The impacts of invasive ecosystem engineers in freshwaters: A review

1. Invasive species are a key stressor in freshwater ecosystems. When these species are also ecosystem engineers, their impacts are exacerbated because they modulate resource availability for a wide range of other species. The aim of this review is to synthesise existing knowledge of the impacts of invasive ecosystem engineers in freshwaters and identify knowledge gaps requiring further research.
2. The four questions explored in this review are: (1) What are the trends in research into invasive ecosystem engineers? (2) What are common negative effects of invasive ecosystem engineers in freshwater? (3) Do all impacts of invasive ecosystem engineers have negative consequences for biodiversity? (4) What happens when multiple ecosystem engineers interact? Four literature searches in Web of Science have been used to identify articles for the review and to estimate relative research effort between terrestrial, marine and freshwater ecosystems.
3. The number of research articles focusing on ecosystem engineers across all ecosystem types is increasing. Despite well-known examples of ecosystem engineer species in freshwaters (e.g. beaver), more research has focussed on terrestrial environments and invasive species.
4. The effects of invasive ecosystem engineers in freshwater systems are varied and often context dependent. Their effects on biodiversity or native ecosystem engineers are often shown to be negative; however, not all effects associated with these species are deleterious to native species. For instance, some invasive ecosystem engineers support native species through the provision of food or refuges.
5. Although freshwater ecosystems are often influenced by multiple species of ecosystem engineers (including native, invasive or both), little is known about interactions between these species or the combined effects of multiple ecosystem engineers. More research is also needed that relates the results of laboratory experiments to the field and develops methods for measuring factors that govern the impact of engineers on ecosystems. Understanding the spatial variability of the impacts of invasive ecosystem engineers as well as their interaction with anthropogenic stressors (e.g. hydrologic modification) is also necessary.
6. The lag in research surrounding invasive ecosystem engineers in freshwater compared to other biomes is concerning, as freshwater ecosystems support biodiversity disproportionate to the area they occupy. Creating predictive models of the impacts of freshwater ecosystem engineers would help anticipate the effects of invasive ecosystem engineers in freshwater and add to the broader understanding of their effects in other biomes.

     

Habitat modification inhibits conspecific seedling recruitment in populations of an invasive ecosystem engineer

Invasive species that strongly modify their physical habitat are a particular management concern. Theoretical models predict that habitat modification could speed spread rates or allow invasion of sites that would otherwise resist invasion. There are few empirical tests of this hypothesis, however. We tested whether habitat modification by invading Spartina alterniflora populations facilitates conspecific seedling recruitment and spatial spread in Willapa Bay, WA, USA. Established S. alterniflora individuals strongly modified their local physical environment. Hydrologic flow, porewater salinity, and light availability were decreased while sediment NH₄ ⁺ increased with increasing S. alterniflora stem density. The S. alterniflora seed bank was greater and spring seedlings were denser within meadows of S. alterniflora than on unvegetated tideflats. However, almost all seedling recruitment after 1 year occurred on tideflats or on meadow edge plots where the above ground S. alterniflora biomass had been removed. Instead of facilitating invasive spread, ecosystem engineering in this system appears to create conditions that inhibit local seedling recruitment. These results suggest that the influence of ecosystem engineering on invasive spread is highly contingent on the relative spatial scales of habitat modification, environmental heterogeneity, and propagule availability. Control activities could change these spatial relationships, however, inadvertently promoting invasive recruitment.     

