DISCUSSION
The extent to which diversity-related processes
(diversity-invasibility hypothesis 1 ), abiotic factors
(environmental-matching hypothesis 2 ) and habitat heterogeneity
(invasion paradox hypothesis 3 ) influence the spread of
non-native aquatic macrophytes in space and time in European lakes has
received little empirical attention. We use E. canadensis as a
model system in which to address this general question using survey and
palaeolimnology data to partial out the significance of different
diversity signatures and abiotic predictors. This enabled us to test
three competing hypotheses and to demonstrate that habitat heterogeneity
has played a defining role in driving variation in E. canadensisabundance over space and time.
We found a nested spatial dependence between E. canadensisabundance and the location of sampling points in each lake (Fig. 4).
This spatial structure in the data suggests that besides water clarity
and depth there might be other unmeasured within-lake abiotic factors
(e.g. surface area and basin morphology) that also influence E.
canadensis abundance. The influence of this spatial structure in
determining E. canadensis abundance diminished with lake
isolation. Such a spatial pattern is in line with our previous studies
of the ULE system showing that eutrophication has spread unevenly across
the lakes (Salgado et al. 2018a; Salgado et al. 2019). In
particular, native macrophyte assemblages in the more eutrophic and
isolated lakes of Group 3 have become more homogenous over time,
unlike those lakes with a higher degree of connectivity to the central
lake (Salgado et al. 2018a). Macrophyte assemblages undergoing such
homogenisation may have reduced effects on E. canadensisabundance arising from any unique lake properties.
After accounting for spatial autocorrelation in the data we found that
variation in water clarity and diversity measures among the lakes
together explained other significant portions of variation in E.
canadensis abundance. In lakes with greater hydrological connectivity
(Groups 1 and 2 ), E. canadensis abundances were
less influenced by water clarity than by beta diversity. This pattern
may be explained by higher prevalence of zebra mussels in these more
connected lakes (and consequently improved water clarity; Salgado et
al. 2019a), and source sink dynamics that maintain heterogeneous
plant associations at the local scale (Salgado et al. 2018a,b). In
contrast, E. canadensis abundances in more isolated headwaters
(Group 3 ) were strongly impacted by low water clarity, floating
plant cover and native Shannon diversity (mostly driven by Digh Lough).
These drivers are consistent with biotic homogenisation in these more
degraded lakes where species-sorting processes previously dominated
(Salgado et al. 2018a).
Much of the variation in E. canadensis abundance over space and
time was related to the interplay of beta diversity and plant cover.
These two native plant community attributes have been found to better
capture macrophyte ecological change dynamics in other human-dominated
landscapes than species richness alone (Capers et al. 2007; Fu et al.
2019). The consistently positive correlation between E.
canadensis abundance and native species richness in each lake over
space and time suggests that in the ULE system, native species richness
does not confer invasibility resistance. Instead, it suggests that
native and non-native species respond similarly to within-lake and
regional habitat heterogeneity. This overwhelms any negative effects of
local diversity on E. canadensis, thus native and non-native
species coexist across the landscape (Levine 2000; Jiang & Morin 2004;
Davis et al. 2005). Although causal relationships are difficult to
discern from our observational data, we propose that locations
favourable for native macrophytes, may generally therefore also favourE. canadensis (Melbourne et al. 2007).
While the presence of diverse native macrophyte species increased the
probability of occurrence of E. canadensis within the lakes,
relationships with macrophyte beta diversity and plant cover suggest
that E. canadensis abundance is be limited by high plant cover.
This pattern was also revealed through time for lake Groups 1 and2 and in regional-scale plant invasion studies (Cleland et al.
2004; Capers et al. 2007; Davies et al. 2007). The
positive association between plant cover and E. canadensisthrough time in Group 3 lakes, likely reflects the overall
responses of macrophyte communities in these lakes to more advanced
eutrophication. Different processes may therefore control the
establishment vs. proliferation of E. canadensis . For
example, spatial and temporal environmental heterogeneity may facilitate
establishment and coexistence by providing a range of opportunities forE. canadensis to invade (Davis et al. 2005; Clark et
al. 2013). However, high native plant cover could lower resource
availability for a non-native colonist, thereby reducing opportunities
to proliferate (Cleland et al. 2004; Davis et al. 2007).
