Printer Friendly

Field study of growth and calcification rates of three species of articulated coralline algae in British Columbia, Canada.


Coralline algae (Corallinales and Sporolithales, Rhodo-phyta) are important components of marine communities worldwide, cementing coral reefs (Steneck and Adey, 1976) and quickly colonizing bare rock to provide habitat for other algae and invertebrates (Kelaher et al., 2002). Corallines and their associated biofilm (Huggett et al., 2006) induce settlement of a wide range of invertebrate larvae, including echinoderms (e.g., Rowley, 1989; Johnson et al., 1991; Swanson et al., 2006), annelid worms (e.g., Gee and Knight-Jones, 1962; Gee, 1965), molluscs (e.g., Barnes and Gonor. 1973; Heslinga, 1981; Rumrill and Cameron, 1983; Morse and Morse, 1984), soft corals (e.g., Sebens, 1983; Benayahu et al., 1989; Lasker and Kim, 1996), and scler-actinian corals (e.g., Harrigan, 1972; Morse et al., 1988; Heyward and Negri, 1999; Kitamura et al., 2007). Even sponges, arguably the oldest of the extant animal phyla. have recently been found to settle and metamorphose preferentially on a species of articulated coralline algae (Avila and Carballo, 2006). Moreover, as they calcify, coralline algae precipitate calcium carbonate in their cell walls, thereby removing carbon from the biological carbon cycle and incorporating it into the geological carbon cycle (Smith, 1972; Steneck, 1986).

Coralline algae are threatened by the decline in ocean pH resulting from increasing atmospheric C[O.sub.2] (Nelson, 2009). Decreases in settlement, growth, and calcification of coral-line algae in response to elevated C[O.sub.2] have already been documented in laboratory studies (Gao et al., 1993; Orr et al., 2005; Jokiel et al., 2008; Kuffner et al., 2008; Martin and Gattuso, 2009; Porzio et al., 2011, 2013; Diaz-Pulido et al., 2012; Ragazzola et al., 2012; Noisette et al., 2013a; Kroeker et al., 2013) and some field studies (Kroeker et al., 2012; McCoy, 2013), although responses may be species-specific (Noisette et al., 2013b) and physiological adaptation may be possible (Ragazzola et al., 2013). As the saturation state of calcium carbonate decreases globally with decreasing pH, calcification, growth, and competitive ability of coralline algae may be impacted (Orr et al., 2005; Andersson et al., 2008; Gao and Zheng, 2010; Kroeker et al., 2013), potentially altering marine communities and near-shore carbon cycles. A loss of coralline algae would have wide-ranging implications for coastal ecosystems, and even a slight decline in growth, skeletal integrity, or calci-fication rates (Ragazzola et al., 2012; McCoy, 2013) would impact marine carbon sequestration worldwide (Smith, 1972; Steneck, 1986; Daume et al., 1999; Andersson et al., 2008; Chung et al., 2011).

Baseline studies of coralline demography are needed if we are to detect the impacts of climate change on corallines in the field, but such studies are lacking in the literature. The complexity of the intertidal zone makes replicating field conditions in a laboratory nearly impossible; field studies are necessary to gain a more complete perspective on the growth rates of organisms (Kholer, 2002; Calisi and Bently, 2009). Coralline algae are often characterized as slow-growing and long-lived, but the literature reveals large discrepancies in estimated ages and growth rates, with very few studies performed in the field (but see Johansen and Austin, 1970; Steneck, 1986; Goldberg and Foster, 2002; Blake and Maggs, 2003; Martone, 2010). For example, individual fronds of Calliarthron, a common genus of articulated coralline algae, have been estimated to live for 3 to 10 years (Johansen and Austin, 1970; Foster, 1975; Martone, 2010). As the ocean changes, it will become increasingly important to have accurate information about the growth of these organisms in the field in order to monitor them for changes in performance. Slow-growing species may be more vulnerable and slower to recover or adapt to changes in climate (Done, 1988; Macdonald et al., 1996)

This study documents the growth and calcification rates of three species of articulated coralline algae commonly found on the coast of British Columbia (Fig. I A, B): Boss-iella plumosa (Manza) P.C. Silva, Corallina vancouveriensis Yendo, and Calliarthron tuberculosum (Postels and Ruprecht) E.Y. Dawson. To date, no prior studies have examined growth rates of corallines in the field along the British Columbia coast, and the goal of this study is to establish baseline data on growth and calcification rates to help characterize the vulnerability of corallines in this eco-system and to explore the potential importance of corallines to nearshore carbon cycles.

