ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on January 31, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(5):765-769; doi:10.1093/icesjms/fsm196
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Factors influencing the recruitment and abundance of Didemnum in Narragansett Bay, Rhode Island
1 Department of Zoology, University of New Hampshire, Durham, NH 03824, USA
2 Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882, USA
Correspondence to L. A. Auker: tel: +1 603 8623647; fax: +1 603 8623784; e-mail: l.auker{at}unh.edu.
Auker, L. A., and Oviatt, C. A. 2008. Factors influencing the recruitment and abundance of Didemnum in Narragansett Bay, Rhode Island. – ICES Journal of Marine Science, 65: 765–769.The non-indigenous colonial tunicate Didemnum sp. A has been observed in Narragansett Bay, Rhode Island, since 2000. We compared weekly recruitment of the species and environmental parameters (i.e. temperature, salinity, chlorophyll a, dissolved oxygen, pH, and nutrient concentrations) over a 6-month period among three sites: (i) the University of Rhode Island Graduate School of Oceanography dock (GSO), (ii) the Department of Environmental Management pier at Fort Wetherill (FW), and (iii) the Prudence Island T-wharf. At the GSO and FW, divers surveyed the sites for percentage cover of Didemnum. To assess the spread of Didemnum in the bay and what factors may predict the tunicate’s presence, we also surveyed intertidal sites in October and November 2005, noting Didemnum presence, salinity, number of boats and moorings, and distances to major ports at each site. GSO had the highest percentage cover of adults and the highest recruitment of the tunicate (p < 0.01), reaching average peak values of 319 individuals per 100 cm2 in September 2005. Temperature and salinity demonstrated the best correlation with recruitment, and higher boat and mooring numbers may be a reliable predictor of tunicate presence. Further monitoring is needed to assess the potential spread of Didemnum throughout Narragansett Bay.
Keywords: Didemnum, distribution, Narragansett Bay, non-indigenous tunicate, recruitment, salinity, substratum, temperature
Received 20 May 2007; accepted 4 December 2007; advance access publication 31 January 2008.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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Didemnum sp. A (hereafter referred to as Didemnum) is a non-indigenous colonial tunicate that has been observed in Narragansett Bay, Rhode Island since 2000. It was detected first in Newport (Pederson et al., 2001), then on the University of Rhode Island (URI) Graduate School of Oceanography (GSO) dock (C. Deacutis, pers. comm.). The species is a strong spatial competitor, colonizes substratum rapidly, and prefers hard-bottom and gravel habitats and artificial substrata (Bullard et al., 2007a). In dominating new habitats, it reduces the abundance of previously established species (Bak et al., 1996; Lambert and Lambert, 2003; Bullard et al., 2007a). Didemnum may also inhibit settlement of scallops on Georges Bank, and it frequently overgrows adult Mytilus edulis and other species of shellfish (Bullard et al., 2007a; Valentine et al., 2007b). Colonies of the tunicate have few organisms willing or able to settle on them, and they have no known predators to control population growth (Bullard et al., 2007a; USGS, 2007).
Our objective was to describe the factors that contribute to the success of Didemnum and to characterize areas prone to invasion by the tunicate. To do so, we examined the seasonal recruitment of Didemnum and the extent of its distribution in Narragansett Bay. We correlated these with water quality factors and characteristics of the sites, respectively. Although the effects of temperature on Didemnum have been studied before (e.g. Osman and Whitlatch, 2007; Valentine et al., 2007a), we explored other factors that may affect Didemnum abundance, additional to temperature.
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Material and methods |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Recruitment
Artificial substrata were deployed for recruitment studies at three stations: (i) the GSO dock, (ii) the Rhode Island Department of Environmental Management pier at Fort Wetherill (FW) State Park, and (iii) the T-wharf dock on southern Prudence Island (SP) (Figure 1). At each station, four grey, 10 x 10 cm2, roughened polyvinyl chloride (PVC) panels were suspended horizontally, facing the seabed, to capture larval recruits. The panels were hung from piers, because there were no floating docks at the sites; their depth, averaging
1 m below the water surface, varied according to tide. Each week from May to October 2005, the panels were removed and replaced with clean panels. National Estuarine Research Reserve personnel maintained SP panels and transported them to URI for analysis. Sessile animals were identified and counted under a dissecting microscope in the laboratory. A two-way analysis of variance (ANOVA) compared Didemnum recruitment among the sites.
