Heteromorphic Life Histories of Certain Marine Algae As Adaptations to Variations in Herbivory

Heteromorphic Life Histories of Certain Marine Algae as Adaptations to Variations in Herbivory

Jane Lubchenco; John Cubit

Ecology, Vol. 61, No. 3. (Jun., 1980), pp. 676-687.

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http://www.jstor.org Mon Mar 24 17:02:11 2008 Ecoloyy, 61(3), 1980, pp. 676-687 1980 by the Ecological Society of America

HETEROMORPHIC LIFE HISTORIES OF CERTAIN MARINE ALGAE AS ADAPTATIONS TO VARIATIONS IN HERBIVORY1

JANELUBCHENCO~'~ Depurtment of Zoology, Oregon State University, Corvullis, Oregon 97331 USA

AND

JOHNCUBIT^'^ Depurtment of Biology, University of Oregon, Eugene, Oregon 97403 USA

Abstract. Many of the annual or ephemeral algae of the mid to high intertidal zones have heteromorphic life histories, existing as upright morphs during seasonal algal blooms and as crustose or boring morphs during other portions of the year. Experimental removal of herbivores on the coasts of New England and Oregon resulted in the occurrence of the upright morphs in the times of year when they were normally absent (summer in our areas), demonstrating that such uprights can survive the summertime physical regime (contrary to earlier speculation). We suggest that the upright and crustose or boring stages of these algae represent mutually exclusive adaptations to fluctuations in grazing pressure: the upright stages are adapted for high rates of growth and reproduction when grazing pressure is low, and the crustose and boring stages are adapted for surviving through times of high grazing pressure. We predict isomorphic species of algae would predominate in these sorts of habitats if grazing pressure were more constant. Key words: algae; Bangia; Codiolum; Conchocelis; herbivores; heteromorphology; life histories; Petalonia; Porphyra; Ralfsia; Scytosiphon; Ulothrix; Urospora.

