Polychaete Abundance Patterns in a Marine Soft-Sediment Environment: The Importance of Biological Interactions Author(s): Sarah Ann Woodin Reviewed

work(s): Source: Ecological Monographs, Vol. 44, No. 2 (Spring, 1974), pp. 171-187 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1942310 . Accessed: 21/12/2011 17:12
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Ecologiac Al'Monog0.raphIs

(1 974 ) 44: 17 1-I 87

POLYCHAETE ABUNDANCE PATTERNS IN A MARINE SOFT-SEDIMENT ENVIRONMENT: THE IMPORTANCE OF BIOLOGICAL INTERACTIONS'
SARAH ANN WOODIN2

Departmientof Zoology, Uniiversity Washinglton, of Seattle, Washhigtoni 98105 Abstract. Samples of infauna and measurementsof temperature,oxygen, salinity,and algal cover were taken from January 1969 to December 1970 at -1.2-ft tidal elevation in a mud flat dominated by polychaetes in Mitchell Bay, San Juan Island, Washington. Mortality of adults afterspawning and variable larval settlement success probably explained much of the variation in population numbers of the four large and numerically important polychaete species, Lumbrineris ilflata, Ariot/lc/la rutbrocinicta, Platynereisbicanialiculata,and A i-mandia brel' is. No correlations were found between the abundances of numericallyimportantspecies and physical factors. Exclosures constructed of 3-mm mesh plastic screening placed on the flat became covered with diatoms. Settlingjuveniles of tube-buildingspecies, such as P. bicanaliculata, Axiothella rubrocincta,and L. inflata, built tubes in this layer of diatoms and thus did not reach the enclosed sediment, while settlingjuveniles of a burrowing species, Armandia brevis, burrowed throughthe diatom layer and reached the sediment. Thus, cleaning the cage surfaces or removing the cage aftersettlementreduced abundances of tube-buildingspecies without disturbingthe sedimentsince adults of all three numerically importanttube builders experience mortalityafter spawning. The manipulation of tube-builder abundances showed that the burrowing species responded to space vacated by tube builders by increased settlementsuccess. Results from experimental variation of A. br-ei'is numbers per unit volume of sediment in the laboratory and abundance data from unmanipulated natural areas also demonstrated the presence of interspecificand intraspecific competitionfor space. Changes in physical factorsdue to algal cover had some impact on population levels but the competitiveinteractionsand behavior patterns,revealed only by observations on the behavior of living organisms and manipulation of the infauLna, demonstrated the importance of biological interactionsto the determinationof species abundance patternsin a soft-sediment environment. Key wortls: Competitioi;
interlactions, biological; polychacte; soft-sedimnent; space.

In general marine benthicecologists have not separated two importantquestions: which species of can those available forsettlement toleratethe physical extremes of an environmentand what determines which of these species exist in an environment.The firstquestion is concerned with physical tolerance limits and life styles. For example, a soft-sediment organismis an unlikely inhabitant a rock face. The of work reportedhere evaluates a portionof the second question,i.e., how important physicalfactorsand biological interactionsare as determinantsof species abundance patternswithin one habitat, an intertidal soft-sediment environment. Physical variables fluctuatewith greateramplitude in the intertidalthan in the borderingsubtidal, thus subjecting organismsinhabiting intertidal the environments to greater physical stress. Research in both typesof marine soft-sediment environments has produced descriptions the fauna and flora and characof

terizationof the physical variables (Thorson 1957). With littleor no biological information available on life-styles species interactions, varietyof matheor a matical techniques have been used in an attemptto explain patterns of species distributionand abundance. The resultantcorrelationsprovide only weak inferencesand do not necessarilyexpose the causal relationships. However, much effort has been directed toward explaining species distributionand abundance patterns using correlations with easily measured physical factors, such as sediment grain size distribution. Depending upon its life style, an organism may require a given size range of sedimentfor tube building, burrowing,or feeding (Wieser 1959). In an analogous manner an organism inhabitinga rocky intertidal region may require a horizontalor vertical surface,crevices,or tide pool. As Levins (1968) explains, a determination such as the requiredsediment range represents only a portion of the fitnesscurve for that organismand that parameter. It may be the optimalportionphysicallybut such a characterization 1 ReceivedMarch 5, 1973; acceptedAugust16, 1973. 2 than the questions: (1) what Current address: Department Zoology,University alone is less interesting of determinesthe boundaries of an organism's realized of Maryland, College Park,Maryland20742.
INTRODUCTION

