------
J. exp. mar. Biol. Ecol. , 1977, Vol. 26, pp. 211-224 --~ Elsevier/North-Holland Biomedical Press
MACROPHYTE-EPIPHYTE BIOMASS AND PRODUCTIVITY IN AN EELGRASS (ZOSTERA MARINA L.) COMMUNITY
POLLY A. PE.NHALE 1 North Carolina State University, Raleigh, North Carolina, U.S.A. and Atlantic Estuarine Fisheries Center, Beaufort, North Carolina, U.S.A.
Abstract: The biomass, productivity (1 4 C), and photosynthetic response to light and temperature of eelgrass, Zostera marina L and its epiphytes was measured in a shallow estuarine system near Beaufort, North Carolina, during 1974. The maximum of the biomass (above-ground) was measured in March; this was followed by a general decline throughout the rest of the ::rear. The average biomass 2 was 105.0 g dry wt m- 2 ; 80.3 g dry wt m- was eelgrass and 24.7 g dry wt m- 2 was epiphytes. The productivity of eelgrass averaged 0.88 mg C g- 1 h- 1 which was similar to that of the epiphytes, 1 1 0.65 mg Cg- h- • Eelgrass and epiphyte productivity was low duri.1g the spring and early summer, gave a maximum during late summer and fall, and declined during the winter; this progression was probably due to environmental factors associated with tidal heights. On an areal basis, the average annual productivity was 0.9 g C m- 2 day- 1 for eelgrass and 0.2 g C m- 2 day_- 1 for the epiphytes. Rates of photosynthesis of both eelgrass and epiphytes increased with increasing temperature to an asymptotic value at which the system was light saturated. Both eelgrass and epiphytes had a temperature optimum of < 29 °C. A negative response to higher temperatures was also reflected in biomass measurements which showed the destruction of eelgrass with increasing summer temperatures. The data suggest that the primary productivity cycles of macrophytes and epiphytes are closely in terrelated.
INTRODUCTION
Seagrass systems have been studied for many years but only recently has their important contribution to the marine environment been evaluated. These systems, which include grasses and algae as primary producers, are widely distributed in coastal areas and are among the most productive in the ocean (McRoy & McMillan, 1973; Thayer, Wolfe & Williams, 1975). Productivity rates for seagrasses alone are high; annual production ranges from 200-3000 g C m -z for turtle grass (Thalassia testudinum) and from 5-600 g C m- 2 for eelgrass (Zostera marina) (Phillips, 1974). The other primary producers in the system are benthic microalgae and macroalgae, phytoplankton, and epiphytic algae attached to the seagrass blades; unfortunately, little is known of their biomass, productivity or interrelationship with the seagrasses. The object of this work was to evaluate the role of one of these primary producers, the epiphytes, in the primary productivity cycle of an eelgrass system near Beaufort, North Carolina. Both eelgrass and epiphyte biomass as well as productivity were
