MARINE ECOLOGY PROGRESS SERIES Vol. 123: 95-106, 1995 I Published July 20 Mar Ecol Prog Ser I L P P
Recurrent destructive grazing of successionally immature kelp forests by green sea urchins in Vestfjorden, Northern Norway
Nils T. Hagen
Department of Fisheries and Natural Science. Bode College. N-8002Bode, Norway
ABSTRACT: Outbreak populations of the green sea urchin Strongylocentrotus droebachiensis Miiller caused widespread decimation of the original Laminaria hyperborea (Gunn.) Fosl. kelp forest in Vest- florden, Northern Norway, during the early 1980s. In the follow~ng decade, some of the resulting urch~n-dominated barren grounds reverted to kelp forest, which, after persisting for more than 5 yr, began to be eliminated yet again. Age analysis of annual growth rings in kelp stipes from field sites at V~rayIsland inlcate that the time of initial kelp recovery varied from site to site but took place between 1984 and 1987. The earliest independent observations of localized macrophyte recovery were made in 1984 at the Harbour Pier site, where, by August 1992, the new kelp forest had already been eliminated by recurrent destructive grazing. Sea urchin density inside re-established kelp forests at 3 other sites on Vaer~yIsland was 45 to 75 ind. m-2 in 1992. These urchin populations had significantly aggregated spatial patterns, and recurrent destructive grazing appeared to be mrmnent. This predic- tion was verified in 1993 when barren grounds reappeared at all study sltes. The threshold conditions for initiation of destructive grazing have been approximated by a curve in the aggregation-density plane. Sea urchins in the Vestfjorden area are infected by the recently discovered epizootic endopara- sitic nematode Echinornermella matsi. In 1992, the prevalence of E. matsiat Varay Island ranged from 8.8% in the barren ground at the Harbour Pier site, to between 13.6 and 21.6% in the successionally immature kelp forest at the 3 other sites. The observed kelp forest recovery at Vceray Island was predicted by the macroparasite hypothesis which states that E. matsi may function as a terminator of sea urchin outbreaks in Northern Norway. However, the succession towards an ecologically mature kelp forest community has been interrupted by the unexpected recurrence of destructive grazing, and the macroparasite hypothesis must therefore be rejected in its present form. Furthermore, these local events may, on the larger time and spatial scales of the current outbreak phenomenon, indicate that the euphotic hard bottom component of the coastal ecosystem in Northern Norway has entered a cyclical domain.
KEY WORDS: Sea urchin outbreak. Kelp forest destruction. Epizootic disease . Aggregation - Strongy- locentrotus . Laminaria . Echinornerrnella
INTRODUCTION et al. 1966, Leighton 1971, Breen & Mann 1976, Fore- man 1977, Hagen 1983) and maintain a barren com- Sea urchins are important agents of disturbance munity configuration dominated by crustose coralline and are frequently regarded as proximate determi- algae (Chapman 1981); and, in part, on evidence nants of community structure in subtidal marine indicating that reduced grazing pressure in such bar- macrophyte habitats (reviews by Lawrence 1975, ren grounds invariably triggers rapid recolonization Lawrence & Sammarco 1982, Dayton 1985, Schiel & of kelp (Breen & Mann 1976, Pearse & Hines 1979, Foster 1986, Harrold & Pearse 1987, Chapman & Duggins 1980, Andrew & Choat 1982, Breen et al. Johnson 1990). This generalization is based, in part, 1982, Hirnrnelman et al. 1983, Dayton et al. 1984, on evidence indicating that outbreak populations of Miller 1985b, Novaczek & McLachlan 1986, Scheib- sea urchins can decimate large kelp forests (Leighton ling 1986, Hughes et al. 1987, Keats et al. 1990). How-
O Inter-Research 1995 Resale of full article not permitted 96 Mar Ecol Prog Ser