Materials and Methods

Coralline algae were studied at Botanical Beach, Port Renfrew, British Columbia (48.529253[degrees] N, 124.453704[degrees] W). Ten plants each of Bossiella plumosa, Corallina van-couveriensis, and Calliarthron tuberculosum were selected from tidepools in the upper-mid intertidal region, about 1.5 m above mean lower low water (Fig. 1A, B). Each plant consisted of about 20-50 segmented upright fronds of dif-ferent sizes, emerging from a crustose base; each frond had one to several branches, each ending in an apical meristem (see Johansen, 1981). Representative voucher specimens of Bossiella plumosa and Corallina vancouveriensis were deposited into the University of British Columbia Herbar-ium for future taxonomic reference (A88702-A88705). All plants had signs of good health including pink color, robust shape, and few epiphytes. Plants growing on mussels or other organisms were not considered. Plants were stained in situ by submersion in resealable plastic bags with 500 ml of 0.04% Calcofluor white solution (Sigma-Aldrich, St. Louis, MO, Fluorescent brightener 28) for 5 to l0 min following the protocol of Martone (2010). Plants were left to grow in the field for 29 days from 9 July to 8 August 2010, after which time all fronds from each plant were harvested. Throughout the experiment, air temperatures were recorded at the Port Renfrew weather station ( and sea surface water temperature and salinity were recorded at the Amphitrite Lighthouse (Fisheries and Oceans Canada, Total solar irradiance and photosynthetically active radiation (PAR) were recorded at the Friday Harbor Laboratories weather tower on San Juan Island, Washington (wx.fhl.washington. edu/vdv) using a pyranometer (LI200X, Campbell Scientific, Logan, UT) and quantum sensor (LICOR, Lincoln, Nebraska), respectively. Tide heights were estimated using Mr. Tides (ver. 3.0, Hahn Software, 2007).

Two metrics were used to calculate growth rates. The first was the change in length of each frond; the second was the change in area. We calculated both metrics for Calliarthron and Bossiella, but only the change in length for Corallina due to its irregular three-dimensional growth habit. For both metrics, 3-7 fronds of varying sizes were selected from each plant and photographed under a black light (330-400 nm, Peak: 365 nm; Effects by Globe Electronics, Ottawa, ON). All photographs were taken using a Canon Inc. (Tokyo, Japan) EOS Rebel XT digital SLR camera with exposure set between 5 and 30 s. ImageJ software ver. 1.43u (U. S. National Institutes of Health, Bethesda, MD) was used to measure the average length of new growth in a linear direction-the distance between the top of the stain and the edge of the meristems on each frond (Fig. IC). To calculate the total growth over 29 days, ImageJ was used to calculate the frond area between the Calcolluor white stain and the edges of frond meristems (see Fig. IC). Up to five random meristems were measured and averaged per frond, and three to seven fronds of varying sizes were measured per plant. The effects of plant identity (n = 9; fixed factor) and frond area (covariate) on linear growth rate were tested using ANCOVA. Growth rates and area were log-transformed and tested for normality (Shapiro-Wilk test) and equal variances (Levene's test). For Bossiella, the total number of meri-stems was also counted to test whether larger fronds have more meristems, as previously documented for Calliarthron (Martone, 2010).

To estimate ages of Bossiella and Calliarthron, growth rate ([delta]A/[delta]t) was plotted against total planform area of each frond (A), and Microsoft Excel software was used to fit a power curve to the data to solve for rate constants K1 and K2:


This equation was rearranged and manually integrated to determine a relationship between area and time:


Thus, it was possible to use frond size (A) to calculate its approximate age (t),and it was possible to predict frond size (A) after a given amount of time,



Fifteen additional, unstained plants of each species were collected from Botanical Beach. These plants were oven-dried at 40 [degrees]C overnight and weighed before being decal-cified overnight in 1 mol I-1 HCI to remove all Ca[CO.sub.3]. Plants were again oven-dried at 40 [degrees]C overnight and weighed once more to determine a value for the percent mass of Ca[CO.sub.3] for each species. Differences in calcium carbonate content were analyzed among species using ANOVA (fixed factor, three levels). To derive a relationship between area and Ca[CO.sub.3], mass of each experimental frond was corrected by each species-specific Ca[CO.sub.3] percentage, and a linear regression was then fitted to frond area plotted against mass Ca[CO.sub.3].


From 9 July to 8 August 2010, solar irradiance often reached 400-850 W m-2 daily, and PAR values often reached 900-1800 pmol M-2 S- I (Fig. 2A). Average daily sea surface water temperatures were 13.1 [+ or -] 0.9 [degrees]C and air temperatures were 15.1 [+ or -] 1.3 [degrees]C (mean [+ or -] SD) (Fig. 2B). During this time period, tide heights dropped below 1.5 m only before 1310 h or after 2100 h, suggesting that tidepool temperatures may not have much exceeded water temperatures. Sea surface salinity was 30.1 [+ or -]. 0.4 psu.

