- Email: [email protected]
Space competition between seagrass and Caulerpa prolifera (Forsskaal) Lamouroux following simulated disturbances in Lassing Park, FL
Journal of Experimental Marine Biology and Ecology 333 (2006) 49 – 57 www.elsevier.com/locate/jembe
Space competition between seagrass and Caulerpa prolifera (Forsskaal) Lamouroux following simulated disturbances in Lassing Park, FL Nathaniel B. Stafford *, Susan S. Bell Department of Biology, University of South Florida—SCA 110, 4202 E. Fowler Avenue, Tampa, FL 33620-5200, United States Received 5 January 2005; received in revised form 22 November 2005; accepted 29 November 2005
Abstract An experimental study was conducted in Tampa Bay, FL to examine the response to disturbance of two co-occurring subtidal plants: the alga Caulerpa prolifera and the seagrass Halodule wrightii (Ascherson). Some recent studies have called into question the assumption that fast-growing rhizoidal Caulerpa species have the potential to outcompete and rapidly replace local seagrasses. In the Fall of 2002 an abrupt appearance of Caulerpa prolifera was noted in a shallow embayment in Tampa Bay previously dominated by seagrasses. Natural disturbance events were simulated by excavating 0.5 0.5 m plots in an area with monospecific C. prolifera and mixed C. prolifera and H. wrightii. Above and below-ground biomass were removed, and recovery of above-ground cover into the newly created gaps was monitored over 15 months. In addition to measuring the recovery of both species, the spatial pattern of Caulerpa recovery from the simulated disturbances was also analyzed. Simulated gaps were rapidly (5–8 months, depending on sampling resolution) and exclusively reoccupied by C. prolifera, with the recovery occurring predominantly via lateral expansion from gap edges rather than colonization by fragments. Therefore, while rhizoidal algae may or may not be able to supplant existing seagrasses by overgrowth or other forms of direct competition, disturbance events that remove seagrass and create bare areas may allow C. prolifera to replace seagrasses over time via preemption of space should an algal bloom such as this be persistent. D 2005 Elsevier B.V. All rights reserved. Keywords: Bloom; Caulerpa; Disturbance; Recovery; Seagrass; Space competition
1. Introduction In the past 15 years rhizoidal algae of the genus Caulerpa have gained notoriety as they have invaded many subtidal landscapes. For example, Caulerpa taxifolia (Vahl) C. Agandh has been recently introduced into new areas of the Mediterranean, where it has * Corresponding author. Tel.: +1 813 974 5420; fax: +1 813 974 3263. E-mail address: [email protected] (N.B. Stafford). 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.11.025
established both persistent and spatially expanding populations among seagrass beds (Meinesz, 1997; Meinesz et al., 2001). Likewise, Caulerpa racemosa has been identified as an invasive species in the western Mediterranean (Piazzi et al., 2001). Additionally, C. taxifolia was reported as an invasive in seagrass beds on the west coast of the U.S.A. in 1999 (Jousson et al., 2000), and has appeared in Australia in recent years as well (e.g. Schaffelke et al., 2002; Millar, 2004). Of special concern in the above studies is that the presence of species of Caulerpa could lead to a habitat
50
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
shift. Specifically, Caulerpa might displace seagrass either by direct overgrowth of the seagrass and/or by rapid occupation of open space by Caulerpa to the exclusion of seagrass (i.e. space preemption, sensu Dudgeon et al., 1999). Caulerpa reproduces by both stolon elongation and fragmentation (Smith and Walters, 1999), and dispersal by fragmentation may be a factor leading to its widespread distribution (Ceccherelli and Cinelli, 1999) and its ability to rapidly colonize seagrass habitats. Previous studies have shown that C. racemosa can displace the seagrass Posidonia oceanica by invading bare areas more quickly than seagrass (Ceccherelli et al., 2000). Caulerpa taxifolia may cause chlorosis and decreased abundance and longevity of P. oceanica (De Villele and Verlaque, 1995). Invasion of seagrass beds by C. taxifolia has also been followed by deterioration of seagrass rhizomes and roots with a corresponding increase of hypoxia in sediments (De Villele and Verlaque, 1995). Therefore, Caulerpa species have been demonstrated to rapidly colonize open space within seagrass beds, as well as to be able to some degree to create new open space by modifying the environment, making it less suitable for seagrasses. In the Fall of 2002, the alga Caulerpa prolifera was noted in Lassing Park, an embayment on the western shoreline of Tampa Bay, FL, U.S.A. This algal species is native to the Caribbean and the Gulf of Mexico, but within Tampa Bay is typically found in low densities and usually as a minor understory component of the canopy of the seagrasses Syringodium filiforme and Thalassia testudinum (Bell, personal observation). Large monospecific beds of Caulerpa are highly unusual in Tampa Bay (although see Avery, 1997). Existing data indicated that the alga was previously absent from the Lassing Park embayment from 1987 to 2000 (Bell et al., 1993; Bell unpublished data) with two seagrasses, Halodule wrightii and Thalassia testudinum, dominating the subtidal landscape before the appearance of C. prolifera in 2002. While the sudden abundance of C. prolifera (hereafter Caulerpa) does not strictly qualify as an invasive event (due to the alga being native to the region), the rapid expansion and space occupation of Caulerpa in Lassing Park is highly unusual and very closely resembles the large scale spatial pattern shifts seen with invasions by other members of the genus (e.g., C. taxifolia). Therefore, investigations on the interactions between seagrass and Caulerpa at Lassing Park should not only provide insight into the mechanisms underlying changing patterns of space occupation by
these macrophytes, but this insight may also be applicable to invasive Caulerpa species as well. Within the Lassing Park subtidal landscape seasonal storm events frequently create blowout gaps (sensu Patriquin, 1975), and the frequency of these blowouts appears to be evidence of a considerable natural disturbance cycle at this site. Gaps provide newly available space in medium-fine sand (median grain size = 0.250 mm, b 1% organic content; Bell et al., 1993) for colonization by macrophytes, and the response of potentially competing cover types to such disturbances is of great interest. In this study we tested the response of seagrass (Halodule wrightii) and Caulerpa to simulated disturbances in order to assess whether either macrophyte had an advantage in disturbance recovery. Halodule wrightii (shoal grass; hereafter Halodule) is a fast-growing pioneer species (Williams, 1990) with rhizome elongation rates at a nearby site of up to 1 m/year (Jensen and Bell, 2001), and was chosen for this experiment because its growth rate makes it the most likely of the seagrasses in Lassing Park to be able to compete with Caulerpa for available space. Additionally, N90% of the small natural gaps of the type simulated here occur within Caulerpa, Halodule, or a mixture of Caulerpa/Halodule at this site (Stafford, unpublished data). In addition to space competition between macrophytes, we also examined the mechanism of Caulerpa expansion/recovery into the simulated disturbances. The contributions of both lateral expansion and fragmentation to space acquisition were compared by analyzing the spatial pattern of recovery into the disturbance gaps. An understanding of the mechanism of regeneration into unvegetated gaps is often informative (e.g., Barrat-Segretain and Amoros, 1996), especially in the case of rapidly expanding macroalgal blooms that dramatically modify the landscape. 2. Methods The study was conducted at Lassing Park (27.25N, 82.63W) in Tampa Bay, FL, a relatively shallow embayment with a mean depth b 1 m. The annual water temperature range for the Tampa Bay region is approximately 13–32 8C (PORTS buoy at the mouth of Tampa Bay), but due to the shallow nature of this site the temperature range of this landscape is likely far more extreme than this nearby open-water data suggests. Additional information on this site, the location of a large seagrass restoration project in the mid-1980s, is available in Bell et al. (1993).
