A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators

Accurate identification of species that are consumed by vertebrate predators is necessary for understanding marine food webs. Morphological methods for identifying prey components after consumption often fail to make accurate identifications of invertebrates because prey morphology becomes damaged during capture, ingestion and digestion. Another disadvantage of morphological methods for prey identification is that they often involve sampling procedures that are disruptive for the predator, such as stomach flushing or lethal collection. We have developed a DNA-based method for identifying species of krill (Crustacea: Malacostraca), an enormously abundant group of invertebrates that are directly consumed by many groups of marine vertebrates. The DNA-based approach allows identification of krill species present in samples of vertebrate stomach contents, vomit, and, more importantly, faeces. Utilizing samples of faeces from vertebrate predators minimizes the impact of dietary studies on the subject animals. We demonstrate our method first on samples of Adelie penguin (Pygoscelis adeliae) stomach contents, where DNA-based species identification can be confirmed by prey morphology. We then apply the method to faeces of Adelie penguins and to faeces of the endangered pygmy blue whale (Balaenoptera musculus brevicauda). In each of these cases, krill species consumed by the predators could be identified from their DNA present in faeces or stomach contents.     

The effects of prey demography on humpback whale (Megaptera novaeangliae) abundance around Anvers Island, Antarctica

Baleen whales and Adelie penguins in the near-shore waters around the Antarctic Peninsula forage principally on Antarctic krill. Given the spatial overlap in the distribution of these krill predators (particularly humpback whales) and their dependence on krill, the goals of this paper are to determine if the inter-annual community structure and relative abundance of baleen whales around Anvers Island is related to krill demography and abundance, and if the potential exists for inter-specific interactions between Adelie penguins and baleen. We use whale sightings and prey data from both net tows and Adelie penguin stomach samples to correlate the abundance of humpback whales with krill demography and abundance from 1993 to 2001. We find significant relationships between whale abundance and the size–frequency distribution of krill targeted by Adelie penguins, as well as the foraging success of Adelie penguins. These findings suggest both krill predators share common prey preferences in the upper portions of the water column around Anvers Island. These findings highlight the need for better knowledge of baleen whale foraging ecology and inter-specific interactions with penguins, as sea ice and krill populations around the Antarctic Peninsula are affected by rapid changes in climate.     

The complete mitochondrial genome sequence of the world's largest fish,the whale shark (Rhincodon typus), and its comparison with those of related shark species

The whale shark (Rhincodon typus) is the largest extant species of fish, belonging to the order Orectolobiformes. It is listed as a “vulnerable” species on the International Union for Conservation of Nature (IUCN)'s Red List of Threatened Species, which makes it an important species for conservation efforts. We report here the first complete sequence of the mitochondrial genome (mitogenome) of the whale shark obtained by next-generation sequencing methods. The assembled mitogenome is a 16,875 bp circle, comprising of 13 protein-coding genes, two rRNA genes, 22 tRNA genes and a control region. We also performed comparative analysis of the whale shark mitogenome to the available mitogenome sequences of 17 other shark species, four from the order Orectolobiformes, five from Lamniformes and eight from Carcharhiniformes. The nucleotide composition, number and arrangement of the genes in whale shark mitogenome are the same as found in the mitogenomes of the other members of the order Orectolobiformes and its closest orders Lamniformes and Carcharhiniformes, although the whale shark mitogenome had a slightly longer control region. The availability of mitogenome sequence of whale shark will aid studies of molecular systematics, biogeography, genetic differentiation, and conservation genetics in this species.     

