Almost nothing is known about the tiger shark in South Atlantic waters

Morphology and systematics

Even though the phylogeny of the Carcharhiniformes order based on familial distribution is still debated by specialists, and cases of non-monophyletic groups and subgroups have been reported (Compagno, 1977, 1988), only two studies concerning tiger shark morphology and systematics were obtained in the present review, both carried out in Southeast Brazil.

The first evaluated dermal denticle characteristics in tiger sharks, as this type of assessment comprises a valuable tool in elucidating phylogenetic relationships and is also useful in clarifying evolutionary adaptations (Poscai et al., 2017). The authors characterized the dermal denticles present on the nictitating membrane of the species through scanning electron microscopy. The species specific denticle shape and distribution was hypothesized as associated with a decreased need for eye protection due to tiger shark head shape, although a role in hydrodynamics and ocular protection cannot be discarded. The second study addressed certain phylogenetic aspects by analyzing the caudal muscle morphology of different Carcharhiniform species (de Oliveira, de Carvalho & Soares, 2019). In both studies, tiger shark morphology was more correlated to Sphyrnidae members than to other Carcharhinidae. These data further corroborate the distinct biological and molecular features that tiger sharks display when compared to other Carcharhinidae representatives, a proposed exclusion from Carcharhinidae, and the indication of Sphyrnidae as a sister group proposed by Naylor et al. (2012). This has, in turn, led to the species’ recent reclassification as Galeocerdidae (Ebert, Dando & Fowler, 2021).

The very low number of publications on tiger shark morphology and systematics in the South Atlantic obtained herein clearly indicate the need for further assessments in this regard. However, it is important to emphasize that, apart from some morphological features (e.g., reproductive organs, ontogenetic growth), data from other regions can be extrapolated to the South Atlantic, mainly concerning systematics and phylogeny. However, it is also important to note that, even when data was already generated by other more-developed regions, additional studies on South Atlantic waters are still encouraged, not only due to the singular importance of the subject itself, but also as a way to prevent colonizing science issues.

An important step in this direction may comprise taking advantage of dead individuals caught in artisanal and commercial South Atlantic fisheries, following the increasing trend for non-lethal studies on this species noted in other regions (Hammerschlag & Sulikowski, 2011). However, it is important to note that carcass decomposition status should be considered when evaluating dead individuals, and sampling should be standardized to individuals in the same decomposition stage, as what is routinely carried out for other marine megafauna representatives, such as marine mammals, where a standardized carcass decomposition code is employed (Geraci & Lounsbury, 2005). This, on the other hand, is not a limiting factor for certain biological samples (e.g., teeth and denticles), of paramount importance for taxonomy and morphology investigations, and opportunistic sampling in these cases is highly encouraged.

Reproduction

Only one study on reproductive aspects was obtained in our search, conducted in 1977 off the coast of Ceará, a Northeastern Brazilian state in the Western Atlantic (Alves, 1977). That study reported that the presence of spermatozoa in the nidimentary glands of adult females is common, suggesting that spermatozoa can survive for long periods of time in females and that fertilization can occur sometime prior to copulation. The study also indicates that females usually carry no more than 36 embryos, comparatively less than the number of embryos reported for other regions (Alves, 1977). The minimum size for sexual maturation was reported in this first assessment as 237 cm for males and 210 cm for females, with no further details on how the total length was taken (e.g., fork length, precaudal length), corroborating previous descriptions by Clark & von Schmidt (1965) for the coast of Florida, in the United States. The authors also report that pregnant females present a gestation period of about 1 year and are found in the area year-round at different pregnancy stages, with more developed embryo stages noted between May and August. Shallower regions (10–25 m) were noted as nursery grounds in the study area. In males, complete reproductive system development and sperm production were reported prior to the complete development of secondary sexual characteristics, such as clasper calcification (Afonso et al., 2012). Neonates (70–90 cm) and mature individuals (>310 cm) were reported only during the first annual quadrant (January–May), suggesting that this period is important for species parturition in Recife, Northern Brazil (Afonso & Hazin, 2014). Although the data presented above cover tiger shark reproductive aspects, it is important to emphasize that this was not the scope of the publications, and because of this, they were not included in the major theme described herein of reproduction. Other assessments not included in our review due to the applied inclusion criteria (only peer-reviewed articles) have further indicated that Southern Brazil has been identified as possible tiger shark parturition and nursery area, given the historical landing of pregnant females in the austral spring, and neonates, and juveniles in the summer and early austral autumn in the state of Paraná (Bornatowski & Abilhoa, 2012). However, no detailed analyses based on nursery area criteria as established by Heupel, Carlson & Simpfendorfer (2007) have been carried out to date, configuring an expressive knowledge gap in this regard.

