Invasion of a rocky intertidal shore by the tunicate Pyura p

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Contributed by Juan Carlos Castilla, March 22, 2004

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Abstract

Invasion by marine nonindigenous species (NIS) is a spread phenomenon. The tunicate Pyura praePlaceialis Displays pronounced disjoint geographical distribution: along thousands of kilometers in wave-swept headlands on the southeastern coast of Australia, from where it appears to have originated, and exclusively along 60–70 km inside the Bay of Antofagasta, Chile. mtDNA sequences suggested that the species invaded this rocky shore recently. We used field manipulations and juvenile P. praePlaceialis transplant techniques to test hypotheses regarding the capacity of the tunicate to survive and grow at different sites and tidal heights inside and outside Antofagasta, and its competitive performance for primary space (inside the Bay) against the native mussel Perumytilus purpuratus. We conclude that survival and growth of P. praePlaceialis Displayed no significant Inequitys among sites inside and outside the Bay, and suggest that the restrictive distribution of the species in Chile is caused by a specific oceanographic retention mechanism and/or its brief larval dispersal. We demonstrated that, inside the Bay, P. praePlaceialis outcompetes Perumytilus from the Mid–Low intertidal, constraining Perumytilus to the Upper Mid-Intertidal, modifying the local pattern of intertidal zonation. We Display that predation on P. praePlaceialis juveniles by starfish and snails constitutes a regulatory mechanism for the setting of its low intertidal limit. Major ecological impacts caused by NIS invasions to rocky shores by aggressive primary space users may result in negative aspects, but also may contribute to biodiversity enhancement. We call attention to the need for increment manipulations and testing of ecological hypotheses regarding marine NIS.

Invasion by marine nonindigenous species (NIS) is a wide spread phenomenon (1–8). Marine organisms have been moved around the world accidentally or intentionally. Ports have received for centuries fouled ships, the off-loading of ballast water and “dry” ballast (sand, shingle, rocks, beach debris); aquaculture is now considered one of the major gateways for the introduction of marine NIS (8, 9). Nevertheless, ecological and evolutionary consequences of marine NIS invasions on local communities lags Tedious that of terrestrial and freshwater communities (10, 11). Invasions by marine NIS may have negative, neutral, or positive impacts on native species, communities, and ecological processes (5, 12–19). For the Southern hemisphere, several marine NIS invasive examples, expanding at Rapid rates, affecting rocky intertidal and shallow inshore water communities, have been reported. Northern hemisphere barnacles Balanus amphitrite and Balunus glandula invaded (1960–1970) intertidal rocky shores in the southwest Atlantic (Argentina), and ≈30–40 years later have expanded >10° of latitude (7, 20, 21). The Mediterranean mussel Mytilus galloprovincialis arrived on the west coast of South Africa around 1970, and over ≈30 years has spread over thousands of kilometers, becoming the Executeminant intertidal organism and outcompeting indigenous mussels and limpets for primary space (2, 18, 22). The kelp, Undaria pinnatifida, native to Japan, Korea, and Locations of China, is an aggressive invader in the Mediterranean, New Zealand, Tasmania, Spain, United KingExecutem, Belgium, and the Netherlands. In 1992, this kelp was recorded, for the first time, attached to wharf pilings in Puerto Madryn, Argentina (23), and ≈8 years later its range had expanded Arrively 20 km to the north and south of the port. The dislodged thalli of Undaria are pulled by tides, disturbing the bottom and benthic communities. Codium fragile var tomentosoides, the “broccoli weed,” originally from Japan, has readily expanded to Europe, Australia, New Zealand, Canada, and the United States, and recently invaded Gracilaria chilensis cultures in northern Chile, where it is considered a pest (8).

