Estuaries Vol. 24, No. 4, p. 623-635 August 2001
Macroalgal Bloom Dynamics in a Highly Eutrophic Southern California Estuary
I~RISTA t~AMER*, I{&RLEEN A. I~O'~%E, and PEGGY FONG
Departmer~t of O,~ganismic Biology, Ecology and Evoh~tion, University of Califmnia, Los Angeles, Los Angeles, CaliJbr,zia 90095 i606
ABSTRACT: A 10-too long monitoring study was carried out in Upper Newport Bay estuary (UNB), Oraage County, Cafifornia, to quantify the macroalgal community of a southern California estuary. Quarterly sampling began December 1996 at 8 stations along the main channel and tidal creeks ranging from the head to the lower end of UNB. At each station, two strata (one at high and one at low elevation) were surveyed. Macroalgal species abundance (% cover and biomass) and algM tissue nitrogen (N) and phosphorus (P) were measured. The algal community changed from sparse macroalgal cover during winter 1996 to larger patches dominated by Euteromorpha i~ttesti~a.lis in spring 1997. The com- munity was characterized by a thick cover of macroalgae comprised of E. i~ttesti~a.lis and Ulva exI)ausa in summer 1997 and U. expausa and Ceraorium spp. in fall 1997. UNB returned to sparse macroalgal cover by spring 1998. In summer and fall 1997~ biomaxs of E. i~ttesti~alis and C,,raoEum reached over 1~000 g wet wt m a each~ and U. exI)ausa biomaxs exceeded 700 g wet wt m a. Tissue N was high in E. i~ttesti~alis and U. expausa collected from UNB (~3% dry wt) and higher in Ceramium (~3.5% dry wt). Tissue P in all three algae ranged from 0.24-0.28% dry wt. Tissue N:P (molar) ratios in E. i~ttesti~talis and U. e~pmtsa ranged from 16.4 to 30.0 and in Ceramium from 21.8 to 40.1. A field experiment was conducted in which E. irttestin~lis was used a.s a bioa.ssay of N and P availability. Algal tissue was cultured under known conditions and samples were deployed throughout the estuary and left for 24 h. Tissue N of algae from these bags showed a nominal increase in N with proximity to file primary nutrient input to the system~ San Diego Creek (p = 0.0251; r~ = 0.200). Our data indicate that UNB is already a highly eutrophic ~stuary~ but macroalgal blooms in UNB may increase if more N is added to the system.
Introduction gae has been documented in many locations Eutrophication of coastal systems is increasing throughout the world (Rudnicki 1986; Raffaelli et worldwide (e.g., Lowthion et al. 1985; Valiela et al. al. 1989; Valiela et al. 1999; Geertz-Hansen et al. 1992; de Jonge 1995; Duarte 1995; McComb and 1993; Peckol et al. 1994; Marcomini et al. 1995; Lukatelich 1995; Nixon 1995; Paerl 1997). Aug- Peckol and Rivers 1995a, b; Hernfindez et al. 1997; mented supplies of nutrients, specifically nitrogen Hauxwell et al. 1998). These blooms are often (N) and phosphorus (P), to coastal systems often composed of opportunistic macroalgae in the gen- have critical effects on coastal ecosystems by in- era Bntero,mc~rpha, Ulva, and Orad[a,ria. Bntero,mc~rpha creasing both primary productivity (Hatcher and and Ulva spp. have high nutrient uptake rates (Ro- Larkum 1983; Oviatt et al. 1986; Lapointe 1989; senberg and Ramus 1984; Fulita 1985; Duarte Lapointe et al. 1992; McGlathery et al. 1992; Duar- 1995) as do species of red algae such as Cera'miu,~z te 1995; Nixon 1995) and biomass accumulation of ,rMn-t~,m (Pedersen and Borum 1997) and macroalgae (Delgado and Lapointe 1994; Fong et (Peckol et al. 1994). High uptake rates, combined al. 199ga,b). In temperate zones, marine systems w-ith the ability to store nutrients (Fujita 1985; are typically limited by N, though secondary limi- Duke et al. 1989; Fong et al. 1994; Aisha et al. tation by P can occur (Howarth 1988; Wheeler and 1995), may allow estuarine macroalgae to prolif- Bj6rnsS, ter 1992; Duarte 1995; Nixon 1995; Taylor erate in systems with episodic nutrient fluxes. As a et al. 1995). result, coastal estuaries subject to pulses of high The association between increased anthropogen- nutrients are often characterized by seasonal ic nutrient loads and nuisance blooms of macroal- blooms of macroalgae (Lowthion et al. 1985; Souls- by et al. 1985; Sfriso et al. 1987; Raffaelli et al. 1989; Valiela et al. 1992; Peckol et al. 1994; Duarte * Corresponding author: present address: Southern Califor- 1995; Nixon 1995; Hern~ndez et al. 1997; Sfriso nia Coastal Water Research Project, 7171 Fenwick Lane, West- minster, California 92683; tele: 714/'372-9237; e-mail: kristak@ and Marcomini 1997). sccwa-p, org. While macroalgae are a natural component of
2001 Estuarine Research Federation 623 624 K. Kamer et al. estuaries, excessively large blooms can have nega- Cillllomla > Upper Newport Bay Area tive ecosystem-wide effects. They can cause anoxic R : '(.. ,-, _ 8;E conditions by periodically blanketing sediments (Sfriso et al. 1987; Young et al. 1998) thereby caus- "N: ,j ing shifts in sediment intZaunal communities (Raf- tZaelli et al. 1991; Ahern et al. 1995). Cellular res- piration by algal mats either at night or during the day when light is below the compensation point in ~ LowG~t M~I ell the bottom layers of the mats can deplete oxygen ~] Constant Water Channel in the water column (Sfriso et al. 1987; Valiela et al. 1992). This can result in fish and invertebrate , fsX .4-o mortality, which may ultimately affect birds and ,,-~ ~:~ other fauna in the food web (Raffaelli et al. 1989). Macroalgae can often remove pulsed nutrient