Threshold foraging behaviour of basking sharks on zooplankton: life on an energetic knife-edge?

The minimum threshold foraging response of basking sharks has not been determined despite the widely held view that has been perpetuated in the literature for the past 45 years that this species cannot use low prey densities for net energy gain and so lives on an energetic ''knife-edge''. An early theoretical estimate suggested basking sharks would expend more energy collecting zooplankton at concentrations less than 1.36 g m^-3 than could be obtained from it. This led to the claim that basking sharks will feed at an energetic loss for much of the annual cycle as zooplankton abundance outside summer months is too low for net energy gain to occur. Here I show from theoretical calculations and behavioural studies on individual and group-feeding sharks in the English Channel that basking sharks have a theoretical threshold prey density of between 0.55 and 0.74 g m^-3 and an observed foraging threshold of between 0.48 and 0.70 g m^-3 (mean = 0.62 g m^-3). The close agreement between theoretical and empirical threshold values suggests basking sharks can achieve net energy gain in much lower zooplankton densities than previously thought. The findings imply that this species may not be reliant upon the ''migration–hibernation'' energy conservation strategy it is purported to exhibit when seasonal zooplankton abundance decreases below 1.36 g m^-3.     

Filter-feeding and cruising swimming speeds of basking sharks compared with optimal models: they filter-feed slower than predicted for their size

Movements of six basking sharks (4.0-6.5 m total body length, L(T)) swimming at the surface were tracked and horizontal velocities determined. Sharks were tracked for between 1.8 and 55 min with between 4 and 21 mean speed determinations per shark track. The mean filter-feeding swimming speed was 0.85 m s(-1) (+/-0.05 S.E., n=49 determinations) compared to the non-feeding (cruising) mean speed of 1.08 m s(-1) (+/-0.03 S.E., n=21 determinations). Both absolute (m s(-1)) and specific (L s(-1)) swimming speeds during filter-feeding were significantly lower than when cruise swimming with the mouth closed, indicating basking sharks select speeds approximately 24% lower when engaged in filter-feeding. This reduction in speed during filter-feeding could be a behavioural response to avoid increased drag-induced energy costs associated with feeding at higher speeds. Non-feeding basking sharks (4 m L(T)) cruised at speeds close to, but slightly faster ( approximately 18%) than the optimum speed predicted by the Weihs (1977) [Weihs, D., 1977. Effects of size on the sustained swimming speeds of aquatic organisms. In: Pedley, T.J. (Ed.), Scale Effects in Animal Locomotion. Academic Press, London, pp. 333-338.] optimal cruising speed model. In contrast, filter-feeding basking sharks swam between 29 and 39% slower than the speed predicted by the Weihs and Webb (1983) [Weihs, D., Webb, P.W., 1983. Optimization of locomotion. In: Webb, P.W., Weihs, D. (Eds.), Fish Biomechanics. Praeger, New York, pp. 339-371.] optimal filter-feeding model. This significant under-estimation in observed feeding speed compared to model predictions was most likely accounted for by surface drag effects reducing optimum speeds of tracked sharks, together with inaccurate parameter estimates used in the general model to predict optimal speeds of basking sharks from body size extrapolations.     

Transatlantic migration and deep mid-ocean diving by basking shark

Despite being the second largest fish, basking sharks (Cetorhinus maximus) have been assumed to remain in discrete populations. Their known distribution encompasses temperate continental shelf areas, yet until now there has been no evidence for migration across oceans or between hemispheres. Here we present results on the tracks and behaviour of two basking sharks tagged off the British Isles, one of which released its tag off Newfoundland, Canada. During the shark's transit of the North Atlantic, she travelled a horizontal distance of 9589 km and reached a record depth of 1264 m. This result provides the first evidence for a link between European and American populations and indicates that basking sharks make use of deep-water habitats beyond the shelf edge.     