A wide range of frond sizes were effectively stained and monitored in each species: 0.07-20.8 [cm.sup.2] in Bossiella, 0.07-44.0 [cm.sup.2] in Calliarthron, and 0.03-13.9 [cm.sup.2] in Car-olina. On average, Bossiella fronds grew in length by 0.22 -[+ or -] 0.05 cm mon- I, Calliarthron fronds grew 0.17 0.03 cm mon- I, and Corallina fronds grew 0.15 [+ or -] 0.02 cm mon - (Figs. 3-4). Fronds of all three species followed similar growth trajectories (ANCOVA, Area X Plant, Boss-iella: P = 0.24, Calliarthron: P = 0.10, Corallina: P = 0.09) (Fig. 3A-C). On average, linear frond growth rate did not vary with frond size (ANCOVA, Area, Bossiella: P = 0.25, Calliarthron: P = 0.59, Corallina: P = 0.75) (Fig. 3A-C), although within each species, fronds from different individual plants grew at slightly different rates (ANCOVA, Plant, Bossiella: P < 0.05, Calliarthron: P < 0.01, Coral-lina: P < 0.05). Mean growth rates were significantly different among species (ANOVA, P < 0.01, Fig. 4). Boss-iella fronds grew significantly faster than fronds produced by Calliarthron and Corallina (Tukey's HSD, P < 0.05; Fig. 4).

The three coralline species do not calcify equally (ANOVA, P < 0.001; Fig. 5). Corallina fronds were com-posed of significantly less Ca[CO.sub.3] (65.2 -[+ or -] 3.0% Ca[CO.sub.3] per dry mass) than fronds produced by Bossiella and Calliar-thron (85.0 [+ or -] 1.7% and 84.2 [+ or -] 1.0% Ca[CO.sub.3] per dry mass, respectively) (Tukey's HSD, P < 0.05; Fig. 5).

In Bossiella, although linear growth rate did not vary with frond size (Fig. 3), larger fronds had more meristems (P < 0.001, R2 = 0.61; Fig. 6A). Because each meristem had the potential for growth, fronds with more meristems added more new frond area per month, thereby growing faster in overall size (P < 0.001, R2 = 0.76; Fig. 6B).

Bossiella and Calliarthron (Fig. 7A, B), and power curves were fitted to calculate constants described by Eq. 1. For Bossiella, K = 0.215 and K2 = 0.836, and for Calliarthron, = 0.080 and K2 = 0.611 (Eq. 1). Thus, according to Eq. 4,

A = (1.451 X 10 [sub.-9])t[sub.6.09] for Bossiella, and C = 35.0 A for Corallina (R2 = 0.84, P < 0.001),

where C is the calculated mass of Ca[CO.sub.3] (milligrams) and A is total planform area ([cm.sup.2]) of a frond. For Bossiella and Calliarthron, combining Eq. 5 and Eq. 6 yielded mass of Ca[CO.sub.3] accumulated per month (Fig. 7C, D):

C = (7.11 X 10[sub.-8])t[sup.6.09] for Bossiella, and C = (2.01 X 10[sub.-2])t[sup.2.57]." for Calliarthron. (7)

Thus, we estimated that the largest observed Bossiella frond (20 cm[sup.2]) had accumulated 1.0 g of Ca[CO.sub.3] in about 4 years (Fig. 7C), whereas a growing Calliarthron. frond accumulated 1.0 g of Ca[CO.sub.3] in 5.6 years (Fig. 7D). The largest observed Calliarthron frond (40 cm[sup.2]) had accumulated approximately 6.0 g of Ca[CO.sub.3] in about 11 years (Fig. 7D).


Growth rates of articulated corallines in the field are generally slow (<3 mm mon[sup.-1]), although still faster than most encrusting and maerl-forming corallines, which may grow less than 2.5 mm per year (Adey and McKihbin, 1970; Blake and Maggs, 2003; Rivera et al., 2004; Frantz et al., 2005; Schafer et al., 2011). This is in contrast to other temperate algae, such as the kelps Nereocystis luetkeana and Alaria marginata, which can produce new blade tissue at rates of 4-14 cm per day (Kain, 1987; Maxell and Miller, 1996; McConnico and Foster, 2005). Growth rates of cor-alline species in British Columbia are similar to those in California. For example, growth rates of Calliarthron tuberculosum growing subtidally off central California range from 0.125 to 0.17 cm/mon (Johansen and Austin, 1970; Goldberg and Foster, 2002), similar to rates reported for intertidal Calliarthron in British Columbia (0.17 cm/mon; Table 1). Johansen and Austin (1970) noted that subtidal growth rates of Calliarthron were fastest in the winter when kelp forests had thinned and light levels in-creased. Similarly, Halfar et al. (2011b) reported that light availability was the primary determinant of growth in long-lived crustose coralline algae. Thus, light availability may help explain the similarity in growth rates of unshaded intertidal corallines described here and unshaded subtidal corallines in California (Johansen and Austin, 1970). Further work is needed to disentangle the individual and interactive effects of abiotic factors (such as light, temperature, and nutrients) on growth rates. In particular, the effect of temperature on coralline growth rates can vary (Kamenos and Law, 2010; Halfar et al. 2011a, b). Interestingly, much faster growth rates have been documented in the closely related species Calliarthron cheilosporioides growing in a California intertidal habitat (0.28 cm/mon; Martone, 2010), suggesting that growth rates may not be generalizable among congeneric coralline species (Table 1).

