Download Heteromorphic Life Histories of Certain Marine Algae as Adaptations

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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Ecoloyy, 61(3), 1980, pp. 676-687
1980 by the Ecological Society of America
HETEROMORPHIC LIFE HISTORIES O F CERTAIN MARINE ALGAE AS ADAPTATIONS TO VARIATIONS I N HERBIVORY1 JANEL U B C H E N C O ~ ' ~
Depurtment of Zoology, Oregon State University, Corvullis, Oregon 97331 U S A AND
JOHNCUBIT^'^
Depurtment of Biology, University of Oregon, Eugene, Oregon 97403 U S A 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.
Heteromorphic algae exhibit a high degree o f independence and differentiationamong the stages o f their
life cycles. Most o f the particular heteromorphic algae
discussed in this paper have two separate, in some
cases self-propagating, and ecologically distinct phases which are so dissimilar in appearance that until recently they had been classified as separate species,
and, in some cases, had been placed in separate families or orders.
Istock (1967) has proposed that evolutionarily such
life cycles should be inherently unstable: as selection
acts independently on the separate stages, one stage
should eventually be eliminated or reduced in favor o f
the other. He cites as examples the loss or reduction
o f larval or adult stages in some insects, cnidarians,
and amphibians. Another more pervasive set o f examples is the loss o f the free-living, haploid, gametophyte stage from the life cycles o f most plants and
animals.
However, Istock (1967, 1970) points out there are
a number o f counterexamples with apparently long- ' Manuscript received 14 February 1979; accepted 1 June
1979; final version received 29 August 1979.
Order of authorship determined by coin toss.
In previous publications, J. Lubchenco Menge.
Present address: Smithsonian Tropical Research Institute, APO Miami, Florida 34002 USA.
established, stable life cycles involving several ecologically distinct stages. T o these we add certain heteromorphic algae, which by Istock's (1967) criteria
should be particularly evolutionarily unstable: the
stages are often found under different growing conditions, and some, rather than being larva-like developmental stages, are capable o f independent self-propagation that allows them to persist indefinitely in the
absence o f any other stage.
Algae with various types o f heteromorphic life
cycles are both phylogenetically and ecologically widespread: heteromorphic algae occur in the three major
divisions o f macroalgae (Chlorophyta, Phaeophyta,
and Rhodophyta) and are found in a variety o f habitats. However, in this paper we concentrate on those
species o f heteromorphic algae which comprise much
o f the macroalgal portions o f seasonal or ephemeral
blooms in the mid to high intertidal zones o f rocky
shores. These species are in the following divisions and
genera: Chlorophyta: Ulothrix and Urospora; Phaeophyta: Petalonia and Scytosiphon; Rhodophyta:
Bangia and Porphyra. Although the algae in this group
are taxonomically quite different,their life cycles and
morphologies have much in common. Each species
has two primary stages: the stage which appears in the
periodic algal blooms is an upright filament, tube, or
blade; the other is a nonupright crust or boring stage.
( A third stage, a small filamentous tuft, is also known
for Petalonia and Scytosiphon.) The convprgence in
June 1980
HERBIVORY AND ALGAL LIFE HISTORIES
the patterns o f life cycles o f these algae suggests their
forms and life histories may be adaptations to a common set o f selective factors; thus, these plants provide
a system to examine the mechanisms by which complex life cycles are selected and maintained. The main
question addressed in this paper is the following: what
is the adaptive significance o f the heteromorphic life
cycles o f these intertidal algae?
An explanation already proposed is that the nonupright morphs are perennating stages which survive
through the physically harsh seasons when the upright
morphs are killed by such stresses as desiccation, insolation, and high temperatures (Conway et al. 1976).
A second hypothesis occurred to each o f us during
our independent studies on the effects o f herbivores
on benthic marine algae. W e observed that in several
heteromorphic species the upright morphs could survive in physically harsh seasons i f protected from herbivores, and that the nonupright morphs were either
themselves grazer-resistant or specifically exploit microhabitats which we infer protect them from grazing.
In this paper we suggest the hypothesis that spatial
and temporal variations in grazing play a major role
in the selection and continued maintenance o f the different morphologies in these life cycles. In the following sections we present the results o f experiments testing this hypothesis on the east and west coasts o f the
United States: in New England (studies o f J.L.) and
in Oregon (studies o f J.C.). Alternate hypotheses and
ways to test them are suggested in the discussion section. I f our interpretations are correct, we predict that
in less variable environments algae with heteromorphic life cycles would not be maintained in such abundance and, instead, algae with isomorphic life cycles
would increase in relative proportion.
677
SEASONAL
CYCLES
OF
:
HERBIVORE ACTIVITY
ULOTHRIX
k
m
B m A
PORPHYRA
vL ' %
O N D
J
F
M
A
M
J
J
A
S
O
FIG. 1 . Subjective evaluations of percent of gastropod
herbivore individuals active and of the relative abundance of
the upright morphs of five heteromorphic algal species on the
New England coast during the year. The herbivores are primarily Littorinu littorea, but also include other snails: L. obtusuta, L . saxatilis, Lucunu vinctu, Murgurites helicinu, and
Acmaea testudinulis. Herbivores not included are isopods,
amphipods, and diptera. Each algal species was recorded as
being common (C), present (P), or absent (A) at each study
area at least monthly for 3 yr. Study areas where gastropod
herbivores are common (protected to intermediate in exposure to wave action) are indicated by the solid portions.
