Coral Reefs (2005) 24: 681–692 DOI 10.1007/s00338-005-0058-5
R EP O RT
Peter J. Mumby Æ Nicola L. Foster Elizabeth A. Glynn Fahy
Patch dynamics of coral reef macroalgae under chronic and acute disturbance
Received: 25 June 2004 / Accepted: 20 September 2005 / Published online: 10 November 2005 Springer-Verlag 2005
Abstract The patch dynamics (colonisation rate, growth rate, and extinction rate) are quantified for two dominant species of macroalgae on a Caribbean forereef in Belize: Lobophora variegata (Lamouroux) and Dictyota pulchella (Ho¨rnig and Schnetter). Measurements were taken on time scales of days, weeks, months, and years during which three hurricanes occurred. All patches were followed on naturally occurring ramets of dead Montastraea annularis. The first hurricane (Mitch) caused massive coral mortality and liberated space for algal colonisation. The cover of Lobophora increased throughout the study and herbivores did not appear to limit its cover within a 4 year time frame. In contrast, the cover of D. pulchella fluctuated greatly and showed no net increase, despite an increase in parrotfish biomass and settlement space. Variation in the overall percent cover of an alga is not indicative of the underlying patch dynamics. The steady rise in the cover of Lobophora took place despite a high turnover of patches (12–60% of patches per year). The patch dynamics of Dictyota were slower (7–20%), but a greater patch density and threefold higher lateral growth rate led to greater fluctuations in total cover. The dynamics of algal patches are size-specific such that larger patches are less likely to become extinct during hurricanes. Keywords Macroalgae Æ Coral Æ Hurricane Æ Patch dynamics Æ Competition Æ Herbivory
Communicated by Biological Editor K. Sullivan Sealey P. J. Mumby (&) Æ N. L. Foster Marine Spatial Ecology Laboratory, School of BioSciences, University of Exeter, Prince of Wales Road, Exeter, EX4 4PS, UK E-mail:
[email protected] Tel.: +44-1392-263798 Fax: +44-1392-263700 E. A. G. Fahy Nova Southeastern University Oceanographic Center, 8000 N Ocean Drive, Dania, FL, 33004, USA
Introduction Fleshy macroalgae play a fundamental, albeit incompletely understood, role in the dynamics and functioning of coral reefs (Steneck and Dethier 1994). First, these reef algae (hereafter referred to simply as macroalgae) pre-empt settlement space that might otherwise be available for settling coral planulae. Second, there is growing evidence that scleractinian corals compete for space with macroalgae (de Ruyter van Steveninck et al. 1988b; Tanner 1995; Jompa and McCook 2002a, 2003). The outcome of such competition includes a decline in the growth rates of both competitors (de Ruyter van Steveninck et al. 1988b; Jompa and McCook 2002a), reductions in the fecundity of corals (Tanner 1995), and even coral mortality (Bak and Engel 1979; Hughes and Tanner 2000; Lirman 2001). A wide variety of disturbance phenomena may result in a change (usually an increase) in the biomass of macroalgae on coral reefs. Such impacts include drastic reductions in urchin density brought about by either disease or removal of predators (Carpenter 1990; Hughes 1994; McClanahan et al. 1996), overfishing of herbivorous fish (Hughes 1994; McClanahan 1997), coral mortality from mass bleaching (Diaz-Pulido and McCook 2002), and rising nutrients (Littler et al. 1993). Unfortunately, reefs dominated by macroalgae tend to support detrital trophic pathways, rather than those associated with high levels of secondary and tertiary production and fisheries (Carpenter 1990). Whilst the cover of macroalgae is a core component of most reef monitoring programmes (Rogers et al. 1994; English et al. 1997), such studies rarely, if ever, investigate the dynamics of algae at the scale of individual patches. Indeed, we have found few accounts of algal patch dynamics in the coral reef literature (exceptions include de Ruyter van Steveninck and Breeman 1987a, b, 1988a; Stiger and Payri 1999). Patch dynamics have great ecological importance, particularly when considering processes of coral recruitment and coral–algal
