Tolerance to hypoxia in Asian green mussels, Perna viridis, collected from a ship hull in the non-native range in eastern Indonesia

Tolerance to fluctuating environmental conditions is regarded as a key trait of successful marine invasive species as it presumably promotes survival in recipient habitats, which are often anthropogenically impacted systems such as harbours. Little is known, however, about how transport of fouling organisms on ship hulls influences the condition of the transported individuals and how this is related to their tolerance to environmental stress. We investigated the influence of transport on a ship hull on the ability of Asian green mussels, Perna viridis, to survive low concentrations of dissolved oxygen (0.5 and 1 mg/l DO). This was done by comparing the performance under stress in mussels from a eutrophic habitat in Jakarta Bay to that of mussels that had spent their lifetime on a passenger ferry crossing the Indonesian Archipelago from Jakarta in the west to West Papua in the east. We found that the mussels that came from the eutrophic habitat survived twice as long as mussels from the ferry when exposed to low oxygen concentrations. Mussels collected from the ferry, however, had a generally higher byssus production under experimental conditions, which can be attributed to their life on a moving object where they are exposed to drag. We suggest that Jakarta Bay mussels survived oxygen stress longer because they had higher Body Condition Indices than their conspecifics from the ship hull and thus had more energy available for stress compensation. These results show that transport on ship hulls can weaken the robustness of P. viridis, if the journey leads the ship through areas of low food supply for mussels, if the stopovers in eutrophic coastal ecosystems are short and if the sailing times are long (several weeks). This finding might explain the lack of establishments of P. viridis in tropical areas of Australia, from where repeated incursions have been reported

A ferry line facilitates dispersal: Asian green mussels Perna viridis (Linnaeus, 1758) detected in eastern Indonesia

While part of a single country, the Indonesian archipelago covers several biogeographic regions, and the high levels of national shipping likely facilitate transfer of non-native organisms between the different regions. Two vessels of a domestic shipping line appear to have served as a transport vector for the Asian green mussel Perna viridis (Linnaeus, 1758) between regions. This species is indigenous in the western but not in the eastern part of the archipelago, separated historically by the Sunda Shelf. The green mussels collected from the hulls of the ferries when in eastern Indonesia showed a significantly lower body condition index than similar-sized individuals from three different western-Indonesian mussel populations. This was presumably due to reduced food supply during the ships’ voyages. Although this transport-induced food shortage may initially limit the invasive potential (through reduced reproductive rate) of the translocated individuals, the risk that the species will extend its distributional range further into eastern Indonesia is high. If the species becomes widely established in eastern Indonesia, there will then be an increased risk of incursions to Australia, where the mussel is listed as a high-priority pest species

Isolation and characterization of 16 polymorphic microsatellite loci for the Asian green mussel Perna viridis (Mollusca, Mytilidae)

The Asian green mussel Perna viridis is an abundant and important ecological and economical species across its native range. However, outside its native range, this species has been considered invasive and concerns have been raised worldwide regarding its potential impacts. Despite this, little work has been done to investigate the genetics of native and/or introduced populations of this species. In the present study, we developed 16 new polymorphic microsatellite markers using the Illumina MiSeq Platform. Four to 15 alleles per locus were detected. There was no evidence of linkage disequilibrium between pairs of loci and all loci were in Hardy-Weinberg equilibrium

Establishment of a taxonomic and molecular reference collection to support the identification of species regulated by the Western Australian Prevention List for Introduced Marine Pests

Introduced Marine Pests (IMP, = non-indigenous marine species) prevention, early detection and risk-based management strategies have become the priority for biosecurity operations worldwide, in recognition of the fact that, once established, the effective management of marine pests can rapidly become cost prohibitive or impractical. In Western Australia (WA), biosecurity management is guided by the “Western Australian Prevention List for Introduced Marine Pests” which is a policy tool that details species or genera as being of high risk to the region. This list forms the basis of management efforts to prevent introduction of these species, monitoring efforts to detect them at an early stage, and rapid response should they be detected. It is therefore essential that the species listed can be rapid and confidently identified and discriminated from native species by a range of government and industry stakeholders. Recognising that identification of these species requires very specialist expertise which may be in short supply and not readily accessible in a regulatory environment, and the fact that much publicly available data is not verifiable or suitable for regulatory enforcement, the WA government commissioned the current project to collate a reference collection of these marine pest specimens. In this work, we thus established collaboration with researchers worldwide in order to source representative specimens of the species listed. Our main objective was to build a reference collection of taxonomically vouchered specimens and subsequently to generate species-specific DNA barcodes suited to supporting their future identification. To date, we were able to obtain specimens of 75 species (representative of all but four of the pests listed) which have been identified by experts and placed with the WA Government Department of Fisheries and, where possible, in accessible museums and institutions in Australasia. The reference collection supports the fast and reliable taxonomic and molecular identification of marine pests in WA and constitutes a valuable resource for training of stakeholders with interest in IMP recognition in Australia. The reference collection is also useful in supporting the development of a variety of DNA-based detection strategies such as real-time PCR and metabarcoding of complex environmental samples (e.g. biofouling communities). ThePrevention List is under regular review to ensure its continued relevance and that it remains evidence and risk-based. Similarly, its associated reference collection also remains to some extent a work in progress. In recognition of this fact, this report seeks to provide details of this continually evolving information repository publicly available to the biosecurity management community worldwid