Areas where gastropod herbivores are rare or absent (exposed sites) are indicated by cross-hatching. Scytosiphon,
Petuloniu, and Porphyra are able to persist longer in exposed
sites. Crustacean herbivores are often abundant at more exposed sites. Their effect on algae is yet to be determined.
The life histories o f these algae are as follows:
1 ) Petalonia fascia (0. F . Miill.) 0 . Kuntze and
Scytosiphon lamentaria (Lyngb.) Link (Phaeophyta:
Scytosiphonaceae).
The upright morphs o f both o f these algae are "winter annuals" in New England (Fig. 1 , Taylor 1957,
Kingsbury 1969). The upright blades of Petalonia (7.545 cm long) and upright tubes o f Scytosiphon (15-70
cm long) appear in tide pools and on the shore from
N e w 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 o f the tar-like crusts previously thought to be species o f Ralfrocky shores o f 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 seaAg.) C. Ag., P. linearis Grev., and P. umbilicalis ( L . ) sonal occurrence o f the ralfsioid crust morph is diffiJ. Ag., and the possibly heteromorphic green alga Ulo- cult to assess accurately because these crusts are difthrix flucca (Dillw.) Thur. in LeJolis. Observations ficult to distinguish in the field from other, valid
were made on all o f 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 sumtosiphon. These plants were studied at four study mer than in the winter in New England.
areas in Massachusetts ( M A ) and Maine ( M E ) from
Petalonia and Scytosiphon differ somewhat in the
fall 1971 until summer 1977. The areas are nonestua- specifics o f 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, M A ; Grindstone Neck, ME; East These gametes do one o f three things: ( 1 ) develop parPoint, 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
tufts or (3) fuse, with the zygote developing into a
(1975)and B. Menge (1976).
678
JANE LUBCHENCO AND JOHN CUBIT
diploid "Ralfsia" crust or tuft. Both haploid and diploid crusts or tufts produce zooids which develop into
upright tubes. Meiosis occurs only when diploid crusts
or tufts form zooids. Wynne (1969) found that his
"Ralfsia" could also produce more "Ralfsia" crusts.
Thus in this species the upright morph is haploid while
the other can be either diploid or haploid, indicating
a partial decoupling o f the morphological and genetic
components.
This decoupling is complete in Petalonia, where all
stages (crusts, tufts, and blades) appear to be of the
same ploidy number. No evidence o f sexuality has
been reported. "Ralfsia" crusts or tufts produce
zooids which develop into either more "Ralfsia," or
tufts or Petalonia blades. Blades produce swarmers
which develop into either crusts, tufts, or blades
(Wynne 1969, Wynne and Loiseaux 1976).
Neither o f these species represents the classical picture o f a strict alternation o f generations (haploid with
diploid). More significantly, both species appear to
possess tremendous morphological flexibility, each
morph being able to produce either more individuals
like itself or the other alternate morph. In other words,
neither genetic nor morphological alternation is obligate. W h y then are there two distinct morphs, each
with this plasticity?
Proximate factors affecting which morph is produced have been investigated in the laboratory. In numerous culture studies, blades o f Petalonia and tubes
o f Scytosiphon were found to be produced mainly under simulated "wintertime conditions ," i.e., short
daylength photoperiods and cool temperatures. The
"Ralfsia" crusts or tufts were obtained under laboratory "summertime conditions," i.e., long daylength
photoperiods and warm temperatures (Wynne 1969,
Roeleveld et al. 1974, Dring and Luning 1975, Nakamura and Tatewaki 1975).
It seems significant that in these laboratory culturing
experiments there was usually some variation in the
response o f plants to temperature and photoperiod;
that is, a small percentage o f the progeny became the
"wrong" morph for a particular set o f conditions
(Wynne 1969, Roeleveld et al. 1974). For example, in
three o f Wynne's experiments with Petalonia, 5-20%,
5-10%, and 0% o f the progeny developed into blades
under summertime conditions (18"-1YC, 16 h light-8
h dark). The potential significance o f this variation will
be discussed below.
Both species' laboratory behavior generally corresponds to their seasonal occurrence in New England:
uprights are produced under wintertime conditions,
and crusts appear primarily under summertime conditions.
2) Bangia fuscopurpurea (Dillw.) Lyngb. (Rhodophyta: Bangiaceae).
This species has two very different phases in its life
history: upright, macroscopic plants which are uniseriate or multiseriate filaments, and an endolithic fila-
Ecology, Vol. 61, No. 3
mentous form previously known as "Conchocelis. "
Upright plants are dioecious and produce two o f three
possible types o f spores: ( 1 ) "monospores" or "neutral spores" which develop into more upright filaments
and one o f the following types o f spores (2) "carpospores" or "alpha spores" which germinate to give
rise to the "Conchocelis" phase, or (3) "spermatia"
or "beta spores" that presumably act as male gametes
and fuse with the cells that develop into carpospores.
The "Conchocelis" phase produces two types o f
spores: ( 1 ) "monospores" which develop into more
' 'Conchocelis " plants, and (2) ' 'conchospores' ' which
develop into the macroscopic upright phase (Sommerfeld and Nichols 1970). Both photoperiodism (Richardson and Dixon 1968, Dixon and Richardson 1970,
Richardson 1970) and temperature (Sommerfeld and
Nichols 1973) have been shown to control the formations and release o f spores o f both phases o f the life
history in the laboratory. In New England, the upright
Bangia filaments measure =lo-20 mm in length and
0.15 mm in diameter and usually appear in DecemberFebruary and persist through March-May (Fig. 1).
The seasonal occurrence o f the "Conchocelis" phase
is not known; however, the plants have been found in
intertidal mollusc and barnacle shells (Bird 1973). The
"Conchocelis" phase is thought to be perennating.