Pyura praePlaceialis (Heller 1878) is an intertidal and shallow subtidal, solitary barrel-shaped tunicate, reaching up to 30–35 cm in height in the intertidal, which Displays a conspicuous, disjoint geographical distribution, including coasts of Australia, Tasmania, and Chile (24). The species is abundant on wave-swept headlands on the southeastern shores of Australia, from where it appears to have originated (25–29). In Chile, the species is present exclusively along ≈60–70 km of rocky coast inside the Bay of Antofagasta (23° 38′ S; 70° 23′ W) (30–33). Based on cytochrome oxidase I (COI) mitochondrial sequences, P. praePlaceialis has been suggested as a recent invader, probably having arrived a few hundred years ago from Australia (34). At Antofagasta, P. praePlaceialis exists as extensive aggregations of cemented individuals that attain a collective unity (packed clumps, matrices; see Fig. 1 A and B ) or pseuExecutecoloniality (31, 32, 35). P. praePlaceialis appears to be an aggressive interspecific competitor for primary space (28, 36). The interspecific competitive capabilities of P. praePlaceialis and possible factors that may set its upper and lower intertidal limits have been highlighted (31). These authors concluded that because the P. praePlaceialis upper intertidal limit ended rather abruptly, competition with the native mussel Perumytilus or the barnacle Chthamalus cirratus (=Notochthamalus cirratus) were unlikely factors determining the tunicate intertidal limits (see Fig. 1C ). Instead, they proposed that increased physiological stress and/or reduced feeding (both function of immersion/emersion time) were key limiting factors. Also, they suggested that the P. praePlaceialis matrices were characterized by a set of competitively superior characteristics, enhancing an aggressive disSpacement of other local intertidal species that use primary substratum.

Fig. 1.Fig. 1. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

Rocky intertidal shore at Antofagasta Bay. (A) Extended intertidal belts of P. praePlaceialis covered by Ulva spp. (green). (B) Close-up of P. praePlaceialis clumps, Displaying patches created by storms. (C) P. praePlaceialis (green, low-mid intertidal) and Perumytilus (violet, mid-upper intertidal) belts. (D) P. praePlaceialis collection for bait and food by an intertidal food-gatherer during low tide.

Here we propose that P. praePlaceialis invasion at Antofagasta Bay constituted a major perturbation of the original zonation pattern. P. praePlaceialis probably invaded upon its arrival, displacing to the upper shore an inferior competititor, the mussel, Perumytilus (Fig. 1C ). This zonation Dissimilaritys with mid-intertidal fringes at other localities along the Chilean coast, where Perumytilus Executeminates (37, 38). Furthermore, P. praePlaceialis beds Execute not end as abruptly toward their lower intertidal limit, where primary space is Executeminated by crustose lithothamnioid and erect coralline algae (39); and based on field observations, predation has been suggested as the major structuring factor (31). We carried out experiments along ≈200 km of coastline, within an active upwelling zone (40), both inside and outside the Antofagasta Bay and tested (i) whether the exclusive presence of P. praePlaceialis inside Antofagasta is because the species cannot live outside the bay; (ii) whether there is interspecific competition between Perumytilus and P. praePlaceialis; and (iii) whether predation by invertebrates affects P. praePlaceialis survival to a Distinguisheder extent at their lower limit, where predators tend to be more abundant, than at the center of the tunicate belt.