Feeding habits of the whale shark (<Emphasis Type="Italic">Rhincodon typus</Emphasis>) inferred by fatty acid profiles in the northern Mexican Caribbean

Whale shark (Rhincodon typus, Smith, 1828) is an endangered species with anthropogenic pressures due to increasing demand of encounter tourism activities. Research efforts to identify management and conservation strategies for this species are needed. The Northern Mexican Caribbean is one of the most important feeding aggregation sites of whale sharks worldwide. In this study, Mexican Caribbean whale shark feeding habits are assessed by means of fatty acid (FA) signature analysis, a biochemical non-destructive technique widely applied in trophic ecology studies. Sub-dermal tissue biopsies of 68 whale sharks and samples of their potential prey (zooplankton) were collected during 2010 and 2011 in two areas with high R. typus abundance. Zooplankton samples (n?=?17) were divided in two categories: mixed zooplankton (several groups of zooplankton) and fish eggs (> 95% of sample components were fish eggs). FA profiles of whale shark tissue sampled between years showed significant variability; while there was no intraspecific differences in FA signature related to sex, size and location. FA profiles of whale sharks and their potential prey were dominated by saturated fatty acids (SFA). R. typus FA signature was significantly different from that of mixed zooplankton; on the other hand, whale shark and fish egg FA profiles formed groups with overlapping values and registered high levels of oleic acid. PUFA average ω3/ ω6 ratio on whale shark FA profiles for both years was below 1. Arachidonic acid (ARA) percentage was higher in whale shark biopsies (13.2% in 2010, 6.8% in 2011) compared to values observed in fish eggs (2.0%) and mixed zooplankton (1.4%). Similarity between FA profiles of whale sharks and fish eggs, low levels of bacterial FA found in R. typus biopsies, as well as whale shark feeding behavior observations in the study area, suggest that R. typus is feeding mainly on surface zooplankton in Mexican Caribbean; however, elevated ARA percentages in whale shark samples may indicate that this species has complementary feeding sources, such as demersal zooplankton, which has been reported in other aggregation sites. Results obtained contribute to the knowledge of the whale shark trophic ecology in the area, but are inconclusive. Further studies are recommended to evaluate whale shark FA profiles from different tissues (muscle or blood); also, broader information is needed about zooplankton FA signature in the study area.     

Future recovery of baleen whales is imperiled by climate change

Historical harvesting pushed many whale species to the brink of extinction. Although most Southern Hemisphere populations are slowly recovering, the influence of future climate change on their recovery remains unknown. We investigate the impacts of two anthropogenic pressures—historical commercial whaling and future climate change—on populations of baleen whales (blue, fin, humpback, Antarctic minke, southern right) and their prey (krill and copepods) in the Southern Ocean. We use a climate–biological coupled “Model of Intermediate Complexity for Ecosystem Assessments” (MICE) that links krill and whale population dynamics with climate change drivers, including changes in ocean temperature, primary productivity and sea ice. Models predict negative future impacts of climate change on krill and all whale species, although the magnitude of impacts on whales differs among populations. Despite initial recovery from historical whaling, models predict concerning declines under climate change, even local extinctions by 2100, for Pacific populations of blue, fin and southern right whales, and Atlantic/Indian fin and humpback whales. Predicted declines were a consequence of reduced prey (copepods/krill) from warming and increasing interspecific competition between whale species. We model whale population recovery under an alternative scenario whereby whales adapt their migratory patterns to accommodate changing sea ice in the Antarctic and a shifting prey base. Plasticity in range size and migration was predicted to improve recovery for ice‐associated blue and minke whales. Our study highlights the need for ongoing protection to help depleted whale populations recover, as well as local management to ensure the krill prey base remains viable, but this may have limited success without immediate action to reduce emissions.     

A review of the biology and ecology of the whale shark

The information available on the biology and ecology of the whale shark is reviewed, and is updated from material published since 1986. Research work carried out on the seasonal aggregation of whale sharks at the Ningaloo Reef in Western Australia is summarized. Future research studies on whale sharks in the Ningaloo Marine Park are discussed in the context of management of sustainable whale shark interaction tourism.     