established, stable life cycles involving several eco- Heteromorphic algae exhibit a high degree of inde- logically distinct stages. To these we add certain het- pendence and differentiationamong the stages of their eromorphic algae, which by Istock's (1967) criteria life cycles. Most of the particular heteromorphic algae should be particularly evolutionarily unstable: the discussed in this paper have two separate, in some stages are often found under different growing condi- cases self-propagating, and ecologically distinct phas- tions, and some, rather than being larva-like devel- es which are so dissimilar in appearance that until re- opmental stages, are capable of independent self-prop- cently they had been classified as separate species, agation that allows them to persist indefinitely in the and, in some cases, had been placed in separate fam- absence of any other stage. ilies or orders. Algae with various types of heteromorphic life Istock (1967) has proposed that evolutionarily such cycles are both phylogenetically and ecologically wide- life cycles should be inherently unstable: as selection spread: heteromorphic algae occur in the three major acts independently on the separate stages, one stage divisions of macroalgae (Chlorophyta, Phaeophyta, should eventually be eliminated or reduced in favor of and Rhodophyta) and are found in a variety of habi- the other. He cites as examples the loss or reduction tats. However, in this paper we concentrate on those of larval or adult stages in some insects, cnidarians, species of heteromorphic algae which comprise much and amphibians. Another more pervasive set of ex- of the macroalgal portions of seasonal or ephemeral amples is the loss of the free-living, haploid, gameto- blooms in the mid to high intertidal zones of rocky phyte stage from the life cycles of most plants and shores. These species are in the following divisions and animals. genera: Chlorophyta: Ulothrix and Urospora; Phae- However, Istock (1967, 1970) points out there are ophyta: Petalonia and Scytosiphon; Rhodophyta: a number of counterexamples with apparently long- Bangia and Porphyra. Although the algae in this group are taxonomically quite different,their life cycles and morphologies have much in common. Each species ' Manuscript received 14 February 1979; accepted 1 June has two primary stages: the stage which appears in the 1979; final version received 29 August 1979. periodic algal blooms is an upright filament, tube, or Order of authorship determined by coin toss. In previous publications, J. Lubchenco Menge. blade; the other is a nonupright crust or boring stage. Present address: Smithsonian Tropical Research Insti- (Athird stage, a small filamentous tuft, is also known tute, APO Miami, Florida 34002 USA. for Petalonia and Scytosiphon.) The convprgence in June 1980 HERBIVORY AND ALGAL LIFE HISTORIES 677 the patterns of life cycles of these algae suggests their SEASONAL CYCLES OF : forms and life histories may be adaptations to a common set of selective factors; thus, these plants provide a system to examine the mechanisms by which com- HERBIVORE ACTIVITY plex life cycles are selected and maintained. The main ULOTHRIX k m question addressed in this paper is the following: what is the adaptive significance of the heteromorphic life cycles of these intertidal algae? An explanation already proposed is that the non- BmA upright morphs are perennating stages which survive through the physically harsh seasons when the upright PORPHYRA %-'Lv morphs are killed by such stresses as desiccation, in- OND J F M A M J J A S O solation, and high temperatures (Conway et al. 1976). FIG.1. Subjective evaluations of percent of gastropod A second hypothesis occurred to each of us during herbivore individuals active and of the relative abundance of our independent studies on the effects of herbivores the upright morphs of five heteromorphic algal species on the New England coast during the year. The herbivores are pri- on benthic marine algae. We observed that in several marily Littorinu littorea, but also include other snails: L. ob- heteromorphic species the upright morphs could sur- tusuta, L. saxatilis, Lucunu vinctu, Murgurites helicinu, and vive in physically harsh seasons if protected from her- Acmaea testudinulis. Herbivores not included are isopods, bivores, and that the nonupright morphs were either amphipods, and diptera. Each algal species was recorded as being common (C), present (P), or absent (A) at each study themselves grazer-resistant or specifically exploit mi- area at least monthly for 3 yr. Study areas where gastropod crohabitats which we infer protect them from grazing. herbivores are common (protected to intermediate in expo- In this paper we suggest the hypothesis that spatial sure to wave action) are indicated by the solid portions. and temporal variations in grazing play a major role Areas where gastropod herbivores are rare or absent (ex- in the selection and continued maintenance of the dif- posed sites) are indicated by cross-hatching. Scytosiphon, Petuloniu, and Porphyra are able to persist longer in exposed ferent morphologies in these life cycles. In the follow- sites. Crustacean herbivores are often abundant at more ex- ing sections we present the results of experiments test- posed sites. Their effect on algae is yet to be determined. ing this hypothesis on the east and west coasts of the United States: in New England (studies of J.L.) and in Oregon (studies of J.C.). Alternate hypotheses and The life histories of these algae are as follows: ways to test them are suggested in the discussion sec- 1) Petalonia fascia (0. F. Miill.) 0. Kuntze and tion. If our interpretations are correct, we predict that Scytosiphon lamentaria (Lyngb.) Link (Phaeophyta: in less variable environments algae with heteromor- Scytosiphonaceae). phic life cycles would not be maintained in such abun- The upright morphs of both of these algae are "win- dance and, instead, algae with isomorphic life cycles ter annuals" in New England (Fig. 1, Taylor 1957, would increase in relative proportion. Kingsbury 1969). The upright blades ofPetalonia (7.5- 45 cm long) and upright tubes of Scytosiphon (15-70 cm long) appear in tide pools and on the shore from New England studies October-November until March-May. Both species Description of sites and species studied.