Comparison of linear growth rates among several species of articulated
coralline algae

    Species       Genus           Average growth     Study Site
                                (cm [mon.sup.-1])

gardneri          Bossiella     0.33               Laboratory

plumosa                         0.22               Intertidal

officinalis       CoraBina      0.22               Laboratory

officinalis                     0.20               Subtidal

off/dm/is                       0.14               Intertidal

vancouveriensis                 0.15               Intertidal

vancouveriensis                 0.41               Laboratory

cheilosporioides  Calliarthron  0.28               Intertidal

tuberculosum                    0.17               Intertidal

tuberculosum                    0.17               Subtidal

tuberculosum                    0.41               Laboratory

spp                             0.13               Intertidal

    Species       State/Country  Reference

gardneri          CA, USA        Smith,

plumosa           BC. Canada     This

officinalis       MA, USA        Co'than

officinalis       N. Ireland     Blake and

off/dm/is         MA, USA        Andrake

vancouveriensis   BC, Canada     This

vancouveriensis   CA, USA        Smith,

cheilosporioides  CA, USA        Martone.

tuberculosum      BC, Canada     This

tuberculosum      CA, USA        Johansen

tuberculosum      CA, USA        Smith,

spp               CA, USA        Goldberg

Growth rates in the field are generally slower than those documented in the laboratory. For example, linear growth rates for Calliarthron tuberculosum and Corallina vancou-veriensis (0.17 and 0.15 cm/mon, respectively) are less than half that found for the same two species in the laboratory (0.41 cm/mon; Table 1). Higher growth rates in the laboratory suggest that natural conditions may limit the growth of coralline algae and that optimized laboratory conditions (e.g., light, nutrients, water motion) may induce unnatural rates of growth. For example, intertidal macroalgae are often nitrogen-limited (Howarth, 1988; Bracken, 2004), so laboratory cultures enriched with nitrogen may elevate growth rates above natural levels. The large discrepancy between laboratory and field growth rates suggests that researchers should be cautious when extrapolating results from laboratory studies to ecological or physiological performance in the field.

Prior studies by Johansen and Austin (1970) and Martone (2010) found that growth rates of coralline algae decrease as frond sizes increase. This decline in growth is expected for many organisms with determinate growth-growth rate decreases as organisms approach their maximum size (Laird, 1964; Kozlowski, 1992). In our study, linear growth rate did not decrease as frond size increased for any of the three species studied. Instead, linear growth rates were constant across all frond sizes (Fig. 3), and overall frond growth rates ([cm.sup.2] mon-1) increased with increasing number of meristems (Fig. 6B). This pattern of increasing growth rate with increasing frond size seems to indicate that articulated coralline algae in British Columbia exhibit primarily indeterminate growth, and they either do not have a predetermined maximum size or are not attaining their maximum size in this habitat. Martone and Denny (2008) demonstrated that articulated corallines experience greater wave-induced drag forces as they increase in size, ultimately dislodging large plants and thereby constraining maximum size. Observed patterns of exponential growth (Fig. 7) may exist only because drag forces limit the size of plants before physiological mechanisms cause growth to decline. Furthermore, Calliarthron may grow larger than other coralline generasimply because Calliarthron thalli (specifically, the joints or "genicula") can resist greater forces than thalli produced by Bossiella or Corallina (Martone, 2006; Janot and Martone, unpubl.). Further testing of the biomechanical properties of coralline algae is necessary to explore these hypotheses and to detect constraints on frond strength and frond size.

Individual fronds of Bossiella were estimated to live 4 years, while the largest Calliarthron fronds were estimated to live 11 years. Since articulated corallines have perennating basal crusts that continually replenish upright fronds, it is difficult to measure the age of a plant. Ages calculated in this study represent growth of individual fronds and should not be used to estimate ages of plants, which are likely much older. Spores of Calliarthron tube rculosum can form a basal crust in less than 1 mon and can begin developing fronds in 2 mon under laboratory conditions (Johansen and Austin, 1970). Such rapid development from spore to first frond suggests that additional data on spore germination rates may not greatly affect age predictions.

