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The ability of a resident community to prevent or reduce the success of new colonizers is a crucial process influencing the distribution of biodiversity (Levine 2000; Byers & Noonburg 2003; Parker, Burkepile & Hay 2006; Pearson, Potter & Maron 2012). This process is known as biotic resistance and is characterized by negative interactions (such as competition and predation) between residents and the species attempting to colonize the community. Biotic resistance is rarely absolute and generally reduces the abundance, fecundity, reproductive output and/or spread of invasive species rather than completely preventing establishment (i.e. biotic containment rather than resistance sensu Levine, Adler & Yelenik 2004). The biotic resistance of a community therefore captures the cumulative effects of interactions between residents and colonizers at all stages of the invasion sequence and across multiple life-history stages.
Many organisms have complex life cycles, in which individuals undergo dramatic developmental transitions before reaching adulthood (Wilbur 1980). Accordingly, each life-history stage might be differentially susceptible to consumers, competitors and environmental variability (e.g. Boege & Marquis 2005). In addition, species interactions at one life stage can influence interactions at later stages (Osenberg, Mittelbach & Wainwright 1992; Vonesh 2005). Nonetheless, studies of biotic resistance are often restricted to interactions between residents and invaders at particular life-history stages (e.g. Hierro, Maron & Callaway 2005; Parker, Caudill & Hay 2007; but see Shea et al. 2005; Dangremond, Pardini & Knight 2010), thereby limiting our ability to accurately predict the probability of successful invasion.
Most studies of biotic resistance to date have focused on competition or predation among adults (e.g. Levine, Adler & Yelenik 2004; Parker, Burkepile & Hay 2006; Parker, Caudill & Hay 2007). The few studies that have investigated multiple mechanisms across life cycles have been in terrestrial plant systems and tend to find that competition is more intense at early stages, and herbivory at later stages (Levine, Adler & Yelenik 2004), although there are exceptions (Shea et al. 2005). It is therefore still unclear whether these mechanisms of biotic resistance operate similarly in other taxa and systems. For example, in marine invertebrates, it is the early life-history stages that are most vulnerable to predation (Osman & Whitlatch 2004), which leads to a very different prediction about the role of predation vs. competition across the ontogeny of an invader.
Variation in abundance at early life-history stages, whether the result of physical processes or biotic interactions, can leave lasting signatures that persist into the adult stages (Roughgarden, Iwasa & Baxter 1985; Levine 2000; Rius, Turon & Marshall 2009), even in the presence of counteracting processes later in life history (e.g. Levine 2000). Demographic models have been used as a way to reconcile how counteracting effects in different life-history stages influence population growth of invasive and native species (Shea & Kelly 1998; Parker 2000; Dangremond, Pardini & Knight 2010), usually based on observational data. Such longitudinal studies can enhance our understanding of the relative importance of biotic resistance mechanisms, but applying this approach might be hindered by logistical constraints in many systems. For instance, dispersal phases or small individuals can be intractable to manipulate or track in the field, while interactions among adults or sedentary stages might be equally difficult to assess under realistic conditions in the laboratory. Further, high mortality or low abundance at early life-history stages could lead to low power to detect effects at later life stages, even if they end up being important for final population size. A complementary approach to following a single cohort involves testing the effects of biotic resistance across the full life cycle using a series of independent experiments conducted on individuals collected from the same population at different life stages. While this approach makes comparisons of effects at different life stages difficult, it can narrow the focus of future efforts by identifying key stages where effects are relatively large and consistent. This may be particularly useful for species with life histories that make longitudinal studies intractable and for which demographic models are difficult to reliably parameterize.
