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Reproductive ecology of four subtidal red algae
119
J. up. mtrr. Biol. Ecol., 1981, Vol. 54, pp. 119-136 ElsevieriNorth-Holland Biomedical Press
REPRODUCTIVE ECOLOGY OF FOUR SUBTIDAL RED ALGAE’
T. L. NORALL, A. C. MATHIESON and J. A. KILAR Deprrrtmentof Botany and Plant Pathology and the Jackson Estuarinc, Laboratory qf the Uniwrsit~, of NewHampshire, Durham. NH 03824, U.S.A. Abstract: The reproduction and stature of the red algae CaNophyl/is cristata (C. Ag.) Kuetz.. Memhranoptrra alata (Huds.) Stackh., Phycodrys r&ens (Huds.) Batt.. and Ptilota serrata Kuetz. were recorded from subtidal populations at Appledore Island, Maine. U.S.A., with respect to time and depth. Only Memhranoptera ahta exhibited a conspicuous seasonal fluctuation of reproduction. A vertical gradient of reproduction was evident, with reduced levels of reproduction in shallow populations of Phycodrys rubens and Ptilota .xrrata, as well as deep populations of Phycodrys rubens, Memhrunopteru alara and Callophyllis c’ristata. Differential stratification of the reproductive phases of Ptilota .serra(a occurred with higher frequencies of tetrasporic plants in deep populations and of cystocarpic plants in shallow populations. In contrast, the haploid and diploid plants of the other three species showed similar distributional patterns. Membranoptera akata, Phycodrys rubens, and Callophyllis cristatu showed a conspicuous decrease in stature during maximum reproduction.
The typical
life history
of the higher
red algae (Florideophycideae)
is triphasic,
with a free-living tetrasporophyte and gametophyte and a “parasitic” carposporophyte. The life history and relative abundance of the phases may, however, vary under different environmental conditions and geographical locations (Dixon, 1965; Fritsch, 1945; Levring, 1947; Mathieson & Burns, considered to be the primary factor determining distribution
of marine
plants
(Hutchins,
1975). Temperature is usually the horizontal (geographical)
1947; Hedgpeth,
1957), while light varia-
tions are usually designated as the paramount factor determining their vertical distribution (Hellebust, 1970). As temperature and light change with depth and season, it was hypothesized that subtidal red algae would exhibit a change in reproduction with depth and time. Accordingly, the present study was initiated in order to examine the reproduction and size (stature) of four subtidal red algae, Membranoptera aluta (Huds.) Stackh., Callophyllis cristata* (C. Ag.) Kuetz., Ptilota serrata Kuetz., and Phycodrys rubens (Huds.) Batt., with respect to time and depth.
’ Published with the approval of the Director of the New Hampshire Agriculture Experiment Station as Scientific Contribution No. 818; also issued as Contribution No. 52 from the Jackson Estudrine Laboratory. * The name Calloph~~llisrristata is employed for the taxon Euthortr c,ris/ata (L.) J. Agardh. according to the interpretation of Hooper & South (1974). 0011-098
I ~81/0000-OOOO~S 02.50 0 Elsevier:North-Holland
Biomedical
Press
120
T.L.NORALLETAL.
Each of the plants
is a boreal
cold-temperate
a broad
distribution,
extending
subtidal
mean low water (Mathieson,
species (Taylor, from
1957) which exhibits
- 1.0 to at least
-24.0
m below
1979).
MATERIALSAND
METHODS
Seasonal collections of Membranoptera alata, Callophyllis cristata, Ptilota serrata, and Phycodrys rubens were made at 6, 12, 18, and 24 m below mean low water (M.L.W.) from the east side of Appledore Island, ME (42”59’20”N :70”36’5O”W). The collections were made at intervals of z 6 wk between July 1974 and June 197.5. Approximately 50 plants of each species were collected at each depth by SCUBA diving. The plants were frozen until later microscopic determinations of reproductive phases and measurements of maximum plant length. Voucher specimens from each depth and each reproductive phase are deposited in the Albion R. Hodgdon Herbarium (NHA) of the University of New Hampshire. Quadrats were not taken because of decompression problems. Thus, neither the abundance of plants per unit area nor growth measurements can be implied from this study. The water temperatures at the site studied were recorded at the surface and at each collecting depth using an armored laboratory grade thermometer. Water samples were taken at the surface and each depth, using a Van Dorn water sampler that was hand-held and triggered by a diver and salinity determinations were made with an American Optical Refractometer (Model 10423). Visual observations of sea conditions (swell heights) were obtained from the nearby Coast Guard Station at White Island (R. Long, pers. comm.), where records of sea state are recorded every 3 h. Numerical values were assigned to the highest daily sea state as follows: ~0.9 m = 0 points, 0.9 to 1.5 m = 1 point, 1.5 to 2.1 m = 3 points, and ~2.1 m = 5 points. Seasonal solar irradiance data were obtained from the U.S. Weather Bureau from values recorded in Portland, ME (B. Fleury, pers. comm.). These values were recorded with a pyranometer, an instrument uniformly sensitive to radiant energy, regardless of the wavelength (Anonymous, 1969). Light attenuation data were obtained with an Inter Ocean Marine Illuminance Meter (Model 510), employing a variety of filters (red, green, blue, and neutral density). The light records were then compared and equated to Type 3 Coastal Water (Jerlov, 1970) and the percentage transmission of different wavelengths was calculated at the four collection depths. A rough model of light quality at each depth was obtained with a combination of percentage transmission (Jerlov, 1970) and spectral composition of sunlight (Moon, 1940; Holmes, 1964). In the calculations, reflection at the sea surface was ignored. Two- and three-way analysis of variance without replication (Sokal & Rohlf, 1969) were run on the reproductive data, which were expressed as a percentage of
REPRODUCTIVE ECOLOGY each reproductive
type and
three-way
sex, period,
two-way
analysis, analysis,
as independent
the mean
were done by evaluating All of the percentages
length
and depth
sex was treated
variables.
OF SUBTIDAL
121
RED ALGAE
of each reproductive
were independent
as a dependent
Tests for significance
variable
of period
type.
variables, and period
and depth
effects at specific
the fit of the data to a second degree polynomial were transformed
by _Y= arc sin &,
as suggested
In the
while in the depths
regression. by Steel &
Torrie (1960). The temperature, salinity and nutrient data (Norall & Mathieson, 1976) were evaluated by linear regression analysis, after transformation by logarithmic function J’ = log,+ (Harvey, 1968, 1975). All of the statistical data were evaluated at the 0.05 level, following Bartlett’s test (Sokal & Rohlf, 1969) for homogeneity of variance.
RESULTS ENVIRONMENTAL DATA Temporal and vertical fluctuations of water temperature are presented in Fig. 1. The shallow depths were warmer in summer while the deeper depths were more uniform throughout the year. The maximum temperatures for the surface (18.2 “C), - 6 m (17.9 “C), and - 12 m (14.0 “C) were recorded in August compared with October at -18 m (10.5 “C) and October-November at -24 m (9.8 “C). The minimum temperature (3.8-4.0 “C) for all depths was in late March. Little variation of salinity was noted (31-33x,). The sea state was relatively calm from June through October (Fig. 1). Thereafter, turbulence increased through December, DEPTH(m) D .---. (j ,2
SEAoSIAy,
. .. . . . _.-._
;ACTOR
1=
1-15
3= 5=
15-21 r21 7 20
20r
0
J
S
0
N
D
J
F
M
A
M
J
1975
Fig.
1. Temporal and spatial variations of water temperature at Appledore Island, ME, and cumulative monthly sea state (0) (swell height) at White Island, NH, based upon the maximum daily values.
122
T. L. NORALL
2oc
ET AL.
d-
ii . : 1 d
100
J
A
Fig. 2. Seasonal
Fig. 3. Spectral
50
variations
N
D
J
197sFM
A
M
J
of total and PAR solar irradiance.
energy distribution (400-700 nm) at -6, - 12, - 18 and -24 m, using Jerlov’s and Moon’s (1940) transmittance and solar energy distribution data.