Dynamics of Whale Shark Occurrence at Their Fringe Oceanic Habitat

Studies have shown that the whale shark (Rhincodon typus), a vulnerable large filter feeder, seasonally aggregates at highly productive coastal sites and that individuals can perform large, trans-boundary migrations to reach these locations. Yet, the whereabouts of the whale shark when absent from these sites and the potential oceanographic and biological drivers involved in shaping their present and future habitat use, including that located at the fringes of their suitable oceanic habitat, are largely unknown. We analysed a 16-year (1998–2013) observer dataset from the pole-and-line tuna fishery across the Azores (mid-North Atlantic) and used GAM models to investigate the spatial and temporal patterns of whale shark occurrence in relation to oceanographic features. Across this period, the whale shark became a regular summer visitor to the archipelago after a sharp increase in sighting frequency seen in 2008. We found that SST helps predicting their occurrence in the region associated to the position of the seasonal 22°C isotherm, showing that the Azores are at a thermal boundary for this species and providing an explanation for the post 2007 increase. Within the region, whale shark detections were also higher in areas of increased bathymetric slope and closer to the seamounts, coinciding with higher chl-a biomass, a behaviour most probably associated to increased feeding opportunities. They also showed a tendency to be clustered around the southernmost island of Santa Maria. This study shows that the region integrates the oceanic habitat of adult whale shark and suggests that an increase in its relative importance for the Atlantic population might be expected in face of climate change.     

1H-NMR comparative study of the active site in shark (Galeorhinus japonicus), horse, and sperm whale deoxy myoglobins.

1H-NMR spectra of deoxy myoglobins (Mbs) from shark (Galeorhinus japonicus), horse, and sperm whale have been studied to gain insights into their active site structure. It has been demonstrated for the first time that nuclear Overhauser effect (NOE) can be observed between heme peripheral side-chain proton resonances of these paramagnetic complexes. Val-E11 methyl and His-F8 C delta H proton resonances of these Mbs were also assigned from the characteristic shift and line width. The hyperfine shift of the former resonance was used to calculate the magnetic anisotropy of the protein. The shift analysis of the latter resonance, together with the previously assigned His-F8 N delta H proton resonance, revealed that the strain on the Fe-N epsilon bond is in the order horse Mb approximately whale Mb < shark Mb and that the hydrogen bond strength of the His-F8 N delta H proton to the main-chain carbonyl oxygen in the preceding turn of the F helix is in the order shark Mb < horse Mb < whale Mb. Weaker Feporphyrin interaction in shark Mb was manifested in a smaller shift of the heme methyl proton resonance and appears to result from distortion of the coordination geometry in this Mb. Larger strain on the Fe-N epsilon bond in shark Mb should be to some extent attributed to its lowered O2 affinity (P50 = 1.1 mmHg at 20 degrees C), compared to whale and horse Mbs.     

Multi-Year Impacts of Ecotourism on Whale Shark (Rhincodon typus) Visitation at Ningaloo Reef,Western Australia

In-water viewing of sharks by tourists has become a popular and lucrative industry. There is some concern that interactions with tourists with ecotourism operations might harm sharks through disruption of behaviours. Here, we analysed five years of whale shark (Rhincodon typus) encounter data by an ecotourism industry at Ningaloo Reef, Western Australia, to assess the impact of ecotourism interactions on shark visitation, within the context of the biological and physical oceanography of the region. Our data base consisted of 2823 encounter records for 951 individual whale sharks collected by ecotourism operators between 2007 and 2011. We found that total encounters per whale shark and encounters per boat trip increased through time. On average, whale sharks re-encountered in subsequent years were encountered earlier, stayed longer and tended to be encountered more often within a season than sharks that were only encountered in a single year. Sequential comparisons between years did not show any patterns consistent with disturbance and the rate of departure of whale sharks from the aggregation was negatively correlated to the number of operator trips. Overall, our analysis of this multi-year data base found no evidence that interactions with tourists affected the likelihood of whale shark re-encounters and that instead, physical and biological environmental factors had a far greater influence on whale shark visitation rates. Our approach provides a template for assessing the effects of ecotourism interactions and environmental factors on the visitation patterns of marine megafauna over multiple years.     

