reed and foster 1984 effect of canopy shading on recruitment

8/3/2019 Reed and Foster 1984 Effect of Canopy Shading on Recruitment

http://slidepdf.com/reader/full/reed-and-foster-1984-effect-of-canopy-shading-on-recruitment 1/13

The Effects of Canopy Shadings on Algal Recruitment and Growth in a Giant Kelp

Forest

Daniel C. Reed; Michael S. Foster

Ecology, Vol. 65, No. 3. (Jun., 1984), pp. 937-948.

Stable URL:

http://links.jstor.org/sici?sici=0012-9658%28198406%2965%3A3%3C937%3ATEOCSO%3E2.0.CO%3B2-P

Ecology is currently published by Ecological Society of America.

Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available athttp://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtainedprior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content inthe JSTOR archive only for your personal, non-commercial use.

Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained athttp://www.jstor.org/journals/esa.html.

Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printedpage of such transmission.

The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers,and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community takeadvantage of advances in technology. For more information regarding JSTOR, please contact [email protected].

http://www.jstor.orgMon Oct 8 21:53:34 2007


http://www.jstor.org/about/terms.html

http://www.jstor.org/journals/esa.html

http://www.jstor.org/journals/esa.html

http://www.jstor.org/about/terms.html




Ecologr. 65(3) . 1984. pp . 937-948i 1984 b) th e Ecolog~cal ociet) of Ame r i c a

THE EFFECTS OF CANOPY SHADING ON ALGAL RECRUITMENT AND

GROWTH IN A GIANT KELP FOREST1

D A N I E LC. REED^ AN D M IC HA ELS. FOST ER

Moss Landing Marine Laboratories, .Irloss Landing, California 95039 LISA

Abstract. The subtidal (10-1 5 m) assemblage in the relatively sheltered giant kelp forest at Still-water Cove in Carm el Bay, California, consists of perennial species forming three major vertical layers:a .liiacrocystis pyrifera surface canopy, a dense subsurface canopy of another kelp, Pterygophoracalifornica, and an understory of articulated and encrusting coralline algae. The kelp canopies aloneor in combination can reduce bottom light to 1 3 % (usually < 1%) of surface influx. The effects oflight reduction by these vegetation layers on algal recruitment a nd subsequ ent growth were determin edby removing various c omb inatio ns of canopies over a 2-yr period, and following subsequent changesrelative to ap propriate controls. Removing both M. pyrifera an d P. californica canopies resulted inmoderate recruitment of these species as well as of the annual brown alga Desmarestia ligulata var.ligulata. None of these algae recruited into control areas where one or both canopies were left intact.Highest brown and red algal recruitment occurred when both kelp canopies plus understory corallinebranches were removed. Rem oval of the latter alone had n o significant effect. The tim e of year whenalgal canopies were removed had little effect on the composition of subsequent algal colonization, as

the recruitment of noncalcareous species occurred primarily du ring a short period in the spring. Theseresults indicate that the relatively low levels of both physical and biological disturbance in StillwaterCove allow the establishment of a few perennial algal species that inhibit their own recruitment, aswell as invasion of other species, by shading. This contrasts with nearby kelp forests subjected togreater and more frequent disturbance, and characterized by a diverse assemblage of annual algalspecies.

Key words: central California; com mu nity structure; competitio n; coralline algae; disturbance;glant kelp forest; light; Macrocystis; Pterygophora; recruitment; shading.

INTRODUCTION prevai l, th e a lgal assemblage is character ized by h igh

Numerous inves t iga t ions have s hown tha t compe- abun dan ces of a few compet i t ively super ior species that

t i t ion fo r l ight p l ays a n imp or tan t r o le in s t r uc tu r ing a r e f r equen tly long l ived and inh ib i t i nvas ion . Graz ing

many ter res t r ia l p lan t communit ies ( for rev iew see d i st u rb a n c e m a y b e e q u a ll y i m p o r t a n t t o c o m m u n i t y

Harper 1977) . Th e ver t ica l s t ructure of subm ar ine g ian t s t ructure . Grazers , by regula t ing a lgal abu ndan ce, mayke lp (Macrocyst i s s pp .) commu n i t i e s i s in m any ways ind ir ec tly a l te r comp e t i t ive in t e r ac tions (Pa ine an d Va-

comparab le to t e r r e s t r i a l f o r e s t s (Kuhneman 1970 , das 1969 , Nico t r i 1977 , Lubchenco 1978 ). Na tu ra l o r

Neushu l 197 1 , Fos ter 1975a) , an d cor re la t ive s tudies ar ti f ic ia l reduct ions in grazer dens i t ies hav e led to in-

sugges t shading by g ian t kelp may af fect unders tory creased a lgal abun dan ce a n d changes in species com -

algae jus t as shading by overs tory t rees af fects under- pos i t ion , an d th is has a l tered p lan t-p lan t compe t i t ion

s to ry p lan t s on l and (Daws on e t a l . 1960 , Neus hu l (Estes e t a l . 1978 , Lubche nco 1978 , Lubchenco and

1965 , Fos te r 1975b) . C om pe t i t ion fo r l igh t may be Menge 1978 , Pea r s e and H ines 1979 , Dugg ins 1980 ) .

even mo re d r amat i c in ke lp fo r est s , a s ligh t in t ens ity Th e e ff ec ts o f phys ica l d i s tu rbance can be mu ch th e

an d qua l i ty a r e a l t e r ed by bo th the vege ta t ion an d the s am e as thos e o f b io log ica l d i s tu rbance; th e d i s tu rbance

water . ma y act d i rec tly on p lan ts or ind irect ly by af fect ing

T h e s t ru c t ur e o f a c o m m u n i t y i s d e p e n d e n t u p o n o the r o rgan i s ms wh ich in te rac t wi th p lan t s. I n m ar ine

bo th t he in t e r ac tions between o rgan i s ms in the c om - macroalgal assemblages , d is turban ce is often caused bymun i ty a nd the physica l na tu r e o f the env i ronm en t . h igh wa te r mo t ion tha t may r emo ve vege ta t ion (Day -

Conne11 (1975) sugges ts that com pet i t i on a nd b io log- ton 197 1 , R os en tha l e t a l . 1974 , Sous a 1979b) .

i ca l d i s tu rbance a r e tw o in te r ac tions tha t p rov ide m os t O u r k n o w le d ge o f t h e i m p o r t a n c e o f c o m p e t i t io n a n d

o f the o rgan iza t ion in na tu r a l commu n i t i e s . The s t ruc - d is turbance in s t ructur ing mar ine a lgal assemblages has

tu r a l signi fi cance o f comp e t i t ion fo r l igh t and / o r s pace com e p r imar i ly f rom in te r t ida l s tud ie s . W ha t l i t tl e has

on a lga l popu la t ions has been s ho wn in a nu mb er o f been d on e in subt idal a lgal assemblages sugges ts that

mar ine commu n i t i e s (Day ton 1975a , Hruby 1976 , s imi la r mechan i s ms may r egu la te commun i ty s t r uc -

Sous a 19 79a , Hodgs o n 1980 , Lubchenco 1980 , Fos te r tu r e in th i s hab i t a t . Herb ivo re s (p r imar i ly s ea u r ch in s

1 9 8 2 ~ ) . n m o s t c a se s w h er e c o m p e t i t i v e i nt e ra c t io n s [Lawrence 1975, B reen and M ann 1976 , Fo rem an 1977,

Duggins 1980]) , an d their pred ators (Es tes an d Pal-' Man uscript received 15 March 1982; revised 10 May 1983;

misa no 1974, Es tes e t a l. 1978) ca n s t rongly inf luenceaccepted 25 May 1983.

