When is a native species invasive? Incursion of a novel predatory marsupial detected using molecular and historical data

Aim

Range expansions facilitated by humans or in response to local biotic or abiotic stressors provide the opportunity for species to occupy novel environments. Classifying the status of newly expanded populations can be difficult, particularly when the timing and nature of the range expansion are unclear. Should native species in new habitats be considered invasive pests or actively conserved? Here, we present an analytical framework applied to an Australian marsupial, the sugar glider (Petaurus breviceps), a species that preys upon on an endangered parrot in Tasmania, and whose provenance was uncertain.

Location

Tasmania, Australia.

Methods

We conducted an extensive search of historical records for sugar glider occurrences in Tasmania. Source material included museum collection data, early European expedition logs, community observation records, and peer‐reviewed and grey literature. To determine the provenance of the Tasmanian population, we sequenced two mitochondrial genes and one nuclear gene in Tasmanian animals (n = 27) and in individuals across the species' native range. We then estimated divergence times between Tasmania and southern Australian populations using phylogenetic and Bayesian analyses.

Results

We found no historical evidence of sugar gliders occurring in Tasmania prior to 1835. All Tasmanian individuals (n = 27) were genetically identical at the three genes surveyed here with those individuals being 0.125% divergent from individuals from a population in Victoria. Bayesian analysis of divergence between Tasmanian individuals and southern Australian individuals suggested a recent introduction of sugar gliders into Tasmania from southern Australia.

Main conclusions

Molecular and historical data demonstrate that Tasmanian sugar gliders are a recent, post‐European, anthropogenic introduction from mainland Victoria. This result has implications for the management of the species in relation to their impact on an endangered parrot. The analytical framework outlined here can assist environmental managers with the complex task of assessing the status of recently expanded or introduced native species.

     

Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations

Introduced species offer unique opportunities to study evolution in new environments, and some provide opportunities for understanding the mechanisms underlying macroecological patterns. We sought to determine how introduction history impacted genetic diversity and differentiation of the house sparrow (Passer domesticus), one of the most broadly distributed bird species. We screened eight microsatellite loci in 316 individuals from 16 locations in the native and introduced ranges. Significant population structure occurred between native than introduced house sparrows. Introduced house sparrows were distinguished into one North American group and a highly differentiated Kenyan group. Genetic differentiation estimates identified a high magnitude of differentiation between Kenya and all other populations, but demonstrated that European and North American samples were differentiated too. Our results support previous claims that introduced North American populations likely had few source populations, and indicate house sparrows established populations after introduction. Genetic diversity also differed among native, introduced North American, and Kenyan populations with Kenyan birds being least diverse. In some cases, house sparrow populations appeared to maintain or recover genetic diversity relatively rapidly after range expansion (<50 years; Mexico and Panama), but in others (Kenya) the effect of introduction persisted over the same period. In both native and introduced populations, genetic diversity exhibited large-scale geographic patterns, increasing towards the equator. Such patterns of genetic diversity are concordant with two previously described models of genetic diversity, the latitudinal model and the species diversity model.     

Body size and invasion success in marine bivalves

The role of body size in marine bivalve invasions has been the subject of debate. Roy et al . found that large-bodied species of marine bivalves were more likely to be successful invaders, consistent with patterns seen during Pleistocene climatic change, but Miller et al . argued that such selectivity was largely driven by the inclusion of mariculture species in the analysis and that size-selectivity was absent outside of mariculture introductions. Here we use data on non-mariculture species from the north-eastern Pacific coast and from a global species pool to test the original hypothesis of Roy et al . that range limits of larger bivalves are more fluid than those of smaller species. First, we test the hypothesis that larger bivalve species are more successful than small species in expanding their geographical ranges following introduction into new regions. Second, we compare body sizes of indigenous and non-indigenous species for 299 of the 303 known intertidal and shelf species within the marine bivalve clade that contains the greater number of non-mariculture invaders, the Mytilidae. The results from both tests provide additional support for the view that body size plays an important role in mediating invasion success in marine bivalves, in contrast to Miller et al . Thus range expansions in Recent bivalves are consistent with patterns seen in Pleistocene faunas despite the many differences in the mechanisms.     

Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird

Global anthropogenic changes are occurring at an unprecedented rate; one change, human-facilitated introduction of species outside their native range, has had significant ecological and economic impacts. Surprisingly, what traits facilitate range expansions post-introduction is relatively unknown. This information could help predict future expansions of introduced species as well as native species shifting their ranges as climate conditions change. Here, we asked whether specific behavioural and physiological traits were important in the ongoing expansion of house sparrows (Passer domesticus) across Kenya. We predicted that birds at the site of initial introduction (Mombasa, introduced approx. 1950) would behave and regulate corticosterone, a stress hormone, differently than birds at the range edge (Kakamega, approx. 885 km from Mombasa; colonized within the last 5 years). Specifically, we predicted greater exploratory behaviour and stronger corticosterone response to stressors in birds at the range edge, which may facilitate the identification, resolution and memory of stressors. Indeed, we found that distance from Mombasa (a proxy for population age) was a strong predictor of both exploratory behaviour and corticosterone release in response to restraint (but only while birds were breeding). These results suggest that certain behavioural and neuroendocrine traits may influence the ability of species to colonize novel habitats.     

Carp (Cyprinus carpio) as a powerful invader in Australian waterways

1. The invasion of carp (Cyprinus carpio L.) in Australia illustrates how quickly an introduced fish species can spread and dominate fish communities. This species has become the most abundant large freshwater fish in south‐east Australia, now distributed over more than 1 million km². 2. Carp exhibit most of the traits predicted for a successful invasive fish species. In addition, degradation of aquatic environments in south‐east Australia has given them a relative advantage over native species. 3. Derivation of relative measures of 13 species‐specific attributes allowed a quantitative comparison between carp and abundant native fish species across five major Australian drainage divisions. In four of six geographical regions analysed, carp differed clearly from native species in their behaviour, resource use and population dynamics. 4. Climate matching was used to predict future range expansion of carp in Australia. All Australian surface waters appear to be climatically suitable for carp. 5. This assessment strongly reinforces the need for immediate management of carp in Australia to include targeted control of human‐assisted dispersal, such as use of carp as bait by anglers, distribution to new locations by anglers and the use of the ‘Koi’ strain in the aquarium industry. 6. Given their historical spread, dispersal mechanisms and ecological requirements, the expansion of carp across most of the remainder of Australia is to be expected.     

Can life‐history traits predict the fate of introduced species? A case study on two cyprinid fish in southern France

1. The ecological and economic costs of introduced species can be high. Ecologists try to predict the probability of success and potential risk of the establishment of recently introduced species, given their biological characteristics.
2. In 1990 gudgeon, Gobio gobio , were released in a drainage canal of the Rhône delta of southern France. The Asian topmouth gudgeon, Pseudorasbora parva, was found for the first time in the same canal in 1993. Those introductions offered a unique opportunity to compare in situ the fate of two closely related fish in the same habitat.
3. Our major aims were to assess whether G. gobio was able to establish in what seemed an unlikely environment, to compare populations trends and life-history traits of both species and to assess whether we could explain or could have predicted our results, by considering their life-history strategies.
4. Data show that both species have established in the canal and have spread. Catches of P. parva have increased strongly and are now higher than those of G. gobio .
5. The two cyprinids have the same breeding season and comparable traits (such as short generation time, small body, high reproductive effort), so both could be classified as opportunists. The observed difference in their success (in terms of population growth and colonization rate) could be explained by the wider ecological and physiological tolerance of P. parva .
6. In conclusion, our field study seems to suggest that invasive vigour also results from the ability to tolerate environmental changes through phenotypic plasticity, rather than from particular life-history features pre-adapted to invasion. It thus remains difficult to define a good invader simply on the basis of its life-history features.     

The fifteenth- and twentieth-century colonization of the Basin of Mexico by the Great-tailed Grackle (Quiscalus mexicanus)

Historical evidence indicates that Great‐tailed Grackles colonized the Basin of Mexico from the Gulf Coast lowlands in the fifteenth century. They were probably assisted by an intentional introduction, but colonization succeeded because of anthropogenic habitat alterations over the previous two centuries. During the Colonial period, grackles withdrew from the Basin, only to recolonize it in recent decades. This withdrawal was also due probably to changes in land use, including drainage of much of the water from the Basin's lakes.     

The characteristics of invasive fishes: what has been learned so far?