Age estimates assume that summer growth rates are representative of growth rates year-round, an assumption that should eventually be tested. Growth rates of Calliarthron tuberculosum vary seasonally in subtidal habitats, increasing when light penetration is greatest (Johansen and Austin, 1970). Because light and water temperatures are greatest in the summertime, we expect that values reported here rep-resent maximum growth rates and that age estimates are, therefore, conservative. If growth rates of intertidal articulated corallines slow down in the winter, as documented for other calcifying and noncalcifying macroalgae (Foster, 1975; Frantz et al., 2005; Halfar et al., 2008, 2013; Kamenos et al., 2008; Dethier and Williams, 2009; Kamenos and Law, 2010), then plants may be older than calculated here, making these slow-growing organisms even slower to grow and recover from disturbance. Preliminary data collected from tidepools on San Juan Island. Washington, from 15 October to 13 November 2013 suggest that growth rates of Calliarthron do not slow down in autumn (0.18 0.04 cm/mon), whereas growth rates of Corallina slow down significantly (0.05 [+ or -] 0.01 cm/mon), supporting the expected patterns proposed here (R. Guenther. University of British Columbia. pers. comm.). Further work is needed to refine the seasonality of articulated coralline growth, especially since these organisms lack the annual bands that have proven useful in determining growth periodicity of rhodolith and encrusting coralline species (Halfar et al., 2008, 2013; Kamenos et al., 2008).

As carbon cycle modeling becomes more advanced and integral to future climate models, accounting for the calcium carbonate (Ca[CO.sub.3]) sequestered by calcifying organisms may be important in fine-tuning these models. For example. using growth rates reported here, we can estimate the amount of calcium carbonate deposited along a stretch of shoreline with large populations of Bossiella. After 2 years, a single Bossiella frond will have deposited approximately 18 mg Ca[CO.sub.3], and after 3 years it will have deposited approximately 200 mg Ca[CO.sub.3]. At our field site, we ob-served Bossiella growing in dense patches of 15 fronds/[cm.sup.2]. so a quick calculation shows that 1 m2 of shoreline dominated by Bossiella may deposit up to 2.7 kg of Ca[CO.sub.3] after 2 years and 32 kg if all plants live to be 3 years old. This estimate assumes that all fronds belong to one cohort, settling together and growing at the same rate, and does not incorporate recruitment dynamics or density dependence, which are currently unknown. Nevertheless, because large swaths of coastline in British Columbia include coralline algae, this carbon sink may be significant, and contributions of coralline algae to carbon sequestration may be non-negligible. Previous research estimated that up to 4 kg Ca[CO.sub.3] m-2 yr-I may be deposited by calcifying sea-weeds-primarily crustose corallines in both temperate and tropical ecosystems (Smith, 1972; Freiwald and Hen-rich, 1994; Chisholm, 2000; Schafer et al., 2011). Results from our field study suggest that Ca[CO.sub.3] deposition rates of articulated corallines in British Columbia may exceed previous estimates. Further refining of growth and demographic rates of coralline algae could lead to a greater understanding of nearshore carbon cycling and modeling of global carbon budgets.


The authors thank F. Hodge, J. Jorve, and R. Guenther for their help in the field, and K. Hind. S. Starko, K. Janot, and three anonymous reviewers for their insightful comments on the manuscript. We gratefully acknowledge the Pacheedaht First Nation and BC Parks for granting permission to conduct this research at Botanical Beach in the Juan de Fuca Provincial Park (Permit 104149). This research was supported by a Natural Science and Engineering Research Council (NSERC) Discovery grant to P.T.M. and an NSERC CREATE scholarship awarded to K.F. through the UBC Biodiversity Research Centre.

Literature Cited

Adey, W. H., and D. L. McKibbin. 1970. Studies on maerl species Phymatolithon calcareum (Pallas) nov. comb. and Lithothamnion caralloides (Crouan) in the Rio Vigo. Bot. Mar. 13: 100-106.

Andersson, A. J., F. T. Mackenzie, and N. R. Bates. 2008. Life on the margin: implications of ocean acidification on Mg-calcite. high latitude and cold-water marine calcifiers. Mar. Ecol. Prog. Ser. 373: 265-273.

Andrake, W., and H. W. Johansen. 1980. Alizarin red dye as a marker for measuring growth in Corallina officMalis L. (Corallinaceae. Rho-dophyta). J. Phycol. 16: 620-622.

Avila, E., and J. L. Carballo. 2006. Habitat selection by larvae of the symbiotic sponge Haliclona caerulea (Hechtel, 1965) (Demospongiae. Haplosclerida). Symbiosis 41: 21-29.