in- puts from the water column before the}, can be 117.90ow 117115~ detected by traditional water sampling methods I (Fong et al. 1998). In pulsed systems, water column Fig. 1. Location of Upper Newport Bay estuary in Orange nutrients rarely correlate with primary producer County, California, with 8 permanent transects (1-8) and sites abundance or productivity, although macroalgal of the E~teromorpha i.mestir~alis bioassay experiment (A-E) tissue N and P values are known to reflect the am- marked. bient nutrient conditions that an alga recently ex- perienced (Bi6rns~ter and Wheeler 1990). Algal tissue N:P ratios can also be used to infer limitation monitoring of the algal community began in De- by either N or P (Wheeler and Bj6rnsS, ter 1992). cember 1996, and continued through March 1998 Tissue N and P content can thus be used as a bio- at 8 permanently established transects in UNB assay to estimate relative differences in nutrient (Fig. 1). Transects were chosen along a gradient levels in different areas of an estuary (Lyngby from the head of the bay, where the primary fresh- 1990; Lyngby and Mortensen 1994; Horrocks et al. water input is, to the lower end of UNB, where the 1995; Fong et al. 1998). highly developed and modified Lower Bay begins. California's wetlands are important habitat for a Four transects were established along the main multitude of organisms as refuges, nurseries, channel (1, 4, 5, 8), two each on the east and west breeding grounds, and foraging areas (Zedler banks. Another four transects were located in tidal 1996). The}, have also been threatened by human creeks (2, S, 6, 7), two of which were off the main development in the last century. Much wetland channel to the east side, and two to the west side. acreage has been lost and surrounding urbaniza- We expected to see greater effects of nutrient en- tion heavily affects that which does remain (Wil- richment, such as higher percent cover and bio- liams and Zedler 1992). Upper Newport Bay mass, and greater tissue nutrient content near the (UNB) is one of the largest remaining estuaries in mouth of San Diego Creek, the main nutrient southern California. It is surrounded by urbanized source, as compared to the more distant sampling areas and is subject to both point and nonpoint sites at the lower end of the estuary. sources of N and P pollution (California Regional At each transect we measured along two S0-m Water Quality Control Board 1997). Nutrient in- strata: the upper stratum was 0.5 m toward the wa- puts and their effects have not been well studied ter from the vascular vegetation line. The lower in southern California (Williams and Zedler 1992; stratum was parallel to the upper stratum and 1.5 but see Peters et al. 1985; Fong 1986; Rudnicki m toward the water from the vascular vegetation 1986) and there are no published reports of algal line. In the tidal creeks, which had steeper banks community percent cover, biomass, or tissue nutri- than the main channel, the lower strata ran along ent content in southern California (for other geo- the bottom of the creek. We sampled along the graphic locales see Lowthion et al. 1985; Pregnall edges of the main channel and in the tidal creeks and Rudy 1985; Sfriso et al. 1987; Peckol and Riv- to characterize the macroalgal community" in both ers 1995a; Herngmdez 1997). The olzlective of this research was to characterize blooms of macroalgae types of environments. in a southern California estuary in terms of sea- To estimate abundance of macroalgae we used sonality, magnitude, and tissue nutrient content. mea~surements of both percent cover and algal bio- mass because both types of measurements can ex- Materials and Methods hibit high variance when algae are distributed ir- FIELD SURVEYS regularly (Sfriso et al. 1987). A 0.25-m e quadrat We conducted a l~InO stud), of UNB to deter- strung with fishing line with 36 intercepts was mine macroalgal communi~ ~ dynamics. Quarterly placed on the benthos at ten randomly chosen Macroalgal Blooms in a Eutrophic Estuary 625 points along each stratum and percent cover of seasons. One-way analysis of variance (ANOVA fac- macroalgal species was recorded. As our second es- tor: algal species) was used to determine differenc- timate of abundance, we measured algal biomass es in algal tissue % N, % R and N:P ratio. Follow- in seasons where it was present in sufficient quan- ing significant one factor ANOVA, Fisher's Pro- tities to allow collection. The macroalgal commu- tected Least Significant Difference test (PLSD) was nity of UNB was dominated by Entero,mo~phca intes used to identify differences among means. tit~cdis-, Ulvca expat~sa, and filamentous red Cerca,mi,~m spp. These algae often become embedded in the NUTRIENT BIOASSAY sediments on which they grow and can be difficult To quantify relative levels of dissolved inorganic to separate from mud. We randomly selected five N and P availabilit7 in UNB along the hypothesized of the ten quadrats where percent cover counts nutrient gradient, we used E. ir~testir~cdis as a bio- were conducted and placed a plastic cylinder 26.5 assay organism. For the bioassay technique to be cm in diameter on the benthos. To standardize our successful, the algae need to be exposed to the collection of algal biomass, we collected all the al- environment long enough that they can accumu- gae inside for 90 s. Algae were kept in a cooler in late nutrients