(1970)
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
123
RED ALGAE
followed by a decreasing sea state, except for April when there was a major storm. As suggested by Szeicz (1974) the photosynthetically active range (PAR) of the daily total radiation (i.e. both direct and diffuse) remains nearly constant at z 500,o. The lowest levels of solar energy and PAR were in December, while the maximum values were in August (Fig. 2). The percentage of PAR at a given depth was calculated for each 25 nm interval (Fig. 3), employing Moon’s (1940) and Holme’s (1964) calculations on solar energy distribution. The blue-green portion (500-550 nm) of the spectrum had the maximum penetration, and the ratio of blue-green/red light increased with depth. REPRODUCTION
Membranoptera alata showed a pronounced seasonal cycle (Table I), with minimum and maximum reproduction in October and December, respectively (Fig. 4). Overall, the plant’s reproduction (i.e. total or both tetrasporic and gemetophytic) was maximal at - 18 m (Fig. 5), primarily due to a high frequency
TABLE I A stattstical
summary
of the reproduction and significant Total reproduction
stature of Mrrnhrrmopr~~r at 0.05 level.
(three-way
Sex
(two-way
Tetrasporic Period Depth 2.65* 1.02
-6m -12m -18 m -24m
Period-total 2.43 8.27* 0.62 20.90*
of variance)
Cystocarpic 2.62 7.04* 7.22* 4.50 (three-way
Sex 1.76
-6m -12m -1X m -24m
analysis
analysis
Spermatangial 2.23 X.23* 16.70* 3.26
of variance)
Depth 2.45 stature
Spermatangial Period Depth 1.10 0.82
(regression-quadratic)
Tetrdsporic 5.X9* 9.82* 4.84 1.99 Total stature
Period x.34*
Cystocarpic Period Depth 1.84 0.59
Period-reproduction
(i.e. F values):
of variance)
Depth 1.88
5.64* % reproduction
analysis
a/r/a
(regression-quadratic)
Period 0.76
*?
T. L. NORALL
124
of tetrasporic
plants (Fig. 6). The reproductive
the same at all four depths being present
ET AL
from November
(Fig.
phenology
of M. data was essentially
7A), with gametophytic
and tetrasporic
plants
to June.
I ..-_.._____./ JAsONDJFMAMJ 1975
Fig. 4. Monthly
A three-way
averages from four depths of the percentage reproduction of Memhrttnoptrrcr Cdophyllis cristata, Ptilotu serruta, and Phycodrys rubens.
analysis
of variance
for total
reproduction
in M. alum
olrrtn,
showed
significant (P 20.05) differences in reproductive types and period but not with depth (Table I). A further two-way analysis of variance of reproduction compared with depth and period only showed a significant tetrasporic-period interaction (Table I). The following period-reproduction interactions (regression quadratic) were also significant: tetrasporic plants at -6 and - 12 m and cystocarpic and spermatangial plants at - 12 and - 18 m. The reproduction of Callophyllis cristata was maximal in August and minimal in November (Fig. 4). Overall, the highest reproduction was at -6 and - 12 m (Fig. 5). The gametophytic and tetrasporophytic generations showed the same distributional pattern (Fig. 6). Shallow-water plants ( -6 m) exhibited a pronounced summer maximum and a winter minimum (Fig. 7B). Cystocarpic plants at - 12 m basically had the same pattern as at -6 m, while tetrasporic plants at - 12 m had a more irregular pattern. Only 19 plants were collected at - 18 m from August through December; at - 24 m no plants were found during July and only 22 plants were collected from January through April. The inadequate sample size may be responsible for the low frequencies of reproductive plants during these periods. A three-way analysis of variance for total reproduction in C. cristata showed no significant differences with sex, depth or period (Table II). A two-way analysis of variance of reproduction compared with depth or period similarly showed no significant differences for any reproductive types, even though significant period effects (regression quadratic) were observed for tetrasporic plants at - 6 and - 24 m,
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
% REPRODUCTION 10 I 6
30 I
1
\
18
-
24
-
-
E
.
12
-
I .
18
-
-
18
-
24
-
-
12
-
18
-
24
-./ yearly
I
100 I
PTILOTA
. \
. \ . ./
10 I 6
100 I
CALLOPHYLLIS
60 I
I
12 -
Fig. 5. Average
./ I
I
30 I
.
.I
/ 20 I
6
\
./
l
E w cl
60 I
1
-
-
.
.
./
6
24
+-----=
\ .
20 I
km)
50 1
,
12
-
STATURE
MEMBRANOPTERA .
-
125
RED ALGAE
I
50 T
PHYCODRYS
./ t
./
reproduction (:‘/,) and stature for Membrwwpte~o LI/UIO, Ptiloto srrrcrta and PhJwdr.vs rubens at four depths.
126
T. L. NORALL
ETAL.
and for cystocarpic plants between - 6 to - 18 m (Table II). Difficulties in sampling design, as noted earlier, prevent any further explanation, other than that the maximum period of female plants was between May and July and for tetrasporic plants between June and August. The reproductive frequency of Ptifota serrata (Fig. 4) varied from 82% (late April) to 637/, (June). Overall, the plant’s reproduction (i.e. total) was maximal at - 18 m
-I
4o_
Callophyllis
MeMbranoptera
40-
1 3020IO-
5 & tY
6 12 18 24
6 12 18 24 30
too-
. Phycodrys
Pti Jota
80604020-
.-•
1 I
I
1
I
l .
6 12 18 24 DEPTH (M) BELOW
M. L.W
Fig. 6. The average yearly reproduction of gametophytic and sporophytic plants of Cullophyllis cristata, Memhranoptera alata, Phycodrys r&ens and Ptiloia serrata at four depths.
REPRODUCTIVE
ECOLOGY
OF SUBTIDAl..
RED ALGAE
127
(Fig. 5), with the tetrasporophytic generation being the primary contributor to this pattern (compare Figs. 5 and 6). Tetrasporic plants had their highest reproductive frequencies at - 12 to -24 m (Fig. 7C), while the greatest frequencies of cystocarpic plants were at -6 and - 12 m. Cystocarpic plants showed an irregular seasonal pattern at each depth.
A
statistical
summary
of the reproduction
and stature of Cu~~~i~h~,~lj.~ cri.rtora (i.e. Fvalues): at 0.05 level.
Total reproduction
(three-way
Sex
analysis
Period 1.87
1.51
O,. reproduction
(two-way
analysis
Tetrasporic Period Depth 0.72 I .06 Period-reproduction
-6m -12m -18m -24m
of variance)
Depth
1.26
* significant
of variance) Cystocarpic Period Depth 2.46 2.70
(regression-quadratic)
Tetrasporic 6.53* 0.39 0.66 9.33*
Cystocarpic 25.40* X%30* 11.60* 0.22 ___
Total stature
(three-way
Sex 6.47 Period-total -6m -I?m -18 m -24m
analysis
of variance)
Depth 10.60* stature
Period 6.87*
(regression-quadratic)
6.8?* 2.62 2.08 3.26
A three-way analysis of variance showed that Ptilota’s reproduction (i.e. total) was signi~cantly different with depth and sex, but not period (Table III}. A two-way analysis of variance showed no significant reproductive differences in period or sex ((i.e. individual generations), nor in period-reproduction with a regression quadratic analysis (Table III). The reproduction of P~JXO&JG rubem was maximal in December and minimal in October (Figs. 4 and 7D). Overall, the plant’s reproduction was maximal at - 12 m (Fig. 5) with the gametophytic and tetrasporophytic generations showing the same distributional pattern (Fig. 6). Tetrasporic plants exhibited their seasonal maxima
T. L. NORALL
128
ET AL.
