Endemic elasmobranch species from South America, accessed through the International Union for Conservation of Nature (IUCN)’s red list of threatened species.
Abstract
Elasmobranchs (sharks and rays) generally have intrinsic biological characteristics (e.g., low fecundity, large body sizes, slow growth rates, late sexual maturity, and long lifespans) that make them highly vulnerable to anthropic actions. Predatory fishing, pollution, and degradation of natural habitats have been declining strongly the populations of sharks and rays worldwide. It is essential to understand the diversity of species that occur in this very limited group (∼1200 species), in addition to identifying their level of endemism in coastal and island areas. In this context, several non-lethal techniques can be developed and used to help better understand the ecology and behavior of these sharks and rays, with the hope of contributing to the conservation of this fascinating group.
Keywords
- diversity
- ecology
- conservation
- non-lethal methods
- marine protected area
1. Introduction
Living fishes are comprised of two primary taxonomic groups, which are classified as bony fishes (class Osteichthyes) and cartilaginous fishes (class Chondrichthyes). The class Osteichthyes makes up about 95% of modern fishes, including an impressive array of body forms. In general terms, the Chondrichthyans have a long evolutionary history, reaching back over 450 million years. Modern chondrichthyans are normally separated into two groups, the Elasmobranchii and the Holocephali [1]. The subclass Elasmobranchii is composed of sharks and batoids (skates and rays) with more than 1200 species across 70 families. The Holocephali is represented only by the chimeras, which include more than 50 species across three families, living mainly in the deep sea [2].
Despite the reduced number of species, compared to bony fish (∼34,000 species), the elasmobranchs can inhabit a wide variety of environments. The sharks and batoids are essentially found in marine ecosystems, being present in all the world’s oceans of both hemispheres, from the Arctic to the Antarctic. However, they also could occur in estuaries and freshwater habitats (e.g., stingrays from the Potamotrygonidae family). This diversity of habitats in which the group can occur is accompanied by a variety of sizes and shapes, ranging from classic aerodynamic-shaped sharks to dorsally flattened skates and rays [3]. Sharks and rays vary greatly in size, from individuals with a maximum total length of ∼23 cm (e.g., the Pygmy ribbontail catshark,
Although historically sharks and rays have been considered long-lived and slow-growing, there is a diverse range of growth patterns and life-history strategies found in chondrichthyans [5]. The differences in energetic absorption, use, and excretion of an individual, enable the most growth functions. For example, when a specimen reaches sexual maturity, there are indicators of increased energy designation to the reproductive system, thus transferring resources away from somatic growth and into reproductive growth. The differences in growth, between males and females, have already been extensively reported, with a pattern that females frequently get a larger size than males [6, 7].
All elasmobranchs exhibit internal fertilization, low fecundity, and late sexual maturity; however, there is an ample range of reproductive models displayed by the group. Particularly for females, it is possible to verify a variety of strategies to provision developing embryos with nutrients. In this sense, organisms can be classified as lecithotrophic, when the embryo’s nutrition occurs exclusively through the yolk sac’s reserves, and matrotrophic, for species where the female supplies embryos with yolk and one or more auxiliary sources of nutrition. Reproductive models are further classified about the site of embryonic development, with species designated as oviparous (e.g., nurse shark,
The elasmobranchs occur at a variety of trophic levels, using a series of strategies to find and capture their prey, ranging from planktivorous species (e.g., Mobula rays) up to carnivorous predators (e.g., Tiger shark,
The intrinsic biological characteristics (e.g., low fecundity, large body sizes, slow growth rates, late sexual maturity, and long lifespans) reported here demonstrate how sharks and rays are highly vulnerable to anthropogenic actions. The identification of essential habitats for feeding and reproduction of elasmobranchs is especially important to preserve the balance and conservation of populations. Predatory fishing, pollution, and degradation of natural habitats have been declining strongly the populations of sharks and rays worldwide. In this sense, the present chapter aimed, in addition to reporting important biological characteristics mentioned here, to highlight the degree of diversity and endemism of elasmobranchs found in South America, in addition to simultaneously highlighting non-lethal alternatives for the development of sustainable research, used to help better understand the ecology and behavior of these sharks and rays, with the hope of contributing to the conservation of this fascinating group.
2. Materials and methods
2.1 Diversity, endemism, and species conservation status
Endemic species are found exclusively in a specific geographic region and are not found naturally in other parts of the world. The methodology used, in this chapter, to evaluate the diversity and endemism of elasmobranchs in South America was conducted through in-depth research carried out on the International Union for Conservation of Nature (IUCN)’s Red List of Threatened Species platform, which allowed the use of series of filters (e.g., habitat occupied by the species, taxonomic description, and area of occurrence, among others). Additional research on manuscripts was also carried out. From the data obtained, it was possible to reach a broad overview of the endemic species that occur in coastal and island environments, in addition to an assessment of their population status. A global total of 1194 elasmobranchs evaluated by the IUCN’s Red List of Threatened Species was verified; among these, 256 correspond to sharks and rays that occur around South America, of which 38 (∼15%) are endemic species. Among the marine elasmobranch’s endemic to South America, 68.4% correspond to rays, and 31.6% were represented by sharks. The species were distributed into 16 families, with a greater number of families being found for batoids than for sharks, with the Rajidae family representing the largest number of skates (Table 1).
