Aquatic Botany, 9 (1980) 73--94 73 Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
A S S E M B L A G E S O F A L G A E A N D I N V E R T E B R A T E S IN S O U T H E R N C A L I F O R N I A P H Y L L O S P A D I X - D O M I N A T E D I N T E R T I D A L H A B I T A T S
JOAN G. STEWART
Scripps Institution of Oceanography, University of California, La JoUa, CA 92093 (U.S.A.)
BARBARA MYERS
San Diego Natural History Museum, San Diego, CA 92112 (U.S.A.)
(Accepted 8 February 1980)
ABSTRACT
Stewart, J.G. and Myers, B., 1980. Assemblages of algae and invertebrates in southern California Phyllospadix-dominated intertidal habitats. Aq uat. Bo t., 9 : 73--94.
The assemblages of macroalgae and macroinvertebrates that coexist in intertidal Phyl- lospadix beds at seven sites in San Diego County, California, are described quantitatively. Most of the algae are attached to benthic substrates (68 of 71 species); one of the 90 re- corded invertebrates is restricted to the blades of Phyllospadix species. The composite data, considered to be characteristic of beds of both P. torreyi S. Watson and P. scouleri W. Hook. at the sites sampled, are compared qualitatively with the biota in various other adjacent and nearby habitats. With the exception of four epibiotic taxa, found only on blades of the surfgrass, the organisms are not uniquely associated with habitats where Phyllospadix plants are present. No patterns of seasonal fluctuation were evident in either species abundance or occurrences. Several ubiquitous species were consistently found in larger numbers, but most were observed infrequently.
INTRODUCTION The species f r o m 9 of the 12 genera of ma r ine f lower ing p lan t s p resen t ly
r ecogn ized (den Har tog , 1970) , including several o f the m o s t widely distri- b u t e d taxa , charac ter i s t ica l ly f o r m dense beds in quie t , shal low ~water, on m u d or sand subs t ra tes . E p i p h y t i c algae are a b u n d a n t and diverse in these s i tua t ions , whe reas few o t h e r mac roa lgae grow on subs t ra tes u n d e r the c a n o p y of blades (van den Ende and Haage, 1963; H u m m , 1964; den Haxtog, 1967; van de r Ben, 1969; den Har tog , 1970; Edwards , 1970; BaUentine and H u m m , 1975 ; Cambr idge , 1975; S hephe rd and Sprigg, 1976; L a r k u m , 1977; Lipkin , 1977) . E p i p h y t i s m on seagrass blades m a y be m u t u a l l y advan tageous u n d e r these e n v i r o n m e n t a l cond i t i ons ( H u m m , 1964; Harl in , 1975 ; Penhale , 1977) ; e p i p h y t i c d i a t o m g rowth has also been s h o w n to have e f fec t s un- favorab le to seagrasses (Sand-Jensen , 1977) . I t has been n o t e d t h a t the algal species assoc ia ted wi th seagrasses, b o t h as e p i p h y t e s and those t h a t occur on
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the substrate under the blades, are with few exceptions the same species that grow elsewhere on hard or sandy-mud surfaces, rather than being uniquely re- lated to the seagrass communi ty (den Hartog, 1967; Edwards, 1970; Ballentine and Humm, 1975; Lipkin, 1977).
Quantified data on seagrass associations are scarce for the macroinverte- brate groups included in this s tudy and comparisons are of limited use where sampling techniques differ substantially (Hooks et al., 1976; Marsh, 1976; Shepherd and Sprigg, 1976). Hooks et al. (1976) concluded that the pre- sence of a certain group of ca. 13 species was "highly predictable", but that these species are no t restricted to the seagrasses which they studied in the northeastern Gulf of Mexico. By way of comparison, Heck Jr. (1977) has con- cluded that differences in the 4 seagrass meadows he examined for inverte- brate associates were primarily due to the proximity of surrounding habitats.
Two species of Phyllospadix on the coast of California grow in habitats very different from those referred to above; they are attached to rock sur- faces in areas where surf is heavy and prevalent. Very few data are available concerning the plants and animals which coexist with these species. The ob- jective of the sampling program discussed here was to gather information that would characterize Phyllospadix-associated assemblages, firstly, to allow comparisons with other seagrass communities that have been comparably sampled elsewhere, and second, to consider whether this biota is shared with different adjacent communities, as has been concluded for other species of seagrass.
