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Effects of experimental overgrowth on survival and change in the turf assemblage of a giant kelp forest
J. Exp. Mar. Biol. Ecol., 1990, Vol. 135, pp. 229-242
229
Elsevier
JEMBE 01377
Effects of experimental overgrowth on survival and change in the turf assemblage of a giant kelp forest A. Keith Miles * and E. Charles Meslow* ‘US Fish and Wildli$eService, Patuxent Wildlt&eResearch Center, Laurel, Maryland, USA: 2US Fish and Wildlife Service, Oregon Cooperative Wild&e Research Unit. Cowallis. Oregon, USA
(Received 9 March 1989; revision received 2 October 1989; accepted 30 November 1989) Abstract: Crustose coralline algae were the prevalent cover among sessile organisms that paved or grew near the substratum, and also the most commonly overgrown species in a giant kelp Macrocystis pyn$ra (L.) C.A. Agardh forest located off San Nicolas Island, California. Giant kelp was the largest and most conspicuous species that overgrew large patches of the substrata; overgrowth among turf organisms also appeared common. To determine the effects of giant kelp holdfasts on crustose coralline algae and other turf organisms, “artificial holdfasts” were placed on 0.125-m2 plots for 5, 8 and 12 months. In these treatments, 50-57x of the crustose coralline algae survived. Because these algae also recruited while covered, the total cover (survivorship plus recruitment) differed by only 7-26% from that sampled at the start of the study. The decline of these algae in control plots was similar to that in the treatment plots mostly because ofovergrowth by sessile invertebrates. Bryozoans increased markedly on the control plots, whereas O-12% survived in the treatment plots. Bryozoans and sponges also recruited under the artificial holdfasts. Some arborescent turf algae survived in the 5- and g-month treatments; articulated coralline algae survived better than did foliose algae. High survival recruitment of crustose coralline algae while overgrown contributed to their prevalence in benthic communities.
Key words: Competition; Giant kelp; Overgrowth; Survival; Turf
INTRODUCTION
Sessile marine organisms commonly compete by overgrowth (Buss&Jackson, 1979). Physical smothering is probably the most familiar of several different forms (e.g., ahelopathy and shading) of direct interference competition that have been grouped into overgrowth (Rutzler, 1970; Dayton, 1971; Stebbing, 1973; Jackson & Buss, 1975; Connell, 1976; Karlson, 1978; Woodin & Jackson, 1979; Russ, 1982; Dayton et al., 1984; Stimson, 1985; Sebens, 1986). Many patterns of overgrowth follow hierarchies of dominant species that consistently overgrow subordinate species (Connell, 1961; Dayton, 197 1; Paine, 1974; Menge, 1976; Osman, 1977; Quinn, 1982; Sebens, 1986). Subordinate species may persist by opportunistic and rapid recruitment, rapid growth, or wide dispersal of propagules Correspondence address: A. K. Miles, US Fish and Wildlife Service, Patuxent Wildlife Research Center, Laurel, MD 20708, USA. This is Oregon Agricultural Experiment Station Technical Paper 8818. 0022-0981/90/$03.50 0 1990 Elsevier Science Publishers B.V. (Biomedical Division)
2.K. MILES AND I+(
230
(Connell
& Slatyer,
1977). These
predators that are temporally species (Menge & Lubchenco, moderate
species
may also survive
by using
refuges
from
or spatially more accessible to them than to dominant 1981; Witman, 1985). Smaller species may better resist
levels of physical or biotic disturbances
parts (Connell,
MESLOU
1971; Lubchenco,
than their larger, dominant
1978; Lubchenco
& Menge,
Cubit, 1980; Hay, 1981; Menge, 1983; Dayton et al., 1984). In the competitive hierarchies of some rocky marine communities,
counter-
1978; Lubchenco
&
large, fast-growing
arborescent algae tend to be the better competitors, followed by thick, fast-growing sessile invertebrates, and then by thicker, slow-growing sessile invertebrates (Dayton, 1975; Buss, 1980; Quinn, 1982; Russ, 1982). Thin, encrusting organisms are commonly the more subordinate species in these hierarchies (Sebens, 1986). Overgrowth interactions among thin, encrusting organisms are often complex and can involve competitive networks, loops, or reversals (Buss &Jackson, 1979; Jackson, 1979: Russ, 1982). Competition theory assumes that subordinate species are killed, damaged or inhibited developmentally by dominant species (Birch, 1957). Overgrowth by direct, physical smothering is a process that supports this assumption. Some sponges and crustose coralline algae can survive overgrowth, but how long they survive or the effects of overgrowth on their development or recruitment are not well-known (Rutzler, 1970; Sara, 1970; Kay & Keough, 1981; Sebens, 1986). Thin, smooth, crustose coralline algae (Rhodophyta, Corallinaceae) were the predominant primary cover in the turf assemblage of a giant kelp h4ucrocysti.s pyrifera 1.. C. A. Agardh forest studied from 1980 to 1984 off San Nicolas Island, California (Miles, 1987). The turf assemblage was identified as sessile organisms that paved the substratum (primary cover) or grew to no > 40 cm high in the adult form (secondary cover). At one sampling bout, the mean cover of crustose coralline algae in 16 random 0.25m2 plots was 17.4”,, (SII r-75.4; Miles, unpubl. data). However, after we scoured the uppermost layer of these plots, the mean cover of these algae was 3 1.9”,, (sn = 7.1 j. This additional cover was found under sessile invertebrates, arborescent algae, or sand that collected in the pitted sandstone substratum. Other observations indicated that the spread of giant kelp holdfasts was an obvious form of overgrowth on the turf assemblage. Entire giant kelp plants were often dislodged by storm-generated
oceanic turbulence.
The large patches resulting from the loss of giant
kelp holdfasts were nearly bare sandstone or contained some calcified remains and crustose coralline algae. It was unclear whether these algae had survived long periods under the holdfasts, survived only around the peripheral of the holdfasts or rapidly colonized the patches after the holdfasts were dislodged. In this study we used artificial holdfasts to investigate the effects of overgrowth of different time intervals on turf species, particularly crustose coralline algae. We also examined changes in cover of these species after experimental coverage was terminated. Our objective was to determine whether the prevalence of crustose coralline algae in the turf assemblage was due to their ability to survive overgrowth or to their ability to rapidly colonize the bare sandstone or calcified remains found after giant kelp holdfasts were detached.
SURVIVALOFKELPFOREST
231
METHODS
We used scuba to conduct observations and experiments in the kelp forest described above. To provide an index of the quantity of turf assemblage affected by giant kelp holdfasts, we counted and tagged giant kelp within a 10 m x 10 m site of the kelp forest at haphazard intervals from 1980 to 1984. Five times during this period we measured the diameter of 50 giant kelp holdfasts selected at random each time (in July 1980, only 10 plants were measured). An estimate of substrata affected by holdfast overgrowth was calculated by multiplying the mean area covered by the 50 holdfasts by the number of plants on the site, divided by the area of the site. In December 1983 we established 35 plots along a line parallel to shore. The plots were established on either side of the line on similar, flat substratum, i.e., we avoided crevices or boulders. The plots were at depths of 9-10 m and were a random number of swim-kicks (2-6) apart. Threaded brass rods were epoxied into holes drilled into the corners of each plot. We sampled permanent points within a 0.125-m2 (35.35 cm x 35.35 cm) area of the plots with a grid that lit exactly over the brass rods. The grid had 49 crosshairs, and we identified and tabulated species found under the crosshairs. Using this sampling method, we could observe changes in abundance and distribution of turf species at the permanent points. Sand > 2 cm deep in the pitted sandstone was not disturbed for any identification of what was beneath it. After the 35 plots were sampled, live were randomly selected as controls, and “artificial holdfast” plates were placed on 26 plots (four were excluded because of damaged or missing brass rods). The plates consisted of a 42 cm x 42 cm x 5-cm reinforced, rigid, foam rubber pad, backed by a 43 cm x 43-cm galvanized steel sheet. The plates fit over the threaded rods and were firmly bolted down on the plots. The plates were similar to giant kelp holdfasts in applying physical pressure, blocking out light, and molding (via the foam pad) to the contour of the substrata. However, unlike the plates, real holdfasts could intertwine and adhere to the substrata. In 1984, we removed 10 randomly selected plates at 5 months (May) and sampled those plots in May, August and December. 10 more were removed at 8 months (August) and the plots sampled in August and December. The final six plates were removed and the plots sampled at 12 months (December). Several assumptions, based on observations and on other studies of overgrowth, were made when sampling. An organism replaced by bare space or calcified, disintegrating remains was assumed to have died. Organisms were recruits if they appeared at points that were formerly bare, contained calcified remains or other organisms; the term recruitment included both vegetatively spreading and colonization by spores or larvae to new points. An organism replaced by a thicker organism at a later sampling interval was presumed to be overgrown; if replaced by a thinner organism, it was presumed to have died and was identified as replaced. An organism, identiIied at a point that was later covered by sand or another organism, which then reappeared at that point was presumed to have survived coverage.