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
To examine patterns of space occupation and acquisition by Caulerpa and Halodule over time, simulated disturbances were utilized to create bare space mimicking natural gaps (blowouts) caused by physical disturbances. In a preliminary survey of local natural disturbances, small blowout gaps had a mean gap diameter at the widest point of 47.7 cm (range = 32– 70 cm; N = 10). Therefore, disturbance was simulated by excavating 0.5 0.5 m areas, creating 20 gaps within the vegetation, and recovery into the newly created gaps was monitored over 15 months. The gaps were created in an area where Halodule patches are interspersed with Caulerpa; prior to the disturbance, the 20 gaps were occupied by approximately 25% Halodule, N 75% Caulerpa (monospecifically and as understory to Halodule), and 0% sand. Disturbance gaps were excavated by placing a rebar frame with an internal area of 50 50 cm onto the bottom. A flat spade was used to sever above- and below-ground vegetation around the interior perimeter of the frame, and then the cut-out square of vegetation was removed by hand. All above and below ground biomass was removed, while as much of the sediment was returned to the gap as possible. All gaps were marked in the approximate center with 1/2W PVC, with the markers protruding about 2W above the sediment. Six gaps were created on November 6, 2002, with the remaining 14 created on November 7, 2002. Reoccupation of space by vegetation after the simulated disturbances was monitored over a 15 month period (November 2002–January 2004) by taking photographs of the gaps using an Olympus C-4000 digital camera on 8 sampling dates. Sampling was conducted when water clarity, water depth, weather, and other logistical considerations allowed. One gap was lost before the first post-disturbance sampling date, and high turbidity and other factors often concealed the remaining gaps or made it impossible to obtain sufficiently clear photographs. As a result, sample size ranged from 15 to 19 across dates, with different gaps missing at different times and identification of specific gaps difficult in many cases. Therefore, while temporal non-independence may be an issue, repeated measures analysis was all but impossible. Images were downloaded to a computer and enhanced for brightness, contrast and color in Microsoft PhotoEditor when necessary. Data were collected by digitally overlaying a 5 5 cell grid onto each photograph and quantifying cover by recording presence/absence in each grid cell. Cover types recorded were Caulerpa, Halodule, and bare sand. No other cover types were present in any sample
51
at any time, except for occasional drift macroalgae, which was removed in the field prior to taking the photographs and was not considered in the analysis. Bare sand cover was recorded to provide data on vegetation density, but sand data were not included in the analysis. The sensitivity required to capture the spatial pattern of the reoccupation of space by Caulerpa and Halodule was unknown, and so three different data sets were collected using three different cover bthresholdsQ (i.e. minimum amounts of cover required in a grid cell in order to qualify as present in that cell). For the first threshold, basic presence/absence (CP = Caulerpa presence; HP = Halodule presence) qualified a grid cell as containing cover if a cover type was present. Ten percent cover (C10, H10) qualified a grid cell as occupied for the second threshold dataset, while 50% cover was required for the third dataset (C50, H50). The bPQ and b10Q thresholds were more sensitive to low levels of cover, and thus were more likely to register the early stages of recovery. On the other hand, the b50Q dataset was most likely to indicate if and when real recovery had occurred and the disturbance gaps were approaching pre-disturbance conditions. Grid cover data were converted to percent cover for each cover type for analysis (# occupied cells 4%). In addition to quantifying total recovery from disturbance, the spatial pattern (and by extension the mechanism) of recovery was also of interest. The 5 5 grid array was divided into 16 perimeter and 9 core cells. Occurrence of vegetation in these two areas was compared to determine whether lateral growth (spread from edge) or fragmentation (haphazard landing and attachment of drifting fragments) were more important in space reoccupation. For overall space occupation of disturbance gaps, the null hypothesis (H01) was a return to pre-disturbance conditions (25% Halodule, N75% Caulerpa), indicating that neither Caulerpa nor Halodule were competitively superior in terms of space occupation following disturbance. Alternatively (HA1), Halodule recovery to less than 25% cover and dominance by Caulerpa would indicate that Caulerpa was better suited to acquiring newly available space via space preemption. Recovery of Halodule to greater than pre-disturbance levels was not expected, since the rapid expansion of Caulerpa into Lassing Park indicated a high growth rate for the alga. Total cover data (means of all gaps per sampling date) were not normally distributed, and were analyzed in SigmaStat 2.03 using Kruskal–Wallis ANOVA on Ranks with Dunn’s Method (equal variances not as-
52
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
Table 1 Summary of Q values from multiple comparisons (Dunn’s Method; SigmaStat 2.03 Kruskal–Wallis ANOVA on Ranks) testing whether cover values (see Fig. 2) were significantly different ( p b 0.05) from Date 0 cover on each later date Date
Presence/absence
10% threshold
50% threshold
CP
HP
C10
H10
C50
H50
11-22-02 12-04-02 12-19-02 04-13-03 06-11-03 07-09-03
5.529 5.001 5.096 1.226 0.925 0.000
5.143 4.079 4.528 2.842 5.632 4.835
6.370 5.720 5.781 2.244 1.346 0.141
4.937 5.287 5.585 3.919 5.471 5.357
6.595 5.986 6.020 2.738 1.289 0.133
5.126 5.447 5.447 5.036 4.939 5.116
A bold value indicates recovery to pre-disturbance conditions (i.e. no significant difference from pre-disturbance conditions). Abbreviations as in text. Sand cover data (not shown) indicate that vegetation density did not resemble prior conditions until the 6th and 5th dates for CP and C10 respectively.
sumed) used for multiple comparisons. To test H01, means of cover values on each date were compared to a data set (Date 0) approximating pre-disturbance conditions (cover of 100% for Caulerpa and 25% for Halodule in all 19 gaps). Possible starting values for Caulerpa cover ranged from 75% to 100% due to its presence in the understory of Halodule; 100% cover was selected as a conservative value, since this set the most stringent standard for Caulerpa to meet to qualify as recovered. Repeated measures analysis of individual
gaps was not attempted because the sample size of specific individual gaps present and identifiable across all dates was small as discussed previously. However, since each date was compared to Date 0 and not to the previous date, and since cover following the return to pre-disturbance conditions is not discussed here, temporal non-independence of data should not have a large effect on the results. For spatial pattern of recovery of Caulerpa, the null hypothesis (H02) was perimeter cover = core cover, indicating no spatially coherent pattern to recovery (random settlement by fragments drives space reoccupation). Alternatively (HA2), recovering vegetation predominantly located in perimeter cells (i.e. perimeter N core) would indicate that recovery occurred mostly around the gap edges (lateral growth drives space reoccupation). Mode of space occupation (core vs. edge) was analyzed in SigmaStat2.03 using one-way ANOVA (Tukey’s Test) where possible, and Kruskal– Wallis ANOVA on Ranks (Dunn’s Method) where data were not normally distributed. Each of the three different datasets (P, 10, 50) were analyzed separately for the effect of spatial location by date. Only the first 6 sampling dates were statistically analyzed for mode of space occupation because vegetation had recovered completely and filled the gaps by the 6th date. Data for the spatial analysis were randomized and subsampled from the full dataset. In order for the com-
Fig. 1. Mean percent cover vs. days elapsed since disturbance for Caulerpa, Halodule and sand. Time is shown in days so as not to obscure the irregularity of sampling dates. At the origin of the x-axis (not shown) all plots had 0% cover of vegetation (100% sand). The main plot shows the first 6 sampling dates, over which the space competition analysis was done. The small plot window at the upper right shows data from the entire study period (439 days); the vertical line indicates the bounds of the main window. Natural seasonal disturbances returned in the Fall and Winter of 2003, resulting in the cover changes recorded after gap recovery was complete. Abbreviations as in text.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
53
Fig. 2. Mean percent cover (F SE) by date for Caulerpa and Halodule at 3 cover thresholds. Note that the y-axis for Halodule is different than for Caulerpa, and that H50 is different than HP and H10. After the 4th sampling date, Halodule declines and virtually disappears, regardless of resolution.
parison of edge to core to be completely spatially independent, half of the images for each date were randomly assigned to edge and half to core, so that edge and core data were never collected from the same gap. Additionally, 9 of the 16 edge cells were randomly selected on each date in order to have an equal-area comparison to the 9 core cells. Since images within each date were randomly assigned to edge and core, and since for edge only 9 of 16 grid cells per date were used, the probability of resampling the same cells on successive dates, and therefore the impact of the temporal non-independence, should be considerably reduced.