1 Present address: W. K. Kellogg Biological Station, Michigan State University, Hickory Corners, Mich., U.S.A.
211 212 POLLY A. PENHALE measured for the period January through December, 1974, as well as the effects of light and temperature on primary productivity. Most studies of epiphytes in their natural state of attachment have been descriptive. Sieburth & Thomas (1973) made scanning electron micrographs of the colonization of eelgrass by its epiphytic community. The eelgrass was initially colonized by the diatom Cocconeis scutellum which formed.a crust, a structure apparently necessary for the further colonization by other micro-organisms. Seasonal patterns of seagrass epiphytes have also been described (Humm, 1964; Reyes-Vasquez, 1970; Brauner, 1975). In distributional studies on the plants, Kita & Harada (1962) and Dodd (1966) found a greater abundance of diatoms on the portion of eelgrass blades farthest from the leaf base. Others have compared the distribution of epiphytes in various places (Pieczynska & Spodniewska, 1963; Edsbagge, 1968; Rautiainen & Ravanko, 1972; Main & Mcintire, 1974). Production estimates of epiphytic communities have often utilized cell counts, biomass changes or chlorophyll a measurements (Brown, 1962; Szczepanska, 1970), but few studies have evaluated the role of epiphytes in the overall productivity of aquatic ecosystems. · Comparative productivity studies based on oxygen change or 14C uptake mea surements have shown that epiphytes can make significant contributions to the total primary productivity of aquatic systems. Jones (19158) estimated that the total annual 2 1 epiphytic productivity, 200 g C m- yr- , was 22 % that of Thalassia testudinum in dense stands in Biscayne Bay, Florida. Most studies, however, have been limited to freshwater environments. Hickman (1971) measured the contribution to the primary productivity of a pond by phytoplankton (2 %), epipelic algae attached to the sedi ment surface (3 %), and epiphytes attached to Equisetum (95 %), but no estimate of the macrophyte productivity was given. Wetzel & Allen (1972) estimated a mean production of 171 g C m- 2 yr- 1 in Lawrence Lake, Michigan; of this, macrophytes contributed 48 %, phytoplankton 30 %, and epiphytic algae (on both emergent and submerged substrata) 22 ~{ These studies provide useful estimates of the importance of epiphytes in the pro ductivity of shallow aquatic systems but certain technical difficulties were involved in each. The epiphytic production data of Jones (1968) were based on measurements of oxygen production by epiphytes colonizing dead or dying Thalassia leaves. Yet, the in ternal cycling of oxygen resulting from photosynthesis has been demonstrated for fresh water angiosperms (Hartman & Brown, 1967), so that if there were any photosynthesis within the dying Thalassia, the oxygen production and probable re-cycling could resulti n over-estimates of oxygen production by epiphytes. Furthermore, if the dead or dying leaves supported increased microbial populations, the resultant oxygen con sumption would give an under-estimate of oxygen production by epiphytes. In the study of Hickman (1971 ), epiphytes were first scraped off Equisetum stems and then incubated with 14C in bottles. This scraping may have altered the rates of epiphyte production because of cell damage, loss, and inability of the epiphytes to interact with the macro phyte. The epiphytic productivity values given by Wetzel & Allen ( 1972) were based EELGRASS-EPIPHYTE BIOMASS AND PRODUCTIVITY 213
on 14C uptake by epiphytes colonizing glass slides. Yet the epiphytes which colonize artificial substrata may not be representative of populations which attach to Jiving substrata, and such an experimental design would eliminate the effect of any inter actions between macrophyte and epiphyte. Epiphytic productivity has here been estimated using the sensitive 14C method on intact plants with their attached epiphytes. The 14C experiments were first carried out in situ and afterwards, the eelgrass and its epiphytes were separated for the measure- ' ment of 14C incorporation. In this way, there was no interference with any interaction nor transfer of material between the macrophyte and its epiphytes. In the only other study using a similar technique, Hickman ( 1974) estimated the productivity of epiphytic diatom populations attached to Chiloscyphus, a leafy liverwort, from 14C incubations followed by sonication to separate the macrophyte and epiphytes.
LOCALITY AND METHODS
This work was carried out in the Newport River e~tuary, North Carolina, on an eelgrass bed in a semi-protected embayment on the southeastern side of Phillips Island (Fig. I). The eelgrass bed, ;:::; 20,000 m 2 in extent was not a permanent feature
ATLANJIC OCEAN SCALE 0 5 10
KM
Fig. 1. Map of the estuarine system near Beaufort, North Caroli:rn, showing Phillips Island in the Newport River estuary, and the eelgrass bed examined. 214 POLLY A. PEN HALE of the estuary prior to 1968 (Thayer, Adams & LaCroix, 1975). The mean tidal height is 1 mat high tide and 0.3 mat low tide.