ever, at the next level of causality there exists a mul- This paper reports regrowth of kelp, as predicted by titude of l~ttleknown factors which, depending on the the macroparasite hypothesis, in an area of Northern initial community configuration, may either control Norway where the original kelp forest was destroyed the onset of destructive grazing or allow a reduction by outbreak populations of Strongylocentrotus droe- in grazing pressure to a level which permits macro- bachiensis in the early 1980s. The unexpected recur- algal recovery. rence of destructive grazing in the successionally im- Currently, the 2 leading hypotheses of sea urchin mature kelp forest is also reported, and the ecological outbreak termination state that the transition from implications of this novel phenomenon are discussed. urchin-dominated barren ground to kelp forest is facil- itated by reintroduction of a keystone predator, or by epizootics of microparasitic (sensu Anderson & May MATERIALS AND METHODS 1979) disease. The keystone predator hypothesis of outbreak termination pertains to only 1 species, the Sampling. Samples of sea urchins and kelp were col- Pacific sea otter Enhydra lutrjs Milne-Edwards (Estes lected by SCUBA divers at 4 previously investigated & Palmisano 1974, Estes & Harrold 1988, Foster & field sites at Vaersy Island on 25 to 27 August 1992 Schiel 1988), while the hypothesis of microparasitic (Mbstad, Lighthouse Bay, Tiny Bay, Harbour Pier). The disease-related outbreak termination, although evoked location of the field sites is described in an earlier in connection with several ~ncidences of sea urchin paper (Hagen 1987, Fig. 1B therein), which is also the mass mortality (Pearse et al. 1977, Boudouresque et source of the pre-1991 raw data figures used in the al. 1980, Lessios et al. 1984, Dayton et al. 1992), has present study. in only 1 instance been supported by conclusive Sea urchins were collecting by repeated spot sam- identification of the suspect pathogenic agent, i.e. the pling of all specimens within reach of a stationary amoeba Paramoeba invadens Jones (Jones 1985, Jones diver. At each field site the sampling spots were hap- & Scheibling 1985, Jones et al. 1985a, b). Other sug- hazardly chosen to randomize the collection, and at gested mechanisms which may reduce the grazing each sampling spot the substratum was thoroughly pressure of sea urchins sufficiently to permit macroal- searched for small and cryptic individuals in an gal recovery include a lack of recruitment of juvenile attempt to ensure that a representative sample was sea urchins (Foreman 1977, Watanabe & Harrold obtained. This method is considered adequate for sea 1991), storm disturbance (Harris et al. 1984, Ebeling et urchins 25 mm in diameter but not for smaller indi- al. 1985, Andrew 1991), or a temporarily increased viduals from the 0 age group cohort. influx of unattached food items (Duggins 1981, Harrold All collected sea urchins were temporarily stored in & Reed 1985). running seawater tanks onboard the research vessel Nevertheless, none of these suggested mechanisms of Nordland College, RV 'Raud'. The collected urchins of outbreak termination appear to be acting upon out- from 2 sites (Msstad and Tiny Bay) were immediately break populations of the green sea urchin Strongylo- processed in a field laboratory on V~rsyIsland, while centrotus droebachiensis Miiller in Northern Norway the urchins from the 2 additional sites (Harbour Pier (Hagen 1983, 1987). Instead a novel hypothesis of and Lighthouse Bay) were transported by RV 'Raud' to outbreak termination by macroparasitic (sensu May & another running seawater facility at The Marine Labo- Anderson 1979) epizootic disease has been proposed ratory of Nordland College and processed by 2 Sep- (Hagen 1992). This hypothesis was inspired by the tember 1992. The test diameter of the collected sea recent discovery of Echinomermella matsi (Jones & urchins