Ecosystem Modeling in Cobscook Bay, Maine: A Boreal, Macrotidal Estuary 2004 Northeastern Naturalist 11(Special Issue 2):143–162 Growth and Productivity of Sublittoral Fringe Kelps (Laminaria longicruris) Bach. Pyl. in Cobscook Bay, Maine ROBERT L. VADAS SR.1,*, BRIAN F. BEAL2, WESLEY A. WRIGHT3, STEVE NICKL3,4, AND SHERI EMERSON3,5 Abstract - We examined the growth, productivity, and turnover of sublittoral fringe populations of Laminaria longicruris in high- and low-flow habitats (headlands and bays, respectively) in Cobscook Bay during 1995 and 1996. We used the hole-punch technique, incorporating increases in length and width (area) to estimate frond growth. Regression analysis was used to predict biomass from frond area. Water temperature, salinity, and nutrients were measured monthly. Kelp tissue was analyzed to assess nutrient-growth relationships. Mean ± SD monthly productivity at Bar Island (low-flow) ranged from 0.42 ± 0.31 to 8.61 ± 2.37 g dry m-2 day-1. Productivity estimates for Mahar Point and Garnet Point (headlands) exhibited a lower and narrower range of values, 0.25 (n = 1) to 3.67 ± 0.79 g dry m-2 day-1 and 0.46 (n = 1) to 5.82 ± 2.27 g dry m-2 day-1, respectively. The overall range of productivity estimates based on carbon was 0.08 (n = 1) to 2.58 ± 0.71 g C m-2 day-1. Growth in these fringe stands was comparable to kelps in general, but productivity was slightly lower, likely due to lower stand densities and, possibly, stress from aerial emergence during low tides. We estimated that 75 hectares of the Bay was in L. longicruris production yielding 3.34 x 107 g C year-1. Introduction Kelp forests are large, nearshore, subtidal stands of canopy-forming macroalgae and are abundant along boreal, sub-arctic shores. Where cold nutrient-rich water is upwelled, giant kelp (> 15 m) often dominate coastlines. Smaller-bodied kelp occur over a wider range of subtidal habitats, but mainly in colder waters and where nutrients are available, at least seasonally. Such populations are common in the northwest Atlantic Ocean (Chapman 1984, Smith 1988). Scattered beds and isolated stands of kelp, e.g., Laminaria longicruris Bach. Pyl., L. saccharina (L.) Lamour., and L. digitata (Huds.) Lamour., occur regularly along the Gulf of Maine (Vadas and Elner 1992, Witman 1987). On several 1Department of Biological Sciences and School of Marine Sciences, University of Maine, Orono, ME 04469. 2Division of Environmental and Biological Sciences, University of Maine at Machias, Machias, ME 04654. 3Department of Biological Sciences, University of Maine, Orono, ME 04469. 4Current address - PO Box 709, Bar Harbor, ME 04609. 5Current address -Santa Rosa Public Works Department, 69 Stony Circle, Santa Rosa, CA 95401. *Corresponding author - vadas@maine.edu. 144 Northeastern Naturalist Vol. 11, Special Issue 2 offshore rock outcrops, kelps form large, open, park-like stands at depth. At some locations, e.g., Columbia Ledge, near Mt. Desert Rock, fairly large body (10 m) L. longicruris occur on the shallow crests of these pinnacles forming dense kelp forests (Vadas and Steneck 1988). In general, however, the fronds of most kelp in the Gulf of Maine rarely exceed three meters in length. Over the last few decades, kelp forests have been recognized as highly productive systems and as valuable habitat for numerous invertebrates and fish. Some estimates place kelp forests among the most productive ecosystems (Mann 1973). Kelp growth in temperate-boreal environments is usually seasonal, but different populations are not necessarily controlled or limited by the same environmental factors. In some locations, light (irradiance) or temperature may be critical, whereas in others nutrients have a major influence on growth (Chapman and Craigie 1978). Some kelp continue to grow throughout winter despite low irradiance levels, e.g., L. longicruris in Nova Scotia (Hatcher et al. 1977) and L. solidungula J. Agardh in the Arctic (Dunton 1985). Subsequently, off-season growth in L. longicruris was attributed to nitrogen availability or storage within the thallus (Gagne and Mann 1981). Gerard and Mann (1979) found that reduced light and nutrient levels limited growth more in exposed than in sheltered populations. Kelp beds also exist as refugial populations, often near low tide and where high energy waters restrict grazing by sea urchins (Himmelman and Lavergne 1985, Mann 1977). Such stands are common along waveexposed shores of the Gulf of Maine and in selected high current flow locations, e.g., Cobscook Bay located near the mouth of the Bay of Fundy (R.L. Vadas, pers. observ.). Macroalgae in Cobscook Bay experience an extreme range of tidal amplitudes, currents, and water movements. A unique aspect of the Bay is the enormous temporal and spatial variation in flow forces generated by the large 6 to 8 m tidal ranges, currents (to 1.8 m s-1), and the geomorphological constrictions of the various basins (Brooks et al. 1999, Garside and Garside 2004). The bays and headlands formed by these features likely affect flow regimes and boundary layer processes such as nutrient uptake (Gerard and Mann 