BIOMASS AND PRIMARY PRODUCTIVITY MEASUREMENTS Standing crop or above-ground biomass measurements were made monthly from January through December, 1974. Eelgrass was harvested by clipping the grass at the sediment surface from two 0.25 m 2 quadrats at each of eight stations located on a northeast-southwest transect through the middle of the eelgrass bed. Any macrophytic algae or invertebrates included in the sample were separated from the eelgrass in the laboratory. The eelgrass (including standing dead) was dried at 90 °C for 48 h and then weighed. Primary productivity estimates, based on in situ 14C measurements, were carried out from January through December, 1974. Plexiglas chambers (10.5 1) with battery operated stirrers were constructed following the design of Dillon (1971). Twice monthly, one dark and one or two light chambers were anchored in the sediments in the eelgrass bed. Four-hour incubations were carried out after inoculation with 5--10 14 14 µCi C-Na2 C03 . Most incubations, lasted from 10.00 to 14.00 hand were general ly carried out from mid-ebb to low tide. After the incubations, the above-ground eelgrass was harvested by clipping the grass at the sediment surface. Each sample was divided into subsamples, placed in plastic bags, and immediately quick-frozen with dry ice. The samples then were returned to the laboratory and stored in the dark at -20 °C. Measurements of water temperature, salinity and pH were made on each sampling date. Total alkalinity was measured by the method described by Karlgren (1962); carbonate alkalinity and available carbon were calculated from the tables of Strick land & Parsons (1968). Daily incident radiation was recorded with an Eppley pyrano meter connected to a strip-chart recorder. Underwater measurements of photosynthe tically active light (400-700 nm) were made with the Lambda quantum meter (Lamb da Instruments Corp., Lincoln, Nebr.) from August through December, 1974. Measurements were made about 10 cm above the sediment in 70 to 100 cm of water. Epiphytes were separated from the eelgrass by using dry ice to quick-freeze the eelgrass-epiphyte samples in the field immediately after collection (slow-freezing was unsatisfactory). The frozen samples then were lyophilized and many epiphytes simply flaked off the blades. Then, each blade was carefully scraped with a flat spatula to remove the remaining epiphytes. Based on microscopic examination it is estimated that with much care and practice, about 70 to 90 ~~of the epiphytes can be so removed without damaging the eelgrass. Other methods tested to separate eelgrass and its epiphytes proved unsatisfactory. A major problem was the particular epiphytic community found on the North Carolina eelgrass, where, the dominant epiphytes throughout much of the year are three species of crustaceous, calcium carbonate-secreting red algae, often covering the complete width of the eelgrass leaf and curving around its margins. Hand scraping EELGRASS-EPIPHYTE BIOMASS AND PRODUCTIVITY 215
fresh eelgrass blades without freezing and drying was ineffective in removing the epiphyte complex. A sonication method similar to that of Hickman (1971) was tested; no combination of time and sonication intensity removed the epiphytes without first shredding the eelgrass. Epiphytes tended to flake off the blades after quick-freezing and thawing; then they could be scraped in the same manner as after lyophilization: however, this method was felt to be unsatisfactory because cell rupture during the freezing and thawing process would probably result in leakage of incorporated 14C. For example, 13 samples separated by scraping in a few ml of filtered sea water after quick-freezing and thawing lost from l 0 to 99 '.lo of incorporated 14C. Once separated and desiccated for 24 h, eelgrass and epiphyte samples were ana lysed for incorporated 14C. Samples were weighed to the nearest 0.01 mg, wrapped in Whatman No. 42 ashless filter paper and compressed into pellets. These pellets were combusted in a Packard Model 305 Tritium Carbon Oxidizer where the evolved C02 was trapped in a scintillation solution. Radioactivity V/as measured with a Beckman LS-2000 Liquid Scintillation system. All counts were corrected for background, recovery efficiency after combustion, and counting efficiency. Production was calculated as follows:
4 2 _ -i (1 C Assim.). (1 C Avail.) (1.06) mg C (g dry wt) 1 h = ------(Wt) (1 4 C Add.) (t) - ' where 14C Assim. is the counts/min (cpm) of the samples, 14C Add. the cpm of the isotope added to the chamber, and 12C Avail. the mg inorganic carbon available in the 10.5-1 chamber. The factor 1.06 is a correction for isotope discrimination. Wt is the dry weight of the eelgrass or epiphyte sample (to the nearest 0.1 mg) and t the length of the incubation period in hours. Dark incubation values were subtracted from light values to correct for non-photosynthetic uptake of 14C.