was measured using vernier callipers with Hagen 1987), a large endoparasitic nematode whose 0.1 mm precision. The kurtosis and skewness of the abundance has reached epizootic proportions in the size-frequency distributions were tested for departure Norwegian outbreak populatlons of S. droebachiensis from a normal distribution as described by Sokal & (Hagen 1987). The macroparasite hypothesis predicts Rohlf (1981). that parasite-induced mortality of adult sea urchins All collected sea urchins were dissected, and the may reduce sea urchin density sufficiently to permit penvisceral coelom of each sea urchin was inspected regrowth of kelp and other non-encrusting macro- under a magnifying lamp to determine whether para- algae, but, unlike the dramatic mass mortalities in- sitic nematodes were present. The null hypothesis of duced by epizootics of microparasitic disease agents no difference in parasite prevalence in the samples (Pearse et al. 1977, Boudouresque et al. 1980, Lessios et from 1983 and 1992 was tested in a 2-way contingency al. 1984, Scheibling & Stephenson 1984, Jones & Scheib- table analysis (G-test; Sokal & Rohlf 1981). Hetero- ling 1985), it is expected that the potential regulatory geneity of variances (Bartlett's test; p < 0.001) and non- impact of E. matsi is reflected by a gradual decline of a normality (see Table 1) precluded the use of ANOVA hea.vily parasitized urchin population. In the analysis of sea urchin test d~ameterdata. In an Hagen Sea urchin outbreak terminationin Northern Norway 97
alternative approach the test diameters of infected and reverted to dense macrophyte beds dominated by the non-infected urchins in samples from 1983 and 1992 perennial kelp Laminaria hyperborea. However, the date were compared using Kolmogorov-Smirnov tests. kelp forest at the Harbour Pier site was confined to a Sea urchin density was estimated by counting all small stand (c100 m across) of L. hyperborea, and urchins inside a 0.25 m2 frame. At each site at least there were a few isolated holes (
Island parallels the pattern of decline HARBOUR PIER TINY BAY during the destruction of the original N = 20 N = 19 kelp forest 12 yr earlier (Hagen 1983).
Sea urchin density and aggregation
The quantitative analysis suggest that sea urchin density in 1992 was similar (Tiny Bay, Harbour Pier) or higher (Mbstad, Lighthouse Bay) than it was in 1983 (Tables 1 & 2). However, in 1984 LIGHTHOUSE BAY the urchin density in Lighthouse Bay, N=18 and outside the Harbour Pier, was sub- jectively estimated at
Fig 2. Laminaria hyperborea and Stron- COMMUNIV STATE gylocentrotus droebachiensjs. Community Mature Barren Immature Barren dynamics at 4 field sites on Vsrcry Island, kelp forest around kelo forest around Northern Norway. During the early 19805, I the mature L. hyperborea kelp forest was replaced by barren grounds dominated by the sea urchin S. droebachiensis. Kelp re- -- growth occurred in the rmd 1980s, but this re-established kelp forest was destroyed and replaced by barren grounds again in the early 1990s when 11 was still succes- sionally immature. Years when observa- tions were made indicated with bold type- -2 face The time of kelp regrowth at Mastad 77 '78 '79 '80 '81 '82 '83 l '84 '85 '86 ' '87 '88 '89 '90 '91 '92 '93 '94 and in Tiny Bay was estimated by ageing 7 YEAR of kelp plants collected in 1992 Hagen: Sea urchin outbreak termination in Northern Norway 99
Table 1 Strongylocentrotus droebachiensis and Echinomermella matsi Sampling data and population characteristics for sea urchins from Vzroy Island, Northern Norway. SE in parentheses, N.total number of collected specimens; N,: number of infected S, droebachiensis; N,:number of replicate density measurements; t,, and tSz:t-values for skewness (g,) and kurtosis (g2) of slze-frequency distribution when tested for departure from normal dlstrlbution. Critical t-values: h,,,,,, = 1.960; bu,,,, = 2.576; tooalrMr= 3.291. S.d.: S. droebachiensis; x2= (N, - 1) V/m: chi-squared test, H": V/m (variance/mean) I-atioof population density = 1; V-m = +l: Morisita's index; Significant test results indicated by asterisks: 'p < 0.05, '.p < 0.01, "'p < 0.001 i, m2 -(v/N,)
