their distribution and habitat preferences, is provided in Appendix I in Supplementary Material.

Distribution Patterns and Habitat Preferences

Of the total number of chondrichthyan species formally reported in Costa Rican waters (99 species), 88% are known to occur in the Pacific Ocean and 24% in the Caribbean Sea (Table 1). Twelve of these species have been reported on both sides of the Panamanian isthmus (i.e., there are anfiamerican species). The number of species reported for the Costa Rican Pacific represents ~58% of the total number of species known to occur in the North Eastern Pacific Ocean (i.e., 151 species, sensu Weigmann, 2016); whereas the number of species reported for the Caribbean Sea represents about 11% of the total number of species known to occur in the North Western Atlantic Ocean (i.e., 216 species, sensu Weigmann, 2016). Such discrepancies reflect considerable differences in the sampling effort as well as the relative lack of basic and applied studies assessing the species richness and population status of chondrichthyans in Costa Rica, particularly in the Caribbean Sea ( Bussing and López, 2009).

All chondrichthyan species known to occur in Costa Rica show marine habits, 39% are found in both marine and estuarine/brackish environments, and only 4% have some affinity to freshwater environments (Appendix I in Supplementary Material). Most species (54%) are restricted to shallow waters (i.e., 0-200 m depth); 6 of which can also be found in waters deeper than 1000 m. Twenty-eight species are usually found at depths between 0 and 1000 m (Appendix I in Supplementary Material). The remaining 18 species are restricted to deep waters, with 16 species usually found between 200 and 1000 m, and 2 species restricted to waters deeper than 1000 m. Interestingly, most of these deepwater species (10 species) were formally reported for Costa Rica within the last 4 years (2014-2017), three of which were formally described (they represented newly discovered species) during this same period from type specimens collected in Costa Rica ( Chimaera orientalis Angulo et al., 2014; Etmopterus benchleyi Vásquez et al., 2015; and Notoraja martinezi Concha et al., 2016). The increase in the number of recently described deep water species in Central America suggests that chondrichthyan richness may increase as research efforts in the region continue.

Coastal chondrichthyans represent ~92% of the formally reported species (79 species in the Pacific and 21 in the Caribbean). Seventy-one of these coastal species are restricted to inshore and/or continental shelf habitats (i.e., there are "obligate" inshore species) and 20 are both inshore (coastal) and offshore (oceanic) species (Appendix I in Supplementary Material). The remaining eight species are "obligate" offshore species, and all of them are present in the Pacific, whereas only three are present in the Caribbean. Pelagic species represent ~47% (43 species in the Pacific and 15 in the Caribbean), whereas 81% exhibit demersal habits (69 species in the Pacific and 18 in the Caribbean; Appendix I in Supplementary Material).

Approximately 35% of the reported species are known to use or depend, in greater or lesser extent, on reef environments (31 species in the Pacific and 9 in the Caribbean), whereas 78% are typically found in "muddy" (estuaries and mangroves) environments (65 species in the Pacific and 19 in the Caribbean; Appendix I in Supplementary Material). These findings highlight the importance of estuarine and reef habitats to chondrichthyans, either as nursery, reproductive, and/or feeding grounds. However, these inshore habitats are also the most susceptible to human degradation and climate change ( Wehrtmann and Cortés, 2009; Jones and Cheung, 2017).

Broad Biogeographic Relationships

Most chondrichthyan species reported for Costa Rica have wide geographical distribution ranges. Forty-eight species are endemic to the ETP; 24 species are circumglobal; 7 species are endemic to the Western Atlantic Ocean; 6 species have distributions that include the entire Indo-Pacific Ocean; 4 species have distributions on the entire Atlantic Ocean; 4 species are found in both the Eastern Pacific and Western Atlantic Oceans; 3 species are reported for the entire Pacific Ocean; and one species is known to occur in both Atlantic and southwest Indian Oceans (Appendix I in Supplementary Material). In the ETP, Costa Rica represents the northern limit of the distribution range for a total of 7 species [i.e., Chimaera orientalis; Gymnura crebripunctata (Peters 1869); Notoraja martinezi; Squatina armata (Philippi 1887); Tetronarce peruana ( Chirichigno, 1963); Tetronarce tremens ( de Buen, 1959); and Urobatis pardalis ( Del Moral-Flores et al., 2015a)], and also represents the southern distribution limit for the spotted ratfish Hydrolagus colliei ( Lay and Bennett, 1839) and the denticled round ray Urotrygon cimar ( López and Bussing, 1998; Angulo et al., 2014; Robertson and Allen, 2015).

Expected Species Richness

Given the current distribution of chondrichthyans in the Pacific and Atlantic coastlines of Latin America, ~182 species are expected to occur in Costa Rican waters, which means an increase of 84% in the total number of reported species. Based on these estimations, Costa Rica would have ~66 and 51% of the chondrichthyan diversity reported in the North-Eastern Pacific and North Western Atlantic Oceans, respectively ( Weigmann, 2016). These values would be more in line with the actual expectations of chondrichthyan diversity in this region, similar to reports for reef and coastal fish assemblages ( Bussing and López, 2009; Robertson and Allen, 2015; Robertson and Van Tassell, 2015). The large discrepancy between expected and reported species known to occur in Costa Rica reflect the need for a profound reassessment of the diversity, geographical distribution, and habitat use patterns of chondrichthyans, both at local and regional scales. Research on poorly studied environments such as open waters and the deep sea remains a priority.

Conservation Status

Fifteen chondrichthyan species reported for Costa Rica are threatened with extinction (Table 2). The lesser electric ray Narcine bancroftii ( Griffith and Smith, 1834), the smalltooth sawfish Pristis pectinata ( Latham, 1794), and the largetooth sawfish Pristis pristis ( Linnaeus, 1758) are listed as "Critically Endangered," whereas the Scalloped hammerhead Sphyrna lewini ( Griffith and Smith, 1834) and the great hammerhead Sphyrna mokarran ( Rüppell, 1837) are listed as "Endangered" based on the IUCN Red List ( IUCN, 2017). The remaining 11 species are listed as "Vulnerable" (see Table 2; IUCN, 2017). In addition, 23 chondrichthyan species are listed as "Near Threatened" (i.e., they may become endangered in the near future) and 11 species are listed as "Least Concern" (i.e., they are widespread and abundant, with a lower risk to become endangered in the near future). What is most concerning, however, is that 41% of the species known to occur in Costa Rica are "Data Deficient" (i.e., inadequate information to assess a species extinction risk based on distribution and population status) (Table 2), which could mean that the number of threatened species may be greater than expected. This highlights the need to generate information on "Data Deficient" species that may help assess their population status.

Studies on Chondrichthyans in Costa Rican Waters

Based on our literature search, the total number of publications ( n = 121) on chondrichthyans increased in the mid 1990s; only two studies were published before 1960 (Figure 2). Interestingly, after 2008 the number of studies doubled ( n = 70), highlighting the growing interest in this group. Three-quarters of studies were scientific publications, 11% books, 9% theses, and 5% official technical reports. Only five of the 10 theses published in Costa Rica focused on sharks, rays, or chimeras; the remaining ones only mentioned or included species lists. Most books ( n = 10) were published as identification guides with general descriptions of common elasmobranch species.

About half of the studies analyzed were on elasmobranchs (37% on sharks, 12% on rays), and less than 1% on chimeras. Only 72% of these studies were conducted in Costa Rican waters ( n = 87), whereas 28% were part of regional or global-scale assessments. Elasmobranchs have been studied more intensively in the Pacific than in the Caribbean (Table 3). Only three studies focused on chimeras. Most studies from the Pacific of Costa Rica were conducted in Isla del Coco (an isolated volcanic island ~500 km from Puntarenas; see Figure 1) and the Golfo de Nicoya, a large and highly productive tropical estuary located in the central Pacific. This could be attributed to the biological importance of Isla del Coco as a marine biodiversity hotspot, a World Heritage site and a center of endemism in the ETP ( Wehrtmann and Cortés, 2009), as well as to the ecological and economic importance of the Golfo de Nicoya in terms of fisheries and food security ( Nielsen Muñoz and Quesada Alpízar, 2006; Wehrtmann and Cortés, 2009).

Table 3. Number of studies on chondrichthyan fishes conducted in Costa Rican waters ( n = 87).

In Costa Rica, chondrichthyan studies have followed three major research areas: (i) fisheries, (ii) taxonomy, and (iii) distribution patterns (Figure 3). These areas accounted for 75 studies (62% of the total number of studies analyzed). Fisheries was the category with most studies ( n = 28), and they generally focused on relatively short-term (<10 year) surveys of the elasmobranch by-catch associated with coastal ( López-Garro et al., 2009; López-Garro and Zanella, 2015; Clarke et al., 2016) and pelagic fisheries ( Whoriskey et al., 2011; Dapp et al., 2013), as well as illegal fishing activities inside MPAs ( Arias and Pressey, 2016; López-Garro et al., 2016). Taxonomical studies, including species descriptions and new records within Costa Rica waters were also an important category ( Angulo et al., 2014; Del Moral-Flores et al., 2015a, b; Concha et al., 2016). This reinforces the need to conduct basic taxonomic studies that may increase the existing chondrichthyan diversity in these waters. Approximately 31% of the reviewed studies included categories as diverse as parasites ( n = 11), life-history traits ( n = 8), feeding ecology ( n = 7), connectivity ( n = 6), and paleontology ( n = 5). Chondrichthyan studies evaluating tourism, spatial ecology, contaminants, and climate change were underrepresented, and accounted for less than 8% (Figure 3).

Our review highlighted the lack of studies on deep water (>1000 m) and Caribbean chondrichthyan populations. Given the increasing exploitation of deep water resources ( Wehrtmann et al., 2012; Clarke et al., 2016), there are some concerns over the ability of chondrichthyans to sustain high fishing levels in these environments ( Simpfendorfer and Kyne, 2009). Similarly, less effort has been given to study Caribbean chondrichthyans in Costa Rica, where reported landings account for less than 4% of national landings ( Fournier and Fonseca, 2007). Therefore, if more landings data are collected from the Caribbean and/or deep-water fisheries, they may revealed previously unrecorded species and conservation priorities.

Chondrichthyan Fisheries in Costa Rica

Fishing is perhaps the most significant and widespread threat affecting chondrichthyans in Costa Rica ( Whoriskey et al., 2011; Dapp et al., 2013; Davidson et al., 2016), as the unique life-history traits of some species, poor landing statistics and limited enforcement make them particularly vulnerable to overexploitation ( Frisk et al., 2005; Arias et al., 2014; Trujillo et al., 2015). In Costa Rica, small-scale (e.g., gillnet and bottom long-line fisheries) and shrimp trawl fisheries catch a large number of sharks and rays in coastal environments ( Herrera-Ulloa et al., 2011; Clarke et al., 2016, 2017). In contrast, pelagic longline and purse seine fisheries catch several shark species in the open ocean as their main target or as bycatch ( Rojas et al., 2000; Arauz et al., 2007). While coastal fisheries capture chondrichthyans with a wide range of sizes and life history strategies, pelagic fisheries tend to catch larger, more vulnerable species ( Whoriskey et al., 2011; Dapp et al., 2013) (Figure 4). The higher proportion of threatened species in pelagic fisheries may result from differences in gear selectivity and the decline of top predators from coastal waters. Moreover, the number of threatened species caught by coastal fisheries may be higher than current assessments indicate due to the large proportion of batoids and carcharhinids categorized as "Data Deficient" (Figure 4).

Figure 4. Number of species per family captured by small-scale, trawl, and pelagic fisheries in Costa Rica. Data deficient and not assessed species are represented in blue, non-threatened species are represented in green and threatened species are represented in red (IUCN Red List categories). Species catch data were obtained from the following studies: Arauz et al. (2007), Benavides et al. (2014), Bystrom (2015), Campos (1986), Clarke et al. (2016), Dapp et al. (2013), López-Garro et al. (2009), López-Garro and Zanella (2015), Rojas et al. (2000), and Whoriskey et al. (2011).

Small-Scale Fisheries (SSF)

In Costa Rica, SSF are highly dynamic, with both spatial and temporal variations in fishing effort along the coastline ( Salas et al., 2007; Araya, 2013). These fisheries operate mainly in the Pacific and land up to 20 species of sharks and rays (Figure 4), some of which are targeted during reproductive aggregations and in nursery grounds ( López-Garro et al., 2009; López-Garro and Zanella, 2015; Clarke et al., 2017). Shark catches in SSF are an important source of low-cost protein for the national consumer market ( Herrera-Ulloa et al., 2011). Therefore, SSF have the potential to greatly impact many elasmobranchs, as documented by Amador (2010) who found that catches of longtail stingray Hypanus longus ( Garman, 1880) declined by 60% between 2005 and 2007. Moreover, since the early 2000s, declines in shark meat landings drove an increase in shark meat imports from Belize, Taiwan, and Panama ( Dent and Clarke, 2015).

Pelagic Fisheries

Pelagic fleets operate mainly in the Pacific Economic Exclusive Zone (EEZ) of Costa Rica, targeting mahi-mahi, swordfish, and large pelagic sharks with longlines and purse seines ( Rojas et al., 2000; Arauz et al., 2007; Whoriskey et al., 2011; Dapp et al., 2013). These fisheries land up to 35 species of sharks and rays (Figure 4). Between 1988 and 1997 pelagic sharks represented over 20% of the national landings volume ( Rojas et al., 2000; Bonilla and Chavarría, 2004), while shark catch rates declined over 60% ( Kyne et al., 2012; Dapp et al., 2013). Similarly, the abundance of S. lewini at Isla del Coco declined by ~45% between 1993 and 2013 ( White et al., 2015).

Most sharks caught in pelagic fisheries are exported, and therefore, trends in exportation records may provide additional information about pelagic shark fisheries. During 2000-2011, Costa Rica was the sixth largest exporter of shark meat products, the eighth largest exporter of shark fins in terms of volume, and seventh in terms of value ( Dent and Clarke, 2015). Between 2000 and 2011, Canada, China, Hong Kong, Indonesia, Malaysia, Singapore, and Taiwan imported an average of 8.9 million USD in shark fins a year from Costa Rica ( Dent and Clarke, 2015). However, Costa Rica only reported an average export of 1.9 million USD in shark fins during the same period. After 2011, Costa Rica fell from the sixth largest exporter to the 28th due to declining catches ( Dent and Clarke, 2015). There are large discrepancies between the landings and exports recorded by the national fishery agency and FAO estimates (Figure 5), yet, the factors driving these discrepancies remain uncertain and require further attention ( Dent and Clarke, 2015; Trujillo et al., 2015).

Figure 5. Fisheries landings and exports of shark products in Costa Rica during 2000-2011. (A) Landings reported by FAO and landings reported by the Costa Rican Fishing Institute (INCOPESCA). (B) Shark meat exports reported by Dent and Clarke (2015) and shark meat landings (INCOPESCA). (C) Shark fin landings estimated by Dent and Clarke (2015) and shark fin landings (INCOPESCA).

The foreign pelagic fleet has the highest fishing capacity and usually targets mahi-mahi, swordfish, and sharks ( Siu and Aires-Da-Silva, 2016). From 2004 to 2010, an average of 36 foreign vessels from China, Cambodia, Indonesia, Panama, Georgia, and the United States landed their catch in Costa Rica ( Siu and Aires-Da-Silva, 2016). Siu and Aires-Da-Silva (2016) reported that due to increased regulations, foreign vessels have not landed in Costa Rica since 2015. However, the lack of information on landings in private docks and fishing effort in the open seas makes it unclear whether foreign fishing vessel activity has actually stopped ( Dent and Clarke, 2015). Moreover, it is also important to consider that there may be foreign fishing fleets that operate within Costa Rican waters, but land their catch elsewhere. Automatic Identification Systems (AIS) tracking data is being increasingly used to detect illegal fishing, trans-shipments and fisheries dynamics, and therefore, represent a powerful management tool that may strengthen the conservation of shark species in the ETP ( Robards et al., 2016; Kroodsma et al., 2017; White et al., 2017).

Trawl Fisheries

Shallow and deepwater bottom trawl fisheries also operate mainly in the Pacific, catching ~34 species of elasmobranchs as bycatch (Figure 4) ( Clarke et al., 2016). Although shark and ray bycatch is not recorded, catch reconstructions estimate that a total of 7.7 tons of bycatch were caught per ton of shrimp between 1950 and 2010, 85% of which was discarded ( Trujillo et al., 2015). Large, slow moving demersal species are the most susceptible to bottom trawling, with the brown smoothhound Mustelus henlei ( Gill, 1863), velez ray Rostroraja velezi (Chirichigno F. 1973), southern banded guitarfish Zapteryx xyster ( Jordan and Evermann, 1896), and panamic stingray Urotrygon aspidura ( Jordan and Gilbert, 1882) comprising over 70% of catches from 2008 to 2012 ( Clarke et al., 2016). At a population level, a recent ecological risk assessment revealed that S. lewini, the prickle shark Echinorhinus cookei ( Pietschmann, 1928) and H. longus were the most vulnerable elasmobranch species ( Clarke et al., 2017). However, Clarke et al. (2016) found these species were no longer an abundant component of the elasmobranch bycatch in recent years (2008-2012).