Donsol: an important reproductive habitat for the world's largest fish Rhincodon typus?

Little is known about the reproductive ecology of the whale shark Rhincodon typus. On 15 March 2020, a free-swimming neonate whale shark was found in the shallow, coastal waters of Donsol, Philippines. The total length of the male shark was 60 cm, falling within the species known size-at-birth. This is the third occurrence of neonatal whale sharks reported in the area, and coupled with the occurrence of juveniles and adults, and anecdotal mating and precopulatory behaviour reported herein, the importance of the site for this endangered species is highlighted.     

Oceanographic and atmospheric phenomena influence the abundance of whale sharks at Ningaloo Reef, Western Australia

Seasonal observations of whale shark abundance recorded by ecotourist operators at Ningaloo Reef, Western Australia from 1999 to 2004 were compared with weekly regional and global oceanographic and atmospheric variables, including average sea surface temperatures, along-shelf wind shear, sea level and the Southern Oscillation Index (SOI). Estimates of these physical variables were derived from either ground-based data or from remote sensing instruments. A generalised linear mixed-effects modelling (GLMM) approach with random sampling and model simulation was used to determine the relationships between the number of whale sharks and all model variants of the environmental parameters, using information-theoretic weights of evidence to rank models. SOI and wind shear had the most support for explaining the deviance in weekly whale shark abundance at Ningaloo Reef during a season. The SOI and wind shear variables positively influenced whale shark abundance such that more sharks were sighted when the Southern Oscillation was stronger and along-shelf winds were increasingly prevalent. This may reflect changes in the strength of oceanographic processes such as the Leeuwin Current (in response to the Southern Oscillation) and wind/current driven upwelling which may affect the abundance of whale sharks transported to the region and/or the availability of their prey by driving productivity changes.     

A surplus no more? Variation in krill availability impacts reproductive rates of Antarctic baleen whales

The krill surplus hypothesis of unlimited prey resources available for Antarctic predators due to commercial whaling in the 20th century has remained largely untested since the 1970s. Rapid warming of the Western Antarctic Peninsula (WAP) over the past 50 years has resulted in decreased seasonal ice cover and a reduction of krill. The latter is being exacerbated by a commercial krill fishery in the region. Despite this, humpback whale populations have increased but may be at a threshold for growth based on these human-induced changes. Understanding how climate-mediated variation in prey availability influences humpback whale population dynamics is critical for focused management and conservation actions. Using an 8-year dataset (2013–2020), we show that inter-annual humpback whale pregnancy rates, as determined from skin-blubber biopsy samples (n = 616), are positively correlated with krill availability and fluctuations in ice cover in the previous year. Pregnancy rates showed significant inter-annual variability, between 29% and 86%. Our results indicate that krill availability is in fact limiting and affecting reproductive rates, in contrast to the krill surplus hypothesis. This suggests that this population of humpback whales may be at a threshold for population growth due to prey limitations. As a result, continued warming and increased fishing along the WAP, which continue to reduce krill stocks, will likely impact this humpback whale population and other krill predators in the region. Humpback whales are sentinel species of ecosystem health, and changes in pregnancy rates can provide quantifiable signals of the impact of environmental change at the population level. Our findings must be considered paramount in developing new and more restrictive conservation and management plans for the Antarctic marine ecosystem and minimizing the negative impacts of human activities in the region.     