-The het- probably alternate (but not in an obligate sense) with eromorphic algal species treated in the studies of the tar-like crusts previously thought to be species of Ralf- rocky shores of New England are the brown algae sia (Phaeophyta: Ralfsiaceae) and perhaps with small Petulonia fascia (0.F. Miill.) 0. Kuntze and Scyto- filamentous tufts, as has been shown for these species siphon lomentaria (Lyngb.)Link, the red algae Bangia elsewhere (Edelstein et al. 1970, Rhodes and Connell fuscopurpurea (Dillw.) Lyngb., Porphyra miniata (C. 1973, review by Wynne and Loiseaux 1976). The sea- Ag.) C. Ag., P. linearis Grev., and P. umbilicalis (L.) sonal occurrence of the ralfsioid crust morph is diffi- J. Ag., and the possibly heteromorphic green alga Ulo- cult to assess accurately because these crusts are dif- thrix flucca (Dillw.) Thur. in LeJolis. Observations ficult to distinguish in the field from other, valid were made on all of these species, but experiments Ralfsia species. The crustose morph, hereafter termed focused on the two brown algae Petulonia and Scy- "Ralfsia," appears to be more abundant in the sum- tosiphon. These plants were studied at four study mer than in the winter in New England. areas in Massachusetts (MA) and Maine (ME) from Petalonia and Scytosiphon differ somewhat in the fall 1971 until summer 1977. The areas are nonestua- specifics of their life cycles, in particular in the ploidy rine and range in exposure to wave action from very levels. According to Nakamura and Tatewaki (1975), protected to very exposed as follows: Canoe Beach Scytosiphon tubes are haploid and produce gametes. Cove, Nahant, MA; Grindstone Neck, ME; East These gametes do one of three things: (1) develop par- Point, Nahant, MA; and Pemaquid Point, ME. All thenogenetically into more haploid tubes, (2) develop areas are described in detail in J. Lubchenco Menge parthenogenetically into haploid "Ralfsiu" crusts or (1975) and B. Menge (1976). tufts or (3) fuse, with the zygote developing into a 678 JANE LUBCHENCO AND JOHN CUBIT Ecology, Vol. 61, No. 3 diploid "Ralfsia" crust or tuft. Both haploid and dip- mentous form previously known as "Conchocelis." loid crusts or tufts produce zooids which develop into Upright plants are dioecious and produce two of three upright tubes. Meiosis occurs only when diploid crusts possible types of spores: (1) "monospores" or "neu- or tufts form zooids. Wynne (1969) found that his tral spores" which develop into more upright filaments "Ralfsia" could also produce more "Ralfsia" crusts. and one of the following types of spores (2) "carpo- Thus in this species the upright morph is haploid while spores" or "alpha spores" which germinate to give the other can be either diploid or haploid, indicating rise to the "Conchocelis" phase, or (3) "spermatia" a partial decoupling of the morphological and genetic or "beta spores" that presumably act as male gametes components. and fuse with the cells that develop into carpospores. This decoupling is complete in Petalonia, where all The "Conchocelis" phase produces two types of stages (crusts, tufts, and blades) appear to be of the spores: (1) "monospores" which develop into more same ploidy number. No evidence of sexuality has ''Conchocelis" plants, and (2) ''conchospores' ' which been reported. "Ralfsia" crusts or tufts produce develop into the macroscopic upright phase (Sommer- zooids which develop into either more "Ralfsia," or feld and Nichols 1970). Both photoperiodism (Rich- tufts or Petalonia blades. Blades produce swarmers ardson and Dixon 1968, Dixon and Richardson 1970, which develop into either crusts, tufts, or blades Richardson 1970) and temperature (Sommerfeld and (Wynne 1969, Wynne and Loiseaux 1976). Nichols 1973) have been shown to control the forma- Neither of these species represents the classical pic- tions and release of spores of both phases of the life ture of a strict alternation of generations (haploid with history in the laboratory. In New England, the upright diploid). More significantly, both species appear to Bangia filaments measure =lo-20 mm in length and possess tremendous morphological flexibility, each 0.15 mm in diameter and usually appear in December- morph being able to produce either more individuals February and persist through March-May (Fig. 1). like itself or the other alternate morph. In other words, The seasonal occurrence of the "Conchocelis" phase neither genetic nor morphological alternation is obli- is not known; however, the plants have been found in gate. Why then are there two distinct morphs, each intertidal mollusc and barnacle shells (Bird 1973). The with this plasticity? "Conchocelis" phase is thought to be perennating. Proximate factors affecting which morph is pro- 3) Porphyra umbilicalis (L.) J. Ag., P. miniata (C. duced have been investigated in the laboratory. In nu- Ag.) C. Ag., and P. linearis Grev. merous culture studies, blades ofPetalonia and tubes As in Bangia, the life history of these species in- of Scytosiphon were found to be produced mainly un- volves two different phases with different morpholo- der simulated "wintertime conditions ," i.e., short gies. The macroscopic Porphyra thalli discussed here daylength photoperiods and cool temperatures. The are leafy sheets usually ranging in size from 3 to 15 cm "Ralfsia" crusts or tufts were obtained under labo- long, are haploid, and alternate with a "Conchocelis" ratory "summertime conditions," i.e., long daylength phase (as described for Bangia) which is usually dip- photoperiods and warm temperatures (Wynne 1969, loid and which bores into and lives in calcareous sub- Roeleveld et al. 1974, Dring and Luning 1975, Naka- strates. mura and Tatewaki 1975). There exists considerable variation among the It seems significant that in these laboratory culturing species with respect to seasonal occurrence and spe- experiments there was usually some variation in the cifics of the life history (Conway 1964, Edelstein and response of plants to temperature and photoperiod; McLachlan 1966, Chen et al. 1970, Bird et al. 1972, that is, a small percentage of the progeny became the Bird 1973, Bold and Wynne 1978, Hawkes 1978). The "wrong" morph for a particular set of conditions foliose phase of P. linearis is a high intertidal winter (Wynne 