Management Challenges

Data Deficiency

A common issue that challenges fisheries management in the ETP is the poor quality and quantity of landing statistics and catch-effort data ( Salas et al., 2007). In Costa Rica, for example, if recorded, landings are typically grouped into broad commercial categories that do not allow us to detect trends even at broad taxonomic levels such as "shark," "ray," or "elasmobranch" ( CGR, 2007). Factors that hinder the collection of adequate landings statistics vary among fisheries. In SSF, there are not enough inspectors to record landings at all the small landing sites scattered across the entire coastline ( Salas et al., 2007). Moreover, a high percentage of catches do not enter the commercial value chain because they are consumed locally, used as bait or discarded ( Salas et al., 2007). In contrast, landings from pelagic fisheries are concentrated in four main ports (Figure 1), where inspectors from the Costa Rican fishing institute regularly monitor shark landings. However, the collection of catch/effort data is hampered by the a lack of onboard observers, distant fishing grounds, long fishing trips, illegal fishing, high-grading, and discarding ( Rojas et al., 2000; Arauz et al., 2007; López-Garro et al., 2016).

In countries like Costa Rica, the costs associated with the management and data collection for SSF would exceed the value of the catch, and therefore, traditional approaches may not be feasible ( Salas et al., 2007). In this case, participatory landings data collection should be deployed in coastal fisher communities to develop extrapolated catch figures for SSF using total effort estimates (e.g., number of fishers). Engaging fisher communities in landings data collection may also be a transparent and socially responsible way to raise local capacity, contribute to decision making and in the process of adaptive management. Large revenues generated from pelagic fisheries could be used to offset costs of deploying these SSF processes and allow the creation of artisanal coastal fisheries management plans.

Data deficiency in national large-scale pelagic fisheries can be offset through the collection and analysis of information by regional fisheries management organization such as the Inter-American Tropical Tuna Commission (IATTC) ( IATTC, 2016; Griffiths et al., 2017). Given the wide-ranging nature of pelagic sharks within the ETP, targeted species and/or populations may benefit from a regional approach to data collection, analysis, and management. For instance, a recent ecological risk assessment conducted by the IATTC revealed that 13 of the 18 highly vulnerable species were sharks ( Griffiths et al., 2017). Yet, management measures have only been implemented for the silky shark Carcharhinus falciformis ( Müller and Henle, 1838) and devil rays Mobula spp. ( IATTC, 2016), highlighting the need to improve management actions for many species that are currently at risk.

Weak Fisheries Management Framework

Although the existing statistical and biological information is not sufficient to adequately assess the status of many of the chondrichthyan stocks within the ETP, scientific, and traditional ecological knowledge indicate that shark landings in this region are decreasing while fishing effort is increasing ( Whoriskey et al., 2011; Kyne et al., 2012; Dapp et al., 2013; Dent and Clarke, 2015). Declines in shark landings have led to concerns over the impacts of fisheries on shark populations within the ETP ( Arauz et al., 2007; Whoriskey et al., 2011; Clarke et al., 2017). Identified drivers of overfishing include corruption and conflicts of interest within the fisheries management agency, weak management frameworks, fleet overcapacity, lack of enforcement, and illegal fishing activities ( CGR, 2007; Arias and Pressey, 2016).

In Costa Rica the industrial fishing sector has a majority representation on the board of directors in charge of fisheries management, potentially driving private interests. Moreover, a lack of resources and capacity severely hinder the implementation of existing fisheries management legislation. NGOs and environmental government organizations, however, have allowed the development of sustainable fisheries projects, and raise awareness about shark finning and illegal fishing in MPAs.

Lack of Enforcement of International Regulations

Implementation is also an issue with international treaties ratified by Costa Rica, such as CITES and CMS (Convention on the Conservation of Migratory Species of Sharks), which promote the protection and conservation of threatened elasmobranch species ( Davidson et al., 2016). At least six threatened shark species ( S. lewini, S. zygaena, S. mokarran, C. longimanus, C. falciformis, and Alopias pelagicus) currently exported from Costa Rica to Hong Kong are regulated by Appendix II of the CITES ( Davidson et al., 2016). Moreover, both Pristis pristis and P. pectinata are included in Appendix I of CITES, which prohibits the extraction and international trade of specimens. However, there is evidence that shark fin traders are still exporting mislabeled and unidentified shark fins, including those of prohibited species ( Abercrombie and Hernandez, 2017). Therefore, illegal shark trade could be reduced by increasing the transparency along the chain of custody for shark products. Building capacities to identify and quantify elasmobranch products throughout the supply chain is also imperative to enforce and comply with national and international regulations ( Abercrombie and Hernandez, 2017).

Management and Research Needs

Adaptive Management Framework

From a biological standpoint, there are many information gaps that must be filled to better guide management and conservation efforts in Costa Rica and other data-poor countries from the ETP. Although the road ahead may seem overwhelming, a useful starting point might be to identify vulnerable species through data-poor ecological risk assessments and implement precautionary management measures. Subsequently, a monitoring program should be established to assess the effectiveness of these management actions in reaching previously defined management targets (Figure 6).

An adaptive management blueprint for a data-poor situation can be illustrated by the Costa Rican shrimp trawl fishery. A recent risk assessment identified S. lewini as one of the most vulnerable bycatch species ( Clarke et al., 2017). Based on our knowledge of the interaction of S. lewini with coastal and pelagic fisheries, precautionary measures should (i) regulate and/or ban the use of coastal gillnets during pupping/breeding seasons ( López-Garro et al., 2009; Zanella and López-Garro, 2015), and (ii) reduce fishing effort offshore, particularly during adult reproductive migrations ( Zanella and López-Garro, 2015). Catch and effort should then be monitored to evaluate fisheries impact on population trends (Figure 6).

Addressing the Social and Economic Incentives of Overfishing

Fishing effort should be reduced by addressing the root causes of overcapacity, which in SSF are the marginalization and displacement of coastal communities ( Pauly, 1990; Fargier et al., 2014). In the 1980s, agrarian reforms displaced farmers from their lands and forced them to settle along the coastline, where fishing was the main source of employment. Fishing effort increased, placing even more pressure on already depleted resources ( Fargier et al., 2014). Therefore, increasing social well-being and employment opportunities in coastal communities should reduce pressure on coastal stocks. In industrial fisheries, diesel subsidies and weak management frameworks are the root causes of overfishing, consequently, the elimination of these subsidies may reduce profitable fishing effort, allowing some stocks to recover ( Clark et al., 2005; Sumaila et al., 2008).

Generating Life-History Data

Given the increasing fishing pressure on chondrichthyans populations in the ETP, generating species-specific life-history information (age/growth, maturity, and fecundity) is a crucial step toward informing fisheries management and conducting reliable stock assessments. In Costa Rica, some studies have examined the distribution, reproduction and diet of demersal and/or coastal elasmobranchs associated with SSF from the Pacific ( Zanella Cesarotto et al., 2010; Clarke et al., 2014, 2016; Espinoza et al., 2015b; Zanella and López-Garro, 2015), providing critical life-history information on threatened and data deficient species, as well as identifying reproductive seasons and critical areas along the coast that may function as nursery, breeding and feeding grounds. This type of work is important to adequately manage fisheries impacts on coastal chondrichthyans, thus facilitating the design and implementation of effective spatial and temporal closures ( Rojas, 2006; Clarke et al., 2014; Zanella and López-Garro, 2015).

Application of Genetic Markers

The use of genetic markers in fisheries management and conservation has resulted in significant insights into the population ecology of exploited chondrichthyan species ( Dudgeon et al., 2012). Numerous studies have revealed different levels of connectivity on a wide range of shark species that occur within Costa Rican waters ( Nance et al., 2011; Galván-Tirado et al., 2013; Cardeñosa et al., 2014; Chabot et al., 2015), providing strong evidence that coastal and pelagic shark populations are not limited to a single EEZ. These findings support the need for regional management approaches that may improve the conservation and/or sustainability of chondrichthyan species. The use of DNA barcoding has also proven to be a valuable approach to identify common elasmobranch species associated with the domestic ( O'Bryhim et al., 2017) and international ( Shivji et al., 2005) Costa Rican trade. Moreover, several shark species have been morphologically and genetically identified from shark fin exports (e.g., C. longimanus, and S. lewini) ( Abercrombie and Hernandez, 2017), proving a useful tool to enforce domestic and international regulations. This is particularly important given that six shark species from Costa Rica are listed on the Appendix II of CITES (Convention on International Trade in Endangered Species of Fauna and Flora).

Given the low number of genetic studies on chondrichthyan species within Costa Rican waters, determining the population structure, philopatric behavior, and local adaptation processes remains crucial. Moreover, the emergence of novel techniques such as eDNA allow researchers to monitor cryptic and/or threatened elasmobranch species based on traces of their DNA found in the environment ( Simpfendorfer et al., 2016; Thomsen et al., 2016; Bakker et al., 2017). Therefore, the use of eDNA may be a relatively cost-effective technique to monitor critically endangered species such as sawfishes ( P. pristis and P. pectinata) within continental waters of Central America and/or conduct regional-scale assessments of chondrichthyan populations within the ETP ( Bakker et al., 2017).

Trophic Ecology

High trophic level predators fulfill a variety of ecological roles in both terrestrial and aquatic ecosystems ( Terborgh and Estes, 2010). Some sharks, for example, are capable of regulating prey dynamics, structuring marine food webs, and ultimately may help maintain ecosystem function and health ( Sergio et al., 2008; Heithaus et al., 2014). Consequently, large-scale population declines of shark species that act as top predators may lead to wide-ranging ecological and economic consequences ( Heithaus et al., 2014; Heupel et al., 2014). However, for most chondrichthyans trophic information is scarce and/or the role they play in aquatic ecosystems have not been defined.

Fisheries management has traditionally focused on understanding the population dynamics of target species rather managing fishing impacts on entire ecosystems ( Gilman et al., 2008), which requires a deeper knowledge of their trophic ecology. In Costa Rica, feeding studies on elasmobranchs have relied on stomach content analysis ( Rojas, 2006; Espinoza et al., 2012, 2013), and only until recently researchers have used stable isotopes to investigate feeding relationships across larger areas ( Espinoza et al., 2015b; Sandoval-Herrera et al., 2016). Stable isotopes of carbon (δ ¹³C) and (δ ¹⁵N) provide useful long-term integrated dietary information on the movements, habitat use and trophic relationships of elasmobranch species ( Hussey et al., 2011, 2012). Therefore, integrating trophic information from stable isotopes with fisheries data is highly relevant to developing sound ecosystem-based management approaches ( Kitchell et al., 2002; Gilman et al., 2008), and should be an important emergent research area in the ETP.

Spatial Ecology

The movement of animals between habitats is a key process that maintains population connectivity, and ultimately persistence ( Olds et al., 2012). Understanding when, where, and why animals move and use specific habitats is crucial to conservation and has direct applications to spatial management planning ( Espinoza et al., 2015a). Despite the relatively low number of published studies on shark movements within Costa Rican waters ( Nalesso, 2014; Calderón-Chávez, 2017), there has been a considerable amount of effort to investigate migratory patterns of threatened species in the ETP region, particularly at offshore/remote MPAs such as Isla del Coco, Islas Galapagos, and Malpelo. Acoustic and satellite tracking data on adult scalloped hammerhead sharks ( S. lewini), for example, has provided important information about their degree of residency and inter-island movements within the ETP ( Bessudo et al., 2011; Ketchum et al., 2014; Nalesso, 2014). From a management perspective, quantifying how much time S. lewini remain at each island (i.e., Isla del Coco, Islas Galapagos, Isla Malpelo), determining when they leave, and identifying potential migratory corridors between these islands is a crucial step to reducing fisheries impacts on their populations. The establishment of large networks of acoustic receivers have also allowed researchers to track the movements of coastal and pelagic species over broad spatial scales (10-1000 km) ( Cooke et al., 2011; Hussey et al., 2015; Espinoza et al., 2016). For instance, in the ETP region, the network MIGRAMAR is generating critical movement information toward the conservation of a wide range of migratory species as well as their critical habitats ( Nasar et al., 2016).

Filling the gaps in elasmobranch spatial ecology (e.g., residency and site fidelity, horizontal and vertical space use, and migratory patterns) is crucial to: (i) quantify the extent of overlap with fisheries operating in the ETP; (ii) identify critical habitats for feeding and reproduction, or potential linkages between ecosystems; (iii) design effective spatial management approaches such as marine reserves or corridors that can increase protection during migration; (iv) evaluate the benefits gained from existing/proposed spatial approaches, particularly for wide ranging species that may only have limited protection; (v) establish or strengthen regional management and conservation approaches to protect cross-boundary species; and (vi) ultimately, define their role in aquatic ecosystems. Movement data on pelagic sharks can also be complemented with information on the spatial distribution of fishing effort (vessel tracking information from both national and international fishing fleets, satellite images) thus increasing our understanding of their degree of spatial and temporal overlap ( Queiroz et al., 2016).

Assessing the Effect of Climate-Driven Changes

Climate-impacts on chondrichthyans are projected to be highest in the tropics, where a decrease in size, abundance, and diversity is expected ( Cheung et al., 2012; Jones and Cheung, 2015). Although chondrichthyans may adapt to a changing climate, current studies have already documented pole-wards shifts of tens to hundreds of kilometers for marine species ( Block et al., 2011; Hazen et al., 2012). Species with slow growing life history strategies and with high affinity to specific habitats (e.g., coral reefs, mangroves, wetlands) are projected to be the most vulnerable to climate impacts ( Chin et al., 2010; Hazen et al., 2012; Waples and Audzijonyte, 2016). To enhance the adaptive capacity of chondrichthyans in the face of these global-scale changes, we need to improve our understanding of species diversity, movement, and distribution patterns.

Conclusions

Despite the increasing number of chondrichthyan studies in Costa Rica over the past decade, there is still a need to redirect efforts toward specific research areas, regions, and species (batoids and chimeras) that currently have major information gaps. The Caribbean coast and the deep-sea, for example, are critical regions where landing statistics and basic biological/ecological information of sharks, rays, and chimeras are lacking ( Cortés et al., 2012). This review also identified important management challenges and research needs that should be addressed to improve the conservation of Chondrichthyans in Costa Rican waters. For instance, improving the quality and quantity of fisheries landing statistics, as well as the knowledge on chondrichthyans that interact with small-scale coastal and pelagic fisheries remains a priority. We proposed an adaptive management framework for chondrichthyan fisheries in data-poor countries where management goals/targets are clearly defined. Due to the uncertainty inherent in data-poor fisheries, applying the precautionary approach to buffer unforeseen impacts on chondrichthyan stocks is needed ( Selkoe et al., 2015). This may allow conducting proper risk and/or stock assessments and monitor the success/progress of the management goals, thus strengthening the conservation of chondrichthyan populations in the region.

Author Contributions

ME, ED, AA, SH, and TC contribute with the literature review, analysis of published data, and writing of the paper.

Funding

This review was funded by the Vicerrectoría de Investigación from the Universidad de Costa Rica (Project No. 808-B7-146).

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors would like to thank many of their colleagues for discussions about different aspects of the biology, ecology, and fisheries management of chondrichthyan fishes in Costa Rica and the Central American region that have helped to frame this review. We would like to thank Raquel Romero Chaves for her help with the map in Figure 1. Finally, we also are thankful for the comments from two reviewers that help improve this manuscript.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2018.00085/full#supplementary-material

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Chondrichthyan Diversity, Conservation Status, and Management Challenges in Costa Rica

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Understanding key aspects of the biology and ecology of chondrichthyan fishes (sharks, rays, and chimeras), as well as the range of threats affecting their populations is crucial given the rapid rate at which some species are declining.

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There are around 1,000 species in this class (Chondrichthyes) of fish. The species in this class have a flexible skeleton made of cartilage instead of bone.

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Molecular and Chromosomal Markers for Evolutionary Considerations in Torpediniformes (Chondrichthyes)

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Molecular and Chromosomal Markers for Evolutionary Considerations in Torpediniformes (Chondrichthyes)

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This website goes over the evidences of mutation found in Modern Chondrichthyes

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Due to their basal position in the vertebrate phylogenetic tree, the study on elasmobranch genetics and cytogenetics can provide remarkable information on the mechanisms underlying the evolution of all vertebrates. In recent years, different molecular approaches have been used to study the relationships between the different taxonomic groups of cartilaginous fish, among them are the physical mapping of specific nucleotide sequences on chromosomes. However, these are controversial, particularly in Torpediniformes in which the species have different karyological parameters. The purpose of this paper is to gather the molecular markers so far present in literature that were used to reconstruct the phylogenetic position of Torpediniformes with respect to the other Batoidea and to discriminate between the various chromosome pairs in the endemic species in the Mediterranean Sea, Torpedo torpedo, T. marmorata and T. nobiliana. The 5S and 18S ribosomal DNA, the HpaI and Alu SINE, the telomeric (TTAGGG)n and the spermatogenesis-related SPATA 16, SPATA 18, and UTY sequences were particularly useful. These last genomic segments were also able to differentiate between the male and the female karyotypes. Moreover, the torpedoes showed a particular genomic organization, especially Torpedo torpedo, in which large quantities of highly repeated DNA and a characteristic distribution of heterochromatin, which is never centromeric, were observed.

1. Introduction

The Chondrichthyes (cartilaginous fish) are one of the three extant major clades of jawed vertebrates and comprise two sister groups, the elasmobranchs (rays, sharks, and skates) and the holocephalans (chimeras and ratfish). They occupy an important phylogenetic position as the sister group to all other jawed vertebrates and as one of the first lineages to diverge in vertebrate evolution [ 1]. Despite this, there have been relatively few studies about chondrichthyan genetics and cytogenetics.

Batoids are one of the biggest systematic groups that are included in elasmobranch fish [ 2]. Most batoids have a strongly depressed disc-like body derived from a rhinobatoid-like (as in rajids) or from a plathyrhinid-like (as in higher myliobatiformes) ancestor [ 3].

