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Is the hyperiid amphipod Themisto gaudichaudii poised to displace krill in the warming region of the Southern Ocean?

Applicant Professor Dr. Wilhelm G. Hagen, since 4/2019
Subject Area Oceanography
Term from 2015 to 2020
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 274981270
 
Final Report Year 2020

Final Report Abstract

Over the last decades, under the influence of warming waters, shrinking of sea-ice extent, and an altered timing of phytoplankton blooms, the southwestern Southern Ocean pelagic realm has experienced an ecological shift from a krill-based to a salp-based ecosystem. This “gelatinous” shift strongly impacts top consumers such as whales, seabirds and seals, depending on Antarctic krill as lipid-rich food, but also alters biogeochemical processes. Another major pelagic player, besides krill and salps, is undergoing a range shift: the hyperiid amphipod crustacean Themisto gaudichaudii. This widespread crustacean dominates the zooplankton north of the sea-ice edge and occupies a range covering a temperature gradient of almost 20°C. It is predicted to expand its distribution poleward and increases in abundance have already been noted in recent years. Knowledge on Themisto is lacking to predict how this carnivorous pelagic species will interact with krill and salps in areas of increasing distributional overlap. Similar poleward range shifts of temperate and polar Themisto species in the northern hemisphere have been observed: T. abyssorum and T. compressa are currently expanding their range and increasing abundances are observed in Arctic seas, whereas T. libellula, a cold-water Arctic species, is undergoing a range contraction. The aims of this project were to investigate: 1) the likelihood of an expansion by characterizing the genetic connectivity and morphological plasticity of Themisto populations, 2) the consequences of this expansion by elucidating the dietary preferences of the carnivorous T. gaudichaudii and 3) its molecular basis to thermal acclimation and adaptation by carrying out temperature-change experiments followed by gene expression profiling of two range-expanding Themisto species, T. gaudichaudii in the Southern Ocean and T. abyssorum in the Arctic Ocean. First, genetic analyses revealed the existence of three widespread lineages with overlapping distributions. Each of them was present in almost all localities sampled except for specimens collected near the Antarctic Peninsula, which were only recovered in cluster 1. This genetic homogeneity spans a wide geographic and environmental gradient, from sub-zero to 13°C water masses. Furthermore, haplotype network patterns and demographic statistics indicate a recent population expansion, or a selective sweep; both scenarios would match with an ongoing poleward range extension, where individuals could be undergoing selective pressures in a colder environment and/or increasing in abundance in the newly colonized regions. Morphological analyses were applied to investigate the occurrence of the two forms observed within T. gaudichaudii: the long-legged bispinosa and the short-legged compressa by determining the ratio of the fifth and sixth pereopods (legs) (= P5/P6 ratio). This ratio decreased with total length and latitude, with the long-legged form being more frequently found at lower latitudes and higher sea surface temperatures. With regard to feeding, the long-legged individuals have an advantage over the short-legged ones for capturing large prey. Hence, this morphological plasticity may represent an ecophenotypic response to temperature and available prey. These different feeding strategies certainly contribute to T. gaudichaudii being a ubiquitous predator in distinct pelagic water masses and prey communities. Second, we investigated T. gaudichaudii’s diet composition by means of metabarcoding analyses of stomach contents of 174 individuals, sampled in 5 different regions across the Southern Ocean. Results indicated a diversified diet varying greatly between the different regions. There was a predominance of krill species, including Antarctic krill, in the diet of Themisto in the Antarctic Peninsula region, where a severe krill decline has been observed. Hence, the poleward expansion of Themisto may further impact local krill stocks and the top predators relying on them. Even though previously considered as trophic dead end, ctenophore reads were also abundant in Themisto’s stomachs, showing that gelatinous zooplankton other than salps play an important role in the Southern Ocean food web. Third, we aimed to compare the thermal stress response on the level of the transcriptome, of the species T. gaudichaudii and T. abyssorum, both undergoing a poleward range shift. Individuals of populations from warmer waters within their distribution centres were exposed to a cold treatment, whereas those living more poleward and in colder waters (0°C) were exposed to a heat-shock treatment. De novo transcriptome assembly was carried out to compare patterns of differentially down- or up-regulated genes according to the thermal treatments. A total of 83 libraries (44 of T. gaudichaudii and 39 of T. abyssorum) were created and utilized for the transcriptome assembly of both species. By comparing the number and function of the differentially expressed transcripts, the heat shock had more metabolic consequences than the cold treatment in both species. In T. gaudichaudii, the metabolic response was more homogeneous in all analysed individuals than was the case for T. abyssorum. Cuticle proteins seem to be an important element in the temperature response in both species. In T. gaudichaudii, cytochrome c oxidase was also involved both in the heat and cold response. In summary, these genetic, morphological, trophic and transcriptomic findings underline the potential of Themisto to become a central player in the pelagic ecosystem near the Antarctic Peninsula, where it will exert a strong top-down pressure on local krill stocks. Its poleward expansion may eventually, through trophic ramifications, alter food web structures and affect top predator populations.