682
competition. For example, a monitoring study may show that average macroalgal cover varies little over time but this reveals nothing of the underlying dynamics: are patches of macroalgae persistent and unchanging, or does an equilibrium exist between rapid patch extinction and colonisation? The ecological functions of persistent algal patches are likely to be very different from those of highly dynamic patches. For a given time interval, more dynamic systems will increase the frequency of coral– algal interactions; a coral will, on average, be more likely to encounter an algal patch if the algal colonisation rate is elevated. However, the greater extinction rate of patches in a dynamic system will also reduce the average duration of coral–algal interactions. Thus, more dynamic systems will result in frequent, but brief, interactions between corals and algae, whereas non-dynamic systems will tend to have relatively infrequent but persistent interactions. The net outcome of such dynamics depends on the susceptibility of corals to algal contact. If corals can tolerate short, but not prolonged, periods of algal contact, then high turnover rates will promote coexistence between corals and the alga because many interactions between coral and alga are relatively brief. In contrast, high turnover rates will be deleterious if even short-lived algal–coral interactions lead to reduced coral survival. Unfortunately, few quantitative data are available on the sensitivities of corals upon contact with fleshy macroalgae (Nugues et al. 2004). Here, we describe the patch dynamics of the dominant species of macroalgae on forereefs in Belize: Lobophora variegata (Lamouroux) and Dictyota pulchella (Ho¨rnig and Schnetter). The study was conducted on the exposed forereef of Glovers Atoll, Belize and began in June 1998. At this point, the reefs had not experienced a hurricane event for 20 years (Hurricane Greta, 1978). This changed 5 months later when the reef was struck by the largest hurricane of the century, Hurricane Mitch (Table 1). Two additional hurricanes occurred during the 4.5 years duration of the study, allowing us to investigate algal patch dynamics under various levels of disturbance.
We describe the natural dynamical processes of patch colonisation, growth, and extinction and test the following hypotheses: – H1: The duration and intensity of a hurricane disturbance influences the patch dynamics of L. variegata and D. pulchella. – H2: Algal colonisation occurs more frequently in larger patches of available settlement space (dead coral covered with filamentous or turf algae). – H3: The survival of algal patches during acute hurricanes is dependent on patch size.
Materials and methods The study was undertaken on the seaward side of Glovers Reef (87 48¢W, 16 50¢N), which is located approximately 30 km from the mainland and 15 km east of the Belize Barrier Reef. Two study sites, each measuring approximately 20·20 m, were located 3 km apart within the Montastraea habitat (Geister 1977) at a depth of 8–12 m and within 100 m of the escarpment. The northern-most site, Long Cay (LC), lies within 1 km of a large sand patch, and corals were more severely impacted by Hurricane Mitch than at the southern site, Middle Cay (MC). The physical environment of the atoll, location of study sites, and impact of Hurricane Mitch are described elsewhere (Mumby 1999; Andrefouet et al. 2002; McClanahan et al. 2004). Both sites were dominated by colonies of the massive coral Montastraea annularis (sensu stricto). M. annularis has a columnar morphology and living tissue is confined to the upper surfaces of the colony (Graus and Macintyre 1982). The upper surface comprises a series of distinct lobes (ramets), which vary in size from 2 to 763 cm2 (mean 37.7±1.7 cm2). Coral mortality events liberate space on these ramets that may subsequently be colonised by macroalgae (Fig. 1).