Scientific name | Family | Habitat | Geography rangy | IUCN |
---|---|---|---|---|
Arhynchobatidae | MN, MDB | Brazil to Argentina | CR | |
Rajidae | MN, MDB | Falkland Islands* | LC | |
Narcinidae | MN | Argentina | DD | |
Rajidae | MN, MDB | Chile | EN | |
Arhynchobatidae | MN | Chile (Malvinas)* | LC | |
Emopteridae | MDB | Chile | LC | |
Rajidae | MDB | Ecuador (Galápagos)* | LC | |
Urotrygonidae | Unknown | Chile | DD | |
Rajidae | MDB | Brazil | LC | |
Narcinidae | MDB | Brazil | VU | |
Pentanchidae | MDB | Ecuador (Galápagos)* | LC | |
Etmopteridae | MDB | Chile | VU | |
Somniosidae | MDB | Chile (Magellanes) | DD | |
Rajidae | Unknown | Ecuador | DD | |
Rajidae | MN, MDB | Brazil | CR | |
Etmopteridae | MDB | Chile | LC | |
Pentanchidae | MN | Brazil | VU | |
Gurgesiellidae | MDB | Brazil | VU | |
Dasyatidae | MN | Brazil* | VU | |
Dasyatidae | MN | Brazil | EN | |
Carcharhinudae | MN | Brazil to Venezuela | CR | |
Rajidae | MDB | Brazil | LC | |
Pentanchidae | MDB | Brazil | VU | |
Rhinobatidae | MN | Brazil to Argentina | CR | |
Arhynchobatidae | MN, MDB | Brazil to Argentina | VU | |
Scyliorhinidae | MN, MDB | Brazil | VU | |
Scyliorhinidae | MDB | Brazil | LC | |
Scyliorhinidae | MDB | Brazil | LC | |
Squalidae | MDB | Brazil | DD | |
Squalidae | MDB | Brazil | DD | |
Squantinidae | MDB | Brazil | LC | |
Arhynchobatidae | MN | Chile | LC | |
Arhynchobatidae | MN | Brazil to Argentina | CR | |
Arhynchobatidae | MN, MDB | Brazil to Chile | NT | |
Triakidae | MN | Ecuador (mainland) | EN | |
Urotrygonidae | MN, MDB | Colombia to Peru | VU | |
Trygonorrhinidae | MN | Brazil to Argentina | EN | |
Narcinidae | MN | Colombia | VU |
The Western Atlantic Ocean has the highest number of records of endemic species, with the majority attributed to Brazil, which hosts 22 species, and only one representative exclusive each for Argentina and the Falkland Islands. In the portion of the South American continent bordered by the Pacific Ocean, Chile is the country with the highest number of endemic records, cataloging nine species, while Colombia, Ecuador, and the Galapagos Islands together have six representatives. In the assessment of the conservation status of species in South America conducted by the IUCN, nearly half of the endemic marine elasmobranch species (40%) are classified within some category of extinction threat. The majority of the species have been assessed as Least Concern (31.5%), followed by the Vulnerable and Data Deficient categories, representing ∼27 and ∼16% of the species, respectively. Four species (10.5%) are classified as Endangered, while the Menni’s Skate (
The type of habitat in which the species occur was also verified, with the same species being present in two types of habitats: Marine Neritic (MN), characterized as a region of the marine environment that is located on the continental shelf, and Marine Deep Benthic (MDB), an environment associated with the ocean floor which may extend beyond the continental shelf. Among the two types of habitats mentioned, most species (n = 16) are restricted to the Marine Deep Benthic habitat. Of the total endemic species evaluated, were verified the occurrence of six species with representatives in island environments (e.g., Lutz’s Stingray
2.2 Anthropogenic threats
A series of human activities are currently threatening marine ecosystems and, consequently, resident or migratory species in all oceans. For elasmobranchs, all this pressure, direct or indirect, can strongly affect the populations of rays and sharks. In this sense, aspects related to fishing pressure, pollution and environmental degradation will be detailed and discussed here.
2.3 Fisheries
Shark and ray populations have declined significantly in recent years as a result of extensive human exploitation throughout the world’s oceans, putting some species at risk of extinction. These species are captured in some fisheries as target species and/or as bycatch, both by artisanal fishing and by large-scale industrial fishing [9]. Due to the great diversity of habitats of these animals, they end up interacting and are susceptible to a wide variety of fishing gear (e.g., bottom trawling, surface trawling, bottom longline, pelagic longline, and trolling; Figure 1).
In all South American countries, sharks and rays are consumed both locally and for export. For example, Brazil, where sharks and rays are sold as “cação” without identifying the species, is one of the countries that consumes the most sharks. It is also one of the countries that exports the most fins to the Asian market [10].
Although fishing for some species is prohibited, they end up being fished as bycatch and, in many cases, returned to the sea. Bottom trawling is responsible for capturing 19 species of endemic rays, followed by gillnets responsible for catching nine endemic species, while longlines are responsible for catching five species (Table 2). Some species are subject to fishing pressure from different fishing gear, such as
Species rays | Trawl | Gillnet | Longline | Recreational | Beach seine |
---|---|---|---|---|---|
2.4 Pollution
Pollution can be defined as the introduction of any substance or energy into the environment at levels that cause deleterious effects on human health and other living organisms and interfere with the functioning of part or all of the ecosystem [13, 14]. Thus, the accumulation of pollutants in natural environments, especially in aquatic ecosystems, has become one of humanity’s greatest concerns in recent decades, since water is an important means of chemical transport, constantly influenced by human activities that occur in terrestrial and river systems [15], in addition to being an excellent solvent.