LIGHT AND TEMPERATURE EXPERIMENTS
Several experiments were designed to test the effect of light and temperature on the photosynthetic rate of eelgrass and its epiphytes. Eelgrass plants, including roots, were placed in l. 7-1 jars covered with neutral density screens (Perforated Products, Brookline, Mass.). Six light levels were used: 100, 50, 30, 15, 5, and l % of the ambient light. Three eelgrass plants were placed in each jar which was then inoculated with 14 14 . 40 µCi C-Na2 C03 Samples incubated in situ received varying light intensities due to tidal fluctuation in the eelgrass bed. To avoid this, later incubations were carried out in a Plexiglas incubation chamber situated on a dock where a running sea water system maintained the temperature in the chamber ~ l °C above ambient water temperature. Primary productivity incubations were carried out from 10.00 to 14.00 h on 24th October, 1974, 7th May, and 22nd July, 1975, at ambient water temperatures of 14°, 21°, and 28 °C, respectively. Sample processing followed the procedure describ ed above except that the plants were divided into roots plus rhizomes and into stems 216 POLLY A. PENHALE plus leaves at the end of the experiment. The root-rhizome incorporation of 14C was measured separately from stem-leaf incorporation.
RESULTS AND DISCUSSION
BIOMASS AND PRIMARY PRODUCTIVITY
The average annual standing crop (above-ground) of eelgrass and its epiphytes was 105.0 g dry wt m - 2 and ~ 25 % of this was epiphytes. Based on the ratio of the dry weights of separated eelgrass and epiphytes, an average of 76.5 % (n = 72) or 80.3 g dry wt m - 2 of the mean yearly biomass was contributed by the eelgrass and 23. 5 ~{, of 2 the biomass (24. 7 g dry wt m - ) was epi phytes. The maximum standing crop of eeigrass (including epiphytes) was in March and this was followed by a subsequent general decline throughout 1974 (Fig. 2). This March maximum was preceded by a steady increase in biomass from the minimum in January. Except for a minor increase in July, there was a decline in biomass from April through September. Monthly biomass values ranged from 47.9 to 162.0 g 2 wt m- •
-- BIOMASS --- TEMPERATURE 200 30
~-, E / ' ~ / 150 I ' \ 25 w I \ 0: ~ ::J :'.' \ t- -0 I
1974
Fig. 2. Above-ground biomass of eelgrass (including epiphytes) and water temperature at Phillips Island during 1974: temperatures measured at 10.00 h in ;::: 70 to 100 cm of water.
The seasonal increase in temperature combined with periodic exposure to high temperatures and partial desiccation probably accounts for the observed decline in eelgrass biomass during the summer. This decline occurred as the water temperature increased during the summer. The temperatures during this work were measured at 10.00 h in approximately 70 to 100 cm of water. Values did not exceed 27.5 °C; however, maximum temperatures generally occur in mid-afternoon and have been as high as 34 °C in the eelgrass bed (J. Thorp, pers. comm.). Biebl & McRoy (1971) found that although eelgrass in Alaska was tolerant of temperatures from 0-35 °C, EELGRASS-EPIPHYTE BIOt./iASS AND PRODUCTKVITY 217 prolonged or frequent temperature rises > 30 °C could re3ult in the destruction of eelgrass. Thayer, Adams & LaCroix (1975) noted that Zostera near Beaufort, North Carolina, began to die when water temperatLres reached ,:::; 28 °C. During the spring tides of late spring through autumn, the water level in the Phillips Island eelgrass bed falls to a few centimeters for several hours. In 1974 these extreme low tides coincided with the mid-afternoon temperature maxima. During such Jo.,v tides, the eelgrass either floats on the water surface or becomes almost completely exposed at which time there is damage due to desiccation. A preference is also reflected in the Arctic and temperate distribution of eelg~ass, which re::ches its southernmost limit on the eastern coast of the United States at Fear, North Carolina (Thayer, Wolfe & Wiiliams, 1975). It is likely, however, that the thermal limits of eelgrass differ between the plants of the northern and southern temperate regions.
2 00
'50
100 / 0 50 /''·, ,/ ------~//' E"' I ------
2 00
197 4
Fig. 3. Productivity (mg C g- 1 h- 1 ) of eelgrass and epiphytes at Phillips Island during 1974.
