Divergent trophic responses of sympatric penguin species to historic anthropogenic exploitation and recent climate change Kelton W. McMahona,1, Chantel I. Michelsonb, Tom Hartc, Matthew D. McCarthyd, William P. Pattersone, and Michael J. Politob,1,2 aGraduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882; bDepartment of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, LA 70803; cDepartment of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom; dOcean Sciences Department, University of California, Santa Cruz, CA 95064; and eSaskatchewan Isotope Laboratory, Department of Geological Sciences, University of Saskatchewan, Saskatchewan, S7N 5E2 SK, Canada Edited by Nils C. Stenseth, University of Oslo, Oslo, Norway, and approved November 4, 2019 (received for review July 30, 2019) The Southern Ocean is in an era of significant change. Historic similar nesting habitats, have similar phenology and breeding overharvesting of marine mammals and recent climatic warming biology, are both considered pagophobic (ice-avoiding) unlike have cascading impacts on resource availability and, in turn, their pagophilic congener the Adélie penguin (Pygoscelis adeliae), ecosystem structure and function. We examined trophic responses and strongly overlap in dietary utilization of Antarctic krill of sympatric chinstrap (Pygoscelis antarctica) and gentoo (Pygo- (Euphausia superba) (11, 12). However, over the last 40 y, scelis papua) penguins to nearly 100 y of shared environmental chinstrap penguin populations within the Antarctic Peninsula change in the Antarctic Peninsula region using compound-specific region have decreased by ∼30 to 53% (13, 14), while those of stable isotope analyses of museum specimens. A century ago, gen- gentoo penguins have had more than a 6-fold increase (14–16). too penguins fed almost exclusively on low-trophic level prey, For example, along the South Orkney Islands, South Shetland such as krill, during the peak of historic overexploitation of marine Islands, and the Western Antarctic Peninsula, chinstrap penguin mammals, which was hypothesized to have resulted in a krill sur- populations are estimated to have declined from as much as 3.1 plus. In the last 40 y, gentoo penguin trophic position has in- million breeding pairs in the 1970s and 1980s to as few as 1.4 ECOLOGY creased a full level as krill declined in response to recent climate million breeding pairs in the 2010s (13), while gentoo penguins in change, increased competition from recovering marine mammal this region increased from ∼31,312 to 243,316 breeding pairs populations, and the development of a commercial krill fishery. during this same time period (15, 16). These divergent population A shifting isotopic baseline supporting gentoo penguins suggests trajectories may be, at least partially, explained by key differences a concurrent increase in coastal productivity over this time. In con- in their trophic niches, which are thought to facilitate ecological trast, chinstrap penguins exhibited no change in trophic position, niche segregation and promote coexistence (5, 17, 18). Chinstrap despite variation in krill availability over the past century. The penguins have a narrow trophic niche with a specialized diet specialized foraging niche of chinstrap penguins likely renders dominated by Antarctic krill (17, 18). Gentoo penguins, conversely, them more sensitive to changes in krill availability, relative to are generalist foragers with a broader and more flexible trophic gentoo penguins, as evinced by their declining population trends niche relative to chinstrap penguins (18, 19). Trivelpiece et al. in the Antarctic Peninsula over the past 40 y. Over the next cen- tury, similarly divergent trophic and population responses are Significance likely to occur among Antarctic krill predators if climate change and other anthropogenic impacts continue to favor generalist over specialist species. We reveal species-specific changes in penguin trophic responses to historic shifts in krill availability over the last century by ap- Antarctica | ecogeochemistry | environmental change | historical ecology | plying new molecular isotope techniques to historic penguin krill surplus museum specimens. Generalist foraging gentoo penguins, whose population increased 6-fold in the last 40 y, showed adaptive shifts in trophic position in concert with changes in Antarctic krill cological responses to shared environmental change can vary availability following historic exploitation of marine mammals Esubstantially among species, even those that are closely re- – and recent climate change. In contrast, chinstrap penguins lated (1 4). Understanding species-specific responses to envi- maintained a consistent krill diet despite changes in krill