Encounter success of free-ranging marine predator movements across a dynamic prey landscape

Movements of wide-ranging top predators can now be studied effectively using satellite and archival telemetry. However, the motivations underlying movements remain difficult to determine because trajectories are seldom related to key biological gradients, such as changing prey distributions. Here, we use a dynamic prey landscape of zooplankton biomass in the north-east Atlantic Ocean to examine active habitat selection in the plankton-feeding basking shark Cetorhinus maximus. The relative success of shark searches across this landscape was examined by comparing prey biomass encountered by sharks with encounters by random-walk simulations of 'model' sharks. Movements of transmitter-tagged sharks monitored for 964 days (16754 km estimated minimum distance) were concentrated on the European continental shelf in areas characterized by high seasonal productivity and complex prey distributions. We show movements by adult and sub-adult sharks yielded consistently higher prey encounter rates than 90% of random-walk simulations. Behavioural patterns were consistent with basking sharks using search tactics structured across multiple scales to exploit the richest prey areas available in preferred habitats. Simple behavioural rules based on learned responses to previously encountered prey distributions may explain the high performances. This study highlights how dynamic prey landscapes enable active habitat selection in large predators to be investigated from a trophic perspective, an approach that may inform conservation by identifying critical habitat of vulnerable species.     

Seasonal Variation in the Spatial Distribution of Basking Sharks (Cetorhinus maximus) in the Lower Bay of Fundy,Canada

The local distribution of basking sharks in the Bay of Fundy (BoF) is unknown despite frequent occurrences in the area from May to November. Defining this species’ spatial habitat use is critical for accurately assessing its Special Concern conservation status in Atlantic Canada. We developed maximum entropy distribution models for the lower BoF and the northeast Gulf of Maine (GoM) to describe spatiotemporal variation in habitat use of basking sharks. Under the Maxent framework, we assessed model responses and distribution shifts in relation to known migratory behavior and local prey dynamics. We used 10 years (2002-2011) of basking shark surface sightings from July-October acquired during boat-based surveys in relation to chlorophyll-a concentration, sea surface temperature, bathymetric features, and distance to seafloor contours to assess habitat suitability. Maximum entropy estimations were selected based on AICc criterion and used to predict habitat utilizing three model-fitting routines as well as converted to binary suitable/non-suitable habitat using the maximum sensitivity and specificity threshold. All models predicted habitat better than random (AUC values >0.796). From July-September, a majority of habitat was in the BoF, in waters >100 m deep, and in the Grand Manan Basin. In October, a majority of the habitat shifted southward into the GoM and to areas >200 m deep. Model responses suggest that suitable habitat from July - October is dependent on a mix of distance to the 0, 100, 150, and 200 m contours but in some models on sea surface temperature (July) and chlorophyll-a (August and September). Our results reveal temporally dynamic habitat use of basking sharks within the BoF and GoM. The relative importance of predictor variables suggests that prey dynamics constrained the species distribution in the BoF. Also, suitable habitat shifted minimally from July-September providing opportunities to conserve the species during peak abundance in the region.     

Annual social behaviour of basking sharks associated with coastal front areas

Comparatively little is known about reproductive behaviour in wild sharks as it has proved extremely difficult to study, especially in large pelagic sharks. Here we describe annual courtship-like behaviour in the second-largest fish species, the basking shark (Cetorhinus maximus), from 25 separate episodes observed and tracked during a five-year study period (1995-1999) off south-west England. Social behaviours observed between paired, or three or four, sharks were consistent with courtship behaviours seen in other shark species, namely nose-to-tail following, close following, close flank approach, parallel and echelon swimming. Mature individuals between 5 and 8 m total body length (L(T)) exhibited these behaviours whereas smaller sharks (3-4 m L(T)) did not. Lead individuals were identified as female on a number of occasions and interactions were prolonged; the longest continuous observation of socializing was 1.8 h, although intermittent track data indicates bouts may last for up to 5-6 h. Locations of courtship-like behaviour events were not distributed randomly and were significantly associated with thermal fronts. Our results indicate that putative courtship behaviour occurs between May and July along oceanographic fronts, probably as a consequence of individuals aggregating to forage in rich prey patches before initiating courtship. Thus, locating the richest prey patches along fronts may be important for basking sharks to find mates as well as food in the pelagic ecosystem. As courtship-like behaviours occur annually off south-west England we speculate that this region may represent an annual breeding area for this protected species, but mating itself probably takes place at depth as it was not seen at the surface.     

