Abstract
In the Antarctic Peninsula, during the chick-rearing period Adélie (Pygoscelis adeliae) and gentoo (P. papua) penguins feed primarily on Antarctic krill (Euphausia superba), which is also exploited by the commercial fishery. Krill length and proportion of juvenile krill consumed by these predators that breed at Stranger Point, South Shetland Islands (from 2007/2008 to 2015/2016), and those collected by the krill fishery in the Mar de la Flota/Bransfield Strait (from 2009/2010 to 2015/2016) were compared to evaluate the potential of each data source as an indicator of changes in the size composition and so, in the demographic structure of the krill population. Overall, the mean krill size taken by gentoo penguins was larger than that ingested by Adélie penguins, which consumed higher proportions of juvenile (≤ 35 mm) and one-year-old (≤ 25 mm) krill. Although the krill size caught by the fishery was statistically similar to that taken by both penguin species, there were differences in the frequency distributions of krill size among the three databases. Furthermore, when only adult krill (> 35 mm) was considered, the three sources of krill data showed a similar inter-annual variation in the availability of adult krill cohorts. Our findings suggest that each database analysed here can potentially provide different information (although complementary) about krill size composition. In addition, inter-annual fluctuations in the smaller size classes of krill likely reflect their first year of recruitment and, therefore, may be used as an indicator of shifts in local krill availability.
Similar content being viewed by others
Data availability
The penguin datasets analysed during the current study are available from the corresponding author on reasonable request. The krill fishery dataset that supports the findings of this study is available from the CCAMLR’s Secretariat but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available.
Code availability
Not applicable.
References
Atkinson A, Nicol S, Kawaguchi S, Pakhomov E, Quetin L, Ross R, Hill S, Reiss C, Siegel V, Tarling G (2012) Fitting Euphausia superba into Southern Ocean food-web models: a review of data sources and their limitations. CCAMLR Sci 19:1–26
Atkinson A, Hill SL, Pakhomov EA, Siegel V, Reiss CS, Loeb VJ, Steinberg DK, Schmidt K, Tarling GA, Gerrish L, Sailley SF (2019) Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat Clim Change 9:142–147. https://doi.org/10.1038/s41558-018-0370-z
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bernard KS, Cimino M, Fraser W, Kohut J, Oliver MJ, Patterson-Fraser D, Schofield OME, Statscewich H, Steinberg DK, Winsor P (2017) Factors that affect the nearshore aggregations of Antarctic krill in a biological hotspot. Deep Sea Res I 126:139–147. https://doi.org/10.1016/j.dsr.2017.05.008
CCAMLR (2014) CCAMLR ecosystem monitoring program standard methods. Commission for the Conservation of Antarctic Marine Living Resources. Hobart, Australia. https://www.ccamlr.org/en/document/publications/ccamlr-ecosystem-monitoring-program-standard-methods
CCAMLR Secretariat (2019) Using krill length data from fishery-dependent and fishery independent data sources to measure changes in the Antarctic krill population structure in the Bransfield Strait. WG-EMM-2019/76. https://www.ccamlr.org/en/wg-emm-2019/76
Cimino MA, Moline MA, Fraser WR, Patterson-Fraser DL, Oliver MJ (2016) Climate-driven sympatry may not lead to foraging competition between congeneric top-predators. Sci Rep 6:18820. https://doi.org/10.1038/srep18820
Dimitrijević D, Paiva VH, Ramos JA, Seco J, Ceia FR, Chipev N, Valente T, Barbosa A, Xavier JC (2018) Isotopic niches of sympatric Gentoo and Chinstrap Penguins: evidence of competition for Antarctic krill? Polar Biol 41:1655–1669. https://doi.org/10.1007/s00300-018-2306-5
Fraser W, Hofmann E (2003) A predator’s perspective on causal links between climate change, physical forcing and ecosystem response. Mar Ecol Prog Ser 265:1–15. https://doi.org/10.3354/meps265001
Gales RP (1987) Validation of the stomach flushing technique for obtaining stomach contents of penguins. Ibis 129:225–343. https://doi.org/10.1111/j.1474-919X.1987.tb03177.x
Grilly E, Santos M, Reid K, Silvestro A (2018) Krill spill: an opportunistic approach to collecting penguin diet and krill length data. CCAMLR WG-EMM-18/45. https://www.ccamlr.org/en/wg-emm-18/45
Hill SL, Atkinson A, Darby C, Fielding S, Krafft BA, Godø OR, Skaret G, Trathan PN, Watkins JL (2016) Is current management of the Antarctic krill fishery in the Atlantic sector of the Southern Ocean precautionary? CCAMLR Sci 23:31–51
Hinke JT, Salwicka K, Trivelpiece SG, Watters GM, Trivelpiece WZ (2007) Divergent responses in Pygoscelis penguins reveal a common environmental driver. Oecologia 153:845–855. https://doi.org/10.1007/s00442-007-0781-4