1969, Roeleveld et al. 1974). For example, in annual. Since no neutral spores are formed by the three of Wynne's experiments with Petalonia, 5-20%, blades and the basal portion does not perennate, 5-10%, and 0% of the progeny developed into blades blades must come solely from conchospores. Con- under summertime conditions (18"-1YC, 16 h light-8 chospores are released only at 13°C in culture, but can h dark). The potential significance of this variation will be found throughout the year in the intertidal. The be discussed below. "Conchocelis" phase has been found in subtidal mus- Both species' laboratory behavior generally corre- sel (Modiolus modiolus) shells (Bird et al. 1972, Bird sponds to their seasonal occurrence in New England: 1973). The foliose thallus of P. miniata occurs in the uprights are produced under wintertime conditions, mid and low intertidal and subtidal regions from spring and crusts appear primarily under summertime con- to summer. All blades apparently come from concho- ditions. spores. Conchospore release is triggered in the labo- 2) Bangia fuscopurpurea (Dillw.) Lyngb. (Rho- ratory at temperatures <13"C (Chen et al. 1970). P. dophyta: Bangiaceae). umbilicalis has several upright forms: (1) perennial ro- This species has two very different phases in its life settes present in the high zone (Edelstein and Mc- history: upright, macroscopic plants which are unise- Lachlan 1966), (2)an elongated morph that appears in riate or multiseriate filaments, and an endolithic fila- the winter in mid zones, and (3) a persistent blade June 1980 HERBIVORY AND ALGAL LIFE HISTORIES 679 phase that occurs in the low intertidal and reproduces by neutral spores to form more blades (Conway 1964, Chen et al. 1970). In the areas reported in this paper, foliose uprights usually appeared in October-November and persisted through May-June where herbivores were present or occurred throughout the year where herbivores were absent or rare, for example, at exposed areas (Fig. 1). 6. Roof p--X, Species ofPorphyra could not always be distinguished '0°1 x--K'x "t;kLp, II 'x--f and are lumped together here. 4) Ulothrix flacca (Dillw.) Thur. in LeJolis (Chlo- rophyta: Ulotrichaceae). Both isomorphic and heteromorphic life cycles have been described for U.flacca elsewhere. Perrot (1972) C. h. w69 enclosure suggests that in France it is really two separate 0-0 Petalonia species, one isomorphic and occurring in the very high 0-, ,o S@asiphm 50 x---x Ephememl intertidal zone and the other heteromorphic and oc- u \ Algae W X-- A, curring lower. The isomorphic species, termed "Form x,. I, \ lo]0 , ; , , , , ; , , , , U ..., A" by Perrot, has upright, filamentous gametophytes ; p--x--x--x, X and sporophytes. Each stage reproduces to form either I i X , \ x--x ! I '\ more plants of the same or the alternate stage. The , D. Herbivore 'x,, ;x' "\x-.X" 50 ,* heteromorphic species, "Form B," has dioecious, up- 'x' Exclusion I x' p.. right, filamentous gametophytes which produce two types of cells: (1) zoospores which develop directly into more upright gametophytes and (2)gametes which fuse to form a zygote that develops into a discoid spo- rophyte resembling the green prostrate Codiolum. This Codiolum-like stage produces aplanospores which develop directly into upright gametophytes. O . . , - . . c . Both photoperiod and temperature are involved as AMJJASONDJFMAMJJA cues in this nonobligate alternation. 1973 1974 The life histories ofthe New England U.flacca have not been investigated, but circumstantial evidence FIG.2. Effect of herbivores on the occurrence of Peta- suggests that at least the heteromorphic form is pres- loniu and Scytosiphon in the high intertidal zone at Grind- ent. Ulothrix occurs as long, slender filaments (10-70 stone Neck, Maine. The numbers below each treatment title mm long, 0.15 mm in diameter) forming dense mats indicate the mean number of grazers present and 95% con- fidence interval. L.1. = Littorina littoreu, L.o. = L. obtusata, which are common throughout the intertidal region L.s. = L. saxutilis. Ephemeral algae are those plants that from October-November to March-May (Fig. 1). usually persist for short periods of time during the year. Pe- When Ulothrix disappears during the spring, "Co- tuloniu and Scytosiphon are ephemeral species by this defi- diolum" appears and persists throughout the summer nition, but are separated from the rest of the ephemeral algae since they are the focus of this experiment. The other ephem- and fall. eral species appearing in this experiment include some het- Herbivore occurrence and algal preference.-The eromorphic and some nonheteromorphic uprights: Bangia most abundant herbivore in the New England rocky fuscopurpureu, Dumontia incrussata, Porphyra spp., Rhi- intertidal zone is the common periwinkle snail Litto- zoclonium tortuosum. Spongomorpha sp., and Ulothrixjuc- rina littorea which occurs in tide pools and on emer- ca. Separate percent cover values for each species were usually taken; occasionally some species were mixed togeth- gent substrata where these heteromorphic algae are er so thoroughly that it was necessary to lump them together found (J. Lubchenco Menge 1975, Lubchenco 1978). (as for Scytosiphon and Petulonia in A and B). The approx- Littorina is usually active from spring (March-May) imate period of seasonal inactivity of the herbivore, 1,ittorinu to late fall (October-November, Fig. I), at just the littoreu, is indicated by the bar at the top of the figure. See text for details of treatments. time when the upright morphs of Scytosiphon, Peta- lonia, Bangia, Porphyra, and Ulothrix are absent (Fig. 1). Laboratory preference experiments indicate that Littorina will readily eat the upright morphs of all of Field herbivore exclusions: design.-During the these species, but not the crustose forms (Lubchenco course of a general investigation of the effectsof rocky 1978). Crusts like these are not totally herbivore re- intertidal herbivores on algae in New England, a series sistant, but are much less preferred than are the up- of 10 x 10 x 3 or 10 x 10 x 5 cm stainless steel mesh right morphs or many other nonheteromorphic upright cages were attached to the rock and used to exclude species. or enclose various herbivores (see J. Lubchenco JANE LUBCHENCO AND JOHN CUBIT Ecology, Vol. 61, No. 3