1979) and thereby influence algal growth rates. Kelp populations in Cobscook Bay, with the exception of Agarum clathratum Dumort., occur largely in scattered, narrow bands in the sublittoral fringe. These kelp, mainly Laminaria longicruris, appear to be refugial stands from grazing herbivores. Sea urchin densities are high (14–52 m-2 at some sites) throughout much of the Bay (Vadas et al. 2000) and support an active sea urchin fishery. Sea urchin feeding fronts are common in the subtidal fringe of Deep Cove and Birch Point (R.L.Vadas, pers. observ.) and likely set the lower limit (Witman 1987) on kelp populations in the Bay. Here we focus on the growth, produc2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 145 tivity, and turnover of several relatively small and isolated sublittoral fringe populations of L. longicruris. These populations may be stressed by aerial exposure during spring tides. We limited our studies to kelp in high- and low-flow habitats (headlands and bays). Of interest was whether these low intertidal-fringe stands of L. longicruris functioned like typical subtidal populations and how much carbon they contributed to the Bay. Most previous studies on productivity of this kelp have utilized deeper subtidal populations (Chapman 1984, Egan and Yarish 1990, Smith 1988). Methods Site selection The growth and productivity of L. longicruris in Cobscook Bay was studied from June 1995 through July 1996 at two sites (Bar Island and Mahar Point) and from June 1995 through November 1995 at a third site (Garnet Point) (Fig. 1). The three sites were within 15 km of each other and presumably reflect two different flow regimes. Mahar Point and Garnet Point are headland sites and represent high-flow habitats, whereas Bar Island represents a lower flow environment. The kelp beds were located in the subtidal fringe, accessible only during the lowest tides of each month. Thus, the time available for sampling at this tidal level was greatly limited, especially during winter. Currents were too swift to measure plants effectively using scuba, and work at all sites was done from the shore during day or night low tides. In situ growth measurements Growth measurements during 1995 and 1996 were made monthly from spring to fall and every other month during winter. Sampling at these intervals assured that holes punched in the blades were not lost as the frond eroded at the distal end (see below). Generally 10 to 20 kelps per site were tagged to determine growth parameters, although when time, tide, and daylight permitted, additional algae were marked. Individuals were initially tagged by carefully looping cable ties with an attached numbered tag around the stipe. In addition, 50 cm of brightly colored flagging tape was attached to the stipe near the tags to help locate marked plants. Many of the cable ties eventually slipped to the holdfast and made it difficult to separate the fronds of marked individuals, especially during summer when plant densities were greatest. Subsequently, only colored flagging tape was used to mark and number thalli. The tape was color coded by date and numbered with black waterproof ink from Sharpie® marker pens. To reduce the possibility of entanglement of tagged individuals, we utilized kelp in which the holdfasts were separated by 1–1.5 m. Marked thalli were usually grouped in 2 linear rows parallel to shore to facilitate locating 146 Northeastern Naturalist Vol. 11, Special Issue 2 and measuring plants on subsequent dates. At each sampling interval, a thorough search of the overlying fronds was made to locate all tagged individuals. The Garnet Point kelp population was followed for only one season because of major disturbance to the site. Density of kelps in fringe populations was determined in midsummer. Because of the short amount of time available for sampling at this tide level, density estimates were made only once at each site during summer. However, direct observations during tagging studies (below) revealed that abundance was greatly reduced during winter. We estimated densities from January to March to be 40% of summer values. To obtain representative samples from these linearly arrayed beds, 1-m2 quadrats were haphazardly placed along a transect parallel to shore. Figure 1. Map of Cobscook Bay kelp study sites during 1995–96 (BF = Bell Farm, BI = Bar Island, GP = Garnet Point, MP = Mahar Point). 