Reproduction data gaps significantly hinder conservation efforts, as they are paramount in proposing both adequate fisheries management and marine protected areas for specific ontogenetic phases (i.e., neonates, juveniles, or pregnant females), especially for nursery areas where neonates and juveniles are more susceptible to human pressure (Heupel et al., 2018; Morgan et al., 2020). We suggest urgent assessments on this topic, and that special attention be given to the southern limits of tiger shark distribution, as different fertility rates and gestational periods may occur due to the lower local temperatures in these regions (Yamaguchi, Taniuchi & Shimizu, 2000; Lombardi-Carlson et al., 2003; Taylor, Harry & Bennett, 2016) requiring differential management plans (Walker, 2005). In addition, as stated in the previous topic, access to dead individuals landed from artisanal and commercial fisheries may also aid in this kind of evaluation, especially as sexing and pregnancy identifications can be easily carried out by non-experts with minimal instruction and do not require special or expensive personnel training. This type of observer-based assessment has been successfully applied in other regions. Furthermore, the use of non-lethal methodologies such as physiological (hormonal profile) and morphological (clasper rigidity and presence of semen in males, presence of mating bite signs in females) parameter evaluations to evaluate reproductive periods, the tagging of mature and pregnant females to identify migratory routes and possible birthing places and the identification of nursery areas, according to Heupel, Carlson & Simpfendorfer (2007) are all suggested to further knowledge in this regard for tiger sharks in the South Atlantic.

Age and growth

No studies specifically on tiger shark age and growth were found in our search, and only one assessment has been conducted on tiger shark growth rates (but reporting no age estimation) to date in the entire South Atlantic (Afonso et al., 2012). This lone study indicates the highest growth rates described in the literature for the species, as one male individual captured off the coast of Recife, Brazil was sexually mature at 304 cm TL and around 3.5 years, at half the age of global estimates for the species, and one female exhibited a significant growth rate following capture-recapture procedures only a few months apart. The authors indicate that, according to available age-at-length models, both individuals should take at least twice as long to reach their observed dimensions, thus indicating accelerated growth in the Recife area (and, possibly, across the Southwest Atlantic) (Fig. 3), postulated as due to local environmental factors and greater prey availability, although further studies with larger sample sizes are required to elucidate this hypothesis.

As tiger shark growth data (with no age estimation) for the South Atlantic are derived from only one male and one female specimen, extreme caution is necessary if extrapolating these data for practical applications. In addition, no ontogenetic assessments associated with age/growth data are available for the South Atlantic, and studies on how environmental factors such as seasonal variations can affect the growth rates of the species are also lacking. As vertebrae comprise the most efficient way to study shark age and growth, and samples from museum/university collections can still be used for historical descriptions, along with fresh samples from commercial landings, future studies should direct efforts to generate such data for the region. Despite the fact that capture-mark-recapture data require long-term efforts and exhibit low success rates, vertebrae analyses are less-expensive and generate more robust data for risk assessments, for example. Thus, it is imperative that age and growth data be determined for the South Atlantic, so more robust and updated regional risk assessments may be performed. Assessments employing a greater number of tagged animals are also encouraged, as spatial ecology data will benefit not only age and growth knowledge, but also migration and movement patterns that are still completely unknown to tiger sharks outside Northeast Brazil (more specifically, the state of Pernambuco).

Feeding ecology

A higher number of papers (n = 12) was found concerning feeding ecology, separated into dietary habits and trophic ecology for discussion purposes, all conducted in Brazil. The reasons why the amount of information on this topic is predominant in the South Atlantic are uncertain, but may be simply a reflection of greater interest in the topic by research groups.