Dense beds of Phyllospadix torreyi S. Watson (1879} and P. scouleri W. Hooker (1838) (surfgrass) occupy extensive portions of the near-shore coast in southern California, from the level of mean-lower low water {MLLW = datum) into adjacent shallow subtidal areas. Even when the beds are exposed at low tide, waves frequently continue to splash over the horizontal plat- forms where beds are most common. Water movement at all times makes diving work difficult and during general surveys, both diving and wading, few epibiotic taxa are observed, leading to the possible conclusion that coexisting organisms may indeed be scarce in these habitats. The data reported here describe the relative abundances of the species of algae and invertebrates, recognizable in the field, which attach to blades of Phyllospadix species or onto the surface of the benthic substrate beneath the canopy in the low intertidal zone. Separate data for seven sites are analyzed and then combined to generally characterize intertidal Phyllospadix-associated organisms which can be observed using our sampling techniques. The assemblages are com- pared with records of organisms in nearby habitats where Phyllospadix is lacking, to test whether they are restricted to the association with Phyllo- spadix or more broadly represent the biota in surrounding areas. No data were collected in subtidal populations; observations suggest they are not markedly different. Fish data were collected concurrently from shallow- water beds adjacent to, or nearby the intertidal s tudy sites and will be re- ported separately by E.E. DeMartini.
75
The morphology and relatively sympatric distributions of PhyUospadix torreyi and P. scouleri (Sauvageau, 1890; Dudley, 1893, 1894; Chrysler, 1907; den Hartog, 1970) are similar. P. torreyi occurs in five of the seven sites from which our data were collected. In the area surrounding the two sites at La Jolla, patches of both species are found close together and may additionally be intermingled with patches of plants intermediate in vegeta- tive characters. No differences were observed, in either epiphytes or under- canopy species composit ion, between the two Phyllospadix species in this area or between data from sites where one or the other species was pre- dominant. For these reasons, PhyUospadix species are treated similarly for the purpose of this study.
Plants of both California species consist of a flattened rhizome with un- branched roots opposite an erect branch at each node, with roots and leafy branches alternating on each side. These erect branches bear leaves 0.5--4 mm wide and up to 2 m long, or flowering stems that are partially concealed by leaves. Sheathed spadices are single or clustered, and dioecious. Rhizomes branch at irregular intervals to form other rhizomes which overlie or adjoin one another to form a frequently buried mat, commonly found on hori- zontal flat rocks.
METHODS
Comparisons of algal and invertebrate species in intertidal habitats where Phyllospadix was present and where it was absent were based on the authors' previous collection records for San Diego County intertidal zones, including intensive work near the sites subsequently sampled.
General sampling design
The sampling program was designed to compare the macroalgal and macroinvertebrate species associated with intertidal platform habitats covered with uniformly dense Phyllospadix at seven sites along 14 km of rocky shoreline in San Diego County, southern California (117 ° 14' W, 32 ° 40' N). Sample data were collected at low tide during daylight hours to standardize observer accuracy, and the same observer collected each set. The nature of the areas sampled and time limitations precluded designs that rely on random-sampling techniques; quadrat locations were haphazardly located within " f ixed" s tudy sites. Presence/absence data were collected for macro- algae and some invertebrates; other invertebrates were counted.
Algal quadrat sampling Previous sampling experience has shown (J. Stewart, unpublished data;
Edwards et al., 1975) that 0.25 X 0.25 m 2 quadrats can adequately indicate presence/absence of species of multiceUular algae which grow in this and similar associations. Cumulative species lists, based on additive quadrat
76
samples made prior to the s tudy indicated that more consistent data were obtained using greater numbers of smaller-sized, replicate quadrats than with fewer 1 × 1 m 2 quadrats. A sample of ten 0.25 X 0.25 m 2 quadrats detected most algal species present at a given s tudy site on one visit.
Invertebrate quadrat sampling Individual invertebrates were counted for taxa with adults greater than ca.