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 147 Only individuals greater than 0.5 m in length were recorded because of the layering of fronds and the difficulty in uncovering fronds and holdfasts at low water. Similar size limitations have been utilized by other workers (Gerard and Mann 1979). Frond growth was determined using a modified hole punch technique (Gerard and Mann 1979, Parke 1948, Smith 1988). Kelp fronds grow from an intercalary meristem, and two parallel holes (6 mm diameter) were punched 10 and 20 cm above the apophysis at each visit to determine growth during the next interval. The width of the frond was determined at 10 and 50 cm, and the average width of these two measurements was used to calculate the area of recent frond growth. Growth was based on the change in area and weight between intervals, which was determined by the distance that the holes moved distally and on average frond width (see below). Our assumption here was that no significant growth occurred beyond the distal holes (Gagne and Mann 1987). The following measurements were made on tagged plants at each sampling date: total frond length, distance from apophysis to the previously punched holes, frond width at 10 and 50 cm, and maximum stipe diameter near the apophysis. Laboratory growth measurements To relate in situ growth measurements to biomass and productivity during an interval, randomly selected kelp plants of various frond lengths (size classes) were collected and analyzed on several occasions. Measurements and wet to dry weight relationships were made on three regions of the thallus: holdfast, stipe, and frond. Holdfasts and stipe segments (10 cm in length) and frond segments (from 10 cm to 20 cm above the apophysis) were cut, weighed wet, and dried. To determine dry weight, plant material was placed in pre-weighed aluminum foil pans and dried at 60 °C to a constant weight. The following traits were recorded for each individual on each sampling date: longest and shortest holdfast diameter, wet and dry holdfast weight, length and maximum diameter of the stipe, wet and dry weight of 10 cm stipe segment, width and thickness of frond at 10 and 50 cm from apophysis, total frond length, and wet and dry weight of 10 cm frond segment. To estimate dry weights of whole fronds, we determined the dry weight of a specific area of each collected frond. At 10 cm above the apophysis, a rectangular segment (above) was removed and dried to a constant weight. This yielded a measure of g dry wt cm-2 for the segment which was used as a correction factor in calculating dry weight of the entire frond. We calculated the area of the total frond by multiplying total length x average width ([width at 10 cm + width at 50 cm]/2). These area estimates were multiplied by the correction factor to obtain an estimate of total frond dry weight. These data yield site-specific dry weight-area relationships (loge [dry wt] = a + b • loge [area]) that were used to estimate frond dry weight of tagged 148 Northeastern Naturalist Vol. 11, Special Issue 2 individuals on each sampling date. Regression analysis was also used to determine if sampling dates and sites could be combined. We estimated total plant biomass for tagged individuals at least once from each site (GP: 9/7/95; MP: 9/8/95, 11/8/95, 2/21/96, 5/17/96, 7/1/96; BI: 9/12/95, 11/27/95, 2/26/96, 4/17/96, 5/19/96, 7/1/96). On each date, we measured wet weights (g) of stipes and holdfasts of untagged plants over a wide range of sizes representing tagged individuals. A ratio of holdfast and stipe wet weight to frond wet weight was calculated for each plant at each site. The site- and date-specific mean ratio was multiplied by the mean frond dry weight (estimated for each site and date, see above) to yield an estimate of dry weight for the stipe and holdfast. This estimate was then added to the frond dry weight to obtain a dry total plant biomass. This biomass estimate was multiplied by stand density to estimate total biomass (g dry wt m-2). The sampling periods from January to June at Bar Island were combined into one sample because of low sample sizes. Because of low sample sizes (due to disturbance), no regression was done on January to June samples from Mahar Point. Samples were combined when slopes were not significantly different. These regressions were applied to the field data for the corresponding sampling period to estimate biomass. The regressions developed for summer (July) 1996 at Bar Island and Mahar Point were also used to estimate the summer (July and August) 1995 samples at these two sites. The samples used to develop regressions for Garnet Point were taken in September 1995. Productivity and turnover The area (length x width) of new growth of the frond was based on elongation rates during four or eight week intervals. Length was characterized as the distance moved by the holes punched in the frond and the width as the average width of the frond measured at 10 and 50 cm. Productivity estimates for Laminaria longicruris were determined by converting the area of new growth into dry weight with the correction factor developed above. Conversion of kelp tissue into grams of carbon was made by multiplying wet weights by 0.06, or dry weights by 0.3 (cf., Mann 1972, Smith 1988, Westlake 1963). Turnover rates and times of Laminaria were based on net productivity estimates made during each interval. Biomass was based on summer densities and average plant weights, except for winter when densities of plants > 50 cm were estimated to be less than 40% of summer values. The number of turnovers per year was calculated as (net productivity x 365) / biomass. Statistics Regression analysis was used to predict dry weight from area with loge transformed variables. Site- and date-specific regressions to esti2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 149 