Table 1 Oceanographic statistics for impact of hurricanes at Glovers Reef between 1998 and 2003 Parameter
Dates when categorised as hurricane Hurricane category Estimated wind speeds during pass of Glovers Reef (ms1) Mean wind speed during non-hurricane conditions (2004) Index of cumulative hurricane stress at study site (HI)c
Hurricane Mitch
Keith
Iris
22 October 1998– 5 November 1998 5 72a
28 September 2000– 6 October 2000 3 21b
04 October 2001– 9 October 2001 4 33b
6.6 (2.2)
3.9 (2.0)
6.6 (2.2)
2781
2678
1557
Table contrasts impact of hurricanes with the non-hurricane conditions that prevailed in 1999, 2002, and 2003. SD given in parentheses http://www.nhc.noaa.gov/1998mitch.html http://www.ssmi.com/cyclone/cyclone.html c For comparison, indices of cumulative hurricane stress in non-hurricane years are 69 (1999); 0 (2002, 2003) a
b
683
colony). We re-calculated our results for a balanced, sixramet subset of the LC data and found that the additional data had not altered our conclusions. We report the full dataset here. Patch dynamics were studied over two time scales. In the main, longer-term study, surveys were made at eight intervals over a 4.5-year period; June 1998, October 1998, December 1998, June 1999, June 2000, May 2001, May 2002, and January 2003. Individual sampling dates were referenced in days since the beginning of the study where day 1 was the 10th of June 1998. Many of the M. annularis colonies experienced high levels of partialcolony mortality after a combination of mass coral bleaching, and Hurricane Mitch struck the atoll during the autumn of 1998. Population parameters for patches were determined for both algal species at sampling periods 2–8. Each parameter was determined between t-1 and t as follows: Fig. 1 Upper surface of M. annularis showing individual ramets and patches of live tissue. Parts of two ramets have been delineated using black for the edge of dead coral (colonised by algae) and white for live coral. Each grid cell on the quadrat measures 10 ·10 cm
Ramets of M. annularis provided a natural substratum on which the dynamics of algal patches could be quantified. All data were acquired by observing the colonisation, growth, and extinction of algal patches on existing, upright colonies of M. annularis. At each site, 20 colonies of M. annularis were selected at random and photographed using a digital video camera. Individual ramets were assigned a unique identity and monitored by placing a 1 m2 quadrat, divided into one hundred 10·10 cm squares, over the colony (a total of 281 ramets were identified). Video sequences were transferred to computer and analysed using custom-built software, VidAna,1 which allowed individual patches of substratum to be delineated on each ramet and their size to be determined (Fig. 1). Individual ramets were projected onto a large (60 cm) monitor so that algal patches were usually magnified fourfold prior to being identified and delineated. To test the accuracy of delineating patches using this technique, we placed a fine metal grid (cell size 1.2·1.2 cm) over randomly chosen patches, and compared the estimated patch size for both methods. There was no significant difference in size estimates (paired t-test p=0.79, n=17), which was due to small effect size (mean difference only 1.2 cm2) rather than low statistical power. Individual ramets were categorised into five size classes, each of which represented one-fifth of the full statistical population of ramet sizes (1–6, 7–12, 12–21, 22–46, 47–763 cm2). For each size class, a sample of six ‘target’ ramets was sampled randomly from different colonies. No colony was sampled more than once at MC; but for reasons unrelated to this study, additional sampling was undertaken at LC (i.e. more ramets per 1 The software is available free of charge from http://www.ex.ac.uk/ msel.
– Colonisation (No. of patches)—Number of new patches (colonisation events) observed from t-1 to t. – Colonisation rate (Proportion of patches month1)—Colonisation expressed as a proportion of the total number of patches at t and scaled per month (30 days). – Net rate of lateral growth (cm2 day1)—Change in algal patch size between December 1998 and June 1999 (ca. 180 days), expressed per day. – Extinction (No. of patches)—Number of patches that disappeared (extinction events) between t-1 and t. – Extinction rate (Proportion of patches month1)—Extinctions expressed as a proportion of the total number of patches at t-1 and scaled per month (30 days). – Persistence (No. of patches)—Number of patches that persisted between t-1 and