The effects of harvesting Macrocystispyrffera on the algal assemblage in a giant kelp forest

R. S . Kimura' & M . S. FosterMoss Landing Marine Laboratories, P.O. Box 223, Moss Landing, CA 95039, U.S.A .I Present address : TERA Corporation, Marine Studies Group, P.O. Box 400, Avila Beach, CA 93424,U.S.A .

Keywords: seaweed, Macrocystis, harvesting, understory algae, light, recruitment, central California

Introduction

It is commonly observed that the abundance ofunderstory algae, including juvenile stages of sur-face canopy kelps, is reduced within stands of adultMacrocystis pyrifera (Dawson et al. 1960; Neushul1965, 1971 ; Rosenthal et al. 1974; Foster 1975,1982). Surface canopies ofM. pyrifera can reducebottom light to < 1 % of the surface intensity (Neu-shul 1971 ; Reed & Foster 1984), and experimentalremoval of this canopy can result in increasedabundance of understory plants (Pearse & Hines1979; Reed & Foster 1984) .Commercial harvesting removes M. pyrifera can-

opy tissue and thus increases bottom irradiation(Neushul 1971). Besides altering the understory flo-ra, including the abundance of M. pyrifera recruits,the continued removal of photosynthetic tissue mayaffect the survivorship of adult M. pyrifera, particu-larly if holdfast growth is reduced (Miller & Geibel1973) . North (1957) observed the bottom vegeta-tion in an area one year after commercial harvest-ing, and noted no differences in plant abundancescompared to adjacent, uncut areas . However, in anearby area where plants were cropped continuous-ly for two years by boat propellers, he found morejuvenile M. pyrifera and foliose red algae . Miller &Geibel (1973) hand-cut the same giant kelp plantsfive times in 14 months . This resulted in the com-plete loss of these plants the following winter, but asin North's study above, this repetitive removal ofsurface canopy also enhanced the abundance ofjuvenileM. pyrifera and foliose red algae relative toadjacent, uncut areas .

Portions of Carmel Bay kelp forest have been

Hydrobiologia 116/117, 425-428 (1984) .© Dr W. Junk Publishers, Dordrecht . Printed in the Netherlands .

harvested once per year since 1973 (R . McPeak,Kelco Co., pers . commun .). Harvesting normallyoccurs in summer when canopies are most luxu-riant and seas are calm . In this study, we comparedchanges in understory algal abundance and re-cruitment in an unharvested area with those in twoother areas harvested at different times of the year .

Methods

The Carmel Bay kelp forest (36° 33'N, 121 0 51 'W)has a total summer surface area of approximately100 ha with M. pyrifera frond densities of 2-3 m -2(Kimura 1980). Algal abundance was determinedduring one year (June 1975 to May 1976) in three30-m radius (- 0.3 ha) study areas arranged in atriangle so the centers were - 100 m apart . Thesesites were established in depths ranging from 15 to18 m, and in a location known to have not beenpreviously harvested. One area was harvested insummer (June) by a commercial harvesting ship .Divers harvested a second area in fall (October) byhand to a depth of 1 .2 m below the surface, tosimulate the effects of commercial cutting . A thirdunharvested area was used to compare naturaltrends with those in the harvested areas . The swathcut by a commercial ship is 8 m wide, but thenumber of adjacent swaths cut is highly variable(D .C . Barilotti, Kelco Co ., pers. commun .). Thus,our areas exceeded the minimum possible width,and were much larger than the 20-m width suggest-ed by Barilotti (pers . commun.) as necessary toeliminate shading by the surrounding plant canopy .

Within each area, the densities of Macrocystis

426

pyrifera, Pterygophora californica, and other largealgae that could be distinguished as individuals,were determined at 1- to 3-month intervals in 20 to23 permanently marked 10-m 2 quadrats initiallypicked at random. Juvenile M. pyrifera (< I mlong) and P. californica (lacking sporophyll scars)were distinguished from adults . Percent cover ofthese and other macroalgae was measured duringeach sampling period using randomly distributedpoint quadrats . A single quadrat consisted of a line3 m long with ten randomly spaced weights. Allplants intersecting an imaginary line perpendicularto the substratum through a weight were noted .Sixty to 120 quadrats were sampled during eachsurvey in each study area . Differences in abundancewithin the harvested and control areas were testedover time (assuming independence) for significance(p < 0.05) using Kruskal-Wallis tests (Sokal &Rohlf 1969) followed by Newman-Keuls multiplecomparisons (Zar 1974) .

Percent cover and overall configuration of theM. pyrifera surface canopy over the entire kelpforest from 1973 to 1979 were estimated by eye fromuniform-size projections of infrared aerial photo-graphs supplied by the State of California Depart-ment of Fish and Game. The canopy cover wasgreatest during summer 1975, and was consideredto be 100%. All other estimates were made relativeto the cover on this date .

Results

Within the study areas, a total of 27 algal taxawere encountered (Table 1) . All species in the har-vested areas were also found in the control area .With the exception of juvenile M. pyrifera andPterygophora californica, seasonal changes in plantdensity and percent cover for all taxa and devel-opmental stages were slight, and were similar be-tween treatments. Figure 1 illustrates this for thecombined category of total understory cover ; datafor individual species are given in Kimura (1980) .