Hinke JT, Cossio AM, Goebel ME, Reiss C, Trivelpiece WZ, Watters GM (2017) Identifying risk: concurrent overlap of the Antarctic krill fishery with krill-dependent predators in the Scotia Sea. PLoS ONE 12(1):e0170132. https://doi.org/10.1371/journal.pone.0170132
Ichii T, Mori Y, Mahapatra K, Trathan PN, Okazari M, Hayashi T, Okuda T (2020) Body length-dependent diel vertical migration of Antarctic krill in relation to food availability and predator avoidance in winter at South Georgia. Mar Ecol Preg Ser 654:53–66. https://doi.org/10.3354/meps13508
Juáres MA (2013) Biología reproductiva y ecología trófica de dos especies simpátricas del género Pygoscelis en las Islas Shetland del Sur, Antártida (Breeding biology and trophic ecology of two sympatric species of the genus Pygoscelis at the South Shetland Islands, Antarctica). PhD thesis, National University of La Plata. http://hdl.handle.net/10915/27166
Juáres MA, Santos M, Negrete J, Mennucci JA, Perchivale PJ, Casaux R, Coria NR (2015) Adélie penguin population changes at Stranger Point: 19 years of monitoring. Antarct Sci 27:455–461. https://doi.org/10.1017/S0954102015000152
Juáres MA, Casaux R, Corbalán A, Blanco G, Pereira GA, Perchivale PJ, Coria NR, Santos MM (2018) Diet of Adélie penguins (Pygoscelis adeliae) at Stranger Point (25 de Mayo/King George Island, Antarctica) over a 13-year period (2003–2015). Polar Biol 41:303–311. https://doi.org/10.1007/s00300-017-2191-3
Krag LA, Herrmann B, Iversen S, Engås A, Nordrum S, Krafft BA (2014) Size selection of Antarctic krill (Euphausia superba) in trawls. PLoS ONE 9:e102168. https://doi.org/10.1371/journal.pone.0102168
Krüger L (2019) Spatio-temporal trends of the krill fisheries in the Western Antarctic Peninsula and South Scotia Arc. Fish Manag Ecol 26:327–333. https://doi.org/10.1111/fme.12363
Lynnes AS, Reid K, Croxall JP (2004) Diet and reproductive success of Adélie and chinstrap penguins: linking response of predators to prey population dynamics. Polar Biol 27:544–554. https://doi.org/10.1007/s00300-004-0617-1
Meyer B, Atkinson A, Bernard KS, Brierley AS, Driscoll R, Hill SL, Marschoff E, Maschette D, Perry FA, Reiss CS, Rombolá E, Tarling GA, Thorpe SE, Trathan PN, Zhu G, Kawaguchi S (2020) Successful ecosystem-based management of Antarctic krill should address uncertainties in krill recruitment, behaviour and ecological adaptation. Commun Earth Environ 1:28. https://doi.org/10.1038/s43247-020-00026-1
Miller AK, Trivelpiece WZ (2007) Cycles of Euphausia superba recruitment evident in the diet of Pygoscelid penguins and net trawls in the South Shetland Islands, Antarctica. Polar Biol 30:1615–1623. https://doi.org/10.1007/s00300-007-0326-7
Nicol S, Clarke J, Romaine SJ, Kawaguchi S, Williams G, Hosie GW (2008) Krill (Euphausia superba) abundance and Adélie penguin (Pygoscelis adeliae) breeding performance in the waters off the Béchervaise Island colony, East Antarctica in 2 years with contrasting ecological conditions. Deep Sea Res PT II 55:540–557. https://doi.org/10.1016/j.dsr2.2007.11.013
Perry FA, Atkinson A, Sailley SF, Tarling GA, Hill SL, Lucas CH, Mayor DJ (2019) Habitat partitioning in Antarctic krill: Spawning hotspots and nursery areas. PLoS ONE 14:e0219325. https://doi.org/10.1371/journal.pone.0219325
Pickett EP, Fraser WR, Patterson-Fraser DL, Cimino MA, Torres LG, Friedlaender AS (2018) Spatial niche partitioning may promote coexistence of Pygoscelis penguins as climate-induced sympatry occurs. Ecol Evol 8:9764–9778. https://doi.org/10.1002/ece3.4445
QGIS Development Team (2019) QGIS geographic information system. Open Source Geospatial Foundation Project. https://qgis.org
Quetin LB, Ross RM (1984) School composition of the Antarctic krill Euphausia superba in the waters west of the Antarctic peninsula in the austral summer of 1982. J Crustac Biol 4:96–106. https://doi.org/10.1163/1937240X84X00525
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reiss CS, Cossio AM, Loeb V, Demer DA (2008) Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES J Mar Sci 65:497–508. https://doi.org/10.1093/icesjms/fsn033
Richerson K, Santora JA, Mangel M (2017) Climate variability and multi-scale assessment of the krill preyscape near the north Antarctic Peninsula. Polar Biol 40:697–711. https://doi.org/10.1007/s00300-016-1994-y
RStudio Team (2018) RStudio: integrated development for R. RStudio Inc, Boston
Russell Lenth (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.5.1. https://CRAN.R-project.org/package=emmeans
Saba GK, Fraser WR, Saba VS, Iannuzzi RA, Coleman KE, Doney SC, Ducklow HW, Martinson DG, Miles TN, Patterson-Fraser DL, Stammerjohn SE, Steinberg DK, Schofield OM (2014) Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula. Nat Commun 5:4318. https://doi.org/10.1038/ncomms5318