in their tissues, but not so long that the field and returned to the laboratory within 6 tissues become saturated and distinction between h. There they were sorted to remove debris, mud, sites is lost. Because we did not know a priori the and animals, rinsed briefly w-ith distilled water to appropriate length of time required for the bio- remove salts, and separated to species. Algae were assay in LrNB, we ran it for 24 and 48 h. placed in a nylon mesh bag, spun in a salad spin- Entero,mo~pha intestinalis was collected fi-om Mugu ner for I minute and wet weighed, and then dried Lagoon, Ventura Count3,, California, on July 7, at 60~ to a constant weight. Algal tissue samples 1998. Algae were kept outdoors at University of were ground with mortar and pestle and sent to California, Los Angeles, in shallow pans filled with the DANR Analytical Laboratory at University of seawater low in nutrients relative to estuarine water California at Davis for tissue N and P analyses. To- (22.81 -+ 0.46 IJAzINO s, 2.10 _+ 0.09 p~M PO4, mean tal N in algal tissue was analyzed by Nitrogen Gas + SE) with constant aeration in order to reduce Analyzer using induction furnace and thermal con- variability in initial tissue N content (Fong etal. ductivity. Total P in algal tissue was quantitatively 1998). The pans were kept at 25~ and covered determined by atomic emission spectroscopy fol- with fiberglass window screening for 7 d. Salinity lowing microwave acid digestion of sample. Tissue was monitored daily and distilled water was added N and P are reported as percent dr}, wt and molar to compensate for evaporation. The day before the N:P ratios were calculated fi-om these data. experiment began, 5 g (_+0.1 g) sub-samples orE. Three-way analysis of variance (ANOVA factors: ir~testir~[is were placed in mesh bags made out of season, transect, stratum) was used to determine nylon window screening and returned to low nu- differences in algal percent cover and algal species trient seawater overnight. Initial subsamples were biomass for E. intestina~is, U. ea~ansa, and Cera,miu~ rinsed briefly with distilled water, dried, and ana- spp. To determine if data complied with ANOVA lyzed for tissue N and P as described above. Initial assumption of homogeneity of variance, residuals tissue N of the algae that were placed in the field versus fitted Y values were plotted. Unequal vari- was 1.605 _+ 0.063% drywt (mean _+ SE) and initial ances in the percent cover data were corrected by tissue P was 0.206 + 0.005% dry wt. The mean transforming the data with arcsin square root cal- molar N:P ratio of initial samples was 17.8 + 0.5. culations. Unequal variances in the algal biomass On July 15, 1998, 10 bags containing algae were data were corrected by taking the log (x + 1) of deployed at each of five sites in LrNB along the the data. Means reported throughout the text were estuarine gradient (A-E; Fig. 1). Bags were at- generated from untransformed data. Due to the tached to bamboo stakes with polypropylene rope patchy nature of the algae, while it was possible to and the stakes were placed at the water's edge at collect biomass, some samples were too small for mid-tide. Bags were placed at similar elevations to analysis of either tissue N or R If there was not assure that the}, were exposed to water for equal enough tissue to conduct both N and P analyses, amounts of time during tidal cycles. A small float we chose to prioritize N over R In several cases our was attached to each bag to suspend it in the water n was
Winter 1996 Spring 1997 S ummer 1997 Fall 1997 Spring 1998 ] Enteromorpha 7- ] ] -7 I intestinalis ___A~ 6- I [] I;PPERSTR,VFA 5- []ml __] [] LOWERSrRATA 4- 2 | 3- im 2- __J I ] I- a
7- Uh,a expansa 6- 5- 7, < 4-
3-
2- 9r [] !- b L..
8-
7- !t Ceramium spp. 6- IIIIi
5-
4-
3-
2-
1-
0 25 50 75 25 50 75 0 25 50 75 25 50 75 0 25 50 75 100
% COVER Fig. 2. Seasonal abundance ofEnteromo~pha intestinalis (top), Ulva expansa (middle), and Cera~ni~n spp. (bottom) in Upper Newport Bay in Winter 1996, Spring 1997, Smaamer 1997, Fall 1997, and Spidng 1998 (bars are -+1 SE). * indicate strata where data were not collected. used for each time period to determine if there There were significant effects of season, transect, was a significant relationship between distance and stratum on percent cover (Table 1). During fiom the nutrient source and tissue N values, tissue winter 1996, E. intestinalis comprised 30% of the P values, or tissue N:P ratios. cover at one stratum but otherwise was absent or present only in very low abundance (<5%). While Results abundance increased in spring 1997, with cover up FIELD SURVEYS---PERCENT COVER to 81%, it remained spatially patchy. E. i~testinalis Percent cover of E. intestinalis showed a strong was most abundant during summer 1997, when it seasonal pattern over the duration of the study ranged from 6-98% cover. Abundance of E. intes- (Fig. 2). Small anaounts were always present in at tinaSs decreased in fall 1997. The maximum per- least a few locations throughout the 16-too study. cent cover sampled was 46% but most of the strata Macroalgal Blooms in a Eutrophic Estuary 627
TABLE 1. Sumnaary of three way ANOVA of the effects of season, stra~ma, transect, and all interactions on percent cover of Entero- morpha intestinalis, Ulva expa.nsa, and Ceg'a.r~aiu.mspp. in Upper Newport Bay (analysis performed on data transformed by arcsm squm-e root).