Herbiwres inactive

A. CONTROL D HERBIVORE EXCL.. E!lQ& REMOVAL

C. L LITTOREA ENCLOSURE F HERB. EXCL., m S 8 EPHEM REM. '"1 4 LI 1

ad*- *,J- /\o -- --x--x-.." X --,* 0 0 a *-8 0 .. " , ' JJASONO JFMAMJJA JJASONDJFMAMJJA

0... ..O Scytosiphar *-a A.-.A x---x Ephememl Algoe

FIG.3. Effect of herbivores and algal competitors on the occurrence of Petalonia and Scytosiphon in the mid intertidal zone of Canoe Beach Cove, Nahant, Massachusetts. See Fig. 2 legend and text for details.

Menge 1975, B. Menge 1976). One of these experi- this experiment was bare, i.e., lacked macroscopic ments was specifically designed to test the effects of plants or animals. Both experiments were on emergent Littorina on Petalonia, Scytosiphon, and their ralf- substrata, i.e., exposed to air at low tide (as opposed sioid crusts; additional information on these interac- to being in tide pools). tions was obtained as a by-product of other experi- Field herbivore exclusions: results.-The results in ments. Fig. 2 support the hypothesis that grazing by L. lit- Each experiment consisted of at least the following torea, not inability to withstand summertime condi- four treatments: (1) an unmanipulated control (no cage tions, caused the absence of Petalonia blades and or roof); (2) a roof control (tests for shading effects of Scytosiphon tubes during the summer. In the the mesh; herbivores have normal access to the area unmanipulated control and the roof control (Fig. 2A, underneath the roof); (3) a Littorina littorea enclosure B), with periwinkle grazing in the spring, summer, and (four periwinkles, usually 1.2-2.0 cm in length en- fall, Petalonia and Scytosiphon appeared only during closed in a cage; this biomass is within the range nor- the winter (December-February). Where L. littorea mally occurring in nonexperimental areas); and (4) was excluded (Fig. 2D, E), Petalonia also appeared herbivorous gastropod exclusion. In all treatments, during the "wrong" time of the year, i.e., in the sum- herbivores such as isopods or amphipods could mer (July-August 1974), and Scytosiphon also colo- and did enter the cage. Various other treatments were nized out of season, i.e., in the spring and summer added as deemed necessary. For example, an herbi- (May-July 1975). Where L. littorea was enclosed (Fig. vore exclosure from which the brown alga Fucus or 2C), neither Petalonia nor Scytosiphon nor any other ephemeral algae was removed was used to separate heteromorphic uprights ever appeared even in the win- effects of herbivores from effects of potential algal ter. Ralfsioid crusts were not observed in any of these competitors on Petalonia or Scytosiphon. treatments, but were present in the general area. Experiments were established at two sites. One set The abundances of Petalonia and Scytosiphon in the was in the high intertidal zone (+1.87 m) at Grindstone herbivore removal experiments were inversely related Neck, on flat, horizontal granite with a cover of to the abundances of various ephemeral algae, sug- ephemeral algae but no algal crusts (Fig. 2). The other gesting that Petalonia and Scytosiphon may compete was on flat, horizontal substratum in the mid zone with other ephemeral algae (Fig. 2D, E) when herbi- (+0.4 m) at Canoe Beach Cove, with no upright algae vores are absent. The experiments in Fig. 3 tested this but with traces of the red crust Hildenbrandia rubra hypothesis. This cage set was in the mid intertidal (Fig. 3). The remainder of the primary substratum in zone where L. littorea is more abundant than in the June 1980 HERBIVORY AND ALGAL LIFE HISTORIES 68 1 high zone experiments of Fig. 2. Here again, Petalonia Fralich 1972, 1973, M. H. Zimmerman,personal com- and Scytosiphon occurred in the control and roof only munication). during the wintertime when the snails are usually less Thus the general pattern of Petalonia and Scytosi- active (Fig. 3A, B). Where L. littorea was enclosed in phon upright occurrence in the field corresponds to cages (Fig. 3C), it prevented most algae (including laboratory culturing results: uprights occur during the Petalonia and Scytosiphon) from becoming estab- winter. The occurrence of a few uprights out of season lished, even in the winter. L. littorea usually retreat (either in herbivore exclusion cages or exposed sites to crevices during the winter and seldom (but occa- where herbivores are rare or ineffective) may be a sionally) forage. Snails enclosed in cages do feed, but result of the small variation in plant response to pho- at reduced rates as compared with the summer. Thus toperiod and temperature reported by Wynne (1969; caged snails can evidently prevent even wintertime see above). occurrence of most algae, unless very dense settle- In similar herbivore exclusion and sometimes in ment of algae (swamping) occurs. Where herbivores competitor removal cages, the other heteromorphic were excluded (Fig. 3D, E, F), algae were more abun- species also appeared out of season. Uprights of Ulo- dant. The particular kind of alga that comes in is prob- thrix, Bangia, and Porphyra were all observed during ably a function of the plants which are available to June, July, and August when they are normally absent colonize and of competitive interactions between (Fig. 1). those plants which do settle (J. Lubchenco Menge 1975, Lubchenco and B. Menge 1978, J. Lubchenco, Oregon studies personal observation). Description of the sites and species studied.-The In all three exclosures (Fig. 3D, E, F) Petalonia Oregon studies were performed at two sites near Coos blades and sometimes Scytosiphon tubes appeared in Bay: South Cove of Cape Arago and Sunset Bay. The July, the "wrong" time of year for blades and tubes. study plots at each site were above the mean high tide Where Fucus and ephemeral algae were continually level on the wave-exposed sandstone rocks of the out- removed, Petalonia and Scytosiplzon continually col- er coast. (The level of the study areas corresponds to onized (Fig. 3F). In herbivore exclusion cages where "Zone 1," the uppermost intertidal zone, in the ephemeral species but not Fucus were removed, Fu- scheme of Ricketts et al. 1969.) cus took over the cage (Fig. 3E) and neither Petalonia At the tidal level of these study areas there are wet nor Scytosiphon occupied primary space. (EAperi- and dry seasons which result from seasonally changing ments on competitive interactions between Fucus and weather conditions and tidal cycles. In the wet season various ephemeral species will be reported elsewhere.) (late autumn, winter, and early spring) air tempera- These results indicate that it is physiologically pos- tures are cooler, precipitation is greater, tidal levels sible for Petalonia blades and Scytosiphon tubes to are higher during the daylight hours, and the rocks exist during the summer months. These plants appear receive more spray and wash from the waves gener- to be normal and healthy, judging by their color and ated by winter storms. During this season the high size. Thus warmer temperatures or longer daylengths rocks are almost continually wet, even at low tide. In neither kill nor stunt them. Similar results have oc- the dry season (late spring, summer, early fall) the curred in a number of other experiments designed to high intertidal rocks often dry out at low tide; this investigate other algae. Upright forms of Petalonia pattern is modified in some years by cool, wet fogs in and Scytosiphon appeared out of season in 33% of the late spring and early summer (Cubit 1975). 15 herbivore exclusion cages where free space was In the areas of the study plots, the most abundant available (i.e., unutilized by other upright algae or an- herbivores in terms of biomass per unit area were the imals; out of a total of 53 herbivore exclusion cages acmaeid limpets, nearly all of which were Collisella in place for 1-5 yr at the four study sites). Moreover, (=Acmaea) digitalis. Chironomid flies, gammarid am- upright Petalonia and Scytosiphon can sometimes be phipods, and littorinid snails were also occasionally found in nonexperimental (uncaged) areas at the abundant in certain areas. "wrong" time of year. In the summer these plants The abundance of algae at these sites varied with were generally in the mid and low zones, both in tide the seasons. In the winter wet season there is a bloom pools and on emergent substrata. J.L. has observed of microalgae (diatoms and blue-greens) and macro- this only a few times in 5 yr, at more wave-exposed algae. Nearly all of the macroalgae comprising this areas, e.g., East Point and Pemaquid Point, where her- bloom are in the genera treated in this paper: Bangia, bivores such as littorinids are less abundant and/or Porphyra, and Urospora. Most of these algae disap- less effective, and waves remove potential competi- pear from the high intertidal zone during the drier con- tors more frequently. Other investigators have also ditions of summer. These plants and their life cycles reported Petalonia and Scytosiphon occurring during are described below. (Bangia fuscopurpurea has been summer and fall months in New England at exposed described in the previous section.) All of these species sites (Lamb and Zimmerman 1964, Mathieson and have heteromorphic life cycles. 682 JANE LUBCHENCO AND JOHN CUBIT Ecology, Vol. 61, No. 3

