Some Ecological Effects of Harvesting Macrocysüs integrifolia

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1 Dniehl and Breen: Some ecological eflects of harvesting Macrocysüs integrifolia 97 Botanica Marina Vol. XXIX, pp. 97-3, 986 Some Ecological Effects of Harvesting Macrocysüs integrifolia L. D. Druehl and P. A. Breen* Department of Biological Sciences, Simon Fräser University, Burnaby, B. C., V5A S6, Canada and * Department Fisheries and Oceans, Fisheries Research Branch, Pacific Biological Station, Nanaimo, B. C. V9R 5K6, Canada (Accepted 29 November 985) Abstract This field study, conducted for 7 months in Barkley Sound, British Columbia, Canada, examined the effect of harvesting the kelp Macrocysüs integrifolia Bory on some conspicuous elements of understory biota. M. integrifolia was completely removed from one plot, partially removed from one plot, and left undisturbed in a control plot. At the end of the study period, the relative abundance of the brown alga Desmarestia ligulata and the green alga Ulva sp. had increased in the harvested plots relative to the control plot. Harvesting, and the resulting changes in understory plant composition, were reflected in the relative abundances of drifting plant fragments available to herbivores. In harvested areas, brown algal fragments other than M. integrifolia (mostly D. ligulata) dominated during the winter; whereas in the unharvested site M. integrifolia dominated the fragment pool throughout the year. None of the herbivores studied (Strongylocentrotus franciscanus, S. droebachiensis, Parastichopus californicus, and Haliotis kamtschatkana} decreased their density in response to harvesting. Gonadal indices of the two sea urchins were lower in the harvested areas, which indicated that these grazers were less well fed. e conclude that removal of M. integrifolia altered the abundance of both understory plants and drifting fragments. These alterations change the forage base for associated herbivores to one which may be less nutritious than in unharvested situations. Introduction Several invertebrate species of potential economic value inhabit the benthic region of commercially harvested kelp beds. The purpose of this study was to measure the responses of four selected invertebrate species to two strategies of harvesting the large kelp Macrocysüs integrifolia Bory. The four species were the red sea urchin, Strongylocentrotus franciscanus (A. Agassiz); the green sea urchin, S. droebachiensis (Muller); the sea cucumber Parastichopus californicus (Stimpson); and the northern abalone, Haliotis kamtschatkana Jonas. The sea cucumber is in part a detritus feeder (Cameron and Fankboner 984); the Present Address: Fisheries Research Centre, Greta Pt., Box 297, ellington, New Zealand sea urchins and abalone are primarily herbivores but may also use detritus äs food. The importance of drifting macrophyte fragments äs food for abalone and sea urchins is well documented (e. g. Cox 962, Irvine 973, see reviews by Mottet 976, 978). e hypothesized that periodic harvests of Macrocysüs will affect these invertebrates in two ways. First, harvesting large quantities of plant material will reduce the amount of food material available to herbivores. Second, dimunition of the Macrocysüs canopy will result in changes in species composition of understory macrophytes, in turn changing the quality of food available to resident invertebrates. This Suggestion is supported by Foster (975), who showed that a canopy of Macrocysüs pyrifera (L.) Botanica Marina / Vol. XXIX / 986 / Fase. 2 Copyright 986 alter de Gruyter Berlin New York

2 98 Druehl and Breen: Some ecological effects of harvesting Macrocystis integrifolia C. Ag. can restrict plant cover and species diversity in the understory. Further, Dayton (97, 975) has demonstrated changes in Community species composition resulting from kelp canopy removal. e tested these hypotheses by examining, in experimentally harvested and control areas, changes in invertebrate density, understory plant density and the density of drifting plant fragments. At the end of the study period, gonadal indices of sea urchins inhabiting the harvested and unharvested areas were compared. Gonad indices of sea urchins reflect both the quantity and the quality of food available (Lees 97, Vadas 977, Larson et al 98). This experimental System was designed to monitor a chain of events leading from the harvest of Macrocystis through predicted changes in the understory flora and concurrent changes in the species compositions of fragments to possible responses of herbivorous invertebrates. Should the experimental harvest stress (starve) the herbivores, two possible responses might be expected stay and starve or emigrate. Materials and Methods Three plots, each extending 25 m along the shore, were established on a west-facing shore of Trevor Channel (48 5.4'N; 25 8.') in Barkley Sound, British Columbia, Canada. The plots were separated from each other by m wide Strips (Fig. ). Four permanent transect lines extending from.4 m above SHOREARD SEAARD Fig.. Schematic illustrating the positioning of the transect lines between +.4 and 6.5 from tide; the upper and lower limits of Macrocystis integrifolia äs observed in June 977; the location of the break in' Substrate type from essentially continuous rock to boulders with some sand (A); and the general location of the.25 m 2 quadrats (B). to 6.5 m below tide level were placed within each plot at intervals of 5 m. In one plot (total harvest) all M. integrifolia plants were removed 3 4 June 977, and individuals subsequently arising in the plot were removed monthly. In a second plot (partial harvest) M. integrifolia plants were cut at the surface on 5 June 977 when tide levels was.9 l.lm above tide level. This partial harvesting was repeated 8 August 977 and 3 May, 23 July and 26 October 978 at the same tide level. A third (control) plot was never harvested. The size of these plots and the effort required to maintain them precluded to the possibility of establishing of replicates. Therefore, we could not discuss our data in inferential statistical terms. Rather, we have followed Hurlbert's (984) suggestions of presenting mean values and their Standard deviations only. Densities of selected understory macrophytes were measured three time (23 June and 9 August 977, 2 August 978) along the same permanent transect line in each treatment plot. All individuals were counted in l m 2 quadrats placed sequentially along both sides of each permanent transect line in each plot. Densities were measured from.3 3.8m below tide level; this was the vertical ränge of M. integrifolia. Because of the great numbers of Ulva sp., percent cover in each treatment was estimated visually on 6 August 977 in randomly placed quadrats, (.25 m 2 ) in each plot. To estimate the abundance of drifting plant fragments, seven permanent quadrats (.25 m 2 ) were located seaward of each plot (Fig. l B). At monthly intervals from August 977 through October 978, all fragments found within the permanent quadrats were collected by hand. The efficiency of the hand harvest method was tested after the first harvest by vacuuming the quadrats with an airlift. The material reclaimed by the airlift weighed less than l % of the hand-harvested material; therefore future harvests were made by hand collection alone. Plant fragments were sorted into six groups: Rhodophyta, Chlorophyta, M. integrifolia, remaining Phaeophyta, sea grasses (Phyllospadix scouleri Hook and Zostera marina L.), and terrestrial plant material. Carbon and nitrogen content and C/N ratios (atomic) for the different fragment classes were determined from the seven quadrats in the control plot on 26 August 977. Dried fragments were pulverized and analysed with a Perkin-Elemer Model 24 Elemental Analyser. \ Residence time of drifting plant fragments in the permanent quadrats was estimated by placing ten rectangular pieces (3.5 3 cm) of Desmarestia ligu- Botanica Marina / Vol. XXIX / 986 / Fase. 2

3 Druehl and Breen: Some ecological effects of harvesting Macrocystis integrifolia 99 lata (Lightf.) Lamour. and M. integrifolia in two quadrats in each plot at low tide, then cotmting those remaining on the following high tide, approx. 6 h later. Densities of the four selected invertebrate species were measured monthly from May 977 through September 978, in the same manner described above for understory plants, but from.4m above to 6.5m below tide level. Only those animals visible without disturbing the Substrate were noted; rocks were not moved but Vegetation was brushed aside during observations. Sea urchin gonad indices were determined on 8 27 January 979 using the method of Kramer and Nordin (975), who found that red and green sea urchins have maximum gonad weight at that time of year (Kramer and Nordin 975, 978). Results Densities of the six conspicuous understory macrophytes in the three treatment plots are shown in Table I for three dates: just after harvesting (23 June 977), six weeks after harvesting (9 August 977), and one year after that (2 August 978). There was considerable variance within treatments and between treatments. Of the six macrophytes studied only Desmarestia ligulata showed a consistent change in plant density: the tendency was for greater densities in the harvested plots. Following initial harvesting, dense mats of Ulva sp. appeared in the harvested plots. By August 977 the three plots showed different percent covers (Table II), with the greatest cover in the totally harvested plot. Table I. Densities (plants m~ 2 (n = 22) plots. ± l S.D.) of selected macrophytes on the control (n = 22), partial (n = 26) and total harvest 23 June August August 978 Pterygophora californica Rupr..4 ± ± ±.28.6 ± ± ± Costaria costata (Turn.) Saunders.9 ± ±..77 ± ± ± ± Laminaria groenlandica Rosenv ± ± ± ± ± Alaria marginata Post & Rupr..59 ±.3.52 ±.8.95 ± ± ±.2.5 ± ± 2.98 Desmarestia ligulata (Lightf.) Lamour ± ± ± ± ± ± ± Macrocystis integrifolia Bory.55 ± ± ± ± ±.73 Table II. Mean percent cover (± S.D.) of Ulva sp. on the control and harvested plots, 6 August 977 (n =,.25 m 2 quadrats). harvest harvest % cover ± Botanica Marina / Vol. XXIX / 986 / Fase. 2

4 Druehl and Breen: Some ecological effects of harvesting Macrocystis integrifolia Tablelll. Mean dry weight (g..25 m~ 2 + l S.D.) of plant Fragments collected monthly from the three treatment sites for October 977-March 978 and October 978 (), (n = 7) and August-September 977 and April - September 978 (S), (n = 8). Fragment type Season harvest Treatments harvest Phaeophyta (excluding Macrocystis) S ± ±.2.7 ± Q S53 ±.659 Macrocystis 's ± ±.2.25 ± ±.6.32 ±.93 Rhodophyta S ± ± Chlorophyta.5 ± ±.5 Sea grasses s s ±.62.4 ± ±.48.2 ±.22. ±. Terestrial plants s.25 ± ±.9.6 ±.9.2 ± ±.7 fragments s.596 ± ± ± ±.822 M. integrifolia and the remaining Phaeophyta (mostly D. ligulata) comprised most of the weight of plant fragments (Table III). The other four plant groups contributed little biomass. Biomass of Macrocystis, other Phaeophyta, Chlorophyta and the total fragments all showed a seasonal trend, with greater amounts during April through September than from October through March (Table III; Fig. 2). The Rhodophyta, seagrass and terrestrial plant groups showed no seasonal change. Terrestrial plant fragments were mostly western red cedar (Thuja plicata Donn.). In summer and winter M. integrifolia was more abundant on the control site than on the other sites (Table III). fragments and other Phaeophyta were most abundant on the control site during summer and on the total harvest site during winter. Movement of M. integrifolia and D. ligulata fragments from test quadrats indicated short residence times (Table IV). After one tide change, less than 3% of the test fragments remained where they had been placed. Direct observations indicated alongshore and off-shore movements. s er xv. Phaeophyta (Excluctng M. integrifoli Macrocystis integrifolia, ^=^^^^^^^ A Harvest o Harvest. - / \ The carbon and nitrogen content of each plant fragment type in the control area in August 977 is shown in Table V. Most of the carbon and nitrogen came from the Phaeophyta including M. integrifolia, which together contributed 87% of the total carbon and 92% of the nitrogen. The lowest C/N ratio was seen in the Chlorophyta. The next lowest ratio was seen in M. integrifolia and the remaining Phaeophyta. There was considerable variance in invertebrate densities within plots and between plots (Table VI). The increased density of Strongylocentrotus franciscanus in the totally harvested plot and the concurrent decrease of its densities in the other two plots äs observed one year following harvest suggests a harvesting response for this species. Fig. 2. The mean standing crop of selected plant fragments äs observed approximately monthly from 7 August 977 to 27' October 978 in the total harvest, partial harvest and control' plots (n = 7). Nutritional state of sea urchiris, äs measured by the gonadal indices of S. franciscanus and S. droebachiensis in January 979, are shown in Table VII. In both species, gonadal index was highest in the control Botanica Marina / Vol. XXIX / 986 / Fase. 2

5 Druehl and Breen: Some ecological effects of harvesting Macrocystis integrifolia Table IV. Movement of plant fragments from.25 m 2 quadrats between low slack water and high slack water, and tidal ränge over the observation period (9 August 978). Values are mean number of fragments remaining in two quadrats at high slack water; the initial number of fragments in each quadrat was. August 9 Macrocystis integrifolia August August August 9 Desmarestia ligulata August August harvest harvest Tidal ränge Table V. Mean dry weight (± S.D.) and mean carbon and nitrogen content, äs percentage of dry weight (+ S.D.), for different fragment types collected from seven.25 m 2 quadrats located within the control site on 26 August 977. If the sample size (n) is less than 7 the particular fragment type was not present in all quadrats. Fragment type (n) Dry weight g.25 m- 2 N % of dry weight C N mg.25 m- 2 C C/N (Atomic) Macrocystis integrifolia.69 ± ± ± ± 2.4 Phaeophyta (excluding M. integrifolia).46 ± ± ± ± 4.9 Rhodophyta Sea grasses Terrestrial plants Chlorophyta fragments (6) (6) () ±.5 ±.24 ± ± ± ± Table VI. Mean pre- (2 May 977) and post-harvest (3 May 978) densities (number m~ 2 ± l S.D.) of the four studied invertebrates in the three research plots (n = 8). Treatment partial harvest harvest Stronglycocentrotus droebachiensis 2 May May ± ± ± S. franciscanus 2 May May ± ±.3 ±..58 ± Parastichopus californicus 2 May May ±.2 : ± ± Haliotis kamtschtkana 2 May May ±..5 ±.3.3 ±.3.6 ± Table VII. Gonadal indices (gonad wet weight/drained fresh body weight ± S.D.) of two species of Strongylocentrotus äs observed during January 979 on the three sites F (female), M (male). (n) Treatment (n) (n) S. droebachiensis () F () M M + F (2) ±.4 (2) (9) (2) ±.7.9 ±.9 (8) (3) (2).7 ±..4 ±.5.5 ±.7 S. franciscanus (3) M M + F (2) ±.4 (H) (9) (2) ±.3 (2) (28) Botanica Marina / Vol. XXIX / 986 / Fase. 2

6 2 Druehl and Breen: Some ecological effects of harvesting Macrocystis integrifolia plot. Gonad colour (also an indicator of nutritional state (Mottet 976)) was lighter in both species in the control plots and darker in the harvested plots. Lighter colour implies a better nutritional state. Discussion Our first hypothesis, that M. integrifolia harvesting will reduce the amount of plant material available to herbivores, was supported by the overall decrease in total plant fragment abundance in the harvested plots in contrast to the control plot. M. integrifolia and other Phaeophyta were the largest contributors to the pool of drifting plant fragments; they were less abundant in the total harvest plot in the summer. M. integrifolia was also less abundant in the total harvest plot in the winter. The results also supported our second hypothesis, that removal of the M. integrifolia canopy might lead to altered Community structure of the understory, in turn leading to changes in the quality of food for herbivores. Desmarestia ligulata, and Ulva sp. were more abundant in the harvested plots following harvesting than in the control plots. Ulvoids, which are an early form in marine macrophyte succession (Vadas 968, Lee 966, Sousa 979) were probably able to dominate after removal of the M. integrifolia canopy increased the amount of light reaching the bottom. Foster (982) noted that the abundance of D. ligulata in California increased when the canopy of M. pyrifera decreased. He suggested that this was a response to increased illumitation. M. integrifolia plants occupied little primary space in the experimental plots, so it seems unlikely that the increased ulvoid and Desmarestia cover following harvesting was a response to newly available free primary space. Representatives of the Chlorophyta had the lowest C/N ratio of any of the algae found in this study. Russell-Hunter (97) suggests that plant materials with lower C/N ratios have higher nutritive value. However, Vadas (977) showed that sea urchins have a relatively low preference for ulvoids compared with other algae; and that ulvoids are associated with lower assimilation and growth rates than the preferred food species. In any case, ulvoids formed only a small part of the drifting plant fragment pool. Thus it appears that, in the short term at least, removal of the M. integrifolia canopy appears to have decreased the quantity and quality of food available to herbivores. Larson et al. (98) examined the relation between diet and gonadal index in S. droebachiensis in the laboratory. They found this species to be a highly selective feeder, whose gonadal index reflected food quality. Thus the lower gonadal indices in the sea urchins in the harvested plots indicate that these herbivores were not äs well fed compared with those in the other two plots. Differences in gonad colour, although not quantified, also support this. However, we cannot attribute this nutritional response to just a change in food quantity or quality. The lower gonadal indices may have resulted from a combination of these. The short residence times of test plant fragments placed in permanent quadrats suggest that the drifting material is washed away quickly. Although we observed differences in fragment biomass among treatment plots, it seems clear that plant parts sloughed off or otherwise lost from a point on the shore must be carried away from that point. Conversely, a totally harvested treatment plot of the size used in this study probably received considerable production from intact kelp beds nearby. However, our plant fragment data demonstrated distinctive differences between the plots consistent with the treatments. Under conditions of commercial harvesting, where many hectares of plant canopy would be removed, differences in drifting plant fragment abundance and herbivore nutrition would be greater than we observed here. Invertebrate densities changed little. Increased red sea urchin density in the total harvest plot may have been a direct response to decreased kelp density. Low (975) suggests that kelp mechanically excludes sea urchins, and that red sea urchins will invade an area from which kelp has been removed. Numerous processes may regulate the macroalgal species composition of Macrocystis forest (Foster 975, 982). In this study, harvesting was implicated in the understory macrophyte changes observed. However, other processes were clearly in Operation. This was demonstrated by temporal changes in plant densities on the control plot (Table I). Earlier studies on M. pyrifera indicate that the frequency of harvesting may influence the understory composition. Kimura and Foster (984) noted that once per year harvests had no measurable effect on understory species structure; whereas Millar and Geibel (973) noted understory changes concommitant with frequent harvesting. Botanica Marina / Vol. XXIX / 986 / Fase. 2

7 Druehl and Breen: Some ecological efiects of harvesting Macrocystis integrifolia 3 Acknowledgements M, Shivji and M. Stanhope conducted all field observations and D. Parker assisted occasionally. K. Lloyd assisted in preparation of the manuscript. This research was funded by the Canadian Department of Fisheries & Oceans and conducted at the Bamfield Marine Station. References Cox, K California abalones, family Haliotidae. Fish. Bull. Calif. 8: -33. Cameron, J. L. and P. V. Fankboner Tentacle structure and feeding processes in life stages of the commercial sea cucumber Parastichopus californicus (Stimpson). /. Exp. Mär. Biol. Ecol. 8: Dayton, P. K. 97. Competition, disturbance, and Community organizations: the provision and subsequent utilization of space in a rocky intertidal Community. Ecol. Monogr. 4: Dayton, R K Experimental studies of algal canopy interactions in a sea otter-dominated kelp Community at Amchilka Island, Alaska. Fish. Bull. 73: Foster, M. S Regulation of algal Community development in a Macrocystis pyrifera forest. Mär. Biol. 32: Foster, M. S The regulation of macroalgal associations in kelp forest. In: (L. Srivastava, ed.) Synthetic and Degradative Processes in Marine Macrophytes. alter de Gruyter, Berlin, New York. pp rhurlbert, S. H Pseudoreplication and design of ecological field experiments. Ecol. Monogr. 54: Irvine, G. V The effect of selective feeding by two species of sea urchins on the structure of algal communities. M. Sc. Thesis, University of ashington, Seattle, ashington, USA. 68 pp. Kimura, R. S. and M. S. Foster The effects of harvesting Macrocystis pyrifera on the algal assemblage in a giant kelp forest. Hydrobiologia 6/7: Kramer, D. E. and D. M. A. Nordin Physical data from a study of size, weight and gonad quality for the red sea urchin (Strongylocentrotus franciscanus [Agassiz]) over a one-year period. Fish. Res. Bd. Can. MS Rept 272: 9. Kramer, D. E. and D. M. A. Nordin Physical data from a study of size, weight and gonad quality for the green sea urchin (Strongylocentrotus droebachiensis) over a one-year period. Fish. Mär. Serv. MS Rept. 476: 68. Larson, B. R., R. L. Vadas and M. Keser. 98. Feeding and nutritional ecology of the sea urchin Strongylocentrotus droebachiensis in Maine, USA. Mär. Biol. 59: Lee, R. S. K Development of marine benthic algal communities on Vancouver Island, British Columbia. In: (R. L. Taylor and R. A. Ludwig, eds) The Evolution of Canada 9 s Flora. Univ. Toronto Press, Toronto, Canada. pp. 2. Lees, D. C. 97. The relationship between movement and available food in the sea urchins Strongylocentrotus franciscanus and Strongylocentrotus purpuratus. M. Sc. Thesis, San Diego State College, San Diego, USA. 9 pp. Low, C. J The effect of grouping in Strongylocentrotus franciscanus, the giant red sea urchin, on its population biology. PhD. Thesis, University of British Columbia, Vancouver, Canada. 6pp. Miller, D. J. and J. J. Geibel Summary of blue rockfish and lingcod life histories; a reef ecology study; and giant kelp, Macrocystis pyrifera, experiments in Monterey Bay, California. Fish. Bull. Calif. 58: -37. Mottet, M. G The fisheries biology of sea urchins in the family Strongylocentrotidae. ash. State Dept. Fish. Tech. Rept. 2: -66. Mottet, M. G The fisheries biology of abalones. ash. State Dept. Fish. Tech. Rept. 37: -8. Russell-Hunter,. D. 97. Aquatic productivity: An Introduction to Some Basic Aspects of Biological Oceanography and Limnology. MacMillan Co., London. 36 pp. Sousa,. P Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol. Monogr. 49: Vadas, R. L The ecology of Agarum and the kelp bed Community. PhD. Thesis, University of ashington. Seattle, ashington, USA. 28 pp. Vadas, R. L Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47: Botanica Marina / Vol. XXIX / 986 / Fase. 2

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