Three decades of longlining in Bimini,Bahamas, reveals long‐term trends in lemon shark Negaprion brevirostris (Carcharhinidae) catch per unit effort

In Bimini, Bahamas, the consistent employment of longlines, beginning in 1982, provided a rare opportunity to explore population trends for large resident sharks. This study assessed three shallow water longline survey periods at this location; 1982–1989, 1992–2002 and 2003–2014, with the aim of determining trends in annual catch per unit effort (CPUE) for an IUCN listed near‐threatened species, the lemon shark Negaprion brevirostris. A general additive model (GAM) was used to analyse the non‐linear annual CPUE values over the entire 32‐year research period. The GAM displayed high variability of annual CPUE, with a peak value of 0·026 N. brevirostris per hook day (hooks day^?1) in 2000. The temporal pattern of CPUE indicated an abundance trend with a complete cycle, from trough to trough, occurring over a period of approximately 18 years. The 1982–1989 survey period saw the highest proportion of mature individuals (19·8%) and the smallest average pre‐caudal length (L_PC; 124·8 cm). The 1992–2002 survey period had the highest average annual CPUE (0·018 hooks day^?1), while the 2003–2014 research period saw largest average L_PC size (134·8 cm) and the lowest average CPUE values (0·009 hooks day^?1) of the entire research period. The long‐term trend identified in this study provides a baseline for future assessment.     

Prey selection and functional response of juvenile lemon sharks Negaprion brevirostris

Prey preference of juvenile lemon sharks Negaprion brevirostris was examined in experiments conducted in field-based pens where the fish were offered meals of live teleosts: grey snapper Lutjanus griseus and yellow fin majorra Gerres cinereus in ratios of L. griseus : G. cinereus varying from 10:0 to 2:8. Relative electivity indices for each treatment showed that N. brevirostris preyed on G. cinereus rather than L. griseus . They showed a prey preference relating to density of G. cinereus (type II functional response) but not to L. griseus .     

Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation

DNA microsatellite markers were used to characterize the population genetic structure of the lemon shark, Negaprion brevirostris, in the western Atlantic. This study demonstrates for the first time the usefulness of microsatellites to study population genetic structure and mating systems in the Chondricthyes. Lemon sharks (mostly juveniles) were sampled non-destructively from four locations, Gullivan Bay and Marquesas Key in Florida, Bimini, Bahamas, and Atol das Rocas, Brazil. At least 545 individuals were genotyped at each of four dinucleotide loci. The number of alleles per locus ranged from 19 to 43, and expected heterozygosities ranged from 0.69 to 0.90. Relatively little genetic structure was found in the western Atlantic, with small but significant values for estimators of F(ST) and R(ST) among populations, theta (0.016) and rho (0.026), respectively. No sharp discontinuities were found between the Caribbean sites and Brazil, and most alleles were found at all four sites, indicating that gene flow occurs throughout the western Atlantic with no evidence for distinct stocks.     

Effect of ration size on growth and gross conversion efficiency of young lemon sharks, Negaprion brevirostris

Young lemon sharks, Negaprion brevirostris , were kept under controlled conditions in an aquarium and fed blue runner, Caranx crysos , at different ration levels. The relationship between feeding rate and growth rate was best described by a von Bertalanffy growth curve, which predicted a maximum growth rate of 140 kJ kg⁻¹ day⁻¹ (0·66% b.w. day⁻¹), a maintenance ration of 199 kJ kg⁻¹ day⁻¹ (1·06% b.w. day⁻¹), and losses due to starvation of -236kJ kg⁻¹ day⁻¹ (1·11% b.w. day⁻¹). The relationship between gross conversion efficiency ( K ₁) and feeding rate was also examined. K₁ ranged from - 64 to 25% and did not drop at high ration levels. Activity levels of both starved sharks and sharks fed at maintenance were not significantly different (0·2 body lengths s⁻¹). K ₁ values generated from both laboratory and field data suggest that young lemon sharks can convert food to new tissue as efficiently as teleosts.     