Seasonal changes in densities of juvenile M. py-rifera and P. californica in each study area areshown in Figure 2 . Some of the original quadratsmarked in each area could not be relocated, so thenumber of replicates varied between, and oncewithin, areas . Natural recruitment of these kelpsoccurred in spring and early summer . In the areaharvested in summer, there was an additional and

Table 1 . Algal taxa encountered in the study areas . Identifica-tion and authorities from Abbott and Hollenberg (1976) .

ChlorophytaDerbesia marina (Lyngb .) Sol .

PhaeophytaCystoseira osmundacea (Turn .) C . AgDesmarestia ligulata (Lightf.) Lamour . var . ligulataDesmarestia ligulata var. firma (C . Ag .) J . Ag.Dictyota binghamiae J . Ag .Macrocystis pyrifera (L .) C . Ag .Pterygophora californica Rupr .

RhodophytaBossiella californica (Dec .) Silva ssp. schmittii (Manza)

Johans .Bossiella spp .Botryoglossum farlowianum (J . Ag.) De ToniCalliarthron tuberculosum (Post . & Rupr.) Daws .Callophyllis flabellulata Harv .Coralline crustFauchea laciniata J. Ag .Fryeella gardneri (Setch .) Kyl.Laurencia spectabilis Post. & Rupr .Laurencia subopposita (J . Ag .) Setch .Nienburgia andersoniana (J . Ag.) Kyl.Noncoralline crustOpuntiella californica (Fart .) Kyl .Pikea californica Harv. .Plocamium cartilagineum (L .) Dix .Polyneura latissima (Harv .) Kyl .Polysiphonia spp .Prionitis lanceolata (Harv.) Harv .Rhodoptilum plumosum (Harv . & Bail .) Kyl .Rhodymenia spp .Schizymenia pacifica (Kyl.) Kyl .Weeksia reticulata Setch.

1002001

0

200100

200l1001

0J

CONTROL

SUMMER HARVEST

FALL HARVEST

1J A S 0 N D J F M A M

975 1976Fig. 1 . Total understory algal cover in the three study areas .Arrows indicate time of Macrocystis pyrifera harvest . Data aremean cover per point quadrat ; n = 60-120 per survey .

NE

O

3.02.0

1 .0-0

9.0810-7.0-6,0-5.0-4.0-3.02.0-1 .0-0

2.0-1 .0-0

50

l

CONTROL N•23

SUMMER HARVEST N •20

FALL HARVEST N•2 1

∎

4A S 0 N D J FM A M

19751976

Fig. 2 . Mean density ± 95% confidence intervals of Macrocystispyrifera (solid line), and Pterygophora californica (broken line)juveniles in the three study areas . Arrows indicate time of har-vest ; *, n = 5 .

significantly greater recruitment of both species thefollowing winter. However, many of these plantswere soon lost during winter storms . In the areaharvested in fall, recruitment times of both specieswere also altered, but not so dramatically ; juvenilesappeared approximately one month earlier thanthose in the unharvested area (Figure 2) .

Seasonal changes in M. pyrifera surface canopycover are shown in Figure 3 . As in most other cen-tral California kelp forests (Miller & Geibel 1973 ;Gerard 1976; Foster 1982), the canopy in CarmelBay undergoes an annual cycle of summer peakabundance, followed by winter reduction due to

aW

>00W

Q

FWSSFWSSFWSSFWSSFWSSFWSW 1973--1974--1975--1976--1977--1978--1979W

Fig. 3 . Seasonal changes in the percent cover of the Macrocystispyrifera surface canopy over the Carmel Bay kelp forest. FW WS= autumn, winter, spring, summer .

removal of fronds and plants during storms . Therehave been no obvious changes in the size or con-figuration of the canopy since 1973 .

Discussion

The results of this one-year study suggest that theonce per year partial harvest of the M. pyriferacanopy in the Carmel Bay kelp forest has no short-term direct or indirect effects on the algae otherthan enhancing kelp recruitment. The variations inrecruitment times in the harvested areas suggestthat M. pyrifera and Pterygophora californicarecruitment is greatly affected by light, and thatspores and/or `dormant' gametophytes are prob-ably available throughout the year . These effects onthe recruitment of M, pyrifera are consistent withthe harvesting study of Miller & Geibel (1973), theboating channel observations of North (1957), andthe kelp canopy removal experiments by Pearse &Hines (1979) and Reed & Foster (1984). In addi-tion, North (1957), Rosenthal et al. (1974), andGerard (1976) found that, under natural condi-tions, M. pyrifera recruitment occurred only aftersurface canopies were thinned by storms .