3. Results Space created by the simulated disturbances was completely occupied by dense, monospecific Caulerpa by the sixth sampling date (8 months), regardless of sampling resolution (Table 1; Figs. 1 and 2). Caulerpa made the only significant recovery from the simulated disturbances. Halodule did not recover to its prior condition (25% of the substrate), only registering notable cover (12.71%) on one date (April 2003) at the basic presence/absence threshold (HP). In fact, Halodule actually declined from low percentages on the first
54
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
Table 2 Core vs. edge comparisons for Caulerpa by date for each cover threshold (data from Fig. 3) Date
11-22-02 12-04-02 12-19-02 04-13-03 06-11-03 07-09-03
Significance CP
C10
C50
0.114 b0.001 b0.001 0.931 0.959 1.000
0.005 b0.001 0.002 0.645 0.189 1.000
0.562 0.118 0.007 0.048 0.574 1.000
tally removed from 400 cm2 plots in the Mediterranean, which under optimum conditions recovered to 80% cover in 3 months (Piazzi et al., 2003); the 2500 cm2 Caulerpa gaps in this study recovered to 80% in approximately 5–6 1/2 months, depending on sampling resolution. In addition, since the test condition of 100% cover of Caulerpa was conservative and overestimated true initial Caulerpa cover, Caulerpa recovered to greater area cover than before the disturbances. These results suggest that natural disturbances that remove
Data were analyzed in SigmaStat2.03 using one-way ANOVA when possible, and Kruskal–Wallis ANOVA on Ranks (denoted by italics) when not. Significant differences ( p V 0.05) between edge and core are in bold.
few sampling dates to only 0.5% cover at the basic presence/absence threshold (HP) by the final sampling date, and to 0% cover at the 10% (H10) and 50% (H50) thresholds. Later dates not used in the analysis suggest the return of the natural disturbance cycle (decrease in Caulerpa and increase of bare sand during winter 2003–2004; see Figs. 1 and 2) and the variability in cover among gaps within the same date increased concordantly (not shown). Results of the spatial analysis examining the mechanism of gap recovery by Caulerpa indicate that recolonization of disturbance gaps occurred mainly from gap edges (Table 2; Fig. 3). As the recovery progressed, all 3 datasets showed significantly greater cover in perimeter cells than in core cells, indicating that although there was some initial recruitment of fragments, space occupation occurred predominantly via lateral growth. By the 4th date (5 months) for CP and C10 and the 5th date (7 months) for C50, edge and core were no longer significantly different, indicating that growth from edge cells had spread into core cells, blurring the distinction between the two categories and likely overwhelming any surviving fragment-derived clumps. Thus, Caulerpa recovered rapidly from the disturbances, and it did so via lateral stolon elongation; Halodule did not recover, and was virtually non-existent 15 months post-disturbance. 4. Discussion The results of this study clearly indicate that Caulerpa prolifera outcompeted Halodule wrightii for newly available space via space preemption in simulated gaps. Within 7 1/2 months of the simulated disturbances, Caulerpa had completely reoccupied the disturbed space. This recovery time is even faster than that found for invasive C. racemosa experimen-
Fig. 3. Mean percent cover (F SE) of Caulerpa in core vs. edge cells at 3 cover thresholds increased. Comparisons were made in SigmaStat 2.03 using one-way ANOVA and Kruskal–Wallis ANOVA on Ranks where appropriate; significant differences between core and edge on each date are indicated by asterisks.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
above and below ground components of subtidal vegetation (i.e. blowouts) could potentially allow Caulerpa prolifera to replace seagrasses in Lassing Park via preemption of space (e.g., Dudgeon et al., 1999), albeit over a time period related to the physical disturbance cycle in this landscape. In addition to suggesting that Caulerpa has the capability to replace seagrasses over time via space preemption, our results also clearly demonstrate that the mechanism by which Caulerpa preempts space so rapidly appears to be predominantly lateral growth and expansion. While some colonization of interior cells did occur initially, the non-significant trend in cover of core cells was actually a decline in 2 of the 3 datasets (CP, C50) between the 1st and the 3rd sampling dates (Fig. 3), when an increase was expected due to growth and expansion of established clumps. The lack of significant differences in the C50 dataset on the first 2 dates is likely due the low number of grid cells in either edge or core having shown recovery sufficient to register at the 50% minimum threshold. The lack of a significant difference in the CP dataset on the first date, on the other hand, is likely a result of the loss of data associated with the method of analysis (sampling only 1/2 the images each for edge and core). Our initial analysis, including all images for both edge and core, was highly significant ( p = 0.005) for CP on the first sampling date, and since a possible lack of independence between edge and core cells taken from the same image is least likely to be an issue in the early stages of recovery when Caulerpa density is at its lowest, we consider this significant result from the initial analysis to be applicable. Overall, these results suggest that the long-term contribution of vegetative fragments to gap colonization may be limited. While not dominant in driving space occupation, fragmentary clumps could nevertheless still play a role in disturbance recovery and general algal survival, however. Small isolated clumps of vegetation could conceivably facilitate lateral stolon extension by modifying slightly the physical conditions in gaps. Fragment attachment success may also vary seasonally. When present, drift algae found in gaps prior to manual removal were usually observed to be heavily embedded with Caulerpa fragments. Decline in the seasonal drift algae occurred contemporaneously with the cover decline in core cells (fragment-generated clumps), suggesting that the presence of drift algae may influence the survival of introduced Caulerpa fragments. Regardless, fragmentation remains important for Caulerpa propagation because the algae must cross large distances to be introduced into new systems, and fragmen-
55
tation is the most likely way for this to occur (Ceccherelli and Cinelli, 1999). Sexual reproduction is not considered a likely mechanism for vegetation recovery into disturbance gaps in Lassing Park. Flowering of seagrasses was not seen in Lassing Park during the course of the experiment (or in the 15 years of data for this site; Bell, unpublished), nor is it considered to be common for Tampa Bay seagrasses in general (e.g., Phillips, 1960). Similarly, no evidence of sexual reproduction by Caulerpa was noted. At other sites with extensive sexual reproduction of seagrasses and with a significant seed bed, seagrasses might fare better in the face of space preemption by Caulerpa than did Halodule in this study. Little is known regarding sexual reproduction in Caulerpa spp., but fragmentation is often suggested as the predominant explanation for the rapid spread of species in this genus (e.g., Ceccherelli and Piazzi, 2001). However, even considering the lack of a known seed bed at this site, the apparent total exclusion of the seagrass by Caulerpa in the simulated disturbances after 15 months was surprising. While Halodule remained present in significant densities just outside the boundaries of many gaps, all expansion of Halodule into gaps was ultimately unsuccessful. One might note that the simulated disturbances were established during the winter season, when Halodule might be expected to show reduced growth. However, lower tides and stronger winds in winter create more frequent natural physical disturbances of the kind simulated here (although blowouts resulting from thunderstorms do occur occasionally in the summer months), so the timing was not inappropriate. Additionally, Halodule did not recover within the entire 15 month study period, which included a full growth season. Whether Halodule recovery may or may not be more successful following the far less common summer disturbances is unknown at this time. Alternative explanations for the inhibition of Halodule from the simulated disturbance gaps implicate Caulerpa directly or indirectly. Caulerpa prolifera is known to have secondary chemical compounds that can reduce herbivory and reduce epiphyte attachment (Paul and Fenical, 1987). The negative effects of such secondary compounds in Caulerpa taxifolia on seagrasses have been shown (e.g., De Villele and Verlaque, 1995). Whether these compounds are present in the belowground tissue of Caulerpa in Lassing Park such that contact inhibition could be occuring when Halodule rhizomes encounter Caulerpa rhizoids, or whether leaching of secondary chemical compounds into the sediments (or water column) might have similar inhibitory effects, is unknown.