New insights into whale shark <Emphasis Type="Italic">Rhincodon typus</Emphasis> diet in Brazil: an observation of ram filter-feeding on crab larvae and analysis of stomach contents from the first stranding in Bahia state

We describe the first record of a whale shark, Rhincodon typus, feeding in Brazilian coastal waters, and the first stranding record in the state of Bahia, Northeast Brazil. In April 2008, an individual of R. typus was observed surface feeding on Dromiidae crab larvae in the continental shelf off the coast of Bahia, near a gas platform. Other fishes were observed foraging in association with the whale shark. We also document the first stranding of R. typus on the coast of Bahia in October 2013. Biometric data confirmed that the stranded whale shark was a juvenile. Stomach content analysis revealed the ingestion of Geryonidae crab larvae. Plastic debris were also found in the gastric lumen of the stranded juvenile whale shark, and we speculate that it could have been a contributing factor to the stranding, and subsequent death of the whale shark. Crab larvae were observed in both of our records and likely to consist as relevant prey items for R. typus in Brazilian continental shelf. Our study provided a contribution on the diet and feeding behaviour of whale sharks in tropical oligotrophic waters and highlights the risks of marine pollution for the species conservation.     

The Biogeochemical Role of Baleen Whales and Krill in Southern Ocean Nutrient Cycling

The availability of micronutrients is a key factor that affects primary productivity in High Nutrient Low Chlorophyll (HNLC) regions of the Southern Ocean. Nutrient supply is governed by a range of physical, chemical and biological processes, and there are significant feedbacks within the ecosystem. It has been suggested that baleen whales form a crucial part of biogeochemical cycling processes through the consumption of nutrient-rich krill and subsequent defecation, but data on their contribution are scarce. We analysed the concentration of iron, cadmium, manganese, cobalt, copper, zinc, phosphorus and carbon in baleen whale faeces and muscle, and krill tissue using inductively coupled plasma mass spectrometry. Metal concentrations in krill tissue were between 20 thousand and 4.8 million times higher than typical Southern Ocean HNLC seawater concentrations, while whale faecal matter was between 276 thousand and 10 million times higher. These findings suggest that krill act as a mechanism for concentrating and retaining elements in the surface layer, which are subsequently released back into the ocean, once eaten by whales, through defecation. Trace metal to carbon ratios were also higher in whale faeces compared to whale muscle indicating that whales are concentrating carbon and actively defecating trace elements. Consequently, recovery of the great whales may facilitate the recycling of nutrients via defecation, which may affect productivity in HNLC areas.     

Stable isotope analysis and fin whale subpopulation structure in the eastern North Atlantic

The North Atlantic fin whale was subject to heavy exploitation in the past and, despite partial recovery, it is still considered endangered. Recent research has questioned its currently accepted subpopulation structure and migratory movements, challenging management and conservation efforts. Here we contribute to this discussion by presenting results of stable isotope analysis of fin whale bones and krill samples collected from fin whale stomachs from two exploited areas, west Iceland and northwest Spain, and comparing these results with North Atlantic isoscapes. In krill, δ¹⁵N values were highly variable and no significant differences in δ¹⁵N and δ¹³C between areas emerged. δ¹⁵N and δ¹³C values in bone were higher than in krill, due to trophic enrichment, and were not significantly different between areas. Both krill and bone results were slightly inconsistent with the local isoscapes, maybe due to seasonal variations in local productivity and in krill diet and, in the case of bone, to its capability to integrate long‐term isotopic values, derived from food consumed in distant areas. Conversely, δ¹⁸O values, which reflect the basal signal of sea water, were consistent with isoscapes and significantly higher in whales from northwestern Spain, possibly indicating migration to breeding grounds located at lower latitudes.     

一头遭鲨鱼袭击和误捕的小须鲸幼仔

A minke whale was by-caught by fishermen in a drift gill net off Shidao, Weihai, Shandong Province on June 15, 2007. The whale, which had been attacked by a shark, was a male with body length 2.43 m, and was suspected to have died soon after the birth. The small size of the whale suggests that a breeding ground for minke whales might exist in the Chinese coastal waters. Evidence of shark attack on this young whale was apparent: half of the fluke was lost and the belly was bitten as well; injuries were not as severe on the caudal peduncle. It was not possible to determine if the shark-related injuries observed occurred prior to the whale being by-caught or were post-mortem. Some conservation measures were proposed in order to better protect the cetaceans in waters off China.     