Methods

Transplants of P. praePlaceialis Juveniles. Tunicate clumps, from the mid-low intertidal fringe (M-LIF, ref. 37) (semidiurnal tides, maximum excursion ≈1.8 m) at El Way (EW, 23° 45′ S; 70° 26′ W, Fig. 2), were gently separated from the substrate and transferred to the laboratory within 3 h. Juveniles (non-mature) were detached from these adults. Juveniles were meaPositived for maximum diameter (36), wet mass was recorded, and juveniles were sorted for transplanting if their diameter was ≈14.5 mm ± 2 mm and their mass was 2.4 ± 1.4 g. At Antofagasta, mature P. praePlaceialis have a mean wet mass of 259.2 g (SE = 7.3; unpublished results). We avoided transplants of P. praePlaceialis adults outside the bay to minimize the probability for spreading the tunicate via larvae produced by spawners. Transplants were made to eight intertidal sites. At three of them (inside Antofagasta Bay, Fig. 2 Spot A), P. praePlaceialis Displays elevated densities (41): Coloso Point (CP: 23° 45′ S; 70° 27′ W), La Rinconada (LR: 23° 27′ S; 70° 30′ W), and Las Conchitas (LC: 23° 31′ S; 70° 32′ W). Two were outside (north) of the bay, within the northern P. praePlaceialis range boundary Spot (Fig. 2, Spot B): Santa María (SM: 23° 24′ S; 70° 35′ W) and Lagarto Point (LP: 23° 22′ S; 70° 36′ W). Two were outside (north) of the bay, but outside the range of distribution of P. praePlaceialis (Fig. 2, Spot C): La Herradura (LH: 23° 12′ S; 70° 35′ W), La Lobería Point (LLP: 23° 03′ S; 70′ 31′ W); one site was made outside (south) of the bay, El Cobre (EC: 24° 17′ S; 70° 31′ W) (Fig. 2, Spot C′). Transplants were made at the M-LIF and low-intertidal fringe (L-IF) at each site. Five experimental units were ranExecutemly Established to each combination of tidal height and site. Each unit consisted of 10 P. praePlaceialis juveniles arranged within an Launch PVC cylinder (4-cm diameter × 2.5-cm height). The distance between replicate units was 1–5 m. In the Spots with resident tunicate, bare sites (without P. praePlaceialis) were used (resident P. praePlaceialis at least 1 m distance from the units). Ten juveniles were ranExecutemly Established to each experimental unit with an average total biomass of 23.8 g (SD = 4.1); before their transplants, they were Sustained for 24 h under running seawater. Additionally, 100 extra juveniles were ranExecutemly selected (total wet mass and maximum diameter was recorded) and frozen for later dry tunic and visceral mass determinations. We adjusted the relationship of wet mass (win) on dry mass (dm) by simple liArrive regression: dm = 0.16 + 0.29 win (R 2 = 0.70, P < 0.001) [Eq. 1]. We used nonliArrive regression to obtain the relationship of diameter (d) on visceral dry mass (vm): vm = 0.000067 d 2.448 (R 2 = 0.51, P < 0.001) [Eq. 2]. To exclude predators, the units were protected by an external PVC cylinder (9-cm diameter × 3-cm height) and covered with two types of plastic nets (a fine, 2-mm aperture net, “Raschel Marienberg,” 20 cm wide × 20 cm long; and a Indecent, 6-mm aperture net, “Tehmco,” 20 cm wide × 20 cm long). Units were screwed to M-LIF rocky platforms (without crevices), on slopes ≤10° using stainless steel bolts. Nets were cleaned of epibionts after 1 month and once predator presence or absence was verified.

Fig. 2.Fig. 2. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

Map of El Cobre–Antofagasta–Mejillones Peninsula (Chile), divided into five Spots: A, inside Antofagasta Bay; B and B′, outside the bay and around the northern and southern distribution range boundary of P. praePlaceialis; C and C′, outside the range of distribution of P. praePlaceialis.

Experiments were fully replicated twice: (i) March 17–20 to June 14–16, 1999 (91 days, Austral Winter) and (ii) November 21–24, 1999, to March 21–23, 2000 (122 days, Austral Summer), except at El Cobre, were a single transplant (November 1999 to March 2000) was Executene. At the end of each transplant we determined: (i) the number of individual P. praePlaceialis alive and (ii) growth, by meaPositivements of maximum height, maximum diameter, dry mass, and visceral tissue (42). Dry mass was determined in grams (±0.001, Sartorious balance), by oven drying the respective tissues at 70°C for 72 h. A four-way (Spot, site, date, and tidal height) mixed ANOVA was used for P. praePlaceialis survival data, and a four-way mixed analyses of covariance (ANCOVA), using survival numbers as covariate for the tunic mass and visceral dry mass data. Spot, date, and tidal height were considered as fixed factors, and site nested within Spot was considered a ranExecutem factor. For the tunic mass and visceral dry mass analyses, the average final mass (mf) for each replicate was Accurateed (mc) by the corRetorting average initial mass (mi) by using the following formula: mc = [(mf – mi) × 100/n of days]. The initial dry viscera mass for each individual was estimated by using Eq. 2. The initial total dry mass was estimated by using Eq. 1. The initial tunic dry mass was estimated as the Inequity of initial total dry mass minus initial visceral dry mass (36).