171

172

SARAH ANN WOODIN

Fcologicail Monograplh% Vol. 44, No. 2

sWh 4.. ....*__.^'O

the showing -1.2-ft area on MitchellBay. San JuanIsland,Washington, of FIG. 1. Aerial photograph study (A) and -1.7-ft(B) stations.

behavior (Reish and Alosi 1968, substrate sive territorial to relative itspotential distribution substrate can and Vahl 1970), organisms tolerate the and distribution (2) whatdetermines organism's Ockelmann of greater thantheextremes thephysical fluctuations these boundaries. within abundance are (Newell 1970), andpredators known can The sameargument be madeformostphysical environment Wherethe tolerance to affectpopulationdynamics(Trevallionet al. of properties an environment. in such as tem- 1970). As Dayton (1971) has demonstrated the variable, physical limits a particular for interthat the rockyintertidal, hypothesis biological the for have beendetermined an organism, perature, the does are to has realized distribution been found be actions important nothaveas a corollary organism's factors.Boththe unimportance physical of distributionrelative than its potential muchmorerestricted for of properties thesubstrate, and (Newell 1970). Thus,theim- biological physical to relative thisfactor larvalsettlement (Wilbiological example, important during are factor and/or of physical portance another son 1968,Gray 1966). is process indicated. on yieldresults and of Conventional sampling techniques patterns organThe distribution abundance imbut zone are notde- population fluctuations not on the relative intertidal ismsinhabiting rocky the of stress. portance biologicaland physical to determinants tolerance physical solelyby their of termined is Connell(1961), Paine (1966), Dayton(1971), and species abundancepatterns.Manipulation both to a that and others have shownexperimentally thebiological morepromising moredifficulttechnique use The substrateis playa signifi- in soft-sediment environments. and of processes competition predation and layeringmust beforethe use of experimental three-dimensional the sediment cant role. However, mustbe disintertidal was notbe disturbed if it is, thecontrol zone or, the techniques rocky manipulative in manner.Infaunal are environ- turbed a replicate organisms as as poorlyunderstood the soft-sediment to observed often and impossible map. Unless rarely ment(for example, Lewis 1964). de- a verylargearea is used, an experiment cannotbe maybe equallyimportant processes Biological in of terminants such patterns the marinesoft-sedi- subsampled. is but environment theevidence lessconvincing. Despite the anticipatedtechnical problems it ment of an appropriate undertake examination a to species (Vas- seemed occur between Sharpareal boundaries manipuexperimental et community using sallo 1969,Sanders al. 1962), speciesshowaggres- soft-sediment

Spring 1974

POLYCHAETE

ABUNDANCE

PATTERNS

173

lation. Crustaceans,polychaetes,and bivalves usually dominate infaunal assemblages and are therefore the mostusefulorganisms experimental for study. Among these,numerousinfaunalcrustaceansand polychaetes are relatively short-livedwhile bivalves are often long-lived(Thorson 1957). In addition polychaetes are intermediate in size and represent an aurea mediocritasfor the investigator between the crustaceans, whose small size makes taxonomy difficult, and the largerbivalves,where sample size becomes a problem. Since polychaetesare short-lived, recolonization of a disturbedarea can be expected withina reasonable time. Also, the polychaete portionof the infauna often encompasses a number of species belonging to a varietyof life styles and trophic levels (Jones 1961). This work reportsdata on the physicalvariables of a mud flat and on the polychaete inhabitants. The descriptivefindingsare interpretedin the light of manipulationof polychaeteabundances, observations on living individuals, life cycles of the component species, and abundances of infauna.
STUDY AREA

The flatis located in MitchellBay on the northwest cornerof San JuanIsland, Washington. The extreme tidal range is approximately13 ft from +10 to -3 ft (0.0 ft = MLLW) (U. S. Coast and Geodetic Survey Tide Tables 1971).3 The main study areas were at -1.2-ft and -1.7-ft tidal elevation (Fig. 1). They were chosen because of the number of polychaete species and their dominance. The numerically importantpolychaete families were Syllidae, Nereidae, Lumbrineridae, Maldanidae, and Opheliidae.
MATERIALS AND METHODS