Undaria pinnatifida: A case study to highlight challenges in marine invasion ecology and management

Marine invasion ecology and management have progressed significantly over the last 30 years although many knowledge gaps and challenges remain. The kelp Undaria pinnatifida, or “Wakame,” has a global non‐native range and is considered one of the world's “worst” invasive species. Since its first recorded introduction in 1971, numerous studies have been conducted on its ecology, invasive characteristics, and impacts, yet a general consensus on the best approach to its management has not yet been reached. Here, we synthesize current understanding of this highly invasive species and adopt Undaria as a case study to highlight challenges in wider marine invasion ecology and management. Invasive species such as Undaria are likely to continue to spread and become conspicuous, prominent components of coastal marine communities. While in many cases, marine invasive species have detectable deleterious impacts on recipient communities, in many others their influence is often limited and location specific. Although not yet conclusive, Undaria may cause some ecological impact, but it does not appear to drive ecosystem change in most invaded regions. Targeted management actions have also had minimal success. Further research is needed before well‐considered, evidence‐based management decisions can be made. However, if Undaria was to become officially unmanaged in parts of its non‐native range, the presence of a highly productive, habitat former with commercial value and a broad ecological niche, could have significant economic and even environmental benefit. How science and policy reacts to the continued invasion of Undaria may influence how similar marine invasive species are handled in the future.     

Responses of a wetland ecosystem to the controlled introduction of invasive fish

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A welcome can of worms? Hypoxia mitigation by an invasive species

Invasive species and bottom‐water hypoxia both constitute major global threats to the diversity and integrity of marine ecosystems. These stressors may interact with unexpected consequences, as invasive species that require an initial environmental disturbance to become established can subsequently become important drivers of ecological change. There is recent evidence that improved bottom‐water oxygen conditions in coastal areas of the northern Baltic Sea coincide with increased abundances of the invasive polychaetes Marenzelleria spp. Using a reactive‐transport model, we demonstrate that the long‐term bioirrigation activities of dense Marenzelleria populations have a major impact on sedimentary phosphorus dynamics. This may facilitate the switch from a seasonally hypoxic system back to a normoxic system by reducing the potential for sediment‐induced eutrophication in the upper water column. In contrast to short‐term laboratory experiments, our simulations, which cover a 10‐year period, show that Marenzelleria has the potential to enhance long‐term phosphorus retention in muddy sediments. Over time bioirrigation leads to a substantial increase in the iron‐bound phosphorus content of sediments while reducing the concentration of labile organic carbon. As surface sediments are maintained oxic, iron oxyhydroxides are able to persist and age into more refractory forms. The model illustrates mechanisms through which Marenzelleria can act as a driver of ecological change, although hypoxic disturbance or natural population declines in native species may be needed for them to initially become established. Invasive species are generally considered to have a negative impact; however, we show here that one of the main recent invaders in the Baltic Sea may provide important ecosystem services. This may be of particular importance in low‐diversity systems, where disturbances may dramatically alter ecosystem services due to low functional redundancy. Thus, an environmental problem in one region may be either exacerbated or alleviated by a single species from another region, with potentially ecosystem‐wide consequences.     

Characterization of microsatellite loci in the European green crab (Carcinus maenas)

Carcinus maenas (Decapoda: Portunidae) has proven a highly successful invasive marine species whose potential economic and ecological impacts are of great concern worldwide. Here, we characterize 14 polymorphic microsatellite loci in C. maenas and its sister species Carcinus aestuarii. These markers will prove useful for fine‐scale genetic analyses of native and introduced populations, for assessment of the sources and routes of invasion and for evaluation of post‐invasion population dynamics.     

Effects of invasive clam (Corbicula fluminea) die‐offs on the structure and functioning of freshwater ecosystems

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Conceptualising the interactive effects of climate change and biological invasions on subarctic freshwater fish