Many different views have been proposed on batoid interrelationships. In this paper, Batoidea higher classification by McEachran and Aschliman [ 3] and Nelson [ 2] has been given. According to these authors, Torpediniformes are to be considered as a sister group to the remaining batoids.

Torpediniformes, commonly named electric rays, are known for being capable of producing an electric discharge (up to 220 volts depending on species), used to stun prey and for defense. Electric rays are found from shallow coastal waters down to at least 1,000 metres depth.

Three species of Torpediniformes, belonging to family of Torpedinidae, are frequent in the Mediterranean Sea, the common torpedo Torpedo torpedo Linnaeus 1758, the marbled electric ray T. marmorata Risso 1810 and the black torpedo T. nobiliana Bonaparte 1835. The first is characterized by yellow-reddish stains on the back with five blue spots surrounded by a black halo; the second is the most common and exhibits a yellowish-brown body with dark spots. The third, purplish-brown back and whitish on the belly, which reaches one meter in length, is much less present. Although monophyly of the batoids (electric rays, sawfishes, guitarfishes, skates, and stingrays) is widely accepted and well corroborated, the interrelationships within batoids remain controversial. In particular, the most contentious issues concern the phylogenetic position of the Torpediniformes.

The aim of this paper was to report the already known molecular markers that were used to reconstruct the phylogenetic position of Torpediniformes with respect to the other Batoidea and to discriminate between the various chromosome pairs in the endemic species in the Mediterranean Sea. The 5S and 18S ribosomal DNA, the HpaI and Alu SINE, the telomeric and the spermatogenesis-related SPATA 16, SPATA 18, and UTY sequences have proved particularly useful. These last genomic markers were also able to differentiate between the male and the female karyotypes.

The molecular methods consisted of the analysis for ribosomal 16S mtDNA and 18S nuclear sequences. The cytogenetic assays collected the classic reconstruction of species karyotype and the fluorescence in situ hybridization (FISH) technique using the genomic fragments mentioned above.

2. Phylogenetic Relationships and Karyological Properties

The superorder taxonomy in cartilaginous fish is undergoing major revisions; currently there is no agreement as regards to the higher systematic level in these species. A large number of different interpretations exists in scientific literature based on morphological characters [ 3- 11], on molecular studies [ 12- 14], and on conventional cytogenetics [ 14, 15].

Many scientists consider that batoids are monophyletic, even if the time of their divergence from the other elasmobranch fish remains controversial. Several more recent morphological lines of evidence seem to support the derivation of batoids from sharks [ 7, 16], but immunological and molecular studies corroborate the hypothesis of batoids as separate from sharks [ 13, 17, 18]. However, molecular phylogenetic evidence published in the last few years has principally focused on relationships among the elasmobranch superorders. In fact, very few molecular studies addressing interrelationships within Batoidea have been published. One of them concerns only the phylogenetic relationships among the major lineages of myliobatoids, including one species for each of the four remaining batoid orders [ 19]. This paper represents the first attempt to introduce a species of Torpediniformes (used as an outgroup) in a phylogenetic reconstruction based on molecular markers (1528 bp of mtDNA: 12S, four tRNAs, fragments of ND1 and ND2).

The karyological approach could provide an informative tool to contribute to the corroboration of systematic relationships in Elasmobranchii, and particularly in Torpediniformes. In fact, many authors agree about an intimate correlation between the development of a new species and the simultaneous modification of its karyotype, confirming the close evolutionary links between chromosome number and morphology, speciation, and morphological diversification [ 20].

The Torpedinidae is the most investigated family of the order as concerns karyological morphology (5 species have been examined to date). Only two species have been studied in the Narcinidae and Narkidae families, while no data are available for the Hypnidae family.

The species belonging to the order of the Torpediniforms exhibit different morphology in their karyotypes. In fact, considering the various species, it can be seen how their karyological parameters are different. They vary from 2 n = 28 and FN (fundamental number) = 56 in Narcine brasiliensis to 2 n = 86 and FN = 86 in Torpedo marmorata and T. tokionis, with intermediate values in T. torpedo (2 n = 66, FN = 78) and Narke japonica (2 n = 54, FN = 82) (Table 1). Moreover, their karyotypes do not show sex chromosomes [ 15].

The genome of many cartilaginous fish underwent a DNA increase during its evolutionary history followed by chromosomal rearrangements mainly in the form of fusions and translocations [ 15].

Especially within the superorder Batoidea karyologic evolution took place from the least evolved species to the most specialized. The progressive reduction of the diploid number, the increase of the number of chromosomes with two arms and the disappearance of microchromosomes occurred, probably as a consequence of polyploidy followed by diploidization and Robertsonian rearrangements (Figure 1) [ 14, 15, 23, 25- 27].

This karyological pattern is clearly evident in the Torpedinidae family. In fact, in T. marmorata only elements with one arm are present, while in T. torpedo and T. nobiliana there is a reduction of the number of uniarmed elements and an increase in the number of biarmed chromosomes; it must also be noted that the FN is similar in all the Torpediniforms, except in Narcine.

In a previous work, the first assessment of relationships among different batoid species by using both ribosomal 16S mtDNA and 18S nuclear sequences was reported. These molecular data were further discussed with karyological evidence coming from the literature [ 14].

The phylogenetic results obtained by the analysis of the two separate gene sequences were similar to those coming from the combined data set. In general, 18S sequences proved better than 16S at resolving higher-order relationships. However, the opposite holds true for the study of lower-order relationships: 16S genes were better at resolving the relationships than the 18S genes, and the combined data set was not more informative than 16S genes.

The molecular relationships based on 16S and 18S sequences placed the Torpediniformes distant from the other batoid species in all the phylogenetic trees coming from this analysis. The result was consistent with the earliest hypotheses by Compagno [ 4, 28, 29] and Maisey [ 30], but also with a more recent interpretation by McEachran et al. [ 8] and McEachran and Aschliman [ 3], who argued that the Torpediniformes are most likely the sister group of the other batoids (Figure 2).

Some studies are currently in progress to implement the information on the evolutionary relationships of other species of electric rays. Research is also being carried out on additional DNA fragments that could be used as molecular markers.

3. Characterization of Repeated Sequences

Only in the last few years different molecular approaches, first of all physical mapping on metaphase chromosomes, have been used to investigate the cytotaxonomic relationship among the living cartilaginous fish [ 27].

Comparative cytogenetics, as a powerful tool to study karyotypic variation, is based on accurate chromosome identification. Physical mapping involves in situ hybridization of specific segments of genomic DNA to their physical location on chromosomes. It is extremely useful in terms of gaining an insight into structural arrangements within the genome. The use of these molecular cytogenetic techniques have often either suggested new taxonomic implications or confirmed the existing phylogenetic relationships among the different fish species analyzed [ 27, 31, 32].

Such molecular cytogenetic techniques were particularly helpful in elasmobranch karyology because in these fish genome compartmentalization is not present, as has also been demonstrated in the majority of teleostean species [ 33, 34].

The human telomeric sequence repeats, , detected by FISH, were assayed on chromosomes of T. torpedo [ 35].

FISH allowed the detection of fluorescent signals on the telomeres of both uni- and biarmed elements. An interstitial and/or paracentromeric labeling on four bi-armed chromosomes was also evident (Figure 3). This interstitial FISH pattern might represent further evidence supporting the hypothesis that karyotype evolution in Torpediniformes occurred by a progressive reduction of chromosome number due to centric fusions [ 26, 36]. In fact, species that underwent karyotype rearrangements as a result of Robertsonian fusions also show nontelomeric sites of the sequences in addition to the telomeric ones [ 37, 38].

Furthermore, the presence of additional interstitial sites of the sequences in T. torpedo could indicate that, from a karyological point of view, this species is in a phase of active evolutionary change. In fact, the interstitial sites containing sequences are often involved in recombination events [ 37].

Other remarkable results came from SINE (Short Interspersed Nuclear Elements) sequences analysis in the Torpedo genome.

Retroposons represent a significant portion of repetitive DNA in Eukaryotes. They are mobile genetic elements that are amplified by a reverse transcription of an intermediate RNA [ 39]. Two large families of retroposons, first identified as interspersed repeated sequences, belong to this genomic component. The LINE (long interspersed nuclear elements) family is made up of long sequences, while the SINE family has short sequences, both irreversibly inserted in the genome [ 40].

The SINE family was amplified in the elasmobranch genome by PCR [ 27] using the primers taken from salmonids ( HpaI family) [ 41] and from humans ( Alu sequences) [ 42].

FISH performed with the HpaI-like SINE probe on the T. torpedo chromosome revealed hybridization signals at the centromeric and/or the paracentromeric region on several biarmed chromosomes, while conspicuous fluorescent signals at the centromeric and/or telomeric level on the acrocentric ones were produced (Figure 4(a)), providing a hybridization pattern that is not coincident with that evidenced by C-banding [ 36]. Such a result is similar to that evidenced by Perez et al. [ 43] on Atlantic salmon and rainbow trout karyotypes where the members of this SINE family are located only in the euchromatic regions of the chromosomes.

The location of these specific Alu-like sequences on the chromosomes of T. torpedo is prevalently at the centromeric level, as in humans [ 44], and sometimes at the telomeric level, indicating an intraspecific polymorphisms (Figure 4(b)).

Marçais et al. [ 45] and Prades et al. [ 44] observed that the block of alphoid DNA at the centromeres of human chromosomes is susceptible to variations in length created by jumping amplification, with an unequal exchange of large alphoid domains between homologous chromosomes, and deletions of large DNA segments. Probably, through a similar mechanism, these Alu-like sequences retrotransposed within the T. torpedo genome to specific sites such as telomeric regions that are particularly exposed to a new insertion of transposable elements [ 46].

The Hpa I-like SINE and Alu-like sequences from T. torpedo were also hybridized on genomic DNA of four species of Batoidea ( Torpedo marmorata, T. torpedo, Raja asterias, and Raja montagui) and two species of Galeomorphii ( Mustelus asterias and Scyliorhinus stellaris). The hybridization patterns shown were practically identical in the two rays and in the two Torpedo species (Figures 5 and 6). The results fixed the relationships present among the species attributed to the different superorders examined [ 29]. In fact, Southern blot analysis revealed a similar hybridization pattern in congeneric species, confirming their close systematic relatedness. The Hpa I-like probe failed to show the hybridization pattern on genomic DNA in Mustelus asterias, probably because the signal of labeling was too weak and under the sensitivity of the technique.

4. Ribosomal Genes: Nucleotide Sequences and Mapping

The ribosomal genes are organized into two multigene families in superior eukaryotes. One of these families contains the major rDNA (45S) that codes for the 18S, 5.8S, and 28S rRNAs, while the other codes for the minor rDNA (5S). The nucleolus organizing regions (NORs) that contain the 45S rDNA can be easily identified in chromosomes by silver nitrate (Ag-NORs) or investigated using certain fluorochromes such as Chromomycin A3, especially in fishes, although these fluorochromes only show heterochromatic GC rich regions [ 47] sometimes interspersed among the ribosomal gene clusters [ 48].

In Torpediniformes chromosomal localization of major ribosomal genes by using FISH technique has often been associated with fluorochrome and silver-staining techniques. Chromomycin A ₃ (CMA ₃) is a GC-rich DNA-specific fluorochrome dye and detects the nucleolar organizing regions (NORs) independently of their activity [ 49] also in cartilaginous fish. Silver (Ag-NOR) staining detects only NORs that are functionally active during the previous interphase [ 50].

Table 2 reports the number and the chromosome location of Ag-NOR s and CMA ₃ sites as well as those of 18S and 5S rRNA genes in the Torpedo species so far studied.

In T. marmorata the silver-nitrate-staining showed Ag-NOR regions at the telomeric level of two or three acrocentric elements. In T. nobiliana, the Ag-NOR-staining showed two telomeric sites of one pair of acrocentric elements and, in at least 20% of the plates examined, the Ag-NOR staining was localized at the telomeric level of one small submetacentric chromosome. In T. torpedo, the Ag-NOR staining showed two telomeric sites of one pair of acrocentric elements. Moreover, in at least 20% of the plates examined, the Ag-NOR staining was localized at the interstitial level of one submetacentric chromosome.

The rDNA FISH probes were able to reveal all rRNA loci on the chromosomes. The CMA ₃ staining and FISH technique using 18S rDNA showed the fluorescent signals only at the telomeric level of two pairs of chromosomes in T. marmorata. In T. nobiliana signals were found at the telomeric level of one pair of acrocentric elements and one pair of submetacentric elements. In T. torpedo, the markers were at the telomeric level of one pair of acrocentric elements, but with a further banding also at the interstitial level of one pair of major submetacentric elements. Figure 7 shows the schematic representation of the chromosomes involved in the species analyzed. Comparing the results with those evidenced in Rajiformes, it is particularly noteworthy that in the genus Raja multiple sites for NORs were found [ 51]. The number of chromosome pairs bearing major rDNA is notably decreased in Torpedo.

As far as 5S rDNA organization is concerned, in the three Torpedo species studied, the results of the amplification products by PCR are similar to those reported in literature for other vertebrates. The length of the bands obtained in the different species varies due to the different size and base composition of the nontranscribed spacer (NTS) region. Moreover, the NTS region contains some TATA-like trinucleotides and other short sequences, such as trinucleotides, dinucleotides and tetranucleotides, which could be involved in the regulation of the gene itself, as has been described for some species of teleosteans [ 52- 54].

The minor ribosomal cluster was, however, localized at the telomeric level of a single pair of acrocentric elements in all three species studied (Figure 7).

The chromosomal localization of 5S rDNA might represent further evidence to support the hypothesis that the karyotype of the Chondrichthyes evolved through fusion of acrocentric elements, forming metacentric or submetacentric ones. The chromosomes bearing the minor ribosomal clusters might, in fact, have been involved in these Robertsonian fusion phenomena that occurred in the karyological evolution of these fish, stemming from a progenitor with more primitive karyotype characteristics such as those of the Raja species.

The study of the organization of ribosomal genes and their chromosomal localization provides a series of informative data, above all when integrated by means of in situ hybridization and sequencing. They, in fact, could provide a better understanding of the molecular bases of the chromosomal structure and function and, more in general, of the arrangements that lead to the processes of speciation.

In cartilaginous fish, sex chromosomes are present in a small number of species ( Rhinobatos schlegelii, R. hynnicephalus, and Carcharodon carcharias) [ 55, 56].

In order to identify new molecular chromosomal markers both to discriminate the different chromosome pairs and to distinguish the probable sex chromosomes in the species Torpedo torpedo, another study on some DNA genomic sequences was performed [ 57].

The research began using specific primers to characterize at the molecular level and to localize on the chromosomes SRY-like sequences; these are the hypothetical regions for sex determination. These are well conserved in mammals, thus allowing the amplification of fragments of entire genes coming from taxonomic groups that are also very heterogeneous. This allowed the amplification of segments of DNA also in this species that had never been studied before in a cartilaginous fish at the molecular genetic level.

As concerns chromosomal localization of the amplification products, the results obtained showed the presence of labels on two pairs of chromosomes in the male, one pair of subtelocentric and one pair of acrocentric elements. In the female, the FISH test showed the presence of labels only on the pair of acrocentric chromosomes. The same result was obtained by hybridizing the male DNA fragments on the female chromosomes and the female DNA probe on the male metaphase plates (Figure 8).

It could seem that the pair of acrocentric elements, which were always marked in both sexes, are homologous, as the patterns of hybridization for these chromosomes and their morphology were the same when FISH was performed with a male or with a female probe. Furthermore, I believe that there is indeed a difference between the genomic composition of the submetacentric elements in the male and in the female, in the light of the nonhybridization on the female chromosomes using the male probe. Further remarkable data came from the sequencing results. The PCR products had similar patterns with two bands of 200 and about 400 bp in length for each sex, that showed, only for the male 400 bp band, an alignment with the human genes SPATA 16, SPATA 18, and UTY.

These genes in man are implicated in the process of spermatogenesis, and presumably also in T. torpedo play a crucial role in sex differentiation. Probably only this 400 bp band of the male is responsible for the difference between the sexes, given that the alignment between the two sequences of 200 bp showed 98% identity. An explanation could lie in the accumulation of random mutations and rearrangements on the sex-specific chromosomes. In fact, it was hypothesized that sex chromosomes, in fish, reach a differentiated state by means of a genetic mechanism called "Muller's ratchet," by which the accumulation of slightly harmful DNA changes in a population over many generations takes place [ 58].

6. Closing Remarks

The main purpose of this paper was to provide an overview of genetic and cytogenetic molecular markers for the analysis of the cytotaxonomic relationships among Torpediniformes and for the reconstruction of evolutionary interrelationships between this superorder and the other batoid species, using the data published up to now, coming prevalently from my research group. For many years this information has been obtained using the classical cytogenetic methods (C-banding, silver nitrate, and fluorochrome staining) that only allow the description of general chromosome morphology.

The chromosome localization of DNA sequences and genes is important for the analysis of chromosome rearrangements and permits an efficient comparative cytogenetic study among batoid fish species.

Some types of molecular markers that seem to be suited to investigate the different levels of applications in the field of comparative cytogenetics and evolutionary studies have been described. The phylogenetic implications coming from the data should be improved to further clarify the existing relationships.

The evidence presented here confirms the particular genomic organization of Torpediniformes, especially T. torpedo, in heteroterms as well as in the superclass of fishes. In this species, large amounts of highly repeated DNA [ 59], high heterogeneity in the genome composition [ 26], and a characteristic distribution of heterochromatin, that is never centromeric [ 36], have all been found.