in January and June at - 6 m, July and November at - 12 m, and July and January at - 18 m (Fig. 7D). Cystocarpic plants showed a seasonal shift in their reproductive phenology with increasing depth (Fig. 7D). The maximum number of cystocarpic plants was in July at - 6 m, and in December at - 12 to - 24 m. The low frequency of male plants masked any pattern, except for the bimodal maxima in late November and June at - 12 m. TAMLE III A statistical
summary
and stature of Pfihfci .SP~~YII~~ (i.e. F values): at 0.05 level.
of the reproduction
Total reproduction
(three-way
analysis
‘!, reproduction
(two-way
analysis
Tetrasporic Period Depth 0.44 2.45 Period-reproduction
-6 -12 -18 -24
m m m m
Period I.85 of variance) Cystocarpic Period Depth 2.92 0.95
(repression-q~ddratic)
Tetrasporic 1.95 2.94
Cystocarpic 1.58 1.63 1.73 0.63
1.07 3.45 Total stature
(three-way
Period-total 3.11 0.79 0.30 1.01
analysis
of variance)
Depth 47.58*
sex 5.83
-6m -12m -18m -24m
of variance)
Depth 7.51*
Sex 53.09*
* significant
___ stature
.-.-.. _.._
Period 3.55*
(regression-quadratic)
The reproductive phenology (i.e. total) of P~?~co~r~~~rupees was signi~cantly different with sex, but not with period or depth (Table IV). Mate plants showed a significant change in reproduction with depth, the maximum and minimum percentage of males was at - 12 and -24 m, respectively (Fig. 7D). No significant period-reproductive differences were detected by a two-way analysis of variance; however, a significant period effect was detected with cystocarpic plants at - 12 m (Table IV).
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
RED ALGAE
129
130
T. L. NORALL
ET AL.
STATURE
The largest plants of Membranoptera alata were found during June to December and the smallest ones between late winter to spring (Fig. 8). Overall, the largest plants were found at - 12 m (Fig. 5), with both the gametophytic and sporophytic generations showing a similar pattern (Fig. 9). No significant differences in stature were found with depth, period or sex (Table I). In contrast, the plant’s stature showed a significant period effect at - 12 and -24 m (Table I).
,,,‘______ / f
... . .I””
3-
z Q
\....
‘i! 1 1
Pycodryr
,A”
.~___.__........................ C&,,&,,ir
_... .“““‘-.......__.._.__.__, ,,....” _/ .‘.‘.‘-..,. ..............._.._.. _,,_,,,_,___ ...’./’ ._---as----.___-_.---- -9, ‘\ ..---____.__
__-. -_-
_C.Membrono~tera
1 JASONDJFMAMJ
Fig. 8. Monthly
averages
1975
from four depths of the mean length (cm) of Membranoptera alatrr, Callophyllis cristata, Ptilota serrata, and Phycodrys rubens.
The stature of Callophyllis cristata was maximal between March and June and minimal in late January (Fig. 8). The largest plants were recorded at - 6 and - 12 m (Fig. 5), with both generations basically showing the same pattern (Fig. 9). The stature of Callophyllis was statistically different with depth and period, but not sex (Table II). The mean size of the fronds also showed a significant period effect at -6m. Ptilota serrata showed its maximum and minimum stature in August and November, respectively (Fig. 8). Overall, the plants increased in size from -6 to -24 m (Fig. 5), with both generations showing an identical pattern, except for the gametophytic plants at -24 m (compare Figs. 5 and 9). The plant’s stature (i.e. total) was significantly different with time (period) and depth but not sex (Table III). In contrast, the mean frond size showed no significant period effects at the four depths when analyzed with a regression quadratic evaluation. The stature of Phycodrys rubens was maximal in August and minimal in January (Fig. 8). The largest plants were recorded at - 12 m and the smallest at -24 m
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
5-
2.0-
4-
1.5-
RED ALGAE
131
-@ .. .... . .. .-,
& 98
3l.O20.5l-
.
MeMbranoptera
calloph,4is
EL-n-n-G 6 121824
I
1
1
I
6 12 18 24
I
z
z g7-
. ..-. .* P
7-
‘.
l.*’
5-
9-
5
f
l. 0.. f
.*
5-
\
3-
3Phycodrys
l-
Pti iota l-
I
I
1
6 121824
I
I
I
I
1
6 12 18 24 DEPTH (M ) BELOW M. L.W.
Fig. 9. The average yearly length of gametophytic and sporophytic plants of Cu//ophylfis crktara, Membranoptera alata, Phycodrys rubens, and Ptilota serrata at four depths.
132
T. L. NORALL
ET AL.
(Fig. 5); both generations showed a similar pattern, except for the gametophytic plants at -24 m (compare Figs. 5 and 9). The stature of Phycodrys was statistically TAHLE IV
A statistical
summary
of the reproduction
Total reproduction
and stature of Plr~c~dr~s at 0.05 level. (three-way
(two-way
Period-reproduction
-6m -12 m -1Sm -24m _____-.I..
1.86 i .69 .._________
-6m -12m -18m -24m
of variance) Spermatangial Period Depth 7.43’ 1.73
(regression-quadratic)
(three-way
analysis
Spermatangial 0.31 0.04 0.19 0.35
of variance)
Depth 5.79*
Sex 3.37 ~___ Period-total
analysis
Cystocarpic 3.35 9.77* 0.48 1.15 _._______~_
Tetrasporic 1.21 2.08
Total stature
Period 0.93
Cystocarpic Period Depth 0.89 1.53
Tetrasporic Period Depth 1.36 0.60 ._~_..^_
* significant
of variance)
Depth 2.51
Sex 1.59* 7; reproduction
analysis
rubrns (i.e. F values):
Period 9.90* -.
stature
(regression-quadmti~}
9.90* 2.71 0.35 1.84
different with depth and period, but not sex (Table IV). The plant’s stature at - 6 m was significantly different over time. STATURE
AND
REPRODUCTION
Fig. 5 compares the average stature and reproduction (i.e. both tetrasporic and gametophytic plants) of all four species at different depths. Membranoptera had its maximum reproduction at - 18 m and its maximum length at - 12 and - 18 m. The depth of maximum reproduction and maximum length were approximately the same for ~a~~oph~Ili.~cristata, while they corresponded for Phycodrys rubens. The maximum reproduction of Pt~lota sermta was at - 18 m, as compared to - 24 m for its longest length. Fig. 10 summarizes the average monthly length and reproduction for the four
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
RED ALGAE
133
species, based upon the depths of maximum stature for each species (Fig. 5). Overall, the period of maximum stature seemed to be just prior to maximum reproduction, with P. set-rata showing the least pronounced pattern. ~e~~ra~upter~ alata and Phycodrys ruhens had a non-synchronous pattern of reproduction and growth, with maximum summer growth and fall-winter reproductive maxima. Callophyllis cristata showed a simultaneous decline in growth and reproduction during the summer and winter and a somewhat earlier growth than reproductive maxima. loo-
-20
Callophyllir Y
/
. .. ... .,,,,..,...I
Mambranoptero
1
IOJASONDJFMAMJ
v/-/T_______
J
ASONDI
FMAMI
1001 /
’ 60 t a & f
JASONDJ
FMAMJ
Fig. 10. Monthly averages of the reproduction (yg) and length (cm) of M~vnh~u-rmopte~ uiuru, Ccdloph~//i.c crkra!n, Ptilorrr srrmtri, and Phycadry.~ rubens, all at - 12 m except for P. scr-rata (at - 24 m).