Present address: De ~a rt m en t f Biological Sciences. Uni- subt idal a lgal assemblages . In the absence of herb i-

versity of California, ~ a n t a arbara, ~a lif or ni a 3106 USA. vore s , algal-algal com pe titi ve inte ractio ns (p rim arily2



938 DANIEL C. REED AN D MICHAEL S. FOSTER Ecology, Vol. 65, No. 3

adults inhibiting juveniles) have been shown to be im-

portant structuring mechanisms (Dayton 1975a, Pearse

and Hines 1979, Duggins 1980). In add ition , differ-

ences in algal composition have been correlated with

spatial and temporal changes in water motion (Barrales

and Lobban 1975, Cowen et al. 1982, Foster 1982b).

In terrestrial forests, the often long-lived species which

form the highest canopy can monopol ize light an d thus

alter understory vegetation (Harper 1977). In subtidal

communities throughout the world, only a few plants

occur whose fronds form a surface canopy, and of these,

Macrocystis spp. is the most abundant and widely dis-

tributed. To our knowledge, only one othe r study con-

ducted in a M. pyrifera forest has experimentally ex-

amined algal competition for light, an d only the effects

of the surface M. pyrifera canopy on understory species

were evaluated (Pearse and Hines 1979).

Our study site, a multilayered Macroc,ystis pyrifera

forest in central California, experiences very low levels

of the types of biological and physical disturbance dis-cussed above. This suggests that competition may be

of primary importance in structuring the algal assem-

blage at this site. We experimentally examined the ef-

fects of shading by overstory plants on understory re-

cruitment and growth, and we present evidence of

inhibition by each layer. In addition, we suggest that,

contrary to many terrestrial forests, the surface canopy

is the shortest lived and that M. pyrzfera can be out-

competed by the longer-lived understory layers.

The experiments in this study were designed to eval-

uate two basic questions. (1) Is this community struc-

tured by competition for light and space among the

algae, and if so, what are the relative competitive abil-

ities of the common species? (2) Following a distur-

bance, what effect do the canopies have on succession?

The experimental design also allows us to predict how

this vertically complex algal assemblage will respond

to various intensities of disturbance.

Experiments were done in Stillwater Cove within

Carmel Bay in central California (36"34'N, 12 1°56'W).

The cove opens to the south, and the Macrocystispyrlf-

era forest is thus protected from large northerly swells

associated with winter storms as well as strong

northwesterly spring winds. The forest grows on a hard,

moderate-relief substratum of sandstone, conglomer-

ate, and lava (Simpson 1972). Low water motion and

lack of suspended sediment result in relatively clear

water, and M. pyrlfera plants are found from just below

the intertidal zone to depths below 30 m.

The kelp forest algal assemblage is characterized by

three layers of perennial algae, a surface Macrocystis

pyrlfera canopy of variable thickness, a subsurface can-

opy of another kelp, Pterygophora calzfornica, and an

understory of articulated and encrusting coralline al-

gae. Pterygophora calzfornica forms dense stands andhas stiff, 1-2 m long stipes tha t support blades at the

top. These blades produce a subsurface canopy, but

rarely touch the bottom. Macrocystis pyrzfera tends to

grow around the perimeter of these stands, but its long

fronds often produce a canopy overlying P. calzfornica.

Seasonal changes are apparent in both kelp canopies,

but fluctuation is greatest in that of M. pyrlfera. Max-

imum plant density and cover of M. pyrifera occur in

early summer, with minimums in late winter (Fig. 2;

Foster 19823).

The articulated coralline algae occur as dense mats

beneath the Pterygophora californica canopy, with

branches extending up to 10 cm above the substratum.

Calliarthron tuberculosum is most abundan t, with oc-

casional plants of C. cheilosporoides, Bossiella califor-

nica spp. schmitti, and B. orbigniana spp. orbigniana.

Encrusting coralline algae occupy space beneath these

mats and elsewhere, and very little bare rock is found

in the cove. Noncalcareous red algae comprise only a

small portion of the understory, and those species that

do occur (Plocamium cartilagineum, Laurencia subop-posita, an d Botryoglossum farlowianum var. farlow-

ianum) are most often found as epiphytes on C. tuber-

culosum. Sessile invertebrate cover is low except on

vertical walls.

The effects of the two kelp canopies (under varying

conditions of development) on algal recruitment were

examined using the experimental design shown in Fig.

1. The term "recruitment" as used here is based on

visual observations of macroscopic plants only (> 1 cm

tall), not observations of microscopic stages in algal

life histories. All underwater work was done using

SCUBA, and plants were identified according to Ab-

bott and Hollenberg (1 976).

Pterygophora efects

To determine the effects of the Pterygophora cali-

fornica canopy alone on algal recruitment under con-

ditions of a sparse surface canopy of Macrocystis pyrlf-

era, 547 P. calzfornica plants were removed in May

1978 from half of the 150-m2 study area located at 15

m depth (hereafter referred to as site 1). Plants were

removed by cutting the stipe just above the holdfast,

leaving the substratum undisturbed. The other half of

the study area was unaltered and was monitored as a

control. At the time of removal, a dense canopy of P.

callfornica blades was present in both the removal and

control sites, and simi lar plant densities were recorded

(7.3 plants/m2 in the removal site based on total counts,

and 6.4 * 0.6 plants/m2 [Z* SE] in the control site

based on counts in 20 randomly placed I -m 2quadrats).

These plants were of similar size, 1.5-2 m tall. As a

result of unusually large swells during the previous

winter, M. pyrifera abundance was reduced in the cove,

and only a sparse canopy of this species was present

over the study area during the time of this first exper-iment (Fig. 2a-c).



- -

CANOPY SHADING AND ALGAL RECRUITMENT

T R E A T M E N T T E S T

+ M ( S P A R S E C A N O P Y ) + PS I T E I M A Y 1 9 7 8 - F E E 1 9 7 9 Pterygophora EFFECT

+ M ( S P A R S E C A N O P Y ) - p >(WITH SPARSE Mocrocyst,s C4 NO PY)

- M + PSlTE I NOV 19 79 - JUL 1980 - M - P ----_.-_---___...

- - -Macrocyst is E F F E C T( D E N S E C A N O P Y )

+ M ( D E N S E C A N O P Y ) + P3IT E 2 NOV 1979 - JUL 1 9 8 0 Pterygophora E F F E C T

+ M ( D E N S E C 4 N O P Y ) - P- _ _ .W I T H D E N S E Mocrocyst,~CANOPY)

FIG. 1. Diagrammatic representation of experiments designed to evaluate the effects of Pterygophora an d Macrocyst~scanopies on algal recruitment. M = Macrocystis; P = Pterygophora;+ = present; - = experimentally remov ed.

T h e r e m o v a l o f Pter,ygophora c allfornic a h a d a d r a - hazardly p laced 1 m 2q u a d r a t s i n b o t h t h e re m o v a l a n d

matic ef fect on subsequ ent a lgal colonizat ion . Ou r ob- con t ro l a r eas in O c tober 1978, an d aga in in F eb ruary

servat ions indicated that recrui tment of Macrocystis 1979 (Tab le 1 ). N ew rec ru i tmen t w as no t obv ious be -

pyrifera a n d P. callfornica occur red a lmos t imm ed i - tw een these t imes , and p lan t dens i ti e s fo r a l l th r ee

ate ly , as these two species rapidly colonized the P. species were re la t ively cons tant for these two sample

calrfornica r emov a l a r ea . N o t iceab ly low er r ec ru i tmen t pe r iods . N o b row n a lgal r ec ru i tmen t w as obs e rved in

by the brown alga Desmarestia ligulata var . l igulata t h e u n m a n i p u l a te d P. callfornica con t ro l a r ea du r ing

(hereaf ter referred t o as D. l igula ta)w as a l s o obs e rved . th i s exper imen t (Tab le 1 ).