56
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
The density of the Caulerpa canopy may also make it difficult for flexible Halodule blades to push through and acquire light, even if they are able to extend laterally belowground into an area of Caulerpa cover. Overgrowth shading is often cited as causative in alterations of seagrass beds when Caulerpa spp. move into a new system (e.g., De Villele and Verlaque, 1995). Gaps were not redisturbed to detect unseen, belowground recovery of Halodule, and so the possible existence, extent and vigor of seagrass rhizome recovery is unknown, although unlikely to be significant since no aboveground manifestation of living below-ground tissue was evident by the end of the experiment. In any event, regardless of the nature and mechanism of its potential exclusion of Halodule, Caulerpa rapidly and exclusively reoccupied the simulated disturbances created at Lassing Park. While these results are clear, will this pattern hold over the long term? Caulerpa may be more susceptible to natural seasonal disturbances than local seagrasses, perhaps because of the lack of a below ground rhizome mat that would provide stability. During the last sampling in January 2004, Caulerpa cover was greatly reduced and was found almost exclusively beneath the canopy of seagrasses, although later field observations showed that Caulerpa recovered within a few months (Stafford, personal observation). Therefore, Caulerpa may utilize seagrass as a refuge, allowing it to persist during the most severe disturbances, which might suggest a minimum threshold of seagrass cover, below which a Caulerpa/seagrass landscape could become unstable. The susceptibility of monospecific Caulerpa prolifera to buprootingQ by storms in comparison to seagrass or to Caulerpa protected by seagrass canopy and rhizomes remains to be determined (see Piazzi et al., 2003). While the long-term stability of landscapes where seagrasses are replaced by Caulerpa is unknown, it is certain that disturbances such as blowouts will, over time, affect every part of the landscape (return interval; e.g., Pickett and White, 1985). Field observations indicate that for parts of Lassing Park, the return interval may be quite short; in the time interval between the last 2 sampling dates, the entire North end of Lassing Park, where the Caulerpa was principally located at the time of this experiment, was dramatically impacted by one or more severe disturbances, resulting in significant removal of vegetation and dramatic alteration of bottom topography. If such a large portion of the landscape can be disturbed over a short time scale at this site, then the potential for Caulerpa to take over large amounts of Lassing Park via space preemption is clear. Additional documentation of the shift in cover patterns in Lassing
Park will provide an important record on the persistence and extent of such macrophyte blooms in seagrass beds. Should the bloom of Caulerpa at this site persist and expand into more seagrass habitat, dramatic and worrisome modification of the shallow subtidal ecosystem may result. Acknowledgements The authors would like to thank the editor and anonymous reviewers, who provided important suggestions on improving this report, Dr. William Ellis (USF), Dr. Bruce Cowell (USF), and Susan Service, who provided insights on the statistical analysis of the gap data, and Justin Bowles (USF), who helped in the excavation of the gaps. N. Stafford was supported by a USF Foundation Fellowship. S. Bell was supported in part by an NSF grant from the Biological Oceanography Program. [AU] References Avery, W., 1997. Distribution and abundance of macroalgae and seagrass in Hillsborough Bay, Florida, from 1986 to 1995. In: Treat, S.F.Proceedings: Tampa Bay Area Scientific Information Symposium, vol. 3. Tampa Bay Regional Planning Council, pp. 151 – 166. Barrat-Segretain, M.H., Amoros, C., 1996. Recolonization of cleared riverine macrophyte patches: importance of the border effect. J. Veg. Sci. 7, 769 – 776. Bell, S.S., Clements, L.A., Kurdziel, J.P., 1993. Production in natural and restored seagrass beds: a case study of a macrobenthic polychaete. Ecol. Appl. 3, 610 – 621. Ceccherelli, G., Cinelli, F., 1999. The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean. Mar. Ecol. Prog. Ser. 182, 299 – 303. Ceccherelli, G., Piazzi, L., 2001. Dispersal of Caulerpa racemosa fragments in the Mediterranean: lack of detachment time effect on establishment. Bot. Mar. 44, 209 – 213. Ceccherelli, G., Piazzi, L., Cinelli, F., 2000. Response of the nonindigenous Caulerpa racemosa (Forsskal) J. Agardh to the native seagrass Posidonia oceanica (L.) Delile: effect of density of shoots and orientation of edges of meadows. J. Exp. Mar. Biol. Ecol. 243, 227 – 240. De Villele, X., Verlaque, M., 1995. Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Bot. Mar. 38, 79 – 87. Dudgeon, S.R., Steneck, R.S., Davison, I.R., Vadas, R.L., 1999. Coexistence of similar species in a space-limited intertidal zone. Ecol. Mon. 69, 331 – 352. Jensen, S.L., Bell, S.S., 2001. Seagrass growth and patch dynamics: cross-scale morphological plasticity. Plant Ecol. 155, 201 – 217. Jousson, O., Pawlowski, J., Zaninetti, L., Zechman, F.W., Dini, F., Di Guiseppe, G., Woodfield, R., Millar, A., Meinesz, A., 2000. Invasive alga reaches California. Nature 408, 157 – 158.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57 Meinesz, A., 1997. L’implacable avancee´ de la taxifolia. La Recherche 297, 46 – 48. Meinesz, A., Belsher, T., Thibaut, T., Antolic, B., Mustapha, K.B., Boudouresque, C., Chiaverini, D., Cinelli, F., Cottalorda, J., Djellouli, A., El Abed, A., Orestano, C., Grau, A.M., Ivesa, L., Jaklin, A., Langar, H., Massuti-Pascual, E., Peirano, A., Tunesi, L., de Vaugelas, J., Zavodnik, L., Zuljevic, A., 2001. The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol. Invas. 3, 201 – 210. Millar, A.J.K., 2004. New records of marine benthic algae from New South Wales, eastern Australia. Phycol. Res. 52, 117 – 128. Patriquin, D.G., 1975. bMigrationQ of blowouts in seagrass beds at Barbados and Carriacou, West Indies, and its ecological and geological implications. Aquat. Bot. 1, 163 – 189. Paul, V.J., Fenical, W., 1987. Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. In: Scheur, P.J.Bioorganic Marine Chemistry, vol. 1. SpringerVerlag, Berlin, pp. 1 – 29. Phillips, R.C., 1960. Observations on the ecology and distribution of the Florida seagrasses. Prof. Pap. 2, Fl. Bd. Conserv. Mar. Lab St. Petersburg , pp. 1 – 72.
57
Piazzi, L., Ceccherelli, G., Cinelli, F., 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Prog. Ser. 210, 149 – 159. Piazzi, L., Ceccherelli, G., Balata, D., Cinelli, C., 2003. Early patterns of Caulerpa racemosa recovery in the Mediterranean Sea: the influence of algal turfs. J. Mar. Biol. Assoc. U.K. 83, 27 – 29. Pickett, S.T.A., White, P.S. (Eds.), 1985. The Ecology of Natural Disturbance and Patch Dynamics. Academic Press. Inc., Orlando, pp. 1 – 472. Schaffelke, B., Murphy, N., Uthicke, S., 2002. Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. Mar. Pollut. Bull. 44, 204 – 210. Smith, C.M., Walters, L.J., 1999. Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. P.S.Z.N.. Mar. Ecol. 20, 307 – 319. Williams, S.L., 1990. Experimental studies of Caribbean seagrass bed development. Ecol. Mon. 60, 449 – 469.