赣江下游及其支流浮游甲壳动物的群落结构

2009年6月、11月和2010年4月对赣江下游浮游甲壳动物的群落结构和时空变化进行研究.共记录浮游甲壳动物21种,其中枝角类14种、桡足类7种.脆弱象鼻溞Bosmina fatalis、微型裸腹溞Moina micrura和中剑水蚤Mesocyclops sp.为优势种.赣江下游干流浮游甲壳动物的最大平均密度和生物量(11.1ind.·L^-1和0.127mg·L^-1)均出现在6月,最小值(1.59ind.·L^-1和0.01mg·L^-1)均出现在4月.袁河支流的枝角类和桡足类密度在6月(4.97±13.28ind.·L^-1和2.07±4.85ind.·L^-1)和11月(2.07±5.21ind.·L^-1和2.24±5.22ind.·L^-1)高于赣江下游干流和锦江支流.香农-威纳指数(H')和马加利夫指数(d)表明赣江下游及其支流水质为中度污染或重污染.水温和小型浮游植物生物量是影响赣江下游浮游甲壳动物密度时空变化的重要因素.     

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.     

Distribution and reproduction of the southern lantern shark from New Zealand

Distribution, population structure and reproduction are described for the southern lantern shark Etmopterus granulosus at the Chatham Rise, New Zealand. Depth of capture for E. granulosus ranged from 744 to 1420 m, with highest catch rates between 800–1200 m. More than twice as many females as males were captured, and the majority of sharks caught were mature, indicating that there may be segregation according to sex and size class. Only 10 of 492 female sharks captured contained ova in uteri, and none contained embryos. The absence of pregnant females suggests that they move to another area or depth prior to pupping. Size of sharks captured ranged from 20·0 to 78·8 cm total length. Females began to mature at 62 cm total length, and males at 52 cm. There was no evidence of a seasonal reproductive cycle. Ovulation appeared to occur when ova reached a diameter of 40–45 mm. The average number of ova in mature females was 12·7. This information is crucial for assessing the impact of fisheries on E. granulosus populations.     

Lamprey parasitism of sharks and teleosts: high capacity urea excretion in an extant vertebrate relic

We observed 10 sea lampreys (Petromyzon marinus) parasitizing basking sharks (Cetorhinus maximus), the world's second largest fish, in the Bay of Fundy. Due to the high concentrations of urea in the blood and tissues of ureosmotic elasmobranchs, we hypothesized that sea lampreys would have mechanisms to eliminate co-ingested urea while feeding on basking sharks. Post-removal urea excretion rates (J(Urea)) in two lampreys, removed from separate sharks by divers, were initially 450 ( approximately 9000 micromol N kg-1 h-1) and 75 times ( approximately 1500 micromol N kg-1 h-1) greater than basal (non-feeding) rates ( approximately 20 micromol N kg-1 h-1). In contrast, J(Urea) increased by 15-fold after parasitic lampreys were removed from non-ureosmotic rainbow trout (Oncorhynchus mykiss). Since activities of the ornithine urea cycle (OUC) enzymes, carbamoyl phosphate synthetase III (CPSase III) and ornithine carbamoyl transferase (OCT) were relatively low in liver and below detection in intestine and muscle, it is unlikely that the excreted urea arose from de novo urea synthesis. Measurements of arginase activity suggested that hydrolysis of dietary arginine made a minor contribution to J(Urea.). Post-feeding ammonia excretion rates (J(Amm)) were 15- to 25-fold greater than basal rates in lampreys removed from both basking sharks and rainbow trout, suggesting that parasitic lampreys have a high capacity to deaminate amino acids. We conclude that the sea lamprey's ability to penetrate the dermal denticle armor of sharks, to rapidly excrete large volumes of urea and a high capacity to deaminate amino acids, represent adaptations that have contributed to the evolutionary success of these phylogenetically ancient vertebrates.     