Barnes, J. R., and J. J. Gonor. 1973. The larval settling response of the lined chiton Tonicella lineata. Mar. Biol. 20: 259-264.

Benayabu, Y., Y. Achituv, and T. Berner. 1989. Metamorphosis of an octocorai primary polyp ana us iniection oy aigat symptoms. aymmusts 72: 159-169.

Blake, C., and C. Maggs. 2003. Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from northern Europe. Phycologia 42: 606-612.

Bracken, M.E.S. 2004. Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga. J. PhycoL 40: 1032-1041.

Calisi, R. M, and G. E. Bently. 2009. Lab and field experiments: Are they the same animal? Harm. Behay. 56: 1-10.

Chisholm, J. R. M. 2000. Calcification by crustose coralline algae on the northern Great Barrier Reef, Australia. LinmoL Oceanogr. 45: 1476-1484.

Chung, I. K., J. Beardall, S. Mehta, D. Sahoo, and S. Stojkovic. 2011. Using marine macroalgae for carbon sequestration: a critical appraisal. J. Appl. Phycol. 23: 877-886.

Colthart, B. J., and H. W. Johansen. 1973. Growth rates or Corallina officinalis (Rhodophyta) at different temperatures. Mar. Biol. 18: 46-49.

Daume, S., S. Brand-Gardner, and W. J. Woelkerling. 1999. Community structure of nongeniculate coralline red algae (Corallinales, Rhodophyta) in three boulder habitats in southern Australia. Phycologia 38: 138-148.

Dethier, M. N., and S. L. Williams. 2009. Seasonal stresses shift optimal intertidal algal habitats. Mar. Biol. 156: 555-567.

Diaz-Pulido, G., K. R. N. Anthony, D. I Kline, S. Dove, and 0. Hoegh-Guldherg. 2012. Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J. Phycol. 48: 32-39.

Done, T. J. 1988. Simulation of recovery of pre-disturbance size in populations of Porites spp. damaged by the crown of thorns starfish Acanthaster planci. Mar. Biol. 100: 51-61.

Foster, M. S. 1975. Algal succession in a Macrocystis pyrifera forest. Mar. Biol. 32: 313-329.

Frantz, B. R., M. S. Foster, and R. Riosmena-Rodriguez. 2005. Clathromorphum nereostratum (Corallinales, Rhodophyta): the oldest alga? J. Phycol. 41: 770-773.

Freiwald, A., and R. Henrich. 1994. Reefal coralline algal build-ups within the Arctic Circle: morphology and sedimentary dynamics under extreme environmental seasonality. Sedimentology 41: 963-984.

Gao, K., and Y. Zheng. 2010. Combined effects of ocean acidification and solar UV radiation on phyotosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob. Change Biol. 16: 2388-2398.

Gao, K.. Y. Aruga, K. Asada, T. Ishihara, T. Akano, and M. Kiyohara. 1993. Calcification in the articulated corallinc algae Corallina pilu-lifera with special reference to the effect of elevated C[O.sub.2] concentration. Mar. Biol. 17: 129-132.

Gee, 1. M. 1965. Chemical stimulation of settlement in larvae of Spiror-bis rupestris. Anim. Behay. 13: 181-186.

Gee, J. M., and E. W. Knight-Jones. 1962. The morphology and larval behaviour of a new species of Spirorbis (Serpulidae). J. Mar. Biol. Assoc. UK 42: 641-654.

Goldberg, N. A., and M. S. Foster. 2002. Settlement and post-settlement processes limit the abundance of geniculate coralline algae on subtidal walls. J. Exp. Mar. Biol. Ecol. 278: 31-45.

Halfar, J., R. S. Steneck, M. Joachimski, A. Krontz, and A. D. Wana-maker. 2008. Coralline red algae as high-resolution climate recorders. Geology 36: 463-466.

Halfar, J., S. Hetzinger, W. Adey, T. Zack, G. Gamboa, B. Kunz, B. Williams, and D. E. Jacob. 2011a. Coralline algae growth-increment widths archive North Atlantic climate variability. Palaeogeogr. Pulaeoclimatol. Palaeoecol. 302: 71-80.

Halfar, J., B. Williams, S. Hetzinger, R. S. Steneck, P. Lebednik, C. Winsborough, A. Omar, P. Chan, and A. D. Wanamaker, Jr. 2011b. 225 years of Bering Sea climate and ecosystem dynamics revealed by coralline algae growth-increment widths. Geology 39: 579-582.

Halfar, J., W. H. Adey, A. Krontz, S. Hetzinger, E. Edinger, and W. W. Fitzhugh. 2013. Arctic sea-ice decline archived by multicentury annual-resolution record from crustose coralline algal proxy. Proc. Natl. Aced Sci. doi: 10.1073/pnas.1313775110.