1) Porphyra perforata J. Ag., P. pseudolanceolata parencies of the plots, a method similar to that of Con- Krishnamurthy, and P. schizophylla Hollenberg (Rho- nell(1970). In the cases where the filamentous Bangia dophyta: Bangiaceae). and Urospora grew so closely intermingled that they The general features of the life histories of these could not be separated their coverage was measured species of Porphyra are similar to those described as a Bangia-Urospora mixture. The relative abun- above for this genus in New England. Most of the dances of these algae are reported here only for the Porphyra plants in the Oregon study areas were <5 first 6 mo following the establishment of each study cm wide and <10 cm long. Size and shape vary some- plot. In the longer term the succession of barnacles, what among the species. For these species, alterna- perennial algae, and other organisms altered the sub- tions of generations between the upright stages and strate and other growing conditions within the exclo- the "Conchocelis" stages may be obligatory, since no sures so that for the purposes of this paper they were other types of reproduction have yet been reported no longer comparable to the controls. (Mumford 1975, Conway et al. 1976). At all times of year, including summer, there was 2) Urospora perlicilliformis (Roth) Aresch. (Chlo- an immediate increase in algal cover following the ex- rophyta: Acrosiphoniaceae). clusion of limpets. Urospora and Bangia were gener- The upright, macroscopic plants are filamentous, ally the first macroalgae to appear in the exclosures, reaching a maximum size of 30-40 mm long and 0.06 often in mixed stands, and were followed by Porphyra mm in diameter. Reproduction in the macroscopic and the isomorphic green alga Ulva. The percent cov- stage is by at least four different reported methods: erage data for the exclosures and controls are sum- (1) fragmentation, (2) asexual production of quadrifla- marized by month for the 2.5-yr period in Table 1. The gellate zoospores, (3) asexual production of akinetes number of plots in which each alga was present is also (nonmotile spores), and (4) sexual reproduction. In the given as a measure of the extent to which the alga last, the zygote develops into a free-living "Codiol- occurred over the study areas. In summer the algal urn" stage that penetrates the encrusting red alga Pet- covers within the exclosures were much greater than rocelis (Abbott and Hollenberg 1976). Chapman and those in the controls for the same months and were Chapman (1976) also report "Gomontia" as the alter- comparable to the natural algal blooms of the winter nate stage of Urospora. months. Experiments and observations.-To investigate sea- From March through October Bangia, Urospora, sonal variations in the effects of limpet grazing on and Porphyra formed higher percent covers and oc- populations of high intertidal algae, sets of limpet ex- curred in more plots of the exclosures than in the con- closures and controls (4-5 of each per set) were trols. With the possible exception of Porphyra, these established at 3-4 mo intervals staggered over a period genera were continually present throughout the year of 2.5 yr. A total of 46 exclosures and 45 controls was in the exclosures as compared to being ephemerally set out in this series of experiments. Each set of study present in the controls. September was the only month plots was randomly selected from a much larger group in which no Porphyra was recorded in an exclosure. of plots that had been chosen earlier for their relative The probable explanation for this is that a total of only similarity. Within each set of study plots, exclosures six exclosures was censused in this month, and that and controls were again designated randomly. The size these six exclosures were probably too new for Por- and shape of a plot was determined by its topography: phyra to have established. Three other, older exclo- the average area of the study plots was 1651 cm2. sures not censused in September, but censused shortly There was no significant difference between the mean before and after (28, 29 August 1972 and 5 October areas of the control and exclosure plots (P > .4). 1972), contained Porphyra on both dates, suggesting Cageless methods were used to exclude the limpets that this alga was present in September as well. since in this high intertidal habitat cages themselves The months of lowest abundance of algae in the con- would be expected to reduce the physical stresses of trols were April and October. In April none of the desiccation, insolation, and high temperatures, as well upright morphs was found in the 13 controls censused, as reduce grazing. A continuous strip of copper paint while Bangia and Urospora were found in 12 and 11 kept the limpets out of the exclosure plots; a discon- of the 13 exclosures, forming up to 26 and 23% covers, tinuous strip of the paint was applied around controls. respectively, with both averaging 3% overall in pure This paint was effective only in the exclusion of lim- stands. In mixed stands, Bangia and Urospora ranged pets; littorinid snails and arthropod grazers were not up to 51% cover with an average over all the exclo- prevented from entering the exclosures. Further de- sures of 15% cover. Porphyra was more rare, but oc- tails of this exclosure technique are reported in Cubit curred in five of the 14 plots. Its percent cover aver- (1975). aged over all exclosure plots was 2% and up to 1% Algal abundance was measured as the percent cov- in individual plots. erage of each genus and was estimated by projecting In October Urospora was the only alga of this group a stratified-random array of points onto color trans- found in the controls: it occurred in trace amounts in June 1980 HERBIVORY AND ALGAL LIFE HISTORIES 683