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.     

Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas

The waters around Bimini (25° 43.70′ N, 79° 18.00′ W) provide an ideal nursery location for juvenile lemon sharks, Negaprion brevirostris, but this habitat is threatened by the development of a large resort. Since 1999 the North Sound (NS) has been subjected to intermittent periods of dredging, the most intensive of which was in March 2001. Possible effects from the development up to June 2006 were investigated by: comparing growth rates of juvenile lemon sharks in the NS, Sharkland (SL) and South Bimini (SB) nurseries between 1995-2005 using before-after, control-impact (BACI) analysis; analyzing survival of juvenile lemon sharks in the NS and SL between 1995–2006; and by comparing habitat structures in the NS and SB nurseries in 2003 and 2005. BACI analysis detected no statistically significant difference between the growth rates of juvenile lemon sharks in the three nurseries before and after the impact date of March 2001. However, a reduction in the survival rate of juvenile lemon sharks in the NS after March 2001 was statistically significant, including a 23.5% decline in first-year survival. Habitat structure of the NS in 2003 and 2005 also varied with the mean percentage cover of the seagrass Thalassia testudinum declining by 17.7% since 2003. Our results indicate a correlation between the development thus far and a decline in the survival rates of juvenile lemon sharks and changes in the habitat structure of the NS. To elucidate further information regarding potential effects of the resort development on juvenile lemon sharks in the NS nursery, we suggest several future research directions.     

Gastric evacuation in the young lemon shark,Negaprion brevirostris,under field conditions

Synopsis Gastric evacuation in young lemon sharks, Negaprion brevirostris, was studied in a field enclosure. Regression analysis was used to evaluate the adequacy of linear, exponential, and square root models in describing the decrease in stomach contents with time after feeding. The linear model produced the best fit and was thus used to compare gastric evacuation at the three temperatures. Gastric evacuation in young lemon sharks is considerably longer than for carnivorous teleosts but shorter than for other elasmobranchs. These differences are the result of differing energy requirements determined by the physiology and behavior of the species.     

Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark,Negaprion brevirostris

Synopsis We have examined the concentrations of reproductively-related steroid hormones in 5 species of carcharhinid sharks, marine fishes possessing the unique attribute of placental viviparity. Measurements of serum estradiol, testosterone, progesterone, dihydrotestosterone, and corticosterone have provided baseline data for these hormones in both immature and adult male and female placental sharks. Our studies include: (1) changes in hormonal levels during maturation, (2) concentrations of circulating steroid hormones during peak breeding season, and (3) hormonal levels during gestation, including the collection of serial samples through and beyond birth from free-ranging lemon sharks. Our data suggest that steroids, important in regulating reproduction in higher mammals, are also essential in these cartilaginous fishes.     

Isolation and characterization of five dinucleotide microsatellite loci in the sandbar shark,Carcharhinus plumbeus

Five dinucleotide markers were isolated and optimized from a microsatellite‐enriched genomic library obtained from the sandbar shark, Carcharhinus plumbeus. Genotypic distributions of all markers were found to be in conformance with the expectations of Hardy–Weinberg equilibrium with four to 39 alleles present per locus. We amplified these loci in two female sharks and their litters. A maternal allele was recovered at each locus in all progeny indicating reliable amplification. More than two paternal alleles were recovered across both litters indicating genetic polyandry. Additionally, these markers were amplified across 10 carcharhiniform species to examine their utility in other studies.     

matesoft: a program for deducing parental genotypes and estimating mating system statistics in haplodiploid species

With the advent of sophisticated genetic markers, studies on mating systems and reproductive apportionment have become increasingly feasible. In particular, paternity analyses in haplodiploid species have gained in power as hemizygous paternal genotypes allow maternal and paternal genotypes to be directly inferred from offspring genotypes. The computer program matesoft offers both newly developed algorithms for inferring maternal and paternal genotypes, and integrated estimation and correction procedures for calculating mating frequency statistics. Standard data are offspring genotypes of male‐haplodiploid organisms, including social Hymenoptera.     