Harrigan, J. 1972. The planula larva of Pocillopora damicomis: lunar periodicity of swarming and substratum selection behavior. Ph.D. thesis, Univ. of Hawaii. 319 pp.

Heslinga, G.A. 1981. Larval development, settlement and metamorphosis of the tropical gastropod Trochus niloticus Linnaeus. Malacologa 20: 349-357.

Heyward, A. J., and A. P. Negri. 1999. Natural inducers for coral larval metamorphosis. Coral Reefs 18: 273-279.

Howarth, R. W. 1988. Nutrient limitation of net primary production in marine ecosystems. Anna. Rev. Ecol. Syst. 19: 89-110.

Huggett, M. J., J. E. Williamson, R. de Nys, S. Kjelleberg, and P. D. Steinberg. 2006. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149: 604-619.

Johansen, H. W. 1981. Coranine Algae. A First Synthesis. CRC Press, Boca Raton, FL. Pp. 57-66.

Johansen, H. W., and L. F. Austin. 1970. Growth rates in the articulated coralline Calliarthron (Rhodophyta). Can. J. Bot. 48: 125-132.

Johnson, C. R., D. G. Muir, and A. L. Reysenbach. 1991. Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar. Ecol. Prog. Ser. 74: 281-294.

Jokiel, P. L., K. S. Rodgers, I. B. Kuffner, A. J. Anderson, E. F. Cox, and F. T. Mackenzie. 2008. Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27: 473-483.

Kain, J. M. 1987. Patterns of relative growth in Nereocystis luetkeana (Phacophyta). J. Phycol. 23: 181-187.

Kamenos. N., and A. Law. 2010. Temperature controls on coralline algal skeletal growth. J. PhycoL 46: 331-335.

Kamenos, N. A., M. Cusack, and P. G. Moore. 2008. Coralline algae are global palaeothermometers with biweekly resolution. Geochim. Co.smochim. Acta 72: 771-779.

Kelaher, B. P., M. G. Chapman, and A. J. Underwood. 2002. Spatial patterns of diverse macrofaunal assemblages in coralline turf and their associations with environmental variables. J. Mar. Biol. Assoc. UK 81: 917-930.

Kholer, R. E. 2002. Landscapes and Labscapes: Exploring the Lab-Field Border in Biology. University of Chicago Press, Chicago, IL. Pp. 1-22.

Kitamura, M., T. Koyama, Y. Nakano, and D. Uemura. 2007. Characterization of a natural inducer of coral larval metamorphosis. J. Exp. Mar. Biol. 340: 96-102.

Kozlowski, J. 1992. Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7: 15-19.

Kroeker, K. J., F. Micheli, and M. C. Gambi. 2012. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clint. Change 3: 156-159.

Kroeker, K. J, R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte, and J.-P. Gattuso. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19: 1884-1896.

Kuffner, L B., A. J. Andersson, P. L. Jokiel, K. S. Rodgers, and F. T. Mackenzie. 2008. Decreased abundance of crustose coralline algae due to ocean acidification. Nat. Geosci. 1: 114 - 117.

Laird, A. K. 1964. Dynamics of normal growth. Pp. 52-55 in Biological and Medical Divisors Annual Report, Argonne National Laboratory, Argonne, IL.

Lasker, H. R., and K. Kim. 1996. Larval development and settlement behavior of the gorgonian coral Plexaura kuna (Lasker, Kim and Coffroth). J. &p. Mar. Biol. Ecol. 207: 161-175.

Macdonald. D. S., M. Little, N. C. Eno, and K. Hiscock. 1996. Dis-turbance of benthic species by fishing activities: a sensitivity index. Aqua:. Conserv. 6: 257-268.

Martin, S., and J. P. Gattuso. 2009. Response of Mediterranean coral-line algae to ocean acidification and elevated temperature. Glob. Change Biol. 15: 2089-2100.

Martone, P. T. 2006. Size, strength, and allometry of joints in the articulated coralline Calliarthron. J. Exp. Biol. 209: 1678-1689.

Martone, P. T. 2010. Quantifying growth and calcium carbonate deposition of Calliarthron cheilosporioides (Corallinales, Rhodophyta) in the field using a persistent vital stain. J. Phvcol. 46: 13-17.

Martone, P. T., and M. W. Denny. 2008. To break a coralline: mechanical constraints on the size and survival of a wave-swept seaweed. J. Exp. Biol. 211: 3433-3441.

Maxell, B. A., and K. A. Miller. 1996. Demographic studies of the annual kelps Nereocystis luetkeana and Costaria costata (Laminariales, Phaeophyta) in Puget Sound, Washington. Bot. Mar. 39: 479-489.