t. In addition, the degree of settlement space was quantified at the scale of ramets: – Uncolonised-available (No. of ramets)—Number of ramets that were available for colonisation (i.e. possessed cropped algal turf, encrusting coralline, or filamentous algae) at t-1 and remained unoccupied by species at t. – Uncolonised-unavailable (No. of ramets)—Number of ramets that were not available for colonisation at t-1 (i.e. dominated by live coral or other fleshy algae) but became available for colonisation by t. To examine the dynamics of macroalgae on shorter time scales of days to weeks, 12 additional colonies of M. annularis were tagged at LC in July 1998. Each was photographed at fifteen intervals within a 3-month period, ranging from consecutive days to consecutive weeks and months. An initial sample of 24 ramets was acquired for each algal species. Half of these were colonised, and half were available for colonisation but not yet colonised. The frequency and type of colonisation and
684
extinction event were then recorded at intervals of 3 days, 1 week, 2 weeks, 4 weeks, and 3 months. No hurricanes occurred during this period. L. variegata was the most common alga on the reef with an overall cover of 26% (data averaged over study). L. variegata has three life forms; decumbent, crust, and ruffled, whose distribution depends on depth, the level of grazing, and habitat (Lewis et al. 1987). This study focused on the decumbent form, which has flat blades arranged in layers, and is found to a depth of ca. 120 m (Littler and Littler 2000). Species of the genus Dictyota were the second-most abundant macroalga on the reefs with a mean cover of 13%. Although D. pulchella was the dominant species of Dictyota at the study site, other species (notably D. humifusa) were occasionally seen below its canopy. Where these species were not associated spatially with D. pulchella, they were ignored (though this occurred rarely). The biomass and density of herbivores were sampled at each site using visual census. Densities of scarids and acanthurids were sampled using a minimum of ten replicate 30·4 m transects, pomacentrids were sampled using a minimum of six 30·2 m transects, and urchins (Echinometra spp. and Diadema antillarum) were sampled using a minimum of five 10·0.5 m transects. Lengths of fishes were converted to biomasses using the allometric relationships of Bohnsack and Harper (1988). The rugosity of reef habitats was calculated using a minimum of ten 2 m chain transects and calculated as the ratio of chain length to horizontal distance. Proxies for hurricane disturbance were generated from oceanographic data (Table 1). The cumulative index of hurricane stress (HI), proposed by Allison et al. (2003), was calculated using equation (1) in which w represents mean wind speed at the eye of the storm (km h1), and d is the distance between Glovers Reef and the storm track (km). The index integrates the intensity, proximity, and duration of all hurricanes passing within 100 km of Glovers Reef during a given year. All hurricane tracks were extracted from the National Hurricane Center database (http:// www.nhc.noaa.gov) and entered into a Geographic Information System where individual tracks were interpolated to 10 min intervals. X HI ¼ W 2 =InðdÞ: ð1Þ Cumulative hurricane stress was greatest during 1998 and at least 45-fold greater than non-hurricane years (Table 1). Mean wind speeds for non-hurricane conditions were acquired from the Smithsonian field station, located 15 km to the east of Glovers Reef. Wind speed was recorded every 10 min, and data were averaged for the months of September and October 2004, which corresponded to the periods of hurricanes (Table 1). Wind speeds were between 5- and 11-fold greater during hurricanes than during 2004 when no hurricanes occurred.
Results Overall trend in coral cover, settlement space and herbivore abundance The cover of living coral declined steadily after Hurricane Mitch for up to 10 months after the event (Fig. 2a, b). Further reductions in coral cover were minimal, suggesting that Hurricanes Keith and Iris had little direct impact. As coral cover declined, more space became free for algal settlement (Fig. 2a, b). However, although algae colonised dead coral, there was no subsequent reduction in the total availability of free space; rather, free space remained high, at ca. three times initial levels, for the duration of the study. At the scale of individual ramets, the availability of free space differed markedly between sites. After Hurricane Mitch, the mean percent cover of free space (per ramet) fluctuated between 13 and 18% at LC with a mean of 15%. In contrast, there was nearly twice as much free space on ramets at MC with fluctuations between 15 and 39% and a mean of 29%. Scarids had the greatest biomass of any herbivorous fish group (Fig. 2e, f). Peaks in the density of juvenile scarids (0.05). The short-term, patch dynamics of D. pulchella at LC included only one extinction event between July and September 1998. In this case, the patch was recolonised within 2 months. A total of eleven colonisation events took place during 82 days, but in a less sporadic fashion