3) Porphyra umbilicalis ( L . ) J . Ag., P. miniata (C.
Ag.) C. Ag., and P . linearis Grev.
As in Bangia, the life history o f these species involves two different phases with different morphologies. The macroscopic Porphyra thalli discussed here
are leafy sheets usually ranging in size from 3 to 15 cm
long, are haploid, and alternate with a "Conchocelis"
phase (as described for Bangia) which is usually diploid and which bores into and lives in calcareous substrates.
There exists considerable variation among the
species with respect to seasonal occurrence and specifics o f the life history (Conway 1964, Edelstein and
McLachlan 1966, Chen et al. 1970, Bird et al. 1972,
Bird 1973, Bold and Wynne 1978, Hawkes 1978). The
foliose phase o f P. linearis is a high intertidal winter
annual. Since no neutral spores are formed by the
blades and the basal portion does not perennate,
blades must come solely from conchospores. Conchospores are released only at 13°C in culture, but can
be found throughout the year in the intertidal. The
"Conchocelis" phase has been found in subtidal mussel (Modiolus modiolus) shells (Bird et al. 1972, Bird
1973). The foliose thallus o f P. miniata occurs in the
mid and low intertidal and subtidal regions from spring
to summer. All blades apparently come from conchospores. Conchospore release is triggered in the laboratory at temperatures <13"C (Chen et al. 1970). P.
umbilicalis has several upright forms: ( 1 ) perennial rosettes present in the high zone (Edelstein and McLachlan 1966), (2) an elongated morph that appears in
the winter in mid zones, and (3) a persistent blade
June 1980 HERBIVORY A N D ALGAL LIFE HISTORIES
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 ) .
Species o f Porphyra could not always be distinguished
and are lumped together here.
4 ) Ulothrix flacca (Dillw.) Thur. in LeJolis (Chlorophyta: Ulotrichaceae).
Both isomorphic and heteromorphic life cycles have
been described for U . flacca elsewhere. Perrot (1972)
suggests that in France it is really two separate
species, one isomorphic and occurring in the very high
intertidal zone and the other heteromorphic and occurring lower. The isomorphic species, termed "Form
A" by Perrot, has upright, filamentous gametophytes
and sporophytes. Each stage reproduces to form either
more plants o f the same or the alternate stage. The
heteromorphic species, "Form B," has dioecious, upright, filamentous gametophytes which produce two
types o f cells: ( 1 ) zoospores which develop directly
into more upright gametophytes and (2)gametes which
fuse to form a zygote that develops into a discoid sporophyte resembling the green prostrate Codiolum.
This Codiolum-like stage produces aplanospores
which develop directly into upright gametophytes.
Both photoperiod and temperature are involved as
cues in this nonobligate alternation.
The life histories o f the New England U .flacca have
not been investigated, but circumstantial evidence
suggests that at least the heteromorphic form is present. Ulothrix occurs as long, slender filaments (10-70
m m long, 0.15 mm in diameter) forming dense mats
which are common throughout the intertidal region
from October-November to March-May (Fig. 1).
When Ulothrix disappears during the spring, "Codiolum" appears and persists throughout the summer
and fall.
Herbivore occurrence and algal preference.-The
most abundant herbivore in the New England rocky
intertidal zone is the common periwinkle snail Littorina littorea which occurs in tide pools and on emergent substrata where these heteromorphic algae are
found ( J . Lubchenco Menge 1975, Lubchenco 1978).
Littorina is usually active from spring (March-May)
to late fall (October-November, Fig. I), at just the
time when the upright morphs o f Scytosiphon, Petalonia, Bangia, Porphyra, and Ulothrix are absent (Fig.
1).
Laboratory preference experiments indicate that
Littorina will readily eat the upright morphs o f all o f
these species, but not the crustose forms (Lubchenco
1978). Crusts like these are not totally herbivore resistant, but are much less preferred than are the upright morphs or many other nonheteromorphic upright
species.
679
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! 50
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0-,
,o S@asiphm
...,
\
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x---x
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A M J J A S O N D J F M A M J J A
1973
1974
FIG. 2. Effect of herbivores on the occurrence of Petaloniu and Scytosiphon in the high intertidal zone at Grindstone Neck, Maine. The numbers below each treatment title
indicate the mean number of grazers present and 95% confidence interval. L.1. = Littorina littoreu, L.o. = L . obtusata,
L.s. = L . saxutilis. Ephemeral algae are those plants that
usually persist for short periods of time during the year. Petuloniu and Scytosiphon are ephemeral species by this definition, but are separated from the rest of the ephemeral algae
since they are the focus of this experiment. The other ephemeral species appearing in this experiment include some heteromorphic and some nonheteromorphic uprights: Bangia
fuscopurpureu, Dumontia incrussata, Porphyra spp., Rhizoclonium tortuosum. Spongomorpha sp., and Ulothrixjucca. Separate percent cover values for each species were
usually taken; occasionally some species were mixed together so thoroughly that it was necessary to lump them together
(as for Scytosiphon and Petulonia in A and B). The approximate period of seasonal inactivity of the herbivore, 1,ittorinu
littoreu, is indicated by the bar at the top of the figure. See
text for details of treatments.