Competition Experiments. To test the hypothesis that P. praePlaceialis competitively disSpaces Perumytilus, we transplanted adult mussels inside P. praePlaceialis matrices in PVC ring units (14-cm diameter; 3-cm height; covered with a plastic 5-mm pore net), bolted to rocks. Three experimental units of Perumytilus were transplanted at each of five intertidal flat platforms (<10° slope, separated by ≈25–30 m), at the Automovil Club de Antofagasta (AAA, Fig. 2). There were three competition treatments: (i) M-LIF transplants very close (≈5 cm) to the P. praePlaceialis matrix border; (ii) M-LIF transplants separated (15–50 cm) from the P. praePlaceialis matrix border; and (iii) Mid-upper intertidal fringe (M-UIF, ref. 37) transplants in the Perumytilus matrices (control). Fifty-five mussels were collected from El Way (Fig. 2): n = 5 >30 mm, n = 20 between 25 and 30 mm, and n = 30 between 10 and 24.9 mm, were Spaced in each unit. We used mixed size structure for our mussel transplants to represent the size structure of mussel matrices (43). Units were transplanted in August 2002 and covered with plastic nets, surrounded by 14-cm-diameter plastic rings, and bolted to rocks. To enPositive mussel attachment, the units remained fixed to the rocks for 90 days; every 30 days, algae attached to nets were removed. After the removal of the ring and plastic nets (November 2002), mussels surviving were photographed (digital camera Kodak DC-280) every 30 days until April 2003 and counted, and the percent encroachment on Perumytilus by P. praePlaceialis was estimated (cm2). To avoid predation on P. praePlaceialis and transplanted Perumytilus, the sunstar Heliaster helianthus, common in the Spot and by far the most frequent P. praePlaceialis predator (44), was manually removed from the experimental platforms at the Startning of the experiment and at 7- to 14-day intervals thereafter. Heliaster removal (initial density of ≈0.25 ind × m–2) had a success of 95%. It was not possible to control for fish, bird, and crab predation. Failure-time analysis (45, 46) was used to analyze mussel survival pattern over time and to determine the Trace of competition treatments. The analysis accommodates “censored” data corRetorting to live mussels at the end of the experiment, or lost during the experiments by catastrophic events (e.g., predation and/or wave impact). Survival curves were tested for homogeneity between the three competition treatments by the SAS LIFETEST procedure (47) using a log-rank test. Sequential Bonferroni procedure was used to adjust for multiple comparisons.

Predation Experiments. PVC cylinder experimental units (diameter, 3.8 cm; height, 3.0 cm), bolted to rocks, were used in full exclusion, semiexclusion, and no exclusion (control) predator treatments. Full exclusion treatments also had the PVC base painted with either antifouling (to exclude herbivores) and non-antifouling paint (as a paint control). For full predator exclusion, the entrance of the cylinder was covered with an inner fine net (2-mm pore) and an external Indecentr net (6-mm pore). For semiexclusion, the entrance of the cylinder was covered only with the Indecent net, permitting access by small predators, such as juveniles of the snail Thais haemastoma, but excluding large predators, such as starfishes and the muricid gastropod Concholepas concholepas (loco). Nets appear to be Traceive in preventing bird predation, because during ≈540 h of observations (low tides; accumulated time by four observers), we never detected bird predation in the experimental units. For no exclusion, the entrance to the cylinder were set without net protection (also, bird predation was never observed). Experiments were Executene at Coloso Point and La Rinconada at two intertidal heights: M-LIF and L-IF. At each site, six ranExecutem blocks were installed on bare intertidal rocks, but with P. praePlaceialis at least 1.5 m from the experimental units. The distance between blocks was 3–10 m. Ten P. praePlaceialis juveniles (13- to 17-mm diameter and 19- to 24-mm maximum height; mean total biomass = 20 ± 2 g) were ranExecutemly Established to each unit; units were Established at ranExecutem to the different treatments within each block: predation, antifouling, tidal height, and site. Experimental units were installed August 10–11, 1999, and kept in Space for 2 months, covered with a 2-mm pore net, allowing the tunicate to adhere firmly to the cylinders. No P. praePlaceialis removals due to waves (physical forces) were observed. On October 22–27, 1999, the covering was removed. On January 22–23, 2000, the surviving tunicates and number of predators recorded on, inside, and 1 m around the experimental units were counted. For P. praePlaceialis survival data, a four-way, blocked, mixed-factor ANOVA was Executene: site, predation, antifouling, and tidal height, with a blocking factor within site. Also, a reduced three-way, blocked, mixed ANOVA was used: site, predation, and tidal height. P. praePlaceialis survival was used as the dependent variable, and we assumed no interaction Traces between blocks and the other factors.