Because of the particular marking pattern that was found with several DNA sequences, the meta and submetacentric pairs of T. torpedo are to be considered as chromosome markers and are a valid instrument to reveal particular linkage groups of evolutionary importance.

The ever closer integration between molecular cytogenetic analysis and the deep sequencing using bioinformatic tools will be important to clarify the genomic and chromosome organization in these fascinating species of cartilaginous fish.

Acknowledgments

The author would like to express her gratitude to Dr. A. Bridgewood for his assistance in revising the English of this manuscript. She would also like to thank Prof. V. Stingo for the critical review of the scientific work and her collaborators, Dr. D. Costagliola, Dr. I. Liguori, and Dr. S. Bencivenga who contributed to some aspects of the research presented in this paper.

References

1. J. S. Nelson, Fishes of the World, John Wiley & Sons, New York, NY, USA, 4th ed edition, 2006.

2. S. Shirai, Squalean Phylogeny: A New Framework of "Squaloid" Sharks and Related Taxa, Hokkaido University Press, Sapporo, Japan, 1992.

3. T. Asahida and H. Ida, "Karyotypes of two rays, View at: Torpedo tokionis and Dasyatis matsubarai, and their systematic," Japanese Journal of Ichthyology, vol. 37, pp. 71-75, 1990. Google Scholar

4. A. Viñas, M. Abuín, B. G. Pardo, P. Martínez, and L. Sánchez, "Characterization of a new HpaI centromeric satellite DNA in Salmo salar," Genetica, vol. 121, no. 1, pp. 81-87, 2004.

5. D. C. Cabral-de-Mello and C. Martins, "Breaking down the genome organization and karyotype differentiation through the epifluorescence microscope lens: insects and fish as models," in View at: Microscopy: Science, Technology, Applications and Education, A. Méndez-Vilas and J. Díaz, Eds., vol. 1 of Formatex Microscopy No. 4, pp. 658-669, Formatex Research Center, Badajoz, Spain, 2010. Google Scholar

6. L. Rocco, D. Costagliola, and V. Stingo, "(TTAGGG)n telomeric sequence in selachian chromosomes," Heredity, vol. 87, no. 5, pp. 583-588, 2001.

7. J. Perez, E. Garcia-Vazquez, and P. Moran, "Physical distribution of SINE elements in the chromosomes of View at: Atlantic salmon and rainbow trout," Heredity, vol. 83, no. 5, pp. 575-579, 1999. Google Scholar

8. R. F. Artoni, W. F. Molina, L. A. C. Bertollo, and P. M. Galetti, "Heterochromatin analysis in the fish species View at: Liposarcus anisitsi (Siluriformes) and Leporinus elongatus (Characiformes)," Genetics and Molecular Biology, vol. 22, no. 1, pp. 39-44, 1999. Google Scholar

9. L. Rocco, D. Costagliola, M. Fiorillo, F. Tinti, and V. Stingo, "Molecular and chromosomal analysis of ribosomal cistrons in two cartilaginous fish, Taeniura lymma and Raja montagui (Chondrichthyes, Batoidea)," Genetica, vol. 123, no. 3, pp. 245-253, 2005.

10. T. Asahida and H. Ida, "Karyotype and cellular DNA content of a guitarfish, View at: Rhinobatos schlegelii," La Kromosomo II, vol. 79-80, pp. 2725-2730, 1995. Google Scholar

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Molecular and Chromosomal Markers for Evolutionary Considerations in Torpediniformes (Chondrichthyes, Batoidea)

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Due to their basal position in the vertebrate phylogenetic tree, the study on elasmobranch genetics and cytogenetics can provide remarkable information on the mechanisms underlying the evolution of all vertebrates. In recent years, different molecular approaches have been used to study the relationships between the different taxonomic groups of cartilaginous fish, among them are the physical mapping of specific nucleotide sequences on chromosomes.

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Chondrichthyes are one of the oldest living group of jawed vertebrates that diverged from a common ancestor of bony vertebrates (Osteichthyes: ray-finned fishes, coelacanths, lungfishes, and tetrapods) in the early Silurian about 420 Ma

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Current Status of Great White Shark Populations

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Current Status of Great White Shark Populations

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So, Are great white sharks endangered? Yes, White sharks are a vulnerable species that need to continue under protection. While many countries have banned white shark fishing, others continue to harvest them from the oceans

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Are great white sharks endangered? The white shark was listed as an endangered species in Canada in 2006, and is estimated to have declined in population close to 80% in North America over the past 14 years.
Did you know that a female white shark takes approximately 35 years to reach sexual maturity and a male 25 years? And when they finally reach this stage, they give birth to only 2-10 pups every two to three years.

@nikodelosllanos

Well, now we can imagine how vulnerable this slow development makes their population numbers, and the long road these creatures have towards success as a shark species.

Now imagine their situation again considering human activity in the oceans.

White sharks had been doing very well before humans brought large scale commercial fishing to their habitats, massive tourism on beaches complete with underwater protection nets, pollution, poaching, and especially illegal fishing. There could be only a few thousand remainings, but this is not an easy figure to estimate when researchers still aren't even sure where they mate and reproduce. In fact, conservationists in some countries have spotted more sharks off the coastline, but they are not sure of the fraction they are really seeing- it could be ten, twenty or up to fifty per cent.

Many locations have documented an increase in marine mammal attacks, but this does not correlate directly to an increasing white shark population. No decreased attacks in other locations have been recorded, so conservationists infer that there could reasonably be more white sharks feeding on these mammals in some areas.

White Shark protection has been reduced

As the world faces the current pandemic, some activities have been drastically reduced- one such area is the patrol and protection of marine resources. Fishing vessels could be taking advantage of this to illegally fish inside protected areas. We have seen news coming from the Galapagos Islands in July reporting vessels poaching, harvesting, fishing illegally, and eliminating sharks within a protected area. We are afraid that this could be happening at Guadalupe Island as well. Most of the protection from illegal vessels comes from ecotourism, conservationists, and yachts visiting the island and now none of these vessels are in the ocean due to park closures.

Guadalupe white sharks are in danger

The ocean's natural balance is kept in check by vulnerable and endangered sharks and other apex predators. This is so important in maintaining our oceans healthy, sustainable and profitable, not only for ecotourism but for regulated fishing companies that can harvest approved amounts of fish without disturbing nature's equilibrium.

If an apex predator like a great white shark disappears

If at some point there is a species made extinct, we will see changes in the ocean's balance in response. For example, if an apex predator like a great white shark disappear from an ecosystem, there would likely be an overpopulation of seals, which were formerly hunted by the sharks. This could then lead to some fish species being wiped out as seals are known to overeat, bringing down the supply of fish on the market and increasing the price of fish. In Cape Cod in the 1970's, the seal population was culled as they were seen as competition for fisherman. White sharks nearly disappeared from the area until seal killing was banned and they began to reproduce in higher numbers in the 21st century. White sharks have since returned, and there is a large community of sharks off of Cape Cod today.

White sharks are widely dispersed around the world, with some areas such as Australia, South Africa and North America being especially well known for their presence. Every shark belongs to a particular community and they tend not to mix among population groups, even if they are capable of traveling long distances such as from South Africa to Mozambique or from Madagascar to Australia.

In South Africa, white shark populations have not done well even though they have been under protection since 1991. On the coast of Durban and Kwazulu-Natal, a 320km coastal protected area saw shark nets killing more than 33,000 sharks of a variety of species, including the white shark. Most shark nets installed to protect swimmers tend to catch different species, not only their target.

In Australia, the white shark has been protected since the 1990's, but the population hasn't seen a significant recovery following their drastic reduction in population in previous decades, from 1950-1990.

White Shark Population

The white shark was listed as an endangered species in Canada in 2006, and is estimated to have declined in population close to 80% in North America over the past 14 years.

Off the California coast, juvenile white shark populations seem to be increasing over the past decade based on commercial fishery data which shows an increased incidental catch of white sharks in gill nets. Regulatory protections introduced in the 1990's which prohibited white shark fishing and imposed regulations on gill net gear could have contributed to this apparent increase in white shark population.

@David Seradell

On Farallon Island in the northeast Pacific, there is evidence of an increase in numbers of adult white sharks. Researchers have been comparing data on elephant seal and other marine mammal attacks in the area, and increasing seal populations seem to be bringing more white sharks to the island. A similar effect is seen at nearby San Miguel Island, where more attacks on pinnipeds have been observed, and carcasses with shark bites have been found in the area.

Guadalupe Island was designated as a Biosphere Reserve by the Mexican government in 2005, and since has since an increase in white shark population. We can attribute this to protection efforts from conservationists and the ecotourism industry increasing education and changing attitudes towards this important predator. One living shark is much more valuable over time that one dead shark.

So, Are great white sharks endangered?

Yes, White sharks are a vulnerable species that need to continue under protection. While many countries have banned white shark fishing, others continue to harvest them from the oceans. If we don't do more to change human behaviour, this species could be at risk of extinction within a century.

Divemaster Martin Ferruggiaro

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Are great white sharks endangered? - Nautilus Liveaboards

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Are great white sharks endangered? The white shark was listed as an endangered species in Canada in 2006, and is estimated to have declined in population close to 80% in North America over the past 14 years. Did you know that a female white shark takes approximately 35 years to reach sexual maturity and a male 25 years?

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Catherine Cushenan, also know as Cat Sharks, has spent the past six years travelling the tropics, studying shark behaviour - with a little bit of tourism action and videography on the side. She is a shark ecologist, drone pilot and freediver from the U.K. whom has dedicated her life to saving the ocean and its inhabitants. Read below to find out about her enviable relationship with sharks.

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BY MARGAUX MONFARED

Sharks, the most notorious apex predator found in our oceans, have existed for over 400 million years. Sharks display a lack of interest towards humans, yet we hunt them down mercilessly. Humans kill over 100 million shark species annually partly due to the heart-breaking misconception, popularised by movies such as Jaws, that sharks should be feared. Despite this irrational fear, sharks are hunted because they are considered to be a highly valuable and desirable species. Of the 500 species of known sharks, 143 are listed as under threat by the IUCN Red list. Sharks are mainly susceptible to fisheries through by catch and the finning industry and could become extinct if we do not act now.

Catherine Cushenan, also know as , has spent the past six years travelling the tropics, studying shark behaviour - with a little bit of tourism action and videography on the side. She is a shark ecologist, drone pilot and freediver from the U.K. whom has dedicated her life to saving the ocean and its inhabitants. Read below to find out about her enviable relationship with sharks.

You've built your life around the ocean. What drew you to it in the first place?

This was actually something that Toddler Cat decided upon at the ripe old age of 2. I watched the Little Mermaid for the first time, and that was pretty much it. There was never anything else I wanted to do.
You have worked with several different species of sharks; can you describe the path you took into shark conservation?
My first ever role directly working with sharks was an internship with La.Ma.Ve in the Philippines. We were using photo identification to study the whale shark population in Oslo. I chose to do it because I had just completed my divemaster course in Indonesia and it was the nearest/ cheapest country I could get to. Little did I know how life changing it would be, I've since worked with whale sharks in five countries, and branched out to blue sharks, great whites, lemons, silkies, pyjama sharks... you name it!

What does a day in the life of a shark ecologist look like?

That's such a difficult question to answer- it changes depending on the country I'm in, the job, and my co-workers! It's often a lot of public interaction- the main goal of most shark ecologists is to encourage all the humans to love sharks as much as we do, so we prioritise outreach and education. This can mean creating media content or even running tours. Then there's the other side of shark ecology- sat behind a laptop slogging through data!
How do you hope your voice and work as a shark advocate will influence others?
The thing that makes me happiest is getting a message from someone who saw my photos/ videos and was inspired to swim with sharks because of me. I try and post as much positive content as possible because, after that one swim, people are usually addicted and that always leads to a greater respect for the ocean.
Why is it so important to engage the community with your work and about sharks?

Things like overfishing, the shark finning trade and marine pollution are often demand based. As we slowly reduce our consumption of fish, companies will stop exploiting fisheries. As people invest more in, bamboo toothbrushes for example, plastic manufacturers will also have to respond by reducing supply. If we can promote the need to protect not only sharks, but our oceans, I believe we can build a more sustainable future.
As a photographer, videographer and drone mama, can you explain the importance of these tools in conservation?
'A picture is worth a thousand words'. I've been at many a bar or social event where I tell people what I do for work. They won't believe me until I whip out a photo or video and show them. Seeing people IN the water with sharks proves they're not as dangerous as we think. On top of that, I had never seen a 'trash island' before, such as the ones in the Maldives, the Philippines, India, etc that circulated on social media. They showed massive rubbish sites the size of Texas floating in our ocean gyres. Without pictures and videos, even I wouldn't have understood the significance of the problem at hand. Media is the most important way to prove the urgency of conversation and that is something we desperately need.

Who or what do you draw your inspiration from?
Everything, everywhere, all the time. My sharky friends inspire me to travel and share and keep learning, while my friends back home and around the world that don't work in the ocean are often a huge influence. I can be having a down day, feeling a little hopeless about the impact I can have on the big wide world, and I'll get a message out of the blue from someone I haven't heard from in years sometimes, saying they loved a photo, or were inspired by a blog I wrote, or learned something from my podcast. Knowing that I'm making a difference, even to a handful of people, is probably the main thing that motivates me to continue even when times get hard.

What has your experience as a woman in ocean science been like?
Honestly, I have barely experienced inequality in my career. I had an awful experience in Mexico a year ago, but otherwise every job I've had has been full of kind, helpful people of every gender. I think it's less likely to find imbalance in this line of work, simply because if you respect the ocean, you can probably respect gender equality too. There are definitely exceptions that prove that rule, but generally speaking, I have felt encouraged by men and women throughout my experiences.

What is one thing you wish someone had told you/taught you a long time ago?
Just apply for the job. Whatever it is. Try for the scholarship. Attempt the record. Invest in whatever certification. There are so many things I haven't done because I didn't feel like I was ready- but in marine biology, everything is learning on the job! Just apply for anything and everything you feel passionate about, because you miss 100% of the shots you don't take. Oh, also, I wish someone had sat me down and forced me to learn R and generally become literate at statistics!

How has the recent COVID-19 pandemic affected (or not) you and your research?
It has been a little bit of a disaster. I got dragged home from heaven, in the Silver Bank of the Dominican Republic. I was working on a liveaboard with Conscious Breath Adventures , who run weeklong humpback whale swim trips. The last 2.5 trips of the season got cancelled due to the pandemic and I was repatriated back to England. I was also supposed to be working in Tonga from July 1st, but that's not happening now. I've been able to work on a few projects though, including my new website www.catsharks.co.uk - but lord knows I'm ready for the ocean now.

Where do you go from here?
With the pandemic I can't be certain. But I've recently invested in a Sony a6500 camera so I'm hoping that my videography and therefore my outreach will step up to a whole new level. Whatever happens, as long as I'm surrounded by the sea, I'll be happy.

BY MARGAUX MONFARED

Sharks, the most notorious apex predator found in our oceans, have existed for over 400 million years. Sharks display a lack of interest towards humans, yet we hunt them down mercilessly. Humans kill over 100 million shark species annually partly due to the heart-breaking misconception, popularised by movies such as Jaws, that sharks should be feared. Despite this irrational fear, sharks are hunted because they are considered to be a highly valuable and desirable species. Of the 500 species of known sharks, 143 are listed as under threat by the IUCN Red list. Sharks are mainly susceptible to fisheries through by catch and the finning industry and could become extinct if we do not act now.

Catherine Cushenan, also know as , has spent the past six years travelling the tropics, studying shark behaviour - with a little bit of tourism action and videography on the side. She is a shark ecologist, drone pilot and freediver from the U.K. whom has dedicated her life to saving the ocean and its inhabitants. Read below to find out about her enviable relationship with sharks.

You've built your life around the ocean. What drew you to it in the first place?

This was actually something that Toddler Cat decided upon at the ripe old age of 2. I watched the Little Mermaid for the first time, and that was pretty much it. There was never anything else I wanted to do.
You have worked with several different species of sharks; can you describe the path you took into shark conservation?
My first ever role directly working with sharks was an internship with La.Ma.Ve in the Philippines. We were using photo identification to study the whale shark population in Oslo. I chose to do it because I had just completed my divemaster course in Indonesia and it was the nearest/ cheapest country I could get to. Little did I know how life changing it would be, I've since worked with whale sharks in five countries, and branched out to blue sharks, great whites, lemons, silkies, pyjama sharks... you name it!

What does a day in the life of a shark ecologist look like?

That's such a difficult question to answer- it changes depending on the country I'm in, the job, and my co-workers! It's often a lot of public interaction- the main goal of most shark ecologists is to encourage all the humans to love sharks as much as we do, so we prioritise outreach and education. This can mean creating media content or even running tours. Then there's the other side of shark ecology- sat behind a laptop slogging through data!
How do you hope your voice and work as a shark advocate will influence others?
The thing that makes me happiest is getting a message from someone who saw my photos/ videos and was inspired to swim with sharks because of me. I try and post as much positive content as possible because, after that one swim, people are usually addicted and that always leads to a greater respect for the ocean.
Why is it so important to engage the community with your work and about sharks?

