Male Sharks Research Articles

Growth and life history variability of the grey reef shark (Carcharhinus amblyrhynchos) across its range.

For broadly distributed, often overexploited species such as elasmobranchs (sharks and rays), conservation management would benefit from understanding how life history traits change in response to local environmental and ecological factors. However, fishing obfuscates this objective by causing complex and often mixed effects on the life histories of target species. Disentangling the many drivers of life history variability requires knowledge of elasmobranch populations in the absence of fishing, which is rarely available. Here, we describe the growth, maximum size, sex ratios, size at maturity, and offer a direct estimate of survival of an unfished population of grey reef sharks (Carcharhinus amblyrhynchos) using data from an eight year tag-recapture study. We then synthesized published information on the life history of C. amblyrhynchos from across its geographic range, and for the first time, we attempted to disentangle the contribution of fishing from geographic variation in an elasmobranch species. For Palmyra’s unfished C. amblyrhynchos population, the von Bertalanffy growth function (VBGF) growth coefficient k was 0.05 and asymptotic length L∞ was 163.3 cm total length (TL). Maximum size was 175.5 cm TL from a female shark, length at maturity was estimated at 116.7–123.2 cm TL for male sharks, maximum lifespan estimated from VBGF parameters was 18.1 years for both sexes combined, and annual survival was 0.74 year-1. Consistent with findings from studies on other elasmobranch species, we found significant intraspecific variability in reported life history traits of C. amblyrhynchos. However, contrary to what others have reported, we did not find consistent patterns in life history variability as a function of biogeography or fishing. Ultimately, the substantial, but not yet predictable variability in life history traits observed for C. amblyrhynchos across its geographic range suggests that regional management may be necessary to set sustainable harvest targets and to recover this and other shark species globally.

Population Structure, Abundance and Movement of Whale Sharks in the Arabian Gulf and the Gulf of Oman

Data on the occurrence of whale sharks, Rhincodon typus, in the Arabian Gulf and Gulf of Oman were collected by dedicated boat surveys and via a public-sightings scheme during the period from 2011 to 2014. A total of 422 individual whale sharks were photo-identified from the Arabian Gulf and the northern Gulf of Oman during that period. The majority of sharks (81%, n = 341) were encountered at the Al Shaheen area of Qatar, 90 km off the coast, with the Musandam region of Oman a secondary area of interest. At Al Shaheen, there were significantly more male sharks (n = 171) than females (n = 78; X2 = 17.52, P < 0.05). Mean estimated total length (TL) for sharks was 6.90 m ± 1.24 (median = 7 m; n = 296). Males (7.25 m ± 1.34; median = 8 m, n = 171) were larger than females (6.44 m ±1.09; median = 7 m, n = 78; Mann-Whitney U test, p < 0.01). Of the male sharks assessed for maturity 63% were mature (n = 81), with 50% attaining maturity by 7.29 m and 100% by 9.00 m. Two female sharks of >9 m individuals were visually assessed as pregnant. Connectivity among sharks sighted in Qatari, Omani and UAE waters was confirmed by individual spot pattern matches. A total of 13 identified sharks were re-sighted at locations other than that at which they were first sighted, including movements into and out of the Arabian Gulf through the Strait of Hormuz. Maximum likelihood techniques were used to model an estimated combined population for the Arabian Gulf and Gulf of Oman of 2837 sharks ± 1243.91 S.E. (95% C.I. 1720–6295). The Al Shaheen aggregation is thus the first site described as being dominated by mature males while the free-swimming pregnant females are the first reported from the Indian Ocean.

Into the wild: developing field tests to examine the link between elasmobranch personality and laterality

The field of animal personality has received considerable attention in past decades, yet few studies have examined personality in the wild. This study investigated docility, a measure of boldness, in two Port Jackson shark (Heterodontus portusjacksoni) populations using field tests, and if laterality differences explained docility levels. We developed a struggle test as an assay for docility, which is particularly amenable to field studies. The struggle test was effective, and repeatable inter-individual docility differences were observed. Sex, but not population, influenced docility scores, with male sharks being less docile than females. This difference is likely due to the contrasting role each sex plays during mating. We also found individualized lateralization. However, no individual-level relationship between lateralization and docility was detected. Despite reported links between laterality and some personality traits, the relationship between laterality and boldness remains inconclusive in sharks. Further studies will prove essential to clarify the mechanisms behind personality traits in vertebrates.