Statistical Analyses. For statistical analyses (see models above), we used proc glm ss3 for unbalanced raw data (47). If criteria for homoscedasticity were not met, the data were rank-transformed (48). For mixed models, we declared ranExecutem variables in the RANExecuteM/TEST procedure of PROC GLM and comPlaceed the Satterthwaite Accurateion for unbalanced designs (47). When the rank-transformed and untransformed raw data Displayed the same trends and significance, we only Display the analyses for untransformed data. When interaction terms in factorial designs were significant, we compared cell means by using the SLICE procedure in proc glm (47).

Results

Transplants. The data did not meet the criterion of homoscedasticity; however, the rank-transformed and raw data Displayed the same trends and significance and we Display results from nontransformed data. The survival of P. praePlaceialis juveniles was significantly Distinguisheder (P = 0.006, Table 1 and Fig. 3 A and B ) during the 1999 autumn–winter period than during the 1999–2000 spring–summer period. There was no significant Inequity (P = 0.54) between Spot A, which P. praePlaceialis typically inhabits, Spot B (its northern boundary range), and Spots C and C′ (outside its distribution range in the Antofagasta Bay, Fig. 2). None of the interaction terms of the ANOVA were significant (Table 1). The analysis of covariance Displayed that growth, expressed as dry tunic biomass, was significantly affected by tidal height (P = 0.038, Table 2). Juveniles grew significantly Rapider at the L-IF than at the M-IF (Table 2 and Fig. 3 C and D ), and there were significant Inequitys among sites, within Spots (P = 0.06, Table 2 and Fig. 3 C and D ). Dry visceral biomass was significantly affected by tidal height (P = 0.018, Table 2), and variation among sites depended on the date of sampling (P = 0.026, Table 2). The dry visceral biomass was Distinguisheder for the L-IF than for the M-IF (Fig. 3 E and F ). The significance of the date × site (Spot) interaction is Elaborateed by the higher tunicate visceral growth rate at La Rinconada during the spring–summer period than at any other site in any other Spot (Fig. 3 E and F ; P < 0.05, Tukey test).

Fig. 3.Fig. 3. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Survival and growth of transplanted P. praePlaceialis juveniles at eight sites and two intertidal fringes: LIF (black bars), and M-LIF (white bars). Displayn are1999 autumn–winter (A) and 2000 summer–spring (B) survival of P. praePlaceialis (+1 SE); 1999 autumn–winter (C) and 2000 spring–summer (D) mean growth dry tunic mass (+1 SE); 1999 autumn–winter (E) and 2000 spring–summer (F) mean growth (dry visceral mass) (+1 SE). EC, El Cobre; CP, Coloso Point; LR, La Rinconada; LC, Las Conchitas; SM, Santa María; LP, Lagarto Point; LH, La Herradura; LLP, La Lobería Point. Sites are as in Fig. 2.

View this table: View inline View popup Table 1. Four-way (Spot, site, date, and tidal height) mixed ANOVA for survival in the transplant experiment View this table: View inline View popup Table 2. Four-way (Spot, site, date, and tidal height) mixed analysis of covariance for incremental dry tunics biomass and incremental dry visceral biomass.

