Insights on long-term ecosystem changes from stable isotopes in historical squid beaks

Background - Assessing the historical dynamics of key food web components is crucial to understand how climate change impacts the structure of Arctic marine ecosystems. Most retrospective stable isotopic studies to date assessed potential ecosystem shifts in the Arctic using vertebrate top predators and filter-feeding invertebrates as proxies. However, due to long life histories and specific ecologies, ecosystem shifts are not always detectable when using these taxa. Moreover, there are currently no retrospective stable isotopic studies on various other ecological and taxonomic groups of Arctic biota. To test whether climate-driven shifts in marine ecosystems are reflected in the ecology of short-living mesopredators, ontogenetic changes in stable isotope signatures in chitinous hard body structures were analysed in two abundant squids (Gonatus fabricii and Todarodes sagittatus) from the low latitude Arctic and adjacent waters, collected between 1844 and 2023. Results - We detected a temporal increase in diet and habitat-use generalism (= opportunistic choice rather than specialization), trophic position and niche width in G. fabricii from the low latitude Arctic waters. These shifts in trophic ecology matched with the Atlantification of the Arctic ecosystems, which includes increased generalization of food webs and higher primary production, and the influx of boreal species from the North Atlantic as a result of climate change. The Atlantification is especially marked since the late 1990s/early 2000s. The temporal patterns we found in G. fabricii's trophic ecology were largely unreported in previous Arctic retrospective isotopic ecology studies. Accordingly, T. sagittatus that occur nowadays in the high latitude North Atlantic have a more generalist diet than in the XIXth century. Conclusions - Our results suggest that abundant opportunistic mesopredators with short life cycles (such as squids) are good candidates for retrospective ecology studies in the marine ecosystems, and to identify ecosystem shifts driven by climate change. Enhanced generalization of Arctic food webs is reflected in increased diet generalism and niche width in squids, while increased abundance of boreal piscivorous fishes is reflected in squids' increased trophic position. These findings support opportunism and adaptability in squids, which renders them as potential winners of short-term shifts in Arctic ecosystems

Variability in tissue-specific trophic discrimination factors (∆13C and ∆15N) between Antarctic krill Euphausia superba and free-ranging Pygoscelis penguins

For top consumers in marine environments, trophic discrimination factors (∆13C and ∆15N) between food and consumers’ tissues are expected to be similar among related species. However, few studies conducted in the laboratory indicate a large variability among species, which should be potentially higher in free-ranging animals. Here, we test for differences in tissue-specific ∆13C and ∆15N values of two wild penguin species (Chinstrap Pygoscelis antarctica and Gentoo P. papua) breeding in sympatry at Livingston Island, Antarctica. A total of 41 adults and 28 chicks, and food items comprised exclusively by Antarctic krill (Euphausia superba, n = 22) in Chinstraps and almost exclusively in Gentoos, were sampled for stable isotope analyses. Overall, Δ13C values varied between -1.8 and 4.0 ‰ and Δ15N values ranged from 1.2 to 6.1 ‰, and these differed between species, tissues and age-classes. Δ13C in adult penguins differed between species for feather and blood. Species-specific differences in Δ13C and Δ15N were seen in chick nail and muscle, while only Δ13C values differed between species in feathers. Our results show that trophic discrimination factors can differ substantially between closely related species consuming similar prey, especially in Δ13C value. Variation in Δ13C was driven by species, tissue and age-class, while variation in Δ15N was mostly driven by tissue type. Trophic discrimination factors may be associated to physiological and/or stress factors which may fluctuate in the wild, and this was particularly evident on chicks. This study highlights the use of diet-specialised species for the determination of trophic discrimination factors in the wild

Cephalopods habitat and trophic ecology: historical data using snares penguin as biological sampler

In the Southern Ocean and adjacent waters, early stages of cephalopods play an important role in food webs as prey to top predators, but few is known regarding their biology and availability. Snares Penguin, Eudyptes robustus, is a top predator endemic to Snares Islands (New Zealand) that feed on cephalopods. As historical data on diet are rare for this species, Snares Penguins were used as biological samplers to evaluate the cephalopod component of its diet, where habitat and trophic level of cephalopods around the Snares Islands was assessed through stable isotope analysis. Moreover, ontogenic changes of juvenile squid were evaluated. Data collection were carried out during the breeding season 1986–87 and its analysis revealed that penguins fed on three juvenile cephalopod species: two squids (Nototodarus sloanii and Moroteuthopsis ingens) and one octopod (Octopus campbelli). Nototodarus sloanii was the most important species in frequency of occurrence and mass, whereas M. ingens was the most important in number. Juvenile squid species showed similar δ13C values, suggesting both occupied similar habitats on the Snares shelf, whereas juvenile O. campbelli showed lower δ13C values. Moreover, O. campbelli fed on higher trophic level (δ15N) prey relative to squid species. Lower diversity and larger sizes of cephalopods were found when compared with data from 2002. This study shows that Snares Penguin can be a good local biological sampler of juvenile cephalopods during their breeding season, providing both essential biogeographic information of cephalopod diversity and relevant historical information for the conservation of this endemic penguin species

Ontogenetic changes in stable isotope (δ13C and δ15N) values in squid Gonatus fabricii (Cephalopoda) reveal its important ecological role in the Arctic