Tidal heightwas establishedfrom high tide mark to -2.0 ftwith a transit. A transectline divided into was laid down fromhigh tide mark to 10-m intervals -1.8 ft, a distance of approximately70 m. At the -1.2-ft study area a 70-m line perpendicularto the transectwas mapped and each meterwas assigned a numberfrom one to seventy. Numbers from one to seventy were then drawn from a random number table and used to choose sites where samples of infauna were taken every other monthfromJanuary 1969 to December 1970. Samples were not taken seasonally at the -1.7-ft station. Sedimentgrain size was determinedfor 14-cm deep cores in June 1969, October 1969, and November 1969 using the standard dry sieve and pipettetechnique (Krumbein and Pettijohn 1938). Mean grain size and sorting (a measure of deviation from the mean in phi units) were calculated accordingto Inman (1952). withU.S. are givenin feetto conform 3Tidal heights Tide Tables. Coast and GeodeticSurvey

Temperature and P02 were determinedin situ in areas with and withoutalgal cover in 2-cm deep increments to 16 cm. Measurements were taken at four stages in the tidal cycle: as the area was uncovered, at the time of extreme low water, just before the area was covered, and with SCUBA at high tide. Depending upon availabilityof equipmentthermistor or mercurythermometers graduated to 10 C were used to measure temperature. The thicknessof the algae, i.e. the numberof layers,was noted if present, and measurementswere taken from areas with and without algae. The pO. was determinedwith Radiometer oxygen electrodes attached to a Beckman or Radiometer gas analyzer and calibrated with water-saturated known gas mixtures. Surface water samples were obtained using a glass syringe,a stopcock filled with glass wool, and a probe. The glass wool did not cause aeration once it was wet; it prevented contaminationby sedimentwhich fouled the electrode membrane. In-sediment water samples were originallyobtained with a syringe,a stopcock, and a 12-cm graduated probe, but in contrast to Brafield (1964) surface water contaminationwas a major problem, compounded by small pore size of the surface sediment,capillary action, and contamination by sediment. This method, therefore,was abandoned and the electrode was placed directly into the sediment (Jansson 1967). were of Samples of waterfordetermination salinity taken in plastic syringesat different depths fromthe sediment surface in a variety of pool sizes during tidal exposure. The samples were analyzed in the laboratoryusing a milliosmometer. Algal cover was monitoredby photographing three random areas at each stationeveryothermonthfrom June 1969 to June 1971. Samples of algae for taxonomic purposes were taken at these sites. For samplingthe benthicfauna, a galvanized steel frame 0.05 m2 by 14 cm deep was pressed into the mud and the enclosed volume was collected eitheras a whole or in 2-cm deep layers. In eithercase it was fixed in formaldehydesolution bufferedwith hexaand methylenetetramine dilutedwithsea waterto 4%. After fixation the sample was sieved through a 1.0-mm and a 0.5-mm sieve and the retained fractions were stained with rose bengal and sorted under a dissectingmicroscope. If algae were present,they were removed prior to the sieving process so that samples with algae would not retain small organisms to a greaterextentthan samples withoutalgae. Before sorting,some samples were passed through a modified flotationprocess using a saturated sucrose solution in a 20-cm column. In all cases the entire fractionretainedby the sieve was sorted. The fixed organisms retained by the sieve were counted and

174
TABLE

SARAH ANN WOODIN

Ecological Monographs Vol. 44, No. 2

1. Abundanceof polychaete infaunarelativeto sievesize within 0.05 m2 samplefrom one -1.2-fttidal elevation February13, 1969 on Sievesize Species 1.0mm 125 39 11 11 5 1 7 18 8 8 3 0 3 3 0.5 mm 426 55 12 12 9 1 8 19 9 22 8 6 3 12

Exogonelourei Lumbrineris inflata Axiothella rubrocincia Platynereis bicanaliculata Armnandia vis bre Nereisvexillosa Scolelepis fuliginosa Naineris dendritica Eupolynirilheterobranchia Ophiodrontus pugettensis Harmothoe imbricata Cirratulus cirratus Capitellacapitata Syllisheteroclaeta