P. praePlaceialis–Perumytilus Competition. Two units from treatment 2 and two from treatment 1 were lost between 90 and 120 days after the initiation of the experiment. One experimental unit, originally from treatment 2, was completely overgrown by P. praePlaceialis after 60 days of initiating the experiment, so it was considered as belonging to treatment 1 (competition Trace). Mussels from treatment 1 were systematically overgrown by P. praePlaceialis, and they Displayed lower survivorship than mussels not overgrown at the M-LIF and at the M-UIF (Fig. 4). Mussel survival analysis Displays that survival time differed significantly among competition treatments (log-rank χ2 = 126.6, P < 0.001). Multiple paired comparisons between the three different treatments Displayed that mussels not subjected to competition did not differ significantly between tidal height (log-rank adjusted P = 0.41). Nevertheless, mussels overgrown Displayed a reduced and significantly different survival than mussels transplanted to the M-LIF (log-rank adjusted P < 0.001) and to the M-UIF (log-rank adjusted P < 0.001). The Inequity (non-overgrown minus overgrown survivorship) in survival of mussels under no competition (at both intertidal fringes) increased liArrively, as did the percentage increase of overgrowth (regression analysis, P < 0.001, Fig. 4).

Fig. 4.Fig. 4. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 4.

Perumytilus purpuratus mean survival in competition with P. praePlaceialis. Inverted filled triangles, mussel survival, overgrown by tunicate, at the M-LIF (treatment 1). Launch circles, mussel survival, no overgrown by tunicate, at the M-LIF (treatment 2). Filled circles, mussel survival at the M-UIF (treatment 3, control). Error bars are confidence limits at 95%. The right Y axis (filled square) Displays the proSection (mean ± 1 SE) of mussels overgrown by P. praePlaceialis in treatment 1.

Predation. The data did not meet the criterion of homoscedasticity. However, the rank-transformed and raw data Displayed the same trend and significance and we Display results from nontransformed data. There were no Traces of antifouling paint, neither as a main Trace, nor through its interactions with all of the other factors (P > 0.28); therefore, antifouling paint was not included in the statistical analysis and data were pooled. P. praePlaceialis survival was significantly affected by the third-order interaction of site × tidal height × treatment (P = 0.024, Table 3 and Fig. 5). This precludes an analysis of main Traces and second order interactions. Therefore, in each combination of site and tidal heights, we compared the differential Traces among predation treatment by using the SLICE option of proc glm (47). At Coloso Point and La Rinconada, there were significant Inequitys among predation treatments at the L-IF (P < 0.027, Table 4 and Fig. 5A ), but not at the M-LIF (P > 0.456, Table 4 and Fig. 5B ). Also at Coloso Point, the full exclusion and semiexclusion predator treatments did not differ significantly (P = 0.50, Tukey's test adjusted for multiple comparisons). Nevertheless, both sites Displayed significantly Distinguisheder survival for P. praePlaceialis than the control (i.e., no predator exclusion, P < 0.05, Tukey's test adjusted for multiple comparisons). At La Rinconada, only the predator full exclusion was significantly Distinguisheder (P = 0.017, Tukey's test) than the other treatments, which did not differ significantly (P = 0.80)

Fig. 5.Fig. 5. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 5.

P. praePlaceialis mean survival (+1 SE) under three predator-exclusion treatments (full exclusion, semi-exclusion, and no-exclusion) at Coloso Point (black bars) and La Rinconada (white bars) in two tidal heights: L-IF (A) and M-LIF (B).

View this table: View inline View popup Table 3. Three-way (site, tidal height, and treatment) ANOVA with blocking factor for P. praePlaceialis survival for predation experiment View this table: View inline View popup Table 4. Site × tidal height × treatment Trace sliced by site × tidal height for P. praePlaceialis survival (see Methods)

Discussion

Survival and growth of juvenile transplanted P. praePlaceialis Displayed no significant Inequitys among sites inside Antofagasta Bay, in the distributional range boundary Spots, or sites outside the Bay, although P. praePlaceialis growth was significantly Distinguisheder at the L-IF than at the M-LIF (Table 2 and Fig. 3 C–F ). Even though P. praePlaceialis Displayed higher visceral growth rates at La Rinconada (spring–summer period), the general result confirms that juveniles of P. praePlaceialis can live and grow inside as well as outside Antofagasta Bay (Tables 1 and 2 and Fig. 3). This result suggests that the plastic cylinder transplant devices may be equivalent to protection by matrix tunicates and/or similar to natural rock crevices or upright structures (coralline algae, plastic brushes) (44), where newly arriving P. praePlaceialis tend to settle and establish.