5 mm in the largest dimension that could consistently be recognized in the field. Cumulative species-acquisition curves showed that 1×1 m 2 quadrats were appropriate for sampling most macroinvertebrates at a site on a given survey date, and the very low abundances made this a reasonable sample size. The number of quadrats actually censused on each visit depended on weather, surf and tide conditions. Only data from quadrats completely searched are tabulated and included in the analyses.
The abundances of several groups of invertebrates were not estimated. Presence of small taxa whose counts were unreliable, colonial forms {sponges, hydroids, bryozoans, ascidians) and boring or buried species (pholad bivalves, nemerteans, polychaetes) are denoted in Table III by an (×).
Areas and times sampled Seven sites in three areas were sampled according to the schedule shown in
Table I. In La Jolla, sites seaward from the breakwater at the Casa Pool and at the foot of Westbourne Street were sampled. In the Sunset Cliffs area
TABLE I
Sampl ing schedule , May 1977- -Apr i l 1978. N um ber s show quadra t s s amp led : I = inver te- b ra te quadra t s ; A = algal quadra t s
Month Casa West- Adair Orchard Pier Ladera Cabrillo Total per Pool bourne street month
street
I A I A I A I A I A I A I A I A
May 23 3 3 1 36 2 3 3 3 9 68 J u n e 4 13 10 4 10 4 13 12 46 Ju ly 3 13 5 13 8 26 O c t o b e r 3 3 3 4 10 4 3 14 16 N o v e m b e r 3 30 10 30 3 3 79 D e c e m b e r 3 1 3 30 7 30 7 3 6 3 21 72 J a n u a r y 4 3 4 3 F e b r u a r y 3 20 3 26 March 3 1 20 2 3 3 26 Apri l 10 30 4 13 4 53
Tota l per si te 7 45 10 35 9 90 8 116 12 60 14 31 15 38
Total quadrats sampled: I = 75; A = 415
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Adair and Orchard lie close to the base of steep cliffs with a very narrow intervening intertidal zone. A third site at Sunset Cliffs (Pier) lies just south of the Ocean Beach Pier where sloping terraces broken by tide pools and shallow channels create diverse intertidal habitats. Further toward Point Loma, a site below Ladera Street and another in the intertidal region ad- ministered by Cabrillo National Monument (Cabrillo) were selected.
Data analysis
The presence/absence algae data were converted to frequency-of-occur- rence proportions; data for counted invertebrates were expressed as numbers m-2.
Similarity and diversity indices were used to characterize groups of species to be compared with single statistics. The Bray--Curtis measure of dissimilar- ity was first applied to a mixture of frequency and meristic data (Bray and Curtis, 1957); as defined by Clifford and Stephenson (1975) it is appropriate to data on algae and invertebrates such as those studied here. Frequency-of- occurrence proportions were transformed to arc-sine values (Sokal and Rohlf, 1969) when calculating this measure for algal data. The most direct statement about species diversity is the total number of species found, shown here in Tables II and III. An index (Herrera, 1976) that assesses diver- sity of presence/absence data such as were collected for algal taxa, and the Brillouin and Shannon--Wiener indices for counted invertebrates, were calcu- lated in order to further compare and summarize the data shown in Tables II and III.
Taxonomy
Nomenclature follows that suggested in Abbott and Hollenberg, 1976 (Marine Algae of California), Light's Manual (Smith and Carlton, 1975), and Marine Shells of Southern California (McLean, 1978). The red alga, Neo- agardhiella gaudichaudii (Montagne) Abbott, is further discussed by Abbott (1978) and 3 decapod crustaceans (see Table III) are treated in Ricketts and Calvin (1968). Voucher specimens for an alga (Gymnogongrus leptophyllus (?) J.Ag.) and for unidentified sponges, hydroids, nemerteans, polychaetes, crustaceans, bryozoans and ascidians are retained in the authors' collections.