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Environmental data
A YSI 6920 sonde at the GSO and a YSI 6600 sonde at FW were used to measure water temperature, salinity, pH, and dissolved oxygen (%DO) data. The sondes, suspended
1 m below the water surface, collected data every 15 min. Each week, a surface water sample was collected for analysis of chlorophyll a (Chl a) and nutrients (NO2+NO3). To analyse for Chl a concentration, 10 ml of each water sample were vacuum-filtered on a 25 mm GF/F filter and treated with a 1% MgCO3 buffer. The samples were then kept at 20°C until they were extracted with 90% acetone and analysed on a Turner Designs fluorometer (Oviatt and Hindle, 1994). Water samples were filtered by pressure through 0.4 µm 47 mm polycarbonate filters and analysed on an Automated Analyser for nutrients (Oviatt and Hindle, 1994). At SP, a YSI sonde, also fixed at 1 m and maintained by the National Estuarine Research Reserve site on Prudence Island, collected temperature, salinity, pH, Chl a, and dissolved oxygen data every 15 min. Monthly nutrient data were also collected from that site. We used multiple regression analysis to compare weekly averages of all factors except NO2+NO3, which was compared as a monthly average, with Didemnum recruitment for each site.
Scuba survey
Scuba divers used an underwater camera and photoquadrat frame (Preskitt et al., 2004) to photograph transects at each of GSO and FW, with five 0.2 m2 quadrats per transect, in August and September 2005. Because of the remote location of the Prudence Island T-wharf and the limited time of the volunteer divers, we did not survey the SP pier. Two replicate transects at each site were 10.4 m long, and the divers sampled quadrats every 2.08 m (standard distance between every other GSO piling) at 3.7 m depth. An image-analysis program was used to measure percentage cover of the tunicate in the photographs. Total area of the image, cropped to the quadrat dimensions, was calculated by the program. Percentage cover of the tunicate was calculated for each quadrat as (area of tunicate/total area)x100. The percentage cover between months and between sites was compared with a Student’s t-test.
Intertidal survey
We chose marina, fishing access, and boat ramp sites (24 total) along the coastline of Narragansett Bay and Rhode Island Sound to survey for the presence of Didemnum from October to November 2005. At each site, we recorded the presence or absence of Didemnum, Global Positioning System (GPS) coordinates, salinity, and substratum information. We surveyed just above and below the waterline at each site between an hour before and an hour after low tide. To calculate the distance from the three main ports in Narragansett Bay (Providence, Quonset Point, and Newport), we used GPS data collected on-site with a Garmin GPSMAP 76S. To count potential vectors of Didemnum spread, we used high resolution aerial photography on Google Earth, taken within the past 3 years by MASS GIS, for boat and mooring counts (Commonwealth of Massachusetts, EOEA). We also used a Student’s t-test (assuming unequal variance) to compare salinity, distance from ports, and number of both recreational and commercial boats between sites where Didemnum was present and where it was absent. Logistic regression demonstrated the significance of each of the variables in predicting presence or absence of Didemnum.
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Results |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Recruitment and environmental data
The GSO site had the largest number of Didemnum recruits throughout the study relative to the other two sites (Figure 2). An ANOVA revealed a statistically significant difference among all three sites (p < 0.01). The environmental variables revealing significant correlation with Didemnum recruitment in a multiple regression analysis were temperature (r = 0.57 at the GSO), salinity (r = 0.68 and r = 0.60 at FW and GSO, respectively), and Chl a (r = 0.50 at FW; Table 1). The temperature at which the tunicate first appeared at each site was 18.4°C at FW, 19.7°C at GSO, and 22.5°C at SP. At the GSO, there was a peak in Didemnum recruitment concurrent with the peak of surface water temperature (Figure 3). There was also a concurrent peak in Didemnum recruitment with salinity at FW (Figure 4). There was a significant correlation between Didemnum and pH at two of the sites; however, it was negative at the GSO (r = 0.67) and positive at SP (r = 0.57). Problems with the pH probes in these sondes resulted in an incomplete dataset for each station, and it is not clear if these correlations would truly be significant if the missing data were present. There was no significant correlation between either percentage DO or NO2+NO3 and recruitment.
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Scuba survey
The scuba transects demonstrated a greater percentage cover of Didemnum at the GSO site (Figure 5). A t-test indicated that there was a significant difference in percentage cover of the tunicate between the sites (p < 0.05). There was no difference between months at each station.