FIG.2. Photograph thethree of cage types:topless, sideless, complete. and 1.0-mm sieve (Table 1). Onlythedata forApril7, 1969,are from 0.5-mm a sieve. Replicability between 0.05-m2 14-cm by deep samples (a minimum 5 m apart)was goodenough of that one sampleadequately represented least the nuat merically dominant members the polychaete of portionof theinfauna (Table 2). The measure simiof larity used was Kendall'scoefficient association, of of is Taib. The use and significance thisstatistic discussedin Looman and Campbell(1960) and Nichols ( 1970). Cages were used to exclude predators, retaina knownnumber predators, of prevent settlement of certainpolychaetes, and increasealgal abundance. Theywereconstructed 3-mm of meshplastic screening attached braidednyloncord to frames by made fromdishpans cutting the bottom by out and sides and topflange (Fig. 2). Each corner thecage was of attached a stainless steelclip or a length nylon by of cordto a 0.5-mdoweldriven themud. The final into in situcage dimensions were28 cm by 34 cm by 12 cm highwiththeedge of thecage penetrating cm 2 intothemud. Unlessalgal or diatomcoverwas desired, cage surfaces werecleanedapproximately two to four times each month.After 6, or 9 months 4, the sediment within cage was sampledas described the above.
PHYSICAL FACTORS AND ALGAL COVER

identified. Only heads and whole organisms were counted. Identification polychaetespecies was based priof marilyon the keys of Berkeleyand Berkeley (1948, 1952) and Banse and Hobson (unpublished). Additional references used were Pettibone (1953), Ushakov (1955), Day (1967), Hartman (1968 and 1969) and Kozloff and Lambert (1969). First a 0.5-mm sieve then a 1.0-mmsieve was used since the majorityof the sediment is retained by a 0.5-mm sieve but not by a 1.0-mmsieve, while 12 of the 13 species and 41 % of the total polychaetenumbers retained by a 0.5-mm sieve are retained by a

TABLE

2. Replicate0.05 m2samples from-1.2-fttidal elevation April7, 1969a Species Sample Sample 1 2 622 52 59 33 43 2 0 6 5 5 5 0 0 1 3 0 9 1 August11, 1969' Sample Sample 1 2 208 14 37 1 15 2 2 2 1 3 12 1 0 1 2 1 0
1

Exogonelourei 661 Lumbrineris 46 inflata Axiothella rubrocincta 50 bicanalicuPlatynereis lata 28 Armandia brevis 38 Nereisvexillosa 3 0 Scolelepisfuliginosa 4 Nainerisdendritica Ih'teroEupolymnia 4 branchia Op/hiodromus pugettensis7 inmbricata 4 Hartnothloi Sphaerosyllis pirifera 23 4 Capitellacapitata 1 Dorvillearudolphi 1 Phyllodoce maculata 0 Glycera capitata 1 Syllisheterochaeta 0 Cirratulus cirratus
b ab = 0.795; P > 0.999. Tab = 0.741; P > 0.999.

263 33 49 3 12 1 2 2 0 5 15 6 2 1 1 0 0 0

The slope of theflatwas 70 fromhightidemark to +1.0-ft,2? from +1.0-ftto -1.2-ft, and 1? from -1.2-ft -1.7-ft to tidalelevation. The sediment distribution the-1.2-ft size at station is presented Table 3. Presumably to the fine in due size grain and thuslargecapillary force thesurface of smallpools of waterranging diameter sediments, in from1 cm to I m and in depthfrom cm to 8 cm 0.1 remained thesurface theflat on of from 1.0 to -1.7 + ftduring tides.Due to this low surface water and the waterretained thesediments, by infauna notexdid

Spring 1974

POLYCHAETE ABUNDANCE PATTERNS

175

surface
water

A.
0

B. 0~~~~~~~~~~~~~0

A4_s

C.
A

8-

xsurfaceDE.F N'2 water A9 DA. sr

Qr)
6) 8

o
10 41

{2

f
0
0

A.

waterk 16

~ ~A A

~~emeatr

-?