Climate change and species invasions represent key threats to global biodiversity. Subarctic freshwaters are sentinels for understanding both stressors because the effects of climate change are disproportionately strong at high latitudes and invasion of temperate species is prevalent. Here, we summarize the environmental effects of climate change and illustrate the ecological responses of freshwater fishes to these effects, spanning individual, population, community and ecosystem levels. Climate change is modifying hydrological cycles across atmospheric, terrestrial and aquatic components of subarctic ecosystems, causing increases in ambient water temperature and nutrient availability. These changes affect the individual behavior, habitat use, growth and metabolism, alter population spawning and recruitment dynamics, leading to changes in species abundance and distribution, modify food web structure, trophic interactions and energy flow within communities and change the sources, quantity and quality of energy and nutrients in ecosystems. Increases in temperature and its variability in aquatic environments underpin many ecological responses; however, altered hydrological regimes, increasing nutrient inputs and shortened ice cover are also important drivers of climate change effects and likely contribute to context‐dependent responses. Species invasions are a complex aspect of the ecology of climate change because the phenomena of invasion are both an effect and a driver of the ecological consequences of climate change. Using subarctic freshwaters as an example, we illustrate how climate change can alter three distinct aspects of species invasions: (1) the vulnerability of ecosystems to be invaded, (2) the potential for species to spread and invade new habitats, and (3) the subsequent ecological effects of invaders. We identify three fundamental knowledge gaps focused on the need to determine (1) how environmental and landscape characteristics influence the ecological impact of climate change, (2) the separate and combined effects of climate and non‐native invading species and (3) the underlying ecological processes or mechanisms responsible for changes in patterns of biodiversity.     

Control of invasive marine invertebrates: an experimental evaluation of the use of low salinity for managing pest corals (Tubastraea spp.)

This study investigated the use of low salinity as a killing agent for the invasive pest corals Tubastraea coccinea and Tubastraea tagusensis (Dendrophylliidae). Experiments investigated the efficacy of different salinities, the effect of colony size on susceptibility and the influence of length of exposure. Experimental treatments of colonies were carried out in aquaria. Colonies were then fixed onto experimental plates and monitored in the field periodically over a period of four weeks. The killing effectiveness of low salinity depended on the test salinity and the target species, but was independent of colony size. Low salinity was fast acting and prejudicial to survival: discoloration, necrosis, fragmenting and sloughing, exposure of the skeleton and cover by biofoulers occurred post treatment. For T. tagusensis, 50% mortality (LC₅₀) after three days occurred at eight practical salinity units (PSU); for T. coccinea the LC₅₀ was 2?PSU. Exposure to freshwater for 45–120?min resulted in 100% mortality for T. tagusensis, but only the 120?min period was 100% effective in killing T. coccinea. Freshwater is now routinely used for the post-border management of Tubastraea spp. This study also provides insights as to how freshwater may be used as a routine biosecurity management tool when applied pre-border to shipping vectors potentially transporting non-indigenous marine biofouling species.     

Unexpected resilience of a seagrass system exposed to global stressors

Despite a growing interest in identifying tipping points in response to environmental change, our understanding of the ecological mechanisms underlying nonlinear ecosystem dynamics is limited. Ecosystems governed by strong species interactions can provide important insight into how nonlinear relationships between organisms and their environment propagate through ecosystems, and the potential for environmentally mediated species interactions to drive or protect against sudden ecosystem shifts. Here, we experimentally determine the functional relationships (i.e., the shapes of the relationships between predictor and response variables) of a seagrass assemblage with well‐defined species interactions to ocean acidification (enrichment of CO₂) in isolation and in combination with nutrient loading. We demonstrate that the effect of ocean acidification on grazer biomass (Phyllaplysia taylori and Idotea resecata) was quadratic, with the peak of grazer biomass at mid‐pH levels. Algal grazing was negatively affected by nutrients, potentially due to low grazer affinity for macroalgae (Ulva intestinalis), as recruitment of both macroalgae and diatoms were favored in elevated nutrient conditions. This led to an exponential increase in macroalgal and epiphyte biomass with ocean acidification, regardless of nutrient concentration. When left unchecked, algae can cause declines in seagrass productivity and persistence through shading and competition. Despite quadratic and exponential functional relationships to stressors that could cause a nonlinear decrease in seagrass biomass, productivity of our model seagrass—the eelgrass (Zostera marina)‐ remained highly resilient to increasing acidification. These results suggest that important species interactions governing ecosystem dynamics may shift with environmental change, and ecosystem state may be decoupled from ecological responses at lower levels of organization.     

