Age‐ and sex‐related dietary specialization facilitate seasonal resource partitioning in a migratory shorebird

1. Dietary specialization is common in animals and has important implications for individual fitness, inter‐ and intraspecific competition, and the adaptive potential of a species. Diet composition can be influenced by age‐ and sex‐related factors including an individual''s morphology, social status, and acquired skills; however, specialization may only be necessary when competition is intensified by high population densities or increased energetic demands.
2. To better understand the role of age‐ and sex‐related dietary specialization in facilitating seasonal resource partitioning, we inferred the contribution of biofilm, microphytobenthos, and benthic invertebrates to the diets of western sandpipers (Calidris mauri) from different demographic groups during mid‐winter (January/February) and at the onset of the breeding migration (April) using stable isotope mixing models. Western sandpipers are sexually dimorphic with females having significantly greater body mass and bill length than males.
3. Diet composition differed between seasons and among demographic groups. In winter, prey consumption was similar among demographic groups, but, in spring, diet composition differed with bill length and body mass explaining 31% of the total variation in diet composition. Epifaunal invertebrates made up a greater proportion of the diet in males which had lesser mass and shorter bills than females. Consumption of Polychaeta increased with increasing bill length and was greatest in adult females. In contrast, consumption of microphytobenthos, thought to be an important food source for migrating sandpipers, increased with decreasing bill length and was greatest in juvenile males.
4. Our results provide the first evidence that age‐ and sex‐related dietary specialization in western sandpipers facilitate seasonal resource partitioning that could reduce competition during spring at the onset of the breeding migration.
5. Our study underscores the importance of examining resource partitioning throughout the annual cycle to inform fitness and demographic models and facilitate conservation efforts.

     

A novel field method to distinguish between cryptic carcharhinid sharks,Australian blacktip shark Carcharhinus tilstoni and common blacktip shark C. limbatus,despite the presence of hybrids

Multivariate and machine‐learning methods were used to develop field identification techniques for two species of cryptic blacktip shark. From 112 specimens, precaudal vertebrae (PCV) counts and molecular analysis identified 95 Australian blacktip sharks Carcharhinus tilstoni and 17 common blacktip sharks Carcharhinus limbatus. Molecular analysis also revealed 27 of the 112 were C. tilstoni × C. limbatus hybrids, of which 23 had C. tilstoni PCV counts and four had C. limbatus PCV counts. In the absence of further information about hybrid phenotypes, hybrids were assigned as either C. limbatus or C. tilstoni based on PCV counts. Discriminant analysis achieved 80% successful identification, but machine‐learning models were better, achieving 100% successful identification, using six key measurements (fork length, caudal‐fin peduncle height, interdorsal space, second dorsal‐fin height, pelvic‐fin length and pelvic‐fin midpoint to first dorsal‐fin insertion). Furthermore, pelvic‐fin markings could be used for identification: C. limbatus has a distinct black mark >3% of the total pelvic‐fin area, while C. tilstoni has markings with diffuse edges, or has smaller or no markings. Machine learning and pelvic‐fin marking identification methods were field tested achieving 87 and 90% successful identification, respectively. With further refinement, the techniques developed here will form an important part of a multi‐faceted approach to identification of C. tilstoni and C. limbatus and have a clear management and conservation application to these commercially important sharks. The methods developed here are broadly applicable and can be used to resolve species identities in many fisheries where cryptic species exist.     

The tooth,the whole tooth and nothing but the tooth: tooth shape and ontogenetic shift dynamics in the white shark Carcharodon carcharias

Results from this study of the white shark Carcharodon carcharias include measurements obtained using a novel photographic method that reveal significant differences between the sexes in the relationship between tooth cuspidity and shark total length, and a novel ontogenetic change in male tooth shape. Males exhibit broader upper first teeth and increased distal inclination of upper third teeth with increasing length, while females do not present a consistent morphological change. Substantial individual variation, with implications for pace of life syndrome, was present in males and tooth polymorphism was suggested in females. Sexual differences and individual variation may play major roles in ontogenetic changes in tooth morphology in C. carcharias, with potential implications for their foraging biology. Such individual and sexual differences should be included in studies of ontogenetic shift dynamics in other species and systems.     

Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning

The diets of two urolophids, the common stingaree Trygonoptera testacea and the kapala stingaree Urolophus kapalensis were analysed and compared to examine resource partitioning between these two morphologically similar sympatric Australian batoids. The diet of T. testacea was polychaete-based, while that of U. kapalensis was dominated by crustaceans (mostly carid shrimps and amphipods). Intraspecific dietary compositions were examined amongst size classes within each of the two species to identify ontogenetic shifts in diet. Differences in the dietary compositions of the smaller total-length classes of T. testacea suggest that their diet shifts as they increase in size, from one dominated by carids to one almost entirely comprising polychaetes. Significant ontogenetic dietary shifts were not identified in U. kapalensis . Although the two species shared eight broad dietary categories, their overall dietary compositions were found to be significantly different. The limited overlap in the dietary compositions of these two sympatric stingarees suggests the possibility of resource partitioning, with interspecific competition being implicated as a possible cue. Possible mechanisms for the partitioning of resources within and between these two species are discussed.     

Age and growth of the sandbar shark, Carcharhinus plumbeus, in Hawaiian waters through vertebral analysis

Age and growth estimates were determined for the sandbar shark, Carcharhinus plumbeus, from Oahu, Hawaii in the central Pacific Ocean. Age estimates were obtained through vertebral centra analysis of 187 sharks. We verified our age estimates through marginal increment analysis of centra and oxytetracycline marking methods of at liberty sandbar sharks. Sizes of sampled sharks ranged from 46 to 147 cm pre-caudal length. Four growth models were fitted to length-at-age data; two forms of the von Bertalanffy growth model, the Gompertz growth model, and a logistic growth model. Males and females exhibited statistically significant differences in growth, indicating that females grow slower and attain larger sizes than males. Growth parameter estimates revealed slower growth rates than previously estimated (based on captive specimens) for Hawaiian sandbar sharks. The von Bertalanffy growth model using empirical length-at-birth provided the best biological and statistical fit to the data. This model gave parameter estimates of L _∞ = 138.5 cm PCL and k = 0.12 year⁻¹ for males and L _∞ = 152.8 cm PCL, k = 0.10 year⁻¹ for females. Male and female sandbar sharks mature at approximately 8 and 10 years of age, respectively.     

Early Miocene (Ottnangian) Mollusca of the Western Paratethys—ontogenetic strategies and palaeo-environments

Early ontogenetic shells of 25 species of brackish water and freshwater molluscs from the Ottnangian (Lower Miocene) Oncophora Beds (Lower Bavaria, South Germany) and Kirchberg Formation (Upper Bavaria, South Germany) are described for the first time. Taxonomic implications are discussed. The investigated bivalves (Cardiidae and Dreissenidae) were characterised by an indirect development with inclusion of a planktonic veliger stage. Among the gastropods only three species of the genus CtyrokiaSchlickum, 1965 were characterised by veliger larvae, all the other gastropod species were direct developers, which hatched as crawling young. The species Agapilia schlickumi nov. sp. (Neritidae), Nematurella pseudozilchi nov. sp. and Nematurella strauchi nov. sp. (Hydrobiidae) are introduced. Our study revealed the co-occurrence of 10 molluscan species in the Oncophora Basin of Lower Bavaria and the Kirchberg Basin of Upper Bavaria and thus indicates similar oligohaline to mesohaline coastal swamp milieus for both depositional environments. The presence of planktonic larval development in gastropods indicates a connection to the open sea.     

Molecular cloning, tissue distribution and ontogenetic expression of sodium proton exchanger isoform 2 ( NHE-2) mRNA in the small intestine of pigs

Molecular cloning, tissue distribution and ontogenetic regulation of sodium/proton exchanger isoform 2 (NHE-2) mRNA expression were evaluated in the pig small intestine during postnatal development. The 2872-bp porcine full cDNA sequence of the NHE-2 (EF672046) cloned in this study showed 80% and 70% homology with known human and mouse gene sequence, respectively. Hydrophobic prediction suggests 13 putative membrane-spanning domains within porcine NHE-2. The porcine NHE-2 mRNA was detected in the brain, liver, kidney, heart, lung, small intestine and muscle. The small intestine had the highest NHE-2 mRNA abundance and the brain, lung and liver had the lowest NHE-2 mRNA abundance (P < 0.05). Along the longitudinal axis, the duodenum had the highest NHE-2 mRNA abundance and the ileum and colon had the lowest NHE-2 mRNA abundance (P < 0.05). The NHE-2 mRNA level was increased from day 1 to day 26 in the duodenum (P < 0.05) and dropped dramatically on day 30 (P < 0.05). There is no difference between day 1 and day 7 (P > 0.05). After day 30, the NHE-2 mRNA level remained the same except on day 90 (P > 0.05). The mRNA expression of NHE-2 was not only differentially regulated by age but also differentially distributed along the small intestine of piglets at early stages and growing stages of life, which may contribute to changes in NHE activity.     

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.     