avail- ronmental change is critical to predicting the resilience and ability and concurrent population declines. These results highlight adaptation of species to disturbances associated with changes in – ’ how responses to shared environmental change can vary sub- climate or human environment interactions. A species ecolog- stantially among closely related species, supporting ecological ical niche, defined as a multidimensional hypervolume that in- niche theory that specialists will be more sensitive to environ- cludes axes relating to trophic dynamics, habitat use, and other mental change than their generalist counterparts. life history requirements (5, 6), can be a key predictor of species’ responses to changes in their environment (1, 7). For example, Author contributions: K.W.M., T.H., and M.J.P. designed research; K.W.M., T.H., M.D.M., specialist species use a narrow window of resources and are and M.J.P. performed research; K.W.M., C.I.M., W.P.P., and M.J.P. analyzed data; and thought to be highly sensitive to environmental change (8, 9). In K.W.M. and M.J.P. wrote the paper. contrast, generalist species have broad or flexible resource use The authors declare no competing interest. and are predicted to be more resilient to disturbances and/or This article is a PNAS Direct Submission. changes in resource availability associated with environmental Published under the PNAS license. change (7, 10). 1K.W.M. and M.J.P. contributed equally to this work. Chinstrap (Pygoscelis antarctica) and gentoo (Pygoscelis papua) 2To whom correspondence may be addressed. Email: [email protected]. penguins co-occur in the Antarctic Peninsula region and provide This article contains supporting information online at https://www.pnas.org/lookup/suppl/ an opportunity to test explicit hypotheses about sympatric species’ doi:10.1073/pnas.1913093116/-/DCSupplemental. responses to environmental change. These sympatric species use First published December 2, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1913093116 PNAS | December 17, 2019 | vol. 116 | no. 51 | 25721–25727 Downloaded by guest on October 4, 2021 (20) proposed a hypothetical framework, invoking dietary re- over time in response to the proposed climate and harvesting- liance on krill, to explain recent population trends in Pygoscelis related changes in the availability of Antarctic krill, i.e., lower penguins as a function of the synergistic interaction of historic trophic positions indicative of higher dietary contribution of krill overexploitation of marine mammals, coupled with recent global in the first half of the 20th century during the proposed krill climate change, on krill availability in the Antarctic Peninsula surplus and higher trophic positions reflecting a switch away from region (Fig. 1). krill during the krill decline of the second half of the 20th century. The sequential overharvesting of seals, baleen whales, and finfish To test these hypotheses, we analyzed the compound-specific from the early 19th to the mid-20th century (12, 21, 22) is stable nitrogen isotope values of individual amino acids (AAs) in hypothesized to have resulted in a surplus of Antarctic krill avail- archived penguin feathers to reconstruct the baseline food web able for the remaining krill predators, such as Pygoscelis penguins nitrogen cycling and penguin trophic positions through time. The – 15 15 (23 25). For example, removal of whales alone in the mid-20th source AA phenylalanine δ N value (δ NPhe) exhibits minimal century is calculated to have led to an ∼150 million metric ton trophic discrimination, providing a proxy for the isotopic signa- surplus of krill annually (21, 23). However, over the past 70 y, ture of nitrogen cycling at the base of the food web, while the 15 15 regional climate change, including ocean warming, sea ice de- trophic AA glutamic acid δ N value (δ NGlu) exhibits strong cline, and ocean acidification, have acted in concert to negatively trophic discrimination [reviewed in McMahon and McCarthy impact the abundance, distribution, and recruitment of krill (26– (36)]. Together, these differentially fractionating AAs provide a 29), although see refs. 30–32. Recent recovery of whale and seal measure of trophic position (TP) that is internally indexed to the populations (33, 34) and a growing Antarctic krill fishery (35) nitrogen isotope value of the base of the food web (36). This have likely further decreased the prior krill surplus and increased approach is particularly valuable for examining biogeochemical competition among Southern Ocean krill predators, including cycling and trophic dynamics in a historical context when it is penguins (Fig. 1). challenging, if not impossible, to a priori characterize the iso- While compelling, the hypothetical