Recrui ts of o the r species (pr imar i ly f leshy red a lgae) Th e effects of Pterygophora cal2fornicaa lone o n a lgal

w ere much l es s abundan t , an d con t r ibu ted l it t le to the rec ru i tmen t in the abs ence o f an overly ing Macrocystis

algal unders tory . Brown algae were counte d in 20 hap- pyrzfera canopy can be eva lua ted by compar ing the

FIG.2. Macrocystis pyrifera canopy cover in the western portion of Stillwater Cove. Canopy traced from aerial infraredphotographs. Relative density index (RD I) = area of kelp in large square + area of large square. 0 indicates location of site1: 0,ite 2. Lack of canopy over site 1 in d-f is due to experimental removal.



940 DANIEL C. REED AND MICHAEL S. FOSTER Ecology, Vol. 6 5 , No. 3

T ~ B L E Density (plants/m2)of all brown algae in the Pterygophora removal and control areas at site 1. prior to (May 1978).and after (October 1978, February 1979) Pterygophora removal.

Algal density (plants/m2)

Pterygophora Pterygophora ~Wa crocystzs Desm arestla No. 1-m2

Treatment Date adults juveniles pyrifera ligulata quadrats

Mean i- 1 SE

Pterygophora May 78 7.3* 0* 0.02* 0* . . .removal Oct 78 0 17.6 1 3.4 9. 6 i 1.4 1.6 i 0.4 20

Feb 79 0 14.1 i 1.7 7.1 t 0.7 1 .4 1 0.4 20

Pterygophora May 78 6.4 i 0.6 0 0 0 20control Oct 78 8.3 i- 1.3 0 0 0 20

Feb 79 6 .7 i 0.6 0 0 0 20

* Densities based on total counts in May 1978.

Pterygophora removal and control areas in site 1 during

the period of November 1979-July 1980 (Fig. 1). As

part of other experiments (see coralline understory ef-

fects and yearly and seasonal fluctuations), the M. py-

rifera canopy, which had developed following the Pcallfornica clearing in May 1978, was removed over

site 1 and from a 20 m wide area surrounding it from

November 1979 to July 1980. In addit ion, allM.pyrlf-

era and P. californica recruits in the Pterygophora re-

moval area were continuously removed during this time.

As a result, these two species were absent (except for

the stand of P. callfornica in the Pterygophora control

area) from site 1 in November 1979. By March 1980,

the annuals that were present in November had died,

and consequently, no brown algae were present in the

study area at this time. Following recruitment in May

1980, the density of Desmarestia ligulata in 20 per-

manent 1-m 2quadrats located in the Pterygophora re-

moval area was 17.1 rfr 5.2 individuals/m2 ( 3 t E).

Although counts were not made prior to their removal,

our observations indicated that the abundances of new-

ly recruited M. pyrlfera and P. californica in the Pter-

ygophora removal site were similar to those found in

this area the previous year. The only brown algal re-

cruitment observed during this time in the Pterygo-

phora control area were two P. callfornica plants that

remained small, and eventually died during their 1st

yr.The effects of a Pterygophora californica canopy un-

der a dense cover of Macrocystis pyrifera were exam-ined by comparison with a second site (site 2; see 0,

Fig. 2) located z 7 5 m from site 1 at 10 m depth. The

understory at site 2, like that of site 1 (and much of

Stillwater Cove [Foster 1982b]), was characterized by

a dense P. cal fornica canopy, a low-lying coralline

mat, and low sessile-invertebrate cover. In November

1979, eight permanent 1 m2quadrats, designated with

plastic tape anchored by concrete nails, were estab-

lished within the P. callfornica stand. The same num-

ber and size of quadrats were marked outside the P.

callfornica canopy. A canopy of M. pyrifera was pres-

ent over the site at this time (Fig. 2d) and, by the timeof spring recruitment the following year, was quite dense

(Fig. 2e). This canopy persisted until the end of the

experiment (Fig. 20. Inhibition as a direct result of the

P. callfornica canopy was not apparent in this exper-

iment, because by July 1980, no recruitment had oc-

curred in any quadrats or surrounding areas of eithertreatment. Recruitment, however, did occur at this time

in site 1, where both kelp canopies were removed (see

above paragraph). This suggests that the effects of P.

californica on algal recruitment are masked when a

dense overlying M. pyrifera canopy is present.

Macrocystis e fec t s

Comparison of the results from the experiments at

sites 1 and 2 conducted at the same time (November

1979 through July 1980; see Fig. I), suggests that a

dense Macrocystis pyrlfera canopy alone is able to pre-

vent brown algal recruitment. As stated above, no re-

cruitment was observed under a dense M. pyrlfera can-

opy in site 2, regardless of whether a P. callfornica

canopy was present. In contrast, substantial brown al-

gal recruitment occurred at the same time in site l ,

where both kelp canopies had been removed. I t appears

a sparse M. pyr fer a canopy is less likely to prevent

such algal colonization, as brown algal recruitment was

observed under both a sparse surface canopy and no

surface canopy (see Pterygophora effects section and

Table 1). Although the evidence for this is derived from

experiments which were done at two different times

during two different years, in both cases substantial

recruitment of brown algae was observed only in thespring.

Kelp cano py e f fects on l ight

Light measurements (using a Li-Cor Model LI- 185

quantum meter with surface and underwater photo-

synthetically active radiation quantum sensors) were

made within the study areas at maximum (July) and

minimum (March) canopy development during two

successive years (1979, 1980), in order to determine

the amount of light reduction occumng under the var-

ious kelp canopies. All measurements were taken dur-

ing late morning hours under overcast skies.Although subsurface light varies considerably in



June 1984 CANOPY SHAD ING AN D ALGAL RECRUITMENT 94 1

I LIGHT UNDER 1o ke lp ca n o p y

comblned Macrocysf~sI- a nd Pferygophoro0 HPfer~gophoroon ly

.Macrocysf/s o n l y

M AR 79 JUL 79 MAR 80 JUL 80

FIG. 3 . Subsurface light intensity at minimum (March)

and maximum (July) Macrocystis canopy development. All

measurements were taken at 15 m depth. Variation is k 1 SD;

n = 4.

Stillwater Cove, measurements made on four different

dates under different conditions of canopy develop-

ment and type show that either a Pterygophora cali-

fornica or dense Macrocystis pyrifera canopy can re-

duce subsurface light intensity to between % and xoofthat found at the same depth, but without a canopy

(Fig. 3). At these low levels (0.1-2.5% of surface light),

the combined effect of both canopies is not much great-

er than their individual effects. Except for the mea-

surements made in March 1980, the light intensity

beneath the kelp canopy or canopies was within or

below the range of 0.5-1% of surface illumination. All

available information indicates that this range is the

lower limit for laminarian growth (Luning 198l ), and

thus reduction in bot tom irradiance caused by the pres-

ence of the kelp canopies is capable of inhibiting algal

recruitment.

Corall ine understory efects

In addition to the various overstory canopy manip-

ulations done at site 1 (see above), the area was si-

multaneously used to examine the effects of the cor-

alline understory on algal recruitment from March to

July 1979. To test the hypothesis that branched cor-

alline algae affect the recruitment and growth of other

plants, coralline branches were removed within 10 per-

manent 1-m2 quadrats located in the kelp canopy re-

moval site. A paint scraper was used to remove the

branches from the substratum, leaving only holdfasts

and encrusting organisms (mostly corallines). The hy-

pothesis that crustose coralline algae (and holdfasts of

articulated species) affect recruitment and growth of

other algae was tested by chipping (with an air-driven

impact hammer) the coralline crust from a 0.0625-m2

area located in each of the branch removal quadrats.