688
a 250
S
A
W
S
S
A
W
S
Number of Ramets
S
A
W
SA
S
A
W
S
Hurricane Iris
Hurricane Keith
Hurricane Mitch
S
W
S
Summer – Winter
200 150 100 50 0
0
200
400
600
800
1000
1200
1400
1600
1800
Time (days)
b
70
S
60
Number of Ramets
A
W
S
S
A
W
S
A
S
W
S
S
A
W
S
S
A
W
S
Hurricane Iris
Hurricane Keith
Hurricane Mitch
Summer – Winter
50 Total Population Uncolonised – available Uncolonised – unavailable Colonisation Extinction Persistance
40 30 20 10 0
0
200
400
600
800
1000
1200
1400
1600
1800
Time (days) Fig. 5 Patch dynamics of D. pulchella on individual ramets of M. annularis from June 1998 to January 2003 at Long Cay (a) and Middle Cay (b). Dates and days (parentheses) are June 1998 (0), October 1998 (112), December 1998 (201), June 1999 (379), June
2000 (735), May 2001 (1,055), May 2002 (1,432), and January 2003 (1,669). The seasons summer, autumn, winter, and spring are denoted S, A, W, S, respectively
than that observed for Lobophora. One event took place in 6 days, three events in another 6 days, three events in 17 days, and four events in 51 days. Simulating the low frequency of observations used in the main study (i.e. observations on a scale of months between day 0 and 82), the observed number of colonisation events would have been ten over the 82-day period, rather than the eleven that actually took place (because one colonisation event compensated for the sole extinction event). In this case, the observed colonisation rate (0.17 month1) would underestimate the actual rate by ca. 9%. Extinction events occurred rarely (one in 82 days) so the total number of ‘missed’ events is likely to be low. Indeed, the actual extinction rate for the summer of 1998 was 0.03 month1, which agreed with the mean observed rate of 0.03 month1 during the main study. Pooling data from both sites, the maximum observed net lateral extension rate of D. pulchella was approximately three times greater than Lobophora at 0.65 cm2 days1 with a mean of 0.11 cm2 day1. Unlike Lobophora, the cover of Dictyota fluctuated dramatically during the study period, with either no net change or a net decline in cover by the end of the
observation period (Fig. 2c, d). Dictyota cover decreased between the summers of 2000 and 2001, and during the last 6 months of the study (summer 2002–winter 2002/ 2003).
Discussion Comparison of dynamics on different temporal scales Studies of population dynamics must usually compromise between the desire to capture short-term colonisation/extinction events and the logistical demands of monitoring over a reasonably long time. In this case, we wished to examine algal dynamics in response to multiple hurricane events and, as a consequence, much of the sampling was carried out at three-monthly to annual intervals. Since patches of algae could colonise and disappear between sampling dates, thereby leading to an underestimate of dynamical rates, we conducted a shortterm study to quantify dynamics at scales of days to months in the absence of intense disturbance. It appears that colonisation rates, determined on a scale of
689
a
0.3 Hurricane Mitch
Rate per month
0.2
Summer – Winter
Hurricane Keith Hurricane Iris
0.1 0 –0.1 –0.2
b
0
200
400
600
1200
1400
1600
1800
0.06 Summer – Winter
Hurricane Mitch Hurricane Keith
0.04 Rate per month
800 1000 Time (days)
Hurricane Iris
0.02 0 Colonisation Rate Extinction Rate Difference
–0.02 –0.04
0
200
400
600
800 1000 Time (days)
1200
1400
1600
1800
Fig. 6 Colonisation and extinction rates (per month) for patches of D. pulchella at Long Cay (a) and Middle Cay (b). To relate days to dates, see Fig. 5. Note that y-axes differ. The overall dynamics
from short-term (3 months) observations at LC are added near the y-axis and without lines
3 months, may be underestimated by approximately 9%, whereas extinction rates are barely influenced by more frequent sampling. In short, quarterly to annual time intervals are appropriate for quantifying the dynamics of L. variegata and D. pulchella.
