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The Non-Native Solitary Ascidian Ciona Intestinalis (L.) Depresses Species Richness ⁎ Julia C

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The Non-Native Solitary Ascidian Ciona Intestinalis (L.) Depresses Species Richness ⁎ Julia C Journal of Experimental Marine Biology and Ecology 342 (2007) 5–14 www.elsevier.com/locate/jembe The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness ⁎ Julia C. Blum ,1, Andrew L. Chang 5, Marcela Liljesthröm 2, Michelle E. Schenk 3, Mia K. Steinberg 4, Gregory M. Ruiz Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, MD 21037, United States Received 1 September 2006; received in revised form 1 October 2006; accepted 9 October 2006 Abstract Non-native ascidians are a dominant feature of many sessile marine communities throughout the world and may have negative effects on species diversity. We tested effects of the non-native Ciona intestinalis on the sessile invertebrate community in San Francisco Bay, where it occurs in dense aggregations. In particular, we compared species richness between PVC panels from which C. intestinalis were experimentally removed to panels with naturally dense C. intestinalis growth, using fouling panels of four sizes (between 49 cm2 and 1177 cm2) to measure the effect of C. intestinalis recruitment on species-area relationships. We initially deployed 120 fouling panels (30 of each size) at a site known to have dense populations of C. intestinalis, assigning these to three different treatments: (1) Experimental removal, whereby new recruits of C. intestinalis were removed on a weekly basis, pulling panels out of the water for a short time period to do so; (2) Manipulated control, whereby panels were removed from the water each week (as in the experimental removal) but without C. intestinalis removal; and (3) Unmanipulated control, which remained in the water throughout the experiment. After 4 months, all of the panels were collected and analyzed to estimate species richness and relative abundance (percent cover) of sessile invertebrates and of C. intestinalis. Across all panels, species richness was negatively correlated with C. intestinalis abundance. The removal of C. intestinalis produced communities with significantly higher species richness than the controls. The overall species composition of treated and control panels was also distinctly different, with many species occurring more often in the absence of C. intestinalis, while others occurred more often on C. intestinalis-dominated panels. These data suggest that C. intestinalis both depress local species diversity and alter community assembly processes to fundamentally change sessile community composition. © 2006 Elsevier B.V. All rights reserved. Keywords: Ascidian; Ciona; Fouling community; Impact; Invasion; Nonindigenous; Species richness ⁎ Corresponding author. Tel.: +1 410 802 7925. E-mail address: [email protected] (J.C. Blum). 1 Present address: Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616. 2 Present address: University of North Carolina Wilmington, 601 South College Road, Wilmington, NC 28403. 3 Present address: School for Marine Science and Technology, University of Massachusetts Dartmouth, 706 South Rodney French Blvd, New Bedford, MA 02744. 4 Present address: University of Delaware, Graduate College of Marine Studies, 233 Cannon Marine Studies Lab, Lewes, DE 19958. 5 Present address: Department of Environmental Science and Policy, University of California, One Shields Avenue, Davis, CA 95616. 0022-0981/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2006.10.010 6 J.C. Blum et al. / Journal of Experimental Marine Biology and Ecology 342 (2007) 5–14 1. Introduction introduced range, where it is often a nuisance fouling species in aquaculture (Kang et al., 1978; Lesser et al., Sessile species, such as terrestrial plants or marine 1992; Castilla et al., 2005). The striking nature of invertebrates, can exhibit dominant growth relative to C. intestinalis recruitment and its worldwide success as other local species. For terrestrial plants, this often in- an invader underscore the importance of understanding volves forming high-density or monospecific stands, its ecological effects. frequently by overgrowing and shading surrounding In the highly invaded San Francisco Bay, we competitors. While both native and introduced plant performed a manipulative field experiment to measure species can exhibit dominance, it is an important factor the effects of C. intestinalis dominance on the diversity in an introduced plant's ability to become invasive. of the local community at several spatial scales. Monospecific stands of both native and introduced in- C. intestinalis (hereafter, Ciona) was first recorded in vasive plants tend to have negative consequences for San Francisco Bay in 1932 (Rodholm, 1932) and a 2001 local plant diversity (Ervin and Wetzel, 2002; Silliman survey observed several areas with approximately 100% and Bertness, 2004). Similar patterns have been ob- cover of primary space (Ruiz et al. unpublished). Due to served among invasive marine algae, most notably the importance of free space as a resource in fouling Caulerpa taxifolia (Verlaque and Fritayre, 1994). communities (Osman, 1977; Sutherland, 1981), we Trends in the consequences of these stands for local hypothesized that Ciona would have a negative effect animal diversity are less clear, with both increases and on local sessile faunal species richness. A pilot study decreases recorded in the literature (e.g., Burger et al., with M. manhattensis in Chesapeake Bay suggested that 2003). such an effect might also result in depression of the For sessile marine invertebrates, the mussel Mytilus positive species-area relationship previously observed californianus is the most familiar example of the effect for marine sessile communities (Schoener and Schoener, of dominant growth; Paine (1966) demonstrated its 1981), as elsewhere (Rosenzweig, 1995). negative effects on primary species diversity (i.e. spe- cies directly attached to the substrate) in the absence of 2. Methods its sea star predator. While in this case M. californianus was a native member of the ecosystem, similar dominant 2.1. Ciona recruitment at experimental site growth patterns have been observed for the introduced mussel Mytilus galloprovincialis in South Africa (Van Recruitment of new Ciona individuals was measured Erkom Schurink and Griffiths, 1990; Robinson et al., at Richmond Marina Bay Yacht Harbor, in the north- 2005). Among other groups of marine invertebrates, eastern part of San Francisco Bay, from February 2002 to numerous ascidian species also exhibit dominant growth March 2003 by deploying five 13.7 by 13.7 cm fouling in their introduced ranges, such as Styela clava (Lambert panels at 1 m depth for 1 month periods in locations and Lambert, 1998), Didemnum sp. A (USGS, 2006), evenly distributed around the site. Panels were retrieved Ciona intestinalis (Carver et al., 2003), and, to some monthly for analysis and replaced with new, bare panels. extent, Molgula manhattensis (JCB, pers. obs.). While All panels used in this study were gray, 0.25 cm thick, these species are able to overgrow surrounding fauna or, sanded PVC. in the case of the solitary species, form dense mono- Panels were individually isolated and transported specific stands (e.g., Lambert and Lambert, 1998 for between the field site and the laboratory in plastic bags C. intestinalis), little information exists on the con- filled with seawater and stored in a cooler. At the lab, sequences of such growth patterns for the diversity of panels were fixed in 10% buffered formalin and pre- the surrounding community. served in 70% ethanol. Ciona recruits were identified We selected the solitary tunicate C. intestinalis to and counted on each panel to determine seasonal measure effects of a high-density ascidian invasion on patterns of Ciona recruitment during the year of the community structure. C. intestinalis has been introduced experiment. from northern Europe into bays on both coasts of North America, in New Zealand, the Mediterranean, Australia, 2.2. Ciona-removal experiment Korea, Hawaii, Chile, South Africa, and Hong Kong (Lambert and Lambert, 1998, 2003; Castilla et al., 2005; To determine the effect of Ciona's presence on Robinson et al., 2005). It exhibits dominant growth fouling community species richness, we compared patterns in both its native range (Koechlin, 1977; fouling panels from which we had experimentally Havenhand and Svane, 1991) and much of its removed Ciona to panels with naturally dense Ciona J.C. Blum et al. / Journal of Experimental Marine Biology and Ecology 342 (2007) 5–14 7 growth. We included four different sizes of fouling retrieved the panels after 17 weeks, between October 23, panels to examine the effect of dense Ciona recruitment 2002 and October 26, 2002. on species-area relationships. During the course of the experiment, 16 of the orig- The four sizes used were 7 by 7 cm (“small”), 13.7 by inal 120 panels were lost. Most losses resulted from the 13.7 cm (“medium”), 21.7 by 21.7 cm (“large”), and weight of settled Ciona exceeding the tensile strength of 34.3 by 34.3 cm (“extra-large”). These panel sizes rep- the plastic cable ties used to attach the panels to their resent multiples of approximately one, four, nine, and bricks. Therefore, losses were especially high among twenty-five times the area of the smallest panel (7 larger panels in the manipulated and unmanipulated by 7 cm), respectively. Each panel was individually control treatment classes. Due to the combination of mounted on a brick and suspended from a floating dock differential panel loss and deployment error, the final set at 1 m depth with the collecting surface of the panel of 104 retrieved panels had treatment-size class facing downwards. The panels remained in the water, replication ranging from 4 replicate panels per class allowing organisms to settle on them and creating a (unmanipulated control-large) to 12 replicate panels per community that we then manipulated. class (unmanipulated control-small). However, 8 out of Panels were assigned to one of three treatments: 12 treatment-size classes contained between 7 and 10 Ciona-removal, unmanipulated control, or manipulated replicate panels, with a median of 8.5 replicate panels control. Treatments were applied weekly for the dura- across all classes.
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