Space competition between seagrass and Caulerpa prolifera (Forsskaal) Lamouroux following simulated disturbances in Lassing Park, FL Nathaniel B. Stafford *, Susan S. Bell Department of Biology, University of South Florida—SCA 110, 4202 E. Fowler Avenue, Tampa, FL 33620-5200, United States Received 5 January 2005; received in revised form 22 November 2005; accepted 29 November 2005
Abstract An experimental study was conducted in Tampa Bay, FL to examine the response to disturbance of two co-occurring subtidal plants: the alga Caulerpa prolifera and the seagrass Halodule wrightii (Ascherson). Some recent studies have called into question the assumption that fast-growing rhizoidal Caulerpa species have the potential to outcompete and rapidly replace local seagrasses. In the Fall of 2002 an abrupt appearance of Caulerpa prolifera was noted in a shallow embayment in Tampa Bay previously dominated by seagrasses. Natural disturbance events were simulated by excavating 0.5 0.5 m plots in an area with monospecific C. prolifera and mixed C. prolifera and H. wrightii. Above and below-ground biomass were removed, and recovery of above-ground cover into the newly created gaps was monitored over 15 months. In addition to measuring the recovery of both species, the spatial pattern of Caulerpa recovery from the simulated disturbances was also analyzed. Simulated gaps were rapidly (5–8 months, depending on sampling resolution) and exclusively reoccupied by C. prolifera, with the recovery occurring predominantly via lateral expansion from gap edges rather than colonization by fragments. Therefore, while rhizoidal algae may or may not be able to supplant existing seagrasses by overgrowth or other forms of direct competition, disturbance events that remove seagrass and create bare areas may allow C. prolifera to replace seagrasses over time via preemption of space should an algal bloom such as this be persistent. D 2005 Elsevier B.V. All rights reserved. Keywords: Bloom; Caulerpa; Disturbance; Recovery; Seagrass; Space competition
1. Introduction In the past 15 years rhizoidal algae of the genus Caulerpa have gained notoriety as they have invaded many subtidal landscapes. For example, Caulerpa taxifolia (Vahl) C. Agandh has been recently introduced into new areas of the Mediterranean, where it has * Corresponding author. Tel.: +1 813 974 5420; fax: +1 813 974 3263. E-mail address: [email protected] (N.B. Stafford). 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.11.025
established both persistent and spatially expanding populations among seagrass beds (Meinesz, 1997; Meinesz et al., 2001). Likewise, Caulerpa racemosa has been identified as an invasive species in the western Mediterranean (Piazzi et al., 2001). Additionally, C. taxifolia was reported as an invasive in seagrass beds on the west coast of the U.S.A. in 1999 (Jousson et al., 2000), and has appeared in Australia in recent years as well (e.g. Schaffelke et al., 2002; Millar, 2004). Of special concern in the above studies is that the presence of species of Caulerpa could lead to a habitat
50
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
shift. Specifically, Caulerpa might displace seagrass either by direct overgrowth of the seagrass and/or by rapid occupation of open space by Caulerpa to the exclusion of seagrass (i.e. space preemption, sensu Dudgeon et al., 1999). Caulerpa reproduces by both stolon elongation and fragmentation (Smith and Walters, 1999), and dispersal by fragmentation may be a factor leading to its widespread distribution (Ceccherelli and Cinelli, 1999) and its ability to rapidly colonize seagrass habitats. Previous studies have shown that C. racemosa can displace the seagrass Posidonia oceanica by invading bare areas more quickly than seagrass (Ceccherelli et al., 2000). Caulerpa taxifolia may cause chlorosis and decreased abundance and longevity of P. oceanica (De Villele and Verlaque, 1995). Invasion of seagrass beds by C. taxifolia has also been followed by deterioration of seagrass rhizomes and roots with a corresponding increase of hypoxia in sediments (De Villele and Verlaque, 1995). Therefore, Caulerpa species have been demonstrated to rapidly colonize open space within seagrass beds, as well as to be able to some degree to create new open space by modifying the environment, making it less suitable for seagrasses. In the Fall of 2002, the alga Caulerpa prolifera was noted in Lassing Park, an embayment on the western shoreline of Tampa Bay, FL, U.S.A. This algal species is native to the Caribbean and the Gulf of Mexico, but within Tampa Bay is typically found in low densities and usually as a minor understory component of the canopy of the seagrasses Syringodium filiforme and Thalassia testudinum (Bell, personal observation). Large monospecific beds of Caulerpa are highly unusual in Tampa Bay (although see Avery, 1997). Existing data indicated that the alga was previously absent from the Lassing Park embayment from 1987 to 2000 (Bell et al., 1993; Bell unpublished data) with two seagrasses, Halodule wrightii and Thalassia testudinum, dominating the subtidal landscape before the appearance of C. prolifera in 2002. While the sudden abundance of C. prolifera (hereafter Caulerpa) does not strictly qualify as an invasive event (due to the alga being native to the region), the rapid expansion and space occupation of Caulerpa in Lassing Park is highly unusual and very closely resembles the large scale spatial pattern shifts seen with invasions by other members of the genus (e.g., C. taxifolia). Therefore, investigations on the interactions between seagrass and Caulerpa at Lassing Park should not only provide insight into the mechanisms underlying changing patterns of space occupation by
these macrophytes, but this insight may also be applicable to invasive Caulerpa species as well. Within the Lassing Park subtidal landscape seasonal storm events frequently create blowout gaps (sensu Patriquin, 1975), and the frequency of these blowouts appears to be evidence of a considerable natural disturbance cycle at this site. Gaps provide newly available space in medium-fine sand (median grain size = 0.250 mm, b 1% organic content; Bell et al., 1993) for colonization by macrophytes, and the response of potentially competing cover types to such disturbances is of great interest. In this study we tested the response of seagrass (Halodule wrightii) and Caulerpa to simulated disturbances in order to assess whether either macrophyte had an advantage in disturbance recovery. Halodule wrightii (shoal grass; hereafter Halodule) is a fast-growing pioneer species (Williams, 1990) with rhizome elongation rates at a nearby site of up to 1 m/year (Jensen and Bell, 2001), and was chosen for this experiment because its growth rate makes it the most likely of the seagrasses in Lassing Park to be able to compete with Caulerpa for available space. Additionally, N90% of the small natural gaps of the type simulated here occur within Caulerpa, Halodule, or a mixture of Caulerpa/Halodule at this site (Stafford, unpublished data). In addition to space competition between macrophytes, we also examined the mechanism of Caulerpa expansion/recovery into the simulated disturbances. The contributions of both lateral expansion and fragmentation to space acquisition were compared by analyzing the spatial pattern of recovery into the disturbance gaps. An understanding of the mechanism of regeneration into unvegetated gaps is often informative (e.g., Barrat-Segretain and Amoros, 1996), especially in the case of rapidly expanding macroalgal blooms that dramatically modify the landscape. 2. Methods The study was conducted at Lassing Park (27.25N, 82.63W) in Tampa Bay, FL, a relatively shallow embayment with a mean depth b 1 m. The annual water temperature range for the Tampa Bay region is approximately 13–32 8C (PORTS buoy at the mouth of Tampa Bay), but due to the shallow nature of this site the temperature range of this landscape is likely far more extreme than this nearby open-water data suggests. Additional information on this site, the location of a large seagrass restoration project in the mid-1980s, is available in Bell et al. (1993).