Organisms were identified in situ to species or to the lowest possible taxon, and then grouped into higher taxonomic units for comparisons. Mean percent cover was calculated by dividing the count of a species . plot ’ by 49 and averaging that value by the number of plots for a given treatment. Two categories of species cover are identified in the results: (1) the surviving cover remaining from the cover sampled at permanent points at the start of the study, and (2) the total cover, which was the surviving cover plus new cover (e.g., recruitment) sampled at other permanent points. We used ANOVA and t tests to analyse differences between treatments and controls. Where required, data were normalized using the arcsine transformation (Steel & Torrie, 1980). RESULX We observed high loss and recruitment of giant kelp in the 10 x 10-m site from 1980 through 1984. Of tagged or known plants, 76.7 “/, were lost between October 1980 and March 1981,41.6% between December 1981 and March 1982, and 40.8’4 between January and March 1983. Counts of all giant kelp found in the site at different times are given in Fig. 1. Giant kelp were dislodged by turbulent water motion that resulted mostly from winter storms as well as summer swell. Also, low illumination at the bottom appeared to reduce survival of some giant kelp recruits (visible, new plants), particularly when these recruits had not reached the surface by the time a dense surface canopy formed over the site. We observed this between October and December 1981 and August and November 1983 (Fig. 1). Seasonally reduced daylength probably added to reduced illumination within the kelp forest during the latter half of these time periods. At the same time substrata were affected by giant kelp loss, additional substrata were affected by plants that survived and new recruits in the site (Fig. 1). Giant kelp recruits were found throughout the site and on all kinds of substrata, including attached to
Macrocyu
jul act
msroct dcc
. mar dec
1980
81
82
Ry_rifera
jsnmarjulsugnov 83
may sup 04
Fig. 1. Number of giant kelp and percent of substrata covered by these kelp periodically from 1980 to 1984
within a 10 x 10-m site adjacent to study plots.
SURVIVAL
OF KELP FOREST
233
arborescent turf algae. When measured, giant kelp holdfasts covered x 6-12% of the site (Fig. 1). The area covered by giant kelp did not relate directly to the number of plants on the site because a few large plants could cover an area which could support many smaller ones. Oceanic conditions were unusually calm around San Nicolas Island between December 1983 and May 1984. This period was characterized by a thick surface canopy, no giant kelp recruits found on the study area, sloughing of arborescent turf algal fronds, and a substantial increase in sessile invertebrates. We did not observe any of these events from January to May in the four previous years. Percent cover of crustose coralline algae in all plots was similar at the start of the study (df = 3,27; F = 0.14; P = 0.94) (Fig. 2). x l/z (50-57.2%) ofthese algae survived, regardless of treatment, and survival did not differ significantly between the treatments (df = 2,23; F = 0.05; P = 0.95) (Fig. 2b-d). Crustose coralline algae apparently propagated to other permanent points under the artificial holdfasts, and some probably survived under dominant species that died from or during treatment. Total cover (survivorship plus recruitment) of these algae differed by only 7.3-25.9% from that sampled in the treatment plots at the start of the study. Because of recruitment, the 12-month treatment had the least change in total cover at treatment termination (Fig. 2d); this recruitment was significantly higher than that in the g-month treatment (df = 2, 23; F = 3.42; P = 0.05; Fisher’s PLSD). Mortality accounted for the greatest loss of crustose coralline algae in the treatment plots and increased with duration of the treatments (Fig. 2b-d). Mortality of these algae in the control plots was low except between December 1983 and May 1984 (Fig. 2a). Intact crustose coralline algae found after treatments were ended, particularly those remaining from the original cover, were lighter in color than those in the control plots. Several days after we terminated the 5- and 8-month treatments, the return of darker coloration indicated that some of these algae probably were still viable. In four of six cases (surviving cover and total cover), crustose coralline algal cover was similar between the treatments and the controls at the time of treatment termination [df = 13 (5, 8 months) and 9 (12 months), t = 0.05; Fig. 2b-d]. A biological explanation was not apparent for the two exceptions. Crustose coralline algal cover decreased in the control plots mainly because of overgrowth by sessile invertebrates (Fig. 2a). In subsequent sampling of the control plots, increases in this algal cover occurred mostly at points where these algae probably had survived overgrowth. In the months following the termination of treatments, total crustose coralline algal cover increased in the treatment plots primarily because of new recruitment (Fig. 2b,c). Ample bare and calcified substrata were available for colonizing turf organisms after the artificial holdfasts were removed, although sessile invertebrates also overgrew cmstose coralline algae during this time. As much as 12.6% of the increase in crustose coralline algal cover was probably algae that survived under sand that had accumulated under the artificial holdfasts and dissipated after they were removed (Fig. 2b,c). We observed a similar accumulation of sand under giant kelp holdfasts. Sand accounted for ~4.4% of the change in cover of these algae in the control plots.
percentcover II
tata
cover
r> surviving percent
cover gained
arecruited to new permanent point pilpreviousfy covered by organism, or 0 by sand percent a morta!it calcifie
60
lost (bare or
d” remains)
covered or replsced by orgsntsm, or tfby sand .-
40 20 0
-20 40
lou 80 60 4cJ
20 0 -20 1Z-month
Dee 83
treatment
flay84
-40
(n =
Aug 84
Dee 84
l-40
Fig. 2. Surviving and total mean percent coyer of crustose coralline algae at permrtnent points in treatmeflt and control p&s. Percent change, percent increase or decrease from one sampling interval to next. N, number of plots *treatment I”‘. Bars, -f-1 SE.
Colonial, encrusting bryozoans (primarily A&mbran@~m sp. nnd Puvasmirtinrr sp., suborder Cheilostomata) most commonly overgrew crustose coralline algae. At the start of the study, bryozoan cover was lower in the control plots than that in the treatment plots (Fig. 3). This trend was reversed after treatment. Bryozoan cover was significantly lower in the treament plats than that in the cuntro1 plots at treatme& termination [df = 13 (5,8 months) and 9 (12 months), t = &OS]. Mortality increased with duration
SURVIVAL OF KELP FOREST Encrusting
Bryozoans
235 percentcover lltotalcover *Isurviving cover
percent
gained
recruitedto new Hpermanentpoint previously covered by orgsnlsm, or 0 by sand
q
percent lost (b) 5-month treatment
1 mortslit (bare or
(n = 10)
calcilieP remains) covered orreplacet by organism,or
Oby
12-monthtreatmentln
sand
= 6) 80 60 40 20 0 -20 -40 -60
Dee 83
Ray 84
Aug 84
Dee
-80
Fig. 3. Surviving and total mean percent cover of encrusting bryozoans at permanent points in the treatment and control plots. Percent change, percent increase or decrease from one sampling interval to next. N, number of plots. treatment - ‘. Bars, + 1 SE.
of artificial holdfast placement and was probably greater than inferred in Fig. 3: l/4 (25.0%) to z l/2 (55.6%) of the bryozoans lost were replaced by crustose coralline algae. These algae either recruited to points formerly occupied by bryozoans or survived underneath bryozoans that died during treatment. The total cover of bryozoans at treatment termination was greater than the surviving cover, indicating that bryozoans had recruited under the artificial holdfasts (Fig. 3b-d). Bryozoans recruited into pockets in the substratum and did not survive direct contact with the artificial holdfasts.