>dgal Group Source df MS F p E.i.ntesti.nalis Season 4 7.251 216.162 0.0001 Transect 7 3.003 89.529 0.0001 Stratum 1 1.762 52.528 0.0001 Season X transect 27 0.453 13.518 0.0001 Season • stratum 4 0.447 13.340 0.0001 Transect X sh'atum 7 0.472 14.068 0.0001 Season • transect • sn'amm 24 0.686 20.448 0.0001 E::-o:- 675 0.084 gZ mj)ansa Season 4 27.377 938.200 0.0001 Transect 7 2.356 80.755 0.0001 Stratum 1 0.232 7.949 0.0050 Season X transect 27 1.214 41.620 0.0001 Season )< sn'aman 4 0.087 2.982 0.0186 Transect X sh'amm 7 0.629 21.539 0.0001 Season )< transect )< sU'amm 24 0.604 20.685 0.0001 Error 675 0.029 C'era.mi~.m spp. Season 4 5.613 394.083 0.0001 Transect 7 2.330 165.604 0.0001 Stratum 1 3.861 271.093 0.0001 Season X transect 27 1.006 70.609 0.0001 Season )< sU'aman 4 1.457 102.286 0.0001 Transect • stratum 7 0.770 54.094 0.0001 Season )< transect )< stratum 24 0.497 34.887 0.0001 Error 675 0.014 had <8% cover, In spring 1998, E. intestineSs cover pense (Table 1), While all transects showed season- ranged from 1-24% and was present at only 4 of al changes in U. expansa abundance, the changes the strata, were not consistent among transects, causing an There were significant interactions between all S interaction between season and transect, Interac- factors of the ANOVA for percent cover of E. intes tion between season and stratum occurred because tineSs (Table 1). The interaction between season in one season U. expense had greater percent cover and transect was caused by consistently low cover in the upper strata as compared to the lower strata, of E. intestinelis at transect 1 (at the lower end of In all other seasons there was no difference be- UNB) regardless of season. There was no seasonal tween strata. There was also a significant interac- effect on E. intestinaSs cover at transect 1 whereas tion between transect and stratum; among tran- all other transects showed seasonal peaks of E. in- sects, there was no consistent pattern with regard testiness. Across seasons, E. intestineSs percent cov- to strata. er was higher in upper strata as compared to lower, Cera,miu~n spp. also exhibited a seasonal pattern except during spring 1997 when there was no dif- of abundance (Fig. 2) with a peak during fall 1997. ference between upper and lower strata. This Its percent cover wa~s significantly affected by sea- caused an interaction between season and stratum. son, transect, and stratum (Table 1). It was found There was also a significant interaction between at only one stratum in w-inter 1996 when it con> transect and stratum because there was no consis- prised 5% of the cover. In summer 1997, Cere'miu~z tent pattern of greater cover in either strata among cover ranged fi-om 1-80% at transects where it oc- transects. curred. During fall 1997, cover of Ce,ra,miu,m Percent cover of U. expansa showed a strong sea- reached 100% at two transects and wa~s patchily dis- sonal pattern over the 16-mo sampling period (Fig. tributed among transects. It was absent from UNB 2). It was significantly affected by season, transect, in the spring seasons. "vghen C~ramiu,m was present, and stratum (Table 1). U. ex~ansa was present in it was more abundant in the lower strata than in very low abundance during winter 1996 and spring the upper strata. 1997 (<1%), and it was absent from our transects There were significant interactions between all in spring 1998. U. ex~ansa was most abundant dur- three factors of the ANOVA. Cera,miu,,m spp. was ing summer and fall 1997. Its cover ranged from never found at transects g and 4, causing an inter- 2-82% in summer and from 4-100% in fall. action between season and transect, Because (_-;e~ There were significant interactions between all g a,miu,m was never present at these transects, they factors of the ANOVA for percent cover of U. ex> did not exhibit the same seasonal patterns ofabun- 628 K. Kamer et al.
tteoe- ble 2). The interaction between season and tran- a summer 1997 [] Ceramiumsll p, [] Ulvaexpansa sect was caused by peaks in abundance in summer 1997 at two transects and a peak in abundance in 1500- 9 Enteromorphaintextinalis fall 1997 at a different transect indication that the effect of season varied with transect. The sea~sonal 1000- effect was lack of biomass in winter and spring sea- sons. Across seasons, biomass was greater in the upper strata in fall 1997, but there were no differ- 500- ences in biomass between upper and lower strata for summer 1997, causing an interaction between
~: 0--- season and stratum. There was not a consistent pat- b) fall 1997 tern of greater E i~testinalis biomass in either the upper or lower strata with regard to transect, re- .2 15011- sulting in significant interaction between transect an d stratum. giomass of U. expansa was also only collected in summer and fall 1997. It was significantly affected by season and transect but not by stratum (Table 9). In summer, U. expar~sa biomass ranged from 6- 771 g wet wt m -2 and was collected everywhere ex- cept transect 1 (Fig. 3a). Mean U. expa.nsc~ biomass 0 -_ ,,,_ ...... in summer from both upper and lower strata was i1.11 L 2021. 31i3L 4 U ,:1L 5t'SL &IJ6L 7[;71. ~l'S I. 816 + 47 g wet wt m -e making it the most abun- Transect dant alga at that time though the maximum re- Fig. 3. Combined algal biomass of Er~te.romco'pha i.ntestir~lis, corded biomass of U. expansa was less than that of U~va expar~sa, and Cerar~h~zaspp. for a) smnmer 1997 and b) fall E. irttestinMis. In fall 1997, biomass ranged from 1997 showing biomass of over 1,500 g wet wt m -s. 20-798 g wet wt m -e and wa,s collected from every transect (Fig. 3b). Mean U. expc~.nsc~ biomass in the fall was similar to summer (259 + 34 g wet wt m 2). dance that the other transects did. This caused an There were significant interactions between fac- interaction between transect and stratum. Across tors of the ANOVA for U. expansa biomass (Table seasons, Ceramiu~# wa,s more abundant in the lower 2). Interaction between season and transect oc- strata, except for the two spring seasons when it curred because three transects had peaks of U. ex- was absent fi-om UNB. This caused an interaction par~sa biomass in summer 1997 while two others between season and stratum. had peaks