The ecological importance of crocodylians: towards evidence‐based justification for their conservation

Large‐bodied predators are well represented among the world's threatened and endangered species. A significant body of literature shows that in terrestrial and marine ecosystems large predators can play important roles in ecosystem structure and functioning. By contrast, the ecological roles and importance of large predators within freshwater ecosystems are poorly understood, constraining the design and implementation of optimal conservation strategies for freshwater ecosystems. Conservationists and environmentalists frequently promulgate ecological roles that crocodylians are assumed to fulfil, but often with limited evidence supporting those claims. Here, we review the available information on the ecological importance of crocodylians, a widely distributed group of predominantly freshwater‐dwelling, large‐bodied predators. We synthesise information regarding the role of crocodylians under five criteria within the context of modern ecological concepts: as indicators of ecological health, as ecosystem engineers, apex predators, keystone species, and as contributors to nutrient and energy translocation across ecosystems. Some crocodylians play a role as indicators of ecosystem health, but this is largely untested across the order Crocodylia. By contrast, the role of crocodylian activities in ecosystem engineering is largely anecdotal, and information supporting their assumed role as apex predators is currently limited to only a few species. Whether crocodylians contribute significantly to nutrient and energy translocation through cross‐ecosystem movements is unknown. We conclude that most claims regarding the importance of crocodylians as apex predators, keystone species, ecosystem engineers, and as contributors to nutrient and energy translocation across ecosystems are mostly unsubstantiated speculation, drawn from anecdotal observations made during research carried out primarily for other purposes. There is a paucity of biological research targeted directly at: understanding population dynamics; trophic interactions within their ecological communities; and quantifying the short‐ and long‐term ecological impacts of crocodylian population declines, extirpations, and recoveries. Conservation practices ideally need evidence‐based planning, decision making and justification. Addressing the knowledge gaps identified here will be important for achieving effective conservation of crocodylians.     

The Function of Marine Critical Transition Zones and the Importance of Sediment Biodiversity

Estuaries and coastal wetlands are critical transition zones (CTZs) that link land, freshwater habitats, and the sea. CTZs provide essential ecological functions, including decomposition, nutrient cycling, and nutrient production, as well as regulation of fluxes of nutrients, water, particles, and organisms to and from land, rivers, and the ocean. Sediment-associated biota are integral to these functions. Functional groups considered essential to CTZ processes include heterotrophic bacteria and fungi, as well as many benthic invertebrates. Key invertebrate functions include shredding, which breaks down and recycles organic matter; suspension feeding, which collects and transports sediments across the sediment–water interface; and bioturbating, which moves sediment into or out of the seabed. In addition, macrophytes regulate many aspects of nutrient, particle, and organism dynamics above- and belowground. Animals moving within or through CTZs are vectors that transport nutrients and organic matter across terrestrial, freshwater, and marine interfaces. Significant threats to biodiversity within CTZs are posed by anthropogenic influences; eutrophication, nonnutrient pollutants, species invasions, overfishing, habitat alteration, and climate change affect species richness or composition in many coastal environments. Because biotic diversity in marine CTZ sediments is inherently low whereas their functional significance is great, shifts in diversity are likely to be particularly important. Species introductions (from invasion) or loss (from overfishing or habitat alteration) provide evidence that single-species changes can have overt, sweeping effects on CTZ structure and function. Certain species may be critically important to the maintenance of ecosystem functions in CTZs even though at present there is limited empirical evidence that the number of species in CTZ sediments is critical. We hypothesized that diversity is indeed important to ecosystem function in marine CTZs because high diversity maintains positive interactions among species (facilitation and mutualism), promoting stability and resistance to invasion or other forms of disturbance. The complexity of interactions among species and feedbacks with ecosystem functions suggests that comparative (mensurative) and manipulative approaches will be required to elucidate the role of diversity in sustaining CTZ functions. Received 25 February 2000; accepted 31 January 2001.     