mate frond dry weight were combined to increase sample size when slopes were not significantly different (p > 0.05). In addition, we investigated the value of adding frond thickness (to determine the volume of the frond) to estimate frond biomass by using forward-selection, stepwise regression analysis. The dependent variable in the model was frond wet weight; the independent variables were frond length, width at 10 cm, width at 50 cm, average width, thickness at 10 cm, thickness at 50 cm, and average thickness. Variables were added until no other contributed significantly (p = 0.15) to the model. This was done by site and date for September and November of 1995 at Bar Island and Mahar Point and for September of 1995 at Garnet Point. Two log-log regressions, one using loge of area and the other using loge of volume as the independent variables with loge of the wet weight of the frond as the dependent variable were calculated using the combined data. Means are presented with ± 1 standard deviation (SD). Hydrographic and kelp tissue data To provide background data for growth patterns, ancillary data were taken monthly on subsurface (- 25 cm) water column variables at low tide from March 1995 to August 1996. Temperature, salinity, and nutrients (phosphate and nitrate) were determined monthly. The Bell Farm site (Fig. 1), which is on the west side of the channel of Whiting Bay, served as the hydrographic station for Bar Island. Samples of kelp were collected systematically at Mahar Point and on several occasions at Garnet Point and Bar Island to measure nutrient levels in tissues and assess nutrientgrowth relationships. Also, we attempted to qualitatively estimate differences in flow regimes at these sites. The methodology and details for nutrient and flow analyses are provided in Vadas et al. (2004). Results Biomass Results from the stepwise regressions for inclusion of frond thickness in the model were equivocal. Average thickness generally performed better in the analyses than the separate thickness measures. Average frond thickness by date was never significant (p > 0.05) in the model. The variable, average frond thickness was significant for only one site (Bar Island, p = 0.01, n = 29) and was the third variable added after length and average width. When data from all sites and dates were pooled (n = 61), length was first to enter the model: (r2 = 0.79, p < 0.0001), followed by average width (r2 = 0.84, p = 0.0002) and average frond thickness (r2 = 0.86, p = 0.0052). Log-log regressions using the pooled data for area to predict wet weight had a slightly higher r2 (0.877) than did the regression using volume (r2 = 0.835). Regressions generated to estimate frond biomass (g dry m-2), and subsequently productivity and turnover, for each sampling period and 150 Northeastern Naturalist Vol. 11, Special Issue 2 site are given in Table 1. Kelp densities (mean ± SD of plants > 50 cm in frond length, used to determine biomass, were highest at Bar Island (12.9 ± 9.04 plants per m2). Densities at Mahar and Garnet Points averaged 9.1 ± 7.2 and 7.0 ± 2.5 plants per m2, respectively. Kelp populations had a single peak of total biomass during summer (Fig. 2). Biomass estimates at the two sites monitored for a year showed similar seasonal patterns, but different absolute levels. Highest within-site estimates occurred during 1996 at Bar Island (1035 g dry m-2) and at Mahar Point (521 g dry m-2). Overall, the highest biomass values during both years occurred at Bar Island. Estimates of biomass for Bar Island and Garnet Point during September 1995 were 2 to 3 times higher than for Mahar Point. In the summer of 1996, biomass estimates at Bar Island were 4 times greater than Mahar Point. The kelp bed at Table 1. Regression analysis of dry weight and area of Laminaria longicruris using combined sites and dates. Sites1 Date Equation2,3 Adj. r2 N BI, MP Sep 1995 loge(W) = -6.4289 + 1.1864 • loge(A) 0.945 27 GP Sep 1995 loge(W) = -6.0223 + 1.1823 • loge(A) 0.898 10 BI, MP Nov 1995 loge(W) = -5.8023 + 1.0775 • loge(A) 0.743 22 BI Winter–spring loge(W) = -6.9113 + 1.1900 • loge(A) 0.847 13 BI, MP Jul 1996 loge(W) = -3.9765 + 0.8700 • loge(A) 0.879 29 1BI = Bar Island, GP = Garnet Point, MP = Mahar Point 2W = Dry weight 3A = Area Figure 2. Biomass of Laminaria longicruris at three sites in Cobscook Bay during 1995–96. Biomass (g dry m-2) 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 151 Mahar Point was disturbed by sea urchin draggers during early spring of 1996. Disturbance from scallop dragging, prevailing winds, and choppy waves directly impacted the Garnet Point site during the fall of 1995 (R.L. Vadas and B. Beal, pers. observ.). The waves from the long fetch and currents tossed dislodged invertebrates, stones, and the shells of shucked scallops onto the narrow kelp bed and the low intertidal zone. The cumulative forces from the waves and debris created a major disturbance to the kelp, resulting in a 95–99% loss of both tagged and untagged plants from the Garnet Point population. The few remaining kelp were severely damaged with an almost complete fraying of fronds and