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Intertidal survey
Of the 24 sites surveyed, nine demonstrated presence of the tunicate (Figure 1). A logistic regression analysis indicated that the tunicate was more likely to be found near sites with large numbers of recreational and commercial boats, moorings, and docks (p < 0.05). None of the sites north of Quonset Point had the tunicate present. A t-test revealed significant differences in number of boats and moorings (p < 0.01) and distance from Newport Harbor (p < 0.05) between invaded sites and non-invaded sites.
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Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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There were significant differences in recruitment between the three sites in Narragansett Bay, the GSO site having the highest average Didemnum recruitment. This site also had a large, established population of the tunicate, as suggested by the scuba transect data. We assumed that the high percentage cover of adult colonies resulted in subsequently high rates of recruitment. As lecithotrophic didemnid larvae do not travel far in the plankton (Olson, 1985; Marshall and Keough, 2003), we speculated that if there were enough suitable substratum, the larvae would settle nearby, creating more colonies. However, the abundances of adult populations may not have accurately reflected abundances of larval recruitment, because Didemnum uses asexual budding in addition to larval recruitment to create more colonies (Bullard et al., 2007b). Moreover, currents in some areas may have been faster, carrying larvae farther from adult colonies.
We suggest several characteristics that are likely to explain the success of Didemnum colonization at the GSO site. The GSO dock orientation, perpendicular to prevailing north–south tidal flow, increased the potential for larvae to settle on the substratum, because larvae will move with the prevailing current (Olson, 1985). Furthermore, there was an abundance of available substratum at the GSO, including plastic pipes, shell fragments, mussel beds, and wooden dock pilings, which the tunicate could colonize readily. Finally, there was little competition with macroalgae in shaded areas of the dock, where Didemnum thrived.
The site has also been invaded previously by two other colonial tunicates, Botrylloides violaceous and Botryllus schlosseri. Auker (2006) determined that the GSO site had more abundant B. violaceous and B. schlosseri recruits than either the FW or the SP site in 2005. These results appear to support the invasion–meltdown theory, which states that previous invaders may facilitate further invasions by other species (Simberloff and Von Holle, 1999).
FW had significantly lower Didemnum abundance in both recruitment and percentage cover than the GSO. The recruitment panels at FW were hung next to a rock wall with abundant macroalgae. The predominant substratum on the seabed was silt, and there was little hard surface in the area on which larvae could settle. However, a few abandoned plastic-coated-wire lobster traps served as suitable habitat and were covered with the tunicate. Although no dives were conducted on SP, the tunicate did reveal a significant increase in percentage cover on panels near the end of the sampling period (Auker, 2006). However, because only two transects were conducted at each site per month for two months, the addition of dive surveys at each site is necessary to determine better the adult abundance of Didemnum. Overall, the data collected for this study suggest that the adult population at the GSO is greater than that at FW and may result in greater propagule pressure, resulting in further recruitment.
Salinity and temperature were the most important environmental factors influencing the tunicate’s distribution and recruitment, respectively. In Narragansett Bay, the salinity ranged from 28.5 to 31.3 psu at all three recruitment sites. Salinity had a significant positive correlation to recruitment in the multiple regression analysis at both GSO and FW. Didemnum was not observed north of Quonset Point in the intertidal survey, most likely because the bay north of that point had, at times, lower salinities (between 15 and 25 psu) as a consequence of fresh-water input into the estuary (Figure 1). Ascidian zygotes and larvae are generally unable to withstand salinities below 20 psu (Millar, 1971). However, as we examined only the surface water for Didemnum, our data did not address deeper waters in the upper bay, which have higher salinity, and therefore may hold populations of Didemnum.
Temperature, although less critical than salinity in determining distribution of Didemnum, is a factor in controlling marine invertebrate sexual reproduction (Millar, 1971). Didemnum peaked in recruitment at the GSO at the same time as summer water temperatures peaked, suggesting a link between temperature and recruitment (Valentine et al., 2007a). However, temperatures on Georges Bank range from 4°C to 15°C annually, and Didemnum thrives there. The tunicate population on Georges Bank does not exhibit the same growth cycles as in shallow-water systems (Valentine et al., 2007a), suggesting that Didemnum is highly adaptive and able to thrive in wider ranges of physical factors, including temperature, than endemic species, a trait shared by other non-native tunicates (Lambert and Lambert, 2003).