As noted previously, the temperature (Fig. l), salinity and nutrient data (Norall & Mathieson, 1976) were evaluated simultaneously with the growth and stature data, employing a linear regression analysis built into the Harvey (1968, 1975) program. No significant correlations could be drawn between the hydrographic data and the mean size of a reproductive gene~tion or the percentage of a given reproductive generation. DISCUSSION Of the four red algae studied only ~~~~r~~o~te~u alata showed a significant (P >; 0.05) seasonal variation of reproduction, which was primarily associated with the tetrasporic generation (Table I). A similar regression analysis of the other
134
T. L. NORALL
ET AL
species showed that 5 of the 8 depth-sex combinations of Callophyllis cristata were sign&ant, while 1 of the 12 combinations for Phycodrys rubens, and none of the 8 depth-reproductive combinations for Ptilota se~rata were significant (Tables II-IV). The synchronized reproductive phenology of Mernbranoptera alata at different depths (Fig. 7A) suggests that it is primarily “triggered” by seasonal differences in day-length at each depth. The low levels of reproduction for Calloph~~flis cristata and Phycodrys rubens at - 24 m (Figs. 5,6,7B and D) may be attributable to reduced light intensities or a change in light quality (Fig. I), as temperature did not change significantly between - 18 and -24 m. P. rubens and Ptiiota serrata both had a “surface” inhibition of their reproduction, as low levels of reproduction occurred at -6 m (Figs. 5, 6, 7C and D). The latter phenomenon may have been due to saturating light intensities (see Mathieson & Norall, 1975a) or inhibiting light quality (Fig. 3) rather than temperature, as P~zycodr~.~rube~zs had its highest reproduction during the summer while Ptilota serrata had a constant level of reproduction at -6 m. Two basic patterns of vertical distribution of haploid and diploid generations were apparent (Figs. 6 and 7): (1) the coexistence of both reproductive phases at different depths, and (2) the dominance of diploid generations within the deep subtidal. P~zycod~ys rubens, ~e~b~anopte~a a~ata, and ~a~~ophy~l~scristata showed the first pattern. The reproductive phases of Prilora were differentially stratified, with a maximum frequency of cystocarpic plants at -6 and - 12 m and the highest frequency of tetrasporic plants at - 18 and - 24 m. Previous physiological studies (Mathieson & Norall, 1975a) have shown that both generations of Ptilota exhibit the same light optimum for net photosynthesis. Even so, the tetrasporic plants have a higher rate of net photosynthesis at a variety of light intensities than the cystocarpic plants. Thus, light intensity per se is not the direct cause of the differential occurrence of tetrasporic and cystocarpic plants. Rather, differential growth and viability could be associated with a variety of factors, including light intensity, light quality, temperature, and nutrients. It is of interest to note that Chondrus crispus exhibits the same stratification (Mathieson & Burns, 1975) and photosynthetic pattern (Mathieson & Norall, 1975b) of its reproductive generations as Ptifota. Other examples of differential proportions of tetrasporic and cystocarpic generations have been noted within the geographical distribution of several red algae (Fritsch, 1945; Levring, 1947; Dixon, 1965). In addition, Barilotti (1973) has described several examples of diploid dominance in the brown alga Zonariu,farlowii in “stressful” or marginal habitats. Callophyllis cristata, Phycodrys rubens, and Ptilota serrata showed significant vertical differences in stature (Table II-IV). Of the three species, Callophyllis showed a decrease from -6 to -24 m (Fig. 9), while Phycodrys showed its maximum stature at - 12 m. Ptilota showed a striking difference in stature, with the tetrasporic generation increasing in size from -6 to -24 m and the gametophytic plants similarly elongating from -6 to - 18 m. Edelstein et al. (1969) and Mathieson &
135
REPRODUCTlVEECOLOGYOFSUBTIDALREDALGAE
Burns
(1975) have recorded
similar
and Chondrus crispus, respectively
morphological-depth
~ i.e. deep-water
plants
patterns
with P. serrafa
are longer
and narrower
than shallow water specimens. The seasonal Ptilotu serruta appearance
variation of stature for PhJjcodrys rubens, Callophyllis (Figs. 8 and IO) can be attributed to two major
of juveniles
and the degeneration
of tissues
after
cristata and factors: the
sporulation.
Large
reproductive plants of each species were vulnerable to storm “pruning”, and they exhibited a decrease in stature during the fall period of maximum sea heights (compare Figs. 1, 8 and 10). A spatial relationship was apparent between stature and reproduction for Phycodrys rubens and Callophyllis cristata (Fig. 5). The mean reproduction and stature of Phycodrys were both maximal at - 12 m, while they were approximately the same ( -6 and - 12 m) for Callophyllis cristata. In contrast, Membranoptera alatu and Ptifota serrata had their highest levels of reproduction at - 18 m versus their longest plants at - 12 and -24 m, respectively. In contrast to the diploid dominance of tetrasporophytes of P. serrata within the deep subtidal (Fig. 6) no differential stature of the gametophytic and sporophytic plants (Table
was apparent III). Overall,
at the 0.05 level but they were different at the 0.10 level there was a trend of increasing stature of tetrasporic versus
gametophytic plants with increasing depth (Fig. 9). Such a trend was not apparent with Phycodrys rubens, Callophyllis cristata or Membranoptera alata (Fig. 9). The higher net photosynthesis of the tetrasporophytes of Ptilota serrata (Mathieson & Norall, 1975a), as well as the larger stature of the diploid plants may contribute to the overall diploid dominance of the tetrasporophytic plants. As noted earlier, however, a variety of interrelated factors, including differential viability of propagules may also be significant. Obviously more questions have been raised than answered regarding the cause and effect relationships of diploid dominance of P. serrata, and the contrasting patterns Callophyllis, and Membranoptera.
of growth
and reproduction
for Phq,codrJ,s,
ACKNOWLEDGEMENTS
We wish to thank several individuals at the University of New Hampshire for their assistance; Drs. A. Baker and R. Kinerson for their critical reading of the paper; Dr. W. Urban and Mr. 0. Durgin for their advice with statistical analyses; Dr. J. Murdoch for helpful comments regarding the irradiance studies; and Mr. Ned McIntosh for his assistance as Captain of the R. I/. Jere A. Chase.
136
T. L. NORALL
ET AL.
REFERENCES
ANONYMOUS, 1969. Recomme?~ded procedures &r measuring rhe produ~t~~~it~ ~~p~unkt~n standing stock und related oceanic properties. National Academy of Sciences, Washington, D.C., 59 pp. BARILOTTI, D. C., 1973. An ecological study of populations of a benthic alga: genetic differences that affect life history strategies in diverse habitats. Ph.D. thesis, University of California, Santa Barbara, 149 pp. DIXON, P. S., 1965. Perennation, vegetative propagation and algal life histories, with species reference to 4spcrmgopsis and other Rhodoph~lta. Bar. ~~it~l~~b~rg.Vol. 3, pp. 67 74. EDELSTEIN, T., J. S. CRAIGII-: & J. M~LACHLAN, 1969. Preliminary survey of the sublittoral Flora of Halifax County. J. Fish. Rex. Bd Gun., Vol. 26, pp. 2703-2713. FRITSCH, F. E., 1945. The structure and reproduction oy the ulgue. Vol. II. Forwrd, Phueoph~ceue, Rhoduphyeoe, M>w~ph~*crne. Cambridge University Press, London, 939 pp. HARVEY, W. R., 1968. Instructions for use of LSMLGP. Ohio State University, (a computer program available at Ohio State University, Columbus, Ohio). HARVEY, W. R., 1975. Least-squares analysis of data with unequal subclass numbers. ARS H-4 Data Systems Appli~tion Division, .~~iculturaI Research Service, U.S. Dept. A.