RESULTS
Epiphyte observations
Most of the species of algae found in Phyllospadix beds were attached to the hard substrates provided by rock or rhizome, or secondarily held in the shallow sediment layer accumulated and at least temporarily stabilized by Phyllospadix rhizomes, and did not grow on blades of the seagrass. Three
85
species of red algae, Erythrocladia subintegra Rosenv., Melobesia mediocris (Fosl.) Setch. & Mason, and Smithora naiadum (Anders.) Hollenb. were found only on the blades of Phyllospadix, the latter two occurring at all sites throughout the year, of ten being very abundant on blades of both species. Species of Melobesia and Erythrocladia consist of small discs of cells that might easily be unrecognized in the field wi thout careful examination of sur- faces, bu t Smithora naiadum is easily seen and was conspicuously jabsent from basiphytes other than Phyllospadix species. Other species found asso- ciated with Phyllospadix blades were actually at tached to basal discs of Smithora naiadum or on white Melobesia crusts, or were seen on old, brown blades. These included ectocarpoid species, diatoms including a large colonial form identified as Berkleya sp. (F. Round, personal communication, 1977), Colpomenia sinuosa (Roth) Derb. & Sol. (< 2 mm in diameter), Ulva sp. (< 5 mm high), Ceramium gracillimum vat. byssoideum (Harv.) Maz. and Polysiphonia simplex Hollenb, all of which are ubiquitous and of ten abundant in intertidal zones. Clumps of Laurencia subopposita (J. Ag.) Setch. fasten to Phyllospadix by encircling the blades with tight coils of tendril-like axes. ThaUi of this species also at tach to benthic substrates and thus are not restricted to epiphytic a t tachment on Phyllospadix. Coralline crusts grow on rhizomes of Phyllospadix but are infrequently observed be- cause these are usually covered with sediments. Acrosorium uncinatum (Turn.) Kyl., an epiphyte occasionally abundant on other algae under Phyllo- spadix, was absent f rom Phyllospadix blades. No differences in epiphyte growth on blades, nor in substrate-attached plants or animals were found be- tween P. torreyi and P. scouleri in the sites sampled. Of the invertebrates, only Notoacmea paleacea (Gould) was restricted to blades of both species of Ph y llospadix.
Compilation of quadrat data
Tables II and III summarize data collected from quadrats at the sites listed in Table I. The names of 68 species found in 415 0.25 × 0.25 m 2 algal quadrats are listed in Table II, and those of invertebrates from 75 1 X 1 m 2 samples are given in Table III; of these 90 taxa, 41 were molluscs.
Data were combined for taxa that could not be reliably identified in the field. Cryptopleura spp. includes C. crispa Kyl., C. corallinara (Nott) Gardn., and possibly juvenile C. violacea (J. Ag.) Kyl. Corallina officinalis var. chilen- sis (Dec.) Kiitz. undoubted ly includes some thalli that could alternatively be identified as C. pinnatifolia (Manza) Daws. Data for the mollusc, Alia carina- ta (Hinds), possibly include very rare occurrences of Mitrella aurantiaca (Dall). Algal "f i laments" comprise combinations of small, mostly filamen- tous thalli which are frequently seen in the form of mats on benthic surfaces. Centroceras clavulatum (C. Ag.) Mont., Ophidocladus simpliciusculus (Crouan & Crouan) Falk., TiffanieUa snyderae (Farl.) Abb., and Polysiphonia simplex are the more common species in this category, while less frequently
86
found axe Platysiphonia clevelandii (Faxl.) Papenf., Pogonophorella califor- nica (J. Ag.) Silva, Pterosiphonia dendroidea (Mont.) Falk., Cladophora colurnb iana Coll., Bryopsis pennatula J. Ag., Petroglossum parvum Hollenb., Chondria arcuata Hollenb. and Anisocladella pacifica Kyl.
Relative abundance
For algae, a qualitative estimate of abundance in single quadrats showed that Plocamium cartilagineum (L.) Dix., Nienburgia andersoniana (J. Ag.) Kyl. and Pterocladia capillacea (Gruel.) Born. & Thur. covered larger amounts of substrate than other species. Laurencia spectabilis Post. & Rupr. and Chondria nidifica Haxv., which covered relatively large amounts of sub- strate in occasional samples, are species with long axes that conceal very small a t tachment surfaces: Acrosorium uncinatum, an alga epiphytic on other algae, was more common in quadrats at Cabrillo and Ladera Street sites during the fall and winter. Most other species occur as few or single thalli per quadrat. Because sampling was restricted to surfaces covered with uniformly dense Phyllospadix, algae with very large thalli which would tend to occupy large amounts of space, (e.g., Egregia menziesii (Turn.) Aresch. or Sargassum muticum (Yendo) Fensh.) were not found in the quadrats sampled. A large proport ion of the substrate in individual quadrats was bare rock or sand around or over rhizomes.