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
To examine patterns of space occupation and acquisition by Caulerpa and Halodule over time, simulated disturbances were utilized to create bare space mimicking natural gaps (blowouts) caused by physical disturbances. In a preliminary survey of local natural disturbances, small blowout gaps had a mean gap diameter at the widest point of 47.7 cm (range = 32– 70 cm; N = 10). Therefore, disturbance was simulated by excavating 0.5 0.5 m areas, creating 20 gaps within the vegetation, and recovery into the newly created gaps was monitored over 15 months. The gaps were created in an area where Halodule patches are interspersed with Caulerpa; prior to the disturbance, the 20 gaps were occupied by approximately 25% Halodule, N 75% Caulerpa (monospecifically and as understory to Halodule), and 0% sand. Disturbance gaps were excavated by placing a rebar frame with an internal area of 50 50 cm onto the bottom. A flat spade was used to sever above- and below-ground vegetation around the interior perimeter of the frame, and then the cut-out square of vegetation was removed by hand. All above and below ground biomass was removed, while as much of the sediment was returned to the gap as possible. All gaps were marked in the approximate center with 1/2W PVC, with the markers protruding about 2W above the sediment. Six gaps were created on November 6, 2002, with the remaining 14 created on November 7, 2002. Reoccupation of space by vegetation after the simulated disturbances was monitored over a 15 month period (November 2002–January 2004) by taking photographs of the gaps using an Olympus C-4000 digital camera on 8 sampling dates. Sampling was conducted when water clarity, water depth, weather, and other logistical considerations allowed. One gap was lost before the first post-disturbance sampling date, and high turbidity and other factors often concealed the remaining gaps or made it impossible to obtain sufficiently clear photographs. As a result, sample size ranged from 15 to 19 across dates, with different gaps missing at different times and identification of specific gaps difficult in many cases. Therefore, while temporal non-independence may be an issue, repeated measures analysis was all but impossible. Images were downloaded to a computer and enhanced for brightness, contrast and color in Microsoft PhotoEditor when necessary. Data were collected by digitally overlaying a 5 5 cell grid onto each photograph and quantifying cover by recording presence/absence in each grid cell. Cover types recorded were Caulerpa, Halodule, and bare sand. No other cover types were present in any sample
51
at any time, except for occasional drift macroalgae, which was removed in the field prior to taking the photographs and was not considered in the analysis. Bare sand cover was recorded to provide data on vegetation density, but sand data were not included in the analysis. The sensitivity required to capture the spatial pattern of the reoccupation of space by Caulerpa and Halodule was unknown, and so three different data sets were collected using three different cover bthresholdsQ (i.e. minimum amounts of cover required in a grid cell in order to qualify as present in that cell). For the first threshold, basic presence/absence (CP = Caulerpa presence; HP = Halodule presence) qualified a grid cell as containing cover if a cover type was present. Ten percent cover (C10, H10) qualified a grid cell as occupied for the second threshold dataset, while 50% cover was required for the third dataset (C50, H50). The bPQ and b10Q thresholds were more sensitive to low levels of cover, and thus were more likely to register the early stages of recovery. On the other hand, the b50Q dataset was most likely to indicate if and when real recovery had occurred and the disturbance gaps were approaching pre-disturbance conditions. Grid cover data were converted to percent cover for each cover type for analysis (# occupied cells 4%). In addition to quantifying total recovery from disturbance, the spatial pattern (and by extension the mechanism) of recovery was also of interest. The 5 5 grid array was divided into 16 perimeter and 9 core cells. Occurrence of vegetation in these two areas was compared to determine whether lateral growth (spread from edge) or fragmentation (haphazard landing and attachment of drifting fragments) were more important in space reoccupation. For overall space occupation of disturbance gaps, the null hypothesis (H01) was a return to pre-disturbance conditions (25% Halodule, N75% Caulerpa), indicating that neither Caulerpa nor Halodule were competitively superior in terms of space occupation following disturbance. Alternatively (HA1), Halodule recovery to less than 25% cover and dominance by Caulerpa would indicate that Caulerpa was better suited to acquiring newly available space via space preemption. Recovery of Halodule to greater than pre-disturbance levels was not expected, since the rapid expansion of Caulerpa into Lassing Park indicated a high growth rate for the alga. Total cover data (means of all gaps per sampling date) were not normally distributed, and were analyzed in SigmaStat 2.03 using Kruskal–Wallis ANOVA on Ranks with Dunn’s Method (equal variances not as-
52
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
Table 1 Summary of Q values from multiple comparisons (Dunn’s Method; SigmaStat 2.03 Kruskal–Wallis ANOVA on Ranks) testing whether cover values (see Fig. 2) were significantly different ( p b 0.05) from Date 0 cover on each later date Date
Presence/absence
10% threshold
50% threshold
CP
HP
C10
H10
C50
H50
11-22-02 12-04-02 12-19-02 04-13-03 06-11-03 07-09-03
5.529 5.001 5.096 1.226 0.925 0.000
5.143 4.079 4.528 2.842 5.632 4.835
6.370 5.720 5.781 2.244 1.346 0.141
4.937 5.287 5.585 3.919 5.471 5.357
6.595 5.986 6.020 2.738 1.289 0.133
5.126 5.447 5.447 5.036 4.939 5.116
A bold value indicates recovery to pre-disturbance conditions (i.e. no significant difference from pre-disturbance conditions). Abbreviations as in text. Sand cover data (not shown) indicate that vegetation density did not resemble prior conditions until the 6th and 5th dates for CP and C10 respectively.
sumed) used for multiple comparisons. To test H01, means of cover values on each date were compared to a data set (Date 0) approximating pre-disturbance conditions (cover of 100% for Caulerpa and 25% for Halodule in all 19 gaps). Possible starting values for Caulerpa cover ranged from 75% to 100% due to its presence in the understory of Halodule; 100% cover was selected as a conservative value, since this set the most stringent standard for Caulerpa to meet to qualify as recovered. Repeated measures analysis of individual
gaps was not attempted because the sample size of specific individual gaps present and identifiable across all dates was small as discussed previously. However, since each date was compared to Date 0 and not to the previous date, and since cover following the return to pre-disturbance conditions is not discussed here, temporal non-independence of data should not have a large effect on the results. For spatial pattern of recovery of Caulerpa, the null hypothesis (H02) was perimeter cover = core cover, indicating no spatially coherent pattern to recovery (random settlement by fragments drives space reoccupation). Alternatively (HA2), recovering vegetation predominantly located in perimeter cells (i.e. perimeter N core) would indicate that recovery occurred mostly around the gap edges (lateral growth drives space reoccupation). Mode of space occupation (core vs. edge) was analyzed in SigmaStat2.03 using one-way ANOVA (Tukey’s Test) where possible, and Kruskal– Wallis ANOVA on Ranks (Dunn’s Method) where data were not normally distributed. Each of the three different datasets (P, 10, 50) were analyzed separately for the effect of spatial location by date. Only the first 6 sampling dates were statistically analyzed for mode of space occupation because vegetation had recovered completely and filled the gaps by the 6th date. Data for the spatial analysis were randomized and subsampled from the full dataset. In order for the com-
Fig. 1. Mean percent cover vs. days elapsed since disturbance for Caulerpa, Halodule and sand. Time is shown in days so as not to obscure the irregularity of sampling dates. At the origin of the x-axis (not shown) all plots had 0% cover of vegetation (100% sand). The main plot shows the first 6 sampling dates, over which the space competition analysis was done. The small plot window at the upper right shows data from the entire study period (439 days); the vertical line indicates the bounds of the main window. Natural seasonal disturbances returned in the Fall and Winter of 2003, resulting in the cover changes recorded after gap recovery was complete. Abbreviations as in text.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
53
Fig. 2. Mean percent cover (F SE) by date for Caulerpa and Halodule at 3 cover thresholds. Note that the y-axis for Halodule is different than for Caulerpa, and that H50 is different than HP and H10. After the 4th sampling date, Halodule declines and virtually disappears, regardless of resolution.
parison of edge to core to be completely spatially independent, half of the images for each date were randomly assigned to edge and half to core, so that edge and core data were never collected from the same gap. Additionally, 9 of the 16 edge cells were randomly selected on each date in order to have an equal-area comparison to the 9 core cells. Since images within each date were randomly assigned to edge and core, and since for edge only 9 of 16 grid cells per date were used, the probability of resampling the same cells on successive dates, and therefore the impact of the temporal non-independence, should be considerably reduced.