Trophic ecology of Squatina guggenheim on the continental shelf off Uruguay and northern Argentina

A total of 1280 (670 females and 610 males) Squatina guggenheim , an angel shark endemic to the south-west Atlantic, was caught during five research cruises (1995, 1997 and 1998) carried out in the Argentine-Uruguayan Common Fishing Zone (AUCFZ) at depths of 3·5–266 m. All angel sharks captured were sexed and measured. Of the 947 examined for stomach contents, 556 (58·7%) contained food and 391 (41·3%) were empty. Numerically, bony fishes were the principal dietary component (89·7%), followed by crustaceans (4·8%) and molluscs (4·4%). The most important prey species were Engraulis anchoita (58·3%), shrimps (4·4%) and Ilex argentinus (2·3%). Male and female diets were not found to differ significantly ( P  > 0·01), however, the diets of different size classes showed significant differences ( P  ≤ 0·01) (group 1, 23–44, group 2, 45–74 and group 3, 75–91 cm L _T). Low rates of cannibalism were observed. The spatial and seasonal variability in the trophodynamics of S. guggenheim is discussed.     

Seasonal differences in routine oxygen consumption rates of the bonnethead shark

Routine oxygen consumption rates of bonnethead sharks, Sphyrna tiburo , increased from 141·3±29·7 mg O₂ kg⁻¹ h⁻¹ during autumn to 218·6±64·2 mg O₂ kg⁻¹ h⁻¹ during spring, and 329·7±38·3 mg O₂ kg⁻¹ h⁻¹ during summer. The rate of routine oxygen consumption increased over the entire seasonal temperature range (20–30° C) at a Q ₁₀=2·34.     

Early growth and juvenile population structure of lemon sharks Negaprion brevirostris in the Atol das Rocas Biological Reserve, off north‐east Brazil

Lemon sharks Negaprion brevirostris were sampled in the Atol das Rocas, a nursery area, on nine occasions from March 1999 to October 2003, during which 157 individuals were tagged and 35 were recaptured. The male : female sex ratio of captured individuals was 1 : 1·12. Mean ±  s . d . growth rates were 24·7 ± 3·4 cm year⁻¹ in total length ( L _T), 20·7 ± 3·2 cm year⁻¹ in fork length, and 19·5 ± 2·7 cm year⁻¹ in precaudal length. There was no significant difference in growth rates between males and females. Mean ±  s . d . increase in mass was 2565 ± 762 g year⁻¹. The von Bertalanffy growth parameters estimated by the Fabens method based on L _T were: k  = 0·077, L _∞ = 399·9 cm and t ₀ = −2·16. Despite the large variation of environmental conditions, particularly of tidal range and currents, and the lack of protective mangrove cover in the nursery area at Atol das Rocas, juvenile lemon sharks grew relatively faster than at other nurseries. Such rapid growth could be a response to abundant food availability or high risk of predation by adults that enter the nursery area.     

Food consumption of vendace Coregonus albula larvae in Lake Lentua, Finland

The daily ration of vendace larvae (mean TL 10·1–12·8 mm) was assessed after a time-intensive field survey in Lake Lentua. Ten larvae were sampled every 2 h throughout the 10-day sampling period and their alimentary tract contents analysed. The gut was cut into four quarters of equal length and each quarter was analysed separately. This procedure enabled the assessment of the proportions of different zooplankton taxa in the diet based on the least degraded first-quarter contents and to reconstruct the entire gut contents. Secondly, the gut passage time of ingested zooplankton was evaluated by comparing the degradation rate of zooplankton in the guts of experimentally fasted larvae to the degradation of zooplankton in the gradient from pharynx to anus among the larvae sampled from the lake. Finally, food consumption was calculated as zooplankton individuals and carbon biomass based on the two variables, gut passage time of constantly feeding larvae and reconstructed gut contents. The daily ration of vendace larvae varied between 14 and 450 zooplankters in the monitored period.     