As a control, 10 permanent 1-m2quadrats were estab-

lished in which the coralline understory was left un-

disturbed. The 20 1-m2quadrats were arranged so eachquadrat was adjacent to a t least two others. Treatments

were randomly assigned within this arrangement. As

noted above, Macrocystis pyrifera an d Pterygophora

callfornica readily colonize when kelp canopy shading

is reduced. To eliminate add itional effects due to these

species, M. pyrlfera and P. californica recruits were

continually removed, usually when < 5 cm tall.

The effects of coralline manipulations under both a

canopy of Pterygophora californica and Macrocystis

pyrifera were examined by establishing, in the kelp

canopy control area, treatments and replicates identical

to those in the kelp canopy removal area. No recruits

were removed in this area, and the surface canopy

formed by surrounding M. pyrlfera plants was not dis-

turbed. This experiment is illustrated in Fig. 4.

Species composition and cover of the algal under-

story were estimated using a point contact method

(Greig-Smith 1964) with modifications for underwater

use similar to those described by Foster (19823). All

vegetation layers above (up to 1 m) and below indi-

vidual points are recorded using this method, so cover

can exceed 100%. Twenty points were sampled in each

of the coralline branch removal and control quadrats.

A 0.0625-m2 frame. subdivided into 100 squares, was

used to estimate cover visually in quadrats chipped to

bare rock. Percent cover data were normalized with an

arcsine transformation for statistical comparisons (So-

kal and Rohlf 1969). Unless otherwise noted, variation

about the mean in the text and figures is k 1 standard

error of untransformed data.

y 'Mocrocystls pyrifnrom c o r a l l l n e c o n t r o l

F ~ t e r y g a p h o r ocolifornico& j c o r a l l i n e b r a n c h e s

scrape to bar e rockremoved

FIG. 4. Schematic representation of the algal assemblage

in site 1 and the experimental manipulations which were per-

formed in March 1979. Replicates not shown.



DANIEL C. REED AND M ICHAEL S. FOSTER Ecology. Vol. 65 . No. 3

Premanipulation Postmanipulation

Kelp Kelp Kelp Kelo

SPECIES Canopy canopy canopy canopyControl Removal Control Removal

Calliarthrontuberculosum

-7Epiphytic Red Algae onC. tuberculosum

EncrustingCorall~nesDesmarestial~oulataDesmarest~akurllensls

Nereocystisluetkeana

Fleshy Red Algae BOther Spec~es

Bare Rock I n----00 50 0 0 50 100100 50 0 0 50 100

i

Coralline Control P E R C E N T COVERCoralline Branch RemovalScrape to Bare Rock

FIG.5 . Mean understory algal percent cover in the kelp canopy remov al and control areas in March 1979, prior to initiatio nof coralline understory treatments, and in July 1979. 130 d after establishment of coralline understory treatments with theremoval of Pterygophora calfornic a an d ,Wacrocyst~spj~rl feraecruits. Epiphy tic red algae include B o t r y o g l o s s u m f a r l o ~ ~ ~ ~ a n u mspp. farlow,ianum, Laurencla subopposlta, an d Plocamium cart l laglneum. Upright coralline algae other than Calllarthrontuberculosurn comprise "other species" category; n =- 10 quadrats for each trea tment. Error bars are t 1 SE .

Al l quad ra t s were s amp led p r io r to the co ral l ine m a-

n ipu la t ions in March 1979 , an d aga in in J u ly 1979 .

Brown algae that recru i ted in to the kelp canopy re-

mova l a r ea fo llowing the Pterygophora clear ing in M ay

1978 were r emove d in Feb rua ry 1979 . C ons equen t ly ,

the unde r s to ry cove r in bo th the ke lp canopy r emova l

and con t ro l a r eas was s imi la r in a ll t h r ee o f the p ro -

pos ed co ra ll ine unde r s to ry t r ea tmen t s p r io r t o the s t a r t

of the exper iment (Fig . 5 ). With in 2 wk af ter man ip-

u la t ions were done, a th ick bu t shor t - l ived d ia tom f i lm

was observed in a l l th ree cora l l ine t rea tments in the

kelp canopy removal s i te . By la te Apr i l , b rown and

f leshy red a lgal recru i tment had s tar ted in cora l l ine

b ranch r emova l a nd con t ro l quad ra t s in th i s s ame a r ea .

N o changes in the unde r s to ry were r eco rded in any

ke lp canopy con t ro l quad ra t s a t t h i s t ime . R ec ru i tme n twas s ignif icant ly h igher in cora l l ine branch removal

quadrats vs . cora l l ine contro l . Pr ior to thei r removal

in May 1979 , the combined mean dens i ty o f Macro-

cystis pyrzfera a n d Pterygophora calzfornica recruits

( these species were co mb ined , as they a re d i ff icu lt to

d is t inguish when smal l ) was 324 .5 k 80.9 ind iv i-

dua l s /m z in the co ral l ine b r anch r em ova l qu ad ra t s , and

11.8 i 7 .3 ind iv idua l s /m2 in co ral l ine con t ro l qua d -

ra ts ( P < . 01 , two- s amp le t tes t) . Desmarestia ligulata

fo l lowed a s imila r pat tern of recru i tme nt (1 12 .0 i 2 1.4

vs. 24.7 + 9 . 3 i n d i v i d u a l s / m 2 , P < . 01 , two- s amp le t

test).

By Ju ly 1979, in the absence of young Lbfacrocystis

pyrIfera a n d Pterygophora calIfornica compe t i to r s ,

Desmarestia ligulata a t t a ined a h igh cove r in bo th the

co ra ll ine b r anch r emov a l a nd con t ro l qu ad ra t s (F ig. 5 ) .

Al though p lan t de ns i ty for th is species d i ffered in these

two t r ea tmen t s ( s ee abo ve pa rag raph ), pe r cen t cove r

d i d n o t (P > . 05 , two- s amp le t test). Desmarestia lig-

d a t a can a t t a in l eng th s up to 8 m (Abbo t t and Ho l -

lenberg 1976) and , as i t does not f loat , can fo rm a de nse ,

low- ly ing canopy. Consequent ly , the b lades of ind i-

v idua l p l an t s f r om o ne quad ra t f r equen t ly ove r lapped

nea rby quad ra t s , b i a s ing the pe r cen t cov e r da ta fo r th i s

species.

Six ind iv iduals of the sur face-cano py-form ing kelp

Nereocystis luetkeana also recru i ted in to the cora l l ine

b ranch r em ova l quad ra t s , and tw o even tua l ly r eached

the sur face . Nereocystis luetkeana d i d n o t o c c u r i n a n yo the r t r ea tm en t (F ig . 5 ). Th e cove r o f Desmarestia ku-

rilensis an d the f leshy red a lgae Bonnemaisonia noot-

ka na , Ca l lophy l li s j l abe llu la ta , F auch ia lac in ia ta ,

Fryeella gardneri, Neoptilota densa, a n d Wee ksia re-

ticulata was s l ight ly h igher in the cora l l ine branch re-

moval quadrats (Fig . 5 ) , bu t overa l l recru i tment of

these species was low, and differences were not s ignif-

i can t ( P > . 2 , two- s amp le t test).

Recru i tm ent was general ly lowes t in qua drats scraped

to bare rock . By Ju ly 1979, cora l l ine crus ts comp r ised

the m a jo r i ty o f the a lga l cove r in thes e qu ad ra t s (F ig.

5) . Mos t of these were the basal por t ions of upr ight

co ra ll ines , a s muc h o f the c ru s t l a t e r deve loped in to



June 1984 CANOPY SHADING AND ALGAL RECRUITMENT 943

T A B L E Summary of the effects of the d~fferent lgal layers on the recruitment of brown algae. M = A2rlacroc~stlsyr~fera.