Thirty-one per cent of all algal quadrats lacked any algae. The species that were subjectively estimated to be abundant in single quadrats were the species observed in the greatest number of quadrats. Acrosorium uncinatum, Nienburgia andersoniana, Plocamium cartilagineum, Pterocladia capillacea and Corallina officinalis var. chilensis were recorded in more than 50% of the quadrats at one or more of the sites. Filaments were observed in 56% of the Pier quadrats; eight other taxa were encountered in 10--50% of the quadrats at individual sites. The mean number of species seen per quadrat ranged be- tween 2.83 and 5.45. Eleven algal taxa were found only at single sites.
Among the invertebrates, Alia carinata was the only species found at all sites. Anthopleura elegantissima (Brandt), a sea anemone, and Lacuna uni- fasciata Carpenter, were each recorded from 6 sites and Notoacmea paleacea from five. The several taxa with the largest numbers of individuals were the most ubiquitous. Even when data from separate quadrats were examined, only seven species were found in numbers greater than one individual per quadrat, these being the three molluscs listed above as being most fre- quently found, Tegula eiseni Jordan and three species of crabs. Data for separate quadrats also show that in 12 quadrats, only single invertebrate species were found, two or three species were recorded in each of 34 quadrats, and in 28, four or more species were found. In one quadrat, no macroinvertebrates were found and eighteen of the 45 taxa counted were found only at single sites. Total areas covered in single quadrats by en- crusting forms, when these were observed, were rarely more than 7 cm 2 and usually less than 3 cm 2.
87
To further document the large number of species with single or few occurrences and the small number of more frequently observed species, the original data can be arranged to show that, of 51 algal species with relevant data, 25 were recorded from 9 or fewer of the 415 quadrats, while 8 species were present in more than 50 of these quadrats. For invertebrates, of 45 spe- cies, 35 were represented by 9 or fewer individuals; 2 species, Lacuna unifas- clara and Notoacmea palaecea, small molluscs, were represented by more than 50 specimens each.
Seasonal fluctuation
No definite patterns in either overall algal or invertebrate abundance were recognized in the field. The only apparent seasonal difference was the depth of the sand on rocks where Phyllospadix was attached, which varied between sites as well as with time. For example, on a November visit to the Orchard site, sand was noted as relatively deep (to 10 cm) in most quadrats. In February and March at the Adair and Orchard sites in some quadrats sand was absent from around and under rhizomes which were exposed as a mesh elevated above bare rock. Quadrats at the Orchard site in April were again heavily sanded-in.
At the Orchard site in October, November and December, and at the Adair site in December and February, very few algal thalli were observed in 80--100% of the algal quadrats. Plants were perhaps temporarily buried, or fewer erect thaUi may have been present in winter months at these sites. Throughout the year, the more common algal species were repeatedly re- corded in similar proport ions and no overall differences in presence/absence data can be related to temporal effects.
One distinct seasonal trend was observed, however, in data for inverte- brate species, in that large specimens of three species of crab, Pugettia pro- ducta (Randall) (to 10 cm across carapace), Cancer antennaris Stimpson, (to 15 cm) and Taliepus nuttallii (Randall) (to 10 cm) were conspicuous in December and January. In December, two specimens of Cancer antennaris were found in one quadrat, three Pugettia producta in two quadrats and 10 Taliepus nuttallii in four quadrats at the Cabrillo site. At the Pier site, also in December, four specimens of Pugettia producta were found in two quadrats, four Cancer antennaris in two quadrats, and three Taliepus nuttallii in two quadrats. In January, Pier site data show that a single quadrat held two Cancer antennaris, three Taliepus nuttalli, and one Pugettia producta. The only other times when any specimens of these three species were ob- served were in June, when one small Pugettia producta (2--4 cm across the carapace) was found in each of three quadrats at Casa site, and October when one small specimen of this species was seen in an Adair site quadrat.