Timing of the Didemnum peak recruitment in Narragansett Bay was later than in other studies. Osman and Whitlatch (2007) found that recruitment peaked in August of 2001 and 2003, and in June 2002 at an open coast site in Long Island Sound. The temperature peak there was also earlier than in Narragansett Bay; daily temperature peaked in July and August (23–25.6°C) during their 2005/2006 study. Valentine et al. (2007a) surmised that sexual reproduction takes place simultaneously with the warmest water temperatures in shallow systems. Our GSO data and those of Osman and Whitlatch (2007) support that conclusion.
Didemnum recruitment did not correlate with the other factors we measured, with a few exceptions. For example, at FW there was some correlation between recruitment and Chl a concentration. We initially assumed that Chl a was an indicator of a potential food source for filter-feeders in the community, but Didemnum, like other ascidians, may feed on particles other than phytoplankton (Petersen, 2007). Additionally, we observed a correlation between recruitment and pH, although it was positive at SP and negative at GSO. Those stations’ sondes each had pH probe failures, resulting in missing data, so the data could not be considered reliable. However, there was a complete set of pH data for FW, and there was no significant correlation between pH and recruitment there.
Potential vectors of Didemnum spread generally include aquaculture and hull fouling (Coutts and Forrest, 2007; Dijkstra et al., 2007). Our study suggests that, because of the significant correlation between Didemnum presence and high boat and mooring counts, hull fouling could be a factor in its spread throughout Narragansett Bay. The bay is a major area of commercial and recreational access for ships and sea traffic, and the East Passage (the channel between Conanicut and Aquidneck Islands) is the only shipping channel in the bay (Ely, 2002). Most of the sites with Didemnum were in the East Passage and close to Newport Harbor, a large commercial port and the first site of discovery of the tunicate in the bay (Pederson et al., 2001). There were also areas of unexpected Didemnum colonization in the East Passage, including Taylor Point on Conanicut Island, an area without marina access or boat ramps, but located near large, anchored commercial tankers.
Because Narragansett Bay is an economic base for commercial fishing and shellfishing (RIDEM, 1998; Ely, 2002), continued spread of this tunicate throughout the bay could have potentially serious economic consequences. However, management of the invasion of this tunicate has been restricted to small-scale attempts in locations such as New England (L. Harris, pers. comm.) and New Zealand (on Didemnum vexillum; Coutts and Forrest, 2007). Coutts and Forrest (2007) studied ways to eradicate the tunicate, and found that many of the techniques that they used to kill the tunicate are effective on small scales, but cannot completely eradicate it from a region. They noted that "baseline knowledge and an effective surveillance regime" are the first requirements for eradication success (Coutts and Forrest, 2007). Now that we have an initial sense of both Didemnum distribution in Narragansett Bay and the factors that influence its success, future monitoring programmes can be developed. From these programmes, perhaps a bay-wide management plan can be established.
In conclusion, several factors led to Didemnum abundance in Narragansett Bay. We contributed an example of peak Didemnum recruitment coinciding with peak summer water temperatures. Moreover, the steady high salinity and ample availability of hard substratum in the lower bay provide a favourable habitat for the tunicate. Didemnum often inhabited locations where there were stationary boats, both commercial and recreational, indicating that such vessels may be a vector in the spread of Didemnum throughout the bay. Several of these sites, as discovered in the intertidal survey, had an abundance of Didemnum colonies. Expanding a recruitment survey to these invaded areas, coupled with measurement of water currents and a clearer understanding of the larval competency period, may further increase our understanding of the larval dispersal and timing of Didemnum.
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Acknowledgements |
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This work was part of LAA's MSc thesis research at the University of Rhode Island, Graduate School of Oceanography. We thank C. Deacutis, J. Collie, and R. Whitlatch for their input during the planning and execution of the methods described here, and D. Melrose and J. Krumholz for their excellent support as scuba divers. We are also grateful to H. Stoffel, A. Ganz, K. Raposa, and T. Kutcher for their valued assistance in the laboratory and field, and to J. Mercer for sharing his expertise in identifying the larvae that settled on the panels. The Rhode Island Natural History Survey funded part of this research via a Wald Grant award. Suggestions from three anonymous reviewers greatly improved the manuscript.
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References |
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