In the control plots, encrusting
bryozoans
cover by May 1984 (Fig. 3a); 2/3 (66.7?,, stratum, calcified remains
occurred
algae. The remaining
and a fleshy crustose
at certain
from 4.1 to 14.7”,, mean total
j of this recruitment
and crustose coralline
grew other sessile invertebrates area. While they increased
increased
red alga uncommon
points in the control
on bare sub-
bryozoans
over-
on the study
plots from December
19X3
through August 1984, encrusting bryozoans were also overgrown (primarily by different bryozoan species), or replaced by crustose coralline algae or bare substratum at other points (Fig. 3a). Encrusting bryozoans did not appear to survive overgrowth by other sessile organisms. Sand covered a large proportion of known encrusting bryozoans at the end of the 5-month treatment (Fig. 3b). After the sand dissipated, the re-occurrence of bryozoans at permanent points 3 months later indicated that some bryozoans may have survived under that sand. However, it is also possible that the original occupants died and were replaced by new conspecific recruits. Encrusting bryozoans recruited rapidly following treatment termination (Fig. 3b,c). Similar to the control plots, > l/3 (38,59,,) to > l/2 (5 1.4”,, ) of these bryozoans overgrew crustose coralline algae. Sponges and tunicates comprised little cover in both the treatment and control plots. Nearly half of the sponge cover sampled in December 1983 (Fig. 4a) survived in the S(43.9”;)) and g-month (43.3%) treatments and < 1:‘lO (6.7%) survived the 12-month treatment. However, because of recruitment, total sponge cover in the 5-month treatment was greater than that sampled at the start of the study, changed little in the &month treatment, and declined by < l/2 (46.7%) in the 12-month treatment (Fig. 4a). Total sponge cover changed little in the control plots. Sponges survived and recruited in pockets in the substratum and appeared in good condition at treatment termination. As with bryozoans, sponges died primarily at contact points with the artificial holdfasts. Tunicates comprised < 5?$ cover on any of the plots. A small percentage of these survived and recruited in the 5-month treatment,
but none survived the 8- and 12-month
treatments. Most other sessile organisms that formed primary cover were uncommon, except for the vermetid tube snail Serpulorbis sp., and holdfasts of arborescent turf algae (Fig. 4b,c). The actual cover and effects of treatments on Serpulorbis were difficult to assess. Many organisms overgrew the extensive shell of Serpulorbis, which appeared to have no effect on the snail. The shells were bleached white or disintegrated at contact points with the artificial holdfasts, particularly in the 12-month treatment, but the snail was often alive. The snail could occupy a small portion of its shell and survive. Serpulorbis recruits were also found in the treatment plots. In the control plots, changes in overgrowing organisms often accounted for changes in Serpulorbis, i.e., whether it was visible to be sampled or not. The cover of arborescent turf algal holdfasts declined slightly in the 5-month treatment, and substantially in the 8- and 12-month treatments (Fig. 4~). The holdfasts sampled at treatment termination were mostly pale-colored, articulated coralline algae. After the 5- and 8-month treatments were terminated, color returned to these holdfasts
SURVIVAL OF KELP FOREST Primary 12 ..
encrusting
(*)
Cover
Secondary (d)
sponges
8 ‘.
60..
6 ..
70.. f 60..
+
4 a’ tf z *
(b) k
16 ..
> 8
14.. 12..
2
10..
8
0 *.
b Q
6 4”
all
Cover
arborescent
algae
90..
10 ‘.
2”. 0.F
231
t
*
*
50 ..
0
:
40 ..
Serpulorbis
30 ..
sp.
t
2 ..
t If+
20 .. 10 ‘.
i 4 I
o.(e)
articulated corallfne algae *
l
30 .’ 20..
+
10..
+
0.
. (1)
foliose
red
algae
40 .’
Dee
83
nay
Aug
-
84 -
Dee Dee
nay -
Aug
Dee
84 -
Fig. 4. Total mean percent cover of other common organisms or groups of organisms that formed primary or secondary cover at permanent points in treatment and control plots. Bars, + 1 SE. *, significant difference in cover between treatment and control at time of treatment termination [df = 13 (5, 8 months) or 9 (12 months), t = 0.051.
indicating that these plants probably were still viable. The cover of the turf algal holdfasts declined in the control plots from December 1983 to May 1984 (Fig. 4~); sessile invertebrates overgrew !z 2/3 (60.0%) of these and the remainder were dead. By August and December 1984, holdfast cover increased either because of recruitment, or re-exposure at points of overgrowth, indicating that short-term overgrowth was probably not harmful to the holdfasts. Some secondary cover (thalli and fronds) of arborescent turf algae was found at
treatment
termination
and appeared
viable (Fig. 4d). Most of this cover was articulated
coralline algae, particularly Calliurthmn sp.. which was the most common ofthese algae. Of the articulated coralline algal cover sampled in December 1983, z 1 3 (30.3”,. 1 survived the j-month
treatment,
survived the 12-month treatment termination of the 5- and g-month
z l/4 (24.5”,,) the X-month treatment, and little (2.5”,, ,I (Fig. 4e). The initial increase in these algae after treatments was mainly due to regeneration of plants
identified in December 1983, but new individual plants were also found. < l/l0 (9.0”;,) of the secondary cover of foliose red algae survived the 5-month treatment, little (< 17;) survived the 8-month treatment, and none survived the 12-month treatment (Fig. 4f). Stolons of Rho@menia sp., which was the most common of these algae, and deteriorated remnants of Gefidium sp. were found in the treatment plots. After the artificial holdfasts were removed, much of the initial foliose red algae regenerated or recruited at or near these stolons and remnants. Secondary algal cover declined in the control plots between the start of the study and May 1984 and did not differ significantly from the effects of the 5-month treatment (Fig. 4d). The timing of this decline coincided with the period of a dense giant kelp canopy mentioned above. In August and December 1984 the surface canopy was thinner than previously observed, and algal cover had increased in the control plots. This cover was significantly greater than that found in plots at the termination of the 8- and 12-month treatments (Fig. 4d).