Physiology

A total of three studies concerning physiology were obtained in our review. One was carried out at the Fernando de Noronha Archipelago with the aim of investigating capture stress effects and the validation of new stress markers for the species (Wosnick et al., 2017). Data on adults, however, are still lacking, as well as potential ontogenetic stress response variations upon capture. Furthermore, the impacts of both scientific and commercial captures are still not fully understood, and, although evidence of high survival rates for the species upon capture has been reported for the Recife coast (Afonso & Hazin, 2014), the physiological pathways involved in tiger shark recovery following capture are still not fully understood. In another assessment, the potential negative effects of fasting on juvenile tiger sharks were evaluated for the first time in the South Atlantic in the state of Maranhão, in the Fernando de Noronha Archipelago, and in the state of Paraná (Wosnick et al., 2020). According to the authors, the observed condition potentially resulted in serious metabolic consequences by preventing digestion and the recovery of lipid stores, although the causes of this restriction are still unclear and may be associated with other yet unidentified pathologies. In another first-time report, hormone (testosterone, progesterone, and B-estradiol) levels in juvenile male tiger sharks tagged in the Fernando de Noronha Archipelago were assessed (Wosnick et al., 2017). The results indicate that steroid hormones might play an important role in both home-range and migratory shark behavior.

Physiological assessments are paramount in understanding many aspects of shark behavior, migration, and stress responses, among others. In fact, recently physiology has been brought forth as indispensable in addressing current and future anthropogenic stressors that both directly and indirectly affect elasmobranchs (Lyons et al., 2019), as it is clear that physiological impairments may significantly compromise fitness parameters and negatively affect population recruitment (Wosnick et al., 2021). Expansion of comparative studies of hormone levels and migratory behavior, increasing the number of captured and tagged animals, as well as including those that have already reached sexual maturity, are strongly suggested. Data on capture stress from commercial fisheries as well as mortality rates are also necessary, along with stress studies focusing on stress upon capture between life stages and sexes. Lastly, as Southern Brazil encompasses the southern limit of distribution of the species, studies in this region should be prioritized, aiming to elucidate the particularities of this population. Studies aimed at investigating and monitoring the health of tiger sharks are also encouraged, especially considering the ingestion of objects that have the potential to compromise affected individuals.

Population structure

A single study was obtained regarding tiger shark population structure in our applied geographic range. The single assessment conducted off the coast of Recife indicates that tiger sharks are more abundant between the coastline and the end of the continental shelf, and that reach larger sizes when compared to other shark species that are part of the local assembly (Afonso & Hazin, 2014). The sex ratio was noted as 0.69:1 (M:F) and local distribution was verified as influenced by annual fluctuations directly associated to seasonality. Abundance was also positively correlated with high and low tide amplitudes and low rainfall. The authors report juveniles as the predominant size class in local captures, with few captured animals above the maturity size of 310–320 cm total length (TL) and a high number of neonates (<100 cm TL) in the first annual quadrant, pointing to a parturition period. The abundance of tiger sharks over the 4 years of study was considered low, however, no evidence that this occurs in the long term was found, although factors (e.g., temperature change and thermoclines) that might affect tiger shark distribution were not established.

As only a single assessment was obtained concerning population structure, long-term analyses comparing seasonal variation are paramount to better understanding distribution trend shifts, both in Brazil and in other South Atlantic areas. Considering the importance of commercial fisheries in generating shark data in Brazil, landing monitoring to describe tiger shark population structure data is highly recommended. However, such a methodology must be used with caution, as individual patterns of the studied fleets can bias the data, generating under- or overestimated predictions. In this context, telemetry studies as a supplementary methodology are recommended, however, often prohibitive due to the high relative costs of telemetry methods (Lippi et al., 2021), and significant cost differences among different tags (e.g., sPAT tags x miniPAT tags—Miller et al., 2019). Moreover, increased sampling periods are suggested, to include a minimum historical series with seasonal variations, as well as regional samplings and comparisons, generating a larger scale database at the East and West Atlantic levels. Abundance associations to abiotic factors such as substrate, turbidity, tide, and temperature, and biotic factors such as prey availability and the presence of competitors, are also required, to understand which factors can influence tiger shark population structure.