Therefore, small changes in population rates had relatively large impacts on the total cover of Dictyota. Hurricane Mitch was the first hurricane to strike Glovers Reef in 20 years and the largest storm of the century. Not surprisingly, the hurricane had a highly detrimental impact on corals, killing large areas of tissue. Since algae cannot settle on living corals (DiazPulido and McCook 2004), both algal species benefited indirectly from the increase in substratum generated by the hurricane. Hurricanes Keith and Iris did not depress coral cover further, and therefore had little indirect impact on the algae. Successive hurricanes often have relatively weak impacts when a reef has been damaged recently and insufficient time has passed for much recovery (Hughes 1989; Rogers 1993; Rogers et al. 1997). The indirect impact of Hurricane Mitch on L. variegata was large, leading to at least 4 years of increasing cover and a small decrease in the latter 6 months at LC. However, the hurricane had little longterm (4 years) impact on D. pulchella. The direct effect of Hurricane Mitch was a massive extinction of algal patches, particularly at LC, which was extensively scoured by sand. The magnitude of this
Overall impact of hurricanes on algal patch dynamics The dynamics of the two algal species were found to differ markedly and in non-intuitive ways. For example, whilst the cover of D. pulchella varied considerably over time, the underlying patch dynamics were relatively stable. In contrast, L. variegata showed a steady increase in cover after Hurricane Mitch, despite greater dynamism in the colonisation and extinction of patches. Thus, variation in the overall percent cover of an alga is not indicative of the underlying patch dynamics. In addition to colonisation and extinction rates, fluctuations in cover depend upon the total number of patches and their lateral growth rates. In the present study, Dictyota was more abundant and its growth rate was approximately three times greater than Lobophora.
690
70
Percent of patches in size category
Fig. 7 Relative size-frequency distribution of patches of D. pulchella at Long Cay (LC) and Middle Cay (MC). Distributions plotted for three points in time with respect to Hurricane Mitch: 1 month before, 1 month after, and 18 months after. Lines are plotted to aid visual interpretation of the pattern but they have no actual meaning
60 1 month pre Mitch, LC 1 month post Mitch, LC 18 mo. post Mitch, LC 1 month pre Mitch, MC 1 month post Micth, MC 18 mo. post Mitch, MC
50 40 30 20 10 0 30
2
Size category of patch (cm )
impact was easily detectable 1 month after the storm, but barely measurable 8 months later (in the summer of 1999) because of rapid recolonisation of algae. The intensity and duration of Hurricanes Keith and Iris were less than those of Mitch, but in each case, at least 6 months elapsed before post-hurricane sampling. Given the rapid response of algae to direct hurricane impacts (as evidenced post Hurricane Mitch), we were unable to test hypothesis 1: that the duration and severity of disturbance influences algal patch dynamics. Whilst it seems likely that the direct impact of the latter hurricanes would have been relatively light, we can only conclude that any direct impact was undetectable after 6–8 months. Impact of patch size on dynamics The fate of individual algal patches was partly determined by their size such that larger patches were less likely to become extinct. Such size refugia may occur because larger patches have a greater number of holdfasts, and simply require more sustained disturbance to be fully removed. Lobophora, and to a lesser extent Dictyota, was more likely to colonise larger patches of free space than smaller patches. Whilst this may seem obvious given that larger ‘targets’ are more likely to receive random settlement, this observation differs in the studies of Lobophora colonisation on reef slopes in Curac¸ao (de Ruyter van Steveninck and Breeman 1987a). The latter study found that Lobophora had very limited dispersal, and was less likely to colonise larger patches of free space as this would require greater dispersal. The apparent paradox may be reconciled by considering the scales of dispersal involved. Lobophora colonised the sides of all
M. annularis colonies monitored in our study, and therefore most uncolonised ramets were within 0.5 m from a source of potential colonisers. In contrast, some of the settlement plates used in the Curac¸ao study were placed at a greater (though not quantified) distance from the main canopy (E. de Ruyter van Steveninck, personal communication). In short, our results may have differed markedly if the uncolonised patches had been located on other substrata, located further from a source of propagules. Other factors impacting algal patch dynamics Although L. variegata is a relatively unpalatable alga (Paul and Hay 1986; Targett et al. 1995), several studies have documented growth limitation by herbivores (de Ruyter van Steveninck et al. 1988b; Jompa and McCook 2002b; Diaz-Pulido and McCook 2003). Whilst it is highly probable that herbivores reduced the growth rate of Lobophora in the present study, there was no clear suggestion that herbivores limited the total cover of this alga; cover increased steadily despite a substantial increase in parrotfish biomass. Other than space, the overall constraints to the cover of Lobophora remain enigmatic and will require careful study over long periods (>5 years) to elucidate. The response of D. pulchella to a vast increase in available substratum was surprising; there was no net increase in cover over a 4-year period (in fact, a net decrease at MC). Clearly, the cover of D. pulchella is not limited by the availability of settlement space. Several other explanations may account for fluctuations of this alga, but all require experimental studies to distinguish their relative importance. We conclude by setting out four hypotheses to be tested in future.