in fall 1997. The effect of season was dependent upon transect. There was also no con- ALGAL ]~IOMASS sistent pattern of greater biomass in either the up- While E. intestinalis was present in all seasons as per or lower strata among transects, causing a sig- indicated by percent cover data, biomass was gen- nificant interaction between transect and stratum. erally sparse in winter and spring seasons. Quan- Cera'miu~ spp. biomass was also collected only in tities were sufficient to allow biomass collection summer and fall 1997. It was significantly affected only" in summer and fall 1997. Biomass was signif- by transect, season, and stratum (Table 2). In sum- icantly affected by transect, season, and stratum mer, 2-140 g wet wt m 2. was collected fi-om 5 stra- (Table 2). In summer, E. intes6natis was collected ta, and none was collected from the other 11 (Fig. from 12 of 16 strata in amounts ranging from 34- Sa). The mean of Cera~ium bioma,ss in summer 1,141 g wet wt m 2 (Fig. Sa). At 7 of those strata fi-om both upper and lower strata was 20 -+ 6 g wet there was >100 g wet wt m 2. The mean of E. in- wt m e making it the least abundant alga during testi,~Mis biomass in summer from both upper and that season. In fall 1997, 5-1,573 g wet wt m -~ was lower strata was 226 -+ 45 (SE) g wet wt m -2. Mean collected from 1.9 strata (Fig. 3b). P~iomass exceed- E. i'ntesti'naSs biomass for fall 1997 was lower than ed 1,500 g wet wt m ~ at two strata and was >1,000 summer (mean - 62 + g6 g wet wt m ~), and E. g wet wt m e at a third. Mean biomass was much intestir~Mis was less abundant than U. expcmsca and higher than in summer (342 + 73 g wet wt m-2), Cera,miwm spp. in fall (Fig. 3b). Biomass of E. it~tes and Cera,mi.zcm was the most abundant alga during ti'nafs exceeded 100 g wet wt m -~ at only 4 of 11 fall 1997. strata from which it was collected. There were significant interactions between the ANOVA for biomass of E. i'ntestinMis showed sig- three factors of the ANOVA for Cera,mizcm spp. bio- nificant interactions between the three factors (Ta- mass (Table 2). Interaction between season and Macroalgal Blooms in a Eutrophic Estuary 629
TABLE 2. Summary of three factor ANOVA of the effects of season, stratum, transect, and all interactions on wet biomass of F~nteromorpha i.ntestinalis, Ulva expansa, and Ce.ra.r~ai.u.mspp. in Upper Newport Bay (analysis performed on data transformed by log(x + 1)).
#Jgal Group Source df MS F p E.i.ntesti.nalis Season 4 4.396 73.979 0.0001 Transect 7 0.641 10.781 0.0001 Stratum 1 0.363 6.104 0.0140 Season X transect 27 0.381 6.406 0.0001 Season • stratum 4 0.201 3.388 0.0099 Transect X sh'atum 7 0.273 4.591 0.0001 Season • transect • sU'amm 24 0.237 3.986 0.0001 Error 300 0.059 U. m'pansa Season 4 13.533 262.404 0.0001 Transect 7 1.510 29.273 0.0001 Stratum 1 0.126 2.446 0.1189 Season ;~ transect 27 0.845 16.376 0.0001 Season )< stratum 4 0.049 0.955 0.4325 Transect x sU'atum 7 0.453 8.782 0.0001 Season )< transect )< stratum 24 0.301 5.845 0.0001 Error 300 0.052 Cera.miwm spp. Season 4 4.254 155.062 0.0001 Transect 7 1.063 88.750 0.0001 Stratum 1 2.124 77.418 0.0001 Season X transect 27 0.669 24.366 0.0001 Season )< su-amm 4 1.029 37.502 0.0001 Transect X sU'atum 7 0.381 13.905 0.0001 Season )< transect )< stratum 24 0.340 12.410 0.0001 En-or 300 0.027 transect occurred because one transect had great- (22.9 + 0.7; p - 0.0001, PLSD). :7. expanse was est Ceramium biomass in summer 1997 while 6 tran- significantly different from E. intestinaSs (p - sects had greatest biomass in fall 1997. Interaction 0.0004, PLSD). occurred between season and stratum. When col- Tissue N of E. intestinMis was variable within the lected, biomass was greater in the lower strata as seasons it was measured. Mean tissue N ranged compared to the upper, but in three seasons no fi-om 1.61-4.22% dry wt in summer 1997 (Table Ceramiu~n biomass was collected. There wa~s also an g). In general, tissue N of E. intestinMis was higher interaction between transect and stratum. Cera,m- at mid-estuary transects (Transects 4--7) than at iu,m biomass was greater in the lower strata at all transects at either end of the estuary. Tissue N of transects except two. E. intestinaSs in fall was similar to that measured in summer, though the range it covered was smaller Tlssus NUTRIENTS (1.87-3.23% dry wt). Tissue P was higher in sun-> Tissue N (p - 0.0030, ANOVA) and P (p - mer 1997 than in fall for E. intestina~is. The mean 0.0184, ANOVA) were significantly different summer P value was 0.287 + 0.009 (SE) % dry wt among E. intestinMis, U expansa, and Cerarniurn spp. whereas in fall it was 0.282 + 0.020. Molar N:P collected from LYNB in summer and fall 1997. Cer ratios for both seasons ranged from 16.4-28.1. a,miu,m had the highest tissue N at 3.477 _+ 0.146% [~ expansa tissue N was higher in summer 1997 dr), wt (mean + SE). It varied significantly from than in fall (Table 4). The mean summer N value both U. expansa tissue N (8.086 + 0.065% dr), wt; was 8.438 + 0.071 (SE) % dry wt. In fall it was p - 0.0063, PLSD) and E. intestinaSs tissue N 2.769 _+ 0.084% dry wt. U. expansa tissue P was also (2.924 + 0.125% dry wt; p - 0.0010, PLSD). E. higher in summer 1997 than in fall. Mean tissue P intestinalis had the highest tissue P at 0.278 + was 0.289 + 0.005% dry wt in summer and 0.2B5 0.009% dry wt. It varied significantly from both U. _+ 0.006% dry wt in fall. Across both seasons, molar e,x~ansa tissue P (0.258 _+ 0.005% dry wt; p - N:P ratios ranged fi-om 19.8-30.0. 0.0447, PLSD) and 4>ra~nium tissue P (0.248 + In contrast to the pattern seen in U. expansa, 0.009% dr), wt; p 0.0036, PLSD). Resulting tissue Ceramiu~n spp. tissue N was higher in fall 1997 than N:P (molar) ratios were also significantly different in summer (Table 5). The mean summer N value among algal species (p = 0.0001, ANOVA). Cer- was 3.029 _+ 0.291 (SE) % dry wt. In fall it was amium had the highest mean N:P ratio (32.5 _+ 3.631 _+ 0.162% dry wt. Ceramium tissue P was also 1.3). It was significantly different from U. ax~ansa higher in fall 1997 than in summer. Mean tissue P (26.3 _+ 0.3; p = 0.0001, PLSD) and E. intestinalis was 0.224 -+ 0.011% dry wt in summer and 0.252 630 K. Kamer et al.