P = Pterjgophora callfornlca. C = Corall~ne ranches. EC = Enc rust~ ngcora ll~ne .+ = Present, - = Absent or expenmen-tally removed.

Test Treatment

Pter j~ophora +M (sparse canopy) +P + C + E Ceffect +M (sparse canopy) -P +C +E C

M + P + C + E CM - P + C + E C+M (dense canopy) +P + C + EC+ M (dense canopy) -P+C +E C

.Wacrocyst~s + M (sparse canopy) -P+ C+ ECeffect -M-P+C+EC

+M (dense canopy) - P + C+EC

C ora ll ine b ranch M - P + C + E Ceffect M - P - C + E C

+ M (dense canopy) +P +C +E C+M (dense canopy) +P- C+ EC

Encrusting coralline -M -P -C+ ECeffect -M-P-C-EC

Calliarthron tuberculosum. R e c r u i t m e n t o f Desmares-

tia ligulata an d the nonca lca r eous r ed a lga Gigartina

corymblfera was a l s o obs e rved in the s c r aped quad ra t s ,

bu t was low and var iab le for both species . Fi f ty- f ive

pe rcen t o f the s u r f ace in thes e quad ra t s r ema ined ba re

rock .

Oth e r than a f ew ep iphy tes on r egene ra ted b r anches

in the co ra l line b r anch r emo va l qua d ra t s , no r ec ru i t-

me n t occu r r ed in an y o f the th r ee co ra l line unde r s to ry

t r ea tmen t s loca ted in the und i s tu rbed ke lp canopy co n -

t ro l s i te dur ing the 130 d fo l lowing the s tar t o f the

expe r imen t (F ig . 5 ). R e c ru i tmen t was no t obs e rved in

a r eas sc r aped to ba r e rock un t i l No vem ber 1979 , 250

d af ter c lear ing , when a few coral l ine crus ts appeared .

A sum ma ry of the ef fects of the d i f feren t a lgal canopies

on recru i tment is presented in Table 2 .

Yearly and seasonal . f luctuations in recruitment

In ord er to ex am ine year - to-year d i fferences in a lgal

r ec ru i tmen t , t he a bov e co ra ll ine man ipu la t ions were

mon i to r e d th rough a n add i t iona l g rowing s eas on , and

al l qua drats were per iodically samp led unt i l Ju ly 1980.As before , Mac rocystis pyrifera a n d Pterygophora cal-

lfornica r ec ru i t s were con t inua l ly r emov ed a s s oon a s

they were dis tinguishable. Except for coralline algae

and the i r ep iphy tes , no p lan t s tha t r ec ru i t ed in the

spr ing of 1979 pers isted through the win ter , so that a l l

brown and f leshy red a lgae recorded in the Ju ly 1980

sample recru i ted in spr ing 1980.

B ased o n th e tw o yea r s s am p led , yea r - to -yea r fluc -

tua t ions in the compos i t ion an d cove r o f the a lgae tha t

r ec ru i ted in to the s i t e appea r to be low (Tab le 3). Des-

marestia ligulata cov er was re la t ively h igh b oth years ,

wi th D. kurilensis cover muc h lower. Nereocystis luet-

keana d id no t appea r in the J u ly 1980 samp l ing ; how-

Brown algalrecruitment Conclusions

None The Pterygophora canopyMod erate prevents successful brown

Low (two recruits) algal recru ~tm ent egard-Moderate less of the co nd ~ti on fNone the A2rlacrocyst~sanopy.None

Moderate Only a dense ,Wacrocystls

Moderate canopy is independentlyNone able to prevent brown

algal recruitment.

Moderate Inhibition of recruitmentHigh by the branched corallineNone layer is only observed inNone the absence of kelp canopy

shading.

High Recruitment is inhibitedLow on newly exposed rock.

eve r , i t was obs e rved in the s p r ing of tha t yea r , bu t a s

in 1979 only in up r igh t co ra l line r emov a l qua d ra t s . I t ,

a long with severa l species of f leshy red a lgae , began to

show s igns of deter iora t ion ear ly in the growing season;

ind iv idua l s were gone by l a t e J une a nd cons equen t ly

were no t r eco rded in th e J u ly s amp l ing pe r iod .

In bo th 1979 an d 1980 , a peak in b row n a lgal r e-

c ru i tme n t occu r r ed in l a t e Apr i l, con t inued fo r -4 w k,

an d then dec l ined . Kim ura (1980 ) found a s imi la r pa t -

t e rn a t a nea rby s i t e in C arm e l B ay . You ng .Macrocystispprzfera a n d Pterygophora californica s po rophy tes were

r a re ly obs e rved a t o the r t imes o f the yea r. R ec ru i tme n t

of f leshy red a lgae a lso seemed to occ ur in the spr ing ,

wi th th e excep t ions o f the pe r enn ia l s pec ies Gigartina

corjwnblfera a n d Weeksia reticulata, which firs t ap-

pea red in the f al l.

I n a n a t t em p t to exam ine s eas ona l d if fe rences in a lga l

r ec ru i tmen t mo re c lo se ly , f ive add i t iona l quad ra t s o f

the three cora l l ine unders tory t rea tments (cora l l ine

con t ro l , co r al l ine b r anch r emov a l , an d s c r aped to ba r e

rock) were es tab l ished in th e kelp remo val are a in s i te

1 in Nove mb er 1979 . At th i s time , the annua l Des-marestia ligulata was s t i l l p resent in the March (Fig .

4) unders tory c lear ings , whi le the unders tory in the

quad ra t s c l ea r ed in Nov em ber consi s ted , be fo re t r ea t -

ments , en t i re ly of cora l l ine a lgae and their ep iphytes

(Fig. 6). By February 1980, the cove r of D. l igulata

had d ropp ed s ignificant ly in the M arch c lear ings (Fig .

6) , an d by M arch , th i s alga had comple te ly d is appea red

f rom thes e quad ra t s (D . C. R e e d a n d M . S. Fos ter ,

personal observation). R egrowth o f Calliarthron tuber-

cu losum w a s a p p a r e n t i n c o r a l l i n e b r a n c h r e m o v a l

quad ra t s c l ear ed in Nove mb er 1979 , a s was the re -

c ru i tmen t o f co ral l ine c ru s t s in to a r eas s c r aped to ba r e

rock (Fig. 6). O ur obs e rva tions ind ica ted tha t b rown



944 DANIEL C. REED AND MICHAEL S. FOSTER Ecology, Vol. 65. No. 3

TABLE. Percent cover of noncalcified algae in the Pterj.gophora removal site following spring recruitment in 1979 and1980. In both years, new A2rlacrocptispyrifera and Pterygophora callfornica were continually rem oved. The same individuals

were not sampled in both years. as no plants persisted longer than 10 mo . X signifies presence of a fleshy red algal species.

July 1979 ( n = 10) July 1980 ( n = 5)

Upright Upright

Coralline coralline Scrape Coralline coralline ScrapeSpecies control removal to bare rock control removal to bare rock

Mean i 1 standard error

Desmarestla llgulata 1 . 1 i 0.9 96.0 i 3.9 94.0 i 4.8 36.0 ? 16.0

Destnarestla hurllensls 1.1 i 0.9 12.0 i 3.5 12.0 i 3.5 80.0 ? 5.8,Vereocj stls l uetke anaFleshy red algae

(all species combined)

Bonnemalsonla nootkanaC a l l o p h ~ l l ~ sIabellulataFaucla laclnlataFr~ eella ardnerlGlgartlna corytnblfera,Veoptllota densaP~ kea obustaWeeksla retlculata

algae did not recruit into any quadrats until late April removal time (Fig. 7b). This increase was probably the

1980. In July, the algal composition of quadrats cleared result of regrowth from basal crusts. Recruitment of

at the two different times were quite similar (Fig. 6) , C . t u b e rc u l o su m was evident throughout the year in

although percent cover of D e s m a r e s t i a spp. was sig- quadrats scraped to bare rock, although there appeared

nificantly lower in all three of the coralline understory to be a lag period, as colonization was not immedia te

treatments in quadrats cleared in November, com- after scraping (Fig. 7c). This lag period may be an

pared to those cleared in March (P < .05 for each artifact of difficulties in distinguishing young coralline

understory treatment, two-sample t test). These results species. In the unmanipulated coralline control quad-

indicate that the time of year manipulations were done rats, C. t u b e r c u l o s u m cover remained relatively con-

had little effect on the timing of algal recrui tment or stant throughout the study (Fig. 7a).

subsequent composition.