l Site Year Sample Mean test Skewness Kurtosis Mean population Aggregation size diameter denslty rJ N~ (mm) 91 tsl g2 ts2 S d, m-2 N, x2 iM Harbour Pier 1981 67 38.8 (1 68) 0.099 0.338 -0.936 1.668 47 8 (10.4) 17 153.5"' 1.755 1983 135 22 40.9 (1.09) -0.989 4.743"' 0.196 0.480 42 5 (4.83) 16 32.9 1.114 1992 148 13 35.9 (1.39) -0.292 1.465 -1.278 3.270' 41.8 (5.76) 20 75.5"' 1.290
Lighthouse Bay 1981 526 50.6 (0.53) -0.752 7.061 "' -0.064 0.302 1983 105 44 41.1 (1.69) -0.103 0.437 -1.356 2.958" 26.1 (5.39) 15 58.4"' 1.507 1992 342 74 30.3 (0.97) 0.402 3.048" 1.291 4.937"' 60.6 (12.26) 20 236.2"' 1.787 Tiny Bay
Table 2. Strongylocentrotus droebachiensis. Single factor analysls of the effect of sampling date on the density of 4 sea urchin populations at V~royIsland, Northern Norway. df: degrees of freedom; MS: mean square. Significant test results indicated by asterisks: 'p < 0.05, "p < 0.01
I ANOVA df MS F-value I
Harbour Pier (1981, 1983, 1992) Resldual Mastad (1981, 1983, 1992) Residual Lighthouse Bay (1983, 1992) Residual Tiny Bay (1983, 1992) Residual
Tukey-Kramer df Difference Cntical post hoc cornpanson value Mdstad 1981 vs Mdstad 1983 29 20.850 31.534 Mdstad 1981 vs Mdstad 1992 32 40.547 38.375" Mastad 1983 vs Mastad 1992 33 19.697 29.772 00 1 1.5 2.0 2.5 3.0 AGGREGATION(j,) Parasite prevalence Fig. 3. Strongylocentrotus droebachiensis. Population density and degree of aggregation in sea urchin samples from Veeray The maximum prevalence of Echinomermella matsi Island, Northern Norway. Three data points connected by at Vzrsy Island decreased from -40 % in 1983 to -20 % a power curve represent samples from the successionally in 1992. This reduction, which occurred at the Light- immature kelp forest. These samples were taken in 1992, house Bay site, was the only significant change in par- at the time of the onset of recurrent destructive grazing. h: asite prevalence (Table 3). However, parasite preva- Morisita's index lence underwent a near significant reduction from 16.3 to 8.8% at the Harbour Pier site, and a near sig- changed at approximately 20 %. These results suggest nificant increase from 7.5 to 14 O/oin Tiny Bay (Table 3). that the prevalence of E, mafsi at V~reryIsland is now At Mastad parasite prevalence remained virtually un- at an intermediate level. 100 Mar Ecol Prog Ser 123: 95-106, 1995
Table 3. Strongylocentrotus droebachjensis and Echinomermella matsi. ever, as mentioned above, it has been Analysis of changes in parasite prevalence in sea urchin populations at observed (Harbour Pier, Lighthouse Bay), V~rayIsland, Northern Norway. G-test of the null hypothesis: parasite or can be inferred from the history of kelp prevalence is independent of sampling date (1983 or 1992). Critical values for G x~"~~~~~= 3.841 and x2onnlll)= 10.828. Significant test results indicated forest recovery (Mbstad, Tlny Bay), that by asterisks: '''p = 0.05, "'p < 0.001 adult sea urchin density at all sites must have been considerably lower at some Site Yea1 Prevalence APrevalence G-value point in the 1984 to 1991 time interval (%) Difference %Change than it was in either 1983 or 1992. The shape of the size-frequency distrib- Harbour Pier 1983 16.3 1992 8.8 -7.5 -46.1 3.697''' utions indicates that recent recruitment 21.1 has been good (Fig. 5). Furthermore, the 20.6 -0.5 -2.4 0.016 presence of urchins 260 mm in test diam- Lighthouse Bay 1983 41.9 eter in all samples from 1992 indicate that 1992 21.6 -20.3 -48.4 15.964 "' there has been a continuous presence of Tiny Bay 1983 7.5 sea urchins at all field sites during the 1992 13.6 6.1 80.9 3.699'" period of kelp recovery (Fig. 5).