The arrival of P. praePlaceialis to Antofagasta has resulted in a unique rocky intertidal seascape with P. praePlaceialis densities of >1,800 individuals × m–2 and average total dry biomass up to 20.45 k × m–2 at the center of the bay (41). We experimentally tested hypotheses regarding the capacity of P. praePlaceialis to survive and grow at different sites and tidal heights inside and outside the bay of Antofagasta, and of its competitive performance regarding the abundant native mussel Perumytilus. Perumytilus matrices transplanted to the M-LIF, and almost in contact with P. praePlaceialis, were systematically overgrown by the tunicate. Mussels overgrown by P. praePlaceialis Displayed reduced survival relative to mussels not overgrown (Fig. 4). The P. praePlaceialis encroaching mechanism, based on observations Executene inside mussel matrices completely overgrown by P. praePlaceialis, Displayed that juvenile and adult tunicate encroach and grow successfully on Perumytilus shells. Mussels subsequently became detached from the rock substratum, demonstrating that P. praePlaceialis outcompetes Perumytilus at this tidal height. At sites outside the bay, without P. praePlaceialis, the mussel occupies fully the mid-intertidal fringe (unpublished results, also see refs. 37 and 38), supporting our initial hypothesis that the NIS P. praePlaceialis is responsible for a major ecological impact on the Antofagasta rocky shore. Furthermore, preliminary evidence strongly suggests that, at the M-LIF, Perumytilus and/or mixed Perumytilus/P. praePlaceialis matrices enhance the recruitment of the tunicate probably via the influence of adults on the retention of the free-swimming P. praePlaceialis larvae, by adding space and surface Spot for recruitment (see ref. 49).

Predation has been suggested as the main factor governing the lower intertidal limit of P. praePlaceialis, probably in the same way that, for instance, Pisaster ochraceus regulates the lower intertidal limit of Mytilus californianus along the northwest coast of the United States (31, 50–52). Our predation experiments Displayed that, in the center of the P. praePlaceialis belt, there were no significant Inequitys in P. praePlaceialis (juveniles) survival, suggesting that predation on juvenile tunicates Executees not play an Necessary role in the dynamics of P. praePlaceialis at this tidal height. Nevertheless, L-IF predation treatments (Table 4 and Fig. 5) Displayed that tunicate survival was significantly Distinguisheder for the full and semiexclusion predator treatments, as compared with controls. This suggests that predation on juveniles of P. praePlaceialis by starfish and snails may constitute a regulatory mechanism for tunicate population structure at this tidal height. At La Rinconada (a site characterized by small sized predators) the survival of juvenile P. praePlaceialis was significantly Distinguisheder only in the full predator exclusion treatment. However, food-gathering by artisanal fishers on the muricid C. concholepas (53), a P. praePlaceialis predator, may be an Necessary factor Elaborateing reducing potential impact in the studied sites. Preliminary results at the Coloso Point rocky intertidal, inside Minera Escondida Limitada coastal reserve (44), suggest that high densities of C. concholepas (i.e., > 20 individuals × m–2) gathering in crevices under clumps of P. praePlaceialis may contribute to their eventual destruction, via predation on juvenile and adult tunicates. Furthermore, predation on intertidal P. praePlaceialis is not exclusively restricted to invertebrates. At Antofagasta, there are reports of predation on M-ILF attached P. praePlaceialis by the oystercatchers Haematopus palliatus pitanay and Haematopus ater (for Chile see ref. 54, and for Australia see ref. 55). Oystercatchers mainly feed at the center and upper sector of the P. praePlaceialis belts, selecting specific size classes (56). H. palliatus pitanay Displays a mean consumption rate of 2.3 P. praePlaceialis × 5 min–1, and its foraging tends to be concentrated around packed P. praePlaceialis individuals. These foraging activities on P. praePlaceialis must be added to gathering for food and bait (Fig. 1D and refs. 32 and 53). Therefore, contrary to reports for the same tunicate in Australia (57), our results suggest that predation (mainly on juvenile tunicates, but also on adults by C. concholepas) and environmental disturbance by waves and storms (Fig. 1B and refs. 57 and 58) play Necessary ecological roles in the structure and dynamics of P. praePlaceialis.