Human interactions

Movements and migration

Of all reported tiger shark catches, 84.6% took place outside the original species distribution proposed (e.g., International Union for the Conservation of Nature, 2018; Ebert et al., 2013) (Domingo et al., 2016). Thus, a new distribution for the species based on data of pelagic longline vessels from several countries, such as the United States, Spain, Japan, Portugal, and Uruguay, was proposed (Domingo et al., 2016). Concerning the South Atlantic, all tiger shark individuals were captured beyond the range of their former distribution, also indicating distribution in waters off the continental shelf (Domingo et al., 2016). Furthermore, the expressive number of captures observed in equatorial waters between South America and Africa indicates a potential ecological corridor, highlighting the importance of collaborations between researchers from both regions to ensure adequate tiger shark’s management within the South Atlantic. In fact, tiger sharks captured and tagged at the Fernando de Noronha Archipelago have been shown to move to distant offshore areas and reach different Southwest African areas (Afonso, Garla & Hazin, 2017). These data suggest the Archipelago as a connecting site for different occurrence areas, linking Atlantic and Indo-Pacific Oceans populations, with mounting evidence from different research fields (Bernard et al., 2016; Domingo et al., 2016; Afonso, Garla & Hazin, 2017; Carmo et al., 2019). In addition, juvenile tiger sharks that inhabit coastal Northeastern Brazil areas seem to use the region as a disperser point for the pelagic environment (Afonso, Garla & Hazin, 2017).

Furthermore, tiger sharks seem to alter their habitats as they grow, expanding their habitats towards the oceanic environment (Afonso & Hazin, 2015), suggesting distribution per ontogenetic stage and movement driver differences (Afonso, Garla & Hazin, 2017). This has been confirmed in the West Atlantic, which also comprises differences in distribution by sex, with a greater number of juveniles of both sexes, measuring <200 cm in TL inhabiting shallow coastal waters (Afonso & Hazin, 2014; Afonso, Garla & Hazin, 2017; Domingo et al., 2016). The occurrence of neonates has also been reported for shallower neritic waters, while a predominance of immature females between 200–260 cm in TL is noted in areas far from the coast (Afonso, Garla & Hazin, 2017). Regarding vertical distribution, juveniles are more predominant between surface waters (>5 m) up to 60 m in depths, although some reports indicate incursions up to 1,000 m (Afonso & Hazin, 2015). As tiger sharks grow from 150 to 300 cm in TL, their maximum diving depth increases up to four-fold, allowing the species to explore different environments, decreasing intraspecific competition, and expanding their ecological niche (Afonso & Hazin, 2015).

In one of the few studies carried out exclusively outside Brazil, tiger sharks tagged around Ascension Island, a British isolated volcanic island located 7°56′ south of the Equator, moved from shallow waters through the thermocline (where the temperature drops from 13.5 to 6 °C) (Madigan et al., 2021). Most dives took place at >20 °C, although frequent dives to lower temperatures were noted, albeit limited to the thermocline floor (150 m). Dissolved oxygen (DO) during dives ranged from 2 to 5 mL⁻¹, with animals expending a considerable time (8.3%) at 2 mL⁻¹, suggesting hypoxia tolerance in the species (Madigan et al., 2021). However, as only one tiger shark was monitored, caution is advised in interpreting the presented data.

Except for Recife and Fernando de Noronha, all occurrence tiger shark data found and included herein are from commercial fishing fleets. Thus, targeted capture assessments or more comprehensive monitoring of commercial fleets are required to further increase knowledge on the species’ area of occurrence. Furthermore, telemetry assisted studies would also be a valuable tool to obtain further information on tiger shark movements and migration, although costs must be considered, as cited in the population structure topic. Evaluations on movements along the Brazilian coast, and the southwest-south connection of Brazil, and the Northeastern regions are mandatory for this topic. It would also be interesting to evaluate if juveniles from other regions carry out the same oceanic incursions. Furthermore, it is paramount to understand if the connection between West and East Atlantic is carried out only by Fernando de Noronha or if it also takes place in the Southeast-South regions of Brazil, to identify the connectivity between sharks in the West and East Atlantic through migratory movements.