DISCUSSION Test diameter and size-frequency distribution Macroalgae recovery Six out of 8 possible tests suggested that sea urchins at Vceroy Island were smaller in 1992 than they were in The first localized regrowth of the macroalgal vegeta- 1983 (Table 4, Fig. 4); only non-infected urchins from tion in Northern Norway was observed in 1984 at MBstad and infected urchins from the Harbour Pier site Vceray Island (Hagen 1987), only 3 to 4 yr after the had similar mean test diameters. This is an indication original kelp forest in this area had been eliminated by of increased abundance of juvenile sea urchins, since outbreak populations of Strongylocentrotus droebachi- sea urchin densities in 1992 were similar or higher ensis (Hagen 1983). By 1992, most of the urchin-domi- than in 1983 (Tables 1 & 2). Infected sea urchins from the re-estab- lished kelp forest (Mastad 1992, Light- Table 4 Strongylocentrotus droebachiens~s and Echlnomermella matsi house Bay 1992, Tiny Bay 1992) were Analysis of the effects of parasite status and sampling date on the test diam- significantly smaller than non-infected eter of sea urchins from V~ruyIsland, Northern Norway. Significant test urchins, whereas no significant size differ- results indicated by asterisks: '')p = 0.05, 'p < 0.05, "p < 0.01, "'p c 0.001 ences were detected between infected and non-infected urchins from the barren Kolmo~orov~Smirnov Test statistic p-value grounds (Table 4, Fig. 4). Harbour Pier In 1992 the peakedness of the size-fre- 1983 infected vs 1983 non-infected 3.173 0.4092 quency distribution of Stongylocentrotus 1983 infected vs 1992 infected 2.014 0.7305 droebachjensis had changed from normal 1983 non-infected vs 1992 non-infected 11.113 0.0077 " 1.131 >0.9999 or leptokurtic, to significantly platykurtic, 1992 infected vs 1992 non-infected at all 4 sites (Table 1, Fig. 5), i.e. the rela- Mastad tive abundance of juvenile sea urchins 1983 infected vs 1983 non-infected 6.840 0.0654 1983 infected vs 1992 infected 28.356 <0.0001"' had increased. Increased juvenile abun- 1983 non-infected vs 1992 non-infected 1.764 0.8277
1 1 dance is also indicated by~ significant- 1992 infected vs 1992 non-infected 17.039 0.0004"' rightward changes in the skewness of the Lighthouse Bay size-frequency distributions at 3 sites and 1983 infected vs 1983 non-infected a drop in significance level at 1 site (Tiny 1983 infected vs 1992 infected Bay) (Table 1; Fig. 5). The absolute abun- 1983 non-infected vs 1992 non-infected dance of adults had evidently decreas- 1992 infected vs 1992 non-infected ed at sites where sea urchin density Tiny Bay appeared unchanged (Harbour Pier, Tiny 1983 infected vs 1983 non-~nfected 1983 infected vs 1992 infected Bay), but juvenile abundance must have 1983 non-infected vs 1992 non-infected increased at sites with higher density 1992 infected vs 1992 non-infected (Mbstad, Lighthouse Bay, Table 1). How- Hagen: Sea urchin outbreak termination in Northern Norway 101
nated barren grounds at Viersy Island 52 HARBOUR MASTAD LIGHTHOUSE TINY BAY had reverted to dense kelp forest, and PIER BAY age determination of the perennial Laminaria hyperborea plants, which can be > 15 yr old (Kain 1967, Sjatun et al. 1993), indicated that widespread kelp regrowth had occurred as early as 1986 to 1987. The new kelp forest at Vieray Island, although 4 to 7 yr old, was still lacking ' the characteristic undergrowth and 36 epiphyte assemblages of the orlginal l- kelp forest (Hagen 1983, Fig. 5 therein, Hagen 1987, Fig. 7 therein). Previous studies in established kelp forests sug- 28 gest that the rugose stipes of Laminaria hyperborea are colonized in a non- linear fashion, whereby the biomass of the attached flora and fauna increases abruptly when the kelp plants are ap- 1983 1992 1983 1992 1983 1992 1983 1992 proximately 5 yr old (Whittick 1983, YEAR Haiszter et al. 1992, Rinde et al. 1992, Haiszter & Qdegaard 1994).However, Fig. 4 Strongylocentrotus droebacl~iens~sand Echinomermelia matsi. Mean the colonization of the stipes in the new test diameter of infected and non-infected sea urchins in samples from V~r@y kelp forest at Varary Island appeared to Island, Northern Norway be delayed, perhaps because propag- ules of the previously associated organisms were scarce was nearly con~pleteat 1 field