Field herbivore exclusions: design.-During the
course o f a general investigation o f the effects of rocky
intertidal herbivores on algae in New England, a series
o f 10 x 10 x 3 or 10 x 10 x 5 cm stainless steel mesh
cages were attached to the rock and used to exclude
or enclose various herbivores (see J. Lubchenco
Ecology, Vol. 61, No. 3
JANE LUBCHENCO A N D JOHN CUBIT
Herbiwres inactive
'"1
0
A. CONTROL
D
HERBIVORE
C. L
F
HERB. EXCL.,
LITTOREA ENCLOSURE
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4 LI
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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 experiments was specifically designed to test the effects of
Littorina on Petalonia, Scytosiphon, and their ralfsioid crusts; additional information on these interactions was obtained as a by-product of other experiments.
Each experiment consisted of at least the following
four treatments: (1) an unmanipulated control (no cage
or roof); (2) a roof control (tests for shading effects of
the mesh; herbivores have normal access to the area
underneath the roof); (3) a Littorina littorea enclosure
(four periwinkles, usually 1.2-2.0 cm in length enclosed in a cage; this biomass is within the range normally occurring in nonexperimental areas); and (4)
herbivorous gastropod exclusion. In all treatments,
herbivores such as isopods or amphipods could
and did enter the cage. Various other treatments were
added as deemed necessary. For example, an herbivore exclosure from which the brown alga Fucus or
ephemeral algae was removed was used to separate
effects of herbivores from effects of potential algal
competitors on Petalonia or Scytosiphon.
Experiments were established at two sites. One set
was in the high intertidal zone (+ 1.87 m) at Grindstone
Neck, on flat, horizontal granite with a cover of
ephemeral algae but no algal crusts (Fig. 2). The other
was on flat, horizontal substratum in the mid zone
(+0.4 m) at Canoe Beach Cove, with no upright algae
but with traces of the red crust Hildenbrandia rubra
(Fig. 3). The remainder of the primary substratum in
this experiment was bare, i.e., lacked macroscopic
plants or animals. Both experiments were on emergent
substrata, i.e., exposed to air at low tide (as opposed
to being in tide pools).
Field herbivore exclusions: results.-The results in
Fig. 2 support the hypothesis that grazing by L. littorea, not inability to withstand summertime conditions, caused the absence of Petalonia blades and
Scytosiphon tubes during the summer. In the
unmanipulated control and the roof control (Fig. 2A,
B), with periwinkle grazing in the spring, summer, and
fall, Petalonia and Scytosiphon appeared only during
the winter (December-February). Where L. littorea
was excluded (Fig. 2D, E), Petalonia also appeared
during the "wrong" time of the year, i.e., in the summer (July-August 1974), and Scytosiphon also colonized out of season, i.e., in the spring and summer
(May-July 1975). Where L. littorea was enclosed (Fig.
2C), neither Petalonia nor Scytosiphon nor any other
heteromorphic uprights ever appeared even in the winter. Ralfsioid crusts were not observed in any of these
treatments, but were present in the general area.
The abundances of Petalonia and Scytosiphon in the
herbivore removal experiments were inversely related
to the abundances of various ephemeral algae, suggesting that Petalonia and Scytosiphon may compete
with other ephemeral algae (Fig. 2D, E) when herbivores are absent. The experiments in Fig. 3 tested this
hypothesis. This cage set was in the mid intertidal
zone where L. littorea is more abundant than in the
June 1980
HERBIVORY A N D ALGAL LIFE HISTORIES
high zone experiments of Fig. 2. Here again, Petalonia
and Scytosiphon occurred in the control and roof only
during the wintertime when the snails are usually less
active (Fig. 3A, B). Where L. littorea was enclosed in
cages (Fig. 3C), it prevented most algae (including
Petalonia and Scytosiphon) from becoming established, even in the winter. L. littorea usually retreat
to crevices during the winter and seldom (but occasionally) forage. Snails enclosed in cages do feed, but
at reduced rates as compared with the summer. Thus
caged snails can evidently prevent even wintertime
occurrence of most algae, unless very dense settlement of algae (swamping) occurs. Where herbivores
were excluded (Fig. 3D, E , F), algae were more abundant. The particular kind of alga that comes in is probably a function of the plants which are available to
colonize and of competitive interactions between
those plants which do settle (J. Lubchenco Menge
1975, Lubchenco and B. Menge 1978, J. Lubchenco,
personal observation).
In all three exclosures (Fig. 3D, E, F) Petalonia
blades and sometimes Scytosiphon tubes appeared in
July, the "wrong" time of year for blades and tubes.
Where Fucus and ephemeral algae were continually
removed, Petalonia and Scytosiplzon continually colonized (Fig. 3F). In herbivore exclusion cages where
ephemeral species but not Fucus were removed, Fucus took over the cage (Fig. 3E) and neither Petalonia
nor Scytosiphon occupied primary space. (EAperiments on competitive interactions between Fucus and
various ephemeral species will be reported elsewhere.)
These results indicate that it is physiologically possible for Petalonia blades and Scytosiphon tubes to
exist during the summer months. These plants appear
to be normal and healthy, judging by their color and
size. Thus warmer temperatures or longer daylengths
neither kill nor stunt them. Similar results have occurred in a number of other experiments designed to
investigate other algae. Upright forms of Petalonia
and Scytosiphon appeared out of season in 33% of
15 herbivore exclusion cages where free space was
available (i.e., unutilized by other upright algae or animals; out of a total of 53 herbivore exclusion cages
in place for 1-5 yr at the four study sites). Moreover,
upright Petalonia and Scytosiphon can sometimes be
found in nonexperimental (uncaged) areas at the
"wrong" time of year. In the summer these plants
were generally in the mid and low zones, both in tide
pools and on emergent substrata. J.L. has observed
this only a few times in 5 yr, at more wave-exposed
areas, e.g., East Point and Pemaquid Point, where herbivores such as littorinids are less abundant and/or
less effective, and waves remove potential competitors more frequently. Other investigators have also
reported Petalonia and Scytosiphon occurring during
summer and fall months in New England at exposed
sites (Lamb and Zimmerman 1964, Mathieson and
68 1
Fralich 1972, 1973, M. H. Zimmerman,personal communication).