Overall, our data support hypotheses 3. Despite observingE. canadensis in all but one site, abundances in lakes were
generally low to moderate. This finding, coupled with a positive
relationship between E. canadensis and speciose communities over
space and time, indicate sufficient environmental heterogeneity within
and among-lakes to enable coexistence of native and non-native
macrophytes (Clark et al. 2013) and hence, reduced the often
described macrophyte homogenisation impacts of non-native species
(Muthukrishnan & Larkin 2020). Habitat heterogeneity was also related
to macrophyte beta diversity and plant cover variation.
Inferring the history of E. canadensis invasion
Palaeolimnological data reveal that at the time, that E.
canadensis colonised the ULE system in the late 1800s, macrophyte
communities were similar to those currently observed in Group 1lakes (Salgado et al. 2019). Simpson (1984) reported a cycle of
local colonization by E. canadensis involving establishment over
a three-year period and a subsequent rapid increase in abundance. Given
the extensive interconnection by winter flooding E. canadensisprobably spread rapidly to many sites. Following its widespread
establishment, E. canadensis probably therefore persisted at
moderate abundances for a long period, co-existing with a reported high
diversity of other submerged species across the lakes (Salgado et al.
2018a). Subsequently, post-1950s, paleoecological data indicate gradual
biotic changes associated with more eutrophic conditions that
intensified after the 1980s (Battarbee 1986) but with differential local
nutrient concentrations influencing biota (Salgado et al. 2019). These
post-1950s biotic shifts involved gradual increases in floating plant
cover and dominance of fine-leaved Potamogeton species (Fig. 5),
although some sites, such as Castle Lough and Mill Lough, have
maintained high macrophyte species diversities and abundances.
Reductions in E. canadensis abundance in the most degraded lakes
of Group 3 and negative associations with plant cover suggest a
gradual decline in abundance across the ULE system over the last three
to four decades leading to its current status of being widespread but
seldom very abundant.
Reconstructing E. canadensis abundance over time based on survey
and sediment core data may have limitations. For instance, some species
may have been unrecorded and detection in sediment cores may be biased
by preservation issues and under-representation of rare or distantly
located macrophyte taxa (Zhao et al. 2006; Clarke et al. 2014).
Our assessments of native macrophyte richness variation over space and
time probably favour the more abundant taxa. Unique lake histories could
have also introduced some discrepancies between the observed currentE. canadensis occurrence and the inferred past abundance (Bennion
et al. 2018). Nevertheless, analyses of both palaeo- and
contemporary data showed a consistent positive relationship betweenE. canadensis abundance and native plant richness in most lakes.
Plant cover, beta diversity, and Shannon diversity similarly emerged as
the main predictors in explaining the temporal variation of E.
canadensis abundance. These lines of evidence coupled with the history
of Elodea spread in the British Isles (Simpson 1984) thus allow
us to hypothesize what the general long-term patterns of E.
canadensis spread in the ULE system would as described above.
Conclusions and perspectives
E. canadensis is commonly reported in the invasion literature to
dominate over native submerged species once well established, and to
exert strong negative ecosystem engineering effects (Rørslett et al.
1986; Schwarz et al. 2015). Conditions considered to favourE. canadensis include high availability of nutrients, suitable
carbon sources, and silty substrates (Schwarz et al. 2015). Such
conditions generally prevailed across our study sites (Salgado et
al. 2019) and would support the environmental-matchinghypothesis 2 . However, our data provide a novel demonstration
that habitat heterogeneity enables the coexistence of native and
non-native plant species at landscape scales. We also found evidence for
invasion resistance in stressful environments or when native plant cover
of native species is high.
Predicting future trajectories of E. canadensis distribution and
abundance is challenging. E. canadensis has spread in the British
Isles by asexual growth, from one giant male clone (Simpson 1984). It is
therefore possible that conditions (e.g. disease) may eventually
challenge the persistence of clonal populations. Furthermore, with
globalization, unexpected and novel invasion dynamics are becoming ever
likelier (Pyšek et al. 2020). Meanwhile, like many other shallow lake
systems, the ULE system is declining through advancing eutrophication,
which, if unabated, will eventually override positive regional species
storage effects (Salgado et al. 2018a). These impacts are likely to
accelerate in forthcoming decades due to climate-driven magnification of
eutrophication effects in lakes (Birk et al. 2020). In addition,
the sibling invasive species, Elodea nuttallii, is rapidly
spreading across the ULE system and outcompeting E. canadensisunder high nutrient-enrichment conditions (Kelly et al. 2015).
Quantifying the dynamics of these two invasive species at both landscape
and temporal scales is critical, therefore, if invasion processes are to
be better understood.