Native and Invasive Smooth Shelled Blue Mussels (Mytilus spp.) in New Zealand: Evolutionary, Biosecurity and Aquaculture Implications

Of the principal taxa in the Mytilus edulis species complex, M. galloprovincialis, commonly known as the Mediterranean mussel, is of interest because of its capacity to invade non-native regions and to compete with native mussel species. This species excels as a dominant competitor for space in intertidal systems, displaying rapid growth rates, high reproductive capacity, and resilience to fluctuations in environmental conditions, especially temperature. These distinctive characteristics allow M. galloprovincialis to thrive even in challenging environments while occupying the niche of native species. In countries such as New Zealand where two invasive lineages of M. galloprovincialis have been reported, the success of the invasive taxa raises questions about its interaction with the endemic Perna canaliculus in aquaculture (i.e., on greenshell mussel farms) and the potential impact on the genetic integrity of the native blue mussel, M. aoteanus. This thesis focusses on research to answer some of the key questions about the success of the M. galloprovincialis invasion in New Zealand. Chapter 2 describes an investigation into the use of the phenotypic expression of shell shape (i.e., shell outline) and shell traits (i.e., morphometric landmarks) for assignment testing of individual valves against the observed genotype identified using the 16S RFLP assay. Phenotypic variation was conserved amongst species (native M. aoteanus from New Zealand – two lineages; invasive M. galloprovincialis – two lineages; native M. planulatus from Tasmania, Australia) despite extensive hybridisation between sympatrically occurring taxa. Discriminant function analysis of combined shell shape and shell trait variation returned an overall 83.6% success rate in the discrimination of the five taxa/lineages used in the study. Four of the tested shell traits; PADV (distance between posterior adductor muscle scar and ventral margin of valve), WID (width), LPR (length of the posterior retractor muscle scar), and LAR (length of the anterior retractor muscle scar) contributed the most overall differentiation in the analysis and should be prioritised when conducting measurements for rapid identification of blue mussels. Chapter 3 describes the development and optimisation of a new molecular protocol of blue mussel identification using High-Resolution Melting (HRM). The primary purpose of this research is to test a panel of single nucleotide polymorphism (SNP) loci against 16S RFLP assay designations with the end goal being the development of a SNP panel that facilitates swift molecular identification of blue mussels, with particular reference to mussels found in New Zealand. Four SNP loci (BM106B, BM38B, BM61Aand PAPM) gave an adequate level of identification to distinguish between the native New Zealand M. aoteanus and the two distinct lineages of M. galloprovincialis. PAPM consistently performed as the most informative genetic marker whilst BM61A was consistently the least informative marker of the panel. The application of these markers to blue mussel tissue samples from outside New Zealand yielded promising results, showing the capacity to discriminate between blue mussel species and species clusters from around the world. The application of these markers to environmental DNA (eDNA) samples collected from British Columbia (west coast of Canada) confirmed an incursion of Southern hemisphere blue mussels. Based on the BM38B locus, the samples detected closely aligned with the melting curve of M. aoteanus, representing the first record of Southern hemisphere Mytilus in the Northern hemisphere. Future testing and investigation of other mussel samples may be beneficial to further refine the capacity of this SNP panel to identify different species and lineages of blue mussels. Chapter 4 describes laboratory experiments to assess differences in feeding physiology between native M. aoteanus and the two lineages of M. galloprovincialis (all collected from Wellington Harbour) under various feeding conditions. Species classifications utilised a Hybrid Index method based on molecular designations from the 16S RFLP and the 4-loci SNP panel discussed in Chapter 3. The designations included Pure Native, Native Backcross, Fn Hybrid, Invasive Backcross, and Pure Invasive. No statistically significant differences in weight-standardised Clearance Rate (CRs) and Absorption Efficiency (AE) were observed across all Hybrid Index classes. These results suggest that blue mussel species in Wellington Harbour exhibit no discernible differences in CRs or AE (and therefore most likely in Net Energy Budget as well), implying functional similarity in feeding physiology. Such a result is consistent with the close evolutionary affinity of the native M. aoteanus to the invasive M. galloprovincialis. Currently however, from a managerial perspective, eradicating the invasive M. galloprovincialis is not cost-effective as ecosystem dynamics, at least in the context of CRs and AE responses, are not greatly affected by its incursion, exerting the same pressure as the native M. aoteanus. Although no differences in feeding physiology were found, this does not exclude the possibly that future generations of hybridisation will not yield deleterious effects and as such future studies should be conducted, particularly with the use of temperature as a factor which becomes more important as global temperatures rise. Chapter 5 describes collaborative research conducted in partnership with the Cawthron Institute at the Cawthron Aquaculture Park (CAP). The primary aim of this chapter is to explore how various stages of P. canaliculus development (age, size) may affect the settlement of blue mussels in controlled environments. In simulated farming experiments where P. canaliculus spat were seeded onto industry standard settlement substrate (which is the standard settlement substrate used in Greenshell™ aquaculture) and blue mussel larvae were added into suspension, the density of P. canaliculus spat did not significantly influence the density of Mytilus spp. settlement. Additionally, during these trials, it was observed that Mytilus spp. exhibited a preference for settling on fibrous coir as opposed to the stocking mesh (Mussock) used to secure P. canaliculus spat onto grow ropes. In simulated spat-catching experiments where both blue mussel larvae and P. canaliculus larvae of the same developmental age were added into suspension and allowed to settle on fibrous coir, the larval density of P. canaliculus had no effect on the settlement of Mytilus spp. larvae, and vice versa. These findings suggest that targeted mitigation of Mytilus spp. is challenging due to their preference for the industry-standard substrate and similarities in settlement behaviour with P. canaliculus. Therefore, mitigation efforts should focus on modelling the seasonal variation in Mytilus spp. larval supply and developing new strategies to address this issue effectively, minimising the overall settlement of Mytilus spp. Targeted mitigation, at this point in time, is not feasible, however modelling for seasonal variation where P. canaliculus larval density is high and blue mussel larval density is low and shifting the timing of spat catching activities may mitigate spatial competition during early stages of aquaculture. In summary, this thesis provides additional support for designating M. aoteanus as the appropriate binomial for the native New Zealand Mytilus species. Both morphometric and molecular evidence clearly distinguish M. aoteanus from the co-existing M. galloprovincialis, despite their similar feeding physiology (described here) and settlement behaviours (described elsewhere). However, ongoing hybridisation and gene flow within New Zealand could jeopardize the genetic integrity of M. aoteanus. Therefore, further research into the physiological responses and phenotypic traits of M. aoteanus is crucial to better understand the distinctions between M. aoteanus and M. galloprovincialis and to develop effective strategies for mitigating the impact of the invasive species on M. aoteanus. Finally, this research contributes to our understanding of the challenges posed by blue mussel fouling in the Greenshell™ industry. This knowledge may lead to the development of more robust tools for predicting and managing the adverse effects of this group on the industry.

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