Gonatus fabricii is the most abundant cephalopod species in Arctic waters, and the only squid that completes its entire life cycle there. In order to understand its ecological role in the Arctic, we conducted stable isotope analyses of beaks from all ontogenetic groups from west and east Greenland waters and the Barents Sea, complemented with morphological data. The values of both delta C-13 and delta N-15 of G. fabricii were not related to sex. Values of delta C-13 showed a small ontogenetic increase, and these values were geographically distinct, with highest levels found in the western part of the study area. Values of delta N-15 showed a dramatic ontogenetic increase (i.e. 10.0 parts per thousand delta N-15; 2.6 trophic levels), from epipelagic juvenile forms to large bathypelagic adults, without significant geographical variation. The observed maximum value of delta N-15 (14.9 parts per thousand) is the highest ever recorded in cephalopod beaks. The estimated trophic level (up to 5.1) compares only to top vertebrate predators in the Arctic: large piscivorous fishes, seals and toothed whales or large benthic scavenging fishes. Thus, G. fabricii is a top invertebrate predator in the Arctic, with the widest isotopic niche observed to date for any species there. Among cephalopods its trophic level is only exceeded by its Antarctic congener, G. antarcticus, and by the Antarctic colossal squid Mesonychoteuthis hamiltoni. Thus, polar squids occupy higher trophic positions than do squids living in warmer regions. Finally, our study shows that G. fabricii descends to bathypelagic layers during ontogenesis, continuously increasing its trophic level by changing prey types and sizes, and avoiding predation pressure

From warm to cold waters: new insights into the habitat and trophic ecology of Southern Ocean squids throughout their life cycle.

Cephalopods play a major role in marine ecosystems, yet very little is known about the dynamics of their habitat use and trophic ecology across the stages of their life cycle, particularly in the Southern Ocean. Here, we used stable isotope analyses of δ13C (a proxy for foraging habitat) and δ15N (a proxy for trophic position) to investigate the habitat use and trophic ecology of 10 squid species, collected from the diet of Antipodean (Diomedea antipodensis antipodensis) and Gibson’s (D. a. gibsoni) albatrosses breeding at Antipodes and Adams Island (South Pacific), respectively. We analyzed isotopes in 2 sections of squid lower beaks, representing 2 stages of the life cycle: the tip of the rostrum (juvenile stage) and the wing (adult stage). Higher δ13C values in early life stages (-20.8 ± 1.7‰) than in adult life stages (-21.6 ± 1.9‰) suggest that Southern Ocean squids tend to move southwards as they grow, with oceanic fronts being an important habitat for these species. Our results also suggest that adults may move southwards with climate change, possibly impacting top predators living on northern islands. Overall, δ15N values revealed an increase in trophic position from early (6.7 ± 2.7‰) to adult life stages (9.0 ± 2.5‰) in all species. Nevertheless, significant differences between δ15N values of the 10 species, in both beak sections, suggest different feeding strategies between species and life stages

Diet and life history reduce interspecific and intraspecific competition among three sympatric Arctic cephalopods

© 2020, The Author(s). Trophic niche and diet comparisons among closely sympatric marine species are important to understand complex food webs, particularly in regions most affected by climate change. Using stable isotope analyses, all ontogenetic stages of three sympatric species of Arctic cephalopods (genus Rossia) were studied to assess inter- and intraspecific competition with niche and diet overlap and partitioning in West Greenland and the Barents Sea. Seven traits related to resource and habitat utilization were identified in Rossia: no trait was shared by all three species. High boreal R. megaptera and Arctic endemic R. moelleri shared three traits with each other, while both R. megaptera and R. moelleri shared only two unique traits each with widespread boreal-Arctic R. palpebrosa. Thus all traits formed fully uncrossing pattern with each species having unique strategy of resource and habitat utilization. Predicted climate changes in the Arctic would have an impact on competition among Rossia with one potential ‘winner’ (R. megaptera in the Barents Sea) but no potential ‘losers’

Mercury biomagnification in a Southern Ocean food web

Biomagnification of mercury (Hg) in the Scotia Sea food web of the Southern Ocean was examined using the stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) as proxies for trophic level and feeding habitat, respectively. Total Hg and stable isotopes were measured in samples of particulate organic matter (POM), zooplankton, squid, myctophid fish, notothenioid fish and seabird tissues collected in two years (austral summers 2007/08 and 2016/17). Overall, there was extensive overlap in δ13C values across taxonomic groups suggesting similarities in habitats, with the exception of the seabirds, which showed some differences, possibly due to the type of tissue analyzed (feathers instead of muscle). δ15N showed increasing enrichment across groups in the order POM to zooplankton to squid to myctophid fish to notothenioid fish to seabirds. There were significant differences in δ13C and δ15N values among species within taxonomic groups, reflecting inter-specific variation in diet. Hg concentrations increased with trophic level, with the lowest values in POM (0.0005 ± 0.0002 μg g-1 dw) and highest values in seabirds (3.88 ± 2.41 μg g-1 in chicks of brown skuas Stercorarius antarcticus). Hg concentrations tended to be lower in 2016/17 than in 2007/08 for mid-trophic level species (squid and fish), but the opposite was found for top predators (i.e. seabirds), which had higher levels in the 2016/17 samples. This may reflect an interannual shift in the Scotia Sea marine food web, caused by the reduced availability of a key prey species, Antarctic krill Euphausia superba. In 2016/17, seabirds would have been forced to feed on higher trophic-level prey, such as myctophids, that have higher Hg burdens. These results suggest that changes in the food web are likely to affect the pathway of mercury to Southern Ocean top predators