Pollutants can also have different properties, such as stock pollutants, which include plastics and other non-biodegradable materials, synthetic chemicals, and/or heavy metals, which tend to accumulate in the environment and in living organisms over time and along the food chain [16]. Among the stock pollutants, plastic is a global concern. Most plastic waste reaches aquatic environments through irregular disposal, and estimates indicate that the discharge of plastic waste into rivers, lakes, and oceans reaches 23 million tons per year [17]. Plastic can be carried by rivers, ocean currents, or even pushed by the wind with ease due to its weight and structure, and can accumulate in true floating islands, such as the Pacific Plastic Vortex, which covers approximately 1.5 million km2 [18]. This is extremely worrying since plastic is a persistent material in the environment and has natural removal rates on the scale of decades to centuries [17]. There are currently several records in the scientific literature on the negative interaction of elasmobranchs with plastic waste in the South Atlantic, especially entanglement, such as that recorded in tiger sharks,
Plastic also ends up being mistakenly consumed by elasmobranchs, especially microplastics. In addition to the potential for bioaccumulation and biomagnification, these plastic wastes also interact with chemical pollutants, which adhere to the plastic particles that facilitate the dispersion of these pollutants [24]. The presence of chemical pollutants has also been constantly observed in aquatic environments, which commonly present a mixture of metals, persistent organic pollutants (POPs), pharmaceuticals, cosmetics, personal hygiene products, surfactants and pesticides [24, 25]. These chemical pollutants also have the capacity for bioaccumulation and biomagnification in elasmobranchs, and many can function as endocrine disruptors or be proven to be carcinogenic and mutagenic. Malformations, for example, have been observed in the Spotback Skate,
2.5 Environmental degradation
The introduction of pollutants into aquatic environments influences environmental conditions such as dissolved oxygen concentration, pH and turbidity, often reducing the quality of these environments. The discharge of domestic sewage, for example, can lead to an increase in the concentration of nutrients that cause excessive growth of algae, which in turn reduce the passage of light and oxygenation of aquatic environments and often produce toxic compounds such as hydrogen sulfide (H2S) and ammonia (NH3), creating dead zones [15]. In freshwater environments, there are numerous reports of eutrophic environments due to excess nutrients from waste from human activities, and in recent years, the number of reports of macroalgae blooms in marine environments has been increasing, with species of the genus Ulva and the genus Sargassum being the algae commonly involved in the green tides and golden tides, respectively [15]. Another effect of the deposition of nutrients from human activities in aquatic ecosystems is nutrient-induced bioerosion, which, in addition to causing degradation of the coral reef structure, also intensifies the effects of ocean acidification [15] and can sometimes cause the death of coral reefs, areas intensively used by sharks and rays for resting, reproduction and feeding.
Changes in the physical structure of the environment, caused by urbanization and the construction of dams, canals, and ports, and by exploitative activities such as predatory fishing with explosives or trawl nets, as well as gas and oil exploration, modify natural landscapes, often reducing the quantity and quality of available aquatic habitats. Habitat characteristics play a fundamental role in the structuring of aquatic communities, influencing the distribution of species and the presence of mesopredators and top predators such as sharks and rays [27]. Species with highly specialized life histories and limited spatial or environmental distribution are more vulnerable to habitat changes. Many shark and ray species use shallow coastal areas as nurseries to protect their neonates and juveniles from large predators and adverse environmental conditions. Thus, the reduction in the quantity and quality of habitats often compromises feeding, reproduction, and shelter areas, which compromises the recruitment of some species and further contributes to the reduction of biodiversity.
Competition for space and food with invasive alien species also compromises the availability and quality of habitats. Biological invasions have complex direct and indirect impacts, often observed in the long term, when invaders are well-established and have large spatial ranges. Invasive alien species affect the richness and abundance of native species, change the behavior of these animals, alter the phylogenetic diversity among communities, and modify trophic networks, increasing the risk of extinction of native species [28]. Overall, there is little direct evidence that invasive alien species threaten elasmobranchs; however, there are several evidence of how invasive alien species interfere with the trophic dynamics of communities, compromising the food supply and the integrity of the natural ecosystems that elasmobranchs depend on [28].
3. Results
3.1 Alternatives for conservation
As previously mentioned, elasmobranch populations are being directly affected by several anthropogenic threats, as well as marine ecosystems, making the group highly vulnerable to various human activities. In this sense, the development of research aimed at investigating the biology, ecology, movement pattern, and habitat use of sharks and rays is being heavily employed through the use of several non-lethal techniques, in the hope of understanding the population dynamics of sharks and rays and, consequently, contributing to the conservation of the group. Among the various non-lethal methods employed in fisheries science, we highlight the study of blood cells and their relationship with pollutant concentrations in the environment, underwater observation (visual census), investigation of movement patterns and habitat use, through the extensive use of electronic tags (telemetry), and even the observation of animal diversity and behavior through Baited Remote Underwater Video (BRUV) and Drones.
3.2 Ecotoxicology
The vulnerability of elasmobranchs has given rise to a new field of study regarding the concentrations and effects of chemical substances of anthropogenic origin on these species. The bioavailability of these substances, that is, their availability for absorption by organisms, is a risk, especially for aquatic organisms, since these animals live submerged and in permanent contact with a mixture of chemical substances [24]. These bioavailable substances can be absorbed through gill respiration and the ingestion of food and water, in the case of marine fish, or through the tegument, the tissue that covers the body of these animals, bioaccumulating in these organisms over time, or biomagnifying through the food chain, especially in top predators, such as sharks and aquatic mammals [29].
