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The effects of Alexandrium pacificum and marine heatwaves on the green-lipped mussel (Perna canaliculus)
Doctoral Thesis   Open access

The effects of Alexandrium pacificum and marine heatwaves on the green-lipped mussel (Perna canaliculus)

Hannah Ellen Greenhough
Doctor of Philosophy - PhD, University of Otago
22/04/2025
Handle:
https://hdl.handle.net/10523/45833

Abstract

Bivalves Mussel Harmful algal blooms Alexandrium Paralytic shellfish toxins Bioactive extracellular compounds Early life stages Multiple stressors Marine heatwaves Exceptional Thesis collection Genomics and transcriptomics Bioassays Climate change impacts and adaptation

Green-lipped mussels (Perna canaliculus, GLM) are New Zealand’s (NZ) most valuable aquaculture species and hold significant economic, environmental, and cultural importance. Since 2010, harmful algal blooms (HABs) caused by the paralytic shellfish toxin (PST)-producing Alexandrium pacificum have occurred regularly in the Marlborough Sounds, NZ’s largest GLM farming region. Additionally, GLM face escalating threats from climate change, including increasingly frequent and intense marine heatwaves (MHWs). These stressors pose significant risks to GLM populations and the farming industry, which relies on juvenile mussels (spat) sourced from the wild. This thesis explores the effects of A. pacificum exposure on several GLM life stages and investigates how MHWs exacerbate these impacts.

Using both in vitro and in vivo assays, GLM were exposed to environmentally relevant concentrations of A. pacificum to investigate mechanisms of toxicity. A range of techniques including flow cytometry, histology, transcriptomics, epigenetics, lipid analysis and mass spectrometry were used to measure the physiological, behavioural and molecular responses of GLM and provide a comprehensive understanding of how A. pacificum and MHWs affect each developmental stage.

The early life stages of GLM, including gametes, embryos, and larvae, were particularly vulnerable to HABs. Whole-cell treatments of A. pacificum caused significant sperm mortality, embryo lysis, and an 85 % reduction in development to veliger (D-stage) larvae at low cell concentrations mirroring those observed in natural blooms. Growth rates of D-stage larvae exposed to Alexandrium spp. were halved during a 4-day exposure and remained impaired after a 4-day recovery period. Both PST-producing A. pacificum and non-PST-producing Alexandrium minutum negatively affected D-stage larvae, suggesting toxicity mechanisms beyond PSTs, potentially involving surface-associated or bioactive extracellular compounds. In contrast, significant hemocyte mortality was observed with cell-free A. pacificum treatments containing high PST concentrations. Later larval stages appeared less affected, indicating stage-specific susceptibility to Alexandrium spp. exposure. These findings highlight the diverse toxic mechanisms of A. pacificum and suggest that HABs could disrupt early GLM development, impacting survival and recruitment in the wild.

MHWs in NZ’s coastal waters often coincide with A. pacificum blooms in GLM farming regions, thus imparting dual stresses on GLM. Experiments investigating the combined effects of these stressors revealed significant stress responses in spat and subadult GLMs. While MHWs alone had minimal impact on spat survival, combined MHW and A. pacificum exposure reduced survival, slowed growth rates and decreased byssal plaque production, critical for attachment and survival. Gene expression analyses in spat exposed to A. pacificum indicated oxidative stress and detoxification responses, with HAB exposure causing more negative effects than MHWs. In subadults, MHWs were the primary stressor, causing reduced PST accumulation, metabolic depression, and impaired immune function. These results demonstrate the differing stress responses of GLM across developmental stages.

This thesis highlights the diverse mechanisms of toxicity exhibited by A. pacificum across multiple GLM life stages and the nuanced interactions between biotic and abiotic stressors. These insights have significantly advanced the knowledge in this field and are essential for developing mitigation strategies to protect the economic, ecological, and cultural value of GLM farming in New Zealand.

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