Matthew J. McHugh

Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis).

Many sharks and skates are particularly vulnerable to overfishing because of their large size, slow growth, late maturity and low fecundity. In Europe dramatic population declines have taken place in common skate (Dipturus batis L.), one of the largest demersal fish in regional shelf seas, leading to extirpations from substantial parts of its former range. Here we report the discovery of cryptic species in common skate collected from the northeast Atlantic continental shelf. Data from nuclear microsatellite markers indicated two clearly distinct clades and phylogenetic analysis of mitochondrial DNA sequences demonstrated monophyly of each one of them. Capture locations showed evidence of strong spatial segregation, with one taxon occurring mainly in waters off the southern British Isles and around Rockall, while the other was restricted to more northerly shelf waters. These apparently cryptic species showed overlapping substrate and depth preferences, but distributional limits were closely related to temperature gradients, potentially indicating thermal limits to their distributions. This discovery of hidden diversity within a large, critically endangered marine vertebrate demonstrates how marine biodiversity can be underestimated, even in such a relatively well-studied and heavily exploited region.

First Analysis of Multiple Paternity in an Oviparous Shark, the Small-Spotted Catshark (Scyliorhinus canicula L.)

Multiple paternity (MP) has been demonstrated in a variety of sharks, although its prevalence and the number of sires per litter vary considerably among species. To date, such analyses have focused on viviparous species that possess only part of the wide spectrum of reproductive strategies developed in elasmobranchs. We analyzed MP in an oviparous species, the small-spotted catshark (Scyliorhinus canicula). In total, 150 neonates originating from 13 different mothers were genotyped using 12 microsatellite loci. MP was commonplace, with progeny from 92% of females sired by multiple males. This result is consistent with the reproductive biology of the species, particularly its protracted breeding season and potential for long-term sperm storage. The significance of these findings is discussed in light of small-spotted catshark behavior, which suggests that the cost of avoiding mating attempts initiated by males may be high and is therefore supportive of convenience polyandry as an explanation for MP. Eggs were followed from the time they were laid to when they hatched, offering a rare opportunity to investigate juvenile development in more detail.

Scaling laws of ambush predator 'waiting' behaviour are tuned to a common ecology.

The decisions animals make about how long to wait between activities can determine the success of diverse behaviours such as foraging, group formation or risk avoidance. Remarkably, for diverse animal species, including humans, spontaneous patterns of waiting times show random ‘burstiness’ that appears scale-invariant across a broad set of scales. However, a general theory linking this phenomenon across the animal kingdom currently lacks an ecological basis. Here, we demonstrate from tracking the activities of 15 sympatric predator species (cephalopods, sharks, skates and teleosts) under natural and controlled conditions that bursty waiting times are an intrinsic spontaneous behaviour well approximated by heavy-tailed (power-law) models over data ranges up to four orders of magnitude. Scaling exponents quantifying ratios of frequent short to rare very long waits are species-specific, being determined by traits such as foraging mode (active versus ambush predation), body size and prey preference. A stochastic–deterministic decision model reproduced the empirical waiting time scaling and species-specific exponents, indicating that apparently complex scaling can emerge from simple decisions. Results indicate temporal power-law scaling is a behavioural ‘rule of thumb’ that is tuned to species’ ecological traits, implying a common pattern may have naturally evolved that optimizes move–wait decisions in less predictable natural environments.

Contrasting demographic histories of European and North American sea lamprey (Petromyzon marinus) populations inferred from mitochondrial DNA sequence variation

Populations of anadromous sea lamprey (Petromyzon marinus) have been found to be largely genetically homogeneous across western Europe, and across the eastern seaboard of North America. However, comparatively little is known of the relationship between the European and North American populations. We quantified the extent of population structuring present over a transatlantic scale using mitochondrial DNA sequences. We found clear segregation of the populations on either side of the Atlantic, and considerable genetic homogeneity within Europe over a spatial scale of over 2000 km. The North American populations contained larger genetic diversity than those from Europe, and coalescent analyses showed a corresponding greater overall effective population size. Employing calibration points based on a dated phylogeny of the Petromyzontiformes, our analyses indicated that the North American population has been increasing in effective size since establishment ~500 000 years ago, while the total European population has only undergone population expansion only within the last 125 000 years. This evidence is consistent with a colonisation of Europe from an older North American population, and with the European population persisting through the last glaciation within regional refugia.

A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe

Elasmobranchs represent important components of marine ecosystems, but they can be vulnerable to overexploitation. This has driven investigations into the population genetic structure of large-bodied pelagic sharks, but relatively little is known of population structure in smaller demersal taxa, which are perhaps more representative of the biodiversity of the group. This study explores spatial population genetic structure of the small-spotted catshark (Scyliorhinus canicula), across European seas. The results show significant genetic differences among most of the Mediterranean sample collections, but no significant structure among Atlantic shelf areas. The data suggest the Mediterranean populations are likely to have persisted in a stable and structured environment during Pleistocene sea-level changes. Conversely, the Northeast Atlantic populations would have experienced major changes in habitat availability during glacial cycles, driving patterns of population reduction and expansion. The data also provide evidence of male-biased dispersal and female philopatry over large spatial scales, implying complex sex-determined differences in the behaviour of elasmobranchs. On the basis of this evidence, we suggest that patterns of connectivity are determined by trends of past habitat stability that provides opportunity for local adaptation in species exhibiting philopatric behaviour, implying that resilience of populations to fisheries and other stressors may differ across the range of species.