Here, we examined how competition and predation at different life-history stages might combine to limit the invasion success of Ciona intestinalis, a marine invertebrate that has reached high abundances in many places outside its native distribution (Rius, Heasman & McQuaid 2011; Collin et al. 2013). Most experimental studies on invasion of marine communities have focused on the interactions (predation, disturbance, resource availability) that mediate the strength of competition during sessile stages (e.g. juveniles and adults; McDougall 1943; Osman 1977; Keough 1984; Stachowicz, Whitlatch & Osman 1999; Grey 2011). We broaden this approach to include all planktonic and benthic stages to examine how interactions throughout the life history combine to affect invasion success. To achieve this, we used an epibenthic system in Northern California, USA, into which Ciona has established and competes with an ecologically, developmentally and morphologically similar native, solitary ascidian – Ascidia ceratodes. This species is the dominant late-successional space-occupier in this system (Nydam & Stachowicz 2007; Edwards & Stachowicz 2011), and thus, we also examine how this resident species responds to potential limiting factors across the life history. Specifically, we quantify (i) growth rate of Ciona and Ascidia, (ii) the effects of competition between Ciona, Ascidia and other relevant native sessile species at fertilization, larval, recruit, juvenile and adult stages and (iii) predation by mobile species on larvae, new recruits and juvenile stages of Ciona and Ascidia. We expected that predation would be important in early life-history stages, as seen in other similar systems (Osman & Whitlatch 2004), but that such effects would decrease as individuals approached adulthood and reached a size refuge from predators. We also expected competition to reduce invader abundance at early stages (e.g. Levine, Adler & Yelenik 2004; Rius, Turon & Marshall 2009), but also at later stages due to space limitations and the resulting thinning (e.g. Guiñez & Castilla 2001). We compared the results of experiments at each life stage to identify the mechanisms that most likely result in the studied introduced species failing to achieve high biomass.
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Our work highlights the importance of studying biotic resistance mechanisms across multiple life-history stages that together limit invasion success. Ciona had faster growth rates than Ascidia (Fig. 2b) and was abundant in mid-successional assemblages (Fig. 2a); had we only looked at this stage, or used medium-term experiments, we might have concluded that Ciona would come to dominate our ecosystem. However, Ciona was more affected by predation across several life-history stages (Fig. 5, see 'Results' for Ascidia in Fig. S4, Supporting information) and was never the late-successional dominant (Figs. 2a and S1, Supporting information). Biotic resistance effects occurred at several stages of the life history (Table 1), but the mechanisms varied with predation being important between larval and juvenile stages, while competition appeared most important during fertilization and the adult stage. Below we discuss these mechanisms and speculate why some regions may be more resistant to invasion by Ciona. Our findings suggest that research considering a single or few life-history stages can lead to incorrect predictions about the impact or success of an introduced species.
As early as the fertilization stage, Ascidia sperm potentially interferes with the fertilization of Ciona eggs. Heterologous sperm can induce glycosidase release in ascidian eggs, which produces an early block to polyspermy that reduces fertilization (Lambert 2000). So in areas where Ascidia are abundant and Ascidia spawn at the same time as Ciona, this process could reduce Ciona fertilization success. However, we found the magnitude of negative effect of Ascidia sperm on Ciona fertilization differed among runs, possibly due to intraspecific variation in the sensitivity to heterospecific sperm. Thus, the importance of prefertilization biotic resistance is difficult to assess in this instance.
Larval behaviour can reduce settlement near competitive dominants (Grosberg 1981; Rius, Turon & Marshall 2009), so it was surprising that Ciona larvae did not alter settlement behaviours in response to the presence of heterospecific larvae or settlers. However, the lack of shared co-evolutionary history between these species means that selection for such avoidance may only be recent. Alternatively, if Ciona occupies an earlier successional stage and can reach reproductive maturity prior to being excluded by other competitors, then such selection might be weak, explaining the lack of avoidance.
Predators had a large and consistent negative effect on Ciona during the larval to the juvenile stages. A surprising result was to find that caprellid amphipods, which are commonly known to be periphyton scrapers or suspension feeders (Caine 1977), actively preyed upon ascidian larvae and settlers in the laboratory. Caprellids occur at very high densities in the field at our site, and their exclusion resulted in large increases in survival of solitary ascidians. Mesopredators are known to prey upon newly settled ascidians in other regions (Osman & Whitlatch 1995), producing major community shifts that reduce the abundance of non-native species (Osman & Whitlatch 2004). Caprellids consumed the larvae and settlers of both species intensely, although they exhibited a preference for Ciona over Ascidia (see Appendix S7, Fig S5, Supporting information). Although our observations require further testing, it appeared that recent Ciona settlers are more weakly attached to the substrate than Ascidia (authors' pers. obs.), and thus might be more easily removed by caprellids. As several-month-old juveniles, only Ciona juveniles disappeared in the field when cages were removed, despite the fact that at this time, Ciona were larger than Ascidia. At this stage, predators such as crabs or fishes likely were responsible, and the greater thickness of Ascidia tunics relative to Ciona could play a role, although we cannot rule out a contribution from chemical or other defences. The general greater susceptibility of the non-native species to a suite of resident generalist predators seen here is consistent with findings for plant–herbivore interactions (Parker, Burkepile & Hay 2006). In our case, the fast growth rate of the exotic relative to the native suggests that predator susceptibility could be due to a growth vs. defence trade-off.