The Seasonal Aggregation of Whale Sharks at Ningaloo Reef, Western Australia: Currents, Migrations and the El Niño/ Southern Oscillation

Whale sharks, Rhincodon typus, seasonally aggregate in coastal waters off Ningaloo Reef, Western Australia. We review the oceanographic setting of the region and present evidence that such aggregations form as a result of migratory behavior associated with climatic and oceanographic processes. We utilise records of whale shark abundance collected at Ningaloo Reef from dedicated searches by boat and aircraft and from log sheets recorded by the tourism industry. Measures of whale shark abundance derived from log sheet data sets were moderately correlated with the Southern Oscillation Index and weakly correlated with coastal sea level, an index of the strength of the Leeuwin Current, and sea surface temperature over the period 1993 to 1998. Abundances of whale sharks derived from boat searches from 1983 to 1992 were also correlated with fluctuations in the Southern Oscillation Index, except during a three year period from 1988 to 1990. We conclude that, at least in some years, there appears to be a link between the abundance of aggregating whale sharks and the physical and biological oceanography of the region, with greater whale shark numbers in La Niña years. The lack of correlation in other years may be due to a combination of uneven quality of data and/or aggregations occurring in response to a complex interaction between the physical and biological oceanography of the region.     

Effects of species biology on the historical demography of sharks and their implications for likely consequences of contemporary climate change

Climate variation is an important factor shaping the demographic histories of many marine species, though impacts likely differ depending on species life history, habitat preferences and ecology. Investigating how species responded to historic climate fluctuations may provide critical insights into a species’ response to current climate change. Despite their ecological diversity, shark species share many similar life history characteristics and may be especially vulnerable to anthropogenic and climate impacts. We compared patterns of genetic variability, mismatch distributions and demographic reconstructions from coalescence approaches among temperate and tropical shark species with differing ecological characteristics, to investigate the effect of the past glaciation cycles on population abundance. Genetic diversity at two mitochondrial DNA regions (ND2 and control region) was assayed in four North Pacific species, Pacific spiny dogfish, Pacific sleeper sharks, salmon shark, and bluntnose sixgill shark. In addition, control region sequences acquired from GenBank for five shark species [tope shark (California/Australia), white shark (California), blacktip shark (eastern and western Gulf of Mexico), lemon shark (Bahamas), and whale shark] were analyzed. General patterns in genetic diversity, mismatch analyses and Bayesian skyline plots supported our hypothesis that species biology affected the impact of climate variation on demographic history. Consequently, our results suggest that effects of contemporary climate change on sharks may be to some degree predictable from species biology, distribution, habitat and the impact of past climate events.     

Seasonal trends in whale shark Rhincodon typus sightings in an established tourism site in the Gulf of California,Mexico

The number of individual whale shark Rhincodon typus sightings registered October 2015–March 2018 in Bahia de La Paz, Mexico, ranged from 73 to 129 animals per season (total 1662), with the majority of them identified as males. Density plot maps showed high correlations in sightings between sample seasons and revealed potential hotspot areas. Our study provides an essential baseline of information for the management of whale shark conservation and the associated touristic activities in the region.     

Global climate drives southern right whale (Eubalaena australis) population dynamics

Sea surface temperature (SST) time-series from the southwest Atlantic and the El Ni?o 4 region in the western Pacific were compared to an index of annual calving success of the southern right whale (Eubalaena australis) breeding in Argentina. There was a strong relationship between right whale calving output and SST anomalies at South Georgia in the autumn of the previous year and also with mean El Ni?o 4 SST anomalies delayed by 6 years. These results extend similar observations from other krill predators and show clear linkages between global climate signals and the biological processes affecting whale population dynamics.