TABLE1. Monthly comparisons of algal covers in limpet exclosures and controls on the Oregon coast. Treatments were set up over a 2.5-yr period and monitored for 6 mo. Percent covers shown are overall means for each month followed by the minima and maxima, respectively, in parentheses. Percent covers of pure and mixed stands of Bangia and Urospora are presented separately (Bangia, Urospora, and B-U mix). The figures for the number of plots in which an alga occurred include plots in which there were only trace amounts (<0.5% cover) of the alga. These occurrence data for Bangia and Urospora are totals for all the plots in which the alga was present regardless of its being in mixed or pure stands. See text for further explanation.

Exclosures Controls Por- B-U Por- N Bangia Urospora B-U mix phyra Total N Bangia Urospora mix phyra Total Jan. % cover No. plots with this alga Feb. % cover No. plots with this alga Mar. % cover No. plots with this alga Apr. % cover No. plots with this alga May % cover No. plots with this alga June % cover No. plots with this alga July % cover No. plots with this alga Aug. % cover No. plots with this alga Sept. % cover No. plots with this alga Oct. % cover No. plots with this alga Nov. % cover No. plots with this alga Dec. % cover No. plots with this alga two of the 20 controls. In the exclosures, however, Porphyra was also present in the exclosures in Oc- Urospora and Bangia were abundant in mixed stands, tober: it was present in six of the 21 exclosures, av- occurring together in 12 of the 21 exclosures, aver- eraging 2% cover overall, and ranging up to 25% cov- aging 25% cover overall and ranging up to 97% cover er. in individual exclosures. The extent and species composition of the algal cov- 684 JANE LUBCHENCO AND JOHN CUBIT Ecology, Vol. 61, No. 3 ers varied considerably among the exclosures; obser- curring crustose and boring "Ralfsia," "Conchocel- vations of colonization patterns within the exclosures is," and "Codiolum" stages such as the study by suggested that this variation resulted from competition Paine et al. (1979) for the crustose red alga Petrocelis among the algal species (as in the New England stud- middendorfJi. The crustose "Ralfsia" morphs in New ies) as well as from grazing by littorinid snails and England are known to be more grazer resistant than other small herbivores which were not excluded in are the upright morphs (Lubchenco 1978). From our these experiments. For instance, those exclosures field observations we infer that the Oregon crustose with a higher degree of structural complexity (crev- morphs and all of the boring morphs are also less ices, holes, barnacles, etc.) harbored higher densities vulnerable to being removed by herbivores. In the of nonlimpet grazers and developed lower percent course of our studies we have observed that the crus- covers of algae. This effect varied from plot to plot tose algae in general are more abundant in, if not en- according to the amount of shelter there. Observations tirely restricted to, areas where herbivores are com- that Porphyra was more common in those portions of mon and active. There is indication from other studies the exclosures where light grazing by littorinid snails that the establishment of at least some species of crus- and other herbivores had reduced the densities of fil- tose algae may require the removal of their upright amentous species of algae suggested that the abun- competitors by herbivores (Vine 1974, Adey and Vas- dance of Porphyra was negatively affected by com- sar 1975, Wanders 1977). petition, but favored by some grazing. There are few field studies applicable to the algae which penetrate or burrow into crustose algae, shells, and wood; however, we presume that within such sub- The results of the experiments presented here in- strata the boring morphs are sufficiently protected dicate that herbivory plays a substantial role in con- from herbivores that their survival exceeds that of the trolling the seasonal abundance of the upright thalli of upright morphs through seasons of, and in habitats of, certain common annual and ephemeral algae of the greater exposure to herbivory (Mumford 1973). (Some intertidal coasts of New England and Oregon. At the of these boring morphs may live within the shells of high algal densities that occurred within the herbivore the grazers themselves.) As with the crustose forms, exclosures, competition apparently also affected the herbivory may also be necessary to maintain the bor- abundances of some species. ing morphs. If the exteriors of the substrata occupied In New England, the upright thalli of Petalonia, by these algae were to become covered with other Scytosiphon, Ulothrix, Bangia, and Porphyra are nor- algae, the algae below the substrate could be smoth- mally winter annuals, but in the experiments where ered or shaded out. they were protected both from herbivores and com- The preceding experiments and observations indi- petitors, they were present in other seasons of the cate that increases of grazing intensity in summer can year. In the field experiments protecting them only prevent the year-round survival of the upright stages from herbivores, these algae still occurred out of sea- of the algae we studied. Thus we suggest that a pri- son, but to a lesser extent than when competitors were mary adaptive value of the nonupright crustose and also removed. In the laboratory experiments, the up- boring stages of these species is both in their ability right thalli of these algae are all highly preferred food to persist through times when the uprights are re- of the common grazers (Lubchenco 1978). Thus graz- moved by grazers and to exist in areas of persistently ing is probably important in ultimately determining the heavy grazing where the upright stages themselves seasonal abundance of the upright morphs. cannot survive. We suggest, however, that under con- On the high intertidal rocks in Oregon, the upright ditions of light grazing the upright stages are compet- morphs of Bangia, Porphyra, and Urospora are also itively superior and have the additional selective advan- primarily winter annuals. Although individuals of tages of rapid establishment, fast growth to reproductive these species may be found at other times of year at maturity, and subsequent production of large numbers lower intertidal levels (and occasionally at higher of propagules. We suggest that for plants such as these levels) the bulk of the populations in the high intertidal in mid to high intertidal habitats, a single type of plant zone occur during the winter (Table 1 "controls"). In cannot serve both functions well, because the adap- the protection of the limpet exclosures these algae tations which confer protection from herbivores are were present and common throughout the year. Den- mutually exclusive with those required for competitive sities of possibly competing species were not experi- superiority, rapid colonization, and high rates of re- mentally manipulated in the Oregon studies. However, production as discussed below. If this is correct, in observations of successional sequences and other habitats of spatially and temporarily heterogeneous growth patterns within the limpet exclosures suggest patterns of grazing, a heteromorphic alga will be more that interspecific competition also may have affected successful than one which is isomorphic. the relative abundances of these algae. Among the adaptations of the nonupright stages Areas yet to be investigated are the demography which may provide protection from herbivores are the and other aspects of the ecology of the naturally oc- following: (1) In the crustose forms muth of the thallus June 1980 HERBIVORY AND ALGAL LIFE HISTORIES 685