&. (DSAD-ARS), Beltsville, MD. HFDGPETH, J. W., 1957. Marine biogeography. In, Treatise on marine ecology and paleoecalog~~, idol. 1. Ecology, edited by J. W. Hedgpeth, Geol. Sot. Am., Washington, D.C., Memoir 67, pp. 359-382. HELLEBUST, J. A., 1970. Light-plants. In, Murine eco/ogy, Vu/. I, edited by 0. Kinne, Wiley-Interscience, London, pp, 125-158. HOLMES, R. W., 1964. A contribution to the physical, chemical and biological oceanography of the northeast tropical Pacific, Atomic Energy Commission Progr. Rep., AEC-UCSD-34~99-4.358 pp. HOOPER, R. & G. R. SOUTFI, 1974. A taxonomic appraisal of Cullo~lr~~/is and Euthoru (Rhodophyta). Br. pl~_rrol. J., Vol. 9, pp. 4233428. HUTCHINS, L. W., 1947. The bases for temperature zonation in geographical distribution. Ecol. Monogr., Vol. 17, pp. 325-335. JIRLOV, N.G., 1970. Light-general introduction. In, Marine wo/oGpy, Vol. I, edited by 0. Kinne, Wiley-Interscience, London, pp. 95-102. LEVRINC;, T.. 1947. Submarine daylight and the photosynthesis of marine algae. GBt&. kl. t~‘etm.&.-o. VittenhSamh. Hundi., Ser. B, Vol. 5, pp. l-89. MATHIESON, A.C., 1979. Vertical distribution and longevity of subtidal seaweeds in northern New England, U.S.A. Bot. Mar., Vol. 30, pp. 511.-520. MATHIESON, A. C. & R. L. BURNS, 1975. Ecological studies of economic red algae. V. Growth and reproduction of natural and harvested populations of Chondrus crispus Stackhouse in New Hampshire. J. t”p. mar. Bioi. &??I., Vol. 17, pp. 137-156. MATWFSOK, A. C. & T. NOR.~LL, 1975a. Physiolo~icaI studies of subtidal red algae. J. c.rp. mar. Biol. Ecoi., Vol. 20, pp. 237-247. M~THIESON, A. C. & T. NORA~.L, 1975b. Photosynthetic studies of Chondrus crispus. Mar. Biol., Vol. 33, pp. 207.-213. MOON, P., 1940. Proposed standard solar-radiation curves for engineering use. J. Franklin Inst., Vol. 230, pp. 583618. NORALL, T. L. & A. C. MATHIESON, 1976. Nutrient and hydrodynamic data for the Great Bay Estuarine System and the adjacent open coast of New Hanlpshire, Jackson Estuarine Laboratory Publication, University of New Hampshire, Durham, N. H., 88 pp. (mimeograph). SOKAL. R. R. & F. J. ROHLF, 1969. Biometry, the principles andpractice yf’statistics in biological reseureh, W. H. Freeman and Company, San Francisco, 776 pp. STEEL, R. G. D. & J. H. TORRIE, 1960. Principles andprocedures in .rtatistics, McGraw-Hill, New York, 481 pp. SIEICZ, G., 1974. Solar radiation for plant growth. J. appl. EC&, Vol. 11.pp. 617-636. TI\YLOK, W. R., 1957. Murine argue of the n~rtheflstern coast o~~#rtl~ America, University of Michigan Press, Ann Arbor, Mich., 509 pp.
J. up. mtrr. Biol. Ecol., 1981, Vol. 54, pp. 119-136 ElsevieriNorth-Holland Biomedical Press
REPRODUCTIVE ECOLOGY OF FOUR SUBTIDAL RED ALGAE’
T. L. NORALL, A. C. MATHIESON and J. A. KILAR Deprrrtmentof Botany and Plant Pathology and the Jackson Estuarinc, Laboratory qf the Uniwrsit~, of NewHampshire, Durham. NH 03824, U.S.A. Abstract: The reproduction and stature of the red algae CaNophyl/is cristata (C. Ag.) Kuetz.. Memhranoptrra alata (Huds.) Stackh., Phycodrys r&ens (Huds.) Batt.. and Ptilota serrata Kuetz. were recorded from subtidal populations at Appledore Island, Maine. U.S.A., with respect to time and depth. Only Memhranoptera ahta exhibited a conspicuous seasonal fluctuation of reproduction. A vertical gradient of reproduction was evident, with reduced levels of reproduction in shallow populations of Phycodrys rubens and Ptilota .xrrata, as well as deep populations of Phycodrys rubens, Memhrunopteru alara and Callophyllis c’ristata. Differential stratification of the reproductive phases of Ptilota .serra(a occurred with higher frequencies of tetrasporic plants in deep populations and of cystocarpic plants in shallow populations. In contrast, the haploid and diploid plants of the other three species showed similar distributional patterns. Membranoptera akata, Phycodrys rubens, and Callophyllis cristatu showed a conspicuous decrease in stature during maximum reproduction.
The typical
life history
of the higher
red algae (Florideophycideae)
is triphasic,
with a free-living tetrasporophyte and gametophyte and a “parasitic” carposporophyte. The life history and relative abundance of the phases may, however, vary under different environmental conditions and geographical locations (Dixon, 1965; Fritsch, 1945; Levring, 1947; Mathieson & Burns, considered to be the primary factor determining distribution
of marine
plants
(Hutchins,
1975). Temperature is usually the horizontal (geographical)
1947; Hedgpeth,
1957), while light varia-
tions are usually designated as the paramount factor determining their vertical distribution (Hellebust, 1970). As temperature and light change with depth and season, it was hypothesized that subtidal red algae would exhibit a change in reproduction with depth and time. Accordingly, the present study was initiated in order to examine the reproduction and size (stature) of four subtidal red algae, Membranoptera aluta (Huds.) Stackh., Callophyllis cristata* (C. Ag.) Kuetz., Ptilota serrata Kuetz., and Phycodrys rubens (Huds.) Batt., with respect to time and depth.
’ Published with the approval of the Director of the New Hampshire Agriculture Experiment Station as Scientific Contribution No. 818; also issued as Contribution No. 52 from the Jackson Estudrine Laboratory. * The name Calloph~~llisrristata is employed for the taxon Euthortr c,ris/ata (L.) J. Agardh. according to the interpretation of Hooper & South (1974). 0011-098
I ~81/0000-OOOO~S 02.50 0 Elsevier:North-Holland
Biomedical
Press
120
T.L.NORALLETAL.
Each of the plants
is a boreal
cold-temperate
a broad
distribution,
extending
subtidal
mean low water (Mathieson,
species (Taylor, from
1957) which exhibits
- 1.0 to at least
-24.0
m below
1979).
MATERIALSAND
METHODS
Seasonal collections of Membranoptera alata, Callophyllis cristata, Ptilota serrata, and Phycodrys rubens were made at 6, 12, 18, and 24 m below mean low water (M.L.W.) from the east side of Appledore Island, ME (42”59’20”N :70”36’5O”W). The collections were made at intervals of z 6 wk between July 1974 and June 197.5. Approximately 50 plants of each species were collected at each depth by SCUBA diving. The plants were frozen until later microscopic determinations of reproductive phases and measurements of maximum plant length. Voucher specimens from each depth and each reproductive phase are deposited in the Albion R. Hodgdon Herbarium (NHA) of the University of New Hampshire. Quadrats were not taken because of decompression problems. Thus, neither the abundance of plants per unit area nor growth measurements can be implied from this study. The water temperatures at the site studied were recorded at the surface and at each collecting depth using an armored laboratory grade thermometer. Water samples were taken at the surface and each depth, using a Van Dorn water sampler that was hand-held and triggered by a diver and salinity determinations were made with an American Optical Refractometer (Model 10423). Visual observations of sea conditions (swell heights) were obtained from the nearby Coast Guard Station at White Island (R. Long, pers. comm.), where records of sea state are recorded every 3 h. Numerical values were assigned to the highest daily sea state as follows: ~0.9 m = 0 points, 0.9 to 1.5 m = 1 point, 1.5 to 2.1 m = 3 points, and ~2.1 m = 5 points. Seasonal solar irradiance data were obtained from the U.S. Weather Bureau from values recorded in Portland, ME (B. Fleury, pers. comm.). These values were recorded with a pyranometer, an instrument uniformly sensitive to radiant energy, regardless of the wavelength (Anonymous, 1969). Light attenuation data were obtained with an Inter Ocean Marine Illuminance Meter (Model 510), employing a variety of filters (red, green, blue, and neutral density). The light records were then compared and equated to Type 3 Coastal Water (Jerlov, 1970) and the percentage transmission of different wavelengths was calculated at the four collection depths. A rough model of light quality at each depth was obtained with a combination of percentage transmission (Jerlov, 1970) and spectral composition of sunlight (Moon, 1940; Holmes, 1964). In the calculations, reflection at the sea surface was ignored. Two- and three-way analysis of variance without replication (Sokal & Rohlf, 1969) were run on the reproductive data, which were expressed as a percentage of
REPRODUCTIVE ECOLOGY each reproductive
type and
three-way
sex, period,
two-way
analysis, analysis,
as independent
the mean
were done by evaluating All of the percentages
length
and depth
sex was treated
variables.