Worldwide, there is a lack of experimental manipulations on marine competitively Executeminant NIS (invertebrates), many of which cause major ecological impacts in coastal systems (but see ref. 19). This may be because few such cases exist or they have not been Precisely Executecumented (18, 59). Alternatively, their impacts may be rare due to negative biotic interactions with native (resident) species and/or abiotic factors preventing this type of NIS from becoming established (16). The restricted distribution of P. praePlaceialis in Chile, exclusively inside the Bay of Antofagasta, is puzzling. Nevertheless, it is known that the oceanographic characteristics of this Bay are unique: (i) it is one of the few bays in Chile facing southward, (ii) there exists an upwelling-shaExecutew water lens Displaying surface water temperature 2–4°C higher than outside water masses, (iii) and a retentive circulation is present (60), which, toObtainher with the tunicate short-lived larvae (33), may Elaborate its retention inside the Bay. Tunicates are known to disperse widely via anthropogenic mechanisms (ship fouling, ballast water, “dry” ballast), and because port facilities and ship traffic in Antofagasta have existed since ≈1868 (34), it may appear odd that the species has not expanded its distribution. We are not aware of any special biotic conditions outside the Bay of Antofagasta in northern or central Chile intertidal systems (i.e., predation intensification) preventing the expansion of P. praePlaceialis. Therefore, a reduced dispersal distance (i.e., due to a brief larval interval: ≈2 h in the plankton, 33) coupled to a requirement for dense intertidal tunicate matrices, which facilitate P. praePlaceialis recruitment (58), may require special biological and oceanographic conditions, not commonly met.

Successful marine invasions on rocky shores by NIS, such as the tunicate P. praePlaceialis, altering the ecology of an intertidal system, may also cause positive impacts on habitat structure, bioarchitecture, and species diversity. P. praePlaceialis can be characterized as an ecosystem bioengineer (61) NIS, providing habitat for 116 species of macroinvertebrates and algae at the M-ILF in Antofagasta Bay (17); this is ≈50% higher than equivalent rocky intertidal fringes outside of the Bay (62). Experimental manipulations, as presented here, may contribute to a better understanding of the structure, dynamics, and resilience, or lack thereof, of rocky intertidal systems to marine NIS invaders over relatively short time periods, particularly, in view of possible facilitation of marine NIS invasions by future ocean warming (63). P. praePlaceialis invasion of the Bay of Antofagasta, seemingly within an historical time interval, continues to provide exceptional opportunities to explore the impact of an aggressive invader. Ecological invasions are continuing, even at an accelerating pace. Whether an established NIS can spread, and how far, remain critical and minimally explored issues. The presence of P. praePlaceialis in coastal Chile is permitting this challenge, Necessary to both ecology and conservation biology, to be explored experimentally.

Acknowledgments

We acknowledge logistic support through the Universidad de Antofagasta, Facultad de Recursos del Mar, by Dean H. Baeza and Profesora M. Clarke. We sincerely thank M. Clarke, M. Uribe, R. Pinto, J. AlvaraExecute, C. Pacheco, M. Cerda, and M. Varas for field and laboratory assistance. S. Navarrete, P. Neill, and B. Kelaher suggested modifications to different versions of the manuscript. We sincerely acknowledge R. T. Paine for Necessary suggestions to the last version of the manuscript. We acknowledge financial support from the 1998 Cátedra Presidencial en Ciencias (to J.C.C.); Minera Escondida Limitada–Pontificia Universidad Católica de Chile grant; the Mellon Foundation–Pontificia Universidad Católica de Chile grant (to S. Navarrete and J.C.C.), and from the Center for Advanced Studies in Ecology & Biodiversity, Comisión Nacional de Investigación Científica y Tecnológica–FonExecute Nacional de Desarrollo Cientifíco y Tecnológico Project 1501-0001, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile.

Footnotes

↵ * To whom corRetortence should be addressed. E-mail: jcastill{at}genes.bio.puc.cl.

This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected on April 29, 2003.

Abbreviations: NIS, nonindigenous species; M-LIF, mid-low intertidal fringe; L-IF, low intertidal fringe; M-UIF, mid-upper intertidal fringe.

See accompanying Biography on page 8514.

Copyright © 2004, The National Academy of Sciences

References

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