The bioaccumulation and biomagnification of substances in elasmobranchs occurs in different tissues, especially in adipose tissues and organs such as the liver, the main organ involved in the detoxification process [30]. Sharks, in particular, have large, fat-rich livers and are very susceptible to the accumulation of lipophilic substances, such as metals and persistent organic pollutants (POPs), and tend to have higher metal concentrations compared to teleosts of similar trophic levels [24]. In South America, high concentrations of POPs were observed in the liver and muscle of blue sharks,
Responses of organisms to contact with these exogenous substances have been used as biomarkers of the health of these animals and the environment in which they live. In South America, the activities of some of these biomarkers have begun to be investigated in sharks and rays, such as studies on the activity of cholinesterases (ChE), enzymes that play an essential role in neuronal and motor functions, in brain and muscle tissues of blue sharks. The brain of blue sharks contains atypical ChE, exhibiting mixed properties of acetylcholinesterase (AChE) and butyrylcholinesterase (BChE), differently from bony fish, which implies different detoxification mechanisms [31]. The activity of the enzyme ethoxyresorufin-O-deethylase (EROD), an essential biotransformation enzyme for the detoxification of a wide range of xenobiotics, was also investigated in the catshark,
Genotoxic responses have also been observed through blood samples collected by non-lethal methods in tiger sharks, lemon sharks, and nurse sharks, sampled in a conservation area in the South Atlantic. Significant variations among species, which are also part of different trophic levels, were observed and associated with the presence of pollutants in the water column, suggesting that contact with pollutants such as metals and surfactants, even in small quantities, can cause genotoxic effects in sharks (Figure 3) [34]. These biomarkers do not provide information about impacts at more complex organizational levels, such as populations, communities and/or ecosystems, but they enable the detection of harmful effects early on at basal levels, which occur on a scale of minutes to weeks, and it is essential to have a correlation between their frequencies and concentrations with the intensity of exposure to the stressor [35].
Relationships between metal and metalloid concentrations and the frequency of genomic damage have also been investigated in tiger sharks, nurse sharks, and lemon sharks, with Al, As, and Zn showing a significant effect on the frequencies of genomic damage for all three species. Interspecific variations were also observed in this study, with Zn influencing the frequencies of binucleate cells and Al the frequencies of total damage and micronuclei in tiger sharks and lemon sharks, and As influencing the frequencies of binucleate cells and notched nucleus in nurse sharks, while showing a strong and positive correlation with most of the metals analyzed [36]. The high frequency of genomic damage over a long period of time is worrying because it can lead to disturbances in development and reproduction that can compromise the fitness of the organisms.
In general, there are still few studies focusing on pollutant levels and their effects on elasmobranchs, with most studies focusing on economically important sharks and rays, highlighting the lack of studies on species with low economic value and critical conservation status. There are also few studies using non-invasive methodologies, with muscle and liver being the most analyzed organs in current ecotoxicological studies. Therefore, the knowledge about the impacts of pollution on the health of these animals is urgent, since pollution of aquatic environments is a growing problem, especially in developing countries, constituting an additional stressor for many elasmobranch species that are already under threat of extinction due to fishing exploitation and habitat loss [37]. Thus, understanding the negative effects associated with pollution can greatly contribute to the implementation of public policies aimed at the conservation of elasmobranchs and their essential habitats.
3.3 Visual census
Visual census is a method used to observe individuals in an aquatic environment directly, through free diving or scuba diving [38]. Visual censuses serve to collect relevant information on spatial ecology, abundance, density, distribution, and population structure, distribution by sex and size, in addition to providing information on behavior in the wild [38, 39]. Visual census has been widely used, especially for endangered species or in marine protected areas, as they do not involve capture [38, 39]. Visual census can be performed in transects, intensive search, or stationary points depending on the objective and species studied. In transects, divers follow a parallel line, noting all the individuals observed. Transects can be used in different environments such as shipwrecks and reef environments [38].
During the visual census, it is possible to evaluate the different behaviors performed by sharks and rays (e.g., resting, swimming, feeding, and reproduction) and correlate them with the environment in which they are being monitored (e.g., type of substrate, depth, temperature, and tide, among others). The Atoll Biological Reserve (Brazil) is an ecological sanctuary for several migratory and resident species. Since it is a marine protected area, where only research activities are carried out, a series of studies involving non-lethal methods have already been carried out to investigate the populations of sharks and rays (e.g., Lemon Shark,
In general terms, the visual census has proven itself over the years to be an extremely efficient, low-cost, and highly recommended technique for investigating shark and ray populations on oceanic islands, clear water, and shallow areas, favoring the implementation of the methodology and providing data acquisition on wild animals, thus contributing to the conservation of populations.
3.4 BRUVS and drones
Recent technological advancements have significantly enhanced the development of non-lethal and non-invasive sampling methods for assessing fish assemblages. This is particularly beneficial in hard-to-reach environments, areas that present risks to samplers, and ecological sanctuaries with high preservation values. Furthermore, research that minimizes impacts on organisms and their habitats is particularly encouraged for endangered species and areas identified as hotspots, where the removal of animals from their environment could have significant effects on their populations, especially in the case of endemic species. In this context, the use of underwater video cameras for inventorying and monitoring fauna and their habitats has been on the rise, as they provide permanent records that do not impact the natural environment [40].
Baited Remote Underwater Video Surveys (BRUVs) have yielded highly satisfactory results on fish and elasmobranch research assemblages in various marine ecosystems [41]. This equipment can be constructed using readily available materials, featuring a relatively simple design that consists of a compact video camera housed in a waterproof case, attached to a base made in various shapes, and directed to a box with baits.