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Between-habitat comparisons
Restriction of taxa to, or exclusion from Phyllospadix beds was assessed qualitatively by comparing records of taxa occurring in various other habitats througout the low-intertidal regions surrounding Phyllospadix- covered rocks, with lists drawn both from quadrat data and additionally from surveys of Phyllospadix outside the sampled sites. With the addition of a few rare or inconspicuous species found under Phyllospadix on the edges of channels, Tables II and III include those taxa observed by the sampling methods used, which inhabit beds of Phyllospadix throughout the study a r e a s .
To test the hypothesis that most of these taxa are not confined to Phyllo- spadix beds, data for both algae and molluscs were evaluated. Except for four species, (three red algae: Smithora naiadum, Melobesia mediocris, Ery- throcladia subintegra; one limpet, Notoacmea paleacea) none of the species in these groups were found to be restricted to an association with either or both Phyllospadix species.
With the exception of certain molluscs restricted to certain niches lacking in Phyllospadix beds and the large thaUi of several species of brown algae, the species observed in rocky habitats outside but near beds of Phyllospadix are those same species recorded from the quadrats within Phyllospadix beds. The size of individual thalli, the form of the algal assemblage and the different relative abundances of the taxa give different appearances to the rock surfaces where Phyllospadix is not the dominant taxon, but the species composit ion is similar throughout this intertidal zone.
Diversity and dissimilarity: between-site comparisons
On the basis of the Bray--Curtis dissimilarity index (B--C), Phyllospadix- covered habitats at all sites are moderately similar, with respect to the algal components (B--C = 0.33--0.68; (B--C (mean) = 0.47 +0.09), but have a greater variability with respect to invertebrate data (B--C mean) = 0.70 +0.18). The Adair site is distinctly different from other sites (B--C = 0.80--0.94), whereas the Pier and Cabrillo sites are relatively similar (B--C = 0.32).
The ratio of D/Dmax for algae, and of Brouillon's and Shannon's measures of diversity for invertebrates (H and H') , indicate that algal diversity is similar at all sites, whereas invertebrate diversity is more variable (Tables II and III).
DISCUSSION
The low intertidal zone where Phyllospadix covers rock surfaces was char- acterized as having a variable, bu t usually rich, biota (Stephenson and Stephenson, 1949) and the assemblages that are found in Phyllospadix beds
89
can be similarly described. The analyses of relative abundances of selected species at sites in this zone, strictly interpreted, have limited meaning apart from the samples they describe, but the species lists, separated from quanti- tative data, are useful for qualitative comparisons with biota in more exten- sive areas.
The similarities between sites assessed here with three diversity indices and the Bray--Curtis (B--C) measure can also be directly compared with the number of species occurring in each site. The D/Dmax ratio used to express diversity of presence/absence algal data is not the equivalent of evenness (J') derived from the Brouillon (H) or Shannon (H') indices (J' -- H'/H'max). The D index has in common with H' and H, that it provides information about spe- cies richness, but lacks an evenness component . Like H' and H, D is more sensitive to the number of species in the analysis and less sensitive to sample size i.e. the number of quadmts, in this case. Herrera (1976) tested the relia- bility of the D index by a comparison of results obtained with Shannon's H' values, and found good agreement between the two. The diversity statistics for algae (Table II) and invertebrates (Table III) can be evaluated in this con- text.
A real paucity of invertebrate species and individuals existed at three sites, Adair, Orchard and Westbourne Street, which had the lowest diversity, least evenness and the fewest species values, a fact which was evident from prior field observations. Extensive and varied mid- to high-intertidal habitats are lacking near the Orchard and Adair sites but surround other sites, including Westbourne Street. The Orchard site somewhat resembles Westbourne Street (B--C = 0.48) in species composit ion and abundance but the Adair site does not (B--C = 0.93). Using combined data from these three sites it was found that Notoacmea paleacea, Lacuna unifasciata, Alia carinata and Pagurus sp. accounted for 163 of the 199 invertebrates counted. With regard to inverte- brates, the greatest diversity and evenness, the largest number of species and countable invertebrates and the largest sample size (number of quadrats) all coincide at the Cabrillo site, which lies within a National Monument park, where human activities are regulated. Of the 163 individuals counted here, 47 were Notoacmea paleacea, 11 were Anthopleura elegantissima, 11 were Tegula eiseni, and 27 were crabs, which accounted for 96 specimens; the other 18 species were present in total numbers of less than 11. The Pier site most closely resembles Cabrillo in terms of B--C dissimilarity (0.32), number of species and diversity and evenness values. Species which occurred at both the Cabrillo and Pier sites were less abundant at the Pier site, whereas many species found at one or both of these sites were not recorded elsewhere. An effect similar to that of National Park protect ion may be seen near the Pier site for Phyllospadix-dominated habitats (although not for upper-intertidal regions), where surge channels separate these lower habitats from the rocky terraces above. These channels are mostly too deep to wade and too broad to be easily jumped except at very low tide with minimal surf.
