Introduction

The introduction of novel species into vulnerable habitats can impact upon the balance of species and allocation of resources. Although chance and timing play an important role [1], invasion success is often attributed to biological traits such as high fecundity, short generation times and environmental tolerance, which allow introduced species to colonise new or disturbed habitats quickly [2,3]. In marine benthic communities, such as intertidal rocky shores, naturally occurring or anthropogenic disturbance can create free-space and reset successional processes [4], opening the door to non-native species and facilitating their establishment [5]. The creation of free-space by the introduction of artificial structures can have a similar effect.

The colonisation of natural habitats by an invasive species following disturbance can be offset by the presence of an established native biota [6], such that the invader occurs in limited numbers and fails to become established in meaningful abundances [7]. In contrast, newly installed artificial structures are depauperate of species, and can become quickly dominated by a limited number of species [8,9] due to features such as reduced habitat heterogeneity [9,10] or increased refugia from predators [11,12]. Artificial structures are rapidly becoming ubiquitous features of the marine environment due to urbanisation and proliferation of both artificial coastal defences and renewable energy schemes [13,14], introducing large expanses of hard substrata in areas that are otherwise sedimentary, often at the expense of natural habitats [14–16].

A primary factor in determining which species will colonise an artificial structure is its placement, and specifically the proximity (connectivity) of the structure to a source population (i.e. a rescue effect). Many marine species exhibit a planktonic larval stage [17], facilitating their dispersal away from their natal patch. Dispersal distance can be described using a combination of physical and biotic processes such as ocean circulation [18], near shore oceanography, wind [19] and planktonic duration [20]. However, spatial and temporal variation in propagule pressure [21] and multiple post-settlement processes [22] such as rate of supply [23], the timing of recruitment [1,24] and availability of resources [25] can confound outcomes such that even small-scale location differences can affect recruitment success.

Artificial structures are implicated in the spread of invasive and non-native species by acting as stepping stones to dispersal across areas of unsuitable habitat (i.e. sedimentary substrata) [26]. Morphological features of the structure can affect the type of species that are able to colonise. Construction materials can range from small cobbles to large boulders or concrete pilings [10] resulting in patches of habitat of different size and shape [12,16,27], which can affect the emergent population or community structure [9,28]. Predicting the recruitment of species to those structures and, specifically, estimating their population size is an important step in determining if a structure has the potential to act as a viable source population that can facilitate spread. If the area of habitat is too small, the population may fail to persist at that location [29], or the adult population will generate too few offspring such that its spread is unviable [30,31]. If the area of habitat is too large, there may be insufficient resources to support the population [25] or insufficient habitat heterogeneity to provide refugia from predation and/or abiotic stress [11,32].

Austrominius modestus (Darwin, 1854) has become widespread along UK coasts since its introduction in the late 1940s [33] and exhibits traits typical of invasive species [2]. Abundant on rocky shores throughout Europe [34], A. modestus can compete with native species of barnacle including Semibalanus balanoides and Balanus improvisus [34] but can also form monocultures on artificial structures [27]. One such artificial structure is the art installation, ‘Another Place’, situated on the west coast of the United Kingdom. Using this unique model system, we created disturbances of different magnitudes to test the hypothesis that small increases in initial free-space would influence the recruitment of Austrominius modestus and additionally, that these changes would affect the success and density of recruits over time. Rate of recruitment to free space plots was monitored every 2 wk over a 10 wk period and predictions of population development and growth were generated.

Methods

Results

Temporal changes in control and cumulative recruitment in 25 cm² plots

Austrominius modestus recruits were recorded on all statues in all plots at all times over the 10 wk but their abundance varied greatly over time and among plots. In control plots, there was significant variation in recruitment over time, increasing week-on-week (with the exception of between wk 6 and 8 where no significant difference was found) from 316 ± 40 per 25 cm² in wk-2 and increasing five-fold to a maximum of 1613 ± 176 per 25 cm² in wk-10 (F_4,45 = 32.45, p < 0.001). The density of A. modestus in 25 cm² cumulative plots increased in line with the bi-weekly recruitment in control plots for the first 6 wk, after which there was a significant decline in recruit density in comparison to the control plots (Figure 1a). Maximum density in 25 cm² cumulative plots reached 974 ± 78 recruits in wk-6 before declining to comparable average densities of 736 ± 29 and 785 ± 54 recruits per 25 cm² in wk-8 and 10 respectively. The decline in recruit density in cumulative plots in comparison to recruitment to control plots was best described by a non-linear 2^nd order polynomial model (R² = 0.89, p < 0.01) (Figure 2).

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Figure 1. Recruit abundances of Austrominius modestus over time.