The number of cameras associated with the structure will depend on the objectives of the investigations: Single-BRUVs are equipped with a single camera and are less effective at estimating organism sizes compared to Stereo-BRUVs, which are constructed with two cameras. The latter not only provides more accurate length estimates but also expands the field of view of the monitored area [42]. The cameras capture underwater images of the species surrounding the equipment, primarily attracted by the bait contained in the boxes, although some animals may also approach the structure out of curiosity about the new presence.
Similar to underwater visual censuses, BRUVs enable the assessment of biodiversity, abundance, and spatial distribution of species, as well as the inference of important data regarding the population structure of a region [43], all without the presence of samplers in the water. Consequently, recent studies have focused on species behavior in their natural habitats using the autonomous recordings obtained from BRUVs, thereby generating much more reliable data on the natural behaviors of these species [44].
The BRUVs have been successfully utilized, particularly in Marine Protected Areas (MPAs), especially in fully protected zones, with the aim of monitoring biodiversity and assessing the effectiveness of these locations [45]. On the other hand, in areas with a high degree of environmental impact, BRUVs are employed to measure the extent of habitat degradation reflected in the species community at each site. In anthropogenically impacted areas of Pernambuco, Brazil, Lutz’s stingray (
Furthermore, the use of BRUVs allows for a greater number of samples to be collected in a shorter time frame and facilitates research in deeper environments due to the autonomy of the equipment, eliminating the need for divers to conduct the work. Globally, the use of BRUVs in scientific studies is on the rise due to their operational advantages and low cost.
However, it is important to note that, like all research methods capable of estimating species abundance and diversity, their use should be coupled with different methodologies to mitigate the sampling biases inherent to each method, as well as to allow for comparisons regarding the precision of the results obtained [47].
Within the same framework of faunal inventory and monitoring of underwater regions using autonomous equipment, remotely operated vehicles (ROVs) represent a more technically advanced data collection tool. In addition to capturing images with an attached video camera, ROVs are equipped with sensors and tools to perform specific tasks, such as collecting samples. The ability of ROVs to operate at depths inaccessible to divers, combined with their capacity to enter confined and narrow spaces, makes this equipment extremely valuable across various sectors, including scientific research.
In marine fauna investigations, ROVs differ from BRUVs in that they do not rely on bait as an attractant. Instead, they are capable of performing movements and actions controlled by an operator remotely, which is particularly beneficial for investigating species in deep regions where endemic species may be identified that would likely go unseen by other methods [48]. However, due to their greater autonomy, efficiency in data generation, and application across various research fronts, the cost of acquiring and operating ROVs remains a barrier to the development of academic research.
Drones, or unmanned aerial vehicles (UAVs), have gained popularity due to their ability to efficiently capture aerial imagery and the wide range of price points available for acquisition. Consequently, these technologies offer a broad array of functionalities that can be applied in various activities and environments.
Drones are model aircraft equipped with an autopilot system and can be either remotely controlled by an operator or fly autonomously, following predefined routes or control programs. Although the images generated by drones provide a perspective from above the water, these devices have become an important tool in research for the identification and monitoring of marine megafauna species. Additionally, they capture behaviors in natural habitats, area usage patterns, and estimates of population structure within ecosystems.
Large pelagic elasmobranchs, such as mobulids and whale sharks, are easily detected by these devices when they migrate to the ocean’s surface [49]. Drones can access areas that would be extremely challenging to reach, particularly in regions with difficult navigation or usage restrictions, and they also have lower logistical costs compared to some traditional research methods. In addition, drones are an essential tool for species conservation due to their ability to monitor the recovery of degraded areas and to document illegal activities in marine protected areas. This capability aids in identifying issues and facilitating the prosecution of those responsible. Technological innovations have not only reduced the size of these devices but also lowered acquisition costs, allowing for an expansion in the number of studies conducted with drones worldwide [49].
3.5 Electronic tagging
The movement patterns of aquatic organisms provide a suitable understanding of ecological and evolutionary processes that occur across different spatial and temporal scales. Sharks and rays should optimize their movements to balance the energetic and life history requirements with the costs of movement, such as reproductive and trophic migrations [50]. The choice of specific habitats within an ecosystem can be crucial to the survival and reproductive success of a species. In the early 1950s, the use of conventional (plastic) tags made it possible to investigate the movement of elasmobranchs. However, due to the limitations of the data obtained by tag-recapture work, biotelemetry techniques were developed in the hope of expanding monitoring both on a geographic scale and in greater detail of habitat use.
Acoustic telemetry is a frequently used method to assess the presence and movement information from aquatic animals, including skates and rays. This tool involves the use of transmitters implanted in the animals to be tracked and a hydrophone (usually called to as an acoustic receiver) that will have the capacity to detect the signal emitted by the transmitters. The data from acoustic telemetry are usually collected in two different ways, be it for active tracking or passive tracking, and each technique has its singular advantages and limitations [51].
Active tracking normally uses specific transmitters that emit continuous acoustic pulses and the signal is monitored by a receiver and hydrophone carried onboard the tracking vessel. Tracking invariably takes place over short durations of a few hours to a few days. The main objective of this technique is to provide detailed, fine-scale (m) tracks of animals by following the signal from the transmitter. The severe nature of this fieldwork means that it can normally only be conducted for a brief time, being therefore, essential that a rapid method of transmitter attachment is used to minimize stress and, consequently, not promote unusual behaviors by the study animal during the tracking [52]. Passive telemetry is based on the use of an array of acoustic receivers (omni-directional hydrophone) installed in underwater stations capable of detecting the presence of an individual, with a coded transmitter, for a long period of time. However, it is not possible to know the location of the individual, which carries the acoustic transmitter, if it is not close to the array of receivers.