High abundance of an invasive species gives it an outsized ecological role

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Higher photosynthesis,nutrient‐ and energy‐use efficiencies contribute to invasiveness of exotic plants in a nutrient poor habitat in northeast China

The roles of photosynthesis‐related traits in invasiveness of introduced plant species are still not well elucidated, especially in nutrient‐poor habitats. In addition, little effort has been made to determine the physiological causes and consequences of the difference in these traits between invasive and native plants. To address these problems, we compared the differences in 16 leaf functional traits related to light‐saturated photosynthetic rate (P_max) between 22 invasive and native plants in a nutrient‐poor habitat in northeast China. The invasive plants had significantly higher P_max, photosynthetic nitrogen‐ (PNUE), phosphorus‐ (PPUE), potassium‐ (PKUE) and energy‐use efficiencies (PEUE) than the co‐occurring natives, while leaf nutrient concentrations, construction cost (CC) and specific leaf area were not significantly different between the invasive and native plants. The higher PNUE contributed to higher P_max for the invasive plants, which in turn contributed to higher PPUE, PKUE and PEUE. CC changed independently with other traits such as P_max, PNUE, PPUE, PKUE and PEUE, showing two trait dimensions, which may facilitate acclimation to multifarious niche dimensions. Our results indicate that the invasive plants have a superior resource‐use strategy, i.e. higher photosynthesis under similar resource investments, contributing to invasion success in the barren habitat.     

Impacts of two invasive mollusks, <Emphasis Type="Italic">Rapana venosa</Emphasis> (Gastropoda) and <Emphasis Type="Italic">Corbicula fluminea</Emphasis> (Bivalvia), on the food web structure of the Río de la Plata estuary and nearshore oceanic ecosystem

This paper quantifies the impacts of two invasive species, Rapana venosa (Gastropoda, Muricidae) and Corbicula fluminea (Bivalvia, Corbiculidae), in the food web of the Río de la Plata estuary and adjacent nearshore oceanic ecosystem. We analyzed certain functional traits of these mollusks assessed by a mass balance trophic model previously constructed for the years 2005–2007. This model incorporates 37 functional groups: three marine mammals species, one coastal bird, 17 fishes, 12 invertebrates, two zooplankton, one phytoplankton, and detritus. The model also includes 5 fishing fleets operating in the area. The results showed that the two invasive species affect multiple ecosystem components both directly and indirectly. R. venosa and the whitemouth croaker, Micropogonias furnieri, exhibited a high level of niche overlap (91%), while C. fluminea exhibited a high level of niche overlap with Mytilidae (94%), which suggests in both cases high levels of competition for similar resources. R. venosa had mixed trophic impacts but exhibited a predominantly top down effect on most bivalves. R. venosa could be a threat to natural resources in the area including to the fishing fleets. C. fluminea negatively influenced phytoplankton and detritus biomass and its positive effects on higher trophic level groups suggest a central bottom-up role in the food web as a bentho-pelagic coupler. Both species had negative impacts on the five fleets modeled, showing that the effects of these invasive species could extend to the socio-economic sector.     

Is salinity an obstacle for biological invasions?