THE FEEDING HABITS OF JUVENILE SCALLOPED HAMMERHEAD SHARKS (SPHYRNA LEWINI) CAUGHT IN THE GULF OF NICOYA, COSTA RICA

Sharks present strong intraspecific changes in feeding habits, which may vary according to size, geographic location and season. This study analyzed the stomach contents of 52 juvenile scalloped hammerhead sharks (25 females and 27 males) caught by artisanal vessels in the Gulf of Nicoya. Regarding the organisms found in the stomachs, 41.07 % were teleost fish, 30.36 % mollusks and 28.57 % crustaceans. Mollusks presented the highest Relative Importance Index (RII) (43.05 %), followed by teleost fish (41.37 %) and crustaceans (15.58 %). Squids (Loliginidae) were the items with the greatest RII (32.57 %). By means of the Pianka index, a relatively low overlap between sexes was identified, suggesting a spatial sexual segregation and, in consequence, an ecological niche separation between male and female hammerhead sharks.

Genetic structure, population demography and seasonal occurrence of blacktip shark Carcharhinus limbatus in Bimini, the Bahamas.

A longline survey was conducted from 2004 to 2014 to investigate the demographic population structure and seasonal abundance of the blacktip shark Carcharhinus limbatus in the Bimini Islands, the Bahamas. All individuals sampled (n = 242) were sub-adult or adults [70·1-145·1 cm pre-caudal length (LPC) range] with no neonates or YOY recorded in Bimini. Carcharhinus limbatus abundance peaked in September, coincident with the largest ratio of female to male sharks and a peak in fresh mating wounds on females. Mitochondrial control region (mtCR) DNA sequences were obtained from C. limbatus at Bimini to test whether Bimini C. limbatus are most closely related to geographically proximate populations sampled on the south-eastern coast of the U.S.A., the closest known nursery areas for this species. Nine mtCR haplotypes were observed in 32 individuals sampled at Bimini [haplotype diversity (h) = 0·821, nucleotide diversity (π) = 0·0015]. Four haplotypes observed from Bimini matched those previously found in the northern Yucatan (Mexico)-Belize and two matched a haplotype previously found in the U.S.A. Four haplotypes were novel but were closely related to the northern Yucatan-Belizean haplotypes. Pair-wise ΦST analysis showed that Bimini was significantly differentiated from all of the populations previously sampled (U.S.A. Atlantic, U.S.A. Gulf of Mexico, northern Yucatan, Belize and Brazil). This indicates that C. limbatus sampled from Bimini are unlikely from the described, proximate U.S.A. nurseries.

Androgen receptors in the bonnethead, Sphyrna tiburo: cDNA cloning and tissue-specific expression in the male reproductive tract

As demonstrated in past studies, androgens appear to play critical roles in regulating reproduction in male sharks. However, little is known about the cell-specific actions of androgens in these fishes. To address this, this study examined androgen targets in reproductive organs of a seasonally reproducing shark, the bonnethead (Sphyrna tiburo). A partial bonnethead AR cDNA clone was isolated and found to exhibit strong homology with known vertebrate ARs. Using RT-PCR and in situ hybridization, AR was found to be expressed in multiple cell types in the male bonnethead testis (premeiotic germ cells, Leydig-like interstitial cells, Sertoli cells, peritubular myoid cells, and mature spermatozoa) and gonadal ducts (stromal cells, luminal epithelial cells, mature spermatozoa). Furthermore, AR expression in these organs was found to vary temporally in relation to the seasonal reproductive cycle. Based on immunocytochemistry, the presence of AR protein in male bonnethead reproductive organs was largely consistent with patterns of AR gene expression with the single exception of mature spermatozoa, which exhibited consistently strong mRNA expression but only inconsistent and weak AR protein immunoreactivity. These results suggest important roles for androgens in regulating germ cell proliferation, hormone production, spermatid elongation, spermiation, and gonadal duct function in male bonnetheads. In addition, high abundance of AR mRNA in bonnethead spermatozoa suggest the potential for de novo protein synthesis following spermiation/copulation and/or a role for AR mRNA in early embryonic development, both of which have been proposed to explain the occurrence of mRNA transcripts in spermatozoa from various vertebrates.

Mating scars reveal mate size in immature female blue shark Prionace glauca.