DISCUSSION
Crustose
coralline
algae, while competitively
subordinate,
cover on rocky substratum in many marine communities 1975; Steneck, 1982, 1983). The prevalence of these
often form the dominant
(Adey, 1969; Adey & Vassar, algae has been attributed to
resistance to biotic and physical disturbances (Bakus, 1966; Paine & Vadas, 1969; Adey & Vassar, 1975; Lawrence, 1975; Vadas, 1977; Menge & Lubchenco, 1981; Steneck, 1983). Herbivores
that feed on overgrowing
arborescent
algae may also facilitate
the
survival of crustose coralline algae (Paine & Vadas, 1969; Adey & Macintyre, 1973; Steneck, 1983). Crustose coralline algae may have yet additional mechanisms for survival and dominance in marine systems where overgrowth by sessile organisms is common. Sebens (1986) reported that crustose coralline algae could survive overgrowth by dominant turf organisms for several months. In our study, these algae not only survived but recruited under simulated overgrowth for periods up to 12 months. These algae also probably survived underneath other organisms that were killed by the artificial holdfasts. Viable crustose coralline algae were found under large giant kelp holdfasts (Miles, 1987), most of which were z 40-50 cm in diameter, indicating that the giant kelp may have been several years old (Dayton et al., 1984). However, we have observed that many kelp recruits could grow together and form a large holdfast in < 1 yr. Crustose coralline algae
SURVIVAL
OF KELP FOREST
239
probably acquired photosynthetic products under the artificial holdfasts by lateral translocation through the thaIli from connecting crusts that were exposed to light (Wetherbee, 1979). R. Steneck (pers. comm., unpubl. data) suggested that lateral translocation is characteristic of thin-layer crustose corahine algae such as that found on the study area. After treatment termination, crustose coralline algal recruitment was probably enhanced by available bare or calcified substratum or by algae that had survived under organisms that died during treatment. Crustose coralline algae occupied available substrata rapidly relative to other sessile, turf organisms. Low recruitment and decrease of crustose coralline algal cover in the control plots indicated that these algae probably competed for space with sessile invertebrates. Calm oceanic conditions and a dense surface kelp canopy during the first half of the study appeared to facilitate sessile invertebrates (see also Rosenthal et al., 1974). The similarity in changes in crustose coralline algal cover in treatment and control plots indicated that the effects of overgrowth by sessile invertebrates and giant kelp holdfasts could be similar. However, the negative effects that dominant organisms might have on crustose coralline algae are probably offset by survival and recruitment of these algae during overgrowth; this is augmented by the more severe effects that giant kelp holdfasts apparently can have on the dominant organisms. Under treatment, arborescent algae revealed survival capabilities that may exist under normal conditions of shading and overgrowth. Turf algae found within established kelp forests probably endure extended periods of low illumination, with occasional periods of greater illumination associated with disturbance and loss of the kelp canopy. Similar capabilities have been suggested for algae exposed to periodically severe herbivory (Lubchenco & Gaines, 1981). In our study, the physical force or pressure exerted by overgrowth, as simulated by the artificial holdfasts, was not enough to kill all arborescent algae by 8 months. These findings indicate that these algae (and other sessile organisms) probably can endure relatively long periods of overgrowth and survive if they are not dislodged with giant kelp holdfasts during turbulent conditions. The dynamics of the turf assemblage were evident from changes observed in the control plots that affected the distribution of organisms at permanent points but not necessarily the overall abundance of those organisms. Mortality and overgrowth by other turf organisms were balanced with recruitment and survival of overgrowth, resulting in relatively constant cover. This relative constancy in species abundance in the control plots was in marked contrast to the pervasive effects of giant kelp overgrowth. Although the estimated area overgrown by giant kelp holdfasts was not large at any time period, this measure was augmented by the loss of giant kelp. In addition, dislodged giant kelp entangle other giant kelp and in turn cause their dislodgement (Rosenthal et al., 1974; Dayton et al., 1984). We observed that the resulting mass of holdfasts often scoured the substrata and further damaged the turf assemblage. If all of these events are taken into account, the actual area affected by giant kelp holdfasts could be calculated over a given time interval. These events in addition to kelp recruitment were continual processes related to the wave-swept exposure and surge of the open,
\.K. MILES AND F..( I\,lESI.OW
7Jii
unprotected
coastline
of San Nicolas Island (see also Dayton
et al., 1984). The rate a~
which the loss of giant kelp impacted the turf assemblage appeared to be dependent on the severity of winter storms and summer oceanic swell. The rate of impact by kelp recruitment illumination
appeared
dependent
at the bottom,
Previous investigations
on the condition
of the surface canopy and subsequent
and on the growth rate of kelp holdfasts. of this San Nicolas Island kelp forest indicated
that changes
in cover of turf organisms were affected substantially by illumination (Miles, 1987). Caging experiments showed that herbivores can affect the abundance and distribution of foliose algae (Miles. 1987). A consistent result of these studies was that crustose coralline algae persisted as the most abundant cover of the turf assemblage. In the present study, we simulated the effects of giant kelp overgrowth and demonstrated that certain turf organisms have adapted strategies for survival. Foremost among these organisms were crustose coralline algae. The effects of giant kelp that inhibited or killed most other organisms in fact contributed to the prevalence of these algae.
ACKNOWLEDGEMENTS
We thank K. Collins, the US Navy and personnel of San Nicolas Island, A. H. Hines, K. Cook, J. Estes, J. Lubchenco, R. Anthony and the anonymous reviewers of this journal. This study was supported by the Cooperative Research Units Center of the US Fish and Wildlife Service.
REFERENCES Adey, W. H., 1969. Investigations on the crustose corallines of the North Atlantic Ocean. Nati. Geogr. SOC. Res. Rep., Vol. 1964, pp. l-4. Adey, W. H. & I. G. Macintyre, 1973. Crustose coralline algae: a re-evaluation in the geological sciences, Geol. Sot. Am. Bull., Vol. 84, pp. 883-904. Adey, W. H. & J. M. Vassar, 1975. Colonization, succession and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologiu, Vol. 14, pp. 55-69. Bakus, G.J., 1966. Some relationships of fishes to benthic organisms on coral reefs. Nature (London). Vol. 210, pp. 280-284. Birch, L.C., 1957. The meanings of competition. Am. Nat., Vol. 91, pp. 5-18. Buss, L. W., 1980. Competitive intransitivity and size-frequency distributions of interacting populations. Proc. Natl. Acad. Sk., Vol. 77, pp. 5355-5359. Buss, L.W. & J.B.C. Jackson, 1979. Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat., Vol. 113, pp. 223-234. Connell, J. H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle, Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. Connell, J.H., 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rainforest trees. In, Dynamics of populations, edited by P. J. den Boer & G. R. Gradwell, Center for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp. 298-312. Connell, J. H., 1976. Competitive interactions and the species diversity of corals. In Coefenferute ecology and behavior, edited by G.P. Mackie, Plenum Press, New York, New York, pp. 51-58.