Epiphyte and eelgrass productivity increased from low rates during the spring and early summer to maximal rates during late summer and fall with a decline during the winter; this trend is probably due to a combination of environmental factors. Yearly net primary productivity rates during 1974 ranged from 0.27-1.80 mg C (g dry wt)- 1 h- 1 for eelgrass and from 0.23 to 1.53 mg C (g dry wt)- 1 h- 1 for epiphytes (Fig. 3). The low tides in 1974 were much lower during the spring and early summer than during the latter part of the year, so that the eelgrass may suffer greater desicca tion and damage during the spring-early summer. Furthermore, the lower tidal height would ailow more light to reach the eelgrass. Since all incubations were carried out near low tide, photoinhibition may be reflected in the lower productivity rates. The variability in the measurements is due to daily changes of temperature, light, turbidity, tides, waves, and winds. 218 POLLY A. PENHALE
Although the biomass decreased during the summer, the accompanying increase in productivity resulted in an autumn maximum in net production on an areal basis (Fig. 4). A similar trend was observed for both eelgrass and its epiphytes; daily productivity showed a general increase from January through July and then a decline throughout the rest of the year. Primary productivity ranged from 0.59-1.25 g C m - 2 day- 1 for eelgrass and from 0.07-0.35 g Cm -z day- 1 for epiphytes.
---EELGRASS
-, \ \ \ \ \ \
1974
Fig. 4. Productivity (g C m- 2 day- 1 ) of eelgrass and ep°]phytes at Phillips Island during i974.
The rate of eelgrass productivity was similar to that estimated for eelgrass in other work based on 14C uptake estimates (Table I). The eelgrass rate was 0.88 mg C 1 1 1 1 (g dry wt)- h - and for epiphytes the rate was 0.65 mg C (g dry wt )- h - • On an areal basis, the yearly mean productivity was 0.85 mg C m -z day- 1 for eelgrass and 0.19 mg C m - 2 day- 1 for epiphytes. The North Carolina eelgrass productivity estimated by Dillon (1971) is almost twice as great as the above values even though a similar field procedure was used in both studies and the two localities investigated are only 2 km apart. This difference may be due to several factors. In Dillon's study,
TABLE I
Eelgrass and epiphyte productivity based on 14C uptake measurements in North Carolina (NC) and Alaska (AK).
Months Mean% Primary Productivity ------of surface Reference 1 1 2 1 producer Site (mgcg- h- ) (gcm- day- ) study light
Epiphytes NC 0.65 0.2 12 60 This paper Eelgrass NC 0.88 0.9 12 60 This paper Eelgrass NC 1.90* I. 7 7 40 Dillon (1971) Eelgrass AK 0.93 5.0 4 100 McRoy (1974) Eelgrass AK 1.18 11.0 4 50 McRoy (1974)
* Value estimated from a figure. EELGRASS-EPIPHYTE BIOMASS AND PRODUCTIVJTY 219
eelgrass productivity estimates were made only January through July (the eelgrass disappeared during the rest of the year at his site). In addition, 14C uptake was measured only in epiphyte-free portions of green eelgrass leaves. In contrast, my samples included colonized leaves (which may have lower productivity rates due to shading by epiphytes) and some standing dead leaves as well as epiphyte-free leaves. Finally, Dillon made no correction for dark uptake of 14C. The estimates of eelgrass productivity in Alaska by McRoy (1974) were made during June through August and the high productivity on an areal basis is due to the much larger standing crop of eelgrass in Alaska. McRoy removed eelgrass from the sediments and incubated the plants in screened glass jars at various light levels. Since a submarine quantum meter was available only during the latter part of my study, it is impossible to compare the amount of light energy received by the eelgrass from the three locations. For rough comparative purposes 60 ~,:; light penetration during my incubation periods may be assumed.