The settlement and subsequent growth of Ca l l i a r - DISCUSSION

t h r o n t u b e r c u l o s u m were followed from March 1979 The results of these experiments show strong com-

to July 1980. There was a slow but steady increase in petitive interactions among the various perennial

growth (cover) of this species independent of branch species of algae that are of major importance in struc-

Novemb er 1979 February 1980 July 1980

SPECIES March 1979 Nov 1979 March 1979 Nov 1979 March 1979 Nov 1979Clearlng Clearing Clearlng Clearing Clearing Clearing

Calliarthron -uberculosum 7Epiphytic Red Algae on

C. tuberculosum 9 -Encrust~ngCorallines

Desmarestialigulata

Desmarestiakurilensis

Fleshy Red Algae1

4Other Species 4 e 4 L?Coralline Control

a Coralline Branch RemovalBare Rock fl- t l b O Scrape to Bare Rock-I-

0 0 5 0 0 0 5 0 1 0 01 0 0 5 0 0 0 5 0 1 0 0 10 0 5 0 0 0 5 0 10 0

PERCENT COVER

FIG.6. Understory algal percent cover of quadrats cleared in March 1979 and in November 1979 in the Pterygophoraremoval area: n = 5 quadrats for each t reatment.



945ANOPY SHADING AND ALGAL RECRUITMENT

a . Coralline Control

8 100 b. Branches Removed

t1 t

FEB JUL NOV FEB JUL

79 79 79 80 80

FIG.7. Percent cover of Calliarthron tuberculosum in thethree coralline understory treatments (ax ) n the kelp canopyremoval and control sites. The coralline understory treatmentquadrats in the kelp canopy control area were cleared in March1979 only. Quadrats in the kelp canopy removal site werecleared in March and November 1979. Coralline algae werenot cleared in any coralline control quadrats. j j on abscissaaxes indicate times when coralline algae were cleared; n = 5for the coralline understory treatment quadrats in the kelpcanopy removal area cleared in November 1979; n = 10

quadrats for all others. 8 - -8 kelp canopy control/Marchclearing. 0---0 kelp canopy removal/March clearing.A . . . . . A kelp canopy removal/November clearing.

turing the subtidal algal association in Stillwater Cove.

Unlike the Pterygophora californica canopy, the per-

sistence and extent of development of the Macrocystis

pyrlfera canopy is greatly affected by local meteoro-

logical and hydrographic conditions, and so is more

variable from year to year. In a calm year, both thesurface M. pyrlfera and subsurface P. callfornica can-

opies are well developed by the spring, and conse-

quently are independently capable ofinhibiting the ma-

jor pulse of algal recruitment which normally occurs

at this time (Fig. 3). In unusually stormy years, wave

surge may remove entire M . pyrijera plants and/or a

higher porportion of fronds per plant, resulting in a

greater reduction in surface canopy. When this occurs,

canopy restoration is delayed (Foster 1982b). Ptery-

gophora californica, unlike M . pyrifera, possesses a

thick, "woody" stipe that is very difficult to break. Loss

of entire plants after storms is rarely observed at Still-

water Cove (D. C. Reed and M. S. Foster, personal

observation). This characteristic, along with a subsur-

face habit, increases its persistence through these pe-

riods of high wave surge. During winter periods of

extreme water motion, large-scale removal of P. cali-

jornica has been observed in other central California

kelp forests (G. Van Blaricom, personal communica-

t ion) , and breakage of the substratum caused by ex-

cessive wave surge may remove bottom cover species

(Foster 19826). We have never observed these phe-

nomena in Stillwater Cove; therefore, despite the dras -

tic reduction in the M . pyrifera canopy by winter storms,

springtime recruitment continues to be inhibited by

the more persistent P. callfornica and branched cor-

alline canopies (Table 1, and text; see Coralline Under-

story Effects).

Our observations of the individual and combined

effects of the three major canopies on algal recruitment

show that recovery from disturbance is affected by all

canopies. Although we have not observed the natural

removal of Pterygophora callfornica or branched cor-allines by storms, the above observations suggest that

the removal of different vegetation layers occurs along

a disturbance gradient. Thus, analyzing the inhibitory

effects of the different algal layers allows the prediction

of community development under different intensities

of disturbance.

If greater storm-associated disturbance occurred in

Stillwater Cove, removing both Macrocystis pyrifera

and Pterygophora callfornica, our results indicate that

both of these perennials would recruit simultaneously

(Table 1). We did not experimentally examine their

interactions after recruitment, but a number of obser-

vations suggest they compete for light, and their com-

petitive abilities differ. Macrocystis pyrlfera forms a

surface canopy during the 1st yr, with small P. cali-

fornica below. We predict that, as both canopies de-

velop during successive years, fewer and fewer plants

recruit into these areas. In time, as the M . pyrlfera

plants are lost due to removal by storms, the more

persistent P. californica continues to develop, and a

dense, monospecific stand is formed, inhibiting further

algal recruitment. Inhibitory effects of P. callfornica

shading on recruitment have been suggested by others

(McPeak 198 1, Pace 198 1). Our observations at Still-

water Cove indicate that P. callfornica only forms densestands in certain habitat types, usually on the tops of

high-relief areas and flat terraces. The reason(s) for the

particular distribution is(are) unknown to us, but as a

result, M. pyrifera can grow and form an overlying

canopy in areas where P. callfornica is sparse or absent.

Continual removal of the dominan t canopy species

led to a significant increase in annual algal cover, con-

sisting primarily of Desmarestia spp., and to a lesser

extent, Nereocystis luetkean a and fleshy red algae (Fig.

5) . Foster (19826) found a similar increase in D. lig-

ulata following the natural removal of Macrocystis py-

rlfera canopy by storms. The opportunistic character-

istics of D. ligulata appear similar to those of the kelp



946 DANIEL C. REED AND MICHAEL S. FOSTER Ecology, Vol. 65, No. 3

Alaria jistulosa found in some Alaskan kelp forests

inhabited by sea otters (Dayton 1975a, Duggins 1980).

Both D. ligulata and A. jistulosa seem unable to invade

established stands of other kelps, but rapidly colonize

areas when other kelp canopies are removed. In ad-

dition, Duggins (1 980) noticed abundan t N. luetkeana

when a Laminaria groenlandica canopy was absent,

and Dayton (1975a), Pearse and Hines (1979), and

Foster (1982b) observed similar increases in fleshy red

understory algae following the removal of kelp canopy

species.

Coralline branches also inhibited algal recruitment,

and although no measurements were taken, this effect

was probably caused by reduced light. Removal of

branches did not increase primary space, because cor-

alline holdfasts were left intact, and clearly provided

suitable space for recruitment. Furthermore, if space

were limiting, one would expect the highest recruit-

ment on quadrats scraped to bare rock, not the lowest

as actually observed. However, this could have resultedfrom some toxic materials (metals?) leaching from the

new exposed rock, or may reflect the presence of "dor-

mant" algal stages which are not removed when the

upright branches are removed. The former hypothesis

is unlikely, as benthic diatoms quickly colonized the

scraped areas. Further experiments are underway to

resolve this question.