Things like overfishing, the shark finning trade and marine pollution are often demand based. As we slowly reduce our consumption of fish, companies will stop exploiting fisheries. As people invest more in, bamboo toothbrushes for example, plastic manufacturers will also have to respond by reducing supply. If we can promote the need to protect not only sharks, but our oceans, I believe we can build a more sustainable future.
As a photographer, videographer and drone mama, can you explain the importance of these tools in conservation?
'A picture is worth a thousand words'. I've been at many a bar or social event where I tell people what I do for work. They won't believe me until I whip out a photo or video and show them. Seeing people IN the water with sharks proves they're not as dangerous as we think. On top of that, I had never seen a 'trash island' before, such as the ones in the Maldives, the Philippines, India, etc that circulated on social media. They showed massive rubbish sites the size of Texas floating in our ocean gyres. Without pictures and videos, even I wouldn't have understood the significance of the problem at hand. Media is the most important way to prove the urgency of conversation and that is something we desperately need.

Who or what do you draw your inspiration from?
Everything, everywhere, all the time. My sharky friends inspire me to travel and share and keep learning, while my friends back home and around the world that don't work in the ocean are often a huge influence. I can be having a down day, feeling a little hopeless about the impact I can have on the big wide world, and I'll get a message out of the blue from someone I haven't heard from in years sometimes, saying they loved a photo, or were inspired by a blog I wrote, or learned something from my podcast. Knowing that I'm making a difference, even to a handful of people, is probably the main thing that motivates me to continue even when times get hard.

What has your experience as a woman in ocean science been like?
Honestly, I have barely experienced inequality in my career. I had an awful experience in Mexico a year ago, but otherwise every job I've had has been full of kind, helpful people of every gender. I think it's less likely to find imbalance in this line of work, simply because if you respect the ocean, you can probably respect gender equality too. There are definitely exceptions that prove that rule, but generally speaking, I have felt encouraged by men and women throughout my experiences.

What is one thing you wish someone had told you/taught you a long time ago?
Just apply for the job. Whatever it is. Try for the scholarship. Attempt the record. Invest in whatever certification. There are so many things I haven't done because I didn't feel like I was ready- but in marine biology, everything is learning on the job! Just apply for anything and everything you feel passionate about, because you miss 100% of the shots you don't take. Oh, also, I wish someone had sat me down and forced me to learn R and generally become literate at statistics!

How has the recent COVID-19 pandemic affected (or not) you and your research?
It has been a little bit of a disaster. I got dragged home from heaven, in the Silver Bank of the Dominican Republic. I was working on a liveaboard with Conscious Breath Adventures , who run weeklong humpback whale swim trips. The last 2.5 trips of the season got cancelled due to the pandemic and I was repatriated back to England. I was also supposed to be working in Tonga from July 1st, but that's not happening now. I've been able to work on a few projects though, including my new website www.catsharks.co.uk - but lord knows I'm ready for the ocean now.

Where do you go from here?
With the pandemic I can't be certain. But I've recently invested in a Sony a6500 camera so I'm hoping that my videography and therefore my outreach will step up to a whole new level. Whatever happens, as long as I'm surrounded by the sea, I'll be happy.

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An interview with Shark Ecologist Catherine Cushenan - WOMEN IN OCEAN SCIENCE

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Catherine Cushenan, also know as Cat Sharks , has spent the past six years travelling the tropics, studying shark behaviour - with a little bit of tourism action and videography on the side. She is a shark ecologist , drone pilot and freediver from the U.K.

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Tracking Sharks to Research and Conserve their Population

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Tracking Sharks to Research and Conserve their Population

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The sharks are tracked in a variety of ways, including with acoustic tags.

There are currently 179 sharks fitted with acoustic tracking tags, and when they get within about 500 meters of a receiver, the receiver records the date and time, Skomal said.

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The best way to avoid great white shark attacks in Cape Cod waters is to figure out where the sharks like to hang out and when they are there, marine biologists said Tuesday.

Experts from the state of Massachusetts and the nonprofit Atlantic White Shark Conservancy held a news conference in Chatham to outline some of the ways they are trying to detect patterns in shark movement and habits.

The goal is to keep beachgoers informed and safe.

"It's no secret that the number of negative interactions between people and sharks has been increasing," said Greg Skomal, the top shark expert with the state Division of Marine Fisheries.

The last fatal shark attack in state waters occurred in September 2018 when a man boogie boarding off Wellfleet was killed.

Sharks are drawn to the region by an abundance of seals, their favorite meal, but people can sometimes get in the way.

Sharks start migrating to the area in May, with peak activity in August, September and October, although white sharks have been detected in area waters as late as Dec. 17, said Megan Winton, staff scientist at the conservancy. Nearly half of their time is spent in waters less than 15 feet (4.5 meters) deep, close to shore, she said.

The sharks are tracked in a variety of ways, including with acoustic tags.

There are currently 179 sharks fitted with acoustic tracking tags, and when they get within about 500 meters of a receiver, the receiver records the date and time, Skomal said.

There are also five real-time receivers deployed along the Outer Cape, the area that faces east toward the Atlantic Ocean where sharks are most active. As soon as these real-time receivers detect a shark, the information is relayed to public safety officials, including lifeguards on the beaches who can clear the water.

But Winton warned that the system can only detect sharks that are tagged, so there is a possibility that an untagged shark will move close to shore without the public knowing.

The public can also check the conservancy's sharktivity app to track shark sightings.

"At the heart of all of this, it is really all about people," Winton said. "We're learning all this information so we can provide it to the public and provide it to the people, so that they can modify their behavior to proactively reduce the risk of having a bad interaction with a great white."

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Researchers track great white sharks to keep public safe

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The best way to avoid great white shark attacks in Cape Cod waters is to figure out where the sharks like to hang out and when they are there, marine biologists said Tuesday.

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Dr Compagno was the Head of the Shark Research Centre and Curator of Fishes , Iziko – South African Museum. He is an internationally recognised expert on sharks who obtained his Ph.D. from Stanford University in the United States. He is a foremost world expert on systematics, morphology, evolution, paleontology, zoogeography, diversity, natural history, and conservation of sharklike fishes.

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AOCA Director and Scientific Advisor

Dr Compagno was the Head of the Shark Research Centre and Curator of Fishes , Iziko - South African Museum. He is an internationally recognised expert on sharks who obtained his Ph.D. from Stanford University in the United States. He is a foremost world expert on systematics, morphology, evolution, paleontology, zoogeography, diversity, natural history, and conservation of sharklike fishes.

He won the Harvard University and Stanford University Scholarships in Biology for graduate work and is also the winner of numerous awards and fellowships. He is the regional vice-chairperson of the IUCN Shark Specialists Group and a research consultant for Fisheries Division of FAO of the United Nations.

He has published over 200 papers, popular articles, reports, web site reports, books and book chapters. His major books include Sharks of the Order Carcharhiniformes, the 1984 FAO catalogue of world sharks, the revised 2001 FAO catalogue of world sharks, and a field guide to southern African cartilaginous fishes co-authored with D. A. Ebert and M. J. Smale.

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AOCA Director and Scientific Advisor Dr Compagno was the Head of the Shark Research Centre and Curator of Fishes , Iziko - South African Museum. He is an internationally recognised expert on sharks who obtained his Ph.D. from Stanford University in the United States.

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Given the conservation status and ecological, cultural, and commercial importance of chondrichthyan fishes, it is valuable to evaluate the extent to which research attention is spread across taxa and geographic locations and to assess the degree to which scientific research is appropriately addressing the challenges they face. Here we review trends in research effort over three decades (1985–2016) through content analysis of every abstract (n = 2,701) presented at the annual conference of the American Elasmobranch Society (AES), the oldest and largest professional society focused on the scientific study and management of these fishes. The most common research areas of AES abstracts were reproductive biology, movement/telemetry, age and growth, population genetics, and diet/feeding ecology, with different areas of focus for different study species or families. The most commonly studied species were large and charismatic (e.g., White Shark, Carcharodon carcharias), easily accessible to long-term established field research programs (e.g., Lemon Shark, Negaprion brevirostris, and Sandbar Shark, Carcharhinus plumbeus), or easily kept in aquaria for lab-based research (e.g., Bonnethead Shark, Sphyrna tiburo). Nearly 90% of all described chondrichthyan species have never been mentioned in an AES abstract, including some of the most threatened species in the Americas. The proportion of female* first authors has increased over time, though many current female* Society members are graduate students. Nearly half of all research presented at AES occurred in the waters of the United States rather than in the waters of developing nations where there are more threatened species and few resources for research or management. Presentations based on research areas such as paleontology and aquarium-based research have declined in frequency over time, and identified research priorities such as social science and interdisciplinary research are poorly represented. Possible research gaps and future research priorities for the study of chondrichthyan fishes are also discussed.

Chondrichthyan fishes (including the sharks, rays, skates, and chimaeras) are considered one of the most threatened vertebrate groups by the International Union for the Conservation of Nature (IUCN) Red List (White and Last, 2012; Dulvy et al., 2014). Many chondrichthyans are considered to be ecologically important (reviewed in Heithaus et al., 2008), morphologically diverse and distinctive (Stein et al., 2018), and both culturally (e.g., Dell'Apa et al., 2015) and economically valuable (e.g., Gallagher and Hammerschlag, 2011 for wildlife tourism). Due to the threatened status of many species and the class's diversity of ecological roles, chondrichthyans have often been the focus of considerable research, management, and advocacy attention (reviewed in Simpfendorfer et al., 2011). Given these ecological, cultural, and commercial values, it is important to review and evaluate the extent to which research attention is allocated across taxa and geographic locations, and to assess the degree to which scientific research is appropriately addressing the challenges these fishes face. Here we consider patterns of chondrichthyan research as presented at the annual scientific conference of a professional society dedicated to the research and management of these fishes in order to assess trends in research over time and identify research gaps. These gaps could be used to help with chondrichthyan conservation efforts and to help a professional society to better achieve its stated goal.

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6 March 2020 Trends in Chondrichthyan Research: An Analysis of Three Decades of Conference Abstracts

D. S. Shiffman, M. J. Ajemian, J. C. Carrier, T. S. Daly-Engel, M. M. Davis, N. K. Dulvy, R. D. Grubbs, N. A. Hinojosa, J. Imhoff, M. A. Kolmann, C. S. Nash, E. W. M. Paig-Tran, E. E. Peele, R. A. Skubel, B. M. Wetherbee, L. B. Whitenack, J. T. Wyffels

Given the conservation status and ecological, cultural, and commercial importance of chondrichthyan fishes, it is valuable to evaluate the extent to which research attention is spread across taxa and geographic locations and to assess the degree to which scientific research is appropriately addressing the challenges they face. Here we review trends in research effort over three decades (1985-2016) through content analysis of every abstract ( n = 2,701) presented at the annual conference of the American Elasmobranch Society (AES), the oldest and largest professional society focused on the scientific study and management of these fishes. The most common research areas of AES abstracts were reproductive biology, movement/telemetry, age and growth, population genetics, and diet/feeding ecology, with different areas of focus for different study species or families. The most commonly studied species were large and charismatic (e.g., White Shark, Carcharodon carcharias), easily accessible to long-term established field research programs (e.g., Lemon Shark, Negaprion brevirostris, and Sandbar Shark, Carcharhinus plumbeus), or easily kept in aquaria for lab-based research (e.g., Bonnethead Shark, Sphyrna tiburo). Nearly 90% of all described chondrichthyan species have never been mentioned in an AES abstract, including some of the most threatened species in the Americas. The proportion of female* first authors has increased over time, though many current female* Society members are graduate students. Nearly half of all research presented at AES occurred in the waters of the United States rather than in the waters of developing nations where there are more threatened species and few resources for research or management. Presentations based on research areas such as paleontology and aquarium-based research have declined in frequency over time, and identified research priorities such as social science and interdisciplinary research are poorly represented. Possible research gaps and future research priorities for the study of chondrichthyan fishes are also discussed.

Chondrichthyan fishes (including the sharks, rays, skates, and chimaeras) are considered one of the most threatened vertebrate groups by the International Union for the Conservation of Nature (IUCN) Red List ( White and Last, 2012; Dulvy et al., 2014). Many chondrichthyans are considered to be ecologically important (reviewed in Heithaus et al., 2008), morphologically diverse and distinctive ( Stein et al., 2018), and both culturally (e.g., Dell'Apa et al., 2015) and economically valuable (e.g., Gallagher and Hammerschlag, 2011 for wildlife tourism). Due to the threatened status of many species and the class's diversity of ecological roles, chondrichthyans have often been the focus of considerable research, management, and advocacy attention (reviewed in Simpfendorfer et al., 2011). Given these ecological, cultural, and commercial values, it is important to review and evaluate the extent to which research attention is allocated across taxa and geographic locations, and to assess the degree to which scientific research is appropriately addressing the challenges these fishes face. Here we consider patterns of chondrichthyan research as presented at the annual scientific conference of a professional society dedicated to the research and management of these fishes in order to assess trends in research over time and identify research gaps. These gaps could be used to help with chondrichthyan conservation efforts and to help a professional society to better achieve its stated goal.

The American Elasmobranch Society (AES, https://elasmo.org) was founded in 1983 with the goal of "promoting the scientific study and management of chondrichthyan fishes." The AES has held an annual scientific conference since 1985, and the abstracts of all talks and posters presented at these conferences are publicly available online ( https://elasmo.org/abstracts). The AES seeks to be a professional home for any researcher studying chondrichthyan fishes regardless of their primary research discipline or institutional affiliation ( Ferry and Shiffman, 2014) and is thus a taxon-focused research society rather than a discipline-based society (e.g., Ecological Society of America, https://www.esa.org) or ecosystem-based society (e.g., Deep-Sea Biological Society, https://dsbsoc.org/). Though it was founded by North Americans and annual meetings take place in the Americas, membership is open to anyone directly involved in chondrichthyan research or management, and annual meetings frequently have representatives from around the globe. In recent years, AES has met as part of the Joint Meeting of Ichthyologists and Herpetologists (JMIH), a multi-society gathering, and it is worth noting that some talks focusing on chondrichthyans have been presented in the sessions of the American Society of Ichthyologists and Herpetologists (ASIH, another professional society that meets as part of JMIH) rather than in AES sessions. However, not all ASIH abstracts are accessible, so they were not analyzed in this study.

Previous studies have analyzed AES abstracts to examine trends in study species, such as Ajemian and Neer (2014) for durophagous rays and Cotton and Grubbs (2015) for deep-sea chondrichthyans. Additionally, a 2015 analysis identified themes in chondrichthyan research by reviewing abstracts from three international multi-society conferences called Sharks International in 1991, 2010, and 2014 ( Huveneers et al., 2015), and see McCallen et al. (2019) for an example of this type of analysis in ecology. Additionally, there is an editorial focusing on general trends in some aspects of shark research throughout the 20 th century ( Castro, 2016). However, no previous studies have examined such a large collection of chondrichthyan science abstracts over such a long time frame nor as comprehensively (the entire lifetime of a professional society) as undertaken here.

A further aim of this analysis is to understand the changing demographics of AES presenters at meetings since the Society began. Nationally, the number of bioscience degrees awarded to women has risen since 1985, and women earned approximately 58% of the bachelor's degrees, 57% of the master's degrees, and 53% of the doctorates in the biosciences in 2014 ( https://www.nsf.gov/statistics/2017/nsf17310/). While these trends indicate increased integration of female scientists across disciplines, it is unknown whether these individuals are limited to certain disciplines or scientific societies. To date, there has not been a demographic study of chondrichthyan researchers.

We seek to fill these data gaps by identifying patterns in chondrichthyan research and research demographics over time using AES abstracts. Research questions included: 1) What research areas, topics, and methods do most AES abstracts focus on? 2) Which chondrichthyan species and/or families are most commonly the focus of AES research? 3) What is the gender of presenting authors? 4) With what type of institutions are first authors affiliated? 5) Is there a geographic bias with respect to where research presented at AES is conducted? 6) How have the answers to these questions changed over time?

MATERIALS AND METHODS

Dataset.-All abstracts of research presented at American Elasmobranch Society conferences are publicly available on the AES website at https://elasmo.org/abstracts ( n = 2,701, 1985-2016; Fig. 1). These abstracts were read, coded, and scored by author DSS following a coding scheme developed by all coauthors (described in detail with representative examples in Supplemental Appendix 1; see Data Accessibility).

Abstracts for poster and oral presentation abstracts were analyzed together. Any abstracts that were submitted but not presented due to an author withdrawing from the conference were included by default, as such information is not available in the database of abstracts. Only abstracts that were part of an AES section at the Joint Meeting of Ichthyologists and Herpetologists are included in the database, though some ASIH talks may mention or focus on chondrichthyan fishes. It is important to note that research presented at AES is not the only chondrichthyan research (some important research from North America and around the world may be presented at other conferences or may be published without ever having been presented at a conference), but analyzing the entire lifetime of the oldest and largest professional society in this discipline is still a useful source of insights into research trends.

Research area.-Each abstract was sorted into a predetermined research area (Supplemental Appendix 1; see Data Accessibility) based on the primary focus of the study as described in the abstract. Some research areas were methods-focused, while others were discipline-oriented or question-oriented. Forty-eight abstracts (1.77%) fit equally well in two different research areas and were counted towards both; those that focused heavily on one research area but briefly mentioned the other were only counted towards the research area of heavier focus (Supplemental Appendix 1; see Data Accessibility). Abstracts from the movement/telemetry and diet/feeding research areas were analyzed on a finer scale according to the primary method or research tool used to perform the study (satellite or acoustic telemetry in movement studies, stable isotope analysis or stomach content analysis in diet studies) because of the availability of such data in the abstracts in order to understand trends in the adoption of newer research methods.