Characterisation of polymorphic microsatellite loci in the small-spotted catshark (Scyliorhinus canicula L.)

Microsatellite markers were characterised in the small-spotted catshark (Scyliorhinus canicula) from unpublished sequences generated from expressed sequence tags and bacterial artificial chromosomes. All seventeen of the loci screened were found to be polymorphic within the population of catsharks tested. The number of alleles identified varied between two and twelve per locus, and the expected heterozygosity ranged from 0.40 to 0.83. Evidence of null alleles was detected in two loci, while one locus showed significant deviation from expectations of Hardy–Weinberg equilibrium. There was no evidence of significant linkage between any loci. Cross-amplification was attempted in six other species of elasmobranch and success generally followed levels of taxonomic relatedness. These markers should be a powerful tool for population genetic and molecular studies of the small-spotted catshark, and may prove useful in other shark species.

Characterisation of polymorphic microsatellite markers for skates (Elasmobranchii: Rajidae) from expressed sequence tags

Simple sequence repeat markers (SSRs, microsatellites) were characterised for skates (Elasmobranchii: Rajidae) from published expressed sequence tags (ESTs) of Leucoraja erinacea. These were tested in four European species (Raja clavata, Raja montagui, Dipturus batis, and Leucoraja naevus). Thirteen of the fourteen amplified loci were polymorphic in at least one species. Polymorphic loci possessed on average 4.5–5.9 alleles per species, and expected heterozygosity ranged from 0.05 to 0.88. Possible null alleles were detected at three loci, while one locus showed significant deviation from Hardy–Weinberg Equilibrium proportions. Three locus-pairs exhibited significant linkage disequilibrium in one or more species. This marker set will be valuable for population genetic analyses of the focal taxa, and may prove useful for studies of other skate species.

Choosing anterior-gear modifications to reduce the global environmental impacts of penaeid trawls

Globally, penaeid-trawl fisheries are faced with three broad sustainability issues: (1) large bycatches; (2) acute benthic-habitat impacts; and (3) high energy consumption. Most resolution efforts have focused on i above, and via bycatch reduction devices (BRDs) installed in the posterior trawl (codend), which typically reduce total bycatches by 30–70%, but are poorly adopted owing to few perceived benefits by fishers. While mandated BRDs will remain a feature of selective penaeid trawling, solutions to habitat impacts and high energy consumption require changes to the anterior trawl, including the spreading mechanisms (e.g. otter boards, beams and sleds), ground gears, and net designs. Further, because such components ultimately determine which organisms enter the codend, it should be feasible to structure anterior-trawl modifications to address all three sustainability issues, including improving selection. We sought to review the feasibility of such an approach here, and located fifty-eight relevant articles: of which 45, 11 and 23 directly or indirectly focused on reducing bycatch, habitat impacts and energy consumption, respectively. Considering these articles, we propose a protocol for holistically improving the environmental efficiency of penaeid trawling involving: (1) selecting the most appropriate multi-net configuration; (2) reducing otter-board angle of attack to ~20°; (3) minimising twine area; and (4) optimising horizontal-trawl opening. Compared to conventional configurations, choosing alternatives within the above protocol could reduce total unwanted bycatches and habitat contact by >70%, while concomitantly lowering drag/fuel costs by >20%. The latter outcome might improve selective penaeid-trawl adoption among global fishing fleets.

A ‘Simple Anterior Fish Excluder’ (SAFE) for Mitigating Penaeid-Trawl Bycatch

Various plastic strips and sheets (termed ‘simple anterior fish excluders’−SAFEs) were positioned across the openings of penaeid trawls in attempts at reducing the unwanted bycatches of small teleosts. Initially, three SAFEs (a single wire without, and with small and large plastic panels) were compared against a control (no SAFE) on paired beam trawls. All SAFEs maintained targeted Metapenaeus macleayi catches, while the largest plastic SAFE significantly reduced total bycatch by 51% and the numbers of Pomatomus saltatrix, Mugil cephalus and Herklotsichthys castelnaui by up to 58%. A redesigned SAFE (‘continuous plastic’) was subsequently tested (against a control) on paired otter trawls, significantly reducing total bycatch by 28% and P. saltatrix and H. castelnaui by up to 42%. The continuous-plastic SAFE also significantly reduced M. macleayi catches by ~7%, but this was explained by ~5% less wing-end spread, and could be simply negated through otter-board refinement. Further work is required to refine the tested SAFEs, and to quantify species-specific escape mechanisms. Nevertheless, the SAFE concept might represent an effective approach for improving penaeid-trawl selectivity.