6810
FIG.

14

18

~~~ ~~~ 26 ~~~~~~~~~22

(0C) Temperature

~43012

16

2'0

24

2, 1970; B and E-June 20, 1970; C and F-July 19, 1970). the -1.2 and -1.7-ft stations (A and D-Feb. Measurements were made as the tide exposed the area (circles), at the time of extreme low water (squares), and just before the area was covered with water (triangles).

algal cover(closed symbols)at with temperatures algal cover (open symbols)and without 3. Sediment

perience desiccation. Sediment temperaturesvaried with tidal height,weather,time of exposure, season, sedimentdepth,and algal cover. Surface water and surface sediment,as expected, layers maximalvariationswhilethe sediment exhibited protecteddeeper levels (Fig. 3). This is in accord with the findingsof Johnson (1965) and Pamatmat (1968). The duration of tidal exposure and the weather stronglyinfluenced the sediment temperatures; for example, during the wintermonths when were below those of the overlying air temperatures sea water at high tide, surface sedimentreadings approximated air temperaturesduring tidal exposure. In addition,the presenceof algal cover providedsome insulationin the summeras is documentedin Fig. 3. in Sea watertemperatures 2 m or more of water at temperatures high tide and extremesurface-sediment during tidal exposure for months when samples of infaunawere taken were maximal in April to August and minimalin October to February (Table 4). of Oxygen determinations surface water samples and directelectrode immersionrevealed oxygen tensions fromgreaterthan saturationduring the day to less than 20 mm Hg during the night. During day-

light,bubbles with tensionsgreaterthan 400 mm Hg were observedboth at hightide and duringperiods of tidal exposure on diatom and large algal surfaces. Thus, oxygen tensionsof surface water seemed to be and photosynaffectedby algal respiratory strongly thetic demands. Sediments below 2-5 mm had no oxygen. This usually coincided with the top of the black layer. water duringtidal The salinityof surface-sediment The salinityof exposure ranged from 28%, to W6Yo the overlying water ranged from 30% to 34%. Sanders et al. (1965) and Johnson(1967) demonstrated elsewhere that although surface water varied in salinitythe sediment salinityremained stable unless the changes were of long duration. Algal cover is both a physical and a biological factor in the sense that it is a biological entitybut its presence changes the physical propertiesof the sediment. Its presence reduces the depth of the oxygenated sedimentlayerso thatthe anoxic layer beginsimbeneaththe algae. Algal cover also insulates mediately the sediment,but in addition it increases the availabilityof food both to herbivoresand deposit feeders (Khailov and Burlakova 1969).

176
TABLE

SARAH ANN WOODIN

-12
ft statin . I

Ecological Monographs Vol. 44, No. 2

3. Summary of sediment grain size analysis: mean grain size, sorting,and percentage by weight per grain size category, sediment from -1.2-ft tidal elevation June 27, 1969 October November 17, 1969 14, 1969 49.9 5.4 4.9 5.6 7.9 9.9 8.7 6.9 0.8 3.29 41.4 16.0 5.2 6.4 7.4 9.3 8.8 4.4 1.0 1.24 mm 3.13
20

Pebble (4.0 to 64.0 mm) Gravel (2.0 to 4.0 mm) Very coarse sand (1.0 to 2.0 mm) Coarse sand (0.5 to 1.0 mm) Medium sand (0.25 to 0.5 mm) Fine sand (0.125 to 0.25 mm) Very fine sand (0.0625 to 0.125 mm) Silt (0.0039 to 0.0625 mm) Clay (< 0.0039 mm) Mean grain size Sorting (phi units)

34.8 8.5 8.9 13.0 11.0 10.9 8.2 4.0 0.7 3.03

60
J F N D JF M A M J A S 0N D JF M A M J

F A S ---969

N D

F -

M A

M J J 97 -

0-

M A M -D----17

1.21 mm 1.21 mm

FIG. 4. Percent algal coverat -1.2-ftand -1.7-ft tidal elevation.Mean and rangeare presented.