SURVIVAL OF KELP FOREST
241
Connell, J.H. & R.O. Slatyer, 1977. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Nut., Vol. 111, pp. 1119-l 144. Dayton, P. K., 1971. Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 351-389. Dayton, P. K., 1975. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol. Monogr., Vol. 45, pp. 137-159. Dayton, P. K., V. Currie, T. Gerrodette, B.D. Keller, R. Rosenthal & D.V. Tresca, 1984. Patch dynamics and stability of some California kelp communities. Ecol. Monogr., Vol. 54, pp. 253-289. Hay, M. E., 1981. The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology, Vol. 62, pp. 739-750. Jackson, J. B. C., 1979. Overgrowth competition between encrusting cheilostome ectoprocts in a Jamaican cryptic reef environment. J. Anbn. Ecol., Vol. 48, pp. 805-823. Jackson, J. B. C. & L. Buss, 1975. Allelopathy and spatial competition among coral reef invertebrates, Proc. N&l. Acad. Sci., Vol. 72, pp. 5160-5163. Karlson, R., 1978. Predation and space utilization patterns in a marine epifaunal community. J. Exp. Mar. Biol. Ecol., Vol. 31, pp. 225-239. Kay, A.M. & M. J. Keough, 1981. Occupation of patches in the epifaunal communities on pier pilings and the bivalve Pinnu bicolor at Edithburgh, South Australia. Oecologiu (Berlin), Vol. 48, pp. 123-130. Lawrence, J.M., 1975. On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol. Anna Rev., Vol. 13, pp. 213-286. Lubchenco, J., 1978. Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am. Nut., Vol. 112, pp. 23-39. Lubchenco, J. & J. Cubit, 1980. Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology, Vol. 61, pp. 676-687. Lubchenco, J. & S. D. Gaines, 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu. Rev. Ecol. Syst., Vol. 12, pp. 405-437. Lubchenco, J. 8c B.A. Menge, 1978. Community development and persistence in a low rocky intertidal zone. Ecol. Monogr., Vol. 48, pp. 67-94. Menge, B., 1976. Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol. Monogr., Vol. 5 1, pp. 429-450. Menge, B., 1983. Components of predation intensity in the low zone of the New England rocky intertidal region. Oecologia (Berlin), Vol. 58, pp. 141-155. Menge, B. & J. Lubchenco, 1981. Community organization in temperate and tropical rocky intertidal habitats: prey refuges in relation to consumer pressure gradients. Ecol. Monogr., Vol. 51, pp. 429-450. Miles, A. K., 1987. Turf assemblage of a Mucrocystis kelp forest: experiments on competition and herbivory. Ph.D. thesis, Oregon State University, Corvallis, Oregon, 136 pp. Osman, R. W., 1977. The establishment and development of a marine epifaunal community. Ecol. Monogr., Vol. 47, pp. 37-63. Paine, R.T., 1974. Intertidal community structure. Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia (Berlin), Vol. 15, pp. 93-120. Paine, R. T. & R. L. Vadas, 1969. The effects of grazing by sea urchins, SnongVlocentTotusspp., on benthic algal populations. Limnol. Oceunogr., Vol. 14, pp. 710-719. Quinn, J.F., 1982. Competitive hierarchies in marine benthic communities. Oecologtu (Berlin), Vol. 54, pp. 129-135. Rosenthal, R. J., W. D. Clarke & P. K. Dayton, 1974. Ecology and natural history of a stand of giant kelp, Macrocystis pyrifera, off Del Mar, California. U.S.N.M.F.S. Fish. Bull., Vol. 72, pp. 670-684. Russ, G. R., 1982. Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologta (Berlin), Vol. 53, pp. 12-19. Rutzler, K., 1970. Spatial competition among Porifera: solution by epizoism. Oecologia (Berlin), Vol. 5, pp. 85-95. Sara, M., 1970. Competition and cooperation in sponge populations. In, The biology of Pon@a, edited by W. G. Fry, Symp. Zool. Sot. London, Vol. 25, pp. 273-284. Sebens, K. P., 1986. Spatial relationships among encrusting marine organisms in the New England subtidal zone. Ecol. Monogr., Vol. 56, pp. 73-96. Stebbing, A. R. D., 1973. Observations on colony overgrowth and spatial competition. In, Living andfossil Bryozoa. Recent advances in research, edited by G. P. Larwood, Academic Press, New York, New York, pp. 173-183.
Steel. R G. D. 6t J. H. Torrie. 1980. Principles undprocedures ofslatisrics: a biometricalapproach. Mctiraw-HIII. New York, New York, second edition, 633 pp. Steneck, R. S., 1982. A limpet-coralline alga association: adaptations and defenses between a selectrvc herbivore and its prey. &o&r, Vol. 63, pp. 507-522. Steneck, R. S., 1983. Escalating herbivory and resulting adaptive trends in calcareous algal crusts. I’&/>hi0k~g.v.Vol. 9. pp. 44-6 I. Stimson, J.. 1985. The effect ofshadingby the table coral Acropora hyacinthus on understory corals. Ecol~~v. 1.01 66. pp, 40-53. Vadas, R. L.. 1977. Preferential feeding: an optimization strategy in sea urchins. Em/. Monogr., Vol. 47, pp. 137-371 Wetherbee, R., 1979. “Transfer connections”: specialized pathways for nutrient translocation in a red alga? Science. Vol. 204, pp. 858-859. Witman, J.D., 1985. Refuges, biological disturbance, and rocky subtidal community structure in New England. Ecol. Monogr., Vol. 55, pp. 421-445. Woodin, S. A. L J. B. C. Jackson, 1979. Interphyletic competition among marine benthos. Am. Zool., Vol. 19, pp. 102%1043
229
Elsevier
JEMBE 01377
Effects of experimental overgrowth on survival and change in the turf assemblage of a giant kelp forest A. Keith Miles * and E. Charles Meslow* ‘US Fish and Wildli$eService, Patuxent Wildlt&eResearch Center, Laurel, Maryland, USA: 2US Fish and Wildlife Service, Oregon Cooperative Wild&e Research Unit. Cowallis. Oregon, USA
(Received 9 March 1989; revision received 2 October 1989; accepted 30 November 1989) Abstract: Crustose coralline algae were the prevalent cover among sessile organisms that paved or grew near the substratum, and also the most commonly overgrown species in a giant kelp Macrocystis pyn$ra (L.) C.A. Agardh forest located off San Nicolas Island, California. Giant kelp was the largest and most conspicuous species that overgrew large patches of the substrata; overgrowth among turf organisms also appeared common. To determine the effects of giant kelp holdfasts on crustose coralline algae and other turf organisms, “artificial holdfasts” were placed on 0.125-m2 plots for 5, 8 and 12 months. In these treatments, 50-57x of the crustose coralline algae survived. Because these algae also recruited while covered, the total cover (survivorship plus recruitment) differed by only 7-26% from that sampled at the start of the study. The decline of these algae in control plots was similar to that in the treatment plots mostly because ofovergrowth by sessile invertebrates. Bryozoans increased markedly on the control plots, whereas O-12% survived in the treatment plots. Bryozoans and sponges also recruited under the artificial holdfasts. Some arborescent turf algae survived in the 5- and g-month treatments; articulated coralline algae survived better than did foliose algae. High survival recruitment of crustose coralline algae while overgrown contributed to their prevalence in benthic communities.
Key words: Competition; Giant kelp; Overgrowth; Survival; Turf
INTRODUCTION
Sessile marine organisms commonly compete by overgrowth (Buss&Jackson, 1979). Physical smothering is probably the most familiar of several different forms (e.g., ahelopathy and shading) of direct interference competition that have been grouped into overgrowth (Rutzler, 1970; Dayton, 1971; Stebbing, 1973; Jackson & Buss, 1975; Connell, 1976; Karlson, 1978; Woodin & Jackson, 1979; Russ, 1982; Dayton et al., 1984; Stimson, 1985; Sebens, 1986). Many patterns of overgrowth follow hierarchies of dominant species that consistently overgrow subordinate species (Connell, 1961; Dayton, 197 1; Paine, 1974; Menge, 1976; Osman, 1977; Quinn, 1982; Sebens, 1986). Subordinate species may persist by opportunistic and rapid recruitment, rapid growth, or wide dispersal of propagules Correspondence address: A. K. Miles, US Fish and Wildlife Service, Patuxent Wildlife Research Center, Laurel, MD 20708, USA. This is Oregon Agricultural Experiment Station Technical Paper 8818. 0022-0981/90/$03.50 0 1990 Elsevier Science Publishers B.V. (Biomedical Division)
2.K. MILES AND I+(
230
(Connell
& Slatyer,
1977). These
predators that are temporally species (Menge & Lubchenco, moderate
species
may also survive
by using
refuges
from
or spatially more accessible to them than to dominant 1981; Witman, 1985). Smaller species may better resist
levels of physical or biotic disturbances
parts (Connell,
MESLOU
1971; Lubchenco,
than their larger, dominant
1978; Lubchenco
& Menge,
Cubit, 1980; Hay, 1981; Menge, 1983; Dayton et al., 1984). In the competitive hierarchies of some rocky marine communities,
counter-
1978; Lubchenco
&
large, fast-growing
arborescent algae tend to be the better competitors, followed by thick, fast-growing sessile invertebrates, and then by thicker, slow-growing sessile invertebrates (Dayton, 1975; Buss, 1980; Quinn, 1982; Russ, 1982). Thin, encrusting organisms are commonly the more subordinate species in these hierarchies (Sebens, 1986). Overgrowth interactions among thin, encrusting organisms are often complex and can involve competitive networks, loops, or reversals (Buss &Jackson, 1979; Jackson, 1979: Russ, 1982). Competition theory assumes that subordinate species are killed, damaged or inhibited developmentally by dominant species (Birch, 1957). Overgrowth by direct, physical smothering is a process that supports this assumption. Some sponges and crustose coralline algae can survive overgrowth, but how long they survive or the effects of overgrowth on their development or recruitment are not well-known (Rutzler, 1970; Sara, 1970; Kay & Keough, 1981; Sebens, 1986). Thin, smooth, crustose coralline algae (Rhodophyta, Corallinaceae) were the predominant primary cover in the turf assemblage of a giant kelp h4ucrocysti.s pyrifera 1.. C. A. Agardh forest studied from 1980 to 1984 off San Nicolas Island, California (Miles, 1987). The turf assemblage was identified as sessile organisms that paved the substratum (primary cover) or grew to no > 40 cm high in the adult form (secondary cover). At one sampling bout, the mean cover of crustose coralline algae in 16 random 0.25m2 plots was 17.4”,, (SII r-75.4; Miles, unpubl. data). However, after we scoured the uppermost layer of these plots, the mean cover of these algae was 3 1.9”,, (sn = 7.1 j. This additional cover was found under sessile invertebrates, arborescent algae, or sand that collected in the pitted sandstone substratum. Other observations indicated that the spread of giant kelp holdfasts was an obvious form of overgrowth on the turf assemblage. Entire giant kelp plants were often dislodged by storm-generated
oceanic turbulence.