site, initiated at another, due to the virtual absence of established kelp forest in and appeared imminent at the 2 remaining sites. One the vicinity of the island. year later, in August 1993, the barren ground site Signs of site-specific macrophyte recovery else- appeared qualitatively unchanged, but there was evi- where in Northern Norway (Skadsheim et al. 1994) dence of destructive grazing at the macrophyte sites. suggest that the observed macrophyte recovery at Canopy cover reductions ranged from -10 to >50%, V~rayIsland is but a local manifestation of a process and the spatial extent of the kelp forest destruction operating on a larger geographic scale. This gradual was proportional to the mean density of the resident and spatially variable transition, from urchin barren urchin population. These results suggest that the new grounds to kelp forest, differs from the rapid kelp kelp forest is being eliminated before it reaches the recolonization which followed when a decade of sea -10 to 20 yr persistence a Laminaria hyperborea forest urchin dominance was terminated by mass mortalities requires to attain ecological maturity (cf. Hais~ter& of Strongylocentrotus droebachiensis off Nova Scotia Odegaard 1994). in the early 1980s (Scheibling & Stephenson 1984, The spatial progression of destructive grazing in the Miller 198513, Novaczek & McLachlan 1986, Scheibling re-established kelp forest at Vieray Island followed a 1986, Johnson & Mann 1988). The swiftness of the site-specific pattern, similar to that of the original kelp Nova Scotian kelp recovery was apparently a result of forest destruction (Hagen 1983). However, the actual complete sea urchin population die-offs along sections grazing process differed in that there was virtually no of the Atlantic coast of the province (Scheibling 1986). undergrowth or epiphyte assemblages for the urchins In contrast, the analyses of sea urchin size frequencies to graze before the new kelp plants were attacked. and kelp age at Vzrsy Island suggest that kelp re- The onset of destructive grazing is governed by the covery has been impeded by the continued presence of local abundance and feeding behaviour of the sea diminishing sea urchin populations. urchins, i.e. the urchins switch from a passive detri- tivorous mode of feeding to an active herbivorous mode of feeding when their local abundance has Recurrent destructive grazing increased beyond a critical threshold value (Mann 1977, Harrold & Reed 1985, Harrold & Pearse 1987). In 1992, destructive grazing of the successionally The critical local abundance threshold of Strongylo- immature re-established kelp forest at Viersy Island centrotus droebachiensis in a Nova Scotian Laminaria 102 Mar Ecol Prog Ser 123. 95-106, 1995
mates from the 3 kelp forest sites at TINY BAY 1983 TINYBAY 1992 Vsersy Island, is apparently the first explicit estimate of these threshold conditions for any kelp forest system (Fig. 3). The curve specifies a testable hypothesis and provides a quantitative predictor of impending destructive graz- ing. The degree of aggregation in the kelp
LIGHTHOUSE LIGHTHOUSE resident urchin populations at Vsersy IBAY 1983 BAY 1992 1 Island was inversely related to population density, i.e, the highest level of aggrega- tion occurred at the lowest population density. This result is contrary to results from laboratory experiments which indi- cate that Strongylocentrotus droebach- iensis becomes increasingly aggregated in response to increasing density (Hagen & Mann 1994).However, both field obser- vations (Bernstein et al. 1981) and labora- tory experiments (Hagen & Mann 1994) suggests that the presence of wolffish, Anarhichas lupus L., makes sea urchins less aggregated. The wolffish is common in the study area. It is a visual predator (Keats et al. 1986), which increases its