TABLE2. Predictions of the predominant life history for mid to high intertidal ephemeral algae under different grazing regimes, according to the definitions and constraints indicated in the footnotes.

If grazing pressure* is: Then we predict: a. Light Isomorphology: competitively superior morphs 1. Constant and (uprights) predominate b. Heavy Isomorphology: grazer-resistant morphs (e.g. crusts and borers) predominate a. Predictable$ Heteromorphology: alternation of production and 2. Variable? and predominance of morphs (e.g. seasonally) b. Unpredictable Heteromorphology: continuous production, but not survival, of both morphs

* The probability that a given individual alga will be removed by herbivory In a given period of time. 7 Grazing pressure fluctuates with the condition that periods of high and low grazing pressure exceed generation tlrnes of nonupright and upright rnorphs, respectively. $ Fluctuations in grazing pressure can be forecast (e g., by correlat~onswith time or other cues from the environment). adheres tightly to the substratum; thus the whole thal- gae may be under bimodal seiection pressures, simul- lus is not lost if an herbivore removes a small portion taneously evolving toward opposing ends of the r and at the base. (2) The thallus is tough, formed of many K continuum of selection. However, if our arguments layers of cells compacted together, and thus may be above are correct, the upright stages exhibit both r more difficult to graze. (3) Some Ralfsia are reported and K characteristics: rapid growth, early maturity, to contain tannins (Conover and Sieburth 1966) which and high reproductive output (r) as well as competitive may be herbivore deterrents. (4) The burrowing forms superiority (K), and the bimodality of selection exists are presumably protected from herbivores by being between this combination and the ability to withstand within other crustose algae or hard substrata such as grazing. shells and wood. In the following discussion we define the term graz- Among the adaptations of the uprights that might ing pressure as the probability with which a given in- contribute to higher growth rates at the expense of dividual alga will be removed by herbivory in a given resistance to herbivory are the following: (1) Since period of time. If the preceding explanations are cor- most of the surface of an upright thallus neither ad- rect we would predict that the relative proportions of heres to the substratum nor is buried in it, and the heteromorphic and isomorphic algae should vary from thallus is either filamentous or only a few cells thick, habitat to habitat according to the seasonal fluctua- the ratio of exposed surface to internal volume of the tions of grazing in those places. In areas where grazing plant is greater than in the nonupright forms. This al- pressure does not fluctuate, we would expect iso- lows potentially higher growth rates through more rap- morphic algae (either upright or nonupright) to pre- id assimilation of nutrients (Odum et al. 1958, Fogg dominate, the type of morph being determined by 1965) and a higher ratio of photosynthetic area per unit grazing intensity (Table 2). If grazing pressure were biomass. (2) Upright forms presumably allocate less constantly low, the upright morphs should outcompete energy and material for attaching themselves to the the nonupright morphs (Table 2, la). If grazing pres- substratum or burrowing through it. (3) With small sure were constantly high, the uprights should be re- points of attachment, the uprights require less space moved and the nonuprights survive in their place (Ta- per unit biomass than the crustose forms, an adapta- ble 2, lb). Under such conditions, algae with obligate tion that is important in space-limited habitats of the alternations of heteromorphic generations should intertidal zone. (4) The uprights are probably not as eventually disappear as one morph or the other is elim- restricted in substrate requirements as are the burrow- inated by competition or grazing. Those algae with ing forms. alternations of heteromorphic generations that are not As noted earlier it has been suggested that the crus- obligate may have one morph survive, but it should be tose and boring stages of heteromorphic algae serve at a lower relative fitness than similar, but isomorphic, as perennating phases through the seasons when the species in which no reproductive efforts are wasted on upright stages are unable to tolerate the physical producing the morphs which do poorly in these con- stresses of the habitat (Wynne 1969, Conway et al. ditions. 1976). Low surface-to-volume ratios and living within In contrast, where grazing pressure does fluctuate perforations of the substrate probably do render these from season to season, conditions should alternately nonupright forms more resistant to desiccation and the favor upright, then nonupright morphs, resulting in damaging effects of insolation and high temperatures. selection for seasonal alternation of these morphs We agree that the nonupright stages serve as peren- (Table 2, 2a). Greater fitness should accrue to those nating phases, but suggest that grazing and perhaps heteromorphic algae which allocate their resources competition should be considered as important factors into the production of nonuprights and uprights in syn- preventing the upright stages of these algae from being chrony with the grazing changes. Just prior to the on- perennial. set of the seasons of increased grazing it should be to Vadas (1979) has suggested that heteromorphic al- the advantage of an upright alga to convert its re- 686 JANE LUBCHENCO AND JOHN CUBIT Ecology, Vol. 61, No. 3 sources to the grazer-resistant morph rather than have bivores by predators, or seasonal influx of algal drift these resources consumed by herbivores. Similarly, may also operate to reduce grazing at other times of selection should favor those algae concentrating their year and change the selective regime for the timing of production of uprights in the seasons of reduced her- production of the various morphs of the heteromor- bivory (Table 2, 2a). phic algae. In other words, rather than the seasonal Finally, if grazing pressure fluctuates in an unpre- abundance of these different morphs being dependent dictable manner, both morphs should be present con- on the timing responses of the plants, the timing re- tinually (Table 2, 2b). Each morph will be favored at sponses are probably dependent on the seasonal sur- some time, but prediction of precisely when is not vival of these morphs. possible. Thus each plant should be most fit by pro- Our experiments do not address factors involved in ducing offspring of both morphs. the origin of heteromorphology; they demonstrate According to this scheme, the New England and only that variation in the grazing regime may maintain Oregon studies reported above are examples of Table this adaptation in the species investigated. 2, 2a in which uprights are favored during the winter The hypotheses and predictions put forth in this pa- months and nonuprights during summer months. In per are not intended to explain the occurrence of het- our field studies, decreases in grazing pressure occur eromorphology in all algae. Rather, we have focused in winter and increases occur in summer. Numerous on one of the mechanisms that may be involved in factors in the physical environment are correlated with selection for heteromorphology of common species the grazing changes and could be used by an alga as that have annual or ephemeral upright thalli in the mid cues to change from one morph to another. These fac- and higher littoral zones. Since the morphologies of tors include temperature, insolation, photoperiod, stages and the patterns of life cycles in other hetero- desiccation, wave force, and salinity. Laboratory cul- morphic algae differ from those we have studied, the turing experiments have demonstrated that the switch selective mechanisms probably also differ. Moreover, from upright to nonupright morphs or vice versa is the hypotheses presented in this paper are subject to under photoperiodic or temperature control or both further testing, particularly regarding the ecology of for Petalonia, Scytosiphon, Bangia, and Porphyra the nonupright stages. For example, more information (Dring 1967, Wynne 1969, Bixon and Richardson 1970, is needed on (1) the demography and phenology of the Sommerfeld and Nichols 1973, Roeleveld et al. 1974). crustose and boring stages, (2) the relative competitive In the Oregon study areas species of Porphyra were abilities of uprights vs. nonuprights, and (3) effects of observed to liberate spores during the first series of other factors, e.g., seasonal burial and scour by sand daytime low tides and warm weather in the spring. which might act similarly or in addition to grazing in For the algae discussed here, it makes little differ- selecting for heteromorphology. ence which cues are used for timing, providing the cues are closely correlated with the seasonal increases and decreases in the probabilities of being consumed We thank the following people for field assistance or com- by herbivores. The strength of selective pressure to ments on versions of this manuscript: L. Ashkenas, R. W. respond to these cues should depend on the closeness Day, P. K. Dayton, S. D. Gaines, M. E. Hay, J. A. Kilar, of the correlation. Conceivably there are environ- E. G. Leigh, B. A. Menge, T. F. Mumford, Jr., J. N. Norris, ments in which the seasonal variations in grazing pres- R. T. Paine, W. P. Sousa, J. A. West, S. D. Williams, and two anonymous reviewers. J. Lubchenco is grateful to N. W. sure are the reverse of those in our study areas; in Riser for use of Northeastern University's Marine Science such areas we would expect opposite responses to the Institute, Nahant, Massachusetts. This paper is contribution same cues, all other factors being equal. The mecha- 51 from that laboratory. J. Lubchenco's research was sup- nisms which we suspect cause the variations of grazing ported by National Science Foundation Grants GA-40003 to J. Lubchenco and GA-35617 and DES72-01578-A01 to B. Menge. pressure in New England and Oregon might follow J. Cubit thanks P. Frank and S. Cook for helpful discussion, other seasonal patterns on other coasts. In New En- T. F. Mumford, Jr. for identifying specimens of Porplzyra, gland the winter reduction in grazing is apparently the and Sigma Xi for a grant-in-aid of research. result of wave action causing littorinids to decrease their grazing activities during the winter months (J. Abbott, I. A., and G. J. Hollenberg. 1976. Marine algae of Lubchenco Menge 1975). Evidently this same phe- California. Stanford University Press, Stanford, California, nomenon also occurs on parts of the Oregon coast USA. where storm-generated waves decrease the densities Adey, W. H., and J. M. Vassar. 1975. Colonization, succes- andlor activities of littorinids (Castenholz 1961, Beh- sion, and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologia 14:55-69. rens 1974, Cubit 1975). In the particular Oregon study Behrens, S. 1974. Ecological interactions of three Littorina areas described in this paper the winter decrease in (Gastropoda, Prosobranchia) along the west coast of North grazing pressure apparently results from a swamping America. Dissertation. University of Oregon, Eugene, Or- of the grazing capacities of the limpet populations by egon, USA. increased algal productivity rather than a reduction of Bird, C. J. 1973. Aspects of the life history and ecology of Porphyra linearis (Bangiales, Rhodophyceae) in nature. the grazing activities of the limpets (Cubit 1975). In Canadian Journal of Botany 51:2371-2379. other habitats factors such as seasonal removal of her- Bird, C. J., L. C.-M. Chen, and J. McLachlan. 1972. The June 1980 HERBIVORY ,4ND A1-GAL LIFE HISTORIES 687

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You have printed the following article: Heteromorphic Life Histories of Certain Marine Algae as Adaptations to Variations in Herbivory Jane Lubchenco; John Cubit Ecology, Vol. 61, No. 3. (Jun., 1980), pp. 676-687. Stable URL: http://links.jstor.org/sici?sici=0012-9658%28198006%2961%3A3%3C676%3AHLHOCM%3E2.0.CO%3B2-H

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The Biology of Brown Algae on the Atlantic Coast of Virginia. II. Petalonia fascia and Scytosiphon lomentaria Russell G. Rhodes; Mary U. Connell Chesapeake Science, Vol. 14, No. 3. (Sep., 1973), pp. 211-215. Stable URL: http://links.jstor.org/sici?sici=0009-3262%28197309%2914%3A3%3C211%3ATBOBAO%3E2.0.CO%3B2-G

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