The objective of this study was to determine the size and maturity status of the male blue sharks Prionace glauca attempting to mate with small, immature females in the north-west Atlantic Ocean. The relationship between male curved fork length (LFC ) and jaw gape was used in conjunction with the diameter of the mating scar to estimate the LFC and infer the maturity status of the male shark that produced the mating scar. The results indicate that mature males with a mean ± s.d. LFC of 218 cm ± 23 cm were attempting to mate with sexually immature females.

A new metric for measuring condition in large predatory sharks.

A simple metric (span condition analysis; SCA) is presented for quantifying the condition of sharks based on four measurements of body girth relative to body length. Data on 104 live sharks from four species that vary in body form, behaviour and habitat use (Carcharhinus leucas, Carcharhinus limbatus, Ginglymostoma cirratum and Galeocerdo cuvier) are given. Condition shows similar levels of variability among individuals within each species. Carcharhinus leucas showed a positive relationship between condition and body size, whereas the other three species showed no relationship. There was little evidence for strong differences in condition between males and females, although more male sharks are needed for some species (e.g. G. cuvier) to verify this finding. SCA is potentially viable for other large marine or terrestrial animals that are captured live and then released.

Environmental Influences on the Abundance and Sexual Composition of White Sharks Carcharodon carcharias in Gansbaai, South Africa

The seasonal occurrence of white sharks visiting Gansbaai, South Africa was investigated from 2007 to 2011 using sightings from white shark cage diving boats. Generalized linear models were used to investigate the number of great white sharks sighted per trip in relation to sex, month, sea surface temperature and Multivariate El Niño/Southern Oscillation (ENSO) Indices (MEI). Water conditions are more variable in summer than winter due to wind-driven cold water upwelling and thermocline displacement, culminating in colder water temperatures, and shark sightings of both sexes were higher during the autumn and winter months (March–August). MEI, an index to quantify the strength of Southern Oscillation, differed in its effect on the recorded numbers of male and female white sharks, with highly significant interannual trends. This data suggests that water temperature and climatic phenomena influence the abundance of white sharks at this coastal site. In this study, more females were seen in Gansbaai overall in warmer water/positive MEI years. Conversely, the opposite trend was observed for males. In cool water years (2010 to 2011) sightings of male sharks were significantly higher than in previous years. The influence of environmental factors on the physiology of sharks in terms of their size and sex is discussed. The findings of this study could contribute to bather safety programmes because the incorporation of environmental parameters into predictive models may help identify times and localities of higher risk to bathers and help mitigate human-white shark interactions.

The determination of maturity stages in male elasmobranchs (Chondrichthyes) using a segmented regression of clasper length on total length

A novel statistical method for estimating the stages of maturity in male sharks and skates based on a segmented regression (SRM) is proposed. We hypothesize that this method is able to find the transition points in the three-phase relationship between total length (TL) and clasper length (CL). We applied an SRM to TL–CL data of nine species, from large pelagic sharks (e.g., Carcharhinus falciformis) to small coastal skates (e.g., Rioraja agassizi), captured in the southwestern Atlantic and northeastern Pacific. As expected, SRM detected two breakpoints, defining three maturity stages (immature, maturing, and mature), in six out of nine species. For three species, it was not possible to find two breakpoints because of incomplete sampling of TL. This novel method is noninvasive, it is applicable to previously collected data, is easy to use, and provides a reliable tool for increasing our understanding of elasmobranch reproductive strategies.

The effects of gender, size and life‐cycle stage on the chemical composition of smoothhound shark (Mustelus mustelus) meat

Knowledge on the chemical composition of foods, and on the variation in such components as influenced by endogenous factors, is required for nutritional labelling, dietetic planning and food processing. This study examined the effects of endogenous factors (gender, size and life-cycle stage) on the chemical components (proximate, amino acid, fatty acid, mineral and mercury contents) of smoothhound shark (Mustelus mustelus) meat. Levels of moisture, protein, lipids, ash, amino acids and most minerals were not affected (P > 0.05) by the gender, size or life-cycle stages of the sharks. The fatty acid content was higher in females than in males, as well as in non-pregnant females compared to pregnant females. Certain fatty acids decreased in quantity in medium-sized sharks (prior to maturity). Pregnant females had higher aluminium (Al) and copper (Cu) levels than non-pregnant females and mercury (Hg) levels were highest in large male sharks. This study has, for the first time, established that endogenous factors have minimal influence on the chemical composition of M. mustelus meat, demonstrating the feasibility of describing an average composition for this species. Additionally, new insights have been obtained on potential safety concerns (mercury) associated with consumption of the meat that require further investigation.