The large patches resulting from the loss of giant
kelp holdfasts were nearly bare sandstone or contained some calcified remains and crustose coralline algae. It was unclear whether these algae had survived long periods under the holdfasts, survived only around the peripheral of the holdfasts or rapidly colonized the patches after the holdfasts were dislodged. In this study we used artificial holdfasts to investigate the effects of overgrowth of different time intervals on turf species, particularly crustose coralline algae. We also examined changes in cover of these species after experimental coverage was terminated. Our objective was to determine whether the prevalence of crustose coralline algae in the turf assemblage was due to their ability to survive overgrowth or to their ability to rapidly colonize the bare sandstone or calcified remains found after giant kelp holdfasts were detached.
SURVIVALOFKELPFOREST
231
METHODS
We used scuba to conduct observations and experiments in the kelp forest described above. To provide an index of the quantity of turf assemblage affected by giant kelp holdfasts, we counted and tagged giant kelp within a 10 m x 10 m site of the kelp forest at haphazard intervals from 1980 to 1984. Five times during this period we measured the diameter of 50 giant kelp holdfasts selected at random each time (in July 1980, only 10 plants were measured). An estimate of substrata affected by holdfast overgrowth was calculated by multiplying the mean area covered by the 50 holdfasts by the number of plants on the site, divided by the area of the site. In December 1983 we established 35 plots along a line parallel to shore. The plots were established on either side of the line on similar, flat substratum, i.e., we avoided crevices or boulders. The plots were at depths of 9-10 m and were a random number of swim-kicks (2-6) apart. Threaded brass rods were epoxied into holes drilled into the corners of each plot. We sampled permanent points within a 0.125-m2 (35.35 cm x 35.35 cm) area of the plots with a grid that lit exactly over the brass rods. The grid had 49 crosshairs, and we identified and tabulated species found under the crosshairs. Using this sampling method, we could observe changes in abundance and distribution of turf species at the permanent points. Sand > 2 cm deep in the pitted sandstone was not disturbed for any identification of what was beneath it. After the 35 plots were sampled, live were randomly selected as controls, and “artificial holdfast” plates were placed on 26 plots (four were excluded because of damaged or missing brass rods). The plates consisted of a 42 cm x 42 cm x 5-cm reinforced, rigid, foam rubber pad, backed by a 43 cm x 43-cm galvanized steel sheet. The plates fit over the threaded rods and were firmly bolted down on the plots. The plates were similar to giant kelp holdfasts in applying physical pressure, blocking out light, and molding (via the foam pad) to the contour of the substrata. However, unlike the plates, real holdfasts could intertwine and adhere to the substrata. In 1984, we removed 10 randomly selected plates at 5 months (May) and sampled those plots in May, August and December. 10 more were removed at 8 months (August) and the plots sampled in August and December. The final six plates were removed and the plots sampled at 12 months (December). Several assumptions, based on observations and on other studies of overgrowth, were made when sampling. An organism replaced by bare space or calcified, disintegrating remains was assumed to have died. Organisms were recruits if they appeared at points that were formerly bare, contained calcified remains or other organisms; the term recruitment included both vegetatively spreading and colonization by spores or larvae to new points. An organism replaced by a thicker organism at a later sampling interval was presumed to be overgrown; if replaced by a thinner organism, it was presumed to have died and was identified as replaced. An organism, identiIied at a point that was later covered by sand or another organism, which then reappeared at that point was presumed to have survived coverage.
Organisms were identified in situ to species or to the lowest possible taxon, and then grouped into higher taxonomic units for comparisons. Mean percent cover was calculated by dividing the count of a species . plot ’ by 49 and averaging that value by the number of plots for a given treatment. Two categories of species cover are identified in the results: (1) the surviving cover remaining from the cover sampled at permanent points at the start of the study, and (2) the total cover, which was the surviving cover plus new cover (e.g., recruitment) sampled at other permanent points. We used ANOVA and t tests to analyse differences between treatments and controls. Where required, data were normalized using the arcsine transformation (Steel & Torrie, 1980). RESULX We observed high loss and recruitment of giant kelp in the 10 x 10-m site from 1980 through 1984. Of tagged or known plants, 76.7 “/, were lost between October 1980 and March 1981,41.6% between December 1981 and March 1982, and 40.8’4 between January and March 1983. Counts of all giant kelp found in the site at different times are given in Fig. 1. Giant kelp were dislodged by turbulent water motion that resulted mostly from winter storms as well as summer swell. Also, low illumination at the bottom appeared to reduce survival of some giant kelp recruits (visible, new plants), particularly when these recruits had not reached the surface by the time a dense surface canopy formed over the site. We observed this between October and December 1981 and August and November 1983 (Fig. 1). Seasonally reduced daylength probably added to reduced illumination within the kelp forest during the latter half of these time periods. At the same time substrata were affected by giant kelp loss, additional substrata were affected by plants that survived and new recruits in the site (Fig. 1). Giant kelp recruits were found throughout the site and on all kinds of substrata, including attached to
Macrocyu
jul act
msroct dcc
. mar dec
1980
81
82
Ry_rifera
jsnmarjulsugnov 83
may sup 04
Fig. 1. Number of giant kelp and percent of substrata covered by these kelp periodically from 1980 to 1984
within a 10 x 10-m site adjacent to study plots.