As Fig. 4 illustrates, algal cover varied seasonally at both the -1.2-ft and -1.7-ft stations,and the seasonal variationin algal cover was similarfor the two stations. Three genera were involved: Ulva, Monostroma, and Enteromorpha. All were temporaryin that few attachment sites were available and most of the algae were not fastenedto a solid object but floating in the water. The amount of attached algae was increased by the behavior of two nereid polychaete species, Platynereisbicanaliculata and Nereis vexillosa. Individualsof all sizes actively"caught" floating algae with theirjaws, pulled the piece down, and attached it to theirtube openings. Depending upon the growth and size of the algal piece relative to the appetiteof thenereid,the algae mightshow noticeable growth(Roe 1971). Over 80% of the attachedalgae was fastened to such tubes. During winter storms algal clumps and theirassociated fauna were washed
TABLE

out of the intertidalzone; thus, some animals were lost in thismanner. Massive mortalityof polychaetes was never observed either during or after very cold (minimal surface-sediment temperature +30 C) or veryhot of (maximal surface-sediment temperatureof +28.4? C) or very rainy periods that coincided with tidal exposure,exceptfor one species thatwill be discussed later. Whetheror not polychaetes are as successful in withstanding physical stressas the lack of obvious mortality would indicatecannot be answeredsince no measurements reproductiveoutput were made. of
SAMPLING DATA

Life history ormation inf In terms of species number, samples of benthic macrofauna (organismsretainedby a 1.0 mm sieve) fromthe -1.2-ft stationare dominatedby polychaete annelids,while the most numerousspecies is a tanaid, Leptochelia savignyi(Table 5). As Table 5 illustrates, three polychaetes (Exogone lourei, Lumbrineris inflata, and Axiothella rubrocincta) are numerically important throughout year while two polychaetes the (Platynereisbicanaliculata and Armandia brevis) are numerically important except duringperiods of adult mortalityafter spawning, when prior to settlement theirpopulation levels are low (e.g. June and August 1969 and June 1970). Three are herbivoresand eat primarilygreen algae, and two are deposit feeders (Table 6). Exogone lourei adults are less than 1 cm long and 1 mm wide, while adults of the other four species are much larger. The majorityof the infaunal crustaceans and bivalves are not discussed but their abundances in seasonal samples and experimental areas are available fromthe author.

4. Extreme sea water (during high tide) and surface-sediment(during low tide) temperaturesat -1.2-ft tidal elevation Temperatures (? C) Date Sea water 6.2 8.5 9.5 11.2 15.0 7.5 6.0 7.2 8.5 13.5 13.8 Sediment 3.0 4.5 9.5 26.0 25.5 7.5 6.0 6.8 23.0 28.0 28.4

January 1969 February 1969 April 1969 June 1969 August 1969 October 1969 December 1969 February 1970 April 1970 June 1970 August 1970

Spring 1974 TABLE

POLYCHAETE 5.

ABUNDANCE

PATTERNS

177

Abundances of infauna at -1.2-ft tidal elevation: January 1969 to December 1970, 0.05 m2 samples 1969 1970 A 0 D / F A J A 575 45 52 133 44 5 7 1 0 18 6 0 0 3 0 5 0 3 N 484 92 158 313 52 1 11 1 2 18 14 0 2 9 17 11 0 0 D 877 168 123 358 47 6 17 18 19 15 4 0 1 22 6 6 10 5 Mean no./m; 8842 1465 1702 2190 720 38 253 177 75 295 130 12 40 175 202 113 60 67 26680 1070 4300

Species Polychaetes Exogone lourei Lumbrinerisinflata Axiothella rubrocincta Platynereisbicanaliculata Armandia brevis Nereis vexillosa Scolelepis fulginosa Naineris dendritica Eupolyninia lieterobranchli Ophiodrornuspugettensis Hlartnothoeimbricata Glycera capitata Phyllodoce maculata Capitella capitata Syllis hieterochaeta Doritillea rudolphi Cirratulus cirratus Sphaerosyllispirifera Tanaid Leptochelia satiggnyi Bivalves" Miscellany')

129 125 661 603 263 663 211 303 57 39 46 91 33 135 37 104 32 11 50 127 49 158 49 79 9 3 72 143 69 30 11 28 5 38 1 12 55 99 77 3 1 0 1 3 1 3 2 1 2 37 12 18 7 0 20 2 5 6 25 0 2 4 29 18 1 4 1 2 0 8 4 3 5 15 16 16 8 7 22 1 5 7 4 3 4 14 15 1 1 2 2 0 1 0 0 2 8 2 4 1 0 1 3 2 5 8 19 4 4 3 19 9 3 1 41 0 22 0 21 8 1 5 2 1 0 1 14 9 5 1 8 0 0 0 0 0 23 6 0 0 0 7 0 520 18 87 519 45 56 365 63 165

639 433 45 33 104 79 165 8 29 8 1 1 12 7 1 0 2 3 19 24 1 4 0 1 1 0 2 9 1 1 10 5 2 1 6 13 1321 942 49 42 193 172

1421 3381 2203 33 242 84 369 94 436

