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Adaptive plasticity as a key for invasion success in disturbed ecosystems

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What makes for a successful ‘invasion’?

A unique natural laboratory combined with controlled experimental exposures sheds light on nitrogen pollution, homogenised global habitats and adaptations in aquatic invasive species.

According to the UN Environmental Programme’s 2023 Invasive Alien Species Report, human activities are responsible for the introduction of more than 37 000 alien species to non-native regions. Not only has this dramatically changed ecosystems, but it also costs the global economy more than EUR 400 billion annually. It is vital that we understand the adaptive mechanisms that make an introduced species become a successful ‘invader’ or perish in the process. With the support of the Marie Skłodowska-Curie Actions programme (MSCA), the INVASOMICS project combined field work with lab experiments to explore the role of adaptive plasticity in helping invasive species survive and thrive.

Preadaptation and transport selection in invasive species

“Survivors of human-driven pressures, like very high levels of nitrogen (eutrophication) in their native environments or very harsh transport conditions including hypoxia and/or excretion products, may have a unique advantage in new regions with similar conditions,” say INVASOMICS coordinator Jonas Jourdan and MSCA fellow Oriol Cano Rocabayera of Goethe University Frankfurt. INVASOMICS chose two model systems to study this preadaptation and transport selection. The first is the eastern mosquitofish (Gambusia holbrooki). Shipped from North Carolina to Spain in 1921 to combat malaria, the very few that survived were released in Extremadura (Spain) and colonised the adjacent waters. Invasive mosquitofish originating in the USA are now found in waters from Europe to Palestine and Russia. The project studied nine mosquitofish populations from three territories: invasive (Extremadura), native (Florida), and the native relatives of European invasive populations (North Carolina). INVASOMICS’ second model system was the gammarids (amphipod crustaceans). They often reach new environments in the ballast waters of ships, out-competing native populations to establish themselves successfully. Three gammarid species with different conservation status from the Main River catchment (Hessen, Germany) were added to the study to enable the investigation of species-specific different tolerances to nitrite pollution.

Natural ‘laboratory’ and controlled laboratory experiments

The wild-caught mosquitofish and gammarid organisms were exposed to non-lethal, realistic levels of nitrite, a highly toxic, naturally occurring compound of the nitrogen cycle whose levels have increased tremendously due to agricultural activity. “INVASOMICS combined the realism of using wild-caught individuals with the advantages of hypothesis testing in controlled laboratory experiments. It was exciting to find the appropriate sites, collect the live wild animals and conduct the exposure tests, and leverage advanced analytical techniques including RNA sequencing and movement tracking,” explains Cano Rocabayera.

Complexity abounds in profiling of invasive species

Whether invasive mosquitofish are more tolerant to eutrophication was difficult to confirm, given similar sublethal effects across all nine mosquitofish populations. However, living in a polluted environment was a differentiator. “Three selected genes were differentially expressed in fish from polluted versus ‘clean’ sites, perhaps indicating recent adaptations to chronic nitrogen pollution,” notes Cano Rocabayera. “Factors such as the smaller but more abundant eggs and embryos in progenitor and invasive populations could also favour rapid colonisation of a newly invaded habitat,” he adds. Gammarids, however, were a different story. Non-native gammarid Gammarus roeselii was highly tolerant to nitrogen pollution: this is the first empirical evidence that the higher tolerance of non-native species can favour colonisation. Furthermore, the species that commonly inhabits more pristine areas was particularly vulnerable. “This is alarming and shows us which waters should be prioritised for conservation measures," stresses Jourdan. “We live in times of rapidly changing environmental pressures yet have little understanding of their interactions with ecosystems. Recent differentiation between populations under different eutrophication pressure clearly plays a crucial role in an organism’s response. Our model systems can help us understand and protect our ecosystems,” Jourdan summarises.

Keywords

INVASOMICS, mosquitofish, invasive species, ecosystems, nitrogen pollution, alien species, eutrophication, Gammaridae, gammarids, adaptive plasticity, preadaptation, transport selection

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