The high cover that solitary ascidians reached on some panels suggests that at least some individuals survive predation, perhaps due to spatial or temporal variation in predation or predator swamping. However, Ciona abundance gradually declined while Ascidia abundance increased and the latter appeared to out-compete the former. While we did not conduct Ascidia removal experiments to test this hypothesis explicitly, other such experiments identify Ascidia as a competitive dominant in this region (Nydam & Stachowicz 2007; Edwards & Stachowicz 2011). Although the mechanisms by which Ascidia dominance is achieved are unknown, adults of Ascidia generally occupy a larger amount of primary space than Ciona because of their lateral attachment to the substrate at early life stages and thus they may be more difficult to displace. Another plausible explanation for the successional shift observed on long-term plates is that predation at the adult stage affects Ciona more than Ascidia, but this remains to be tested.
Despite our findings of multiple biotic resistance mechanisms across the complex life cycle of Ciona, resistance was not absolute as Ciona is still present. A possible explanation is that high propagule pressure (via the arrival of allochthonous propagules through shipping or from the resident Ciona adults) produces enough individuals to compensate the negative effects of biotic resistance and is able to maintain the population. Another mechanism by which competitive exclusion might be prevented involves regular disturbance (Margalef 1963; Connell 1978). Observations of old panels in Bodega Harbour revealed large aggregates of Ascidia detach when they become too heavy or fouled by epibionts (authors' personal observation), as seen in other gregarious organisms (Stachowicz et al. 2002). This process is unrelated to predation and might facilitate persistence of Ciona. Furthermore, if recruitment of Ciona coincides with times of reduced Ascidia recruitment (and low predator abundance), this could help facilitate coexistence, as occurs for competitively inferior bryozoans in this system (Edwards & Stachowicz 2011). Similarly, in terrestrial ecosystems, the performance of invaders is constrained by both biotic and abiotic factors and the interaction of these factors determines invasion success (Going, Hillerislambers & Levine 2009).
There is a growing recognition of the importance of analysing the consequences of ecological processes across multiple life-history stages (Grosberg & Levitan 1992; Boege & Marquis 2005), and as shown here, invasion biology studies could also benefit from adopting such an approach. Our results on effect sizes (Table 1) indicate that predation and to a lesser extent competition have strong negative effect on Ciona and likely contribute to the failure of Ciona to dominate Bodega Harbour assemblages. A true assessment of the relative importance of these mechanisms for Ciona population size and whether mechanisms interact synergistically or antagonistically await further experiments. However, it seems likely that given the considerable temporal and spatial variation in Ascidia recruitment (Edwards & Stachowicz 2011) and caprellid abundance (Fig. 6) that both mechanisms contribute to the biotic containment of Ciona. As a result, this species fails to dominate Bodega Harbour in the way that has been observed elsewhere. Indeed, it is possible that predation and competition play complementary roles that enhance the resident community's resistance to Ciona invasion more than either would alone. In San Francisco Bay, located just c. 70 km south of Bodega Harbour, Ascidia is rare due to fluctuating salinities associated with seasonal freshwater influx (Chang 2009), but the fast growing Ciona periodically reach very high abundances (Blum et al. 2007). Contrary to what we found in Bodega Harbour, caprellid abundance in San Francisco Bay, and also in Tomales Bay (a site close to Bodega Harbour), peaks during fall and early winter, and is extremely low during spring and summer (A.L. Chang, pers. comm.). The lack of ecologically similar resident competitors or reduced predator abundance in San Francisco could both contribute to reduced biotic resistance and increased abundance of Ciona there and elsewhere in the world where Ciona becomes dominant (Rius, Heasman & McQuaid 2011; Collin et al. 2013). Definitive answers await comparative experiments conducted across the life history of these and other potential invaders in distinct biogeographical regions. Most mechanisms of biotic resistance are far from absolute (Levine, Adler & Yelenik 2004), perhaps in part because they are spatially and temporally variable. Future work should consider this possibility and conduct factorial experiments, as well as fecundity estimates per capita at each life-history stage, to understand the relative importance of different biotic resistance mechanisms across the life history and ultimately, to evaluate their role in population growth and persistence.