Thus the general pattern of Petalonia and Scytosiphon upright occurrence in the field corresponds to
laboratory culturing results: uprights occur during the
winter. The occurrence of a few uprights out of season
(either in herbivore exclusion cages or exposed sites
where herbivores are rare or ineffective) may be a
result of the small variation in plant response to photoperiod and temperature reported by Wynne (1969;
see above).
In similar herbivore exclusion and sometimes in
competitor removal cages, the other heteromorphic
species also appeared out of season. Uprights of Ulothrix, Bangia, and Porphyra were all observed during
June, July, and August when they are normally absent
(Fig. 1).
Oregon studies
Description of the sites and species studied.-The
Oregon studies were performed at two sites near Coos
Bay: South Cove of Cape Arago and Sunset Bay. The
study plots at each site were above the mean high tide
level on the wave-exposed sandstone rocks of the outer coast. (The level of the study areas corresponds to
"Zone 1," the uppermost intertidal zone, in the
scheme of Ricketts et al. 1969.)
At the tidal level of these study areas there are wet
and dry seasons which result from seasonally changing
weather conditions and tidal cycles. In the wet season
(late autumn, winter, and early spring) air temperatures are cooler, precipitation is greater, tidal levels
are higher during the daylight hours, and the rocks
receive more spray and wash from the waves generated by winter storms. During this season the high
rocks are almost continually wet, even at low tide. In
the dry season (late spring, summer, early fall) the
high intertidal rocks often dry out at low tide; this
pattern is modified in some years by cool, wet fogs in
the late spring and early summer (Cubit 1975).
In the areas of the study plots, the most abundant
herbivores in terms of biomass per unit area were the
acmaeid limpets, nearly all of which were Collisella
(=Acmaea) digitalis. Chironomid flies, gammarid amphipods, and littorinid snails were also occasionally
abundant in certain areas.
The abundance of algae at these sites varied with
the seasons. In the winter wet season there is a bloom
of microalgae (diatoms and blue-greens) and macroalgae. Nearly all of the macroalgae comprising this
bloom are in the genera treated in this paper: Bangia,
Porphyra, and Urospora. Most of these algae disappear from the high intertidal zone during the drier conditions of summer. These plants and their life cycles
are described below. (Bangia fuscopurpurea has been
described in the previous section.) All of these species
have heteromorphic life cycles.
682
JANE LUBCHENCO AND JOHN CUBIT
1) Porphyra perforata J. Ag., P. pseudolanceolata
Krishnamurthy , and P. schizophylla Hollenberg (Rhodophyta: Bangiaceae).
The general features of the life histories of these
species of Porphyra are similar to those described
above for this genus in New England. Most of the
Porphyra plants in the Oregon study areas were <5
cm wide and <10 cm long. Size and shape vary somewhat among the species. For these species, alternations of generations between the upright stages and
the "Conchocelis" stages may be obligatory, since no
other types of reproduction have yet been reported
(Mumford 1975, Conway et al. 1976).
2) Urospora perlicilliformis (Roth) Aresch. (Chlorophyta: Acrosiphoniaceae).
The upright, macroscopic plants are filamentous,
reaching a maximum size of 30-40 mm long and 0.06
mm in diameter. Reproduction in the macroscopic
stage is by at least four different reported methods:
(1) fragmentation, (2) asexual production of quadriflagellate zoospores, (3) asexual production of akinetes
(nonmotile spores), and (4) sexual reproduction. In the
last, the zygote develops into a free-living "Codiolurn" stage that penetrates the encrusting red alga Petrocelis (Abbott and Hollenberg 1976). Chapman and
Chapman (1976) also report "Gomontia" as the alternate stage of Urospora.
Experiments and observations.-To investigate seasonal variations in the effects of limpet grazing on
populations of high intertidal algae, sets of limpet exclosures and controls (4-5 of each per set) were
established at 3-4 mo intervals staggered over a period
of 2.5 yr. A total of 46 exclosures and 45 controls was
set out in this series of experiments. Each set of study
plots was randomly selected from a much larger group
of plots that had been chosen earlier for their relative
similarity. Within each set of study plots, exclosures
and controls were again designated randomly. The size
and shape of a plot was determined by its topography:
the average area of the study plots was 1651 cm2.
There was no significant difference between the mean
areas of the control and exclosure plots (P > .4).
Cageless methods were used to exclude the limpets
since in this high intertidal habitat cages themselves
would be expected to reduce the physical stresses of
desiccation, insolation, and high temperatures, as well
as reduce grazing. A continuous strip of copper paint
kept the limpets out of the exclosure plots; a discontinuous strip of the paint was applied around controls.
This paint was effective only in the exclusion of limpets; littorinid snails and arthropod grazers were not
prevented from entering the exclosures. Further details of this exclosure technique are reported in Cubit
(1975).
Algal abundance was measured as the percent coverage of each genus and was estimated by projecting
a stratified-random array of points onto color trans-
Ecology, Vol. 61, No. 3
parencies of the plots, a method similar to that of Connell(1970). In the cases where the filamentous Bangia
and Urospora grew so closely intermingled that they
could not be separated their coverage was measured
as a Bangia-Urospora mixture. The relative abundances of these algae are reported here only for the
first 6 mo following the establishment of each study
plot. In the longer term the succession of barnacles,
perennial algae, and other organisms altered the substrate and other growing conditions within the exclosures so that for the purposes of this paper they were
no longer comparable to the controls.