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The differences found in invertebrate data collected at different sites are possibly, in part, a consequence of the different sample sizes at each site; they are probably, to some extent, a reflection of the population structure of the many "infrequently-observed" species, too. Pielou (1974) has stated that: "Estimates of the proportional amounts of the rarer species .will usually have large sampling errors and are likely to be unreliable". Furthermore, part of the variability in invertebrate data among sites can hypothetically be ascribed to such differences as accessibility to human activity and the extent and richness of adjacent habitats and associated biota.
Algal data were found to be far more similar between all sampled sites than data for invertebrates. Similar D/Dmax and B--C values indicate that a moderate degree of species richness, homogenei ty of samples, and similarity in species composi t ion is shared by all sites.
Four species were found attached only directly to green, apparently healthy Phyllospadix blades, while ca. 10 secondary epiphytes were infre- quently observed on bases of algal thaUi on the blades or on brown blades. There were 13 epiphytes recorded for Phyllospadix in Abbot t and Hollen- berg (1976). The apparent restriction of two of the algae, Melobesia medio- cris and Erythrocladia subintegra, to Phyllospadix may be a reflection of the incompleteness of the present data. The latter species has been reported as common on other algae in seagrass communities on the Texas coast (Ed- wards, 1970) and melobesioid species are taxonomically confusing and wide- ly distributed on many algal basiphytes. Smithora naiadum has been grown on artificial substrates (Harlin, 1973) and also grows on Zostera marina L. (Hus, 1902). Since extensive laboratory examination of blades of Phyllo- spadix was not a part of this study, it is probable that inconspicuous algal species, in addition to the larger taxa we record, grow on surfgrass.
Among invertebrates, only Notoacmea paleacea, a limpet, is confined to Phyllospadix blades. A report of finding juveniles of this mollusc on Halidrys dioica Gardn. and Corallina spp. (Bishop and Bishop, 1973) requires con- firmation, in view of the difficulty of distinguishing between juvenile limpets of several similar species.
Two previous studies have involved plants and animals associated with Phyllospadix species. Harlin (1971, 1973) studied the relationships between Smithora naiadum and the two species (Zostera marina and P. scouleri) on which it grows at San Juan Island, Washington. Near La Jolla, California, Bishop and Bishop (1973) removed intact masses of P. torreyi from three rocky intertidal rocks and separated out all molluscs. Lacuna unifasciata and Notoacmea paleacea accounted for more than 93% of the specimens re- covered. Tricolia rubrilineata (Strong), Alia (as Mitrella) carinata and Litto- rina scutulata Gould, were each found in proport ions of about 2.0%. The Lacuna and "Mitrella" species were also found on Z. marina in other locali- ties nearby. Tricolia rubrilineata and Littorina scutulata do not appear in the present data. Specimens of T. rubrilineata were less than 5 mm in size and therefore excluded by the sampling technique used, and although L. scutu-
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lata is common in pools in the mid-intertidal zone above the beds of Phyllo- spadix near the Pier site, it was not seen in the quadrats sampled.
A visit to the lower-intertidal region near La Jolla (November 1 9 4 7 - January 1948) by Stephenson and Stephenson (1972) produced a list of animals considered characteristic of this zone, including two species (in ad- dition to Haliotis spp., today rare everywhere in southern California inter- tidal regions) not found in this survey of Phyllospadix beds. These two spe- cies, Anthopleura artemisia (Pickering in Dana) and Linckia columbiae Gray, do not at present inhabit the intertidal in southern California (Allen, 1976). Of the low-intertidal "Cryp to fauna" listed separately by Stephenson and Stephenson (1972), only Crepipatella (as Crepidula) lingulata (Gould), a gastropod that attaches to hard non-buried surfaces, is absent from the Phyllospadix assemblage described here.