Study species.-The focal study species of each abstract was noted when applicable. If an abstract reported a long list of species (e.g., which chondrichthyans were caught as part of a sampling survey), no focal study species was recorded from that abstract. In the case of three species groups (mako sharks Isurus spp.; sawfishes Pristis spp. and Anoxypristis spp.; and manta rays [Mobulidae] not including non-manta mobula rays, Mobula spp.), the individual species was not always mentioned in the abstract, and therefore these genera were grouped together for analytical purposes (i.e., any mention of any species of mako shark was recorded as "mako shark"). The IUCN Red List status of each commonly mentioned species or grouped-together genus (at the time of this analysis) was noted.

Demographics and affiliation.-When possible to identify, the gender of the first author of each abstract was recorded, using a list of common male and female first names from the U.S. Census Bureau ( https://www.ssa.gov/oact/babynames/limits.html) with a binary male/female gender score system. While we recognize and acknowledge that gender is not binary and this assessment of first names may not match someone's self-identified gender, we cannot assess self-identified gender from first names alone. Additionally, no member has ever identified as non-binary in our membership demographic surveys. Therefore, each mention of the gender-coded data in this study will be marked with an asterisk (*) to indicate that the gender code does not indicate self-identified gender. In cases where only the author's initials were used, or in cases where the author's gender was not possible to determine by first name, no gender was recorded.

When available, the primary professional affiliations of abstract first authors were sorted into categories (e.g., college or university, National Oceanic and Atmospheric Administration [NOAA], aquarium, museum, state-level government agency, non-profit). Mote Marine Laboratory, an independent facility, was considered its own category. The Bimini Biological Field Station is currently an independent research facility (though it was not for most of its existence), but nearly all research conducted at this research facility listed the author's home college or university as the primary affiliation, so only the primary affiliation was categorized.

Geographic scope of work.-When provided, the region, nation, or US state where research took place was recorded (excluding aquarium-based chondrichthyan research), though this is not necessarily where the author's primary affiliation is located. Globally, Canada, Mexico, and the United States were analyzed as separate countries, while other regions were analyzed as a group due to low sample size in countries within those regions as well as frequent lack of specificity within abstracts. States and regions within the waters of the United States were analyzed by state, and in three cases (Gulf of Mexico, New England, and Chesapeake Bay) a body of water rather than a state political boundary was mentioned.

RESULTS

Research area.-All abstracts except for 49 could be categorized into one of the identified research areas. The most common research areas ( Fig. 2) that AES abstracts sorted into were reproductive biology ( n = 264 abstracts), movement/ telemetry ( n = 237), age and growth ( n = 192), population genetics ( n = 176), and diet/feeding ecology ( n = 173). Though Figure 2 mentions only the most common research areas, see Supplemental Appendix 1 (see Data Accessibility) for the breakdown of all presentations by research area.

Overall, more abstracts within movement/telemetry ( Fig. 3A) and diet/feeding ecology ( Fig. 3B) used the relatively older methods (acoustic telemetry and stomach content analysis, respectively). However, since 2011, in both cases, more abstracts have focused on the relatively newer method (satellite telemetry and stable isotope analysis, respectively). There were no noteworthy trends in the framing or content of reproductive biology, population genetics, or age and growth abstracts identified during this study.

Within studies on biomechanics and functional morphology, 68 abstracts focused on the biomechanics of feeding or biting or the biology of teeth or jaws, 26 abstracts focused on swimming biomechanics including associated muscles or fins, and 20 focused on skeletal structure or function. No other research areas were broken down further due to low sample sizes.

Twenty-one abstracts were categorized as social science or interdisciplinary, despite the identification of this discipline as a conservation research priority ( Jacques, 2010; Simpfendorfer et al., 2011). Paleontology-focused talks were more common ( Fig. 4B) prior to the year 2000 ( n = 15, 1.8% of pre-2000 abstracts) than they have been in the years since ( n = 11 since 2000, 0.05% of post-2000 abstracts).

Study species.-Five hundred eleven abstracts (18.9%) either did not include a focal study species or included a list of more than five; all other abstracts included study species that were categorized. One hundred fifty-three chondrichthyan species were mentioned in at least one abstract, and 74 were mentioned in at least five abstracts. The overwhelming majority of abstracts focused on species that are a member of superorder Galeomorphii ( n = 1,465; most commonly those in the families Lamnidae, n = 197; Sphyrnidae, n = 204; and Carcharhinidae, n = 648; Fig. 5), followed by those in the superorder Batoidea ( n = 749; most commonly those in the families Myliobatidae, n = 68; Mobulidae, n = 75; Dasyatidae, n = 103; and Rajidae, n = 217; Fig. 5). Within abstracts mentioning the superorder Squalomorphii, 63% were for the family Squalidae and the rest were mostly for the families Hexanchidae and Somniosidae.

Seven of the species or groups that were featured more than 50 times are considered by the IUCN Red List to be threatened (White Shark, Sandbar Shark, Spiny Dogfish, Scalloped Hammerhead, mako sharks, manta rays, and sawfishes; Fig. 6). One Critically Endangered species (Daggernose Shark Isogomphodon oxyrhynchus) found in the waters of the Americas has never been mentioned in an AES abstract. It should be noted that nearly half of all sawfish abstracts in the history of AES were from a 2016 organized symposium ( n = 37, 41.6% of all sawfish abstracts) focusing on the biology and conservation of sawfishes, showing the value of a single focused effort such as an invited symposium to address an identified research gap.

Fig. 6

Demographics and affiliation.-The Society began with 109 founding members and, as of 2018, had 444 members (507 members in 2016 through this analysis). The AES collected its first-ever Society-wide demographic data in 2017, which found that 55.8% of members filling out the survey identify as female (202 out of 362 member respondents) and no member responded as identifying as a non-binary gender. Additionally, this 2017 demographic survey found that 34 members identify as Hispanic/Latino, 14 as Asian, three as African-American, 13 as "other," one as American Indian or Alaska Native, and one as Pacific Islander, compared to 279 that identify as white (not Hispanic or Latino). Additionally, 123 members report being the first in their family to attend graduate school.

First author binary gender based on first name could be determined for 2,247 abstracts (83%); the rest were presented in years where only first initials were listed or were presented by someone with a first name that was not categorizable as male or female using our scheme. Overall, 31.3% of AES abstracts for which the first author's gender could be categorized were delivered by women* ( Fig. 4A). The proportion of AES abstracts with female* first authors has increased steadily over time (as low as 4.3% in 1991) and was approaching 50% (44.4%) in 2016.

Affiliation was listed for 2,390 abstracts. Seventy-nine percent of AES abstracts for which an affiliation could be determined listed a university or college as the first author's primary affiliation. NOAA, Mote Marine Laboratory, aquariums, state wildlife management agencies, and museums were the primary affiliation for between 2% and 5% of the remaining talks. One talk was delivered by the owner of a SCUBA business, and four talks were delivered by presenters affiliated with the US Navy. Talks delivered by first authors with aquariums as their primary affiliation were more common in the past ( n = 38 abstracts pre-2000, 5.4% of pre-2000 abstracts) than in recent years ( n=34 abstracts since 2000, 1.4% of post-2000 abstracts) despite an increasing trend in the total number of abstracts presented ( Fig. 4B).

Geographic scope of work.-The geographic scope of work was categorizable for 1,124 abstracts. Of these, 49% percent of field research submitted as AES abstracts took place in the waters of the United States ( Table 1), primarily within the waters of California and Florida, though it should be noted that both California and Florida contain diverse ecosystems and multiple research institutions. The next most frequent nations or regions outside of the US where AES abstract research took place were the waters of South America, the waters of the Greater Caribbean (including the Bahamas), and the waters of Mexico. Within South America ( n = 113 abstracts), the most common country where research took place was Brazil ( n = 53), though abstracts with research taking place in the waters of Brazil are less common in recent years (24 abstracts pre-2000, 2.7% of pre-2000 abstracts, 29 abstracts since 2000, 1.6% of post-2000 abstracts).

Table 1

The countries or geographic regions where the research described in abstracts took place. Countries are the United States, Canada, and Mexico. All other areas on the map were grouped together as regions (due to low sample size in individual countries or a lack of country-specific reporting in abstracts, though n ≥ 5 is noted parenthetically). The Chesapeake Bay (including Virginia and Maryland), New England (including Maine and Massachusetts), and the Gulf of Mexico (including Alabama, Louisiana, and Texas) were grouped together due to lack of specificity in many abstracts in these regions, all others refer to the waters of individual states.

DISCUSSION

This study identified several patterns in research focus and the demographics of researchers in chondrichthyan science, and it also identified research gaps. Specifically, this analysis showed that certain study species and study methods dominate the abstracts submitted to AES and that some identified research priorities receive comparatively less attention. Additionally, this analysis shows that abstracts presented at AES focusing on some research areas have declined over time, as has the proportion of presenters with certain affiliations. The percentage of female-presenting authors has increased over time, but AES still shows underrepresentation of several minority groups. This information can be used to help set future research priorities for the discipline of chondrichthyan science in general and can help the American Elasmobranch Society specifically to better achieve its stated goals.

While focusing on conference abstracts does not capture every research trend in our field, analyzing the entire scope of the largest and oldest professional society in our field does highlight interesting and relevant trends. While it is unknown how many of these abstracts were eventually published, an analysis ( Verde Arregoitia and González-Suárez, 2019) found that about 60% of abstracts submitted to the Society of Conservation Biology were published within approximately two years of the conference.

Research area.-Many of the abstracts presented at AES are part of research areas related to threatened species conservation or fisheries management. Studies related to age and growth, reproductive biology, and populations are important to generating effective science-based fisheries management regulations, while studies related to movement are important for establishing spatial protections like marine protected areas (reviewed in Shiffman and Hammerschlag, 2016a).

Our study demonstrates an increase in the use of stable isotope analysis and a shift away from reliance on stomach content analysis, reflecting advances in stable isotope methodology and the use of non-lethal methods to investigate feeding ecology (see Shiffman et al., 2012). Huveneers et al. (2015) reported a similar finding in the relative frequency of these methods in abstracts for Sharks International. Our study also illustrates an increase in the use of satellite telemetry as a research method compared with acoustic telemetry. This trend was not observed with Sharks International abstracts ( Huveneers et al., 2015), and Hussey et al. (2015) found that acoustic telemetry was more commonly used than satellite telemetry for studies on elasmobranch movement. Our results also suggest that satellite telemetry studies are biased towards comparatively well-understood species. Greater use of satellite telemetry in research submitted to AES meetings may be due to distinct study species of interest, or greater financial resources available to researchers working in the Americas compared to less developed areas.

It is increasingly recognized that the social sciences are necessary to generate data important for the conservation and management of chondrichthyan fishes ( Jacques, 2010; Simpfendorfer et al., 2011). Management success is likely to be limited without understanding the social-ecological systems driving chondrichthyan population declines ( Jacques, 2010). Given that social science methodologies are an established research priority and that AES seeks to be an institutional home for all types of chondrichthyan research, the low representation of social science talks at AES is noteworthy and potentially worthy of corrective action. Huveneers et al. (2015) noted that the number of social science focused talks at Sharks International is both higher than that of AES, and increasing over time, suggesting that this important research is indeed happening but not being presented at AES. This research gap can be interpreted as a call to action for the Society to encourage additional social science and interdisciplinary research.

Research on elasmobranch biomechanics and functional morphology have largely focused on the evolution of their feeding modes (although swimming is a close second). Perhaps this is driven by public fascination of many elasmobranchs as top predators, because elasmobranchs are a major lineage of jawed vertebrates often used as models of early gnathostome evolution, or due to the taxonomic diversity associated with various jaw morphologies. More recent studies of elasmobranch functional morphology and biomechanics have used material testing to compare shark teeth performance (e.g., Whitenack and Motta, 2010) and vertebral strength (e.g., Porter et al., 2006) across multiple taxa, finite element analysis to study mechanical properties (e.g., Jayasankar et al., 2017), computational fluid dynamics (e.g., Divi et al., 2018), and computed tomography scanning (e.g., Kolmann et al., 2016).

Although other research disciplines focused on nearshore species or species of high commercial interest, studies on functional morphology and biomechanics included studies on some of the clades most underrepresented in AES abstracts, particularly torpediniforms (e.g., Lesser Electric Ray, Narcine bancrofti [ Dean and Motta, 2004a, 2004b; Dean et al., 2006, 2008], torpedo rays [ Lowe et al., 1994]), freshwater potamotrygonid rays ( Kolmann et al., 2016), and less frequently studied species of orectolobiform sharks ( Ramsay and Wilga, 2007; Motta et al., 2010). Interestingly, elasmobranch feeding morphologists seem to have found means of studying some of the largest and most experimentally intractable species, such as the planktivorous Mega-mouth Shark ( Megachasma pelagios), Whale Shark ( Rhincodon typus), and mobulid rays ( Tomita et al., 2011; Motta et al., 2010; Paig-Tran et al., 2013). Scientists have also studied jaw protrusion in deep-water species such as the Goblin Shark ( Mitsukurina owstoni; Nakaya et al., 2016) and cranial biomechanics of the White Shark ( Wroe et al., 2008). AES authors also have conducted research in comparing the functional ecology of extant and extinct taxa, i.e. representing not just current trends in biodiversity but historical ones as well ( Whitenack and Motta, 2010; Whitenack et al., 2011). However, functional morphology and biomechanical research on underrepresented groups like guitarfishes (excluding Pristis), panrays (Zanobatidae), many squalomorph sharks (but see Claes et al., 2013), and deepwater skates are still lacking.

Other methods, such as molecular techniques, are categorized as their own method-based category of research talks at AES meetings rather than being grouped according to their application. As a result, studies showing the integration of genetics with more traditional tools to study questions related to systematics, dispersal, and reproduction may appear to be less common among AES abstracts than they truly are. Additionally, while abstracts in the research areas of reproductive biology, age and growth, and population genetics have remained largely unchanged over time, this does not imply a lack of progress in these disciplines.

Some research methods, including paleontology and research performed at aquariums or zoos, have declined in frequency among AES abstracts over time. However, this research is definitely still being published, it is just not being presented at AES. Over 700 chondrichthyan paleontology papers have been published since the year 2000 (Google Scholar search by author LW), and the Association of Zoos and Aquariums (AZA) reports that US and Canadian aquarium-based researchers are currently running approximately 75 research projects at AZA facilities, plus many more field-based research projects (H. Fatzinger, North Carolina Aquariums, pers. comm.). Aquarium professionals have many possibly competing conferences including the Regional Aquatics Workshop (RAW), International Aquarium Conference (IAC), and the International Elasmobranch Husbandry Symposium; attending those meetings instead of AES may partially explain the decline in aquarium-based research presentations at AES.

Study species.-Sharks in the superorder Galeomorphii were studied far more frequently than other chondrichthyan groups, and the most studied species were coastal and frequently encountered, and/or commercial important to fisheries. The relative focus on these species may be due to logistical or funding considerations. Similarly, Ajemian and Neer (2014) noted that very few AES abstracts focused on rays, and Cotton and Grubbs (2015) noted that relatively few AES abstracts focused on deep-sea chondrichthyans despite the taxonomic richness and ecological diversity of these lineages, likely due to relative logistical difficulties in accessing these species. Huveneers et al. (2015) also noted a bias towards larger and more well-known species in abstracts presented at Sharks International conferences. It should be noted that these species, while logistically easier to access for study purposes, are perhaps not the most in need of scientific research to support their management.

Nearly 90% of all recognized chondrichthyan species, including many IUCN Red List Endangered or Critically Endangered species found in the waters of the Americas, have never been mentioned in an AES abstract ( Fig. 7). This bias towards the most charismatic or most easily accessible (e.g., coastal species vs. deep-sea or pelagic species) study species has resulted in an obvious taxonomic research gap. Skates and rays, which are historically and currently underrepresented in AES abstracts, are as a group more threatened than sharks as a group ( Dulvy et al., 2014) and therefore could benefit from additional research attention if conservation of these species remains a goal of AES researchers. Our understanding of taxonomic priorities depends largely on our evolutionary or systematic understanding of taxa; the oversampling of some lineages and the undersampling of others in the larger chondrichthyan phylogeny hinders scientific and management progress in this case ( Stein et al., 2018). Many AES members report a desire to generate scientific data to save threatened species ( Ferry and Shiffman, 2014) and report personal involvement in ocean conservation efforts ( Shiffman and Hammerschlag, 2016b), making the research gap in our understanding of particularly threatened or little known species an obvious priority for future research.

Fig. 7

Studies on rays (morphology or otherwise) have largely been limited to families represented by perhaps one or two 'model' species, such as Urotrygonidae being largely represented by studies on Urobatis halleri and U. jamaicensis, to the exclusion of any species from the more diverse sister genus Urotrygon. Representation of the largest stingray family, Dasyatidae, was also driven by studies on a few select taxa, namely eastern United States taxa like Hypanus americanus and H. sabinus. Similarly, while presentations on sawfishes have become increasingly common, any research on other guitarfishes (Rhinopristiformes) is lacking. As mentioned previously, low representation of certain taxa in studies presumably reflects their ease of capture, which may explain why deeper water and continental shelf taxa such as electric rays, deepwater myliobatiforms (e.g., Hexatrygon, Plesiobatis) and the skate families Anacanthobatidae, Arhynchobatidae, and Gurgesiellidae are discussed infrequently at meetings, and studied infrequently in general (except when encountered as by-catch). In other words, research has not been led according to which clades are the most species-rich or evolutionarily distinctive ( Stein et al., 2018), but rather by which taxa are easiest to procure, either by researchers or through targeted-fisheries and by-catch. Research on the lesser studied but harder to access species should be considered a research priority in the future.