Transmitters used in acoustic telemetry (active or passive) can be attached to sharks and rays externally or internally. External tagging can be done in several ways. For sharks, it is extremely usual to attach transmitters to the dorsal fin of the specimen, while for rays, this attachment can be done to the pectoral fin, tail, or even the blowhole (Figure 6a). Internal tagging involves a surgical procedure in which a small incision (∼4 cm) is made in the animal’s abdominal cavity, the transmitter is inserted, and the incision is sutured (Figure 6c and d). The choice of tagging technique (internal or external) should be based on the ecology of the species. In this sense, it is very important to evaluate the biology and behavior of the animal to choose the best form of tagging, ensure the retention of the transmitter, and consequently, the success of the monitoring.
An additional tool, which is widely used in research around the world, is satellite telemetry (Figure 6b). Individual movement patterns are recorded remotely while the tag is fixed to a specimen, and the data are transmitted
4. Discussion
4.1 Challenges and perspectives
The endemic species of elasmobranchs (sharks and rays) in South America face numerous challenges and opportunities for conservation. Here’s an overview of the key challenges and perspectives. Many species are targeted for their meat, fins, and cartilage, leading to significant population declines, and unsustainable fishing practices exacerbate this problem. Combined with this, coastal development, pollution, and habitat degradation (such as the deforestation of mangroves and the destruction of coral reefs) threaten critical breeding and nursery habitats for these species. Rising sea temperatures and ocean acidification can impact the health of marine ecosystems by affecting food availability and habitat suitability for elasmobranchs, which, without enforcement of fishing regulations and illegal fishing activities, contribute to the decline of endemic species. Another key factor is that many endemic species lack comprehensive research data, hampering effective conservation strategies, and this knowledge gap can make it difficult to assess population health and trends. Finally, as coastal communities expand, interactions between humans and elasmobranchs can lead to conflicts, further complicating conservation efforts.
From perspectives, we can initially mention the conservation initiatives that culminate in the growing awareness and defense of marine conservation aimed at protecting elasmobranch habitats and populations, in addition to the creation of marine protected areas (MPAs) as crucial for the preservation of biodiversity. Promoting sustainable fishing practices can also help restore populations of overexploited species, and certification programs and community-led management initiatives are gaining momentum. Investment in research can help fill knowledge gaps and the development of citizen science projects, and partnerships between governments, NGOs, and academic institutions can improve monitoring efforts. In this sense, local community involvement in conservation efforts promotes management and can lead to more effective management of marine resources, as well as strengthening legal structures and international agreements can help protect elasmobranchs, combined with collaborative efforts between countries. South American species are essential for transboundary species management.
Addressing the challenges faced by endemic elasmobranchs in South America requires a multifaceted approach that includes sustainable practices, strong legal frameworks, community engagement, and dedicated research efforts. By prioritizing these areas, it is possible to create a more favorable environment for the survival of these unique and vital species.
5. Conclusions
Almost half of the endemic sharks and rays in South America are classified within some category of extinction threat. Therefore, non-lethal research methods are strongly encouraged for studies involving this group. Additionally, demystifying the consumption of elasmobranchs in South America, particularly those lacking species identification labels, is also aimed at curbing the illegal trade of threatened species. These measures offer hope for the conservation of shark and ray populations, which are essential for maintaining the balance of marine ecosystems.
Acknowledgments
This chapter is dedicated to Professor Dr. Fábio Hazin for all his contributions to Fishery Science and for transforming the lives of all his students with the best opportunities. The authors are thankful to the Departamento de Pesca e Aquicultura at the Universidade Federal Rural de Pernambuco for all the professional support.
References
- 1.
Nelson JS, Grande TC, Wilson MV. Fishes of the World. 5th ed. Hoboken: Wiley; 2016. 711p. DOI: 10.1002/9781119174844 - 2.
Whitenack L, Kim S, Sibert EC. Bridging the gap between chondrichthyan paleobiology and biology. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 1-29. DOI: 10.1201/9781003262190 - 3.
Paig-Tran EWM, Porter ME, Ferry LA, Whitenack LB. How to build a shark biomechanics and bioinspiration. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 59-103. DOI: 10.1201/9781003262190 - 4.
White WT, O’Neill HL, Naylor GJP. Taxonomy and diversity of extant elasmobranchs. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 31-57. DOI: 10.1201/9781003262190 - 5.
Harry AV, Smart JJ, Pardo SA. Understanding the age and growth of chondrichthyan fishes. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 178-202. DOI: 10.1201/9781003262190 - 6.
Cortés E. Life history patterns and correlations in sharks. Reviews in Fisheries Science. 2000; 8 :299-344. DOI: 10.1080/10408340308951115 - 7.
Merwe AB, Lyons K, Kacev D, Feldheim K. Elasmobranch mating systems. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 203-222. DOI: 10.1201/9781003262190 - 8.
Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK. Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series. 2014; 495 :291-298. DOI: 10.3354/meps10597 - 9.
Pacoureau N, Rigby CL, Kyne PM, et al. Half a century of global decline in oceanic sharks and rays. Nature. 2021; 589 :567-571. DOI: 10.1038/s41586-020-03173-9 - 10.
Barreto RR, Bornatowski H, Motta F, Santander-Neto J, Vianna GMS, Lessa R. Rethinking use and trade of pelagic sharks from Brazil. Marine Policy. 2017; 85 :114-122 - 11.