McConnico, L., and M. Foster. 2005. Population biology of the intertidal kelp, Alaria marginata Postels and Ruprecht: a non-fugitive annual. J. Exp. Mar. Biol. Ecol. 324: 61-75.

McCoy, S. J. 2013. Morphology of the crustose coralline alga Pseudolitho-phyllum muricatum (Corallinales, Rhodophyta) responds to 30 years of ocean acidification in the Northeast Pacific. J. Phvcol. 49: 830-837.

Morse, A. N. C., and D. E. Morse. 1984. Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. J. Exp. Mao. Biol. Ecol. 75: 191-215.

Morse, D. E., N. Hooker, A. N. C. Morse, and R. A. Jensen. 1988. Control of larval metamorphosis and recruitment in sympatric agariciid corals. J. Exp. Mar. Biol. Ecol. 116: 193-217.

Nelson, W. A. 2009. Calcified macroalgae-critical to coastal ecosystems and vulnerable to change: a review. Mar. Freshw. Res. 60: 787-801.

Noisette, F., G. Duong, C. Six, D. Davoult, and S. Martin. 2013a. Effects of elevated pC[O.sub.2] on the metabolism of a temperate rhodolith Lithothamnion corallioides grown under different temperatures. J. Phy-col. 49: 746-757.

Noisette, F., H. Egilsdottir, D. Davoult, and S. Martin. 2013b. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J. Exp. Mar. Biol. Ecol. 448: 179-187.

Orr, J. C., V. J. Fabry, 0. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikun, N. Gruber, A. Lshida, F. Joos et al- 2005. An-thropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.

Porzio, L., M. C. Baia, and J. M. Hall-Spencer. 2011. Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400: 278 -287.

Porzio, L., S. L. Garrard, and M. C. Buia. 2013. The effect of ocean acidification on early algal colonization stages at natural C[O.sub.2] vents. Mar. Biol. 160: 2247-2259.

Ragazzola, F., L. C. Foster, A. Form, P. S. L. Anderson, T. H. Hans-teen, and J. Fietzke. 2012. Ocean acidification weakens the structural integrity of coralline algae. Glob. Change Biol. 18: 2804-2812.

Ragazzola, F.. L. C. Foster, A. U. Form, J. Buscher. T. H. Hansteen, and J. Fietzke. 2013. Phenotypic plasticity of coralline algae in a high C[O.sub.2] world. Ecol. Evol. 3: 3436-3446.

Rivera, M. G., R. Riosmena-Rodriguez, and M. S. Foster. 2004. Age and growth of Lithothamnion muelleri (Corallinales. Rhodophyta) in the southwestern Gulf of California, Mexico. Cienc. Mar. 30: 235-249.

Rowley, R. J. 1989. Settlement and recruitment of sea urchins (Strongy-locentrotus spp.) in a sea-urchin barren ground and a kelp bed: Are populations regulated by settlement or post-settlement processes? Mar. Biol. 100: 485-494.

Rumri S. S., and R. A. Cameron. 1983. Effects of gamma-aminobu-tyric acid on the settlement of larvae of the black chiton Katharina tunicata. Mar. Biol. 72: 243-247.

Schafer, P., H. Fortunato, B. Bader, V. Liebetrau, T. Bauch, and J. J. G. Reijmer. 2011. Growth rates and carbonate production by coralline red algae in upwelling and non-upwelling settings along the Pacific coast of Panama. Palaios 26: 420-432.

Sebens, K. P. 1983. Settlement and metamorphosis of a temperate soft-coral larva (Alcyonium siderium Verrill): induction by crustose algae. Biol. Bull. 165: 286-304.

Smith, S. V. 1972. Production of calcium carbonate on the mainland shelf of southern California. Limnol. Oceanogr. 17: 28-41.

Steneck, R. S. 1986. The ecology of coralline algal crusts: convergent patterns and adaptative strategies. Annu. Rev. Ecol. Syst. 17: 273303.

Steneck, R. S., and W. H. Adey. 1976. The role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal reef builder. Bot. Mar. 19: 197-216.

Swanson, R. L., R. de Nys, M. J. Huggett, J. K. Green, and P. D. Steinberg. 2006. In situ quantification of a natural settlement cue and recruitment of the Australian sea urchin Holopneustes purpurascens. Mar. Ecol. Prog. Series 314: 1-14.


Botany Department and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

* To whom correspondence should he addressed. E-mail: pmartone@
COPYRIGHT 2014 University of Chicago Press
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2014 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Fisher, K.; Martone, P.T
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:1CANA
Date:Apr 1, 2014
Previous Article:Handed behavior in hagfish-an ancient vertebrate lineage and a survey of lateralized behaviors in other invertebrate chordates and elongate...
Next Article:Burrowing behavior in mud and sand of morphologically divergent polychaete species (Annelida: Orbiniidae).

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters