MARINE ECOLOGY PROGRESS SERIES Published August 10 Mar. Ecol. Prog. Ser.

Adventitious branching as a herbivore-induced defense in the intertidal brown alga distich us

Kathryn L. Van Alstyne*

Department of Zoology, NJ-15.University of Washington, Seattle. Washington. 98195,USA and Friday Harbor Laboratories, Friday Harbor, Washington 98195,USA

ABSTRACT Adventitious branches are produced following lnjury in at least 5 specles of in the family . Field experiments showed that these structures can be induced in the intertidal brown alga Fucus distichus by mechanical damage to the plant apices. The mean number of adven- titous branches on F.distichus and the percent of plants with adventitious branches was positively correlated with the density of littonne snails Ljttorina sitkana and L. scutulata near the plants at 8 locations within the main beach of Tatoosh Island, Washington, USA,suggesting that the production of these structures is a response to grazing by the snails. In laboratory feeding experiments, both L. sitkana and L. scutulata preferred normal meristematic tissue (apices) over adventitious branches. Thus. adventitious branches appear to funcbon as an herbivore-induced defense that protects newly produced tissues from damage by grazers. Neither L. s~tkananor L. scutulata showed a preference for wngs over adventitious branches. Concentrations of polyphenolic compounds were about 10 to 70 % higher in adventitious branches than apices but were 20 to 50 O/O lower than phenolic levels in wings.

INTRODUCTION existing tissues or newly produced structures. Exam- ples of defenses that protect existing tissues are Many organisms protect themselves from predators increased production of plant secondary metabolites by being chemically or morphologically defended following grazing (Havel 1986) and the production of (Rosenthal & Janzen 1979, Harborne 1982, 1986, Hay & spines in existing zooids of bryozoans (Harvell 1984, Fenical 1988, Van Alstyne & Paul 1988). Although 1985). Embryonic induction of morphological defenses these defenses confer a selective advantage upon the in zooplankton (Cilbert 1966, 1967, 1980) and the pro- organisms that produce them, they are also presumed duction of adventitious shoots in trees (Bryant 1981, to have a cost associated with their production 1982) are examples of the latter type of induced de- (Rhoades 1979). Therefore, many organisms do not fense. produce defenses continuously, but instead produce Fucus distichus ssp. edentatus de la Pyl. (POW.)(=F. them only when the risk of predation is high. Damage garderni), an intertidal temperate brown algal rock- by predators is frequently used as a cue for the produc- weed, is among the least preferred foods of the her- tion of new or additional defenses. Predator-induced bivorous snails Littorina sitkana and Littorjna scutulata defenses are common and have been reported to occur (Van Alstyne 1988b). Like many fucoid brown algae, F. in protozoans, rotifers, cladocerans, bryozoans (Harvell distichus produces large quantities of polyphenolic 1985, 1986), barnacles (Lively 1986a, b) seaweeds compounds (Steinberg 1985, Van Alstyne 1988a, b). (Lewis et al. 1987, Van Alstyne 1988a) and vascular The presence of these types of compounds is associated plants (see review by Havel 1986). In general, preda- with low rates of feeding by many temperate her- tor-induced defenses are of 2 types: they protect either bivores including littorine snails (Geiselman 1980, Geiselman & McConnell 1981. Van Alstyne 1988131, Present address: University of Guam Marine Lab, UOG turban snails (Steinberg 1985) and echinoderms Station, Mangilao, Guam 96923, USA (Anderson & Velimirov 1982). The production of

:Q Inter-Research/Printed in F. R. Germany 017 1-8630/89/0056/0169/S 03.00 170 Mar Ecol. Prog. Ser 56: 169-176, 1989

phenolic compounds by brown algae has recently been within a single location. Laboratory feeding experi- revlewed by Ragan & Glombitza (1986). ments examined the susceptibility of adventitious When Fucus dstichus is physically damaged, the branches, apices, and mng tissue to the herbivorous produchon of chemical defenses in existing tissues is snails Littor~nasitkana and L. scutulata. induced (Van Alstyne 1988a). Over a 2 wk penod following damage, concentrations of polyphenolic compounds increase throughout the midribs of the alga METHODS by ca 20 "". The increase in polyphenolic levels in these tissues appears to provide substantial protection Field measurements and experiments. Previous against the herbivorous snail Littorina sitkana. Previ- laboratory studies have shown that the production of ously damaged plants with higher levels of defenses adventitious branches is initiated by damage to the are consumed about 50 '10 less than undamaged plants. algal thallus (Fulcher & McCully 1969, 1971, Moss Thus, this induced chemical defense protects existing 1961); however, there have been no studies of the tissue against future grazing. In addition, Fucus spp. natural causes of adventitious branch production. If also produce regenerative outgrowths when they are adventitious branches in nature result from grazing by wounded (Oltmanns 1904, Fritsch 1959). These herbivores then their abundances should be correlated growths, termed adventive or adventitious embryos, with herbivore activity. A survey was made of 10 loca- occur most often from the plant midrib (Fulcher & tions on Tatoosh Island, Washington, USA. These McCully 1969) and occasionally from the wings of the included: Pole Island Draw, Strawberry Draw, and 8 injured plants (Moss 1961). locations on the main beach of the island. In each Adventive embryo formation begins with a thicken- location, I measured the number of adventitious bran- ing of the tissue immediately adjacent to the site of the ches occurring on the first 10 to 20 reproductive plants injury (Moss 1961). After about 1 wk in culture, the that I encountered within a randomly selected l m by medullary cells adjacent to the wound surface give rise l m area. Herbivore densities were also quantified by to elongating filaments whch grow through the wound counting the number of Littorina sitkana and L. surface. Here, the apical cells of the filaments divide scutulata occurring within a 10 by l0 cm quadrat repeatedly and eventually proliferate into small bran- haphazardly placed in 3 areas within the same l m by ches that resemble developing Fucus embryos. The l m area at each location. Littorina spp. were the only term 'adventive embryo' is therefore a misnomer since Fucus-consuming herbivores encountered in the quad- these tissues anse from medullary cells and are not rats. The Pole Island Draw, Strawberry Draw and main embryonic in origin. For this reason I will refer to these beach sites differed greatly in exposure, degree of structures as adventitious branches throughout the rest shading, and substrate composition; however, the sites of this paper. Electron microscopic studies have shown on the main beach of Tatoosh Island were similar to one that there is an initial loss of polyphenolic compounds another. The main beach sites were chosen to be within from the wound surface (Fulcher & McCully 1971), 50 m of one another and at approximately the same however the polyphenols became re-established in tidal height in an attempt to minimize the effects of these tissues 5 to 10 d after injury. stresses caused by other factors such as available sun- Terrestrial vascular plants produce similar out- Light, water motion and desiccation. A least squares growths in regenerating tissues (Steward 1968). linear regression was used to test for correlations Moreover, adventitious branches in terrestrial plants between mean Littonna spp, densities and (1) mean have higher concentrations of defensive compounds numbers of adventitious branches on F distichus; (2) than normal branches and are less palatable to grazers percent of Fucus distichus with adventitious branches (Bryant 1981). moss(1961) and Fulcher & McCully of the 8 sit.es on the main beach. (1969) suggested that the formation of adventitious A set of clipping experiments was carried out at the branches in brown algae can occur following damage Friday Harbor Laboratories on San Juan Island, to the plants caused by herb~vory.Thus, adventitious Wash~ngton, to determine if mechanical damage to branches of fucoid brown algae may be analogous to Fucus distichus could induce the formation of adven- adventitious shoots produced by many tree ; titious branches in the field. In July 1987, 30 non- however, the role of these structures in reducing graz- reproductive plants ranging from 10 to 20 cm in length ing has not been addressed. (holdfast to most distal apex) were tagged with 6 to In this study, I examine the phenomenon of adven- 8 mm wide strips of surveyor's tape. The plants were all titious branch production following grazing as a means growing on a large (ca 2 m long X l m wide X 2 m of protecting newly regenerating algal tissues from high) boulder. On 20 of these plants, 5 of the aplces on grazers. Field measurements were made that correlate each alga were clipped ca 1 cm from the ends. Her- adventitious branch production with grazer densities bivorous snails frequently graze the margins of the Van Alstyne: Induced dcfenses in a brown alga 171

blades and the apices of the plants, so this type of towels before being weighed. Two similarly sized damage is similar to damage that might occur by graz- pieces (0.1 to 0.6 g) of adventitious branches and apices ing. The remaining 10 plants were left unclipped and or adventitious branches and wing tissues were placed served as controls. In October 1987 the apices of the 13 into a single quadrant of the partitioned plastic boxes clipped and 8 control plants that remained were along with 5 to 15 snails. Five L. sjtkana or 10 L. examined for evidence of adventitious branch forma- scutulata were added to each quadrant in experiments tion. The maximum lengths of the adventitious bran- in which one of the pair was a short adventitious ches were also measured. branch. Ten L. sitkana or 15 L. scutulata were added to Preference experiments. Relative preference of Lit- each quadrant in preference experiments involving torina sitkana and L. scutulata for adventitious bran- medium and long adventitious branches. Plant pieces ches, wing tissue, and apical meristematic tissue (Fig. were weighed prior to adding the snails and then 4 d later in order to quantify the amount of each tissue type eaten by the littorines. Grazing rates were compared for each combination of tissues using each littorine species. There were 8 replicates for each combination of snails and plant tissues. Four quadrants holding pieces of tissue in the absence of snails sewed as controls for these experiments. Results for all preference experiments were analyzed using a Student's t-test for data with unequal variances (Sokal & Rohlf 1981). The amount of algal tissue con- sumed by the snails was calculated as the initial weight Fig. 1. Fucus dishchus. A: Apical menstem; L: long adventiti- minus the final weight for each tissue in an individual ous branch growing from midrib, M. midrib; S: short adven- feeding experiment. The consumption rate of the titious branch growing from apex; W: wing apices or wing tissues was then subtracted from the consumption rate of the adventitious branches in each 1) were determined in laboratory feeding experiments. replicate giving a single data point for each replicate of In these experiments, comparisons of consumption the experiment. The relative differences in mass rates by both L. sitkana and L. scutulata were made changes of the pair of tissues were then compared for between the following pairs of tissues: short (

RESULTS their 2 major grazers, Littorina sitkana and L. scutulata, in very localized areas beneath the plants. The percent Adventitious branching occurs commonly among age of plants that contained adventitious branches was species of fucoid macroalgae (Table 1). On Tatoosh also highly correlated with the density of Littorina spp. (r Island, 40 to 100 "; of the Fucus distichus at the 10 = 0.885, p = 0.004, using a least squares linear regres- locations surveyed around the island had at least one sion). The damage that I observed on these wounded adventitious branch (Table 2). The mean numbers of plants appeared to be primarily a result of grazing. Both adventitious branches ranged from 0.5 per plant at the L. sitkana and L. scutulata were often observed to be site with the lowest density of herbivores to 4.7 per plant feeding on the damaged plants. In addition, most of at a site with relatively higher Littorina spp, densities; these plants showed holes and scraped surface in the however, F. distichus at the site with the highest snail wings and receptacles that are characteristic of littorine densities, Pole Island Draw, did not have the highest grazing (pers. obs.) rather than having the tears in the proportions of plants with adventitious branches nor the thallus and abraded surfaces that are characteristic of greatest densities of adventitious branches per plant. damage produced by waves. The presence of adventitious branches within a single The laboratory clipping experiments demonstrated location, the main beach of Tatoosh Island, corres- that adventitious branching in Fucus distichus can be ponded well with Littorina spp. densities. Mean num- induced in the field by mechanical damage to the bers of adventitious branches on adult Fucus distichus plants. Of the clipped apices, 35 % developed adven- were highly correlated (r = 0.904, p<0.001, using a titious branches whereas none of the unchpped control least squares linear regression) with the abundance of plants did (Table 3). Adventitious branch formation

Table 1. Occurrence of adventitious branching in members of the brown algal family Fucaceae

Species Location Source

Fucus vesiculosus Moss (1961) McLachlan & Chen (1972) Ketch Harbor, Nova Scotia, Canada Fulcher & McCully (1969) Morris Point, Nova Scotia, Canada Fulcher & McCully (1969) Narragansett. Rhode Island, USA K. Van Alstyne pers. obs. Fucus distichus Tatoosh Island, Washington. USA K. Van Alstyne pers. obs. Friday Harbor, Washington, USA K. Van Alstyne pers. obs. Fucus spiralis Tatoosh Island, Washington, USA K. Van Alstyne pers. obs. Friday Harbor, Washington, USA K. Van Alstyne pers obs. Pelvet~acdnaliculata Moss (1961) Pelvetiopsis lirnita ta Tatoosh Island, Washington, USA K. Van Alstyne pers. obs.

-: location not given

Table 2. Lttorina spp. and Fucus dist~chus.Herbivore densities and adventitious branch production at 10 sites on Tatoosh Island, Washington, USA Herbivore densities (as no. m-2) are means of numbers of herbivores in a 10 cm X 10 cm quadrat within 3 haphazardly chosen locations at each site. The percent of F. distichus with adventltlous branches (AB) and the mean number (S 1 SD) of adventitious branches per plant were obtained from counts from reproductive plants sampled from within a 1 m X 1 m area at each locatlon

Location L sitkana L. scutulata O/O w~th No, of AB's N density density AB's

Strawberry Draw Pole Island Draw Main Beach Site I Site I1 Site 111 Site IV Site V Site V1 Site V11 Site VIII Van Alstyne: Induced defenses in a brown alga 173

Table 3 Fucus distichus. Production of adventitious branches on clipped and unclipped aplces

Clipped Unclipped

Proportion of plants with 62 '1:, 0% adventitious branches Percent of apices per plant with 35.4 +10.0 0.0 2 0.0 adventitous branches (2f 1 SD)

occurred on at least one of the damaged apices in 62 O/O of the clipped plants. Three months after clipping the apices, the advenhtious branches ranged in length from

Fig. 3. (A) Littorina sitkana and (B)L. scutulata preferences for short (S), medium (M) and long (L)adventitious branches and wing tissue (W). Consumption rates are given as the mean amount of tissue consumed (in mg) f l SE from 16 replicate experiments, p-values are from Student's t-test comparing the relative differences in mass changes between wings and adventitious branches during the feeding expenments (Sokal & Rohlf 1981). NS: p>0.05

sumption rates by either littorine snail between adven- titious branches and wing tissues (Fig. 3). Consumption rates of apices by L. sitkanawere 3 times those of wing tissues (Fig. 4). L. scutulataconsumed twice as much apical meristem tissue as wing tissue. Concentrations of phenolic compounds in adventiti- ous branches were highest in short adventitious bran- ches (Table 4) and decreased as these structures

Fig. 2. (A)httorina sitkana and (B)L. scutulata preferences for short (S), medium (M) and long (L)adventitious branches and apical meristematic tissue (A).Consumption rates are given as the mean amount of tissue consumed (in mg) f l SE from 8 replicate experiments. p-values are from a Student's t-test con~paringthe relative differences in mass changes between apices and adventitious branches during the feeding experi- ments (Sokal & Rohlf 1981) Littonna sitkana(Fig. 2A) and L. scutulata(Fig. 2B) preferred Cp<0.05 using a Student's t-test) apices over adventitious branch tissue. L. sitkanaconsumed apices L. sitk. L. scut. ca 6 times as much as short adventitious branches, 3 Fig. 4. Consumption rates of Littorina sitkana and L. scutulata times as much as medium adventitious branches, and for wings (W) and apical meristems (A) of Fucus d~stichus. twice as much as long adventitious branches. Con- Consumption rates are given as the mean amount of tissue sumption rates of apices by L. scutulatawere about 10 consumed (in mg) ? 1 SE from 16 replicate experiments. p- values are from a Student's t-test comparing the relative times greater than those of short adventitious branches, differences in mass changes between wings and adventitious and 3 times those of medium and long adventitious branches during the feeding experiments (Sokal & Rohlf branches. There were no significant differences in con- 1981). NS: p> 0.05 l74 Mar Ecol. Prog. Ser. 56: 169-176, 1989

Table 4. Fucusdistichus. Phenolic concentrations (as % of dry adventitious branches on plants is positively correlated weight) in adventitious branches and apical meristematic tis- with herbivore density, further suggesting that the for- sues. Values are given as means of 10 replicate measurements If: mation of adventitious branches is a result of damage 1 SE. These values are significantly different using a l-way analysis of variance (F = 8.4593, p < 0.001). Stain reaction by herbivores; adventitious branches were not found indcates the results of staining extracts run on Thin Layer on plants which showed no signs of herbivore damage. Chromatography plates with Lindt's Reagent, a stain specific for Although adventitious branches on Tatoosh Island phloroglucinol derivatives. t : positive reaction; -: no reaction appear to have be formed primarily in response to herbivore damage, their formation may also be induced Tissue type Phenolic N Stain by mechanical damage, such as that produce by waves concen- reac- at other locations. tration tion Adventitious branches represent a previously unde- Short adventitious branches 5.68 t 1 72 10 + scribed form of defense against marine herbivores. (< l cm long) Algal morphological defenses include thallus shape Medium adventitious branches 4.53 f 1.93 10 + and form (Littler & Littler 1980, Hay 1981, Steneck & (1 to 2 cm long) Watling 1982, Taylor & Hay 1984), production of Long adventitious branches 3.73 t 1.01 10 + (2 to 3 cm long) heteromorphic thalli (Lubchenco & Cubit 1980), thallus Apical meristems 3.41f0.48 9 + toughness (Watson & Norton 1985a, b) and the produc- Wings 6.99 f 2.10 10 + tion of protuberances (Steneck & Paine unpubl.), spines (K.Van Alstyne & V. Paul unpubl.) and cuticles (Gaines 1985). Adventitious branches may arise because dam- increased in length. Medium adventitious branches age to the thallus changes the relationships between had 20 % lower levels of polyphenolics than did short cells in a way that causes the production of meristema- adventitious branches. Long adventitious branches had tic cells. Alternatively, they may have been selected for about 40 % lower concentrations. Concentrations of as a way of producing new tissues that are grazer- phenolics in short and medium adventitious branches resistant. and in medium and long adventitious branches were Consumer-induced morphological defenses have indistinguishable (p > 0.05 using an SNK analysis). been previously described in only a few marine organ- Phenolic concentrations of apices were comparable to isms. For example, Padina jamaicensis, a tropical those in long adventitious branches, whereas wing brown alga, produces a turf-like morphology in tissues had phenolic levels that were about 18 % grea- response to grazing by herbivorous fish (Lewis et al. ter than those found in short adventitious branches. 1987). The encrusting bryozoan Membranipora mem- branacea induces spine production in response to a chemical cue provided by the nudibranch predator DISCUSSION Dondella steinbergae (Harvell 1984, 1985, 1986). The intertidal barnacle Chthamalus anisopoma responds to In Fucus distichus, adventitious branches are the presence of the carnivorous gastropod Acanthina induced by damage to the thallus of the plant. In field angelica by growing in a bent morphology which experiments, clipping the apices of the thallus stimu- reduces further predation by the snail (Lively 1986a, b). lated the formation of these structures. In laboratory In addition, induced morphological defenses have been experiments, the production of adventitious branching well documented in several species of freshwater zoo- has been induced by cutting Fucus midribs (Fulcher & plankton. Rotifers and Daphnia have widely varying McCully 1969). Thus, the production of adventitious morphologies which are environmentally induced, branches can be caused by mechanical damage and either through the presence of predators or by chemical does not require the presence of herbivores. However, cues obtained dietanly (Have1 1986). Fucus distichus is field observations suggest that most of the damage in F. the only marine organism in which predator-induced dishchus tissues seen at Tatoosh Island was caused by chemical defenses have been described (Van Alstyne grazing from the 2 Littorine snails, Littonna sitkana and 1988a). L. scutulata. Thus, most of the adventitious branches on Adventitious branches provide a method for pro- F. djstichus at Tatoosh probably result from damage liferating numerous branches from a non-apical part of due to littorine grazing. The site at which the field the plant. If the thallus is likely to break at the point measurements of adventitious branches were taken, where the plant is wounded, then the production of the main beach on Tatoosh Island, 1s protected from adventitious branches would allow the proliferation of most heavy wave action. Therefore, it is unlikely that new tissues at or below the point of injury. Multiple the damage that these plants receive is due to abrasion branch production may cause some self-shading in from objects moved by water. The mean number of these tissues although this may not be detrimental to a Van Alstyne: Induced defenses in a brown alga 175

high intertidal alga. Observations of adventitious bran- Acknowledgements. Thanks are due to T Daniel, P. Kareiva, ches in the field suggest that they can become repro- R. Paine, V Paul, S. Williams and 5 anonymous reviewers for ductive at a small size (5 to 10 cm long). Thus, multiple their comments on this manuscript. I also thank the Makah Tribal Council for allowing me access to Tatoosh Island and D. branch production may allow the alga to produce large Willows and the staff at the Friddy Harbor Marine Lab for numbers of relatively quickly under the providing laboratory facilities. This study was supported by unfavorable condition of intense herbivory. Addition- NSF grant OCE 84-15707 to R. Paine, Whitehall Foundation ally, adventitious branch production often occurs from grant #83548 to D. Rhoades and by an NSF Predoctoral Fellowship and grants from the Lerner Grey Fund for Marine small plants that have been entirely grazed back to the Research and Sigma Xi to K.L.V midrib. In these plants, all blade and meristematic bssue is removed by herbivores and adventitious bran- ches provide a mechanism for the generation of new meristem. LITERATURE CITED Adventitious branches contain higher levels of Anderson, R. J., Velimirov, B. (1982).An experimental invest.- polyphenolic compounds than do apices; however, gation of the palatability of kelp bed algae to the sea phenolic levels of these structures are not as high as urchin Parechinus angulosus, Leske P.S.Z.N.I.:Mar. Ecol. those found in wing tissue. Brown algal polyphenolic 3: 357-373 Behrens, S. (1972). The role of wave impact and desiccation on compounds have been shown to be feedng deterrents the distribution of bttorina sitkana Phhppi, 1845. Veliger towards herbivorous gastropods and urchins, including 15: 129-132 Littorina littorea in New England, USA (Geiselman & Bryant, J. P. (1981). Phytochemical deterrence of snowshoe McConnell 198 1, Steinberg in press). The high levels of hare browsing by adventitious shoots of four Alaskan phenolic compounds may contribute to adventitious trees. Science 213: 889-890 Bryant, J. P. (1982). The regulation of snowshoe hare feeding branches being less preferred by Littorina spp. than are behavior during winter by plant antiherbivore chemistry. apices. However, morphological characteristics of Proc. internat. Lagornorph Conf. 1. 720-731 adventitious branches, such as branch clumping, and Fritsch, F. E. (1959). The structure and reproduction of the thallus shape, thickness, and toughness, undoubtedly algae. Vol. 11. Cambridge University Press. London Fulcher, R. G., McCully, M. E. (1969). Histological studies on also contribute to their being a low preference food the genus Fucus. IV. Regeneration and adventive embry- (Van Alstyne 1988b). ony. Can. J. Bot. 47: 1643-1649 Adventitious branching in Fucus appears to be Fulcher, R. G., McCully, M. E. (1971). Histological studies on analogous to adventitious shoot production by terrestri- the genus Fucus. V An autoradiographic and electron al trees. Bryant (1981, 1982) demonstrated that like microscopic study of the early stages of regeneration. Can. J. Bot. 49: 161-165 adventitious branches, adventitious shoots are less Gaines, S. D. (1985). Herbivory and between-habitat diversity- palatable and better defended chemically than are the differential effectiveness of plant defenses in a marine mature growth twigs. He postulates that herbivore- plant. Ecology 66: 473-485 induced changes in levels of defensive compounds in Geiselman, J. A. (1980). Ecology of chemical defenses of algae against the herbivorous snail, Littorina Littorea, in the New these shoots may be responsible for 10 yr cycles in England rocky intertidal community. Ph. D. thesis, Woods snowshoe hare populations. It is unlikely that adven- Hole Oceanographc Institution/Massachusetts Institute of titious branch production by Fucus has a significant Technology effect on littorine populations since these snails do not Geiselman, J. A., McConnell, 0. J. (1981). Polyphenols in appear to be food limited (Behrens 1972); however, brown algae Fucus r~esiculosus and Ascophyllum nodosum: chemical defenses against the marine herbivor- they probably do have an impact on the fitness of the ous snail, Littonna littorea. J. chem. Ecol. 7: 11 15-1 133 plants producing them, by reducing grazing on newly Gilbert, J.J. (1966). Rotifer ecology and embryological induc- growing tissues. tion. Science 151. 1234-1237 In summary, advenbtious branches appear to func- Gilbert, J. J.(1967). Asplanchna and postero-lateral spine production in Brachionus calyciflorus. Arch. Hydrobiol. 64: tion as an herbivore-induced defense, occurring in 1-62 response to wounds inflicted by grazing and reducing Gilbert, J. J. (1980). Developmental polymorphism in the the susceptibility of regenerating tissues from further rotifer Asplanchna sieboldi. Am. Scient. 68: 636-646 attacks by grazers. The tissue reorganization that Harborne, J. B. (1982). Introduction to ecological biochemis- occurs when Fucus distichus is wounded results in the try Academic Press, London Harborne, J. B. (1986). Recent advances in chemical ecology. formation of numerous proliferating branches each Nat. Product Rep. (Lond.) 1986: 323-344 growing from a newly formed apex. Thus, the indi- Harvell, C D. (1984). Predator-induced defense in a marine vidual branches in an adventitious branch can be con- bryozoan. Science 224: 1357-1359 sidered equivalent to single apical meristems. The Harvell, C. D. (1985). Partial predation, inducible defenses, and the population biology of a marine bryozoan (Mem- results of these feeding experiments indicate that branipora membranacea). Ph. D. thesis, University of adventitious branches are less susceptible to herbivore Washington, Seattle attacks than are ordinary apical meristematic tissue. Harvell. C. D (1986). The ecology and evolution of inducible 176 Mar. Ecol. Prog. Ser. 56: 169-176, 1989

defenses in a marine bryozoan: cues, costs, and conse- Progress in phycological research, Vol. 4. Biopress, p quences. Am. Nat. 128: 810-823 129-24 1 Havel, .l. (1986). Predator-induced defenses. a review. In: Rhoades, D. F (1979) Evolution of plant chemical defense Kerfoot, W. C., Sih. A. (eds.) Predahon: direct and indirect against herbivores. In. Rosenthal, G. A., Janzen, D. H. effects on aquatic communities. Univ. Press of New Eng- (eds.) Herbivores: their interaction with secondary plant land, Hanover, p. 263-278 metabolites. Academic Press. New York, p 1-55 Hay, M. E. (1981). The functional morphology of turf-forming Rosenthal, G. A., Janzen, D. H. (1979). Herbivores: their seaweeds: persistence in stressful marine habitats. Ecol- interaction with secondary plant metabolites. Academic ogy 62: 739-750 Press, New York Hay, M. E., Fenical, W. (1988). Chemically mediated sea- Sokal, R.R., Rohlf, F. J (1981). Ri.ometry W. H. Freeman and weed herbivore interactions. Ann. Rev. Ecol. Syst. 19: Co.. New York 111-145 Steinberg, P. D. (1985). Feeding preferences of Tegula fune- Lewis, S. M,,Norris, J. N., Searles, R. B. (1987).The regulation bralis and chemical defenses of marine brown algae. Ecol. of morphological plasticity in tropical reef algae by herbiv- Monogr. 55: 333-349 ory. Ecology 68: 636-64 1 Steinberg, P. D. (in press). The effects of quantitative and Littler, M. M., Littler, D. (1980). The evolution of thallus form qualitative variation in phenolic compounds on feeding in and survival strategies in benthic marine macroalgae. field three species of marine herb~vores.J. exp and laboratory test of a functional form model. Am. Nat. mar. Biol. Ecol. 116: 25-44 Steneck, R. S., Watling L. (1982). Feeding capabilities ana Lively, C. M. (1986a). Competition, comparative life histories, limitations of herbivorous molluscs: a functional group and maintenance of shell dimorphism in a barnacle. Ecol- approach. Mar. Biol. 68: 299-319 ogy 67: 858-864 Steward, F. C. (1968). Growth and organization in plants. Lively, C. M. (1986b) Predator-induced shell dimorphism in Addison-Wesley, Reading the acorn barnacle Chthamalus anlsopoma. Evolution 40: Swain, T S., Goldstein, J. L. (1964). The quantitative analysis 232-242 of phenolic compounds. In: Pridham, J. B. (ed.) Methods in Lubchenco, J., Cubit, J. (1980) Heteromorphic life hstories of polyphenol chemistry. MacMillan, New York, p. 131-146 certain marine algae as adaptations to variations in herbiv- Taylor, P. R., Hay, M. E. (1984). Functional morphology of ory. Ecology 61: 676-687 intertidal seaweeds: adaptive significance of aggregate vs. McLachlan, J., Chen, L. C.-M. (1972). Formation of adventive soLitary forms. Mar. Ecol. Prog. Ser. 18: 295-302 embryos from rhizoidal f~laments in sporelings of four Van Alstyne, K. L. (1988a). Herbivore grazing increases species of Fucus (Phaeophyceae). Can. J. Bot. 50: polyphenolic defenses in the intertidal brown alga Fucus 1841-1844 distichus. Ecology 69: 655-663 Moss, B. L. (1961).Wound healing and regeneration in Fucus Van Alstyne, K. L. (1988b). The ecology and evolution of vesiculosus L. Proc. int. Seaweed Symp. 4: 117-122 antiherbivore defenses in fucoid brown algae. Ph. D. Oltmanns, F. (1904). Morphologie und Biologie der Algen. thesis. Univ. of Washington. Seattle Vol. 1 Fischer, Jena Van Alstyne, K. L., Paul, V. J. (1988) The role of secondary Peterson, P., Renaud, P. (in press). Analysis of feeding prefer- metabolites in med~atingecological interactions. Proc. 6th ence experiments. Oecologia (Berl.) int. Coral Reefs Congr (in press) Ragan, M. A., Craigie, J. S. (1978). Phenolic compounds in Watson, D. C., Norton, T A. (1985a). Dietary preferences of brown and red algae. In: Hellebust, J. A., Craipe, J. S. the common periwinkle, Littorina llttorea (L.).J, exp. mar (eds.) Handbook of phycological methods, Vol. 11. Cam- Biol. Ecol. 88: 1-19 bridge Univ. Press, Cambridge, p. 157-179 Watson, D. C., Norton, T. A. (1985b). The physical characteris- Ragan, M. A, Glombitza, K. (1986). Phlorotannins, brown t~csof seaweed thalli as deterrents to littorine grazers. algal polyphenols. In: Round, F. E., Chapman, D. J. (eds.) Botanica mar. 28: 383-387

This article was submitted to the editor Manclscript first received: January 10, 1989 Revised verslon accepted: Apnl 14, 1989