SURVIVAL
OF KELP FOREST
233
arborescent turf algae. When measured, giant kelp holdfasts covered x 6-12% of the site (Fig. 1). The area covered by giant kelp did not relate directly to the number of plants on the site because a few large plants could cover an area which could support many smaller ones. Oceanic conditions were unusually calm around San Nicolas Island between December 1983 and May 1984. This period was characterized by a thick surface canopy, no giant kelp recruits found on the study area, sloughing of arborescent turf algal fronds, and a substantial increase in sessile invertebrates. We did not observe any of these events from January to May in the four previous years. Percent cover of crustose coralline algae in all plots was similar at the start of the study (df = 3,27; F = 0.14; P = 0.94) (Fig. 2). x l/z (50-57.2%) ofthese algae survived, regardless of treatment, and survival did not differ significantly between the treatments (df = 2,23; F = 0.05; P = 0.95) (Fig. 2b-d). Crustose coralline algae apparently propagated to other permanent points under the artificial holdfasts, and some probably survived under dominant species that died from or during treatment. Total cover (survivorship plus recruitment) of these algae differed by only 7.3-25.9% from that sampled in the treatment plots at the start of the study. Because of recruitment, the 12-month treatment had the least change in total cover at treatment termination (Fig. 2d); this recruitment was significantly higher than that in the g-month treatment (df = 2, 23; F = 3.42; P = 0.05; Fisher’s PLSD). Mortality accounted for the greatest loss of crustose coralline algae in the treatment plots and increased with duration of the treatments (Fig. 2b-d). Mortality of these algae in the control plots was low except between December 1983 and May 1984 (Fig. 2a). Intact crustose coralline algae found after treatments were ended, particularly those remaining from the original cover, were lighter in color than those in the control plots. Several days after we terminated the 5- and 8-month treatments, the return of darker coloration indicated that some of these algae probably were still viable. In four of six cases (surviving cover and total cover), crustose coralline algal cover was similar between the treatments and the controls at the time of treatment termination [df = 13 (5, 8 months) and 9 (12 months), t = 0.05; Fig. 2b-d]. A biological explanation was not apparent for the two exceptions. Crustose coralline algal cover decreased in the control plots mainly because of overgrowth by sessile invertebrates (Fig. 2a). In subsequent sampling of the control plots, increases in this algal cover occurred mostly at points where these algae probably had survived overgrowth. In the months following the termination of treatments, total crustose coralline algal cover increased in the treatment plots primarily because of new recruitment (Fig. 2b,c). Ample bare and calcified substrata were available for colonizing turf organisms after the artificial holdfasts were removed, although sessile invertebrates also overgrew cmstose coralline algae during this time. As much as 12.6% of the increase in crustose coralline algal cover was probably algae that survived under sand that had accumulated under the artificial holdfasts and dissipated after they were removed (Fig. 2b,c). We observed a similar accumulation of sand under giant kelp holdfasts. Sand accounted for ~4.4% of the change in cover of these algae in the control plots.
percentcover II
tata
cover
r> surviving percent
cover gained
arecruited to new permanent point pilpreviousfy covered by organism, or 0 by sand percent a morta!it calcifie
60
lost (bare or
d” remains)
covered or replsced by orgsntsm, or tfby sand .-
40 20 0
-20 40
lou 80 60 4cJ
20 0 -20 1Z-month
Dee 83
treatment
flay84
-40
(n =
Aug 84
Dee 84
l-40
Fig. 2. Surviving and total mean percent coyer of crustose coralline algae at permrtnent points in treatmeflt and control p&s. Percent change, percent increase or decrease from one sampling interval to next. N, number of plots *treatment I”‘. Bars, -f-1 SE.
Colonial, encrusting bryozoans (primarily A&mbran@~m sp. nnd Puvasmirtinrr sp., suborder Cheilostomata) most commonly overgrew crustose coralline algae. At the start of the study, bryozoan cover was lower in the control plots than that in the treatment plots (Fig. 3). This trend was reversed after treatment. Bryozoan cover was significantly lower in the treament plats than that in the cuntro1 plots at treatme& termination [df = 13 (5,8 months) and 9 (12 months), t = &OS]. Mortality increased with duration
SURVIVAL OF KELP FOREST Encrusting
Bryozoans
235 percentcover lltotalcover *Isurviving cover
percent
gained
recruitedto new Hpermanentpoint previously covered by orgsnlsm, or 0 by sand
q
percent lost (b) 5-month treatment
1 mortslit (bare or
(n = 10)
calcilieP remains) covered orreplacet by organism,or
Oby
12-monthtreatmentln
sand
= 6) 80 60 40 20 0 -20 -40 -60
Dee 83
Ray 84
Aug 84
Dee
-80
Fig. 3. Surviving and total mean percent cover of encrusting bryozoans at permanent points in the treatment and control plots. Percent change, percent increase or decrease from one sampling interval to next. N, number of plots. treatment - ‘. Bars, + 1 SE.
of artificial holdfast placement and was probably greater than inferred in Fig. 3: l/4 (25.0%) to z l/2 (55.6%) of the bryozoans lost were replaced by crustose coralline algae. These algae either recruited to points formerly occupied by bryozoans or survived underneath bryozoans that died during treatment. The total cover of bryozoans at treatment termination was greater than the surviving cover, indicating that bryozoans had recruited under the artificial holdfasts (Fig. 3b-d). Bryozoans recruited into pockets in the substratum and did not survive direct contact with the artificial holdfasts.
In the control plots, encrusting
bryozoans
cover by May 1984 (Fig. 3a); 2/3 (66.7?,, stratum, calcified remains
occurred
algae. The remaining
and a fleshy crustose
at certain
from 4.1 to 14.7”,, mean total
j of this recruitment
and crustose coralline
grew other sessile invertebrates area. While they increased
increased
red alga uncommon
points in the control
on bare sub-
bryozoans
over-
on the study
plots from December
19X3
through August 1984, encrusting bryozoans were also overgrown (primarily by different bryozoan species), or replaced by crustose coralline algae or bare substratum at other points (Fig. 3a). Encrusting bryozoans did not appear to survive overgrowth by other sessile organisms. Sand covered a large proportion of known encrusting bryozoans at the end of the 5-month treatment (Fig. 3b). After the sand dissipated, the re-occurrence of bryozoans at permanent points 3 months later indicated that some bryozoans may have survived under that sand. However, it is also possible that the original occupants died and were replaced by new conspecific recruits. Encrusting bryozoans recruited rapidly following treatment termination (Fig. 3b,c). Similar to the control plots, > l/3 (38,59,,) to > l/2 (5 1.4”,, ) of these bryozoans overgrew crustose coralline algae. Sponges and tunicates comprised little cover in both the treatment and control plots. Nearly half of the sponge cover sampled in December 1983 (Fig. 4a) survived in the S(43.9”;)) and g-month (43.3%) treatments and < 1:‘lO (6.7%) survived the 12-month treatment. However, because of recruitment, total sponge cover in the 5-month treatment was greater than that sampled at the start of the study, changed little in the &month treatment, and declined by < l/2 (46.7%) in the 12-month treatment (Fig. 4a). Total sponge cover changed little in the control plots. Sponges survived and recruited in pockets in the substratum and appeared in good condition at treatment termination. As with bryozoans, sponges died primarily at contact points with the artificial holdfasts. Tunicates comprised < 5?$ cover on any of the plots. A small percentage of these survived and recruited in the 5-month treatment,
but none survived the 8- and 12-month
treatments. Most other sessile organisms that formed primary cover were uncommon, except for the vermetid tube snail Serpulorbis sp., and holdfasts of arborescent turf algae (Fig. 4b,c). The actual cover and effects of treatments on Serpulorbis were difficult to assess. Many organisms overgrew the extensive shell of Serpulorbis, which appeared to have no effect on the snail. The shells were bleached white or disintegrated at contact points with the artificial holdfasts, particularly in the 12-month treatment, but the snail was often alive. The snail could occupy a small portion of its shell and survive. Serpulorbis recruits were also found in the treatment plots. In the control plots, changes in overgrowing organisms often accounted for changes in Serpulorbis, i.e., whether it was visible to be sampled or not. The cover of arborescent turf algal holdfasts declined slightly in the 5-month treatment, and substantially in the 8- and 12-month treatments (Fig. 4~). The holdfasts sampled at treatment termination were mostly pale-colored, articulated coralline algae. After the 5- and 8-month treatments were terminated, color returned to these holdfasts
SURVIVAL OF KELP FOREST Primary 12 ..
encrusting
(*)
Cover
Secondary (d)
sponges
8 ‘.
60..
6 ..
70.. f 60..
+
4 a’ tf z *
(b) k
16 ..
> 8
14.. 12..
2
10..
8
0 *.
b Q
6 4”
all
Cover
arborescent
algae
90..
10 ‘.
2”. 0.F
231
t
*
*
50 ..
0
:
40 ..
Serpulorbis
30 ..
sp.
t
2 ..
t If+
20 .. 10 ‘.
i 4 I
o.(e)
articulated corallfne algae *
l
30 .’ 20..
+
10..
+
0.
. (1)
foliose
red
algae
40 .’