Inhibition of settlement caused by the abrasive ac-

tion of algae has been documented in intertidal (Black

1974, Dayton 1975b), and subtidal communities (Ve-

limirov and Griffiths 1979). That the subtidal articu-

lated corallines produce a similar whiplash effect is

unlikely, as their branches are stiff, intertwined, and

not subject to the extremes of water motion found in

the intertidal zone. Furthermore, if abrasion were im-

portant, one would not expect the observed common

occurrence of uncalcified epiphytes on Calliarthron

tuberculosum. Hruby and Norton (1979) found that a

thick turf of Enteromorpha intestinalis significantly re-

duced the number of algal spores reaching the under-

lying substratum. However, the C. tuberculosum mats

are far less dense than E. intestinalis turf. Thus, it is

also unlikely that our results reflect the effects of a

bamer to spore settlement on the bottom.

Articulated coralline algae do inhibit algal recruit-ment, but it is unlikely that any natural storm distur-

bance common to Stillwater Cove could remove the

tough thalli of these low-growing plants. If such a dis-

turbance did occur, the results show that unless all

adult kelp were removed so there was no source of

spores, kelp recruitment and growth would quickly

lower light to predisturbance levels, and coralline

branches would probably slowly regenerate from re-

maining holdfasts (Fig. 7b). If holdfasts were also re-

moved, coralline recovery to predisturbance levels

would simply take longer (Fig. 7c).

A diverse assemblage of small invertebrates, someof which are grazers, occurs in the coralline mats (Reed

198 I). Because of the difficulties encountered in trying

to remove these animals from the mats without dis-

turbing the plants, their impact was not directly de-

termined. However, the evidence available suggests that

their effects on recruitment are small relative to the

effects of the coralline branches. There was substantial

algal recruitment on coralline mats in the kelp canopy

removal area, and essentially none in the kelp canopy

control (Fig. 5), but the invertebrates associated with

the mats were undisturbed in both sites. It is possible

that the invertebrate fauna differed in mats due to

changes in water flow or predators as a result of our

kelp canopy manipulations. We did not measure water

motion, but qualitative observations indicated that the

abundance of potential fish and invertebrate predators

was similar in both kelp canopy removal and control

areas, and that the coralline mat fauna was similar.

However, all of the possible ways coralline mats and

their associated fauna may be affected by canopy ma-

nipulations that, in turn, affect algal recruitment war-rant further experimentation.

The only large invertebrate grazers commonly found

in Stillwater Cove are sea hares (Aplysia callfornica),

bat stars (Patiria miniata), and turban snails (Tegula

spp.). Sea urchins (Strongylocentrotus spp.), abalone

(Haliotis spp.), and kelp crabs (Pugettia spp.), impor-

tant herbivores in many California kelp forests, are

rare. The few large sea urchins and abalone present are

restricted t o crevices, where they probably feed on drift

algae (Lowry and Pearse 1973). The low densities of

these latter, potentially important , large herbivores may

be attributed to the presence of the sea otter, Enhydra

lutris, which has inhabited the cove since 1956 (Ebert

1967). These grazers are important prey of the sea otter

in California (Ebert 1968, Wild and Ames 1974), and

a variety of evidence suggests that sea otters can be

important in structuring near-shore algal communities

by limiting herbivore densities (Estes and Palmisano

1974, Estes et al. 1978, Duggins 1980). Little is known

about the structure of the algal communi ty in Stillwater

Cove prior to the re-establishment of sea otters. Macro-

cystis pyrifera was present (Andrews 1945), but per-

haps, as shown by Duggins (1 980)in southeastern Alas-

ka, under conditions of intense grazing, other perennials

were less abundant. If cortical rings in Pterygophoracalifornica are annual (as proposed by Frye 19 18), hen

the time since the re-establishment of sea otters in

Stillwater Cove closely parallels the proposed age of

the older P. callfornica stands based on our ring counts.

As many as 18 rings were counted in plants tha t were

removed from the study site in May 1978, "22 yr after

the re-introduction of sea otters into the cove. These

dense stands may have developed after sea otters re-

moved large grazers.

The giant kelp forest a t Stillwater Cove experiences

low levels of biological and physical disturbance. Un-

der these conditions, perennial algal species are ableto monopolize light, and thus exclude other algae as



947une 1984 CANOPY SHADING AND ALGAL RECRUITMENT

well as inhibit their own recruitment. I n contrast, near-

by giant kelp forests located 45-60 km north on a more

wave-exposed coast experience greater a nd m ore fre-

quen t levels of both physical an d biological dis turbance

(Cowen et al. 1982, Foster 19826). Thes e exposed for-

ests grow on a soft mudstone bottom that is easily

eroded by the high water m otio n experienced through-

out m uch o f the year. Shifting patches of sand also buryand abrade the substratum. Consequently, plants ar e

frequently removed. In addition, sea urchin (Stron-

gylocentrotus franciscanus) densitie s are relatively high,

as the are a is beyond the present range of sea otters.

Grazing by these urchins affects algal com posi tion an d

abundance, and may lead to a higher species richness

(Cowen 1979). This combi ned physical a nd biological

disturbance appears to reduce the survival of long-

lived, slow-growing perennial species. Th e understor y,

in the absence of continual overstory shading but dis-

turbed by water motion, sand abrasiodbur ial, an d sea

urchin grazing is characterized by a relatively rich as-semblage of rapidly growing, apparentl y ann ual species

which flourish during periods of a bunda nt light.

Experimentally induced disturbances (i.e., selective

canopy removals) allowed annual algal species to in-

vade th e otherwis e perennial algal assemblage at Still-

water Co ve (Fig. 5). The composition of the understory

(Desmarestia spp. and fleshy red algae) soon began to

resemble th at of nearby kelp forests, which are typified

by greater disturbance. Only under conditions of fre-

quent disturbance m ight this a nnual algal assemblage

be maintained, particularly because the re cruitme nt of

slower-growing perennial s was also high. W itho ut the ir

periodic removal, long-lived perennials become re-es-

tablished, increasing competition for light and reducing

chances for survival of other species.

The fieldwork could not have been accomplished without

the help of diving partners P. Bentivegna, J. Heine, G. Ichi-

kawa, M. Kelly, R. Walker, and especially D. Rose, and R.

Van Wagenen. R. Ogren generously shared his work and ideas

on the ecology of Pterygophora. D. Duggins, J. Estes, M.

Josselyn, J. Oliver, D. Schiel, W. Sousa, G. Van Blaricom,

and S. Woodin provided constructive comments on drafts of

the manuscript. Infrared aerial photographs were provided

by the California Department of Fish and Game and R. Van

Wagenen, and were analyzed by R. Van Wagenen. We aregrateful to the Pebble Beach Corporation for allowing access

to Stillwater Cove. Financial support was provided by the

California Department of Fish and Game and The David and

Lucile Packard Foundation, and field support by Moss Land-

ing Marine Laboratories.

Abbott, I. A,, and G. J. Hollenberg. 1976. Marine algae of

California. Stanford University Press, Stanford, California,

USA.

Andrews, H. L. 1945. The kelp beds of the Monterey region.

Ecology 26:24-37.

Barrales, H. L., and C. S. Lobban. 1975. The comparative

ecology ofMacrocystispyrijera with emphasis on the forests

of Chubut, Argentina. Journal of Ecology 63:657-677.Black, R. 1974. Some biological interactions affecting in-

tertidal populations of the kelp Egregia laevigata. Marine

Biology 28: 189-198.

Breen, P. A,, and K. H. Mann. 1976. Destructive grazing

of kelp by sea urchins in eastern Canada. Journal of the

Fisheries Research Board of Canada 33: 1278-1283.