LIGHT AND TEMPERATURE EFFECTS ON PHOTOSYNTHESIS Since the initial experiment to test the effect of light and temperature on the photo synthetic rates of eelgrass and epiphytes used non-saturating light levels, it was necessary to calculate the maximum photosynthetic rates. The calculated Pmax for this experiment ( 15 °C) was 1.19 mg C (g dry wt)- 1 h - 1 for eelgrass and 1.11 mg C (g dry wt )- 1 h - 1 for epiphytes. These rates were obtained by assuming the photosynthetic curve to be a rectangular hyperbola of tre form,
I p = Pmax--, l+Io.5
where Pis the photosynthetic rate (mg C (g dry wt )- 1 h - l) under particular light and temperature conditions and P max is the light saturated rate at the same temperature. The photosynthetically active light,!, was measured directly using a Lambda quantum
meter. 10 . 5 is the calculated light at which P equals one half P max- Values of P max and
10 _5 were calculated from a linear regression plot of l/P against/ (Riggs, 1963). These calculations were not necessary in expeiiments carried out at 22° and 29 °C since saturating light levels were used. The effect of light on the photosynthetic rate of both eelgrass and epiphytes follows the usual pattern in algae, photosynthesis increasing with increasing light to an asymptotic value where the system becomes light saturated (Parsons & Takahashi 1973). For both eelgrass and its epiphytes, light saturation was between 600 and 700 µE m - 2 sec- 1 (Fig. 5). No photo inhibition was observed at 15° and 29 °C, while at 22 °C the photosynthetic rates reached a maximum and then slowly declined as the 2 1 light fluxes exceeded 600 µE m - sec- • McRoy (1974) found a similar pattern of photosynthetic rates in Alaskan eelgrass; however, light saturation was reached at the 2 1 lower light flux of about 300 11E m - sec - . The difference in light saturation values 220 POLLY A. PENHALE
for eelgrass in North Carolina and Alaska indicates adpatation to different solar regimes. More detailed comparisons of light effects on photosynthesis of the two eelgrass populations cannot be made since McRoy's photosynthesis curve is based on average productivity and light measurements made over a 4-month period at unspeci fied temperatures.
EPIPHYTES
,,"'----- 3.00 ------22 c
2 .00
.'.c: 15 c - 1.00 .... ------~ ------~ ------'m u en E .,, .,, EELGRASS w :i:: 1-z ~3.00 0 l- I/''----- o -- ... _ :i:: / "- I 2 00 / / /" / / 15 c l.00 / .. .,, ... -----.. ------/ c
,I /
600 1200 1800 2400 LIGHT FLUX (µE m·2 s·1)
Fig. 5. Photosynthesis and light flux for eelgrass and epiph:ytes at three temperatures: dashed por tion of the 15 °C curves calculated.
Both eelgrass and its epiphytes show a temperature optimum for photosynthesis of < 29 °C (Fig. 5). This is consistent with my biomass results which indicated a negative response by eelgrass to increasing summer temperatures. Biebl & McRoy (1971) noted similar effects of temperature on the photosynthetic rate of subtidal eelgrass; as the temperature increased from 0° to 30 °C, the eelgrass photosynthetic rate increased while at higher temperatures, the rate rapidly declined. In general, the photosynthetic rate of eelgrass was lower than that of the epiphytes in the light and temperature experiments in which plants were selected for a relatively heavy epiphyte cover in order to obtain sufficient experimental material. One reason for the lower eelgrass photosynthetic rate may be that the eelgrass received lower light EELGRASS-EPJPHYTE BIOMASS AND PRODUCTIVITY 221
levels due to shading by the epiphytes. The epiphytic cover can be very dense, particu larly during the summer and fall when calcareous red algae are abundant on the grass at Phillips Island. The abundance of epiphytes can be estimated from epiphyte dry weight. Based on twice monthly samples taken during 1974, a range of 17-52 % of the dry weight of eelgrass samples was epiphytes. The epiphyte biomass as percentage of the total leaf plus epiphyte biomass reached a maximum during April, decreased from May through July and rose again during August and September. A rapid autumn decline in epiphytes led to the lowest percen tage in winter (Fig. 6 ). These changes may reflect seasonal changes in the occurrence of epiphyte species. The variation in the seasonal occurrence of epiphytic algal species (excluding diatoms) on Zostera marina in the Beaufort, North Carolina area has been given in detail by Brauner (1975). He found a total of79 species of epiphytic algae which included 11 species of Cyanophyta, 12 species of Chlorophyta, 26 species of Rhodophyta, and 30 species of Phaeophyta. No attempt was made to repeat this work although a cursory examination of eelgrass blades indicated the presence of many of the same species. Brauner observed that half of the Rhodophyta species became established in the spring, and these probably contributed to the spring maxi mum in my study. The summer and fall were most conducive to the growth of Chloro phyta and Cyanophyta. The most conspicuous change observed during this period was, however, the increase in biomass of three species of calcium carbonate-secreting red algae which appeared to be a major component of the second maximum. The autumn decline and winter minimum of proportional epiphyte biomass followed the pattern observed by Brauner, who noted a sharp decline in all algal groups in the fall with nearly half of the species terminating growth at that time.