Santa Cruz F, Ernst B, Arata JA, Parada C (2018) Spatial and temporal dynamics of the Antarctic krill fishery in fishing hotspots in the Bransfield Strait and South Shetland Islands. Fish Res 208:157–166. https://doi.org/10.1016/j.fishres.2018.07.020
Santora JA, Reiss CS, Cossio AM, Veit RR (2009) Interannual spatial variability of krill (Euphausia superba) influences seabird foraging behavior near Elephant Island, Antarctica. Fish Oceanogr 18:20–35. https://doi.org/10.1111/j.1365-2419.2008.00490.x
Santos M, Capurro A (2017) Domain 1 marine protected area preliminary proposal part B: conservation objectives. SC-CAMLR-XXXVI/BG/22:1–35. https://www.ccamlr.org/en/sc-camlr-xxxvi/17
Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York. ISBN 978-0-387-75968-5
Siegel V (2016) Biology and ecology of Antarctic krill. In: Piepenburg D (ed) Advances in polar ecology, vol 1. Springer International Publishing, Switzerland
Tarling GA, Hill S, Peat H, Fielding S, Reiss C, Atkinson A (2016) Growth and shrinkage in Antarctic krill Euphausia superba is sex-dependent. Mar Ecol Prog Ser 547:61–78. https://doi.org/10.3354/meps11634
Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci 108:7625–7628. https://doi.org/10.1073/pnas.1016560108
Volkman NJ, Presler P, Trivelpiece WZ (1980) Diets of pygoscelid penguins at King George Island, Antarctica. Condor 82:373–378. https://doi.org/10.2307/1367558
Watkins JL, Buchholz F, Priddle J, Morris DJ, Ricketts C (1992) Variation in reproductive status of Antarctic krill swarms; evidence for a size-related sorting mechanism? Mar Ecol Prog Ser 82:163–174. https://www.jstor.org/stable/24827327
Watkins JL, Reid K, Ramm D, Zhao XY, Cox M, Skaret G, Fielding S, Wang XL, Niklitschek E (2016) The use of fishing vessels to provide acoustic data on the distribution and abundance of Antarctic krill and other pelagic species. Fish Res 178:93–100. https://doi.org/10.1016/j.fishres.2015.07.013
Watters GM, Hinke JT, Reiss CS (2020) Long-term observations from Antarctica demonstrate that mismatched scales of fisheries management and predator-prey interaction lead to erroneous conclusions about precaution. Sci Rep 10:2314. https://doi.org/10.1038/s41598-020-59223-9
Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–112
Wilson RP (2010) Resource partitioning and niche hyper-volume overlap in free-living Pygoscelid penguins. Funct Ecol 24:646–657. https://doi.org/10.1111/j.1365-2435.2009.01654.x
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. In: Saveliev AA, Smith GM, Samet J, Tsiatis A, Wong W (eds) Statistics for biology and health. Springer New York, New York. https://link.springer.com/book/10.1007%2F978-0-387-87458-6
Acknowledgments
We thank all field and laboratory assistants who helped collecting and analysing stomach content samples associated with this study. The authors also thank the scientific observers working as part of the CCAMLR Scheme of International Scientific Observation who collected the krill length data from the fishery and the CCAMLR’s Secretariat for providing the data extract of these data. We thank the anonymous reviewers and editors for their helpful comments and suggestions on improving the manuscript. Finally, we are very grateful to Jorge M. Viccichi and Claudio Matko for their unconditional support and their significant contributions.
Funding
The FONCYT—Agencia Nacional de Promoción Científica y Tecnológica (Grant: PICTO 2010-0111) and the Instituto Antártico Argentino – Dirección Nacional del Antártico (PINST-05) provided financial and logistical support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests. The krill fishery data was provided by the CCAMLR’s Secretariat (Hobart, Tasmania) and has been published in accordance with the rules adopted by the Twenty-Second Meeting of the Commission (CCAMLR-XXII, paragraphs 12.1 to 12.6; https://www.ccamlr.org/en/document/publications/rules-access-and-use-ccamlr-data).
Ethical approval
All procedures involving Adélie and gentoo penguins were conducted under appropriate international, national and/or institutional guidelines for the care and use of animals. All necessary approvals were obtained. Each year, sampling was completed under the permit granted by the Dirección Nacional del Antártico (Environmental Management Office).
Consent to participate
Not applicable.
Consent for publication
Consistent with CCAMLR Rules for data Access and Use.
Additional information
Responsible Editor: T. A. Clay.
Reviewers: undisclosed experts.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Juáres, M.A., Grech, M.G., Casaux, R. et al. Size structure of Antarctic krill inferred from samples of Pygoscelid penguin diets and those collected by the commercial krill fishery. Mar Biol 168, 22 (2021). https://doi.org/10.1007/s00227-021-03831-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03831-0