TABLE 3. E,nteromorph, a i,ntestinalis tissue N and P values and tissue N:P (molar) ratios from summer and fall 1997. gleans are given with standard error and n. Transects where no samples were collected were omitted fi'om the table.
Tissue I',~ Tissue P Tissue N P
,-qeasol: Tral:sect ~qtratulTl Meal: BE n M e an SE n M e an BE n Surmner 2 Upper 2.380 0.279 4 0.250 0.015 3 19.3 2.2 3 Lower 8 Upper 1.610 0.211 4 0.203 0.007 3 16.4 2.5 3 Lower 2.688 0.297 5 0.260 0.009 5 25.0 2.7 5 4 Upper 3.279 0.603 2 0.335 0.005 2 21.7 4.3 2 Lower 4.224 0 1 0.390 0 1 24.0 0 1 5 Upper 2.911 0.240 2 0.240 0 1 24.6 0 1 Lower 3.465 0.389 2 0.290 0 1 23.5 0 1 6 Upper 3.992 0.173 3 0.317 0.027 3 28.1 1.5 3 Lower 7 Upper 3.642 0.083 5 0.320 0.009 5 25.3 1.2 5 Lower 3.597 0.282 2 0.860 0 1 20.7 0 1 8 Upper 2.981 0 1 0.270 0 1 24.4 0 1 Lower 2.716 0.141 4 0.295 0.022 4 20.7 1.7 4 Fall 3 Upper 1.866 0.072 2 0.175 0.015 2 23.7 1.1 2 Lower 6 Upper 3.234 0 1 0.290 0 1 24.7 0 1 Lower 7 Upper 3.035 0.189 2 0.260 0.010 2 25.8 0.6 2 Lower 8 Upper Lower 2.679 0 1 0.230 0 1 25.8 0 1
_+ 0.012% dry wt in fall. Highest mean tissue N and There was no significant relationship between P values of Cera,mium were measured at Transect 7, tissue N:P ratio and site (p 0.0747, r ~ 0.1S2; lower stratum, in fall 1997. Molar N:P ratios in Fig. 4c). Ratios ranged fiom 1S.2-24.9 for all five summer and fall 1997 ranged from 21.8-40.1. sites tested.
NUTRIENT e)I OASSAY Discussion In the E. intestinMis bioassay experiment, algae UNB is a highly eutrophic system. The estuary ex- placed closer to the nutrient source experienced perienced large seasonal blooms of macroalgae greater increases in tissue N than algae further which are often characteristic of systems subject to fi-om the source (Fig. 4a). There was a significant large inputs of nutrients (Rudnicki 1986; Sfi-iso et positive linear relationship between proximity to al. 1987; Raffaelli et al. 1989; Valiela et al. 1992; the mouth of San Diego Creek and accumulation Geertz-Hansen et al, 1998; Peckol et al, 1994; Mar- of tissue N (p - 0.0251) after 24 h. Tissue N per- comini et al. 1995; Peckol and Rivers 1995a,b; Her- cent change from initial was greater for sites at the nSndez et al. 1997; Young et al. 1998). During sun-> head of the estuary, where San Diego Creek enters mer and fall 1997 when blooms ofE. intestindis, U the estuary, than it was for transects further dowal expansa, and Cemrnium spp, occurred, some areas the bay. Distance fi-om San Diego Creek only ex- surveyed were completely covered w-ith macroal- plained 20% of the variabilit3r (r 2 - 0.200). The gae. Chrer 150 g dry wt m e of algae were collected significant relationship detected after ,94 h disap- during peaks of algal abundance (transformation peared after 48 h exposure in the estuary. After 48 of our biomass wet weight data to dry weight; Fong h percent change in mean tissue N at all sites and I(amer unpublished data). Research in other ranged fi-om 54-73% and there was no consistent nutrient rich ~ystems has yielded results within the spatial pattern of change in tissue N among sites. same order of magnitude. Pregnall and Rudy E. i~testinalis did not show consistent increases (1985) reported yields fi-om field collections of En in tissue P values with increasing proximity to the tero,mm/)h,a and Ulva spp. ranging from 800-750 g nutrient source after 24 h (Fig. 4b). There was no dry wt m ~. HernSndez et al. (1997) collected 200- significant relationship between site and tissue P 875 g dry wt m -2 of U/va spp., and Lowthion et al. percent change from initial (p - 0.0859, r 2 - (1985) reported lower values of 31-50 g dry wt m e 0.123). There was also no significant relationship ofEnteromm/)ha spp. Another bloom forming green between percent change from initial in tissue P macroalga, Cladophora vagabundc~, was found in the and site after 48 h. Changes in tissue P were also field at densities >1 kg dry wt m -e (Peckol and much lower in magnitude than changes in tissue N. Rivers 1995a). The red alga Gracila,r'ia tihvah, iae Macroalgal Blooms in a Eutrophic Estuary 631
TABLE 4. Ulva expa,usa tissue N and P values and tissue N:P (molto') ratios from stumbler and fall 1997. Means are given with standard error and n. Transects where no samples were collected were omitted fl-om the table.