I n the present study, the most dramatic effect wasobserved in the area harvested in summer where, bythe following winter, there was an additional andlarge recruitment of kelp . Thus, harvesting imme-diately enhanced recruitment, but later removal bystorms reduced the differences in kelp abundancebetween harvested and nonharvested areas . Fur-thermore, harvesting as currently done in this kelpforest has not altered either the seasonal cycle of thecanopy or the area and configuration of the entireforest. Rosenthal et al. (1974) suggested that peri-odic recruitment combined with high survivorshipcreates a more multi-aged M. pyrifera populationthat may be less susceptible to catastrophic lossduring storms . Winter storm intensity varies in cen-tral California (Foster 1982), and it is possible thatthe winter recruits in the summer-harvested areasmay survive during certain years . If so, this maycontribute to a more varied age structure of the M.pyrifera population .

These results suggest that the adult mortality ofM. pyrifera and subsequent increases in the redalgal understory observed by Miller & Geibel(1973) probably reflect these authors' admittedly

427

428

high harvesting rates . The differences in understoryred algal response between our study and that ofMiller & Geibel (1973) may also be due, in part, totime and site differences . The studies were done indifferent years, and the results may partially reflectsome unknown, long-term variation in algal re-cruitment and growth . In addition, the latter studywas done at a shallower site without an understorycanopy of P. californica . The increased irradiationas a result of harvesting in shallower water mayhave been greater at Miller & Geibel's (1973) site .As suggested by Foster (1982) and shown by Reed& Foster (1984), light reduction by P. californicacan also greatly reduce the recruitment and growthof bottom cover red algae, even in the absence of aM. pyrifera surface canopy . Therefore, site-specificdifferences in community structure, as well as har-vesting extent, rate, and timing, should be consid-ered in assessing the effects of harvesting on par-ticular kelp forest communities .

Acknowledgements

We thank D. Hunt, J. Houk, K. McCleneghan,R . McPeak, D. Miller, and T . Thompson for theiradvice and assistance . J . Heine and D. Schiel madehelpful comments on the manuscript . The state ofCalifornia Department of Fish and Game gener-ously provided field support . Financial support forthe research was provided by NOAA, National SeaGrant College Program, under Grant No . 04-6-158-44021, Project No. R/CZ-21, California Sea GrantCollege Program, and for presentation of the paperby Kelco Co .

References

Abbott, I . A . & G . J . Hollenberg, 1976 . Marine Algae of Cali-fornia . Stanford University Press, Stanford, 827 pp .

Dawson, E . Y ., M . Neushul & R . D. Wildman, 1960 . Seaweedsassociated with kelp beds along southern California andnorthwestern Mexico . Pac. Nat . I : 1-81 .

Foster, M . S ., 1975 . Regulation of algal community develop-ment in a Macrocystis pyrifera forest. Mar. Biol. 32 :331-342 .

Foster, M . S., 1982 . The regulation of macroalgal associations inkelp forest . In L. Srivastava (ed .), Synthetic and DegradativeProcesses in Marine Macrophytes. Walter de Gruyter & Co .,Berlin : 185-205 .

Gerard, V. A ., 1976 . Some aspects of material dynamics andenergy flow in a kelp forest in Monterey Bay, California .PhD Thesis, Univ. Calif., Santa Cruz, 173 pp.

Kimura, R. S ., 1980 . The effects of harvesting Macrocystispyrifera on understory algae in Carmel Bay, California . MAThesis, Calif. St. Univ ., Fresno, 108 pp .

Miller, D . J . & J . J . Geibel, 1973 . Summary of blue rockfish andlingcod life histories; a reef ecology study; and giant kelp,Macrocystis pyrifera, experiments in Monterey Bay, Cali-fornia . Fish Bull . 158, St . Calif. Dept . Fish & Game, Sacra-mento, 137 pp .

Neushul, M ., 1965 . SCUBA diving studies of vertical distribu-tion of benthic marine plants. Proc. mar. biol. Symp . 5 :161-176 .

Neushul, M ., 1971. Submarine illumination in Macrocystisbeds . In W . J . North (ed .), The Biology of Giant Kelp Beds(Macrocystis) in California . Beih. Nova Hedwigia 32, J .Cramer, Lehre: 241-254 .

North, W . J ., 1957 . Cutting of kelp . In W . J . North (ed .), KelpInvestigations Program Annual Report for the Period I July1956-30 June 1957 . Univ . Calif. Inst . Mar. Resour., La Jolla :20-24 .

Pearse, J . S . & A. H. Hines, 1979 . Expansion of a centralCalifornia kelp forest following the mass mortality of seaurchins . Mar. Biol . 51 : 83-91 .

Reed, D . C . & M . S . Foster, 1984 . The effects of canopy shadingon algal recruitment and growth in a giant kelp forest .Ecology 65: 937-948 .

Rosenthal, R . J ., W . D . Clark & P . K . Dayton, 1974 . Ecologyand natural history of a stand of giant kelp, Macrocystispyrifera, off Del Mar, California. Fish. Bull . 72 : 670-684 .

Sokal, R . R . & F. J . Rohlf, 1969 . Introduction to Biostatistics .W. H. Freeman & Co . Press, San Francisco, 375 pp .

Zar, J . H ., 1974 . Biostatistical Analysis . Prentice-Hall, Inc .,Englewood Cliffs, 620 pp .