Pollom R, Barreto R, Charvet P, Faria V, Herman K, Marcante F, Rincon G. The IUCN Red List of Threatened Species. 2020. DOI: 10.2305/IUCN.UK.2020-3.RLTS.T45925A104130004.en - 12.
Dulvy NK, Acuña E, Bustamante C, Concha F, Herman K, Velez-Zuazo X. Sympterygia lima. In: The IUCN Red List of Threatened Species. 2020, 2020; e.T44643A124436532. DOI: 10.2305/IUCN.UK.2020-3.RLTS.T44643A124436532.en - 13.
GESAMP Joint IMCO/FAO/UNESCO/WMO Group of Experts on the Scientific Aspects of Marine Pollution (GESAMP). Rep. 1st Sess. London: IMCO; 1969. p. 28 - 14.
ACIESP. Glossário de Ecologia. São Paulo: Publicação ACIESP. N° 57; 1987; 271p - 15.
Reichelt-Brushett A. Marine pollution in context. In: Marine Pollution–Monitoring, Management and Mitigation. Cham: Springer Nature Switzerland; 2023. pp. 1-22 - 16.
Garai P, Banerjee P, Mondal P, Saha NC. Effect of heavy metals on fishes: Toxicity and bioaccumulation. Journal of Clinical Toxicology. 2021; S :18 - 17.
MacLeod M, Arp HPH, Tekman MB, Jahnke A. The global threat from plastic pollution. Science. 2021; 373 (6550):61-65 - 18.
Gomes CA. O plástico, a nova praga ambiental. Medio Ambiente and Derecho: Revista electrónica de derecho ambiental. 2019; 35 :1-12 - 19.
Afonso AS, Fidelis L. The fate of plastic-wearing sharks: Entanglement of an iconic top predator in marine debris. Marine Pollution Bulletin. 2023; 194 :115326 - 20.
Barreto R et al. Macro-debris ingestion and entanglement by blue sharks (Prionace glauca Linnaeus, 1758) in the temperate South Atlantic Ocean. Marine Pollution Bulletin. 2019; 145 :214-218 - 21.
Sazima I et al. Plastic debris collars on juvenile carcharhinid sharks ( Rhizoprionodon lalandii ) in Southwest Atlantic. Marine Pollution Bulletin. 2002;44 (10):1149-1151 - 22.
Bucair N et al. Underestimated threats to manta rays in Brazil: Primacies to support conservation strategies. Global Ecology and Conservation. 2021; 30 :e01753 - 23.
Parton KJ, Galloway TS, Godley BJ. Global review of shark and ray entanglement in anthropogenic marine debris. Endangered Species Research. 2019; 39 :173-190 - 24.
Alves LM et al. Elasmobranchs as bioindicators of pollution in the marine environment. Marine Pollution Bulletin. 2022; 176 :113418 - 25.
Araújo CBBD. Genotoxicidade comparativa de grandes peixes pelágicos em duas unidades de conservação do Atlântico Equatorial: Arquipélago de Fernando de Noronha e Arquipélago de São Pedro e São Paulo [Thesis]. Recife, Brazil: Programa de Pós-Graduação em Biologia Animal, Universidade Federal de Pernambuco; 2024. p. 115 - 26.
Hauser-Davis RA, Barbosa-Filho ML, Pereira LHSDS, Lopes CA, Moreira SC, Rocha RC, et al. First record of a morphologically abnormal and highly metal-contaminated Spotback skate Atlantoraja castelnaui (Rajiformes: Arhynchobatidae) from southeastern Rio de Janeiro, Brazil. Journal of Threatened Taxa. 2020;12 (11):16510-16520 - 27.
Araújo CBBD. Estruturação espacial e relações tróficas das assembleias de peixes do Atol das rocas, o único atol do Atlântico Sul [Dissertation]. Recife, Brazil: Programa de Pós-Graduação em Ecologia, Universidade Federal Rural de Pernambuco; 2017. p. 88 - 28.
Pyšek P, Hulme PE, Simberloff D, Bacher S, Blackburn TM, Carlton JT, et al. Scientists' warning on invasive alien species. Biological Reviews. 2020; 95 (6):1511-1534 - 29.
Tiktak GP et al. Are concentrations of pollutants in sharks, rays and skates ( Elasmobranchii ) a cause for concern? A systematic review. Marine Pollution Bulletin. 2020;160 :111701 - 30.
Hauser-Davis RA et al. Metal concentrations and metallothionein metal detoxification in blue sharks, Prionace glauca L . from the Western North Atlantic Ocean. Journal of Trace Elements in Medicine and Biology. 2021;68 :126813 - 31.
Alves LM, Lemos MF, Correia JP, da Costa NA, Novais SC. The potential of cholinesterases as tools for biomonitoring studies with sharks: Biochemical characterization in brain and muscle tissues of Prionace glauca. Journal of Experimental Marine Biology and Ecology. 2015; 465 :49-55 - 32.
Martins MF, Costa PG, Bianchini A. Maternal transfer of polycyclic aromatic hydrocarbons in an endangered elasmobranch, the Brazilian guitarfish. Chemosphere. 2021; 263 :128275 - 33.
Fuentes-Rios D et al. EROD activity and biliary fluorescence in Schroederichthys chilensis (Guichenot 1848): Biomarkers of PAH exposure in coastal environments of the South Pacific Ocean. Chemosphere. 2005;61 (2):192-199 - 34.
Araújo C et al. Comparative genomic damage among three shark species with different habits: Sublethal impacts of human origin in a protected island environment in the South Atlantic. Marine Pollution Bulletin. 2023; 191 :114924 - 35.