Stable isotopes of carbon and nitrogen as indicators of diet and trophic structure of the fish community in a shallow hypereutrophic lake

Stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopes were employed to elucidate energy flows and trophic interactions in Lake Apopka, a hypereutrophic lake in central Florida, U.S.A. Isotope compositions of lake biota ranged from −27·1 to −3·0‰ for δ¹³C, and from 3·7 to 13·9‰ for δ¹⁵N. The food web was based primarily on plankton production with diatoms, Microcystis and zooplankton dominating the diet of fish. Carbon isotope evidence showed that pico- and nano-phytoplankton were not a direct carbon source for fish, but were important to zooplankton. δ¹⁵N mass balance estimates indicated that planktivorous fish obtained 48–85% of their diets from zooplankton. The ∼3‰ range of δ¹⁵N in gizzard shad reflected increasing dependence on zooplankton as fish grew whereas the positive relationship between total length and δ¹⁵N of largemouth bass reflected increasing predation on larger planktivorous fish with growth. The broad ranges of δ¹³C (−25·9 to −9·5‰) and δ¹⁵N (5·8 to 14·4‰) of blue tilapia were indicators of diet diversity. Two presumed omnivores (brown bullhead and white catfish) and piscivores (black crappie, largemouth bass and Florida gar) were found to depend on planktivorous fish. However, stable isotope data revealed no trophic links between blue tilapia, an abundant fish in the near-shore area, and piscivores.     

Serendipitous re-sighting of a basking shark Cetorhinus maximus reveals inter-annual connectivity between American and European coastal hotspots

Transatlantic stock mixing in basking sharks Cetorhinus maximus is supported by low genetic diversity in populations throughout the Atlantic Ocean. However, despite significant focus on the species' movements; >1500 individual sharks marked for recapture and >150 individuals equipped with remote tracking tags, only a single record of transatlantic movment has been previously recorded. Within this context, the seredipitous re-sighting of a female basking shark fitted with a satellite transmitter at Malin Head, Ireland 993 days later at Cape Cod, USA is noteworthy.     

Seasonal variability in growth of larval Japanese anchovy Engraulis japonicus driven by fluctuations in sea temperature in the Kii Channel, Japan

Seasonal variability in the growth of larval Japanese anchovy Engraulis japonicus was examined through otolith microstructure analysis based on the samples collected from the northern side (inner area, IA) and the southern side (outer area, OA) of the Kii Channel from April 2006 to March 2007. Growth trajectories (otolith backcalculated mean standard length of 5 day intervals from 5 days after hatch to 24 days) as well as the most recent 5 day mean growth rate of larvae before capture ( G ₅) differed among months. Growth trajectories showed the same pattern as G ₅. In IA, mean ± s.d. G ₅ ranged from 0·31 ± 0·04 mm day⁻¹ (January) to 0·73 ± 0·06 mm day⁻¹ (October). In OA, mean ± s.d. G ₅ ranged from 0·36 ± 0·05 mm day⁻¹ (January) to 0·79 ± 0·11 mm day⁻¹ (August). G ₅ values declined from November to January and then started to increase. In general, the seasonal patterns of growth were similar between IA and OA, and a clear seasonal pattern in growth was identified. When the relationships among larval growth rate, sea temperature, zooplankton density and larval density were examined, growth rate was positively related with sea temperature in both areas and not related with the other factors. The similar pattern in growth observed between IA and OA was probably due to the low spatial variability in sea temperature compared to its seasonal variability.     