Population genetics

Although tiger sharks exhibit a circumglobal distribution in both tropical and temperate waters, information on population connectivity, dynamics and genetic structure, only began to be unraveled in the last decade (Andrade et al., 2021; Bernard et al., 2016; Carmo et al., 2019). The studies retrieved herein indicate confirmed genetic differentiation between tiger sharks from the West Atlantic, North Atlantic, and Southwest Atlantic, and an isolated population identified in Hawaii (Andrade et al., 2021; Bernard et al., 2016). Studies indicate that the separation between Indo-Pacific and West Atlantic populations took place only about 1 million years ago, with the Southwest Atlantic serving as a connection point between ocean basins, allowing for population breeding through incursions along the South African tip (Bernard et al., 2016). Furthermore, mitochondrial DNA analyses indicate a matrilineal intra-oceanic population structure, where the gene flow is highly influenced by females, mainly by philopatry (Bernard et al., 2016). It is important to note that this may lead to different fishing vulnerabilities between males and females, in turn resulting in genetic diversity imbalances in the long term, due to altered male to female ratios and pregnant female densities and, consequent significant diversity losses. Thus, efforts to conserve the species should be revised considering these differences (Bernard et al., 2016).

Atlantic and Pacific population differences were confirmed in further studies by Carmo et al. (2019), who also obtained new relevant information on the local barriers that affect tiger shark gene flows. This author reported three highly structured populations in the Atlantic, off the coasts of the United States, Panama, and Brazil, with two distinct populations centered in the Brazilian states of Pará, in northern Brazil, and São Paulo, in southeastern Brazil. The Fernando de Noronha Archipelago population exhibits a genetic structure with haplotypes from all Atlantic populations, comprising the most diverse population (Andrade et al., 2021; Carmo et al., 2019), denoting breeding between tiger sharks from both hemispheres, connecting the North Atlantic to the South Atlantic, with the Southwestern Atlantic in fact comprising a bridge between populations, as noted previously by other authors (Bernard et al., 2016). Thus, Fernando de Noronha has again been noted as a tiger shark convergence center, reinforcing its ecological and conservation relevance (Andrade et al., 2021; Carmo et al., 2019).

Decreases in the genetic variability of tiger sharks from the South Atlantic have been described by Mendes et al. (2016), excluding Fernando de Noronha individuals. Interestingly, the Florida population (Gulf of Mexico), one of the most studied globally, presents only 1.7% of the observed diversity of the Fernando de Noronha Archipelago (Carmo et al., 2019). From a conservationist point of view, these data reveal significant tiger shark fragility and vulnerability at regional levels. Isolated populations are also more likely to lose genetic diversity through overfishing, as gene flow through migration events is very low (Carmo et al., 2019). Therefore, the Fernando de Noronha Archipelago should be recognized as a tiger shark sanctuary, due to its essential gene flow role and consequent maintenance of healthy populations (Andrade et al., 2021; Carmo et al., 2019).

Genetic tools are paramount in unveiling population structure, through parameters such as genetic drift, mutation, and selection (Holmes et al., 2017) and genetic connectivity dynamics, also allowing for historical samples to be genotyped and assigned back to their population of origin (Sort et al., 2021). In fact, knowledge in this regard for many large-bodied, highly migratory, apex predator sharks across their global ranges are still very limited (Bernard et al., 2016). Thus, although a relatively high amount of tiger shark population genetics data is reported in the retrieved studies in our review, it is clear that further assessments are required, although genetic techniques, similarly to telemetry methods, are also relatively prohibitive in certain regions, due to high costs. Some efforts to create and validate quick, low cost and easily applicable methods, such as PCR analysis based on 5S rDNA repeat unit amplification have been noted, to contribute to conservation efforts in general (Natesh et al., 2019) and even specifically to shark conservation management (Pinhal et al., 2008), although these are relatively scarce and spaced between. Increasing sampling events is required, also focusing on islands and oceanic outcrops to identify potential new points of convergence. The number of animals sampled in the West and mainly, the East Atlantic, should be increased, aiming to investigate the presence of regional subpopulations. The comparison of populations more susceptible to human pressures (mainly fisheries) with more protected populations also allows for assessments on the potential loss of tiger shark genetic diversity.

In short, many knowledge gaps were noted, even for more traditional studies. The situation worsens when new methodologies are considered, as the associated costs are a prohibitive factor. Table 1 below presents knowledge gaps and questions not yet investigated or that require more effort in view of each of the topics discussed herein.

As some significant knowledge gaps on major research areas were also observed, a summary on future directions is also presented (Table 2).