Isolation and characterization of microsatellite loci in the whale shark (Rhincodon typus)

In preparation for a study on population structure of the whale shark (Rhincodon typus), nine species-specific polymorphic microsatellite DNA markers were developed. An initial screening of 50 individuals from Holbox Island, Mexico found all nine loci to be polymorphic, with two to 17 alleles observed per locus. Observed and expected heterozygosity per locus ranged from 0.200 to 0.826 and from 0.213 to 0.857, respectively. Neither statistically significant deviations from Hardy-Weinberg expectations nor statistically significant linkage disequilibrium between loci were observed. These microsatellite loci appear suitable for examining population structure, kinship assessment and other applications.     

Social polyandry, parental investment, sexual selection, and evolution of reduced female gamete size

Abstract Sexual selection in the form of sperm competition is a major explanation for small size of male gametes. Can sexual selection in polyandrous species with reversed sex roles also lead to reduced female gamete size? Comparative studies show that egg size in birds tends to decrease as a lineage evolves social polyandry. Here, a quantitative genetic model predicts that female scrambles over mates lead to evolution of reduced female gamete size. Increased female mating success drives the evolution of smaller eggs, which take less time to produce, until balanced by lowered offspring survival. Mean egg size is usually reduced and polyandry increased by increasing sex ratio (male bias) and maximum possible number of mates. Polyandry also increases with the asynchrony (variance) in female breeding start. Opportunity for sexual selection increases with the maximum number of mates but decreases with increasing sex ratio. It is well known that parental investment can affect sexual selection. The model suggests that the influence is mutual: owing to a coevolutionary feedback loop, sexual selection in females also shapes initial parental investment by reducing egg size. Feedback between sexual selection and parental investment may be common.     

Reproductive biology,multiple paternity and polyandry of the bull shark Carcharhinus leucas

To improve understanding of bull shark Carcharhinus leucas reproductive biology, we analysed reproductive traits from 118 bull sharks caught along Reunion Island coasts (Western Indian Ocean), including 16 gravid females. Specific microsatellite loci were used to investigate the frequency of multiple paternity. Males and females reached maturity at c. 234 cm and 257 cm total length (L_T), respectively, and litter sizes ranged from 5 to 14 embryos. Analysis of the 16 litters collected in various months of the year indicated that parturition occurs between October and December, with a size at birth c. 60–80 cm L_T and that the gestation period is probably c. 12 months. Assuming a 1 year resting period and a period of sperm storage (4–5 months) between mating (in June–September) and fertilisation, the reproductive cycle of bull sharks at Reunion Island would be biennial. At least 56.25% of the litters investigated were polyandrous, sired by 2–5 males. Several males that each sired several litters conceived during the same or distinct mating seasons were detected, suggesting both a seasonal aggregation of sharks to mate and some male fidelity to mating site. Altogether, these findings provide valuable information for both shark risk management and conservation of the species in the Western Indian Ocean.     

Pedigree simulations reveal that maternity assignment is reliable in populations with conspecific brood parasitism,incomplete parental sampling and kin structure

