Wandering albatross, Diomedea exulans, and the flightless moth, Pringleophaga marioni, on sub-Antarctic Marion Island : a case of thermal ecosystem engineering

Haupt, Tanya Magdeleen (2014-04)

Thesis (PhD)--Stellenbosch University, 2014.

Thesis

ENGLISH ABSTRACT: Recent work has shown that on sub-Antarctic Marion Island, caterpillars of the flightless tineid moth, Pringleophaga marioni, have much higher and considerably less variable populations in recently abandoned nests of the wandering albatross, Diomedea exulans, compared to old nests and other plant communities. Since no evidence for nutrient input was provided, it was hypothesised that wandering albatrosses serve as thermal ecosystem engineers by providing a warm microhabitat in which caterpillar growth and survival are improved. In this thesis, I used a multidisciplinary approach integrating physiology, ecology and behaviour, to better understand the reason for the high caterpillar biomass in nests, and explore the hypothesis of thermal ecosystem engineering. My first objective was to provide a more quantitative life-cycle estimate for P. marioni by rearing caterpillars at different temperature regimes, and in so doing estimate the effects of temperature on development and survival (Chapter 2). Contrary to previous estimates of 2-5 years, a year-long life cycle estimate was found, and although development was fastest at high temperatures of 15°C, caterpillars had low survival. Development time was similar at the fluctuating temperatures of 5-15°C and 10°C, with a longer duration at 5°C. By conducting a more extensive sampling effort of caterpillar biomass and temperature in nests (Chapter 3), I showed that recently abandoned nests had a significantly higher abundance of caterpillars compared to nests from which chicks had recently fledged, as well as older nests. Temperature data collected over a c. one year period showed that temperature in occupied nests remained high during the entire year of occupancy and events at which P. marioni experience chill coma were substantially reduced. Consequently, the effects of thermal acclimation on the physiological and behavioural responses of P. marioni caterpillars were explored. First, how temperature affects the metabolic rate of caterpillars was examined (Chapter 4). Metabolic rate was significantly higher at a low acclimation temperature of 5°C compared to 15°C, providing partial support for metabolic cold adaptation. No evidence was provided that caterpillars reduce their metabolic rates to conserve water, and caterpillars responded to fluctuating temperatures by depressing their metabolic rates. Second, the relationship between thermal preference and locomotor performance of caterpillars was examined (Chapter 5). A common assumption made is that animals will prefer temperatures that maximise performance. Preference was significantly lower (c. 8°C) compared to the optimum temperature for locomotion (c. 23°C), and it was suggested that caterpillars may prefer lower temperatures where survival or assimilation efficiency is maximised. Lastly, if nests provide a fitness advantage, either caterpillars or ovipositing female moths may likely seek out nests. Using choice experiments (Chapter 6), I showed that caterpillars are unlikely to use thermal or chemosensory cues to locate nests and showed a strong avoidance to high temperatures of 15°C. This latter response initially does not appear to fit with the idea that caterpillars favour warm nest temperatures. Although such high temperatures may occasionally be reached in wandering albatross nests, there is considerable daily fluctuation. Variable temperatures including high temperatures of 15°C did not have deleterious effects on caterpillar growth rates and survival, and development was fastest at the fluctuating temperature of 5-15°C compared to 5°C. Caterpillars may also experience chill coma events less often in warm nest environments. Collectively, these findings suggest that the thermal engineering by wandering albatross may indeed improve caterpillar growth and survival. Additional factors were also identified that may contribute to the high abundance of caterpillars in nests (e.g. differential mortality in and out of nests because of mouse predation; high temperatures enhance decomposition rates) (Chapter 7), therefore leaving much scope for future work to further explore this unique interaction between wandering albatross and flightless moth caterpillars.