OF SUBTIDAL
121
RED ALGAE
of each reproductive
were independent
as a dependent
Tests for significance
variable
of period
type.
variables, and period
and depth
effects at specific
the fit of the data to a second degree polynomial were transformed
by _Y= arc sin &,
as suggested
In the
while in the depths
regression. by Steel &
Torrie (1960). The temperature, salinity and nutrient data (Norall & Mathieson, 1976) were evaluated by linear regression analysis, after transformation by logarithmic function J’ = log,+ (Harvey, 1968, 1975). All of the statistical data were evaluated at the 0.05 level, following Bartlett’s test (Sokal & Rohlf, 1969) for homogeneity of variance.
RESULTS ENVIRONMENTAL DATA Temporal and vertical fluctuations of water temperature are presented in Fig. 1. The shallow depths were warmer in summer while the deeper depths were more uniform throughout the year. The maximum temperatures for the surface (18.2 “C), - 6 m (17.9 “C), and - 12 m (14.0 “C) were recorded in August compared with October at -18 m (10.5 “C) and October-November at -24 m (9.8 “C). The minimum temperature (3.8-4.0 “C) for all depths was in late March. Little variation of salinity was noted (31-33x,). The sea state was relatively calm from June through October (Fig. 1). Thereafter, turbulence increased through December, DEPTH(m) D .---. (j ,2
SEAoSIAy,
. .. . . . _.-._
;ACTOR
1=
1-15
3= 5=
15-21 r21 7 20
20r
0
J
S
0
N
D
J
F
M
A
M
J
1975
Fig.
1. Temporal and spatial variations of water temperature at Appledore Island, ME, and cumulative monthly sea state (0) (swell height) at White Island, NH, based upon the maximum daily values.
122
T. L. NORALL
2oc
ET AL.
d-
ii . : 1 d
100
J
A
Fig. 2. Seasonal
Fig. 3. Spectral
50
variations
N
D
J
197sFM
A
M
J
of total and PAR solar irradiance.
energy distribution (400-700 nm) at -6, - 12, - 18 and -24 m, using Jerlov’s and Moon’s (1940) transmittance and solar energy distribution data.
(1970)
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
123
RED ALGAE
followed by a decreasing sea state, except for April when there was a major storm. As suggested by Szeicz (1974) the photosynthetically active range (PAR) of the daily total radiation (i.e. both direct and diffuse) remains nearly constant at z 500,o. The lowest levels of solar energy and PAR were in December, while the maximum values were in August (Fig. 2). The percentage of PAR at a given depth was calculated for each 25 nm interval (Fig. 3), employing Moon’s (1940) and Holme’s (1964) calculations on solar energy distribution. The blue-green portion (500-550 nm) of the spectrum had the maximum penetration, and the ratio of blue-green/red light increased with depth. REPRODUCTION
Membranoptera alata showed a pronounced seasonal cycle (Table I), with minimum and maximum reproduction in October and December, respectively (Fig. 4). Overall, the plant’s reproduction (i.e. total or both tetrasporic and gemetophytic) was maximal at - 18 m (Fig. 5), primarily due to a high frequency
TABLE I A stattstical
summary
of the reproduction and significant Total reproduction
stature of Mrrnhrrmopr~~r at 0.05 level.
(three-way
Sex
(two-way
Tetrasporic Period Depth 2.65* 1.02
-6m -12m -18 m -24m
Period-total 2.43 8.27* 0.62 20.90*
of variance)
Cystocarpic 2.62 7.04* 7.22* 4.50 (three-way
Sex 1.76
-6m -12m -1X m -24m
analysis
analysis
Spermatangial 2.23 X.23* 16.70* 3.26
of variance)
Depth 2.45 stature
Spermatangial Period Depth 1.10 0.82
(regression-quadratic)
Tetrdsporic 5.X9* 9.82* 4.84 1.99 Total stature
Period x.34*
Cystocarpic Period Depth 1.84 0.59
Period-reproduction
(i.e. F values):
of variance)
Depth 1.88
5.64* % reproduction
analysis
a/r/a
(regression-quadratic)
Period 0.76
*?
T. L. NORALL
124
of tetrasporic
plants (Fig. 6). The reproductive
the same at all four depths being present
ET AL
from November
(Fig.
phenology
of M. data was essentially
7A), with gametophytic
and tetrasporic
plants
to June.
I ..-_.._____./ JAsONDJFMAMJ 1975
Fig. 4. Monthly
A three-way
averages from four depths of the percentage reproduction of Memhrttnoptrrcr Cdophyllis cristata, Ptilotu serruta, and Phycodrys rubens.
analysis
of variance
for total
reproduction
in M. alum
olrrtn,
showed
significant (P 20.05) differences in reproductive types and period but not with depth (Table I). A further two-way analysis of variance of reproduction compared with depth and period only showed a significant tetrasporic-period interaction (Table I). The following period-reproduction interactions (regression quadratic) were also significant: tetrasporic plants at -6 and - 12 m and cystocarpic and spermatangial plants at - 12 and - 18 m. The reproduction of Callophyllis cristata was maximal in August and minimal in November (Fig. 4). Overall, the highest reproduction was at -6 and - 12 m (Fig. 5). The gametophytic and tetrasporophytic generations showed the same distributional pattern (Fig. 6). Shallow-water plants ( -6 m) exhibited a pronounced summer maximum and a winter minimum (Fig. 7B). Cystocarpic plants at - 12 m basically had the same pattern as at -6 m, while tetrasporic plants at - 12 m had a more irregular pattern. Only 19 plants were collected at - 18 m from August through December; at - 24 m no plants were found during July and only 22 plants were collected from January through April. The inadequate sample size may be responsible for the low frequencies of reproductive plants during these periods. A three-way analysis of variance for total reproduction in C. cristata showed no significant differences with sex, depth or period (Table II). A two-way analysis of variance of reproduction compared with depth or period similarly showed no significant differences for any reproductive types, even though significant period effects (regression quadratic) were observed for tetrasporic plants at - 6 and - 24 m,
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
% REPRODUCTION 10 I 6
30 I
1
\
18
-
24
-
-
E
.
12
-
I .
18
-
-
18
-
24
-
-
12
-
18
-
24
-./ yearly
I
100 I
PTILOTA
. \
. \ . ./
10 I 6
100 I
CALLOPHYLLIS
60 I
I
12 -
Fig. 5. Average
./ I
I
30 I
.
.I
/ 20 I
6
\
./
l
E w cl
60 I
1
-
-
.
.
./
6
24
+-----=
\ .
20 I
km)
50 1
,
12
-
STATURE
MEMBRANOPTERA .
-
125
RED ALGAE
I
50 T
PHYCODRYS
./ t
./
reproduction (:‘/,) and stature for Membrwwpte~o LI/UIO, Ptiloto srrrcrta and PhJwdr.vs rubens at four depths.
126
T. L. NORALL
ETAL.
and for cystocarpic plants between - 6 to - 18 m (Table II). Difficulties in sampling design, as noted earlier, prevent any further explanation, other than that the maximum period of female plants was between May and July and for tetrasporic plants between June and August. The reproductive frequency of Ptifota serrata (Fig. 4) varied from 82% (late April) to 637/, (June). Overall, the plant’s reproduction (i.e. total) was maximal at - 18 m
-I
4o_
Callophyllis
MeMbranoptera
40-
1 3020IO-
5 & tY
6 12 18 24
6 12 18 24 30
too-
. Phycodrys
Pti Jota
80604020-
.-•
1 I
I
1
I
l .
6 12 18 24 DEPTH (M) BELOW
M. L.W
Fig. 6. The average yearly reproduction of gametophytic and sporophytic plants of Cullophyllis cristata, Memhranoptera alata, Phycodrys r&ens and Ptiloia serrata at four depths.