Composition, structure and distribution of the ichthyoplankton in a Mediterranean coastal lagoon

The species composition and assemblage structure of the ichthyoplankton from the Mar Menor Lagoon in south‐east Spain are given. The fish larvae were sorted from zooplankton samples collected at 20 stations with a plankton net (50 cm mouth diameter and 500 μm mesh) during 36 surveys between February and December 1997. A total of 39 575 fish larvae representing 14 families, 22 genera and 36 species were identified. Gobiidae was the most dominant family (77·0%) followed by Blenniidae (19·4%) and Atherinidae (1·3%). The most abundant species were Gobius niger and Gobius paganellus , which accounted for 42·7 and 19·3% of the total respectively. These species were followed in order of relative abundance by Pomatoschistus marmoratus (13·9%), Parablennius pilicornis (9·4%), Lipophrys pavo (7·7%), Atherina boyeri (1·3%) and Parablennius tentacularis (1·3%). The high species diversity (2·0–2·8 bits individual⁻¹ for the annual diversity spectra at each sampling station) reflected a diverse assemblage of species. The main commercial species in the lagoon (Sparidae and Mugilidae) were poorly represented among the ichthyoplankton and they probably enter the lagoon on the bottom as recruits. Chlorophyll a concentration in the water column was the main factor explaining the seasonal variation in larval abundance. Spatial distribution of larvae was related to hydrographical circulation patterns in the lagoon and the movement of marine‐spawned larvae through the channels connecting the lagoon with the Mediterranean Sea.     

Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina

The reproductive biology of blacknose sharks Carcharhinus acronotus in the western North Atlantic Ocean was studied by examining specimens collected in the coastal waters of South Carolina. Males begin the maturation process between 875 and 910 mm fork length ( L _F), as indicated by the presence of functional claspers and siphon sacs. The presence of vitellogenic oocytes and developing oviducal glands and uteri indicated that females begin to mature at c . 870 mm L _F. Length at which 50% of the population reached maturity was 896 and 964 mm L _F, equivalent to 4·3 and 4·5 years, for males and females, respectively. Gonado‐somatic indices suggested that spermatogenesis and vitellogenesis began after December. Mating took place during the end of May and the beginning of June. Fertilization occurred during late June and early July, suggesting that female blacknose sharks were capable of sperm storage. Based on the timing of fertilization and occurrence of females carrying near‐term pups in late May and early June, the gestation period for blacknose sharks was c . 11 months. Female blacknose sharks reproduced biennially based on the absence of vitellogenic oocytes in near‐term females and there being no indication of vitellogenesis in postpartum females. Male blacknose sharks were capable of reproducing annually as indicated by turgid genital ducts, which were observed in all mature males collected during late May and early June.     

Use of Photo-Identification and Mark-Recapture Methodology to Assess Basking Shark (Cetorhinus maximus) Populations

Following centuries of exploitation, basking sharks (Cetorhinus maximus) are considered by IUCN as Endangered in the Northeast Atlantic, where they have now been substantially protected for over two decades. However, the present size of this population remains unknown. We investigated the use of photo-identification of individuals’ dorsal fins, combined with mark-recapture methodology, to investigate the size of populations of basking shark within the west coast of Scotland. From a total of 921 encounters photographed between 2004 and 2011, 710 sharks were found to be individually identifiable based on dorsal fin damage and natural features. Of these, only 41 individuals were re-sighted, most commonly both within days of, and close to the site of, the initial encounter. A smaller number were re-sighted after longer periods of up to two years. A comparison of the distinguishing features of individuals on first recording and subsequent re-sighting showed that in almost all cases these features remained little changed, suggesting the low re-sighting rate was not due to a loss of distinguishing features. Because of the low number of re-sighting we were not able to produce reliable estimates for the long-term regional population. However, for one 50 km diameter study area between the islands of Mull, Coll and Tiree, we were able to generate closed-population estimates for 6–9 day periods in 2010 of 985 (95% CI = 494–1683), and in 2011 of 201 (95% CI = 143–340). For the same 2011 period an open-population model generated a similar estimate of 213 (95% CI = 111–317). Otherwise the low rate and temporal patterning of re-sightings support the view that such local basking shark populations are temporary, dynamic groupings of individuals drawn from a much larger regional population than previously supposed. The study demonstrated the feasibility and limitations of photo-identification as a non-invasive technique for identifying individual basking sharks.