The three species of boring clam recorded at our sites where broken sub- strate revealed their presence, are perhaps more common than the data show. Coan (1964) and Turner (1955) refer to Platydon cancellatus (Conrad) and Penitella penita (Conrad), respectively, as common species. Parapholas cali- fornica (Conrad) is described as the most common borer at Monterey (Haderlie et al., 1974). "Nestling species" (see Evans, 1967) are found in holes drilled originally by PeniteUa penita and include Diplodontus orbellus (Gould), Cumingia californica Conrad, and Semele rupicola Dall, at the Phyllospadix sites studied here.
No quantified estimates of abundances are available for the two algal epi- phytes commonly found on species of Phyllospadix. Both Melobesia medio- cris and Smithora naiadum are abundant on blades of bo th surfgrass species at some localities but , at other times or within different areas of the beds, are of ten less frequent or rare; no consistent qualitative differences in occur- rences were recognized. The few epiphytic taxa recorded in this s tudy con- trast with published comments about other seagrass associations which hold great numbers of epiphytic taxa. For example, 90--183 species were found on Posidonia oceanica (L.) Delile in the Mediterranean (van der Ben, 1969; Edwards et al., 1975), over 100 species on Posidonia australis Hook. f. and Zostera capricorni Aschers. in Australia (Larkum, 1977), 113 on Thalassia testudinum Banks ex KSnig (Humm, 1964), and 66 species on four species of seagrass in the Gulf of Mexico (Ballentine and Humm, 1975). Several authors (e.g. Lipkin, 1977, for Cymodocea nodosa (Ucria) Aschers.) have re- marked on the relative abundance and ubiqui ty of encrusting taxa and their utilization by other algae for secondary at tachment, observations applicable to Phyllospadix epiphytes.
Of the two algal species common on Phyllospadix, Melobesia mediocris represents a taxon of ten cited by other workers as either restricted to, or most common on, a variety of seagrasses, whereas Smithora naiadum is re- corded only for species of Zostera and Phyllospadix. The Phyllospadix com- muni ty differs from other seagrasses in the low number of epiphytes, the large number of species of benthic-attached algae and in the physical factors
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present in the environment, but resembles other marine flowering plants in that the associated algae and invertebrates are representative of the biota in the surrounding area. The canopy of Phyllospadix blades provides protection from excessive light, temperature and desiccation during emergence for species on the rock substrates that are not otherwise found exposed habitats. The exposure of epiphytes on blade surfaces to these same physical conditions, in addition to the high-intensity water movement present in Phyllospadix habitats when the beds are submerged may be factors affecting the successful attachment and growth of algae on Phyllospadix blades.
The possibility that blade width might be correlated with the number of attached organisms was considered in this study. Many of the species of sea- grass characterized as bearing abundant epiphytes have blades 5 mm or more in width; blades of Halodule wrightii Aschers. and Syringodiurn filiforrne Kiitz. are as narrow as blades of Phyllospadix species. Ballentine and Humm (1975) include these two species in their study describing numerous and abundant epiphytes in seagrass beds. In St. Croix, Virgin Islands, neither spe- cies has abundant epiphytes (I.A. Abbott, personal communication, 1979).
The data on invertebrates reported here were collected by examining the blades, the exposed stems and rhizomes, and the surfaces of the rock or sand substrate during low tides when the beds are uncovered by water. Kikuchi and P~r~s {1977) summarize and compare animal data from studies of sea- grass communities and attempt some generalized conclusions. Most of the lists they discuss resulted from diving surveys or laboratory studies of col- lected material and include microfauna, swimming or very mobile animals and infauna, groups excluded by our methods.
ACKNOWLEDGEMENTS
We thank the National Park Service for cooperation with the portion of the study conducted within Cabrillo National Monument. Ecologists in the U.S. Army Corps of Engineers, Los Angeles District Office, recognized the need for information concerning Phyllospadix beds in southern California and supported the work described here. We are grateful to E.E. DeMartini for advice on analytic procedures.
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