Demographic analyses of the dusky shark, <Emphasis Type="Italic">Carcharhinus obscurus,</Emphasis> in the Northwest Atlantic incorporating hooking mortality estimates and revised reproductive parameters

Demographic analyses were conducted for the dusky shark, Carcharhinus obscurus, in the Northwest Atlantic. Fishery-independent, fishery-dependent, and previously published data were used to estimate age specific by-catch mortality and reproductive cycle for incorporation into the analyses. Correspondence analyses were conducted for viability (dead or alive), shark length, month, soaktime, and region. Dead sharks were associated with small size, long soak times, and the spring season, while live sharks were associated with large size and shorter soak times. Data on reproduction suggested a 3-year reproductive cycle consisting of a 2-year gestation period and a 1-year resting period. Litter sizes ranged from 3–12 embryos. Decreasing age-specific fishing mortality and a 3-year reproductive cycle were used in age structured life tables which incorporated stochasticity in life history parameters through Monte Carlo simulation to estimate annual population growth. Demographic analyses showed that the dusky shark population would decline even at low levels of fishing mortality despite low natural mortality for neonates. The demographics of this species make it among the most vulnerable to excessive fishing mortality, and suggest stringent regulatory measures may be required to recover collapsed populations.     

Age and growth of the blacknose shark, <Emphasis Type="Italic">Carcharhinus acronotus</Emphasis>, in the western North Atlantic Ocean with comments on regional variation in growth rates

We examined the age and growth of the blacknose shark, Carcharhinus acronotus, in the western North Atlantic Ocean by obtaining direct age estimates using vertebral centra. We verified annual deposition of growth increments with marginal increment analysis and validated it by analyzing vertebrae marked with oxytetracycline from a female blacknose shark held in captivity. Von Bertalanffy growth parameters indicated that female blacknose sharks have a lower growth constant (k), a larger theortical maximum size (L), and are longer lived than males. We compared these growth parameters for blacknose sharks in the western North Atlantic Ocean to growth parameters for blacknose sharks collected in the eastern Gulf of Mexico to test for differences between regions. Females in the western North Atlantic Ocean have a significantly lower L, lower k, and a higher theoretical longevity than females in the Gulf of Mexico. Males in the western North Atlantic Ocean have a higher L<>, lower k, and higher theoretical longevity than males in the Gulf of Mexico. The significant differences between these life history parameters for blacknose sharks suggest that, when possible, future management initiatives concerning blacknose sharks should consider managing the populations in the western North Atlantic and the Gulf of Mexico as separate stocks.     

The effect of biogeographic and phylogeographic barriers on gene flow in the brown smoothhound shark,Mustelus henlei,in the northeastern Pacific

We assessed the effects of the prominent biogeographic (Point Conception and the Peninsula of Baja California) and phylogeographic barriers (Los Angeles Region) of the northeastern Pacific on the population connectivity of the brown smoothhound shark, Mustelus henlei (Triakidae). Data from the mitochondrial control region and six nuclear microsatellite loci revealed significant population structure among three populations: northern (San Francisco), central (Santa Barbara, Santa Catalina, Punta Lobos, and San Felipe), and southern (Costa Rica). Patterns of long‐term and contemporary migration were incongruent, with long‐term migration being asymmetric and occurring in a north to south direction and a lack of significant contemporary migration observed between localities with the exception of Punta Lobos that contributed migrants to all localities within the central population. Our findings indicate that Point Conception may be restricting gene flow between the northern and central populations whereas barriers to gene flow within the central population would seem to be ineffective; additionally, a contemporary expansion of tropical M. henlei into subtropical and temperate waters may have been observed.     

Dyadic brain modelling,mirror systems and the ontogenetic ritualization of ape gesture

The paper introduces dyadic brain modelling, offering both a framework for modelling the brains of interacting agents and a general framework for simulating and visualizing the interactions generated when the brains (and the two bodies) are each coded up in computational detail. It models selected neural mechanisms in ape brains supportive of social interactions, including putative mirror neuron systems inspired by macaque neurophysiology but augmented by increased access to proprioceptive state. Simulation results for a reduced version of the model show ritualized gesture emerging from interactions between a simulated child and mother ape.     

Genetic profiling reveals illegal international trade in fins of the great white shark, <Emphasis Type="Italic">Carcharodon carcharias</Emphasis>

Great white sharks are protected by national legislation in several countries, making this species the most widely protected elasmobranch in the world. Although the market demand for shark fins in general has continued to grow, the value and extent of utilization of white shark fins in trade has been controversial. We combine law enforcement with genetic profiling to demonstrate that illegal trade in fins of this species is occurring in the contemporary international market. Furthermore, we document the presence of fins from very young white sharks in the trade, suggesting a multiple-use market (food to trophies) exists for fins of this species. The presence of small fins in the trade contradicts the view that white shark fins have market value only as large display trophies, and not as food. Our findings indicate that effective conservation of protected shark species will require international management regimes that include monitoring of the shark fishery and trade on a species-specific basis.     