HARBOUR HARrnUR consumption of sea urchins in response to PlER 1981 PlER 1992 increasing sea urchin density (Hagen & N-67 N=148 I Mann 1992). It is possible, therefore, that increasing density may have made the sea urchin populations more attractive to foraging wolffish. It is also possible that lower levels of aggregation in barren grounds (Fig. 3) may be related to an increased presence of wolffish. The observed recurrence of destructive DIAMETER (mm) grazing by Strongylocentrotus droe- bachiensis at Vzrsy Island is apparently Fig. 5. Strongylocentrotus droebachiensis and EchinomerrneUa rnatsi. Size- frequency distributions of infected and non-lnfected sea urchlns In samples '"precedented for Norwegian from V~r0vIsland, Northern Norway There is only von Duben's (1847) 150 yr old report of kelp forest destruction prior to the current sea urchin outbreak. This is longicruris forest was estimated at ca 2 kg urchin bio- different from the situation in the Northwest Atlantic mass m-2 (Breen & Mann 1976). However, the local where there is 1 historical report of kelp bed destruc- abundance or density of a population is rarely equal tion by S. droebachiensis (Scott 1902), several anecdo- to its mean value but may vary depending on the tal references to past sea urchin outbreaks (Stephens population's degree of aggregation (Pielou 1977, 1972, Adey & Macintyre 1973, Breen 1980, Wharton & Hurlbert 1990). Therefore, the estimation of a local Mann 1981, Pnngle et al. 1982, Miller 1985a) or high density threshold for the onset of destructive grazing densities of S. droebachiensis (Stimpson 1854, Verrill In a kelp forest requires an estlmate of the sea urchin 1866, Ganong 1885, Dexter 1944, Swan 1966), 1 well- population's degree of aggregation in addition to an documented outbreak (Breen & Mann 1976, Wharton estimate of its mean density. In general, the threshold & Mann 1981, Miller & Colodey 1983, Scheibling & conditions wlll include a range of mutually depen- Stephenson 1984, Mlller 1985b, Schelbllng 1986), and dent density and aggregation values. The curve in most recently a suggestion that yet another outbreak is the aggregation-denslty plane, which connects esti- underway (Scheibling et al. 1994). Hagen: Sea urchin outbreak termination in Northern Norway 103
Dynamics of outbreak termination an unimodal shape with a peak in the smaller size classes (Hagen 1992). The observed changes in the The rocky subtidal habitat at Vzr~yIsland has gone size-frequency distributions of Strongylocentrotus from undisturbed Laminan'a hyperborea forest, to droebachiensis from V~r0yIsland are consistent with Strongylocentrotus droebachiensis-dominated barren thls prediction. Parasite-related host mortality is also ground, to immature kelp forest, and back to barren expected to prevent accumulation of Infected indi- ground again in little more than 10 yr (Figs. 2 & 6).The viduals in the larger size classes. Again, the results are observed kelp forest recovery was predicted by the consistent with this prediction, as the mean test dia- macroparasite hypothesis which states that epizootic meter of infected sea urchins in the kelp forest was occurrence of the endoparasitic nematode Echinomer- smaller than, and in the barren ground equal to, the mella matsi may terminate sea urchin outbreaks in mean test diameter of non-infected sea urchins. This Northern Norway by reducing the density of adult sea may, furthermore, be an indication that the suscepti- urchins sufficiently to permit recovery of macroalgae bility of small urchins to infection by Echinomermella (Hagen 1987, Hagen 1992). matsi is independent of the prevailing community con- Density reduction caused by parasite-related host figuration, whereas, large, presumably well-nourished mortality is expected to alter the size-frequency distri- urchins in the kelp forest are less susceptible than their bution of the sea urchins, from an unimodal shape with starved counterparts in the barren grounds. a peak in the larger size classes, to a bimodal shape or Whether the observed kelp forest recovery at Vzr~y Island was actually induced by Echinomermella matsi is still a matter of debate, as it has been suggested that BARREN GROUND hitherto unknown sources of adult sea urchin mortality Strongylocentrotus droebach~ensfsabundant may be operating independently or in conjunction with Echinomermella matsi prevalent Lamlnaria hyperborea absent E. matsi (Stien 1993, Skadsheim et al. 1994). Neverthe- Crustose coralllne algae dominant less, the succession towards an ecologically mature kelp forest community has been interrupted by the unexpected recurrence of destructive grazing, and the DESTRUCTIVE Urchin denslty macroparasite hypothesis must therefore be rejected GRAZING A in its present form. It is also evident that the basic I dichotomy between barren ground and kelp forest, Urchln density J. which has been used as a descriptive metaphor for & aggregation KELP outbreaks of Strongylocentrotus droebachiensis in the ~ncreasing RECOVERY Northwest Atlantic (e.g. Chapman & Johnson 1990), A j. does not exhaust the dynamic possibilities of the inter- IMMATURE KELP FOREST action between macrophytes and sea urchins in Strongylocentrotus droebachiensls present Northern Norway. (>f- Echinomermella matsi prevalent The possibility of cyclical sea urchin-mediated Laminana hyperborea dominant changes in community structure has been discussed by Sparse associated flora & fauna earlier authors (Mann 1977, Scheibling 1984), but all previously known transitions between barren ground and kelp forest have been irregular occurrences with- out any detectable periodicity (reviews by Harrold &
UNDISTURBED KELP FOREST Pearse 1987, Chapman & Johnson 1990). The situation Strongylocentrotus droebachiensis scarce or absent in Northern Norway differs by providing a macro- Echinomermella matsi unknown parasitic disease agent as a theoretically plausible Laminaria hyperborea dominant mechanism for sustaining future alternations (cf. May Abundant associated flora 8 fauna & Anderson 1979, May 1983). A tentative etimate for the period of future alternations is provided by the Fig. 6. Strongylocentrotus droebachlensis, Echinomermella approximately decade long interval from the initial matsi and Laminarla hyperborea. Scenario based on observed sea urchin outbreak dynamics at Vzray Island, Northern kelp forest destruction until the recurrence of destruc- Norway: a barren ground configuration is established after tive grazing. the initial destruction of the undisturbed kelp forest. Sub- Local events at Vter~yIsland are part of a large-scale sequent kelp recovery is followed by recurrent destructive outbreak phenomenon which started in the late 1970s grazing which prematurely Interrupts the succession towards and involves much of the Norwegian coastline be- a mature, undisturbed kelp forest, and the ecosystem enters a cyclical domain which precludes proper termination of the tween 64 and 69" N (Sivertsen 1982, Hagen 1983). outbreak Signs of local scale macroalgae recovery elsewhere in 104 marEcol Prog Ser
the outbreak area (Skadsheim et al. 1994) may there- Dayton PK, Currie V, Gerrodette T, Keller BD, Rosenthal R, fore mark the beginning of new waves of kelp forest Tresca DV (1984) Patch dynamics and stablllty of some destruction, rather than marking the end of the out- California kelp commun~tles.Ecol Monogr 54-253-289 Dayton PK, Tegner MJ, Parnell PE, Edwards PB (1992) Tem- break. On a larger scale these events may be an indi- poral and spatial patterns of disturbance and recovery in a cation that the euphotic hard-bottom component of the kelp forest community. Ecol Monogr 62(3):421-445 coastal ecosystem has entered a cyclical domain where Dexter RW (1944) The bottom community at Ipswich Bay, barren ground alternates with immature kelp forest in Massachusetts. Ecology 25:352-359 Diiben v (1847) Om de norske Echinider. In: Anonymous (ed) a hitherto unrecognized manner. Forhandlinger ved de skandinaviske naturforskeres fjerde mode i Christianla den 11-18 Juli 1844. Grondahl, Chris- tiania, p 250-255 (in Norwegian) Acknowledgements. I thank 0.A. Schlstad for SCUBA lving Duggins DO (1980) Kelp beds and sea otters. an experimental assistance, P. Torrissen for the safe operation of RV 'Raud', approach. Ecology 61:447-453 and H. H. Ludvigsen for assistance in the laboratory. Thanks Duggins D0(1981) Sea urchins and kelp: the effects of short also go to H. K. Marshall for improving the linguistic content term changes in urchin diet. Lirnnol Oceanogr 26: of the manuscript, to G. M. Jones and J. M. Watanabe for 391-394 commenting on an earlier draft, and to 3 anonymous referees Ebeling AW, Laur DR, Rowley RJ (1985) Severe storm distur- for valuable criticism. My employer, Bod~College, Norway, bances and reversal of community structure in a southern generously provided technical assistance and laboratory California kelp forest. 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This article was submitted to the editor Manuscript first rece~ved:October 11, 1994 Revised version accepted: February 21, 1995