REPRODUCTIVE
ECOLOGY
OF SUBTIDAl..
RED ALGAE
127
(Fig. 5), with the tetrasporophytic generation being the primary contributor to this pattern (compare Figs. 5 and 6). Tetrasporic plants had their highest reproductive frequencies at - 12 to -24 m (Fig. 7C), while the greatest frequencies of cystocarpic plants were at -6 and - 12 m. Cystocarpic plants showed an irregular seasonal pattern at each depth.
A
statistical
summary
of the reproduction
and stature of Cu~~~i~h~,~lj.~ cri.rtora (i.e. Fvalues): at 0.05 level.
Total reproduction
(three-way
Sex
analysis
Period 1.87
1.51
O,. reproduction
(two-way
analysis
Tetrasporic Period Depth 0.72 I .06 Period-reproduction
-6m -12m -18m -24m
of variance)
Depth
1.26
* significant
of variance) Cystocarpic Period Depth 2.46 2.70
(regression-quadratic)
Tetrasporic 6.53* 0.39 0.66 9.33*
Cystocarpic 25.40* X%30* 11.60* 0.22 ___
Total stature
(three-way
Sex 6.47 Period-total -6m -I?m -18 m -24m
analysis
of variance)
Depth 10.60* stature
Period 6.87*
(regression-quadratic)
6.8?* 2.62 2.08 3.26
A three-way analysis of variance showed that Ptilota’s reproduction (i.e. total) was signi~cantly different with depth and sex, but not period (Table III}. A two-way analysis of variance showed no significant reproductive differences in period or sex ((i.e. individual generations), nor in period-reproduction with a regression quadratic analysis (Table III). The reproduction of P~JXO&JG rubem was maximal in December and minimal in October (Figs. 4 and 7D). Overall, the plant’s reproduction was maximal at - 12 m (Fig. 5) with the gametophytic and tetrasporophytic generations showing the same distributional pattern (Fig. 6). Tetrasporic plants exhibited their seasonal maxima
T. L. NORALL
128
ET AL.
in January and June at - 6 m, July and November at - 12 m, and July and January at - 18 m (Fig. 7D). Cystocarpic plants showed a seasonal shift in their reproductive phenology with increasing depth (Fig. 7D). The maximum number of cystocarpic plants was in July at - 6 m, and in December at - 12 to - 24 m. The low frequency of male plants masked any pattern, except for the bimodal maxima in late November and June at - 12 m. TAMLE III A statistical
summary
and stature of Pfihfci .SP~~YII~~ (i.e. F values): at 0.05 level.
of the reproduction
Total reproduction
(three-way
analysis
‘!, reproduction
(two-way
analysis
Tetrasporic Period Depth 0.44 2.45 Period-reproduction
-6 -12 -18 -24
m m m m
Period I.85 of variance) Cystocarpic Period Depth 2.92 0.95
(repression-q~ddratic)
Tetrasporic 1.95 2.94
Cystocarpic 1.58 1.63 1.73 0.63
1.07 3.45 Total stature
(three-way
Period-total 3.11 0.79 0.30 1.01
analysis
of variance)
Depth 47.58*
sex 5.83
-6m -12m -18m -24m
of variance)
Depth 7.51*
Sex 53.09*
* significant
___ stature
.-.-.. _.._
Period 3.55*
(regression-quadratic)
The reproductive phenology (i.e. total) of P~?~co~r~~~rupees was signi~cantly different with sex, but not with period or depth (Table IV). Mate plants showed a significant change in reproduction with depth, the maximum and minimum percentage of males was at - 12 and -24 m, respectively (Fig. 7D). No significant period-reproductive differences were detected by a two-way analysis of variance; however, a significant period effect was detected with cystocarpic plants at - 12 m (Table IV).
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
RED ALGAE
129
130
T. L. NORALL
ET AL.
STATURE
The largest plants of Membranoptera alata were found during June to December and the smallest ones between late winter to spring (Fig. 8). Overall, the largest plants were found at - 12 m (Fig. 5), with both the gametophytic and sporophytic generations showing a similar pattern (Fig. 9). No significant differences in stature were found with depth, period or sex (Table I). In contrast, the plant’s stature showed a significant period effect at - 12 and -24 m (Table I).
,,,‘______ / f
... . .I””
3-
z Q
\....
‘i! 1 1
Pycodryr
,A”
.~___.__........................ C&,,&,,ir
_... .“““‘-.......__.._.__.__, ,,....” _/ .‘.‘.‘-..,. ..............._.._.. _,,_,,,_,___ ...’./’ ._---as----.___-_.---- -9, ‘\ ..---____.__
__-. -_-
_C.Membrono~tera
1 JASONDJFMAMJ
Fig. 8. Monthly
averages
1975
from four depths of the mean length (cm) of Membranoptera alatrr, Callophyllis cristata, Ptilota serrata, and Phycodrys rubens.
The stature of Callophyllis cristata was maximal between March and June and minimal in late January (Fig. 8). The largest plants were recorded at - 6 and - 12 m (Fig. 5), with both generations basically showing the same pattern (Fig. 9). The stature of Callophyllis was statistically different with depth and period, but not sex (Table II). The mean size of the fronds also showed a significant period effect at -6m. Ptilota serrata showed its maximum and minimum stature in August and November, respectively (Fig. 8). Overall, the plants increased in size from -6 to -24 m (Fig. 5), with both generations showing an identical pattern, except for the gametophytic plants at -24 m (compare Figs. 5 and 9). The plant’s stature (i.e. total) was significantly different with time (period) and depth but not sex (Table III). In contrast, the mean frond size showed no significant period effects at the four depths when analyzed with a regression quadratic evaluation. The stature of Phycodrys rubens was maximal in August and minimal in January (Fig. 8). The largest plants were recorded at - 12 m and the smallest at -24 m
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
5-
2.0-
4-
1.5-
RED ALGAE
131
-@ .. .... . .. .-,
& 98
3l.O20.5l-
.
MeMbranoptera
calloph,4is
EL-n-n-G 6 121824
I
1
1
I
6 12 18 24
I
z
z g7-
. ..-. .* P
7-
‘.
l.*’
5-
9-
5
f
l. 0.. f
.*
5-
\
3-
3Phycodrys
l-
Pti iota l-
I
I
1
6 121824
I
I
I
I
1
6 12 18 24 DEPTH (M ) BELOW M. L.W.
Fig. 9. The average yearly length of gametophytic and sporophytic plants of Cu//ophylfis crktara, Membranoptera alata, Phycodrys rubens, and Ptilota serrata at four depths.
132
T. L. NORALL
ET AL.
(Fig. 5); both generations showed a similar pattern, except for the gametophytic plants at -24 m (compare Figs. 5 and 9). The stature of Phycodrys was statistically TAHLE IV
A statistical
summary
of the reproduction
Total reproduction
and stature of Plr~c~dr~s at 0.05 level. (three-way
(two-way
Period-reproduction
-6m -12 m -1Sm -24m _____-.I..