AFRIKAANSE OPSOMMING: Onlangse werk het getoon dat op sub-Antarktiese Marion Eiland ruspes van die vlerklose mot Pringleophaga marioni baie hoër en aansienlik minder veranderlike bevolkings het in onlangs verlate neste van die Grootalbatros, Diomedea exulans, in vergelyking met die ou neste. Aangesien daar geen bewyse vir voedingstof insette is nie, is die hipotese dat die Grootalbatros dien as ‘n termiese ekosisteem ingeneur deur die verskaffing van 'n warm mikrohabitat waarin ruspe oorlewing en groei verbeter. In hierdie tesis gebruik ek 'n multidissiplinêre benadering deur fisiologie, ekologiese en gedrag te integreer om die rede vir die hoë ruspe biomassa in neste beter te verstaan, en die hipotese van 'n warm ekosisteem ingeneur te verken. My eerste doelwit was om 'n meer kwantitatiewe lewensiklus skatting vir P. marioni te voorsien deur ruspes by verskillende temperatuur groot te maak, en sodoende die effek van temperatuur op die ontwikkeling en oorlewing te bepaal (Hoofstuk 2). In teenstelling met die vorige skattings van 2-5 jaar, is daar tans ‘n jaar lank lewensiklus skatting gevind, en hoewel ontwikkeling die vinnigste was by hoë temperature van 15°C, het die ruspes lae oorlewing vertoon. Ontwikkelingstyd was soortgelyk by wisselende temperature van 5-15°C en 10°C, met 'n langer duur by 5°C. Deur die uitvoer van 'n meer intensiewe monsterneming van ruspe biomassa en temperatuur in neste (Hoofstuk 3), het ek getoon dat onlangs verlate neste 'n aansienlike hoër aantal ruspes het in vergelyking met die neste van waar kuikens onlangs volwaardig was, sowel as ouer neste. Temperatuur data versamel oor 'n tydperk van ongeveer een jaar het getoon dat die besette neste se temperatuur hoog gebly het gedurende die hele jaar van besetting. Gevolglik is die effek van 'n warm akklimasie op die fisiologiese en gedrags reaksies van P. marioni ruspes verken. Eerstens is die effek van hoë temperatuur op die metaboliese tempo van ruspes ondersoek (Hoofstuk 4). Metaboliese tempo is aansienlik hoër na 'n lae akklimasie temperatuur van 5°C in vergelyking met 15°C, die verskaffing van gedeeltelike steun vir metaboliese koue aanpassing. Geen bewyse is gevind dat die ruspes hul metaboliese tempo verminder om water te bewaar nie, en ruspes reageer op wisselende temperature deur hul metaboliese tempo te verlaag. Tweedens is die verhouding tussen hitte voorkeur en die bewegings prestasie van ruspes ondersoek (Hoofstuk 5). ‘n Algemene aanname is dat diere temperature sal verkies waar hulle maksimum sal presteer. Voorkeur was aansienlik laer (c. 8°C) in vergelyking met die optimum temperatuur vir beweging (c. 23°C), en dit is voorgestel dat ruspes laer temperature waar oorlewing of assimilasie doeltreffendheid geoptimaliseer word kan verkies. Ten slotte, indien neste 'n fiksheid voordeel inhou, sal ruspes of eierleênde vroulike motte waarskynlik neste uitsoek. Deur die gebruik van keuse eksperimente (Hoofstuk 6), het ek getoon dat ruspes onwaarskynlik hitte of chemosensoriese leidrade gebruik om neste op te spoor en het 'n sterk vermyding aan hoë temperature van 15°C. Die laasgenoemde reaksie is in kontras met die idee dat ruspes ten gunste is van warm nes temperature. Alhoewel sulke hoë temperature soms bereik kan word in Grootalbatros neste, is daar ' n aansienlike daaglikse vernadering. Veranderlike temperature insluitende hoë temperature van 15°C het nie nadelige uitwerking op die ruspe se groei en ontwikkeling nie en is die vinnigste by die wisselende temperature van 5-15°C in vergelyking met 5°C. Die hoë optimale veranderlike temperatuur dui daarop dat ruspes meer aktief kan wees in warm neste wat lei tot verhoogde verbruik en groei. Ruspes kan ook minder dikwels verkillingskoma ervaar in warm nes omgewings. Gesamentlik dui hierdie bevindinge daarop dat die hitte ekosisteem ingeneur deur die Grootalbatros inderdaad ruspe oorlewing en groei kan verbeter. Daar is egter ander faktore wat geïdentifiseer is wat ook kan bydra tot die hoë oorvloed van ruspes in neste (bv. differensiële mortaliteit in en uit die neste as gevolg van muis predasie, hoë temperature verhoog ontbindingstempo) (Hoofstuk 7), dus laat ruimte vir toekomstige werk.

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