Publications

  • (2017). INTERPELAGIC: Interactions between key players of the Southern Ocean zooplankton: amphipopds, copepods, krill and salps. In: Boebel O (ed.). The expedition PS103 of the Research Vessel POLARSTERN to the Weddell Sea in 2016/17. Berichte zur Polar- und Meeresforschung 710: 95-111
    Havermans C, Schöbinger S, Schröter F
  • (2018) A biodiversity survey of scavenging amphipods in a proposed marine protected area: the Filchner area in the Weddell Sea, Antarctica. Polar Biology 41(7): 1371-1390
    Havermans C, Seefeldt MA, Held C
    (See online at https://doi.org/10.1007/s00300-018-2292-7)
  • (2018) Bottom-up and top-down triggers of diversification: A new look at the evolutionary ecology of scavenging amphipods in the deep sea. Progress in Oceanography 164: 37-51
    Havermans C, Smetacek V
    (See online at https://doi.org/10.1016/j.pocean.2018.04.008)
  • (2018) Understanding processes at the origin of species flocks with a focus on the marine Antarctic fauna. Biological Reviews 93(1): 481-504
    Chenuil A, Saucède T, Hemery L, Eléaume M, Féral JP, Améziane N, Lecointre G, Havermans C
    (See online at https://doi.org/10.1111/brv.12354)
  • (2019) A survival pack for escaping predation in the open ocean: amphipod-pteropod associations in the Southern Ocean. Marine Biodiversity 49(3): 1361-1370
    Havermans C, Hagen W, Zeidler W, Held C, Auel H
    (See online at https://doi.org/10.1007/s12526-018-0916-3)
  • (2019) Pelagic amphipods in the Eastern Fram Strait with continuing presence of Themisto compressa based on sediment trap time series. Frontiers in Marine Science 6: 311
    Schröter F, Havermans C, Kraft A, Knüppel N, Beszczynska-Moeller A, Bauerfeind E, Nöthig E
    (See online at https://doi.org/10.3389/fmars.2019.00311)
  • (2019) Predatory zooplankton on the move: Themisto amphipods in high-latitude marine pelagic food webs. Advances in Marine Biology Vol 82, Elsevier 42 pp.
    Havermans C, Auel H, Hagen W, Held C, Ensor NS, Tarling GA
    (See online at https://doi.org/10.1016/bs.amb.2019.02.002)
  • (2020). Polares Plankton: Kleinlebewesen im sich wandelnden Südpolarmeer. Biologie in unserer Zeit 50(1): 28-35
    Beszteri B, Havermans C, Auel H, Hagen W, Trimborn S
    (See online at https://doi.org/10.1002/biuz.202010694)
  • Crustacean guide for predator studies in the Southern Ocean. Scientific Committee on Antarctic Research. Cambridge, UK, 255 pp.
    Xavier JC, Cherel Y, Boxshall G, Brandt A, Coffer T, Forman J, Havermans C, Jazdzewska A, Kouwenberg J, Schnabel K, Schiaparelli S, Siegel V, Tarling GA, Thatje S, Ward P, Gutt J
 
 

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