1.86 i .69 .._________
-6m -12m -18m -24m
of variance) Spermatangial Period Depth 7.43’ 1.73
(regression-quadratic)
(three-way
analysis
Spermatangial 0.31 0.04 0.19 0.35
of variance)
Depth 5.79*
Sex 3.37 ~___ Period-total
analysis
Cystocarpic 3.35 9.77* 0.48 1.15 _._______~_
Tetrasporic 1.21 2.08
Total stature
Period 0.93
Cystocarpic Period Depth 0.89 1.53
Tetrasporic Period Depth 1.36 0.60 ._~_..^_
* significant
of variance)
Depth 2.51
Sex 1.59* 7; reproduction
analysis
rubrns (i.e. F values):
Period 9.90* -.
stature
(regression-quadmti~}
9.90* 2.71 0.35 1.84
different with depth and period, but not sex (Table IV). The plant’s stature at - 6 m was significantly different over time. STATURE
AND
REPRODUCTION
Fig. 5 compares the average stature and reproduction (i.e. both tetrasporic and gametophytic plants) of all four species at different depths. Membranoptera had its maximum reproduction at - 18 m and its maximum length at - 12 and - 18 m. The depth of maximum reproduction and maximum length were approximately the same for ~a~~oph~Ili.~cristata, while they corresponded for Phycodrys rubens. The maximum reproduction of Pt~lota sermta was at - 18 m, as compared to - 24 m for its longest length. Fig. 10 summarizes the average monthly length and reproduction for the four
REPRODUCTIVE
ECOLOGY
OF SUBTIDAL
RED ALGAE
133
species, based upon the depths of maximum stature for each species (Fig. 5). Overall, the period of maximum stature seemed to be just prior to maximum reproduction, with P. set-rata showing the least pronounced pattern. ~e~~ra~upter~ alata and Phycodrys ruhens had a non-synchronous pattern of reproduction and growth, with maximum summer growth and fall-winter reproductive maxima. Callophyllis cristata showed a simultaneous decline in growth and reproduction during the summer and winter and a somewhat earlier growth than reproductive maxima. loo-
-20
Callophyllir Y
/
. .. ... .,,,,..,...I
Mambranoptero
1
IOJASONDJFMAMJ
v/-/T_______
J
ASONDI
FMAMI
1001 /
’ 60 t a & f
JASONDJ
FMAMJ
Fig. 10. Monthly averages of the reproduction (yg) and length (cm) of M~vnh~u-rmopte~ uiuru, Ccdloph~//i.c crkra!n, Ptilorrr srrmtri, and Phycadry.~ rubens, all at - 12 m except for P. scr-rata (at - 24 m).
As noted previously, the temperature (Fig. l), salinity and nutrient data (Norall & Mathieson, 1976) were evaluated simultaneously with the growth and stature data, employing a linear regression analysis built into the Harvey (1968, 1975) program. No significant correlations could be drawn between the hydrographic data and the mean size of a reproductive gene~tion or the percentage of a given reproductive generation. DISCUSSION Of the four red algae studied only ~~~~r~~o~te~u alata showed a significant (P >; 0.05) seasonal variation of reproduction, which was primarily associated with the tetrasporic generation (Table I). A similar regression analysis of the other
134
T. L. NORALL
ET AL
species showed that 5 of the 8 depth-sex combinations of Callophyllis cristata were sign&ant, while 1 of the 12 combinations for Phycodrys rubens, and none of the 8 depth-reproductive combinations for Ptilota se~rata were significant (Tables II-IV). The synchronized reproductive phenology of Mernbranoptera alata at different depths (Fig. 7A) suggests that it is primarily “triggered” by seasonal differences in day-length at each depth. The low levels of reproduction for Calloph~~flis cristata and Phycodrys rubens at - 24 m (Figs. 5,6,7B and D) may be attributable to reduced light intensities or a change in light quality (Fig. I), as temperature did not change significantly between - 18 and -24 m. P. rubens and Ptiiota serrata both had a “surface” inhibition of their reproduction, as low levels of reproduction occurred at -6 m (Figs. 5, 6, 7C and D). The latter phenomenon may have been due to saturating light intensities (see Mathieson & Norall, 1975a) or inhibiting light quality (Fig. 3) rather than temperature, as P~zycodr~.~rube~zs had its highest reproduction during the summer while Ptilota serrata had a constant level of reproduction at -6 m. Two basic patterns of vertical distribution of haploid and diploid generations were apparent (Figs. 6 and 7): (1) the coexistence of both reproductive phases at different depths, and (2) the dominance of diploid generations within the deep subtidal. P~zycod~ys rubens, ~e~b~anopte~a a~ata, and ~a~~ophy~l~scristata showed the first pattern. The reproductive phases of Prilora were differentially stratified, with a maximum frequency of cystocarpic plants at -6 and - 12 m and the highest frequency of tetrasporic plants at - 18 and - 24 m. Previous physiological studies (Mathieson & Norall, 1975a) have shown that both generations of Ptilota exhibit the same light optimum for net photosynthesis. Even so, the tetrasporic plants have a higher rate of net photosynthesis at a variety of light intensities than the cystocarpic plants. Thus, light intensity per se is not the direct cause of the differential occurrence of tetrasporic and cystocarpic plants. Rather, differential growth and viability could be associated with a variety of factors, including light intensity, light quality, temperature, and nutrients. It is of interest to note that Chondrus crispus exhibits the same stratification (Mathieson & Burns, 1975) and photosynthetic pattern (Mathieson & Norall, 1975b) of its reproductive generations as Ptifota. Other examples of differential proportions of tetrasporic and cystocarpic generations have been noted within the geographical distribution of several red algae (Fritsch, 1945; Levring, 1947; Dixon, 1965). In addition, Barilotti (1973) has described several examples of diploid dominance in the brown alga Zonariu,farlowii in “stressful” or marginal habitats. Callophyllis cristata, Phycodrys rubens, and Ptilota serrata showed significant vertical differences in stature (Table II-IV). Of the three species, Callophyllis showed a decrease from -6 to -24 m (Fig. 9), while Phycodrys showed its maximum stature at - 12 m. Ptilota showed a striking difference in stature, with the tetrasporic generation increasing in size from -6 to -24 m and the gametophytic plants similarly elongating from -6 to - 18 m. Edelstein et al. (1969) and Mathieson &
135
REPRODUCTlVEECOLOGYOFSUBTIDALREDALGAE
Burns
(1975) have recorded
similar
and Chondrus crispus, respectively
morphological-depth
~ i.e. deep-water
plants
patterns
with P. serrafa
are longer
and narrower
than shallow water specimens. The seasonal Ptilotu serruta appearance
variation of stature for PhJjcodrys rubens, Callophyllis (Figs. 8 and IO) can be attributed to two major
of juveniles
and the degeneration
of tissues
after
cristata and factors: the
sporulation.
Large
reproductive plants of each species were vulnerable to storm “pruning”, and they exhibited a decrease in stature during the fall period of maximum sea heights (compare Figs. 1, 8 and 10). A spatial relationship was apparent between stature and reproduction for Phycodrys rubens and Callophyllis cristata (Fig. 5). The mean reproduction and stature of Phycodrys were both maximal at - 12 m, while they were approximately the same ( -6 and - 12 m) for Callophyllis cristata. In contrast, Membranoptera alatu and Ptifota serrata had their highest levels of reproduction at - 18 m versus their longest plants at - 12 and -24 m, respectively. In contrast to the diploid dominance of tetrasporophytes of P. serrata within the deep subtidal (Fig. 6) no differential stature of the gametophytic and sporophytic plants (Table
was apparent III). Overall,
at the 0.05 level but they were different at the 0.10 level there was a trend of increasing stature of tetrasporic versus
gametophytic plants with increasing depth (Fig. 9). Such a trend was not apparent with Phycodrys rubens, Callophyllis cristata or Membranoptera alata (Fig. 9). The higher net photosynthesis of the tetrasporophytes of Ptilota serrata (Mathieson & Norall, 1975a), as well as the larger stature of the diploid plants may contribute to the overall diploid dominance of the tetrasporophytic plants. As noted earlier, however, a variety of interrelated factors, including differential viability of propagules may also be significant. Obviously more questions have been raised than answered regarding the cause and effect relationships of diploid dominance of P. serrata, and the contrasting patterns Callophyllis, and Membranoptera.
of growth
and reproduction
for Phq,codrJ,s,
ACKNOWLEDGEMENTS
We wish to thank several individuals at the University of New Hampshire for their assistance; Drs. A. Baker and R. Kinerson for their critical reading of the paper; Dr. W. Urban and Mr. 0. Durgin for their advice with statistical analyses; Dr. J. Murdoch for helpful comments regarding the irradiance studies; and Mr. Ned McIntosh for his assistance as Captain of the R. I/. Jere A. Chase.
136
T. L. NORALL
ET AL.
REFERENCES
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