Surface behaviour of bait-attracted white sharks at Dyer Island (South Africa)

Six research expeditions were conducted at Dyer Island to observe the surface behaviour of white sharks in the presence of bait. Observations were made from a commercial cage-diving boat. We observed 140 white sharks that exhibited 9 different types of behaviour: parading, bait following, visual inspection, breach, tail slap, tail stand, spy hop, repetitive aerial gaping, and head-up vertical emerging. Breach and tail slap were most often performed by male sharks, and tail slap and tail stand were more often performed by mature animals. The ethogram consisted of an average of 20 behavioural units, with a significant transitional pattern from bait follow to parading and from parading to bait follow. The individual surface behaviour of white sharks is not a simple stimulus–response reflex, but rather a complex tactical situation in which animals show plastic responses. Many aspects of white shark surface behaviour resemble those of other predator species that spend time at the surface.

Presence of longfin mako shark Isurus paucus (Chondrichthyes: Lamnidae) in the south-eastern Gulf of Mexico, Tabasco, Mexico

A male longfin mako shark Isurus paucus of 303 cm total length was found during the monitoring of small scale fishery in Nuevo Torno Largo, Tabasco. This is the first record of the species in the south-eastern Gulf of Mexico. The specimen was caught by a small longline vessel at 18 o 49′45″N 94 o 08′14″W. Snout and ventral coloration, pectoral fin length and dorsal fin position were used to verify the identification.

Accuracy of species identification by fisheries observers in a north Australian shark fishery

Despite the importance of observers to collect data for effective fisheries management worldwide, their species-identification abilities are rarely assessed. Misidentifications could compromise observer data particularly in diverse, multi-species fisheries such as those in the tropics where visual identification is challenging. Here, we provide the first estimates of the ability of scientific observers to identify five species of morphologically similar carcharhinid sharks (Carcharhinus leucas, C. amboinensis, C. tilstoni, C. sorrah and C. brevipinna) in a fishery in northern Australia. We compared observer field identifications of sharks with genetic validation (814bp mtDNA NADH dehydrogenase subunit 4) to quantify species identification errors. We used binomial generalised linear models to determine the influences of species, gender, total length, and the observer's experience on identification error. We found that identification error (∼20%) depended predominately on the species in question (highest error for C. tilstoni). Male sharks were misidentified less frequently than females, and error decreased marginally with increasing total length. Surprisingly, we found no statistical evidence that observer experience influenced identification error. Our results provide the first benchmark of identification accuracy of observers for carcharhinid sharks in northern Australia and show that estimates of error in species identifications need to be incorporated into management strategies to ensure successful recovery of the many recently over-fished shark populations.

Is the Megamouth Shark susceptible to mega-distortion? Investigating the effects of twenty-two years of fixation and preservation on a large specimen of Megachasma pelagios (Chondrichthyes: Megachasmidae)

On 18 August 1988, the third reported Megamouth Shark (Megachasma pelagios Taylor, Compagno and Struhsaker, 1983) became stranded on a beach in Western Australia. The 5.15 m TL male shark (WAM P.29940–001) was preserved at the Western Australian Museum (WAM) and put on public display. Many deep water chondrichthyan species, including M. pelagios, possess soft and fl abby muscle tissue and a poorly calcifi ed skeleton. Such species are prone to distortion through dehydration due to the fi xation and preservation process. Such distortions may result in taxonomic and nomenclatural issues. The WAM Megamouth Shark was recently relocated, providing an opportunity to remeasure the specimen to allow a comparison with measurements taken of the specimen when it was fresh, and to assess the extent of change to these measurements after 22 years of preservation. We found that with the exception of the pelvic-fi n, that we hypothesise is the fl eshiest part of M. pelagios with the least skeletal support, the specimen has suffered little to no distortion over this time. However, there has been some degradation of teeth and denticles that is most likely due to the acidity of the formalin solution.