Population-specific Survival during Exposure to Hypoxia and Heat: Global Change Increases Stress Tolerance of the Asian Green Mussel (Perna viridis)

Global change is defined by the combination of all aspects altered by the influence of human populations. Consequences for marine ecosystems are, for example, rising sea temperatures, ocean acidification, eutrophication, pollution, habitat destruction, and non-natural range expansion. Aim of my thesis was to investigate whether human impact can lead to a population-specific change in tolerance to environmental stress of a marine invertebrate. As study organism I chose the Asian green mussel (Perna viridis) a bivalve with a wide indigenous and non-indigenous distribution range in tropical and subtropical oceans. I compared tolerance to hypoxia and heat stress between two indigenous populations from Indonesia and a non-indigenous population from Hongkong. The indigenous populations came from habitats of different anthropogenic influence. The first, Jakarta Bay, is a polluted and eutrophicated site located close to a harbour. The second indigenous population came from a pristine nutrient-poor habitat in the Sunda Strait. The non-indigenous population was sampled in a polluted harbour in Hongkong where it exists under constant anthropogenic influence. In laboratory experiments in Bogor, Indonesia, I exposed the mussels to hypoxia and heat stress for three and ten days, respectively. The same experiments were conducted by my colleague, Charles Ma, in Hongkong. As an indicator of stress tolerance, I measured mortality of the mussels every day and calculated survivorship in every replicate as the sum of daily survival. Comparing stress tolerance between populations revealed that the non-indigenous, anthropogenic-influenced population from Hongkong was more tolerant to hypoxia and heat stress than the indigenous populations from Indonesia. Within the indigenous populations, stress tolerance of the mussels that came from the polluted site was higher. However, this was only statistically significant for hypoxia stress. The experiments showed that anthropogenic influence can increase the ability of a population to survive environmental stress. This can result either from adaptation to local or dispersal-related stress or from a better physical condition in eutrophicated environments. Both mechanisms may increase the potential of non-natural range expansion, lead to a shift in the fundamental niche of a species and facilitate biological invasion

Body condition indices of Asian green mussels, Perna viridis, from Indonesia

While part of a single country, the Indonesian archipelago covers several biogeographic regions, and the high levels of national shipping likely facilitate transfer of non-native organisms between the different regions. Two vessels of a domestic shipping line appear to have served as a transport vector for the Asian green mussel Perna viridis (Linnaeus, 1758) between regions. This species is indigenous in the western but not in the eastern part of the archipelago, separated historically by the Sunda Shelf. The green mussels collected from the hulls of the ferries when in eastern Indonesia showed a significantly lower body condition index than similar-sized individuals from three different western-Indonesian mussel populations. This was presumably due to reduced food supply during the ships' voyages. Although this transportinduced food shortage may initially limit the invasive potential (through reduced reproductive rates) of the translocated individuals, the risk that the species will extend its distributional range further into eastern Indonesia is high. If the species becomes widely established in eastern Indonesia, there will then be an increased risk of incursions to Australia, where the mussel is listed as a high-priority pest species

Asian green mussels (Perna viridis) transplanted between Jakarta Bay and Lada Bay, West Java, Indonesia (April 2012 - November 2013)

The Asian green mussel Perna viridis is tolerant to environmental stress, but its robustness varies between populations from habitats that differ in quality. So far, it is unclear whether local adaptations through stressinduced selection or phenotypic plasticity are responsible for these inter-population differences. We tested for the relevance of both mechanisms by comparing survival under hypoxia in mussels that were transplanted from an anthropogenically impacted (Jakarta Bay, Indonesia) to a natural habitat (Lada Bay, Indonesia) and vice versa. Mussels were retrieved 8 weeks after transplantation and exposed to hypoxia in the laboratory. Additional hypoxia tests were conducted with juvenile mussels collected directly from both sites. To elucidate possible relationships between habitat quality and mussel tolerance, we monitored concentrations of inorganic nutrients, temperature, dissolved oxygen, salinity, phytoplankton density and the mussels' body condition index (BCI) for 20 months before, during and after the experiments. Survival under hypoxia depended mainly on the quality of the habitat where the mussels lived before the hypoxia tests and only to a small degree on their site of origin. Furthermore, stress tolerance was only higher in Jakarta than in Lada Bay mussels when the BCIs were substantially higher, which in turn correlated with the phytoplankton densities. We explain why phenotypic plasticity and high BCIs are more likely the causes of populationspecific differences in hypoxia tolerance in P. viridis than stress-induced selection for robust genotypes. This is relevant to understanding the role of P. viridis as mariculture organism in eutrophic ecosystems and invasive species in the (sub)tropical world