Tissue N Tissue P Tissue N P
,-qeasol: Tral:sect Stratul~l Meal: SE i: Meal: S]~ n Meal: SE n Summer 2 Upper 3.306 0.115 5 0.246 0.012 5 30.0 1.5 5 Lower 5.751 0 1 3 Upper 1.991 0 1 Lower 2.940 0.685 2 4 Upper 3.527 0.076 4 0.298 0.007 4 26.3 0.5 4 Lower 3.623 0.072 4 0.308 0.008 4 26.2 1.0 4 5 Upper 3.332 0.392 3 0.267 0.022 3 27.6 2.2 3 Lower 3.048 0.594 2 0.275 0.045 2 24.4 0.8 2 6 Upper 3.977 0.132 2 0.310 0 1 27.5 0 1 Lower 3.933 0.094 2 7 Upper 3.732 0.139 5 0.306 0.005 5 27.0 0.8 5 Lower 3.852 0.144 3 0.323 0.008 8 26.4 0.8 8 8 Upper 3.349 0.036 5 0.288 0.010 5 25.9 0.9 5 Lower 3.130 0.105 5 0.288 0.010 5 24.2 1.3 5 Fall 1 Upper 2.184 0 1 0.180 0 1 26.9 0 1 Lower 2.835 0.057 4 0.245 0.005 4 25.6 0.1 4 2 Upper 2.880 0.092 4 0.222 0.009 4 28.8 1.6 4 Lower 2.926 0 1 0.220 0 1 29.5 0 1 3 Upper 1.573 0.064 3 0.153 0.009 3 22.8 0.7 3 Lower 2.143 0.123 5 0.240 0.013 5 19.8 0.6 5 4 Upper 3.056 0.132 5 0.236 0.006 5 28.7 1.2 5 Lower 2.539 0 1 0.190 0 1 29.6 0 1 5 Upper 3.169 0.360 5 0.256 0.024 5 27.3 1.9 5 Lower 2.603 0.180 5 0.230 0.009 5 25.0 0.8 5 7 Upper 3.247 0.491 2 0.275 0.035 2 26.1 0.6 2 Lower 3.354 0.180 3 0.297 0.017 3 25.1 1.6 3 8 Upper 2.840 0.249 5 0.226 0.014 5 27.7 1.1 5 Lower 2.971 0.183 5 0.246 0.012 5 26.7 0.5 5
which is highly abundant in Waquoit Bay, Massa- (Pregnall and Rudy 1985). Lowthion et al. (1985) chusetts, has been found at densities >100 g dry found that macroalgae (principally Entero,no~pha) wt m 2 (Valiela et al. 1992), which is similar to the peaked every summer for 6 yr in Langstone Har- bioma~ss of the red Cera~iu~n spp. fiom UNB. born-, England, and were practically absent in win- Our two estimates of abundance, percent cover ter. The Lagoon of Venice exhibited maximum ma- and biomass measurements, proved to be valuable eroalgal biomass in late spring-summer (Marcom- in different seasons. When macroalgal cover was ini et al. 1995), and Sfriso et al. (1987) reported sparse, it was not practical to measure biomass be- high Ulva 'rig'ida biomass in May and July of one cause the small, fine pieces of algae on the sedi- year. Hern~ndez et al. (1997) reported semi-an- ment surface could not be quantitatively collected. nual peaks (June and December) in abundance During those times, cover was an effective tool in for Ugva in the Palmones River estuary, Spain. In characterizing the community. Measurements of southern California, other estuaries also experi- biomass were a good tool for characterizing the ence seasonal blooms of macroalgae (Peters et al. macroalgal community during bloom m, ents. Dur- 1985; Rudnicki 1986) though the blooms occur in ing summer and fall 1997, cover measurements of- winter or spring seasons. Variation in the timing of ten reached 100% for many strata and did not al- bloom events among estuaries may be related to low for distinction between these strata. However, temperature or other factors that influence bloom biomass estimates for the same strata showed dif- dynamics. ferences in macroalgal abundance between the We did not see higher cover, biomass, or tissue strata. nutrient content of E. intestinaSs or [L e~x~)ansanear The algal community of UNB showed strong sea- the mouth of San Diego Creek as we had expected. sonal patterns. Macroalgae were sparse in winter Instead, algae were patchily distributed throughout and spring seasons probably due to light and/or the estuary. Water movement at the mouth of San temperature limitation. Similar patterns of ma- Diego Creek is downstream, possibly preventing ac- croalgal seasonal abundance hm~e been document- cumulation of macroalgae in the upper reaches of ed for other areas. In Coos Bay, Oregon, Entero- UNB. Entero,mmpha and [gva tend to form large 'mo~J)ha and Ulva were abundant July-October mats that detach from the substrate (Sfriso et al. 632 K. Kamer et al.