Removal of an Intracoelomic Hook via Laparotomy in a Sandbar Shark (Carcharhinus plumbeus)

A twenty-one-year-old male sandbar shark (Carcharhinus plumbeus) demonstrated signs of chronic weight loss even though its appetite remained unchanged. In addition, the gradual development of a red, circular lesion on its ventral body was noted. After months without any significant changes, a ventral fistula appeared revealing the tip of a wire exposed within its center. The shark was immobilized via intramuscular remote injection through dartgun with etomidate; removed from its exhibit tank; and clinically examined with radiographic imaging, a cell blood count/serum chemistry evaluation, and the use of a metal detector along the body wall. A metallic hook was identified in the coelom about 10 cm cranial to the external fistula. The shark was transferred to an isolation pool for 1 mo. A second immobilization via immersion in eugenol was conducted in order to perform a celiotomy. The hook was located in a liver lobe and was surgically removed. After a prolonged recovery from anesthesia, the shark was released into its primary tank and recovered uneventfully, although some of the skin sutures sloughed prematurely.

Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kashima-nada, Japan

The white shark, a top predator inhabiting the world’s oceans, is an endangered species. However, knowledge of its life-history traits and population structure is still limited. We hypothesised that life-history traits would vary among populations because the species’ various habitats are diverse and change through time. Age was estimated by counting growth bands in the centra of white sharks caught in Japan. The von Bertalanffy growth parameters were estimated at L∞ = 455 cm TL, k = 0.196 year–1 and t0 = –1.92 years for males and L∞ = 607 cm TL, k = 0.159 year–1 and t0 = –1.80 years for females. The growth rate to maturity was higher than that known for individuals from California and South Africa. Male sharks matured at 310 cm TL at 4 years of age and females began to mature at ~450 cm TL and 7 years. The D-loop-region sequences of mitochondrial DNA extracted from Japanese white sharks and GenBank datasets from sharks of California, Australia, New Zealand and South Africa indicate that Japanese white sharks form a monophyletic clade separate from the populations of other regions. The results suggest that unique life-history traits of Japanese white sharks may be caused by genetic differences.

Morphology and Lectin histochemistry of the testes of brown-banded bamboo shark (Chiloscyllium punctatum)

The testes of three brown-banded bamboo male sharks collected from Okinawa Churaumi Aquarium, Japan were used in this study. The testes were studied grossly and microscopically. In addition, conventional and lectin histochemistry (panel of 8 HRP lectins, UEA-I, DBA, LCA, PNA, ConA, PHA-E4, WGA and RCA 120) were applied for studying the glycoconjugates.

A genetic assessment of polyandry and breeding‐site fidelity in lemon sharks

We here employ 11 microsatellite markers and recently developed litter reconstruction methods to infer mating system parameters (i.e. polyandry and breeding-site fidelity) at a lemon shark nursery site in Marquesas Key, Florida. Four hundred and eight juvenile or subadult sharks were genotyped over eight complete breeding seasons. Using this information, we were able to infer family structure, as well as fully or partially reconstruct genotypes of 46 mothers and 163 fathers. Multiple litter reconstruction methods were used, and novel simulations helped define apparent bias and precision of at least some mating system parameters. For Marquesas Key, we find that adult female lemon sharks display high levels of polyandry (81% of all litters sampled) and stronger fidelity to the nursery site than do males. Indeed, few male sharks sired offspring from more than one litter during the course of the study. These findings were quite similar to previous results from another lemon shark nursery site (Bimini, Bahamas), suggesting conserved mating system parameters despite significant variation in early life-history traits (i.e. body size and growth) among sites. The finding of at least some site fidelity in females also supports the need for careful conservation of each nursery.

Non-lethal assessment of reproductive characteristics for management and conservation of sharks

Chondrichthyans are one of the most vulnerable groups of marine species, with increasing numbers being listed as endangered or threatened. Fundamental to the conservation and management of any animal is an understanding of their reproduction and particularly, the size at which individuals enter the reproductive population. Size at maturity in sharks is typically obtained by macroscopic examination of the gonads after sacrificing the fish. Using the draughtboard shark Cephaloscyllium laticeps as a case study, we found that equivalent information can be obtained nondestructively using steroid hormone levels measured from a blood sample. This technique allowed us to release the shark after only 1 to 2 min of handling. A combination of plasma steroid hormone concentrations and an external measurement (total length for females and clasper length for males) was used to determine that over 90% of female and 95% of male sharks were either juveniles or adults. The estimates of size at maturity from the hormone analysis were within 3% of equivalent values of dissected sharks. Once validated, hormone levels can also be used to determine seasonal reproductive patterns for the adult population. Our results demonstrated how measurement of plasma levels of steroid hormones can provide a non-destructive method for obtaining reproductive data necessary for managing vulnerable and endangered shark species. The development of a non-destructive sampling tool also allows for improved ethical investigation into this vulnerable group of marine fishes.