3. Results Space created by the simulated disturbances was completely occupied by dense, monospecific Caulerpa by the sixth sampling date (8 months), regardless of sampling resolution (Table 1; Figs. 1 and 2). Caulerpa made the only significant recovery from the simulated disturbances. Halodule did not recover to its prior condition (25% of the substrate), only registering notable cover (12.71%) on one date (April 2003) at the basic presence/absence threshold (HP). In fact, Halodule actually declined from low percentages on the first
54
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
Table 2 Core vs. edge comparisons for Caulerpa by date for each cover threshold (data from Fig. 3) Date
11-22-02 12-04-02 12-19-02 04-13-03 06-11-03 07-09-03
Significance CP
C10
C50
0.114 b0.001 b0.001 0.931 0.959 1.000
0.005 b0.001 0.002 0.645 0.189 1.000
0.562 0.118 0.007 0.048 0.574 1.000
tally removed from 400 cm2 plots in the Mediterranean, which under optimum conditions recovered to 80% cover in 3 months (Piazzi et al., 2003); the 2500 cm2 Caulerpa gaps in this study recovered to 80% in approximately 5–6 1/2 months, depending on sampling resolution. In addition, since the test condition of 100% cover of Caulerpa was conservative and overestimated true initial Caulerpa cover, Caulerpa recovered to greater area cover than before the disturbances. These results suggest that natural disturbances that remove
Data were analyzed in SigmaStat2.03 using one-way ANOVA when possible, and Kruskal–Wallis ANOVA on Ranks (denoted by italics) when not. Significant differences ( p V 0.05) between edge and core are in bold.
few sampling dates to only 0.5% cover at the basic presence/absence threshold (HP) by the final sampling date, and to 0% cover at the 10% (H10) and 50% (H50) thresholds. Later dates not used in the analysis suggest the return of the natural disturbance cycle (decrease in Caulerpa and increase of bare sand during winter 2003–2004; see Figs. 1 and 2) and the variability in cover among gaps within the same date increased concordantly (not shown). Results of the spatial analysis examining the mechanism of gap recovery by Caulerpa indicate that recolonization of disturbance gaps occurred mainly from gap edges (Table 2; Fig. 3). As the recovery progressed, all 3 datasets showed significantly greater cover in perimeter cells than in core cells, indicating that although there was some initial recruitment of fragments, space occupation occurred predominantly via lateral growth. By the 4th date (5 months) for CP and C10 and the 5th date (7 months) for C50, edge and core were no longer significantly different, indicating that growth from edge cells had spread into core cells, blurring the distinction between the two categories and likely overwhelming any surviving fragment-derived clumps. Thus, Caulerpa recovered rapidly from the disturbances, and it did so via lateral stolon elongation; Halodule did not recover, and was virtually non-existent 15 months post-disturbance. 4. Discussion The results of this study clearly indicate that Caulerpa prolifera outcompeted Halodule wrightii for newly available space via space preemption in simulated gaps. Within 7 1/2 months of the simulated disturbances, Caulerpa had completely reoccupied the disturbed space. This recovery time is even faster than that found for invasive C. racemosa experimen-
Fig. 3. Mean percent cover (F SE) of Caulerpa in core vs. edge cells at 3 cover thresholds increased. Comparisons were made in SigmaStat 2.03 using one-way ANOVA and Kruskal–Wallis ANOVA on Ranks where appropriate; significant differences between core and edge on each date are indicated by asterisks.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
above and below ground components of subtidal vegetation (i.e. blowouts) could potentially allow Caulerpa prolifera to replace seagrasses in Lassing Park via preemption of space (e.g., Dudgeon et al., 1999), albeit over a time period related to the physical disturbance cycle in this landscape. In addition to suggesting that Caulerpa has the capability to replace seagrasses over time via space preemption, our results also clearly demonstrate that the mechanism by which Caulerpa preempts space so rapidly appears to be predominantly lateral growth and expansion. While some colonization of interior cells did occur initially, the non-significant trend in cover of core cells was actually a decline in 2 of the 3 datasets (CP, C50) between the 1st and the 3rd sampling dates (Fig. 3), when an increase was expected due to growth and expansion of established clumps. The lack of significant differences in the C50 dataset on the first 2 dates is likely due the low number of grid cells in either edge or core having shown recovery sufficient to register at the 50% minimum threshold. The lack of a significant difference in the CP dataset on the first date, on the other hand, is likely a result of the loss of data associated with the method of analysis (sampling only 1/2 the images each for edge and core). Our initial analysis, including all images for both edge and core, was highly significant ( p = 0.005) for CP on the first sampling date, and since a possible lack of independence between edge and core cells taken from the same image is least likely to be an issue in the early stages of recovery when Caulerpa density is at its lowest, we consider this significant result from the initial analysis to be applicable. Overall, these results suggest that the long-term contribution of vegetative fragments to gap colonization may be limited. While not dominant in driving space occupation, fragmentary clumps could nevertheless still play a role in disturbance recovery and general algal survival, however. Small isolated clumps of vegetation could conceivably facilitate lateral stolon extension by modifying slightly the physical conditions in gaps. Fragment attachment success may also vary seasonally. When present, drift algae found in gaps prior to manual removal were usually observed to be heavily embedded with Caulerpa fragments. Decline in the seasonal drift algae occurred contemporaneously with the cover decline in core cells (fragment-generated clumps), suggesting that the presence of drift algae may influence the survival of introduced Caulerpa fragments. Regardless, fragmentation remains important for Caulerpa propagation because the algae must cross large distances to be introduced into new systems, and fragmen-
55
tation is the most likely way for this to occur (Ceccherelli and Cinelli, 1999). Sexual reproduction is not considered a likely mechanism for vegetation recovery into disturbance gaps in Lassing Park. Flowering of seagrasses was not seen in Lassing Park during the course of the experiment (or in the 15 years of data for this site; Bell, unpublished), nor is it considered to be common for Tampa Bay seagrasses in general (e.g., Phillips, 1960). Similarly, no evidence of sexual reproduction by Caulerpa was noted. At other sites with extensive sexual reproduction of seagrasses and with a significant seed bed, seagrasses might fare better in the face of space preemption by Caulerpa than did Halodule in this study. Little is known regarding sexual reproduction in Caulerpa spp., but fragmentation is often suggested as the predominant explanation for the rapid spread of species in this genus (e.g., Ceccherelli and Piazzi, 2001). However, even considering the lack of a known seed bed at this site, the apparent total exclusion of the seagrass by Caulerpa in the simulated disturbances after 15 months was surprising. While Halodule remained present in significant densities just outside the boundaries of many gaps, all expansion of Halodule into gaps was ultimately unsuccessful. One might note that the simulated disturbances were established during the winter season, when Halodule might be expected to show reduced growth. However, lower tides and stronger winds in winter create more frequent natural physical disturbances of the kind simulated here (although blowouts resulting from thunderstorms do occur occasionally in the summer months), so the timing was not inappropriate. Additionally, Halodule did not recover within the entire 15 month study period, which included a full growth season. Whether Halodule recovery may or may not be more successful following the far less common summer disturbances is unknown at this time. Alternative explanations for the inhibition of Halodule from the simulated disturbance gaps implicate Caulerpa directly or indirectly. Caulerpa prolifera is known to have secondary chemical compounds that can reduce herbivory and reduce epiphyte attachment (Paul and Fenical, 1987). The negative effects of such secondary compounds in Caulerpa taxifolia on seagrasses have been shown (e.g., De Villele and Verlaque, 1995). Whether these compounds are present in the belowground tissue of Caulerpa in Lassing Park such that contact inhibition could be occuring when Halodule rhizomes encounter Caulerpa rhizoids, or whether leaching of secondary chemical compounds into the sediments (or water column) might have similar inhibitory effects, is unknown.