(a) Mean recruit abundance (± SE) in 25 cm² control and cumulative plots every 2 wk (n = 10), (b) mean recruit abundance (± SE) in plots of difference area (cm²) (n = 10), and (c) mean recruit density per cm² in cumulative plots in plots of different sizes (n = 40). Letters over bars (a–d) indicate post-hoc comparison outcomes with the same letter indicating no significant difference between recruit abundance/density. All plots irrespective of initial clearance size are pooled in (b). The period when all cumulative plots were 100% colonised is shown (dotted line).

https://doi.org/10.1371/journal.pone.0074457.g001

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Figure 2. Comparative recruit density in cumulative and control plots.

Change in recruit abundance in 25 cm² control and cumulative plots. Recruitment was estimated every 2 wk using non-destructive photographic sampling and image analysis. Control plots were disturbed (cleared) every 2 wk and estimates are compared to its paired cumulative plot on the same statue. Cumulative plots were undisturbed following the initial clearance. Significant regression is shown (solid line; R² = 0.89) and dashed lines indicate 95% confidence intervals. 45^o line indicates the point where recruitment is the same in control and cumulative plots.

https://doi.org/10.1371/journal.pone.0074457.g002

Discussion

We tested the ability of an invasive species to colonise artificial habitat following the removal of adults and creation of free-space. Comparisons of control and cumulative plots of the same size revealed differences in recruitment rate dependent on the pre-existence of juvenile conspecifics within a plot and remaining free-space. While recruit abundance changed over time, firstly increasing until all free-space became occupied after 6 wk followed by a reduction in recruit abundance after 8 to 10 wk to a stable density, there was no change in recruit density with changes in plot size indicating that recruitment was not limited in this area [40]. This suggests that in other non-recruitment limited areas, a similar growth model could be used to predict the recruitment of A. modestus on newly installed artificial structures.

Gaines and Roughgarden [41] suggested that space is only important when recruitment is limited and that when the supply of larvae is saturating (non-limited), recruitment is simply a function of the amount of available space [42]. Given that space alone could be used to predict A. modestus density, this suggests that larval supply is not limited (sensu [40]). The high reproductive output of an adult A. modestus and annual presence within the plankton [35] was reflected in the high rate of recruitment and rapid colonisation of free-space within 6 wk of clearance. Recruit density was initially high and all free space was filled quickly before the number of recruits declined. Post-settlement mortality can be controlled by density-dependent processes [38,43,44] and thus by changes in propagule pressure [38,45]. After 6 wk, all available space was filled and recruit densities exceeded 40 individuals cm^-2. Recruits grew rapidly, but after 8 wk, mortality was observed in extant individuals, which was attributed to excessive crowding (Bracewell, pers. obs.) and is indicative of the availability of resources (carrying capacity) within the habitat. Competition for resources including space is a common source of mortality for recruits [38] and some sessile species can reduce mortality from space-limits by displaying morphological plasticity [46], but when progeny vastly outnumber available space, some mortality is inevitable. Maximum population size (assuming densities can be supported and food is not limited) will most likely be determined by the minimum size of an individual [47].

Whilst gregarious behaviour is an important aspect of settlement and recruitment of many barnacle species, including A. modestus [48], no obvious gregarious recruitment patterns were observed at the relatively small spatial scales tested in this study (Knights pers. obs). Gregarious behaviour is a result of chemical cues that can be short lived in the field and can be initiated in response to the presence of other barnacle species [49]. Considering the length of the sampling period, the high levels of recruitment to the statues, and the lack of any other barnacle species, any initial behavioural responses may have been obscured. Additionally, Knight-Jones [48] found that during intense periods of settlement of A. modestus the distribution of barnacles on to settlement plates was even, in contrast to gregarious clumping during periods of light settlement. Despite high post-settlement mortality and an apparent lack of aggregated settlement behaviour, recruit densities on the statues remained high (~40 individuals cm^-2) and more than double those reported on natural habitats [50]. Artificial structures are often characterised (especially when first installed) by opportunistic species, low species richness, an absence of predators and assemblages markedly different to those on natural shores [32] where higher species diversity, competition and predation can infer natural resistance to invasion [6]. The absence of a diverse or established community can lead to artificial structures being dominated by introduced species [8,51] and here this was illustrated by dense monocultures of A. modestus.

Artificial structures have been implicated as vectors of non-native species spread especially following disturbance (e.g. [26,52]). Clearly, invasive species can colonise disturbed areas quickly as shown by the rapid expansion of A. modestus throughout the UK and Europe [34] and the rate at which monocultures of A. modestus were re-established following their removal in this study. Given that artificial structures are likely to continue to proliferate and that current climate change projections suggest greater disturbance, free-space is likely to become available more frequently in the future. Correlations between disturbance and invasion success are becoming more widely documented (e.g. [5,53]) and suggest that the abundance of native species is likely to decline, although these relationships are far from straightforward [5]. Under these conditions, highly competitive and fast-colonising invasive species, such as A. modestus, are expected to increase in both abundance and distribution and the proliferation of artificial structures could act to support their expansion.

Acknowledgments

Thanks to Sefton Council for granting permission to undertake the study and also to Samson Harper and Alisha Imam for help with data collection in the field.