stipes. It was impossible to continue in situ growth studies there, and the site was abandoned in late fall 1995. Growth, elongation, and hydrography There was a clear seasonal pattern of frond growth in Cobscook Bay (Fig. 3). During 1995, growth rates peaked in or prior to July and began declining in early fall. Growth was minimal between December and February 1996, but increased rapidly during spring. Frond elongation rates during 1995 were similar at the three sites, except for a steep decline at Garnet Point during fall due to scallop dragging. Similar patterns of growth were evident during 1996 at Bar Island and Mahar Point. Elongation rates in winter and spring, respectively, ranged from 0.69 (0.31) to 2.17 (0.95) cm frond-1 day-1 at Bar Island, and from 0.81 (n = 1) to 2.49 (0.29) cm frond-1 day-1 at Mahar Point (Table 2). Figure 3. Variation in frond elongation rates for Laminaria longicruris at three sites in Cobscook Bay during 1995–96. 152 Northeastern Naturalist Vol. 11, Special Issue 2 Although elongation rates in 1996 were slightly higher than in 1995, variation was considerably higher in 1996, thereby blurring possible differences between years. Table 2. Monthly frond measurements of Laminaria longicruris at three sites in Cobscook Bay during 1995–96. Frond Frond2 New growth FER3 (cm # plants length (cm) width (cm) (cm) blade-1 day-1) Date (days)1 mean SD mean SD mean SD mean SD Bar Island 07/15/95 10 (31) 184.9 51.4 30.6 6.5 47.3 13.1 1.53 0.42 08/11/95 38 (27)4 210.4 63.4 35.9 6.3 37.0 25.2 1.21 0.63 09/09/95 25 (29)5 189.9 58.3 40.0 7.4 41.4 26.7 1.24 0.64 11/28/95 11 (80) 135.9 28.3 29.2 5.8 79.8 26.9 1.00 0.34 01/18/96 3 (51) 93.2 44.8 27.5 11.0 35.0 15.7 0.69 0.31 03/21/96 16 (63) 130.7 52.5 28.8 7.0 26.7 8.7 0.95 0.31 04/17/96 6 (27)6 97.6 43.5 41.2 9.8 49.7 30.5 1.33 0.56 05/18/96 15 (31)7 181.3 64.4 49.1 11.4 92.0 46.6 2.17 0.95 07/01/96 8 (44) 251.9 92.4 47.8 6.8 80.9 40.6 1.83 0.92 07/30/96 12 (29) 251.4 73.8 48.0 9.3 61.7 20.2 2.13 0.70 Mean 14.4 (41.2) 174.3 56.6 36.9 8.8 55.1 22.4 1.41 0.50 Mahar Point 07/13/95 10 (30) 165.6 97.3 27.6 9.1 55.7 20.1 1.86 0.67 08/11/95 47 (29) 140.1 58.8 29.6 9.0 53.3 14.2 1.76 0.50 09/08/95 18 (28) 134.5 47.7 28.3 8.0 51.2 12.1 1.83 0.43 11/08/95 7 (61) 144.8 35.7 26.4 4.0 94.0 25.0 1.54 0.41 01/16/96 12 (69) 111.7 43.5 22.1 4.2 60.1 27.5 0.87 0.40 02/21/96 1 (36) 110.0 - 24.5 - 29.0 - 0.81 - 03/23/96 5 (31) 192.9 19.7 36.4 7.8 46.5 25.1 1.50 0.81 04/17/96 1 (25) 48.0 - 28.0 - 27.0 - 1.08 - 05/17/96 7 (30) 183.8 57.9 36.8 6.8 74.6 8.8 2.49 0.29 06/18/96 13 (32)8 141.2 60.5 31.1 16.5 52.0 12.3 1.56 0.44 07/01/96 12 (13)9 128.8 50.1 22.3 8.1 24.0 24.3 1.69 1.95 07/30/96 12 (29)10 117.4 32.8 16.8 5.1 50.3 39.1 1.49 0.98 Mean 12.1 (34.4) 134.9 38.0 27.5 5.8 51.5 19.8 1.54 0.46 Garnet Point 07/14/95 21 (29) 94.4 46.5 26.6 8.9 31.4 10.3 1.08 0.36 08/11/95 28 (28) 100.5 40.9 32.2 9.2 29.6 10.4 1.06 0.37 09/07/95 10 (27)11 118.4 41.7 37.9 9.0 48.4 22.0 1.60 0.43 11/08/95 1 (62) 79.3 - 10.1 - 39.5 - 0.64 - Mean 15 (36.5) 98.1 16.2 26.7 12.0 37.2 8.6 1.09 0.39 1Days between samples. 2Frond width is mean of frond width taken at 10 cm and 50 cm above apophysis. 3FER = frond elongation rate. 4Three kelps 58 days from previous sampling period. 5Two kelps 87days from previous sampling period. 6Two kelps 55 days from previous sampling period. 7Seven kelps 58 days from previous sampling period. 8One kelp 62 days from previous sampling period. 9Two kelps 45 days from previous sampling period. 10Three kelps at 42 days from previous sampling period. 11One kelp at 55 days from previous sampling period. 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 153 Distinct seasonal patterns were evident in both temperature and nitrate profiles at the three sites (Fig. 4). The patterns were not coincident, but rather showed inverse relationships to each other. The pattern for salinity was relatively flat (ca. 32 ppt) throughout the year, except at Bell Farm where there was considerable freshwater runoff in spring. Soluble phosphate showed a slight depression during late winter-early spring, but otherwise is similar throughout the year. Growth at the three sites appeared to be coincident with seasonal temperature curves, and therefore indirectly with irradiance levels (Fig. 4). However, maximum growth rates were achieved following maximum winter nitrate levels. Frond tissue nitrogen levels showed a seasonal pattern of change, being highest from fall through winter and lowest in mid- to late summer (Fig. 5). Percent nitrogen ranged from 1% in August to 3% in March at Mahar Point, the site with regular monthly tissue samples. Limited samples at Garnet Point showed a similar pattern from July Figure 4. Relationship between environmental variables and growth o f Laminaria longicruris at three sites in Cobscook Bay during 1995–96. A. Frond elongation rate (growth). B. Temperature and salinity of water samples. C. Nitrate and soluble phosphorus content of water samples. 