56
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57
The density of the Caulerpa canopy may also make it difficult for flexible Halodule blades to push through and acquire light, even if they are able to extend laterally belowground into an area of Caulerpa cover. Overgrowth shading is often cited as causative in alterations of seagrass beds when Caulerpa spp. move into a new system (e.g., De Villele and Verlaque, 1995). Gaps were not redisturbed to detect unseen, belowground recovery of Halodule, and so the possible existence, extent and vigor of seagrass rhizome recovery is unknown, although unlikely to be significant since no aboveground manifestation of living below-ground tissue was evident by the end of the experiment. In any event, regardless of the nature and mechanism of its potential exclusion of Halodule, Caulerpa rapidly and exclusively reoccupied the simulated disturbances created at Lassing Park. While these results are clear, will this pattern hold over the long term? Caulerpa may be more susceptible to natural seasonal disturbances than local seagrasses, perhaps because of the lack of a below ground rhizome mat that would provide stability. During the last sampling in January 2004, Caulerpa cover was greatly reduced and was found almost exclusively beneath the canopy of seagrasses, although later field observations showed that Caulerpa recovered within a few months (Stafford, personal observation). Therefore, Caulerpa may utilize seagrass as a refuge, allowing it to persist during the most severe disturbances, which might suggest a minimum threshold of seagrass cover, below which a Caulerpa/seagrass landscape could become unstable. The susceptibility of monospecific Caulerpa prolifera to buprootingQ by storms in comparison to seagrass or to Caulerpa protected by seagrass canopy and rhizomes remains to be determined (see Piazzi et al., 2003). While the long-term stability of landscapes where seagrasses are replaced by Caulerpa is unknown, it is certain that disturbances such as blowouts will, over time, affect every part of the landscape (return interval; e.g., Pickett and White, 1985). Field observations indicate that for parts of Lassing Park, the return interval may be quite short; in the time interval between the last 2 sampling dates, the entire North end of Lassing Park, where the Caulerpa was principally located at the time of this experiment, was dramatically impacted by one or more severe disturbances, resulting in significant removal of vegetation and dramatic alteration of bottom topography. If such a large portion of the landscape can be disturbed over a short time scale at this site, then the potential for Caulerpa to take over large amounts of Lassing Park via space preemption is clear. Additional documentation of the shift in cover patterns in Lassing
Park will provide an important record on the persistence and extent of such macrophyte blooms in seagrass beds. Should the bloom of Caulerpa at this site persist and expand into more seagrass habitat, dramatic and worrisome modification of the shallow subtidal ecosystem may result. Acknowledgements The authors would like to thank the editor and anonymous reviewers, who provided important suggestions on improving this report, Dr. William Ellis (USF), Dr. Bruce Cowell (USF), and Susan Service, who provided insights on the statistical analysis of the gap data, and Justin Bowles (USF), who helped in the excavation of the gaps. N. Stafford was supported by a USF Foundation Fellowship. S. Bell was supported in part by an NSF grant from the Biological Oceanography Program. [AU] References Avery, W., 1997. Distribution and abundance of macroalgae and seagrass in Hillsborough Bay, Florida, from 1986 to 1995. In: Treat, S.F.Proceedings: Tampa Bay Area Scientific Information Symposium, vol. 3. Tampa Bay Regional Planning Council, pp. 151 – 166. Barrat-Segretain, M.H., Amoros, C., 1996. Recolonization of cleared riverine macrophyte patches: importance of the border effect. J. Veg. Sci. 7, 769 – 776. Bell, S.S., Clements, L.A., Kurdziel, J.P., 1993. Production in natural and restored seagrass beds: a case study of a macrobenthic polychaete. Ecol. Appl. 3, 610 – 621. Ceccherelli, G., Cinelli, F., 1999. The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean. Mar. Ecol. Prog. Ser. 182, 299 – 303. Ceccherelli, G., Piazzi, L., 2001. Dispersal of Caulerpa racemosa fragments in the Mediterranean: lack of detachment time effect on establishment. Bot. Mar. 44, 209 – 213. Ceccherelli, G., Piazzi, L., Cinelli, F., 2000. Response of the nonindigenous Caulerpa racemosa (Forsskal) J. Agardh to the native seagrass Posidonia oceanica (L.) Delile: effect of density of shoots and orientation of edges of meadows. J. Exp. Mar. Biol. Ecol. 243, 227 – 240. De Villele, X., Verlaque, M., 1995. Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Bot. Mar. 38, 79 – 87. Dudgeon, S.R., Steneck, R.S., Davison, I.R., Vadas, R.L., 1999. Coexistence of similar species in a space-limited intertidal zone. Ecol. Mon. 69, 331 – 352. Jensen, S.L., Bell, S.S., 2001. Seagrass growth and patch dynamics: cross-scale morphological plasticity. Plant Ecol. 155, 201 – 217. Jousson, O., Pawlowski, J., Zaninetti, L., Zechman, F.W., Dini, F., Di Guiseppe, G., Woodfield, R., Millar, A., Meinesz, A., 2000. Invasive alga reaches California. Nature 408, 157 – 158.
N.B. Stafford, S.S. Bell / Journal of Experimental Marine Biology and Ecology 333 (2006) 49–57 Meinesz, A., 1997. L’implacable avancee´ de la taxifolia. La Recherche 297, 46 – 48. Meinesz, A., Belsher, T., Thibaut, T., Antolic, B., Mustapha, K.B., Boudouresque, C., Chiaverini, D., Cinelli, F., Cottalorda, J., Djellouli, A., El Abed, A., Orestano, C., Grau, A.M., Ivesa, L., Jaklin, A., Langar, H., Massuti-Pascual, E., Peirano, A., Tunesi, L., de Vaugelas, J., Zavodnik, L., Zuljevic, A., 2001. The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol. Invas. 3, 201 – 210. Millar, A.J.K., 2004. New records of marine benthic algae from New South Wales, eastern Australia. Phycol. Res. 52, 117 – 128. Patriquin, D.G., 1975. bMigrationQ of blowouts in seagrass beds at Barbados and Carriacou, West Indies, and its ecological and geological implications. Aquat. Bot. 1, 163 – 189. Paul, V.J., Fenical, W., 1987. Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. In: Scheur, P.J.Bioorganic Marine Chemistry, vol. 1. SpringerVerlag, Berlin, pp. 1 – 29. Phillips, R.C., 1960. Observations on the ecology and distribution of the Florida seagrasses. Prof. Pap. 2, Fl. Bd. Conserv. Mar. Lab St. Petersburg , pp. 1 – 72.
57
Piazzi, L., Ceccherelli, G., Cinelli, F., 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Prog. Ser. 210, 149 – 159. Piazzi, L., Ceccherelli, G., Balata, D., Cinelli, C., 2003. Early patterns of Caulerpa racemosa recovery in the Mediterranean Sea: the influence of algal turfs. J. Mar. Biol. Assoc. U.K. 83, 27 – 29. Pickett, S.T.A., White, P.S. (Eds.), 1985. The Ecology of Natural Disturbance and Patch Dynamics. Academic Press. Inc., Orlando, pp. 1 – 472. Schaffelke, B., Murphy, N., Uthicke, S., 2002. Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. Mar. Pollut. Bull. 44, 204 – 210. Smith, C.M., Walters, L.J., 1999. Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. P.S.Z.N.. Mar. Ecol. 20, 307 – 319. Williams, S.L., 1990. Experimental studies of Caribbean seagrass bed development. Ecol. Mon. 60, 449 – 469.