Dee
83
nay
Aug
-
84 -
Dee Dee
nay -
Aug
Dee
84 -
Fig. 4. Total mean percent cover of other common organisms or groups of organisms that formed primary or secondary cover at permanent points in treatment and control plots. Bars, + 1 SE. *, significant difference in cover between treatment and control at time of treatment termination [df = 13 (5, 8 months) or 9 (12 months), t = 0.051.
indicating that these plants probably were still viable. The cover of the turf algal holdfasts declined in the control plots from December 1983 to May 1984 (Fig. 4~); sessile invertebrates overgrew !z 2/3 (60.0%) of these and the remainder were dead. By August and December 1984, holdfast cover increased either because of recruitment, or re-exposure at points of overgrowth, indicating that short-term overgrowth was probably not harmful to the holdfasts. Some secondary cover (thalli and fronds) of arborescent turf algae was found at
treatment
termination
and appeared
viable (Fig. 4d). Most of this cover was articulated
coralline algae, particularly Calliurthmn sp.. which was the most common ofthese algae. Of the articulated coralline algal cover sampled in December 1983, z 1 3 (30.3”,. 1 survived the j-month
treatment,
survived the 12-month treatment termination of the 5- and g-month
z l/4 (24.5”,,) the X-month treatment, and little (2.5”,, ,I (Fig. 4e). The initial increase in these algae after treatments was mainly due to regeneration of plants
identified in December 1983, but new individual plants were also found. < l/l0 (9.0”;,) of the secondary cover of foliose red algae survived the 5-month treatment, little (< 17;) survived the 8-month treatment, and none survived the 12-month treatment (Fig. 4f). Stolons of Rho@menia sp., which was the most common of these algae, and deteriorated remnants of Gefidium sp. were found in the treatment plots. After the artificial holdfasts were removed, much of the initial foliose red algae regenerated or recruited at or near these stolons and remnants. Secondary algal cover declined in the control plots between the start of the study and May 1984 and did not differ significantly from the effects of the 5-month treatment (Fig. 4d). The timing of this decline coincided with the period of a dense giant kelp canopy mentioned above. In August and December 1984 the surface canopy was thinner than previously observed, and algal cover had increased in the control plots. This cover was significantly greater than that found in plots at the termination of the 8- and 12-month treatments (Fig. 4d).
DISCUSSION
Crustose
coralline
algae, while competitively
subordinate,
cover on rocky substratum in many marine communities 1975; Steneck, 1982, 1983). The prevalence of these
often form the dominant
(Adey, 1969; Adey & Vassar, algae has been attributed to
resistance to biotic and physical disturbances (Bakus, 1966; Paine & Vadas, 1969; Adey & Vassar, 1975; Lawrence, 1975; Vadas, 1977; Menge & Lubchenco, 1981; Steneck, 1983). Herbivores
that feed on overgrowing
arborescent
algae may also facilitate
the
survival of crustose coralline algae (Paine & Vadas, 1969; Adey & Macintyre, 1973; Steneck, 1983). Crustose coralline algae may have yet additional mechanisms for survival and dominance in marine systems where overgrowth by sessile organisms is common. Sebens (1986) reported that crustose coralline algae could survive overgrowth by dominant turf organisms for several months. In our study, these algae not only survived but recruited under simulated overgrowth for periods up to 12 months. These algae also probably survived underneath other organisms that were killed by the artificial holdfasts. Viable crustose coralline algae were found under large giant kelp holdfasts (Miles, 1987), most of which were z 40-50 cm in diameter, indicating that the giant kelp may have been several years old (Dayton et al., 1984). However, we have observed that many kelp recruits could grow together and form a large holdfast in < 1 yr. Crustose coralline algae
SURVIVAL
OF KELP FOREST
239
probably acquired photosynthetic products under the artificial holdfasts by lateral translocation through the thaIli from connecting crusts that were exposed to light (Wetherbee, 1979). R. Steneck (pers. comm., unpubl. data) suggested that lateral translocation is characteristic of thin-layer crustose corahine algae such as that found on the study area. After treatment termination, crustose coralline algal recruitment was probably enhanced by available bare or calcified substratum or by algae that had survived under organisms that died during treatment. Crustose coralline algae occupied available substrata rapidly relative to other sessile, turf organisms. Low recruitment and decrease of crustose coralline algal cover in the control plots indicated that these algae probably competed for space with sessile invertebrates. Calm oceanic conditions and a dense surface kelp canopy during the first half of the study appeared to facilitate sessile invertebrates (see also Rosenthal et al., 1974). The similarity in changes in crustose coralline algal cover in treatment and control plots indicated that the effects of overgrowth by sessile invertebrates and giant kelp holdfasts could be similar. However, the negative effects that dominant organisms might have on crustose coralline algae are probably offset by survival and recruitment of these algae during overgrowth; this is augmented by the more severe effects that giant kelp holdfasts apparently can have on the dominant organisms. Under treatment, arborescent algae revealed survival capabilities that may exist under normal conditions of shading and overgrowth. Turf algae found within established kelp forests probably endure extended periods of low illumination, with occasional periods of greater illumination associated with disturbance and loss of the kelp canopy. Similar capabilities have been suggested for algae exposed to periodically severe herbivory (Lubchenco & Gaines, 1981). In our study, the physical force or pressure exerted by overgrowth, as simulated by the artificial holdfasts, was not enough to kill all arborescent algae by 8 months. These findings indicate that these algae (and other sessile organisms) probably can endure relatively long periods of overgrowth and survive if they are not dislodged with giant kelp holdfasts during turbulent conditions. The dynamics of the turf assemblage were evident from changes observed in the control plots that affected the distribution of organisms at permanent points but not necessarily the overall abundance of those organisms. Mortality and overgrowth by other turf organisms were balanced with recruitment and survival of overgrowth, resulting in relatively constant cover. This relative constancy in species abundance in the control plots was in marked contrast to the pervasive effects of giant kelp overgrowth. Although the estimated area overgrown by giant kelp holdfasts was not large at any time period, this measure was augmented by the loss of giant kelp. In addition, dislodged giant kelp entangle other giant kelp and in turn cause their dislodgement (Rosenthal et al., 1974; Dayton et al., 1984). We observed that the resulting mass of holdfasts often scoured the substrata and further damaged the turf assemblage. If all of these events are taken into account, the actual area affected by giant kelp holdfasts could be calculated over a given time interval. These events in addition to kelp recruitment were continual processes related to the wave-swept exposure and surge of the open,
\.K. MILES AND F..( I\,lESI.OW
7Jii
unprotected
coastline
of San Nicolas Island (see also Dayton
et al., 1984). The rate a~
which the loss of giant kelp impacted the turf assemblage appeared to be dependent on the severity of winter storms and summer oceanic swell. The rate of impact by kelp recruitment illumination
appeared
dependent
at the bottom,
Previous investigations
on the condition
of the surface canopy and subsequent
and on the growth rate of kelp holdfasts. of this San Nicolas Island kelp forest indicated
that changes
in cover of turf organisms were affected substantially by illumination (Miles, 1987). Caging experiments showed that herbivores can affect the abundance and distribution of foliose algae (Miles. 1987). A consistent result of these studies was that crustose coralline algae persisted as the most abundant cover of the turf assemblage. In the present study, we simulated the effects of giant kelp overgrowth and demonstrated that certain turf organisms have adapted strategies for survival. Foremost among these organisms were crustose coralline algae. The effects of giant kelp that inhibited or killed most other organisms in fact contributed to the prevalence of these algae.
ACKNOWLEDGEMENTS
We thank K. Collins, the US Navy and personnel of San Nicolas Island, A. H. Hines, K. Cook, J. Estes, J. Lubchenco, R. Anthony and the anonymous reviewers of this journal. This study was supported by the Cooperative Research Units Center of the US Fish and Wildlife Service.
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