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The forgotten krill : the biology and ecological function of Thysanoessa macrura in the Southern Ocean ecosystem


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Wallis, JR ORCID: 0000-0003-2932-612X 2019 , 'The forgotten krill : the biology and ecological function of Thysanoessa macrura in the Southern Ocean ecosystem', PhD thesis, University of Tasmania.

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The importance of euphausiids or ‘krill’ in the Southern Ocean has long been documented, establishing important links between lower trophic levels and apex predators. Although more than 20 species of euphausiids are found within these mid – high latitude waters of the Southern hemisphere our current understanding of the function and role of euphausiids as a collective is almost exclusively restricted to the Antarctic krill, Euphausia superba. Whilst the importance of E. superba is well documented, its role as a keystone species has overshadowed the study of other euphausiid species in the Southern Ocean and limited the research needed to understand fundamental biology and ecology of those species. Despite being considered the second most abundant euphausiid species in the Southern Ocean, Thysanoessa macrura is one of these largely understudied species. Although T. macrura is beginning to be recognised as a species that requires more attention due to its significant biomass and abundance, current studies are generally restricted to describing population demography and ecology; however, the lack of concise information on the fundamental biology of the species makes providing a context to the role of T. macrura impossible.
Despite being a smaller euphausiid, high and calorific-rich lipid reserves, coupled with an extensive and ubiquitous latitudinal distribution from the sub-Antarctic to the Antarctic continent, indicate an importance of T. macrura that is currently underexplored for the pelagic ecosystem of the Southern Ocean. Abundances of T. macrura often exceed those of E. superba in regions including Prydz Bay (east Antarctica), Bransfield Strait (west Antarctica Peninsula), lower latitudes of the Antarctic Pacific Ocean, and may form a more important trophic connection in the Indian Ocean region of the Southern Ocean. A winter reproductive period for T. macrura has been indicated by the appearance of larval stages during June to August, however no direct information is currently reported on the reproductive cycle and fecundity of this species. The quantitative information on the diet of T. macrura is scarce and lacks the detail required to conceptualise their role and function in the ecosystem. This shortage of foundation information often necessitates the use of assumptions based on E. superba to understand the ecology of T. macrura in an ecosystem context. The current understanding of T. macrura, despite being limited, indicates a difference in fundamental biological and ecological processes between the two species that make such assumptions tenuous at best.
This PhD thesis focuses on filling vital knowledge gaps in the biology and ecology of T. macrura. A bottom-up approach is taken by first providing a foundation of fundamental biological information, including reproduction and life history. Ecological processes of this species are then conceptualised and developed to understand feeding ecology and population dynamics. Specifically, this thesis provides (1) the first conceptual model of gonadal development, maturation and fecundity estimates, (2) descriptions of the larval development, and (3) the diet of T. macrura from early larval stages to adults, identifying ontogenetic shifts
and overlap in feeding ecology. Building upon these biological processes, (4) the population demography of T. macrura is explored in the important Kerguelen Plateau region. Key highlights of each chapter are summarised below.
(1) Gonadal development and maturation of T. macrura during late winter in high latitude waters confirms a winter reproductive period previously assumed from observational evidence of larvae. Analysis of ovaries and direct oocyte counts allowed for the first estimate of T. macrura fecundity, which scales strongly with female length, resulting in a surprisingly high egg production of > 2200 eggs female\(^{-1}\) during a reproductive period. (2) After hatching, the resulting larvae undertake a series of developmental steps, with the morphological characteristics of post-naupliar stages consisting of 3 calyptopis and 6 furcilia stages described in detail, allowing for the avoidance of misidentification with larvae of other euphausiid species with overlapping distributions. Despite expecting an influence of temperature on the size of larvae due to the latitudinal range of the species, T. macrura larvae appear to be able to capitalise on the increased primary productivity during their appearance in surface waters, indicating that food availability is a more important driver of larval growth and development than temperature.
(3) Although diatoms were common, protozoan and metazoan prey, particularly copepods identified by their mandibles, were found to be the most important contributor to the diet of adult T. macrura. Coupling microscopic examination of guts with analysis of lipid profiles and fatty acid biomarkers emphasised the importance of carnivory to T. macrura, particularly predation on the copepod Calanoides acutus. The first evidence of the diets of larval T. macrura confirm their ability to graze phytoplankton. Additionally, mouthpart morphology of larvae suggests a niche overlap with adults, consuming prey of similar size-range, although the ability of larvae to capture larger motile prey is reduced due to the lack of fully developed secondary feeding appendages.
(4) Despite a ubiquitous distribution at the oceanic scale, T. macrura populations are not homogenous, responding strongly to environmental drivers. Spatial heterogeneity of T. macrura over the Kerguelen Plateau was driven by water mass properties and the presence of the copepod C. acutus, a dominant prey source. Adult T. macrura reached abundances up to 162 ind. 1000 m\(^{-3}\) accompanied by high abundances of early furcilia stages in excess of 4000 ind. 1000 m\(^{-3}\) . The total lipids of T. macrura were found to be reaching their maximum recorded in the literature (> 40% of dry weight), stored as predominantly wax esters as a lipid mass within the free carapace space.
A conservative mean biomass of 1.66 mg m\(^{-3}\) was calculated for T. macrura across the southern Kerguelen Plateau region, with peaks up to 9.53 mg m\(^{-3}\) . This high biomass, coupled with high, energy-rich lipid content throughout most of the year indicates T. macrura forms a substantial energy source for vertebrate predators in the high productive Kerguelen Plateau region.

Item Type: Thesis - PhD
Authors/Creators:Wallis, JR
Keywords: Population Biology, Southern Ocean krill, Reproductive Biology, Life History, ecology
DOI / ID Number: 10.25959/100.00034624
Copyright Information:

Copyright 2019 the author

Additional Information:

Chapter 2 appears to be the equivalent of a pre-print version of an article published as: Wallis, J. R., Kawaguchi, S., Swadling, K. M., 2018. Sexual differentiation, gonad maturation and reproduction of the Southern Ocean euphausiid Thysanoessa macrura (Sars, 1883) (Crustacea: Euphausiacea), Journal of crustacean biology, 38(1), 107-118

Chapter 3 appears to be the equivalent of a pre-copyedited, author-produced version of an article accepted for publication in Polar biology following peer review. The version of record, Wallis, J. R., 2018. A description of the post-naupliar stages of Southern Ocean krill (Thysanoessa macrura), Polar biology, 41(12), 2399-2407 is available online at:

Chapter 5 appears to be the equivalent of a pre-print version of an article published as: Wallis, J. R., Maschette, D., Wotherspoon, S., Kawaguchi, S., Swadling, K. M., 2020. Thysanoessa macrura in the southern Kerguelen region: Population dynamics and biomass, Deep-sea research part II, Topical studies in oceanography, 174, 104719

Appendix E is the following published article: Wallis, J. R., Smith, A. J. R., Kawaguchi, S., Discovery of gregarine parasitism in some Southern Ocean krill (Euphausiacea) and the salp Salpa thompsoni, Polar biology, 40, 1913–1917, published 2017, Springer Verlag

Appendix F is the following published article: Wallis, J. R., Melvin, J., King, R., Kawaguchi, S., 2019. In situ growth rate estimates of Southern Ocean krill, Thysanoessa macrura, Antarctic science, 31(3), 116-122

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