75 1987; Duarte 1995; Young et al. 1998) ; we observed a) 0 such mats floating throughout the estuary while we were sampling. This may also be why E. i,~testinalis e. 0 ~ 0 0 tissue N was highest mid-estuary rather than at the E 50 head of the estuary near the primary nutrient O & source (California Regional Water Quality Control Board 1997; Boyle and Kamer unpublished data). o ~ Cera,tzi'u'm spp. was attached to the sediments and 25 therefore not able to move throughout the estuary as E. intestinalis and U. expansa were (Kamer per- sonal observation). The highest Cercamiur~z tissue N z and P values were measured in samples taken from Transect 7 which was the closest transect to the o o o mouth of San Diego Creek where Ceramiu,m nutri- ~ O ents were measured. Because Cera,~dum is not mo- -25 bile, its tissues reflected higher nutrient content b) o o closer to the nutrient source as we expected. ~ 20 Macroalgal tissue N in UNB (~9-4% dry wt) was comparable to levels found in other field studies. 0 0 0 E Wheeler and Bj6rnsSter (1999) found tissue N O 15 & content in E. intestinaSs ranging fi-om 2.09-5.11%
TABLE 5. Ceramic,m, spp. tissue N and P values and tissue N:P (molar) ratios fi'om stumbler and fall 1997. Means are given with standard error and n. Transects where no samples were collected were omitted from the table.
Tissue 1N Tissue P Tissue N P
Season Tral:sect Stratul~l Meal: SE i: Meal: S]~ n Meal: SE n Summer 2 Upper Lower 2.578 0.290 4 0.233 0.029 4 25.2 3.3 4 6 Upper Lower 3.868 0.365 4 0.213 0.009 4 40.1 2.7 4 8 Upper Lower 2.252 0.287 2 0.230 0.010 2 21.8 3.7 2 Fall 1 Upper Lower 3.259 0.443 5 0.200 0 1 30.4 0 1 2 Upper 2.922 0.260 2 0.180 0 1 39.1 0 1 Lower 3.484 0.418 5 0.235 0.010 4 34.6 3.6 4 5 Upper 1.316 0 1 0.110 0 1 26.5 0 1 Lower 6 Upper 3.931 0.283 4 0.248 0.020 4 36.4 5.5 4 Lower 8.988 0.083 5 0.282 0.011 5 81.6 1.9 5 7 Upper 3.168 0.244 2 0.190 0 1 34.1 0 1 Lower 4.492 0.092 5 0.304 0.012 5 32.9 h0 5
Chaeto,mo~pha linu,m and 33 to 44 in species of Cod macroalgal cover during summer and fall seasons ium. Larned (1998) found a ratio of 48.5:1 (total with biomass comparable to that of bloom events N:total P) for Ulvafasdata. The higher N:P ratio at other locales. The levels of N in macroalgal tis- found in other green macroalgae suggest that sue collected from UNB indicate that the system is bloom-forming green macroalgae in UNB are not enriched with N. Yet the algae in UNB may not be saturated with N, and they may have the ability to saturated with N as indicated by their N:P ratio, take up more N. Further inputs of N to this system which were lower than others that have been re- may continue to fuel algal blooms and cause the ported. Further inputs of N may" be utilized by the current conditions to worsen unless other factors algae. Additional nutrients entering the system due such as light or temperature become limiting. to continual growth and development in the wa- The E. intestinatis bioassay may be too sensitive tershed have the potential to exacerbate these al- for use in a system as nutrient-rich as UNB appears gal blooms, increasing their magnitude and dura- to be. After 24 h, distance from San Diego Creek tion. only explained 20% of the variability observed, and after 48 h, increases in tissue N were great enough ACKNO1,VLED GMENTS to obscure any potential spatial relationships. Us- This work was funded by the California Water Resources Cen- ing the bioassay over a shorter time scale, such as ter, the Environmental Protection Agency Water and Watm~ a few hours, may provide better insight into nutri- sheds Program #R825381, and a University, of California at Los ,amgeles Academic Senate grant. We thank the Califol"nia De- ent dynamics in highly enriched systems. High var- partment of Fish and Game for site access and use of their ca- iability between replicates at a site may have oc- noes. Special thanks are extended to Risa Cohen, Damion Gas- curred if nutrients were not spatially homogenous. tellum, and Steve Kim for help in the field and to Dm-io Diehl Nutrients may travel through the water column in and Jonathan Fmgerut for invaluable assistance ruth Fig. 1. discrete packets and could have affected some, but LITERATURE CITED not all, replicates at one site. Though only 20% of the variability may be explained by distance, we ,~Fa~,J., j. LYONS@ McL~, aND I. VALI~I,A. 1995. Invm~ tebrate response to nutrient-induced changes in macxophyte suggest two mechanisms for the increase in tissue assemblages m Waquoit Bay. Biological B~lletin 189:241-242. N with proximity to San Diego Creek. Either N was AmSHA, K. A., E. F. SHABANA, M. S. EL-ABYAD, I. A. KOBBIA, AND removed from the water column as the flow from F. SCHANZ. 1995. Pulse feeding with nitrate and phosphate m San Diego Creek moved through the estuary, or relation to tissue composition and nutrient uptake by some concentrations of N entering UNB in the San Di- macroalgae from the Red Sea at Ghardaqa (Egypt). Jo~rnal of Basic Miorobiolo~ 35:135-145. ego Creek flow were diluted by mixing with tidal ATmNSON, M. J. AND S. V. Sa~rrI-I. 1983. C:N:P ratios of benthic waters. If the former occurred, then N was re- m~rine plants. Lbn.nolo~, a,nd Ocea,nog'ra.[)h)~28:568-574. tained by the system, either sequestered in the sed- BJdSRNSATER, B. R. AND P. A. WH~wV~. 1990. Effect of nitrogen iments or taken up by the algae and was not simply and phosphorus supply on growth and tissue composition of 07va fenestrata and Enteromo~pha intestinalis (Ulvaies, Chloro- flushed out to the ocean. phyta). Journal of Ph),colog), 26:603-611. In conclusion, our data indicate that UNB is a CaLIFO~ KeOIONAL WATER QUALITY' CONTROL BOARD. 1997. highly eutrophic system. UNB experienced high Staff report on the nutrient total maxhmlm daily load for 634 K. Kamer et al.
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