At all times of year, including summer, there was
an immediate increase in algal cover following the exclusion of limpets. Urospora and Bangia were generally the first macroalgae to appear in the exclosures,
often in mixed stands, and were followed by Porphyra
and the isomorphic green alga Ulva. The percent coverage data for the exclosures and controls are summarized by month for the 2.5-yr period in Table 1. The
number of plots in which each alga was present is also
given as a measure of the extent to which the alga
occurred over the study areas. In summer the algal
covers within the exclosures were much greater than
those in the controls for the same months and were
comparable to the natural algal blooms of the winter
months.
From March through October Bangia, Urospora,
and Porphyra formed higher percent covers and occurred in more plots of the exclosures than in the controls. With the possible exception of Porphyra, these
genera were continually present throughout the year
in the exclosures as compared to being ephemerally
present in the controls. September was the only month
in which no Porphyra was recorded in an exclosure.
The probable explanation for this is that a total of only
six exclosures was censused in this month, and that
these six exclosures were probably too new for Porphyra to have established. Three other, older exclosures not censused in September, but censused shortly
before and after (28, 29 August 1972 and 5 October
1972), contained Porphyra on both dates, suggesting
that this alga was present in September as well.
The months of lowest abundance of algae in the controls were April and October. In April none of the
upright morphs was found in the 13 controls censused,
while Bangia and Urospora were found in 12 and 11
of the 13 exclosures, forming up to 26 and 23% covers,
respectively, with both averaging 3% overall in pure
stands. In mixed stands, Bangia and Urospora ranged
up to 51% cover with an average over all the exclosures of 15% cover. Porphyra was more rare, but occurred in five of the 14 plots. Its percent cover averaged over all exclosure plots was 2% and up to 1%
in individual plots.
In October Urospora was the only alga of this group
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
N
Bangia
Urospora B-U mix
Controls
Porphyra
Total N
Bangia
Urospora
B- U
mix
Porphyra
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,
Urospora and Bangia were abundant in mixed stands,
occurring together in 12 of the 21 exclosures, averaging 25% cover overall and ranging up to 97% cover
in individual exclosures.
Porphyra was also present in the exclosures in October: it was present in six of the 21 exclosures, averaging 2% cover overall, and ranging up to 25% cover.
The extent and species composition of the algal cov-
684
JANE LUBCHENCO AND JOHN CUBIT
ers varied considerably among the exclosures; observations of colonization patterns within the exclosures
suggested that this variation resulted from competition
among the algal species (as in the New England studies) as well as from grazing by littorinid snails and
other small herbivores which were not excluded in
these experiments. For instance, those exclosures
with a higher degree of structural complexity (crevices, holes, barnacles, etc.) harbored higher densities
of nonlimpet grazers and developed lower percent
covers of algae. This effect varied from plot to plot
according to the amount of shelter there. Observations
that Porphyra was more common in those portions of
the exclosures where light grazing by littorinid snails
and other herbivores had reduced the densities of filamentous species of algae suggested that the abundance of Porphyra was negatively affected by competition, but favored by some grazing.
The results of the experiments presented here indicate that herbivory plays a substantial role in controlling the seasonal abundance of the upright thalli of
certain common annual and ephemeral algae of the
intertidal coasts of New England and Oregon. At the
high algal densities that occurred within the herbivore
exclosures, competition apparently also affected the
abundances of some species.
In New England, the upright thalli of Petalonia,
Scytosiphon, Ulothrix, Bangia, and Porphyra are normally winter annuals, but in the experiments where
they were protected both from herbivores and competitors, they were present in other seasons of the
year. In the field experiments protecting them only
from herbivores, these algae still occurred out of season, but to a lesser extent than when competitors were
also removed. In the laboratory experiments, the upright thalli of these algae are all highly preferred food
of the common grazers (Lubchenco 1978). Thus grazing is probably important in ultimately determining the
seasonal abundance of the upright morphs.
On the high intertidal rocks in Oregon, the upright
morphs of Bangia, Porphyra, and Urospora are also
primarily winter annuals. Although individuals of
these species may be found at other times of year at
lower intertidal levels (and occasionally at higher
levels) the bulk of the populations in the high intertidal
zone occur during the winter (Table 1 "controls"). In
the protection of the limpet exclosures these algae
were present and common throughout the year. Densities of possibly competing species were not experimentally manipulated in the Oregon studies. However,
observations of successional sequences and other
growth patterns within the limpet exclosures suggest
that interspecific competition also may have affected
the relative abundances of these algae.
Areas yet to be investigated are the demography
and other aspects of the ecology of the naturally oc-
Ecology, Vol. 61, No. 3
curring crustose and boring "Ralfsia," "Conchocelis," and "Codiolum" stages such as the study by
Paine et al. (1979) for the crustose red alga Petrocelis
middendorfJi. The crustose "Ralfsia" morphs in New
England are known to be more grazer resistant than
are the upright morphs (Lubchenco 1978). From our
field observations we infer that the Oregon crustose
morphs and all of the boring morphs are also less
vulnerable to being removed by herbivores. In the
course of our studies we have observed that the crustose algae in general are more abundant in, if not entirely restricted to, areas where herbivores are common and active. There is indication from other studies
that the establishment of at least some species of crustose algae may require the removal of their upright
competitors by herbivores (Vine 1974, Adey and Vassar 1975, Wanders 1977).