154 Northeastern Naturalist Vol. 11, Special Issue 2 (0.93%) to December (2.24%). Irregular samples from Bar Island were inconclusive. Tissue phosphorus levels were broadly similar at Mahar and Garnet Points, being lowest in August and highest in late fall and winter (Fig. 5). The limited tissue data for Bar Island followed the general pattern of the other sites. Productivity Productivity of L. longicruris showed a strong pattern of seasonal activity and is clearly lowest between November and April (Fig. 6). Within-year patterns varied slightly among the three sites. Highest estimates in 1995 were in September at Garnet Point. In 1996, the highest estimates were in June and July at Bar Island. There was considerable variation in productivity, particularly during the periods of rapid growth. Productivity estimates also varied between years. Specific Figure 5. Nitrogen (%) and p h o s p h o r u s (ppm) content in Laminaria longicruris tissue at three sites in Cobscook Bay during 1995–96 (BI = Bar Island, GP = Garnet Point, MP = Mahar Point; N = nitrogen, P = phosphorus). Figure 6. Productivity of Laminaria longicruris at three sites in Cobscook Bay during 1995–96. 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 155 estimates of productivity at Bar Island ranged from 0.42 ± 0.31 to 8.61 ± 2.37 g dry m-2 day-1 (Table 3). The mean estimates of productivity for Mahar Point and Garnet Point exhibited a lower and narrower range of values, 0.25 (n = 1) to 3.67 ± 0.79 g dry m-2 day-1 and 0.46 (n = 1) to 5.82 ± 2.27 g dry m-2 day-1, respectively. To permit comparison with previous studies, productivity estimates were also converted to carbon and expressed as g C m-2 day-1. The overall range of productivity estimates based on carbon was 0.08 (n = 1) g C m-2 day-1 to 2.58 ± 0.71 g C m-2 day-1. Table 3. Mean frond biomass, productivity1, and turnover of Laminaria longicruris at three sites in Cobscook Bay during 1995–96. Biomass Productivity (g dry m-2) (g dry m-2 day-1) Turnover # of days Date mean SD mean SD per year for turnover Bar Island 07/15/1995 443.8 136.1 4.36 1.32 3.59 101.7 08/11/1995 579.8 196.1 4.20 2.16 2.64 138.3 09/09/1995 648.5 290.5 3.17 1.88 1.78 205.1 11/28/1995 327.7 139.8 2.23 1.04 2.49 146.6 01/18/1996 66.4 43.3 0.42 0.31 2.32 157.3 03/21/1996 99.6 60.4 0.51 0.26 1.86 196.2 04/17/1996 279.7 172.0 3.09 1.89 4.03 90.6 05/18/1996 651.9 291.7 6.88 3.69 3.85 94.8 07/01/1996 858.4 287.1 7.27 3.47 3.09 118.1 07/30/1996 866.3 236.0 8.61 2.37 3.63 100.6 Mean 482.2 286.9 4.07 2.79 2.93 124.6 Mahar Point 07/13/1995 263.6 172.8 3.47 1.88 4.81 75.9 08/11/1995 240.8 114.5 3.47 1.48 5.26 69.4 09/08/1995 261.6 120.4 3.06 1.30 4.27 85.5 11/08/1995 199.6 69.8 2.07 0.79 3.79 96.3 01/16/1996 42.0 26.6 0.29 0.20 2.49 146.6 02/21/1996 43.4 - 0.25 - 2.07 176.3 03/23/1996 135.2 31.9 0.76 0.38 2.06 177.2 04/17/1996 47.4 - 0.96 - 7.36 49.6 05/17/1996 330.5 151.3 3.67 0.79 4.06 89.9 06/18/1996 209.9 162.2 1.82 1.26 3.16 115.5 07/01/1996 179.8 98.0 2.64 3.05 5.36 68.1 07/30/1996 124.9 48.3 1.83 1.33 5.36 68.1 Mean 173.2 95.9 2.03 1.26 4.17 87.5 Garnet Point 07/14/1995 301.5 285.8 2.64 1.80 3.20 114.1 08/11/1995 390.3 293.7 3.17 2.03 2.96 123.3 09/07/1995 526.1 266.5 5.82 2.27 4.04 90.3 11/08/1995 65.3 - 0.46 - 2.58 141.5 Mean 320.8 193.7 3.02 2.20 3.20 114.1 1See Table 1 for number of plants sampled and number of days between sampling periods. 156 Northeastern Naturalist Vol. 11, Special Issue 2 Turnover Monthly estimates of turnover rates of L. longicruris varied throughout the year (Table 3). There was a subtle trend to these rates, being slightly higher in spring and somewhat lower during winter. However, the mean number of turnovers per year for the three sites was similar and ranged from 2.9 to 4.2. Based on monthly estimates, turnover times at the three sites ranged from 7 (Mahar Point) to 29 (Bar Island) weeks. Kelp fronds at Garnet Point turned over in 16 weeks (average of 3.2 turnovers per year). Discussion These studies were undertaken to determine kelp growth and productivity in Cobscook Bay. We were also interested in determining if the variation in flow regimes affected productivity, how fast fronds were turning over, and the general contribution of kelp populations to detrital pools in the Bay. Our data show that these sublittoral fringe populations are productive strips of shoreline. The kelp bed at Bar Island had maximum productivity values of 8.61 ± 2.37 (mean = 4.07 ± 2.79) g dry m-2 day-1 (Table 3). Maximum estimates for the other two sites, Mahar and Garnet Points, were 3.67 ± 0.79 (mean = 2.03 ± 1.26) and 5.82 ± 2.27 (mean = 3.02 ± 2.20) g dry m-2 day-1, respectively. The estimates for the latter two sites must be regarded as tentative since scallop dragging occurred at or near both sites, thereby reducing productivity. Frond elongation rates exhibited a seasonal pattern of growth consistent with this latitude (45°) and marine biogeographic region. Mean growth rates peaked (2.2–2.5 cm frond-1 day-1 ) in late spring–early summer, declined in early fall, and were minimal during winter. These rates (Table 2) are comparable to values from Nova Scotia (Gerard and Mann 1979) and for non-digitate Laminaria spp. in general (Egan and Yarish 1990). The seasonal pattern for growth rates is typical for the region (Brady-Campbell et al. 1984), but differs in an important way. Unlike most populations in Nova Scotia and southern New England, kelps in Cobscook Bay continued to grow well into summer, and growth did not decline until fall. Anderson et al. (1981) had observed a similar pattern in the St. Lawrence estuary. The wide range of intra-annual variability in our growth rates probably reflect patterns of mortality, low in summer, when large fronds remained intact and relatively persistent for several months, and very high in late fall to early spring. Mortality in the latter period likely reflects high natural mortality and the short (2 yr) life span of L. longicruris (Smith 1985). Also, ice disturbance (especially at Bar Island), damage from winter storms, and freshwater runoff from snow melt contributed to mortality. Smith (1985) acknowledged ice damage to be a problem at his shallower (2–3 m) site. In addition, anthropogenic 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 157 disturbance due to dragging for sea urchins and scallops, most notably at Garnet Point, contributed additively to kelp mortality. Growth rates closely paralleled temperature from summer through fall, similar to that observed for kelp by Hatcher et al. (1977). However, the increase in growth during spring preceded the rise in temperature (Fig. 4a,b), suggesting that irradiance levels rather than temperature per se controlled spring growth in Laminaria. Interestingly, Phinney et al. (2004) suggested that the modulation of temperature by tidal action could account for the seasonal pattern of productivity in phytoplankton and benthic diatoms in Cobscook Bay. They theorized that, on the basis of Garside and Garside (2004), nutrients were not limiting to these microalgal groups. However, nutrients, especially nitrate, appear to be important in controlling kelp growth in Cobscook Bay. This is supported by the presence of high nitrate levels throughout winter prior to rapid growth. Garside and Garside (2004) showed indirectly that nitrate was utilized in Cobscook Bay by both micro- and macro-algae, and that herbivores, through the regeneration of ammonia, played a large role in making nitrogen available. Experimental studies by Chapman and Craigie (1977) demonstrated that kelps could continue to grow during summer in Nova Scotian waters when provided with nitrogen. Also, several kelp species, including L. longicruris, can accumulate nitrate in their tissues during surplus periods and utilize it when nutrients are depleted in the water column (Chapman and Craigie 1978, Egan and Yarish 1990); this appears to be the situation with L. longicruris in Cobscook Bay. Nitrogen levels in the fronds were highest prior to rapid growth in the spring and lowest in late summer following the period of sustained growth (Fig. 5). Gagne and Mann (1981) indicated that L. longicruris had different growth strategies depending on nitrogen, and that nitrogen availability, and not temperature, determined the seasonality of growth in their studies. The relatively high productivity estimates for Bar Island in 1996 (Fig. 6) suggest that kelp biomass and productivity in Cobscook Bay may be higher at low flow sites. However, our attempts to detect differences in relative flow rates at this and other sites were inconclusive (Vadas et al. 2004). One possible explanation for the higher production at Bar Island is frond morphology. Individuals at that site had a higher frond-to-stipe ratio than plants at other sites. Fronds at Bar Island were wider and had a larger surface area than kelps at the headlands (Table 2). Such thallus features are characteristic of kelps in lower flow regimes (Gerard and Mann 1979). Conversely, lower frond to stipe ratios are characteristic of kelp in wave exposed habitats (Kain 1971), and were exhibited by plants in high flow regimes at several (non-studied) sites in the Bay (R.L.Vadas, pers. observ.). In addition, the kelp bed at Bar Island was denser than the populations 158 Northeastern Naturalist Vol. 11, Special Issue 2 at the two high-flow sites. Unfortunately, disturbance from the direct (Mahar Point) and indirect (Garnet Point) effects of dragging on plants and the lack of paired replicate low -low sites prevents a clean test of the flow hypothesis. The seasonal estimates of productivity (0.08 [n = 1] to 2.58 ± 0.71 g C m-2 day-1) observed for kelp in Cobscook Bay are within the range of other estimates from the northwest Atlantic Ocean. The mean productivity estimates (g C m-2 day-1) for our three sites are 1.22 ± 0.84 (Bar Island), 0.61 ± 0.378 (Mahar Point), and 0.91 ± 0.66 (Garnet Point: incomplete, five month estimate). Earlier mean productivity estimates (g C m-2 day-1) from eastern Nova Scotia range from 1.17 (Hatcher et al. 1977) to 5.21 (Mann 1982). Gerard and Mann (1979), also working in eastern Nova Scotia, observed a value of 1.77 g C m-2 day-1 (see Smith 1988). In general, these estimates are slightly higher than the values observed in Cobscook Bay. However, our estimates of mean productivity are more similar to those (1.12 g C m-2 day-1) from southwestern Nova Scotia (Gagne and Mann 1981, Smith 1988). Our estimates are lower than estimates from southern New England (Brady-Campbell et al. 1984, Egan and Yarish 1990). These two patterns suggest that the productivity of Laminaria longicruris has a latitudinal trend, possibly mediated through irradiance and/or temperature. Also, the depth and turbidity created by the (6–8 m) tidal range, and the strong currents and extensive mudflats, respectively, may limit light penetration and hence, kelp growth in the Bay. In addition, our estimates of productivity are slightly lower than other Laminaria species (1.43 g C m-2 day-1, Kain 1979) from outside this geographic area. However, the general similarity of data from divergent regions and kelp species suggests that sublittoral fringe populations in Cobscook Bay are as efficient as typical subtidal populations. The differences in production appear to be due to the lower density of plants in these stands. Alternatively, we may have underestimated productivity because of 1) the limited size range (> 50 cm) of plants used in our density estimates, and 2) the disturbance and damage to fronds from dragging at Garnet and Mahar Points. Total (areal) productivity for Laminaria longicruris in Cobscook Bay was surprisingly high given the narrow width of the kelp beds. Estimates were made based on the areal estimates of various habitat types made by Larsen et al. (2004). We determined the area of kelp based on their “algal flat” category, which indicated that both green and brown algae contributed to this class. Also, our observations suggest that kelps generally are not a dominant feature of this algal flat category. However, when kelp are present at a site, they tend to form a canopy and a small bed. Therefore, we estimate conservatively that 10% of their algal flat category, or 75 hectares, of the Bay is in Laminaria production. Using the above value for Bar Island (1.22) x 75,000, total kelp production 2004 R.L. Vadas, B.F. Beal, W.A. Wright, S. Nickl, and S. Emerson 159 in the Bay is estimated to be 91,500 g C day-1 or 3.34 x 107 g C year-1. The exclusion of Agarum clathratum, a slow growing kelp (Mann 1973, Vadas 1968), Laminaria saccharina, and Saccorhiza dermatodea (Bach. Pyl.) Aresch., an annual kelp, from our studies necessarily means that total kelp production is an underestimate. Fringe kelp populations in Cobscook Bay are contributing large amounts of carbon to the Bay’s ecosystem and may be recycling carbon more quickly than typical subtidal forests. The average length of fronds at the three sites ranged from 0.98 ± 0.16 m at Garnet Point to 1.74 ± 0.57 m at Bar Island (Table 2). These fronds are turning over 3 to 4 times per year (Table 3). Much of this biomass is cycled into the Bay as drift and detrital material, either naturally or inadvertently through disturbance from dragging. A smaller fraction is consumed directly and indirectly (drift) by herbivores (e.g., Littorines, green sea urchins). Thalli of fringe plants may be more easily damaged because of their emergence and exposure to the elements on low tides. Wind, freezing air temperatures, thermal stress or bleaching, cast-up debris, and ice scour (at Bar Island) can be sources of disturbance during exposure to air, and likely increase the probability of breakage or dislodgement. In addition, because of the shallow nature of these sites, hydrodynamic effects may be accelerated, thereby increasing frond damage and turnover. The latter is consistent with the pattern of frond turnover in Cobscook Bay, which was highest at the high-flow (headland) sites. Interestingly, the impact of dragging, observed at Garnet Point in the fall of 1995, resulted in a large and premature pulse of energy to sea urchins as well as herbivorous gastropods in the subtidal. Drift kelp is known to be an important source of nutrition to sea urchins in nearshore communities (Dean et al. 1984, Mann 1977, Minor and Scheibling 1997). In this case, dragging appears to have accelerated the recycling process and increased the amount of detrital inputs in the fall, instead of a more gradual detrital contribution throughout fall and winter. What effect(s) the annual fall dragging and premature kelp turnover have on benthic community structure and the functioning of the Bay may be significant, but remains unknown. Acknowledgments We thank Nancy Prentiss, Pam and Phil Garwood, Jennifer Aspinall, Jeff Rodzen, and Ken Vencile for field and laboratory assistance; Bruce Hoskins for running the nutrient analyses; and Dennis Anderson for assistance with figures. We thank property owners on Cobscook Bay (Bob and Terry Bell, Mr. and Mrs. Alfred Devin, and Nancy and Mark Prentiss) for allowing us access to their shorelands. We acknowledge the support of the Maine Agricultural and Forestry Experimental Station and the Maine Sea Grant Program. This work was conducted as part of a research program, “Developing an Ecological Model of a 160 Northeastern Naturalist Vol. 11, Special Issue 2 Boreal, Macrotidal Estuary: Cobscook Bay, Maine,” funded by a grant from the A.W. 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