Modern genetic parentage methods reveal that alternative reproductive strategies are common in both males and females. Under ideal conditions, genetic methods accurately connect the parents to offspring produced by extra-pair matings or conspecific brood parasitism. However, some breeding systems and sampling scenarios present significant complications for accurate parentage assignment. We used simulated genetic pedigrees to assess the reliability of parentage assignment for a series of challenging sampling regimes that reflect realistic conditions for many brood-parasitic birds: absence of genetic samples from sires, absence of samples from brood parasites and female kin-structured populations. Using 18 microsatellite markers and empirical allele frequencies from two populations of a conspecific brood parasite, the wood duck (Aix sponsa), we simulated brood parasitism and determined maternity using two widely used programs, cervus and colony . Errors in assignment were generally modest for most sampling scenarios but differed by program: cervus suffered from false assignment of parasitic offspring, whereas colony sometimes failed to assign offspring to their known mothers. Notably, colony was able to accurately infer unsampled parents. Reducing the number of markers (nine loci rather than 18) caused the assignment error to slightly worsen with colony but balloon with cervus . One potential error with important biological implications was rare in all cases—few nesting females were incorrectly excluded as the mother of their own offspring, an error that could falsely indicate brood parasitism. We consider the implications of our findings for both a retrospective assessment of previous studies and suggestions for best practices for future studies.     

In the intimacy of the darkness: Genetic polyandry in deep-sea luminescent lanternsharks Etmopterus spinax and Etmopterus molleri (Squaliformes,Etmopteridae)

Multiple paternity seems common within elasmobranchs. Focusing on two deep-sea shark species, the velvet belly lanternshark (Etmopterus spinax) and the slendertail lanternshark (Etmopterus molleri) we inferred the paternity in 31 E. spinax litters from Norway (three to 18 embryos per litter) and six E. molleri litters from Japan (three to six embryos), using 21 and 10 specific microsatellites, respectively. At least two E. spinax litters were sired from multiple fathers each, with highly variable paternal skew (1:1 to 9:1). Conversely, no clear signal of genetic polyandry was found in E. molleri.     

Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus)

Levels of parental relatedness can affect offspring survival and susceptibility to disease. We investigated parental relatedness of live and dead Halichoerus grypus pups between and within island populations and between possible causes of mortality. Nine microsatellites were used to calculate internal relatedness (IR) and standardized mean d2. We find that pups with higher than average levels of IR have significantly lower survival and that this varied between island populations and that certain loci contributed to the effect more than others. Although, there were no significant differences between causes of mortality, peritonitis, infection and stillborn had the highest levels of IR. These results provide evidence that parental relatedness is an important determinant of pre-weaning pup survival in the grey seal and that this may vary with cause of mortality given a larger sample size.     

Breeding system, colony structure, and genetic differentiation in the Camponotus festinatus species complex of carpenter ants

All social insects live in highly organized societies. However, different social insect species display striking variation in social structure. This variation can significantly affect the genetic structure within populations and, consequently, the divergence between species. The purpose of this study was to determine if variation in social structure was associated with species diversification in the Camponotus festinatus desert carpenter ant species complex. We used polymorphic DNA microsatellite markers to dissect the breeding system of these ants and to determine if distinct C. festinatus forms hybridized in their natural range. Our analysis of single-queen colonies established in the laboratory revealed that queens typically mated with only a single male. The genotypes of workers sampled from a field population suggested that multiple, related queens occasionally reproduced within colonies and that colonies inhabited multiple nests. Camponotus festinatus workers derived from colonies of the same form originating at different locales were strongly differentiated, suggesting that gene flow was geographically restricted. Overall, our data indicate that C. festinatus populations are highly structured. Distinct C. festinatus forms possess similar social systems but are genetically isolated. Consequently, our data suggest that diversification in the C. festinatus species complex is not necessarily associated with a shift in social structure.     

Development and characterization of eight new microsatellite markers for the haremic sandperch,Parapercis cylindrica (family Pinguipedidae)

Eight di‐, tri‐ and tetranucleotide microsatellite markers were developed for the haremic sandperch Parapercis cylindrica using a linker‐ligated, magnetic bead enrichment protocol. Screening of at least 17 individuals showed these markers to be polymorphic with observed heterozygosity ranging from 0.381 to 1.000 (mean = 0.742) and the numbers of alleles ranging from three to 18. The average polymorphic information content for these eight loci was 0.723. These markers may be used for parentage studies aimed at exploring the complex mating strategies employed by this haremic coral reef fish and will be valuable for population genetic studies.