Adam ML et al. Espécies sentinelas: Monitoramento Ambiental com base em biomarcadores de efeito cito-e genotóxico. Revista CEPSUL - Biodiv e Conser Marinha. 2023; 12 :e20230002-e20230002 - 36.
Araújo CBB, de Mendonça SA, de Lima Viana D, da Fontoura Martins M, Costa PG, Bianchini A, et al. Effects of blood metal (loid) concentrations on genomic damages in sharks. Environmental Pollution. 2024; 359 :124569 - 37.
Wosnick N, Niella Y, Hammerschlag N, Chaves AP, Hauser-Davis RA, da Rocha RCC, et al. Negative metal bioaccumulation impacts on systemic shark health and homeostatic balance. Marine Pollution Bulletin. 2021; 168 :112398 - 38.
Branco I. Ecologia da raia, Dasyatis americana (Hildebrand and Schroeder, 1928), na região metropolitana do Recife - PE e na ReBio Atol das Rocas - Brasil 2015 [thesis]. Pernambuco, Brazil: Federal Rural University of Pernambuco; 2015 - 39.
Mendonça SA, Macena BCL, Araujo CBB, Bezerra NPA, Hazin FHV. Dancing with the devil: Courtship behaviour, mating evidences and population structure of the Mobula tarapacana (myliobatiformes: Mobulidae) in a remote archipelago in the equatorial mid-Atlantic Ocean. Neotropical Ichthyology. 2020;18 (3):e200008. DOI: 10.1590/1982-0224-2020-0008 - 40.
Struthers DP, Danylchuk AJ, Wilson ADM, Cooke SJ. Action cameras: Bringing aquatic and fisheries research into view. Fisheries. 2015; 40 (10):502-512. DOI: 10.1080/03632415.2015.1082472 - 41.
Whitmarsh SK, Fairweather PG, Huveneers C. What is big BRUVver up to? Methods and uses of baited underwater video. Reviews in Fish Biology and Fisheries. 2017; 27 :53-73. DOI: doi.org/10.1007/s11160-016-9450-1 - 42.
Schramm KD, Harvey ES, Goetze JS, Travers MJ, Warnock B, Saunders BJ. A comparison of stereo-BRUV, diver operated and remote stereo-video transects for assessing reef fish assemblages. Journal of Experimental Marine Biology and Ecology. 2020; 524 :151273 - 43.
Rolim FA, Rodrigues PF, Langlois T, Neves LM, Gadig OB. A comparison of stereo-videos and visual census methods for assessing subtropical rocky reef fish assemblage. Environmental Biology of Fishes. 2022; 104 :413-429. DOI: 10.1007/s10641-022-01240-w - 44.
Parton KJ, Doherty PD, Parrish M, Shearer P, Myrick K, Shipley ON, et al. Opportunistic camera surveys provide insight into discrete foraging behaviours in nurse sharks ( Ginglymostoma cirratum ). Environmental Biology of Fishes. 2023;106 :19-30. DOI: 10.1007/s10641-022-01366-x - 45.
Rolim FA, Langlois T, Rodrigues PFC, et al. Network of small no-take marine reserves reveals greater abundance and body size of fisheries target species. PLoS One. 2019; 14 :e0204970 - 46.
Bezerra NPA, Correa AL, Hazin FHV, Garla R. First use of baited remote underwater video stations to assess fish diversity in the metropolitan region of Recife, northeastern Brazil. Revista de Biologia Tropical. 2022; 70 (1):332-347. DOI: 10.15517/rev.biol.trop..v70i1.45915 - 47.
Rhodes N, Wilms T, Baktoft H, Ramm G, Bertelsen JL, Flávio H, et al. Comparing methodologies in marine habitat monitoring research: An assessment of species-habitat relationships as revealed by baited and unbaited remote underwater video systems. Journal of Experimental Marine Biology and Ecology. 2020; 526 :151315 - 48.
Vieira RP, Cunha MR. In situ observation of chimaerid speciesin the Gorringe Bank: New distribution records for the north-East Atlantic Ocean. Journal of fish biology. 2014; 85 (3):927-932 - 49.
Frixione MG, García MD, Gauger MF. Drone imaging of elasmobranchs: Whale sharks and golden cownose rays co-occurrence in a zooplankton hot-spot in southwestern sea of Cortez. Food Webs. 2020; 24 :e00155 - 50.
Humphries NE, Sims DW. Optimal foraging strategies: Lévy walks balance searching and patch exploitation under a very broad range of conditions. Journal of Theoretical Biology. 2014; 358 :179-193. DOI: 10.1016/j.jtbi.2014.05.032 - 51.
Mull CG, Andrzejaczek S, Udyawer V, Dwyer RG. Advances in methods, understanding, and applications of elasmobranch movement ecology. In: Carrier JC, Simpfendorfer CA, Heithaus MR, Yopak KE, editors. Biology of Sharks and their Relatives. 2nd ed. Boca Raton: CRC Press; 2022. pp. 358-399. DOI: 10.1201/9781003262190 - 52.
Speed CW, Field IC, Meekan MG, Bradshaw CJA. Complexities of coastal shark movements and their implications for management. Marine Ecology Progress Series. 2010; 408 :275-293. DOI: 10.3354/meps08581 - 53.
Branco-Nunes I, Veras D, Oliveira P, Hazin F. Vertical movements of the southern stingray, Dasyatis americana (Hildebrand and Schroeder, 1928) in the biological reserve of the Rocas Atoll, Brazil. Latin American Journal of Aquatic Research. 2016;44 :216-227. DOI: 10.3856/vol44-issue2-fulltext-3