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 substrata the boring morphs are sufficiently protected
from herbivores that their survival exceeds that of the
upright morphs through seasons of, and in habitats of,
greater exposure to herbivory (Mumford 1973). (Some
of these boring morphs may live within the shells of
the grazers themselves.) As with the crustose forms,
herbivory may also be necessary to maintain the boring morphs. If the exteriors of the substrata occupied
by these algae were to become covered with other
algae, the algae below the substrate could be smothered or shaded out.
The preceding experiments and observations indicate that increases of grazing intensity in summer can
prevent the year-round survival of the upright stages
of the algae we studied. Thus we suggest that a primary adaptive value of the nonupright crustose and
boring stages of these species is both in their ability
to persist through times when the uprights are removed by grazers and to exist in areas of persistently
heavy grazing where the upright stages themselves
cannot survive. We suggest, however, that under conditions of light grazing the upright stages are competitively superior and have the additional selective advantages of rapid establishment, fast growth to reproductive
maturity, and subsequent production of large numbers
of propagules. We suggest that for plants such as these
in mid to high intertidal habitats, a single type of plant
cannot serve both functions well, because the adaptations which confer protection from herbivores are
mutually exclusive with those required for competitive
superiority, rapid colonization, and high rates of reproduction as discussed below. If this is correct, in
habitats of spatially and temporarily heterogeneous
patterns of grazing, a heteromorphic alga will be more
successful than one which is isomorphic.
Among the adaptations of the nonupright stages
which may provide protection from herbivores are the
following: (1) In the crustose forms muth of the thallus
June 1980
HERBIVORY AND ALGAL LIFE HISTORIES
685
TABLE
2. 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:
a. Light
1. Constant and
b. Heavy
a . Predictable$
2. Variable? and
b. Unpredictable
Then we predict:
Isomorphology: competitively superior morphs
(uprights) predominate
Isomorphology: grazer-resistant morphs (e.g.
crusts and borers) predominate
Heteromorphology: alternation of production and
predominance of morphs (e.g. seasonally)
Heteromorphology: continuous production, but
not survival, of both morphs
* T h e probability that a
given individual alga will b e removed b y herbivory In a given period of time. 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 b e forecast (e g., by correlat~onswith time or other cues from the environment). 7
adheres tightly to the substratum; thus the whole thallus is not lost if an herbivore removes a small portion
at the base. (2) The thallus is tough, formed of many
layers of cells compacted together, and thus may be
more difficult to graze. (3) Some Ralfsia are reported
to contain tannins (Conover and Sieburth 1966) which
may be herbivore deterrents. (4) The burrowing forms
are presumably protected from herbivores by being
within other crustose algae or hard substrata such as
shells and wood.
Among the adaptations of the uprights that might
contribute to higher growth rates at the expense of
resistance to herbivory are the following: (1) Since
most of the surface of an upright thallus neither adheres to the substratum nor is buried in it, and the
thallus is either filamentous or only a few cells thick,
the ratio of exposed surface to internal volume of the
plant is greater than in the nonupright forms. This allows potentially higher growth rates through more rapid assimilation of nutrients (Odum et al. 1958, Fogg
1965) and a higher ratio of photosynthetic area per unit
biomass. (2) Upright forms presumably allocate less
energy and material for attaching themselves to the
substratum or burrowing through it. (3) With small
points of attachment, the uprights require less space
per unit biomass than the crustose forms, an adaptation that is important in space-limited habitats of the
intertidal zone. (4) The uprights are probably not as
restricted in substrate requirements as are the burrowing forms.
As noted earlier it has been suggested that the crustose and boring stages of heteromorphic algae serve
as perennating phases through the seasons when the
upright stages are unable to tolerate the physical
stresses of the habitat (Wynne 1969, Conway et al.
1976). Low surface-to-volume ratios and living within
perforations of the substrate probably do render these
nonupright forms more resistant to desiccation and the
damaging effects of insolation and high temperatures.
We agree that the nonupright stages serve as perennating phases, but suggest that grazing and perhaps
competition should be considered as important factors
preventing the upright stages of these algae from being
perennial.
Vadas (1979) has suggested that heteromorphic al-
gae may be under bimodal seiection pressures, simultaneously evolving toward opposing ends of the r and
K continuum of selection. However, if our arguments
above are correct, the upright stages exhibit both r
and K characteristics: rapid growth, early maturity,
and high reproductive output (r) as well as competitive
superiority (K), and the bimodality of selection exists
between this combination and the ability to withstand
grazing.
In the following discussion we define the term grazing pressure as the probability with which a given individual alga will be removed by herbivory in a given
period of time. If the preceding explanations are correct we would predict that the relative proportions of
heteromorphic and isomorphic algae should vary from
habitat to habitat according to the seasonal fluctuations of grazing in those places. In areas where grazing
pressure does not fluctuate, we would expect isomorphic algae (either upright or nonupright) to predominate, the type of morph being determined by
grazing intensity (Table 2). If grazing pressure were
constantly low, the upright morphs should outcompete
the nonupright morphs (Table 2, la). If grazing pressure were constantly high, the uprights should be removed and the nonuprights survive in their place (Table 2, lb). Under such conditions, algae with obligate
alternations of heteromorphic generations should
eventually disappear as one morph or the other is eliminated by competition or grazing. Those algae with
alternations of heteromorphic generations that are not
obligate may have one morph survive, but it should be
at a lower relative fitness than similar, but isomorphic,
species in which no reproductive efforts are wasted on
producing the morphs which do poorly in these conditions.