Connell, J. H. 1975. Some mechanisms producing structure

in natural communities: a model and evidence from field

experiments. Pages 460-490 in M. L. Cody, and J. Dia-

mond, editors. Ecology and evolution of communities.

Belknap Press, Harvard University, Cambridge, Massa-chusetts, USA.

Cowen, R. K. 1979. Trophic interactions within a central

California kelp forest. Thesis. California State University,

Hayward, California, USA.

Cowen, R. K., C. R. Agegian, and M. S. Foster. 1982. The

maintenance of community structure in a central California

giant kelp forest. Journal of Experimental Marine Biology

and Ecology 64: 189-20 1.

Dawson, E. Y., M. Neushul, and R. D. Wildman. 1960.

Seaweeds associated with kelp beds along southern Cali-

fornia and northwestern Mexico. Pacific Naturalist 1: 1-8 1.

Dayton, P. K. 1971. Competition, disturbance and com-

munity organization: the provision and subsequent utili-

zation of space in a rocky intertidal community. Ecological

Monographs 41:35 1-389.- 1975a. Experimental studies of algal canopy inter-

actions in a sea otter dominated kelp community at Am-

chitka Island, Alaska. United States National Marine Fish-

eries Service Fishery Bulletin 73:230-237.

. 19758. Experimental evaluation of ecological dom-

inance in a rocky intertidal algal community. Ecological

Monographs 45: 137-1 59.

Duggins, D. 0. 1980. Kelp beds and sea otters: an experi-

mental approach. Ecology 61:447-453.

Ebert, E. E. 1967. Food habits of the southern sea otter

Enhydra lutris nereis, and ecological aspects of their pop-

ulations and distributional expansion. MRO Report 67- 18,

California Department of Fish and Game, Sacramento, Cal-

ifornia, USA.

. 1968. A food habits study of the southern sea otter,Enhydra lutris nereis. California Department of Fish and

Game 54:33-42.

Estes, J. A., and J. F. Palmisano. 1974. Sea otters: their role

in structuring nearshore communities. Science 185:1058-

1060.

Estes, J. A,, N. S. Smith, and J. F. Palmisano. 1978. Sea

otter predation and community organization in the western

Aleutian Islands, Alaska. Ecology 59:822-833.

Foreman, R. 1977. Benthic community modification and

recovery following intensive grazing by Strongylocentrotus

droebachiensis. Helgolaender Wissenschaftiche Meeresun-

tersuchungen 30:468-484.

Foster, M. S. 19 75 ~.Algal succession in a Macrocystispy-

rifera forest. Marine Biology 32:3 13-329.

- 19756. Regulation of algal community developmentin a Macrocystis pyrifera forest. Marine Biology 32:33 1-

342.

- 1982a. Factors controlling the intertidal zonation

of Iridaeaflaccida (Rhodophyta). Journal of Phycology 18:

285-294.

- 1982b. The regulation of macroalgal associations in

kelp forests. Pages 185-205 in L. Srivastava, editor. Syn-

thetic and degradative processes in marine macrophytes.

Walter deGruyter, Berlin, Germany.

Frye, T. 19 18. The age of Pterygophora californzca. Publi-

cation of Puget Sound Biological Station 2:65-7 1.

Grieg-Smith, P. 1964. Quantitative plant ecology. Second

edition. Butterworth's, London, England.

Harper, J. L. 1977. Population biology of plants. Academic

Press, New York, New York, USA.Hodgson, L. M. 1980. Control of the intertidal distribution



948 DANIEL C. REED AND MICHAEL S. FOSTER Ecology, Vol. 65, No. 3

of Gastroclonium coulteri in Monterey Bay, California. Ma-

rine Biology 57:121-1 26.

Hruby, T. 1976. Observations of algal zonation resulting

from competition. Estuarine and Coastal Marine Science

4:231-233.

Hruby, T., and T. A. Norton. 1979. Algal colonization on

rocky shores in the Firth of Clyde. Journal of Ecology 67:

65-77.

Kimura, R. S. 1980. The effects of harvesting Macrocystispyrifera on understory algae in Carmel Bay, California. The-

sis. California State University, Fresno, California, USA.

Kuhnemann, 0 . 1970. Algunas consideraciones sobre 10s

bosques de Macrocystis pyrijera. Physis (Buenos Aires) 25:

273-296.

Lawrence, J. M. 1975. On the relationships between marine

plants and sea urchins. Oceanography and Marine Biology

Annual Review 13:2 13-286.

Lowry, L. F., and J. S. Pearse. 1973. Abalones and sea

urchins in an area inhabited by sea otters. Marine Biology

23:213-219.

Lubchenco, J. 1978. Plant species diversity in a marine

intertidal community: importance of herbivore food pref-

erence and algal competitive abilities. American Naturalist

112:23-39.

- 1980. Algal zonation in the New England rocky

intertidal community: an experimental analysis. Ecology

611333-344.

Lubchenco, J., and B. A. Menge. 1978. Community devel-

opment and persistence in a low rocky intertidal zone. Eco-

logical Monographs 59:67-94.

Luning, K. 198 1. Photobiology of seaweeds: ecophysiolog-

ical aspects. Proceedings of the International Seaweed Sym-

posium 10:35-55.

McPeak, R. 198 1. Fruiting in several species ofLaminariales

from southern California. Proceedings of the Interna tional

Seaweed Symposium 8:404-409.

Neushul, M. 1965. SCUBA diving studies of vertical dis-

tribution of benthic marine plants. Proceedings of the Ma-

rine Biological Symposium 5:16 1-1 76.

- 197 1. The kelp communi ty of seaweeds. Nova Hed-

wigia 32:265-267.

Nicotri, M. E. 1977. Grazing effectsof four marine intertidal

herbivores on the microflora. Ecology 58:1020-1032.

Pace, D. 198 1. Kelp community development in Barkley

Sound, British Columbia following sea urchin removal.

Proceedings of the International Seaweed Symposium 8:

457-463.

Paine, R. T., and R. L. Vadas. 1969. The effects of grazing

by sea urchins, Strongylocentrotus spp. on benthic algal

populations. Limnology and Oceanography 14:7 10-7 18.Pearse, J. S., and A. H. Hines. 1979. Expansion of a central

California kelp forest following the mass mortality of sea

urchins. Marine Biology 51:83-9 1.

Reed, D. C. 198 1. The effects of competition for light and

space on the perennial algal assemblage in a giant kelp

(Macrocystis pyrifera) forest. Thesis. San Francisco State

University, San Francisco, California, USA.

Rosenthal, R. J., W. D. Clark, and P. K. Dayton. 1974.

Ecology and natural history of a stand of giant kelp, Mac-rocystis pyrifera, off Del Mar, California. United States Na-

tional Marine Fisheries Service Fishery Bulletin 72:670-

684.

Simpson, J. 1972. The geology of Carmel Bay, California.

Thesis. United States Naval Postgraduate School, Monte-

rey, California, USA.

Sokal, R. R., and F. J. Rohlf. 1969. Biometry. W. H. Free-

man, San Francisco, California, USA.

Sousa, W. P. 1979a. Experimental investigation of distur -

bance and ecological succession in a rocky intertidal algal

community. Ecological Monographs 49:227-254.

- 19796. Disturbance in marine intertidal boulder

fields; the nonequilibrium maintenance of species diversity.

Ecology 60:1225-1239.

Velimirov, B., and C. L. Griffiths. 1979. Wave-induced kelp

movement and its importance for community structure.

Botanica Marina 22: 169-1 72.

Wild, P. W., and J. A. Ames. 1974. A report on the sea

otter Enhydra lutris L. in California. California Department

of Fish and Game Marine Resources Technical Report 20:

1-93.

reed and foster 1984 effect of canopy shading on recruitment

Documents