691
H1—Scarids allocate more of their grazing towards the top of M. annularis colonies after corals experience mass mortality Although the cover of D. pulchella and biomass of scarids were not negatively correlated, scarids are highly likely to influence the cover of this alga and in potentially subtle ways. Larger adult scarids such as Sparisoma viride and Scarus vetula take approximately 40% of their bites from Dictyota (Mumby, unpublished data). Many parrotfish also prefer to feed on dead Montastraea because it has relatively low density, which facilitates consumption (Bruggemann et al. 1994). Indeed, pooling across all parrotfish species, 55% (8,800 bites) of all observed bites were taken from dead Montastraea at the study site in July 2000 (Mumby, unpublished data). Given that dead Montastraea is a preferred feeding substratum, the intensity of grazing may increase in this microhabitat without requiring a numerical response in the biomass of parrotfishes (i.e. fish may switch more of their bites to this microhabitat once more of it becomes available after coral mortality). This phenomenon may also partly explain the maintenance of large areas of grazed substratum once the corals had declined. The apparent lack of correlation between free space and scarid biomass could be attributable to a reallocation of grazing preferences towards dead Montastraea rather than a direct numerical response of parrotfishes. H2—Damselfishes preferentially remove D. pulchella from their territories Colonies of M. annularis provide a habitat for the damselfish Stegastes planifrons (Tolimieri 1995, 1998). Whilst Hinds and Ballantine (1987) did not find Dictyota in the guts of S. planifrons, their territories often include Dictyota spp. (de Ruyter van Steveninck 1984). Preferential weeding of undesirable algal species has been documented in some pomacentrids (Lassuy 1980), but whether this is a feasible mechanism for the control of D. pulchella remains to be tested.
H4—Low temperatures in winter limit the growth rate and cover of D. pulchella The dynamics of Dictyota exhibit seasonality. In upwelling zones of Colombia, Dictyota bartayresiana blooms during seasonal upwelling when temperatures decline and nutrient levels rise (Diaz-Pulido and Garzon-Ferreira 2002). Contrasting effects of temperature have been observed in non-upwelling zones. Liddell and Ohlhorst (1986) recorded a reduction in the cover of Dictyota species during cooler winter months in Jamaica, and the winter reductions in cover reported here from the last 6 months of the study are also consistent with a temperature-dependent control of cover. Two possible mechanisms may account for such dynamics. First, temperature- and possibly light-induced reductions in growth rate may allow grazers to reduce the standing crop of algal tissue in winter. Second, colonies of Dictyota may reduce their standing crop through reproduction. Unfortunately, data on the reproduction of D. pulchella are scarce, but information is available for other genera, and these are considered by some to be representative of the order (Van den Hoek et al. 1995). Studies by Hoyt (1907, 1927) on Dictyota dichotoma collected from Jamaica reported gamete production a few days prior to neap tide, followed by gamete liberation after the highest succeeding spring tide during the summer months. Recent studies in the Azores (Neto 2000) recorded an increase in the abundance and biomass of D. dichotoma in summer, but reproduction showed no clear seasonality. In short, basic studies of the reproductive biology of these common macroalgae are needed in order to understand their dynamics. Acknowledgements This study was funded by the Royal Society and NERC (NER/A/S/2001/01127). We thank Tom Opishinski for providing meteorological data from the Smithsonian field station and Stuart Kininmonth (AIMS) for the GIS analysis. This is contribution 26 from Glovers Reef Marine Station.
References H3—Grazing by the urchin Echinometra spp. may limit D. pulchella on M. annularis Grazing by the urchin Echinometra spp. may contribute to the control of D. pulchella without urchins exhibiting a numerical response. The plasticity of urchin populations in response to changes in density or food availability is well documented (Carpenter 1981; Levitan 1988). Conceivably, an increase in food availability whilst urchin densities remain low might be compensated by an increase in the size of feeding apparatus, rather than a positive numerical response in urchin density. Furthermore, the higher density of urchins at MC may partly explain the increase in grazed substratum at this site. Densities of D. antillarum remain barely measurable at both sites (