On the Origins of the Spanish Word ‘tiburón’, and the english word ‘shark’

Large sharks were known to the Greeks and Romans, and references to large sharks of the Mediterranean are found in the writings of classical writers. However, large sharks are conspicuously absent from the medieval bestiaries that described the then known fauna. The explanation for this interesting omission is simple: Medieval man did not encounter large sharks because he fished mainly in rivers and close to shore and did not venture far into the ocean to catch fish, and the few large European sharks did not venture into rivers or shallow waters. The Spanish and the English first encountered large sharks in the American tropics. Both groups borrowed Amerindian words to designate them. The Spanish borrowed the word tiburón from the Carib Indians, and, later, the English borrowed tiburón from the Spanish and used it for about 100 years. In the late sixteenth century, the English borrowed the word xoc from the Mayans and it became the English word shark.     

Huffmanela selachii n. sp. (Nematoda: Trichosomoididae: Huffmanelinae): A new species infecting the skin of the great hammerhead shark (Sphyrna mokarran) and the blacktip reef shark (Carcharhinus melanopterus) in the Arabian Gulf,off-shore Saudi Arabia

From January 2017 - December 2019, 75 out of 850 (8.8 %) great hammerhead sharks from the Arabian Gulf had skin lesions of black irregular discolorations on the ventral surface of the head. The lesions consisted of pencil-like lineations often advancing forward by about 2 mm in back-and-forth looped scribbles often forming a relatively linear bands of about 5–7 cm wide. Similar lesions were also found in the blacktip reef shark from the same area within the same period, and consisted of straight to irregular black lines, extended indiscriminately across the skin of the sharks. Microscopic examination of the skin revealed the presence of dark-brown eggs exhibiting the spindle or ellipsoidal eggs characteristic of Huffmanela sp. The morphometrics of eggs from both hosts were similar (62.9–89.9 μm long and 29.3–56.1 μm wide). The eggshells were smooth with polar plugs protruding or not, with an abruptly truncated crown-like or shoulder-like collar surrounding the plug. The eggs were only found in the epidermal layer of the skin. Based on the unique morphometrics of the eggs, we report a new species, named: Huffmanela selachii n. sp.. This appears to be the first report of Huffmanela from either the great hammerhead shark or the blacktip reef shark, and the third reported Huffmanela in sharks from the Arabian Gulf. It is also one of few species reported from connecting waters of the greater Indian Ocean. This new finding contributes to our understanding of the diversity and ubiquity of Huffmanela sp. in marine creatures.     

Food habits and ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in Hawaii

The sandbar shark, Carcharhinus plumbeus, is a wide-ranging coastal species in tropical and temperate regions, and it is the most common species of shark in Hawaii, as in many locations where it occurs. Information on the diet and feeding habits of this species in the Pacific Ocean are extremely limited. For this study we quantified the diet of sandbar sharks in Hawaii based on records collected during the Hawaii Cooperative Shark Research and Control Program from 1967 to 1969. During this program a total of 565 stomachs were examined, of which 265 contained food. Sharks ranged in size from 59 to 190 cm total length. Teleosts were the most common prey group, but both cephalopods and crustaceans also occurred frequently. Ontogenetic changes in diet of sandbar sharks were apparent, with crustaceans forming a greater proportion of the diet of smaller sharks. Both cephalopods and elasmobranchs increased in importance with increasing shark size. Prey diversity also increased with size, with large, mobile, and reef prey species found more commonly in the diet of larger sharks. Mature male and female sharks appeared to segregate by depth, though major differences in the diet between the sexes were not apparent. However, there was some evidence of dietary differences between sharks caught in different depths and seasons. The results of this study suggest that sandbar sharks in Hawaii and throughout the world, are primarily piscivores, but also consume a variety of invertebrate prey, and that their diet varies with geographical location and stage of development.     

Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris

Because sharks possess an unusual suite of reproductive characteristics, including internal fertilization, sperm storage, relatively low fecundity, and reproductive modes that range from oviparity to viviparity, they can provide important insight into the evolution of mating systems and sexual selection. Yet, to date, few studies have characterized behavioral and genetic mating systems in natural populations of sharks or other elasmobranchs. In this study, highly polymorphic microsatellite loci were used to examine breeding biology of a large coastal shark, the lemon shark, Negaprion brevirostris, at a tropical lagoon nursery. Over six years, 910 lemon sharks were sampled and genotyped. Young were assigned into sibling groups that were then used to reconstruct genotypes of unsampled adults. We assigned 707 of 735 young sharks to one of 45 female genotypes (96.2%), and 485 (66.0%) were assigned to a male genotype. Adult female sharks consistently returned to Bimini on a biennial cycle to give birth. Over 86% of litters had multiple sires. Such high levels of polyandry raise the possibility that polyandry evolved in viviparous sharks to reduce genetic incompatibilities between mother and embryos. We did not find a relationship between relatedness of mates and the number of offspring produced, indicating that inbreeding avoidance was probably not driving pre- or postcopulatory mate choice. Adult male sharks rarely sired more than one litter at Bimini and may mate over a broader geographic area.     

Body shape, diet and ontogenetic diet shifts in young fish of the Sinnamary River, French Guiana, South America

A total of 1468 young fish representing 66 taxa from the Sinnamary River, French Guiana was classified by complete cluster analysis of mean relative body width and mean relative body height into four groups. These had anguilliform, disciform, flat or intermediate body shapes and belonged chiefly to Gymnotiformes, Perciformes, Siluriformes and Characiformes, respectively. Several of the taxa shifted from one to another body shape during ontogenesis. Seven diet groups were defined by complete cluster analysis. Among these, six groups were represented by carnivorous fish. The three most frequent groups had diets of (1) mainly insect larvae and small crustaceans, (2) insect larvae, and (3) predominantly terrestrial insects. The majority of the fish taxa showed ontogenetic diet shifts. Carnivorous fish usually switched from small-size prey, such as small crustaceans, to intermediate-size prey, such as insect larvae and/or to large-size prey, such as insects and/or fish. However, taxa differed in their capacities to switch from small prey to intermediate and/or to large prey. Taxa of different body shapes had significantly different diets. Disciform fish fed mainly on aquatic insect larvae and terrestrial insects but also, in small amounts, on small curstaceans. Most anguilliform taxa ate insect larvae. Individuals belonging to the depressiform or intermediate morphotype had varied diets ranging from plant debris and substratum to fish.     

Influence of selected factors on the dietary compositions of three targeted and co‐occurring temperate species of reef fishes: implications for food partitioning

The dietary compositions of three medium to large targeted fish species, which co‐occur over reefs in temperate waters of south‐western Australia, were determined. These data were then used to ascertain statistically the extent to which body size, season and habitat influence the diets of these species and the degree to which food resources were partitioned among and within those species, and thus reduced the potential of interspecific and intraspecific competition. On the west coast, Bodianus frenchii (Labridae) and Epinephelides armatus (Serranidae) spent their whole life over prominent limestone reefs, as did Glaucosoma hebraicum (Glaucosomatidae) in all but juvenile life, when it lived over low‐relief, limestone substrata. The dietary composition of each species changed with increasing body size, which, in G. hebraicum, was particularly pronounced at c. 300 mm total length (L_T) and therefore at the size when this species shifts habitat. When the three species co‐occurred over the same reefs, their dietary compositions were significantly different, with that of B. frenchii being by far the most discrete, reflecting a far greater contribution by sedentary taxa. Thus, the diet of B. frenchii was distinguished from those of the other two species in containing substantial volumes of bivalve and gastropod molluscs and echinoid echinoderms and essentially no teleosts. Although the diets of G. hebraicum and particularly E. armatus were dominated by teleosts, and especially for larger individuals, the former species ingested greater volumes of cephalopods and small crustaceans. The pointed jaws of B. frenchii, with their forwardly directed and interlocking anterior incisors, are ideally adapted for biting and retaining their invertebrate prey, which are attached to or reside within reef crevices. In contrast, the mouths of G. hebraicum and E. armatus are broader and rounder and contain numerous small, slender and inward‐pointing teeth. These teeth, in conjunction with prominent backward‐curved canines in E. armatus, facilitate the capture and retention of fish prey. Observations in situ indicate that G. hebraicum is a suction feeder, while E. armatus is predominantly a ram feeder. Although reef environments on the west and south coasts differ, the diet of B. frenchii on these coasts differed only slightly. Interspecific differences in diet, combined with size‐related changes in dietary compositions and the occupation of different habitats by juvenile and adult G. hebraicum, reduce the potential for competition for food resources among and within B. frenchii, G. hebraicum and E. armatus and thus helps facilitate the coexistence of these species which historically have been abundant over reefs in south‐western Australia.