Demographics and affiliation.-The current percentage of abstracts with female*-categorized authors (44.4%), while it has increased over time, is less than the overall demographics of the Society (55.8% of members self-identify as female) and with the number of bioscience degrees awarded to women* (53-58%, NSF). This trend is not unique to AES ( Simon et al., 2007), although causal factors have not been fully explored. From these limited data, the reasons for this trend are unclear, and follow-up survey targeting AES members could clarify reasons for demographic trends in this Society. Abstracts for non-symposium talks and posters are generally accepted upon submission, so it is unlikely that bias in abstract acceptance is in play.

Within the Society, work has begun through an equity and diversity committee to devise efforts to combat this failure to retain female and minority members. It may also benefit the Society to engage in education to help AES members, especially those in leadership roles, to learn how to better recognize and combat instances of bias in chondrichthyan science and the profession at large. Efforts could be made for symposia, where presenters are invited, to ensure diversity with respect to gender, race, or other factors. For example, the American Society for Microbiology annual meeting has shown gains in the gender balance of speakers after examining its own invited presenter gender data and sharing it with their program committee ( Casadevall and Handelsman, 2014). It is also possible that women are either attending AES, but not presenting, or not attending at all. In addition to examining past attendance records, it may be helpful to survey the membership about how members make decisions to present at and/or attend AES. Other studies show that women may find more barriers to conference travel, such as family-care duties ( Moss-Racusin and Rudman, 2010) and gender biases in grant awards that may fund conference travel ( Bornmann et al., 2007). It is important to note that while the percentage of female AES members and presenting authors has increased over time, the Society has low representation of African-American and Hispanic/Latino members compared to the United States as a whole and compared to NSF statistics of life sciences degree recipients. Further study should seek to address these issues of representation and inclusivity to ensure that AES conferences are a safe and welcoming event for everyone.

Geographic scope of work.-Some geographic regions are underrepresented as an area of study among abstracts submitted to AES, including some areas with high numbers of threatened species or widespread overfishing (see Momigliano and Harcourt, 2014). While this may be a consequence of the North American focus of the Society, it has also been noted that many developing countries have little infrastructure for chondrichthyan research, and that much of the research performed in these countries is performed by researchers based in the United States ( Huveneers et al., 2015). Some of these regions may benefit from research partners based in the developed world to increase local capacity. The decline in presentations taking place in nations such as Brazil matches membership trends in the Society, which have been attributed to Brazil founding its own local chondrichthyan research societies (SBEEL, founded in 1997), and therefore perhaps no longer attending the American Elasmobranch Society conference (J. Wyffels, AES Secretary, pers. comm.).

Conclusions and recommendations.-If the goal of AES is to be a home for chondrichthyan researchers of any discipline, purposeful action may be required to welcome researchers from these disciplines back into the community or into the community for the first time. This can take many forms, including invited symposia focusing on topics of interest or offering travel rewards. The fact that half of the sawfish-related abstracts in the entire history of the Society were associated with one invited symposium shows that this approach can be an extremely effective way to increase the Society's focus on a research topic, though symposia may result only in a temporary bump in Society attention.

The trends in chondrichthyan research discerned from AES abstracts may be useful for setting research priorities or determining future directions for the Society itself. These abstracts may also be useful for countless other research projects, and we invite any other interested researchers to explore this publicly accessible dataset at https://elasmo.org/abstracts.

ACKNOWLEDGMENTS

The authors represent current, former, and emerging leaders of the American Elasmobranch Society. Author DSS would like to acknowledge funding and support from the Liber Ero Postdoctoral Fellowship Program, the Earth to Oceans Group at Simon Fraser University, and the Save Our Seas Foundation. Author MAK was supported by a Friday Harbor Labs Post-doctoral Fellowship (NSF-DBI PRFB 1712015), and author NKD was supported by Natural Science and Engineering Research Council Discovery and Accelerator Awards, Canada Research Chairs Program, and the Shark Conservation Fund. Author MPT would like to thank NSF grant IOS-1932757 for funding some of the open access fees. The authors would all like to thank the members of the American Elasmobranch Society for generating the data used in this study, and for helpful feedback on the presentation of these data at the 2017 meeting. Other than lead author DSS, authorship order is alphabetical by last name.

© 2020 by the American Society of Ichthyologists and Herpetologists

D. S. Shiffman , M. J. Ajemian , J. C. Carrier , T. S. Daly-Engel , M. M. Davis , N. K. Dulvy , R. D. Grubbs , N. A. Hinojosa , J. Imhoff , M. A. Kolmann , C. S. Nash , E. W. M. Paig-Tran , E. E. Peele , R. A. Skubel , B. M. Wetherbee , L. B. Whitenack , and J. T. Wyffels "Trends in Chondrichthyan Research: An Analysis of Three Decades of Conference Abstracts," Copeia 108(1), 122-131, (6 March 2020). https://doi.org/10.1643/OT-19-179R

Received: 14 January 2019; Accepted: 28 November 2019; Published: 6 March 2020

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Trends in Chondrichthyan Research: An Analysis of Three Decades of Conference Abstracts

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Given the conservation status and ecological, cultural, and commercial importance of chondrichthyan fishes, it is valuable to evaluate the extent to which research attention is spread across taxa and geographic locations and to assess the degree to which scientific research is appropriately addressing the challenges they face.

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WWF supports research and monitoring of white sharks as they migrate to and from the Gulf of California. Sharks are tagged and the movements are tracked by satellite. This information on their behavior will help with a management plan for the protected area where they are found (Guadalupe Island Biosphere Reserve), such as how to protect them from bycatch and to regulate tourism.

HOW YOU CAN HELP

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The great white shark is the world's largest known predatory fish. It has 300 teeth, yet does not chew its food. Sharks rip their prey into mouth-sized pieces which are swallowed whole. The shark's heavy, torpedo-shaped body allows it to cruise efficiently for long periods of time, and then suddenly switch to high speed bursts in pursuit of prey-sometimes leaping out of the water. It feeds on a broad spectrum of prey, from small fish, such as halibut, to large seals and dolphins.

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The great white shark population is decreasing due to years of being hunted by man for fins and teeth, and often as a trophy for sport fishing. Learn more about what WWF is doing to protect its future, and how you can help.

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HEATHER MARSHALL, PHD
Field Lab Consulting co-founder Dr. Heather Marshall is a marine scientist specializing in shark stress physiology. Her research interests are focused primarily on shark physiological ecology, with an emphasis on capture-related stress physiology and post-release mortality.

KRISTINE STUMP, PHD
Dr. Kristine Stump is a marine biologist specializing in tropical marine ecology. Her research interests and background include shark ecology, predator-prey interactions, fish spawning aggregations, effects of anthropogenic activities on species and habitats, and using telemetry to investigate spatial ecology.

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kristine stump, phd

Dr. Kristine Stump is a marine biologist specializing in tropical marine ecology. Her research interests and background include shark ecology, predator-prey interactions, fish spawning aggregations, effects of anthropogenic activities on species and habitats, and using telemetry to investigate spatial ecology.

Dr. Stump has years of marine policy experience in Washington, D.C. working at the federal level toward the establishment of an Integrated Ocean Observing System (IOOS) for the U.S. In addition, she has worked in The Bahamas on science-based policy and management of marine resources.

Dr. Stump served as the Principal Investigator of the Bimini Biological Field Station in Bimini, Bahamas, where she researched the effects of nursery habitat loss on lemon sharks ( Negaprion brevirostris). As a Postdoctoral Research Associate at the Shedd Aquarium, she spent several years as Chief Scientist aboard Shedd's research vessel in The Bahamas, where she used acoustic telemetry to study the migrations of endangered Nassau grouper ( Epinephelus striatus) to and from spawning aggregations.

A certified Atlantic and Gulf Rapid Reef Assessment (AGRRA) surveyor, Dr. Stump has conducted numerous reef surveys and collaborated on coral restoration efforts in Florida and The Bahamas.

Dr. Stump has over ten years of teaching experience at graduate, undergraduate and high school levels, including leading courses on biology, marine and island ecology, tropical marine ecology, coral reef ecology and invertebrate zoology and environmental science. Most recently, she was a Lecturer of Marine Conservation Biology in the graduate program at the University of Miami Rosenstiel School of Marine and Atmospheric Science. Currently, Dr. Stump teaches at a private independent school in Miami, FL.

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Dr. Kristine Stump is a marine biologist specializing in tropical marine ecology. Her research interests and background include shark ecology, predator-prey interactions, fish spawning aggregations, effects of anthropogenic activities on species and habitats, and using telemetry to investigate spatial ecology. Dr. Stump has years of marine policy experience in Washington, D.C.

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Recovery plan for the White Shark (Carcharodon carcharias)

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Recovery plan for the White Shark (Carcharodon carcharias)

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This recovery plan sets out the research and management actions necessary to stop the decline of, and support the recovery of, the white shark in Australian waters. The plan considers the conservation requirements of the species across its range and identifies the actions to be taken to ensure the species' long-term viability in nature and the parties that will undertake those actions

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Department of Agriculture, Water and the Environment

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About this document

This document constitutes the Australian National Recovery Plan for the White Shark. The plan considers the conservation requirements of the species across its range and identifies the actions to be taken to ensure the species' long-term viability in nature and the parties that will undertake those actions. This is a revision of the 2002 White Shark ( Carcharodon carcharias) Recovery Plan (EA, 2002) and should be read in conjunction with the 2013 Issues Paper for the White Shark ( Carcharodon carcharias) (DSEWPaC, 2013).

This recovery plan sets out the research and management actions necessary to stop the decline of, and support the recovery of, the white shark in Australian waters. The overarching objective of this recovery plan is to assist the recovery of the white shark in the wild throughout its range in Australian waters with a view to:

improving the population status, leading to future removal of the white shark from the threatened species list of the EPBC Act

ensuring that anthropogenic activities do not hinder recovery in the near future, or impact on the conservation status of the species in the future.

Issues paper

The accompanying issues paper provides background information on the biology, population status and threats to the white shark.

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Department of Agriculture, Water and the Environment

# data[].attributes.attachment_link.description
About this document This document constitutes the Australian National Recovery Plan for the White Shark. The plan considers the conservation requirements of the species across its range and identifies the actions to be taken to ensure the species' long-term viability in nature and the parties that will undertake those actions.

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Researchers of UNC Institute of Marine Sciences

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Researchers of UNC Institute of Marine Sciences

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The longest running shark survey in the U.S. takes place off the coast of North Carolina. After nearly 50 years, Carolina researchers are still making discoveries.

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The survey methods may be the same, but the science has evolved - and so have the stakes.

Since 1972, researchers from the UNC Institute of Marine Sciences (IMS) have used baited longlines to capture and release sharks in order to gather data critical to understanding the ancient predators. The baseline established in 1972 relied on visual observation of the sharks' size and species. While size and species type are still important, today's Carolina scientists are studying isotopes from tissue samples and the molecular makeup of cells for clues about breeding, eating habits and other behaviors and even wider ecosystem trends and warning signs.

Using the latest research methods, from a small sample of a shark's tissue, a scientist can learn about the health and abundance of the shark's principal prey and, in turn, which species are declining or emerging in the ecosystem. Those variances often indicate habitat loss, over-fishing or even pollution affecting a key species in the food chain. By leveraging the largest and longest-running collection of data on shark populations in the U.S. with new research techniques, future researchers can use sharks as a litmus test for ocean health and climate change.

Fishing for data

Professor Frank Schwartz officially started the shark survey in 1972, although he unofficially began collecting data on sharks off the coast of North Carolina in 1965. What's most remarkable about the program, however, is how consistent it has remained over nearly a half century. The researchers gather survey samples from the same location using the same gear - including the same type of boat - meaning that ostensibly the data is comparable across time. The composition of shark species in each survey is the only changing variable - sharpnose and blacknose are now caught more frequently than other species, in contrast to the overall diversity of past data.

The survey takes place on a 48-foot research vessel, the Capricorn, at two locations off the coast of Shackleford Banks in Carteret County, North Carolina. Once every two weeks in the spring, summer and fall, the Capricorn's captain navigates to fixed stations, between one and seven miles out to sea, while a crew of faculty, staff and graduate students deploy a trawling net out behind the boat to catch small bait fish. The crew members then bait up to 100 hooks on short lines, called gangions, and attach those at intervals to the mainline, which they trail behind the boat for almost a mile. After exactly one hour, they reel in the mainline and, one by one, researchers identify, measure and record information about the day's catch.

The goal is to gather all the necessary data quickly to avoid harming the sharks, so all faculty, staff and graduate students aboard work simultaneously. They identify each shark by species and then record the length from the end of the snout to the tip of the tail. Depending on the researchers aboard that day, different biological samples are also taken - a small piece of tissue, a blood draw or a swab of the shark's digestive track. Finally, they tag the shark, in case it is ever caught again by another fisherman or group, and release it back into the water. The entire process takes less than two minutes per shark. Forty-eight years of practice makes perfect.

Did you know? Sharks tagged off the coast of North Carolina have migrated all the way to California.

Although ecologists have measured and identified over 10,000 sharks since the beginning of the survey, current research has shifted to examining sharks at the microscopic level.

Old survey, new research

Ph.D. candidate Jeff Plumlee in the enviroment, ecology and energy program (E3P) in the College of Arts and Sciences studies how sharks fit into the food web by analyzing what molecules make up their cellular structure, using the concept "you are what you eat."

"I collect a small tissue sample from the sharks and look at the stable isotopes that make up those tissues, and calculate the proportion of naturally occurring carbon, nitrogen or sulfur isotopes that make up the shark," Plumlee said. "I can then identify what food sources most closely resemble the signatures we see within the sharks' tissues, which gives us an idea of what the sharks' primary food sources are and helps us understand what other species are dietarily important within the food web."

Plumlee isn't alone in his research; graduate student Savannah Ryburn, also of the E3P program, is trying to answer the same research question but through a different technique.

"I swab each shark's intestinal tract for fecal matter and use DNA analysis to break down the different living organisms that make up its diet," said Ryburn. She and Plumlee can later compare the results of their respective studies and check if they jibe.

Ryburn's research is well-suited to the shark survey, but she originally planned on conducting her study almost 3,000 miles away at the Galapagos Science Center. The travel required for her research this summer became impossible during the COVID-19 pandemic, and when she and her advisor, Professor John Bruno of the department of biology in the College of Arts and Sciences, searched for a local alternative, they found the perfect fit for her at the IMS.

Both Plumlee and Ryburn's research provides new ways for ecologists to map out how sharks fulfill different roles in a variety of ecosystems. Sharks are highly migratory and travel long distances, even traversing oceans depending on the season, and their diets can vary widely depending on location and time. When sharks co-occur, there is a partitioning of resources among different species of sharks that is based on their dietary preferences and life stage. However, how and when sharks change their diets is still not fully understood by scientists. The new methods used by the researchers at IMS to track sharks' diets and molecular makeup will help researchers understand diet specialization among, and potentially even within, shark species.

The importance of tracking different sharks' diets is also based on the species' role as "ecosystem engineers" that regulate the diversity and distribution of prey. That regulation is essential to maintaining the precarious balance in estuaries, shallow bodies of water where fresh and salt water meet, which serve as essential habitat for animals that make up a large portion of the coastal food web. Sharks, small fish and even shellfish all live in estuaries for at least part of their life cycles, and many live in the brackish water for their entire life cycle.

Balancing the ecosystem

According to Associate Professor Joel Fodrie at the IMS, sharks are key species to measure because they often represent the health of their ecosystem.

"Sharks serve as a 'canary in the coal mine,'" said Fodrie. "They integrate all the irregularities that surround them, so if the water quality gets screwed up, or the crab population suddenly decreases, sharks register all those changes and can reflect the fact that your system is performing differently."

Although these "canaries" have a bigger bite, sharks are as vulnerable to environmental changes as any other species. Some sharks rely upon healthy estuaries to reproduce, and smaller sharks make the brackish, shallow water their permanent home. When their natural prey either exceeds its population or decreases suddenly, there can be disastrous repercussions for marine life from the top to the bottom of the food web.

Fodrie uses a recent observation of the sea turtle population to illustrate the effect: "Sea turtle numbers are increasing because there's less control on their population due to decline in shark numbers. But, as a result, in some parts of the world turtles are mowing sea grass down at an irreplaceable rate. Sea grass is a habitat and breeding ground for smaller fishes and invertebrates, so without those grasses we see these smaller animals decline in numbers - some of which are ecologically or economically prized themselves."

Surveying the decline

The diversity of shark species found off the coast of North Carolina in different seasons has remained steady at around 50 since the first UNC-IMS longline shark survey, but data shows a clear decline in overall shark population since 1972.

"There are several species of sharks that are thought to be overexploited, mostly medium to large species, like dusky sharks or sandbar sharks," said Fodrie. "The survey data would suggest that since the 1980s, the numbers of medium to large sharks in North Carolina have slowly declined."

The decrease in population may be due to any one or a combination of factors: habitat loss, pollution or food sources disappearing. An irrational fear of shark attacks also permeates popular culture and silences calls for preservation, usually cited as beginning when "Jaws" hit theaters in 1975. In response to that fear, Fodrie said he would remind everyone that their chances of being attacked by a shark are so small, it's almost incalculable.

"Sharks are incredibly efficient and skillful hunters, so they would only bite a human if they were confused by either sight or smell and mistook you for prey," said Fodrie. "Under normal circumstances they have no interest in humans. Everyone who has been in the ocean has likely been within 100 yards of a shark, but only an average of five people die from shark encounters per year in the entire world."

Did you know? You're more likely to die being struck by a champagne cork than from a shark encounter.

The survey continues

The hallmark of the IMS shark survey is its longevity, and as the second faculty member to lead the project, Fodrie hopes the survey will continue for another 50 years.