In contrast, where grazing pressure does fluctuate
from season to season, conditions should alternately
favor upright, then nonupright morphs, resulting in
selection for seasonal alternation of these morphs
(Table 2, 2a). Greater fitness should accrue to those
heteromorphic algae which allocate their resources
into the production of nonuprights and uprights in synchrony with the grazing changes. Just prior to the onset of the seasons of increased grazing it should be to
the advantage of an upright alga to convert its re-
686
JANE LUBCHENCO AND JOHN CUBIT
sources to the grazer-resistant morph rather than have
these resources consumed by herbivores. Similarly,
selection should favor those algae concentrating their
production of uprights in the seasons of reduced herbivory (Table 2, 2a).
Finally, if grazing pressure fluctuates in an unpredictable manner, both morphs should be present continually (Table 2, 2b). Each morph will be favored at
some time, but prediction of precisely when is not
possible. Thus each plant should be most fit by producing offspring of both morphs.
According to this scheme, the New England and
Oregon studies reported above are examples of Table
2, 2a in which uprights are favored during the winter
months and nonuprights during summer months. In
our field studies, decreases in grazing pressure occur
in winter and increases occur in summer. Numerous
factors in the physical environment are correlated with
the grazing changes and could be used by an alga as
cues to change from one morph to another. These factors include temperature, insolation, photoperiod,
desiccation, wave force, and salinity. Laboratory culturing experiments have demonstrated that the switch
from upright to nonupright morphs or vice versa is
under photoperiodic or temperature control or both
for Petalonia, Scytosiphon, Bangia, and Porphyra
(Dring 1967, Wynne 1969, Bixon and Richardson 1970,
Sommerfeld and Nichols 1973, Roeleveld et al. 1974).
In the Oregon study areas species of Porphyra were
observed to liberate spores during the first series of
daytime low tides and warm weather in the spring.
For the algae discussed here, it makes little difference which cues are used for timing, providing the
cues are closely correlated with the seasonal increases
and decreases in the probabilities of being consumed
by herbivores. The strength of selective pressure to
respond to these cues should depend on the closeness
of the correlation. Conceivably there are environments in which the seasonal variations in grazing pressure are the reverse of those in our study areas; in
such areas we would expect opposite responses to the
same cues, all other factors being equal. The mechanisms which we suspect cause the variations of grazing
pressure in New England and Oregon might follow
other seasonal patterns on other coasts. In New England the winter reduction in grazing is apparently the
result of wave action causing littorinids to decrease
their grazing activities during the winter months (J.
Lubchenco Menge 1975). Evidently this same phenomenon also occurs on parts of the Oregon coast
where storm-generated waves decrease the densities
andlor activities of littorinids (Castenholz 1961, Behrens 1974, Cubit 1975). In the particular Oregon study
areas described in this paper the winter decrease in
grazing pressure apparently results from a swamping
of the grazing capacities of the limpet populations by
increased algal productivity rather than a reduction of
the grazing activities of the limpets (Cubit 1975). In
other habitats factors such as seasonal removal of her-
Ecology, Vol. 61, No. 3
bivores by predators, or seasonal influx of algal drift
may also operate to reduce grazing at other times of
year and change the selective regime for the timing of
production of the various morphs of the heteromorphic algae. In other words, rather than the seasonal
abundance of these different morphs being dependent
on the timing responses of the plants, the timing responses are probably dependent on the seasonal survival of these morphs.
Our experiments do not address factors involved in
the origin of heteromorphology; they demonstrate
only that variation in the grazing regime may maintain
this adaptation in the species investigated.
The hypotheses and predictions put forth in this paper are not intended to explain the occurrence of heteromorphology in all algae. Rather, we have focused
on one of the mechanisms that may be involved in
selection for heteromorphology of common species
that have annual or ephemeral upright thalli in the mid
and higher littoral zones. Since the morphologies of
stages and the patterns of life cycles in other heteromorphic algae differ from those we have studied, the
selective mechanisms probably also differ. Moreover,
the hypotheses presented in this paper are subject to
further testing, particularly regarding the ecology of
the nonupright stages. For example, more information
is needed on (1) the demography and phenology of the
crustose and boring stages, (2) the relative competitive
abilities of uprights vs. nonuprights, and (3) effects of
other factors, e.g., seasonal burial and scour by sand
which might act similarly or in addition to grazing in
selecting for heteromorphology.
We thank the following people for field assistance or comments on versions of this manuscript: L. Ashkenas, R. W.
Day, P. K. Dayton, S. D. Gaines, M. E. Hay, J. A. Kilar,
E. G. Leigh, B. A. Menge, T. F. Mumford, Jr., J. N. Norris,
R. T. Paine, W. P. Sousa, J. A. West, S. D. Williams, and
two anonymous reviewers. J. Lubchenco is grateful to N . W.
Riser for use of Northeastern University's Marine Science
Institute, Nahant, Massachusetts. This paper is contribution
51 from that laboratory. J. Lubchenco's research was supported by National Science Foundation Grants GA-40003 to J.
Lubchenco and GA-35617 and DES72-01578-A01 to B. Menge.
J. Cubit thanks P. Frank and S. Cook for helpful discussion,
T. F. Mumford, Jr. for identifying specimens of Porplzyra,
and Sigma Xi for a grant-in-aid of research.
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Heteromorphic Life Histories of Certain Marine Algae as Adaptations to Variations in
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Jane Lubchenco; John Cubit
Ecology, Vol. 61, No. 3. (Jun., 1980), pp. 676-687.
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