Invasive species are increasingly recognized as one of the main threats to biodiversity and both an urgent need and a unique tool for ecological research. Although attempts to identify future invasive species are not new to ecology, rigorous quantitative analyses emanate mostly from the last decade. In 2001, quantitative studies dealing with the distinguishing ecological features of invasive species were reviewed but no papers on fish species were identified. Subsequently, several quantitative studies have addressed this issue for freshwater fishes, including those that have focused on California, Colorado, the Great Lakes of North America and the Iberian Peninsula. In the present paper, 12 such studies are reviewed and compared with regard to their conclusions and methodology. The issues of different invasion stages and comparison strategies, propagule pressure, information-theoretic analyses v . sequential techniques, use of phylogenetic comparative methods and spatial scale are discussed. Non-native fish transport and release are the least investigated although taxonomy and human interests seem key in these first initial stages. Establishment success, which has received more study, seems more multi-factorial, context-dependent and more mediated by species-specific life-history traits. The dispersal and impact phases are less understood, although the comparison of traits (and taxonomy) between native and invasive species and particularly its variability holds promise. The lack of data on propagule pressure and the use of sequential techniques for observational data sets with many intercorrelated variables could affect the conclusions of previous studies. Research on the dispersal, impact and particularly transport and introduction phases should be prioritized rather than establishment. All the studies identified were at temperate latitudes in the northern hemisphere; studies in other regions and comparison of different regions and multiple scales are lacking.     

Insect diversity over 36 years at a protected Sierra Nevada (California) site: towards an evaluation of the insect apocalypse hypothesis

1. Recent authors have suggested that declines of insect abundance or diversity, documented first for particular insect taxa of high interest (e.g., butterflies, bees), may apply to insect diversity more generally. This has led to an urgent call for analysis of additional longitudinal datasets to examine trends in general insect diversity.
2. Here we present a dataset gathered from 1982 to 2018 by advanced undergraduate students and graduate students enrolled in a taxonomy course that involved collecting as many insect families as possible over a 5-week period at a high-elevation protected forested site in the Sierra Nevada, California, USA.
3. The data do not support any consistent gain or loss of family-level richness between 1982 and 2018 (no linear trend); a non-linear model suggested a possible small decrease in family-level richness collected between 1986 and 1990, followed by a gradual increase from 1990 to 2018. Neither weather variables nor collector experience or skill appeared to explain among-year variation in collected insect diversity.
4. We urge caution in attempting to draw conclusions from single-site, longitudinal datasets like this one; a definitive answer to the hypothesis of a broad, global decline of insect diversity will require the joint analysis of many datasets like the one we share here.

     

Decline of Native Freshwater Fishes in a Mediterranean Watershed on the Iberian Peninsula: A Quantitative Assessment

We examined changes in the distribution of 9 native and 18 introduced freshwater fishes in the south-eastern Pyrenees watershed, Iberian Peninsula, using data from 1996, 1984–1988 and historical information. This region suffers many modifications to its freshwater ecosystems that are linked to human activity in the Mediterranean regions. Fish communities, stream physical habitat and environmental degradation were assessed at 168 sites from 11 basins in 1996. Seven native species (78%) showed decline from previous data, one of which became extirpated in the first half of the 20th century. On the other hand, introduced species are expanding. As a consequence, intact native communities are increasingly rare, declining from presence in 22% of river courses in 1984–1988 to 15% in 1996. The most typical community type is a mixture of native and introduced species occupying 30% of river courses. Stream degradation seems to be the main cause of this process because fish communities differed between degraded streams and streams suffering less impact. A principal component analysis showed that water pollution and modifications to the habitat were the two anthropogenic factors that accounted for most changes in the fish community integrity. Habitat alteration, primarily through construction of dams and water diversions, has fragmented habitats and isolated native fish communities in headwater streams. Current protection measures do not offer effective conservation of threatened species and communities. A global conservation and restoration programme from an ecosystem-based approach is essential to reverse the trend affecting native freshwater fishes in this Mediterranean region.     

Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous round goby, Neogobius melanostomus, in Great Lakes tributaries

Dispersal strategies are important mechanisms underlying the spatial distribution and colonizing ability of all mobile species. In the current study, we use highly polymorphic microsatellite markers to evaluate local dispersal and colonization dynamics of the round goby (Neogobius melanostomus), an aquatic invader expanding its range from lake to river environments in its introduced North American range. Genetic structure, genotype assignment and genetic diversity were compared among 1262 round gobies from 20 river and four lake sites in three Great Lakes tributaries. Our results indicate that a combination of short-distance diffusion and long-distance dispersal, collectively referred to as 'stratified dispersal', is facilitating river colonization. Colonization proceeded upstream yearly (approximately 500 m/year; 2005-2009) in one of two temporal replicates while genetic structure was temporally stable. Contiguous dispersal from the lake was observed in all three rivers with a substantial portion of river fish (7.3%) identified as migrants. Genotype assignment indicated a separate introduction occurred upstream of the invasion front in one river. Genetic diversity was similar and relatively high among lake and recently colonized river populations, indicating that founder effects are mitigated through a dual-dispersal strategy. The remarkable success of round goby as an aquatic invader stresses the need for better diffusion models of secondary range expansion for presumably sessile invasive species.