"A data set this extensive is uniquely remarkable, and our data will be important to future researchers in multiple fields," said Fodrie. "Shark population numbers can also be used to measure the effects of climate change and pollution in the ocean, which will be very valuable in the near future."

During trips to sea in the summer of 2020, the survey has reflected a slight increase in populations of threatened species since 2018. Fodrie believes this is a positive sign that some threatened species may be making a comeback, which is a trend he's happy to record.

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The past, present and future of shark research - The Well

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The survey methods may be the same, but the science has evolved - and so have the stakes. Since 1972, researchers from the UNC Institute of Marine Sciences (IMS) have used baited longlines to capture and release sharks in order to gather data critical to understanding the ancient predators.

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Extinction risk and conservation of the world's sharks and rays

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Extinction risk and conservation of the world's sharks and rays

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The rapid expansion of human activities threatens ocean-wide biodiversity. Numerous marine animal populations have declined, yet it remains unclear whether these trends are symptomatic of a chronic accumulation of global marine extinction risk. We present the first systematic analysis of threat for a globally distributed lineage of 1,041 chondrichthyan fishes—sharks, rays, and chimaeras. We estimate that one-quarter are threatened according to IUCN Red List criteria due to overfishing (targeted and incidental). Large-bodied, shallow-water species are at greatest risk and five out of the seven most threatened families are rays. Overall chondrichthyan extinction risk is substantially higher than for most other vertebrates, and only one-third of species are considered safe.

The largest sharks and rays are in the most peril, especially those living in shallow waters that are accessible to fisheries. A particular problem is the ‘fin trade’: the fins of sharks and shark-like rays are a delicacy in some Asian countries, and more than half of the chondrichthyans that enter the fin trade are under threat. Whether targeted or caught by boats fishing for other species, sharks and rays are used to supply a market that is largely unmonitored and unregulated. Habitat degradation and loss also pose considerable threats, particularly for freshwater sharks and rays.

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Shark species, as an apex predator of the sea, are critical to the stability and health of ecological systems. Without these sharks present, prey populations such as pinnipeds or fish will significantly increase. This will subsequently result in a top-down effect in the food chain.

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Researchers from the Large Marine Vertebrates Research Institute Philippines (LAMAVE) 

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Researchers from the Large Marine Vertebrates Research Institute Philippines (LAMAVE) 

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LAMAVE has been working on supporting MPA creation and enhancement, identifying priority areas for conservation and understanding sharks and rays’ spatial ecology in the Philippines and the Coral Triangle since 2012.

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Large Marine Vertebrates Research Institute Philippines

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SHARK RESEARCH & CONSERVATION

Amid the global decline of shark and ray species, collecting baseline information is crucial to develop effective management tools to aid in their conservation. According to recent reports, more than 25% of sharks and rays are now threatened with extinction and the list includes many of the species present in the Philippines.

SHARKS IN THE PHILIPPINES

The Philippines is one of the world's hotspots for shark and ray diversity with a great number of species present, at least historically. Unfortunately, most of them are very hard to find nowadays, mostly due to overfishing. Approximately 200 species of sharks and rays are thought to inhabit Philippine waters, yet data on the current status of their populations in the country is limited.

Sharks and rays are highly vulnerable species. Their life strategy of growing to a relatively large size, reaching sexual maturity very late in life and producing a small number of offspring put them at great risk of overexploitation, making it hard for them to cope with common threats like overfishing and habitat degradation.

Targeted hunting and by-catch, and why tourism is not a solution for all

Targeted hunting is still a common practice in the Philippines, primarily representing a cheap source of protein for the local communities, and in a few cases, a highly demanded local dish. When coupled with the extensive by-catch, both from millions of small scale fishers and the commercial fishing fleet, there is a very little hope left for shark populations to survive.

Even iconic sharks like the pelagic thresher sharks, that attract thousands of visitors from around the world to the island of Malapascua in Cebu, are still landed illegally by the thousands in the nearby provinces.

Reducing the mortality of these animals from fishery operations is the only hope to save the global shark population. Though a complex task involving fishers' livelihood, behavioral change, alternative fishing practices and gear use, genuine interest and participation from the local communities, and strong political will, we may be able to change the fate of these oceanic predators to thrive in the oceans once again

While shifting to tourism is the best solution for some communities, it is not an easy option to scale up nor is it appropriate for all scenarios. It often comes at a great social and cultural cost.

Marine Protected Areas - a solution?

MARINE PROTECTED AREAS - A SOLUTION - WHEN OF SUFFICIENT SIZE AND PROPERLY MANAGED
Many of the smaller and more threatened shark and ray species do not migrate and consequently spend most of their life along the shores of the same island or municipality, often concentrating around healthier or richer habitats. For them, medium-size Marine Protected Areas, when properly designed and managed are the best and most sustainable long-term solution.

The Philippines has one of the highest number of Marine Protected Areas in the world, with over 1800 designated areas (nearly 20% of the world MPAs), in paper at least. Most of them unfortunately, are not managed at all and those that are usually have low patrolling and surveillance activity. To add to this, most of the MPAs are not designed following any specific biological criteria or to protect a specific target species. Above all, they are too small to include enough range to protect sharks and rays, even the most sedentary of them.

Medium and large size MPAs, especially when designed to specifically protect sharks and rays, are a great solution to ensure the conservation of these species and allow their population to recover and start recolonizing many of the shark barren reefs in the country.

Tubbataha Reefs Natural Park and World Heritage Site is an exemplary success and a reflection that proper management and appropriate size makes a difference to the future of these animals. Now, 30+ years after its inception, the park hosts one of the largest recorded densities of grey reef sharks and white tip reef sharks in the world.

Apo Reefs Natural Park is a good example of adequate size (15,792 ha plus 11,677 ha buffer zone) for shark protection. However, it has displayed poor enforcement, governance and management for many years, with disputes over the use of its waters by local governments and communities. Despite these challenges, reef sharks and rays are still present at levels much higher than areas that receive no protection at all.

OUR WORK

Our main strategy to ensure the conservation of sharks and rays in the Philippines is to understand the spatial use (how animals use the environment and how much space they need) of these species and to identify priority areas for their conservation. These data are then used to create tools and provide information to assist in the design of new MPAs or enhance existing ones, in collaboration with local and national stakeholders.

To further complicate the issue, every year a few species of shark move great distances, migrating to breeding grounds or in search of food. For these species, like the tiger sharks, hammerhead sharks, silky sharks, thresher sharks as well as the whale sharks, a single localzied MPA, even if relatively large, is insufficient to guarantee their survival, once they start migrating and leave the boundaries of the MPA.

In such cases, a solution is establishing Networks of MPAs in areas where these species spend the majority of their life, or in areas that are particularly important such as mating and pupping grounds, cleaning stations, and feeding aggregation sites. These networks, complimented by Protected Migratory Corridors to allow for safe passage between these sites, would provide effective protection for these migratory species.

All of the above require a great deal of work and collaboration among the communities, fishing industry and local government units (LGUs), as well as political engagement and buy in, and proper enforcement to attain impactful results. Even when not all the stars are aligned, they still work better than many other solutions and are especially better than doing nothing at all.

LAMAVE has been working on supporting MPA creation and enhancement, identifying priority areas for conservation and understanding sharks and rays' spatial ecology in the Philippines and the Coral Triangle since 2012.

To collect data in support of our conservation work we apply many different research methods including but not limited to:

Habitat assessment

Tourism Economic Evaluation

UAV (drone) surveys

Focal Animal Follows at cleaning stations (behavioral study)

Rapid Bycatch Assessment (Focal Group Discussion, House Hold Interview, Key Informant Interview)

Market and landing surveys

Nationwide Shark and Ray Assessment

Most of the shark and ray population assessments around the world are done through data obtained from fisheries (fishery dependent data), basically counting how many shark you can catch with the same effort in the same area year after year, and then compute what, most probably, is left alive.

In 2015 we partnered with the Global Fin Print Project as part of an international effort to assess the current status of live sharks and rays in coral reefs worldwide, focusing on a standardized method to count free swimming sharks and rays. As the Philippine counterpart, our team deployed Baited Remote Underwater Video Systems (BRUVS) in multiple sites across the country to gain an understanding of shark and ray biodiversity and abundance, in general and more specifically comparing inside and outside protected areas.

After 3 years of data collection the project will be repeated again in five (5) years to compare and identify changes in the presence and abundance of these species in selected sites.

The results show a general lack of reef sharks across the country, even in good habitats, confirming that overfishing has long taken a toll on most remaining populations. It also shows that within properly designed and managed protected areas, like Tubbataha Reefs Natural Park and World Heritage Site, shark and ray populations still thrive, offering a ray of hope for the future of these threatened and charismatic species.

KEY FINDINGS:

Updated as of April 2020

General absence of sharks and rays outside large protected areas.

While size is important, management and enforcement is equally fundamental and large protected areas with poor management have shark density 10 times lower than in well managed large protected areas.

Most shark populations have been extirpated in the Philippines and urgent actions are needed to save these species.

Tubbataha Reefs Natural Park and the Cagayan Ridge

TUBBATAHA REEFS NATURAL PARK

Tubbataha Reefs Natural Park and World Heritage Site (TRNP) is located in the Sulu Sea, approximately 170 km southeast of Puerto Princesa City, Palawan, and approximately 100 km south of Cagayancillo, which is the closest human settlement.

It was established as a no-take MPA in 1988, listed as a United Nations Educational, Scientific and Cultural Organization World Heritage Site in 1993, included in the Philippines National Integrated Protected Area System (NIPAS; Republic Act No. 7586) since 2009 and is presently the largest no-take MPA in the country, covering an area of approximately 1000 km2.

Its boundaries are enforced year-round by marine park rangers consisting of personnel from the Tubbataha Management Office, Philippine Coast Guard, Philippine Navy, and representatives from the local government unit (LGU) of Cagayancillo, who conduct regular joint patrols and monitor vessel activity throughout the park using a radar system.

The park is a popular tourist destination, although recreational diving activities are mostly limited to a March-June window due to the unfavourable weather condition for dive boats during the rest of the year.

Despite having been a shark diving destination for at least two decades, little was known about the status of the population of sharks and rays within and outside the park boundaries, the effectiveness of the park for each species, and the diversity and richness of these species in the park.

SHARK ABUNDANCE AND DIVERSITY

LAMAVE first began working in Tubbataha Reefs Natural Park in 2015 to assess shark and ray abundance and diversity. In collaboration with the Tubbataha Management Office, the team identified the presence of 15 species of sharks and rays within the waters of the park using Baited Remote Underwater Visual Systems (BRUVS) and Underwater Visual Surveys, reporting at time of publication. While Underwater Visual Survey (UVS) and BRUVS reported some of the highest densities of grey reef sharks and whitetip reef sharks known worldwide.

MARINE PROTECTED AREA DESIGN AND SHARK MOVEMENT

To better comprehend the role of Tubbataha Reefs Natural Park (TRNP) in the conservation of different kinds of sharks and rays, in 2015 we started using telemetry (tagging) to follow individual animal movements within and outside the park boundaries. This method allows us to understand not only where, when and how different species use the park, but also provides an insight into their long range movement across the Sulu Sulawesi ecoregion.

We selected 4 species that represented the different "Type" (taxonomic group) of sharks and rays that move around the park: whale shark and manta ray (large filter feeders known for long range movements), grey reef shark (small-to-medium-sized reef associated shark, highly abundant in the park year round and fairly resident), and the tiger shark (a species of shark often associated with particular coral reefs, known to be capable of large migration and to come back regularly to the same feeding and pupping area).

In collaboration with Tubbataha Management Office (TMO) and under the supervision of Palawan Sustainable Development Council (PCSD), we tagged over 30 individuals using satellite tags (whale sharks and tiger sharks) and acoustic tags (tiger shark, manta ray, grey reef shark).

Most of the tags deployed have a life span of approximately 10 years and are still actively transmit data year-round.

Preliminary data show a high residency of grey reef sharks, with very little movement between the north and south atolls and Jessie Beasley shoal that form TRNP, and no recorded movement outside the park boundaries. Manta rays displayed long periods of residency with daily presence for several months before disappearing. Tiger sharks appear to be relatively resident moving widely around the park and visiting nearby reefs like Cagayancillo but also engaging in long range movements south towards Mindanao. Lastly, individual whale sharks use the park only for a day or so, before continuing their movement across the whole Sulu Sea, towards the Bohol Sea and Pacific on the east and south towards Borneo and the Sulawesi.

Using the data from TRNP, not only can we support and enhance the management of the Park, but we are helping create several additional Marine Protected Areas designed and dedicated specifically for the conservation of sharks and rays in South East Asia.

CAGAYANCILLO - A NEW SHARK HAVEN?

Tubbataha Reefs Natural Park and World Heritage Site sits in the waters of the Municipality of Cagayancillo (Palawan). Cagayancillo includes several other isolated small island, atolls and shoals where coral reefs are still in pristine condition and supports a relatively low human population.

In 2016 we expanded our work from TRNP to the waters of the entire municipality.

Preliminary data from the Baited Remote Underwater Video surveys show promising results. Populations of both reef and pelagic species of sharks and rays remain common in deep waters, but are absent in shallow reef and areas close to the human settlements.

The current focus of the project, in collaboration with WWF-Philippines, is to assess the feasibility of establishing a dedicated 'shark sanctuary' managed by the local communities to allow the shark populations to recover to levels similar with that of TRNP. We are also working to support the development of dedicated shark diving tourism in the area, bringing non-extractive (without killing the animal) livelihood to this remote area.

KEY FINDINGS:

Updated as of April, 2020

TRNP hosts one of the highest densities of grey reef sharks and whitetip reef sharks in the world

Highest chance to encounter hammerhead and tiger sharks in the Philippines

Presence of large schools of pelagic sharks like silky sharks offshore from the reef systems.

Identified and confirmed the presence of 23 shark & ray species inside TRNP

Acoustic telemetry confirmed connectivity between TRNP and Cagayancillo for manta rays and tiger sharks.

Highest density of scalloped hammerhead shark in the North Sulu Sea

Absence of reef sharks in the shallow reefs of Cagayancillo due to overfishing

High presence of eagle ray and the only reported encounter with a rare ornate eagle ray

Shark Highway: Open Telemetry Network

Identifying priority areas for the conservation of sharks and rays is the fundamental first step to be able to design and create effective protection mechanisms like Marine Protected Areas (MPAs) to prevent these species from local extinction.

But protecting isolated habitats alone, while fundamental, is often not enough especially for larger species that can travel thousands of kilometres a year. First, protected areas need to be connected with each other and designed not individually but as a network. Then these areas need to be connected by safe passage zones, or migratory corridors, that allowed individual animals to move between important habitats reducing the chances of getting fished.

To be able to identify these areas and understand the movement and connectivity between them, we created the first Open Access Acoustic Telemetry Network in South East Asia.

WHAT IS AN OPEN ACCESS ACOUSTIC TELEMETRY NETWORK?

Acoustic telemetry is a relatively affordable way to determine movement patterns and habitat use of animals utilizing small, low-cost tags, active for up to 10 years, that emit at regular intervals, a coded inaudible ultrasound unique for each tagged individual. These sounds are picked up and recorded by a network of listening stations (acoustic receivers) placed in strategic locations across the country.

The most important aspect is the "Open Access" which means the code and receivers used are universal and anyone can purchase and deploy their own tags and additional listening stations and utilize the data downloaded from the whole network. This is very important to ensure both the maximum coverage for large scale study, but above all, to allow local research groups without large initial funding to only purchase a few cheap tags and utilize the existing network of receivers at no cost.

The network is available to any type of movement studies for all marine species, not limited to sharks and rays. LAMAVE is working to expand the network across the Tawi-Tawi, Visayas, Palawan and Southern Luzon to increase the resolution of local movement studies, as well as collaborating and supporting neighbouring countries like Malaysia and Indonesia to build their own network and join the Open Access database.

By the end of 2020 LAMAVE and the Open Access Acoustic Telemetry Network partners will have deployed 35 Acoustic Receivers and tagged over 50 sharks including tiger sharks, pelagic thresher sharks, grey reef sharks and reef manta rays.
If you are interested to join the Open Access Acoustic Telemetry Network for your own research project contact us here or to support the network by helping to purchase acoustic tags and receivers, please click here.

Tubbataha Reefs Natural Park: the first comprehensive elasmobranch assessment reveals global hotspot for reef sharks. R. Murray, S. Conales Jr., G. Araujo, J., Labaja, S. Snow, S. Pierce, A., Songco, A. Ponzo; Journal of Asia-Pacific Biodiversity, October 2018

Occurrence of the rare and Endangered Ornate Eagle Ray, Aetomylaeus vespertilio (Bleeker, 1852) (Chondrichthyes, Myliobatidae), at a remote marine protected area in the Philippines. Araujo, A., Snow, S.J., Cornish, A., Murray, R., Delijero, K., Ponzo, A., Dygico, M. Check List. 2018

Satellite tracking of juvenile whale sharks in the Sulu and Bohol Seas, Philippines. Gonzalo Araujo, Christoph A. Rohner, Jessica Labaja, Segundo J. Conales, Sally J. Snow, Ryan Murray, Simon J. Pierce and Alessandro Ponzo, PeerJ. 2018

Latest News on Sharks from LAMAVE:

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Shark research and conservation in the Philippines - Large Marine Vertebrates Research Institute Philippines

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Amid the global decline of shark and ray species, collecting baseline information is crucial to develop effective management tools to aid in their conservation. According to recent reports, more than 25% of sharks and rays are now threatened with extinction and the list includes many of the species present in the Philippines.