Invasions of freshwater habitats by marine and brackish species have become more frequent in recent years with many of those species originating from the Ponto‐Caspian region. Populations of Ponto‐Caspian species have successfully established in the North and Baltic Seas and their adjoining rivers, as well as in the Great Lakes–St. Lawrence River region. To determine if Ponto‐Caspian taxa more readily acclimatize to and colonize diverse salinity habitats than taxa from other regions, we conducted laboratory experiments on 22 populations of eight gammarid species native to the Ponto‐Caspian, Northern European and Great Lakes–St. Lawrence River regions. In addition, we conducted a literature search to survey salinity ranges of these species worldwide. Finally, to explore evolutionary relationships among examined species and their populations, we sequenced the mitochondrial cytochrome c oxidase subunit I gene (COI) from individuals used for our experiments. Our study revealed that all tested populations tolerate wide ranges of salinity, however, different patterns arose among species from different regions. Ponto‐Caspian taxa showed lower mortality in fresh water, while Northern European taxa showed lower mortality in fully marine conditions. Genetic analyses showed evolutionary divergence among species from different regions. Due to the geological history of the two regions, as well as high tolerance of Ponto‐Caspian species to fresh water, whereas Northern European species are more tolerant of fully marine conditions, we suggest that species originating from the Ponto‐Caspian and Northern European regions may be adapted to freshwater and marine environments, respectively. Consequently, the perception that Ponto‐Caspian species are more successful colonizers might be biased by the fact that areas with highest introduction frequency of NIS (i.e., shipping ports) are environmentally variable habitats which often include freshwater conditions that cannot be tolerated by euryhaline taxa of marine origin.     

Tolerance to salinity and thermal stress by larvae and adults of the serpulid annelid Ficopomatus enigmaticus

The serpulid annelid Ficopomatus enigmaticus is a widely distributed invader of shallow‐water, brackish habitats in subtropical and temperate regions, where it has numerous damaging ecological and economic effects. Its distributional pattern suggests that temperature and salinity play important roles in limiting its distribution, but because other factors often covary with these, drawing strong conclusions from these patterns is difficult. In an effort to more clearly identify the effects of these factors, we examined tolerance to acute thermal (16–28°C) and salinity (0–35 psu) stress by larvae (5‐day exposure, unfed) and adults (14‐day exposure, unfed) of F. enigmaticus in the laboratory experiments. Larvae showed higher mortality at the highest temperature tested 28°C; adult survival was unaffected by temperature. Neither larvae nor adults survived exposure to pure freshwater (0 psu), but survived well at salinities ranging 3.5–35 psu. In addition, high salinity did not slow tube growth in adults. These results suggest that salinity stress, in particular, does not directly limit the distribution of F. enigmaticus to low‐salinity habitats. Experimental work on the distribution of F. enigmaticus is uncommon in the literature, but is likely needed to identify the abiotic or biotic factors that limit the distribution of this frequently invasive species.     

COASTAL DIATOM‐ENVIRONMENT RELATIONSHIPS IN THE BRACKISH BALTIC SEA1

High‐quality calibration data sets are required when diatom assemblages are used for monitoring ecological change or reconstructing palaeo‐environments. The quality of such data sets can be validated, in addition to other criteria, by the percentage of significant unimodal species responses as a measure of the length of an environmental gradient. This study presents diatom‐environment relationships analyzed from a robust data set of diatom communities living on submerged stones along a 2,000 km long coastline in the Baltic Sea area, including 524 samples taken at 135 sites and covering a salinity gradient from 0.4 to 11.4. Altogether, 487 diatom taxa belonging to 102 genera were recorded. Detrended canonical correspondence analysis showed that salinity was the overriding environmental factor regulating diatom community composition, while exposure to wave action and nutrient concentrations were of secondary importance. Modeling the abundances of the 58 most common diatom taxa yielded significant relationships with salinity for 57 taxa. Twenty‐three taxa showing monotonic responses were species with optimum distributions in freshwater or marine waters. Thirty‐four taxa showing unimodal responses were brackish‐water species with maximum distributions at different salinities. Separate analyses for small (cell biovolume <1,000 μm³) and large (≥1,000 μm³) taxa yielded similar results. In previous studies along shorter salinity gradients, large and small epilithic diatom taxa responded differently. From our large data, we conclude that counts of large diatom taxa alone seem sufficient for indicating salinity changes in coastal environments with high precision.