...~ 40 >- ii: 5 ...0 30 w :;) ...0 ;: 20 >- a: 0 ;;. 10 M A M A N D
1974
Fig. 6. Epiphyte biomass as a percentage of the total leaf plus epiphyte biomass during 1974.
It is possible that variations in both biotic and abiotic material comprising the material measured as epiphyte weight account for the observed productivity pattern rather than true seasonal rate changes since, although the term epiphyte has been used to refer to epiphytic algae, the material weighed consists of a diverse assemblage of other microscopic organisms (bacteria, fungi, protozoans) which may change 222 POLLY A. PEN HALE throughout the year. The species composition of epiphytic algae varies seasonally a:ntl the resultant biomass changes may result in varying dry weights during the year. In addition, the epiphyte weight includes any inorganic material such as calcium carbo nate, silt, mud, or broken diatom frustules, which may be enmeshed in the attached community. Since all epiphyte data were calculated as dry weight, the variation in both biotic and abiotic material comprising the epiphytic community may affect these results. Since the seasonal pattern in epiphytic productivity expressed in g ash-free dry wt, i.e., a measure of organic matter, is very similar to productivity expressed per g dry wt epiphytes (Fig. 7), it seems that these estimates reflect true rate changes rather than dry weight changes of the epiphytic community throughout the year. No distinct seasonal pattern was observed in the percentage of organic matter in the epiphytic community. The percentage of organic matter was caiculated from the loss of weight of epiphyte samples upon ashing at 500 °C for 36 h. Based on twice monthly samples during 1974, an average of 31±8 % organic matter was measured; the range was 24 to 54 ~·~ (s.E. = 1.5).
5 OD I I .1 " -per g dry w1 J I I I ....'..:- 4 00 ---per ilsh f1ec rt1y wt I I I / I / / I u / I / I 3 oo I E I I \ ___ , I I - I I \ > I I ~ 7 00 I \ :> .,..,. .. , I \ a \ 0 ',,, __ ...... / \ \ ll.. 1 00 I \
M A M 1074
Fig. 7. Average monthly productivity of epiphytes (per g dry wt epiphytes and per g dry wt organic: matter) during 1974.
There is no doubt that the epiphytes attached to Zostera marina play an important role in the primary productivity cycle of this seagrass community; furthermore, the data suggest that there is a close interrelationship between macrophyte and epiphyte production. The epiphytes contributed a yearly average of 24 ~~ of the total leaf plus epiphyte biomass. An average 18 % of the total eelgrass and epiphyte productivity on an areal basis was due to the epiphytes. Since eelgrass serves as a substratum for epiphyte attachment, the biomass of the eelgrass influenced that of the epiphytes. For example, the eelgrass biomass reached a maximum in March and generally decreased during the summer and fall; there was a corresponding maximum and decline in epiphyte biomass. EELGRASS-EPIPHYTE BIOMASS AND PRODUCTIVITY 223
ACKNOWLEDGMENTS
I wish to thank Ors J. E. Hobbie, W. 0. Smith, Jr, D. W. Stanley, and G. W. Thayer for their constructive criticism of the manuscript. Research facilities were provided by the Atlantic Estuarine Research Center, Beaufort, North Carolina; I am grateful to the staff for their cooperation and assistance. This study was supported in part by a cooperative agreement between the United States Energy Re>earch Develop ment Agl?ncy (ERDA) and the National Marine Fisheries Service (NOAA).
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