Data for April 1969 were excluded from this calculation Abundances of species are available from the author.

since a ().5 1mmsieve was used on that datc.

Leptochelia savignyi,Exogone lourei, Lumbrineris inflata, Axiothella rubrocincta,and Platynereis bicanaliculata build tubes thatopen onto the surfaceor into the oxygenatedsedimentlayers. The burrower, Arinandiabrevis,does not build a tube but individuals are normallyfound within3 cm of the sedimentsur-

of face (Table 6). Depth distributions the six numerically importantspecies are shown in Table 7. Most of the individualsfound below 6 cm may have been pushed down by the sampler frame. The vast majorityof the polychaetesoccur within4 cm of the sedimentsurface.

TABLE

6.

Life stylesof the dominant polychaete species Trophic level" Reproductive type Broods its young on ventral surface Nov.-Feb. Comments Builds a tube; often in the top 2 cm of sedimentor in the oxygenated layer surrounding larger organisms' tubes

Species

Exogone lourei Berkeleyand Berkeley Herbivore (Syllidae) Lumbrinerisinflata Moore (Lumbrineridae) Axiothella rubrocincta (Johnson) (Maldanidae) Platynereisbicanaliculata (Baird) (Nereidae.) Herbivore

Builds temporarytube with Lays egg masses attached to undersides of rocks and shells surface opening throughoutthe year Builds permanenttube with surface opening Builds permanenttube with surface opening; shows territorialityand "gardening" behavior

Deposit feeder Reproductive method not occurs known; settlement throughoutthe year Herbivore Discrete synchronousspawns with peaks June-Sept.; planktonic development withsettlementafter 3 to 4 weeks; (Roe 1971)

is Armandia brev (Moore) (Opheliidae)

Does not build a tube; burrows Deposit feeder Free spawn Apr.-Nov.; planktonicdevelopment with in top 3 cm of sediment settlementafter3 to 4 weeks; may have 2 or 3 generations per summer (Hermans 1964 and 1966)

a Determinedby gut contentsand observationson livingorganisms.

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TABLE

SARAH ANN WOODIN

Ecological

Monographs Vol. 44, No. 2

7. Abundances of numerically important species on April 7, 1969 (A), August 11, 1969 (B), December 7, 1969 (C), and April 22, 1970 (D) in 0.05 m2 samples analyzed in 2-cm deep incrementsat -1.2-ft tidal elevation Surface to 2 cm 2 cm to 4 cm
67

4 cm to 6 cm
23

6 cm to 8 cm
6

8 cm to 10 cm
2

1O cm to 12 cm 0 0 0 0 0 0 2 2 0 0 1 0 0 0 0 0 0 0 0 0 4
0 8

12 cm to 14 cm
4

Total
661

ExogoeI

lourei

B C D

551

201 209 600 16 16 37 25 22 18 49 82 21 3 143 150 21 12 27

99

62 2 16 13 17 0 7 9 31 0 16 6 0 0 14 9 0
0

0 0 17 6 0 0 0 7 0 0 2 0 0 0 1 7 0 0 3 0 13
0

0 0 1 5 0 0 4 2 0 0 1 1 0 0 0 0 0 0 1 0 5
0

0 0 1 3 0 0 6 5 0 0 1 0 0 0 0 1 0 0 1 0 5
0

0 0 4 3 0 0 1 3 0 0 1 0 0 0 0 0 0 0 0 0 3
0

263 211 639 46 33 37 45 50 49 49 104 28 3 143 165 38 12

99

Luinbrinerisinflatk

A B C D A B C D A B C D A B D
C

Axiotllal rubrocincta

Platynereis hicanaliculata

Arnmandia brevis

29 519 365 1321

Leptochelia savignyi

B C D

462 358 1170

52 7 121

No data available for April 1969.

Natural history information the six numerically for dominantspecies was used to design the manipulation experimentsand to interpretthe abundance data. Due to the small size of Exogone lourei (adults are less than 1 cm long and 1 mm wide) many were not retainedby a 1.0-mmsieve. Thus the abundance patterns of E. lourei in natural and manipulated areas will not be discussed. A bundance levels The abundances of the four numerically important and large polychaete species (Lumbrineris intlata, A xiothellarubrocincta, Platynereis bicanaliculata,and Armnandia brevis) are quite variable throughoutthe year (Fig. 5). One hypothesis explain the consistencyof replito cate values in space is that the causes of the population fluctuationsfor each species occur uniformly or in patch sizes of less than 0.05 m2 at -1.2-ft tidal elevation. Given adequate settlement the imporby tant species this result is not surprisingsince most physical fluctuationsoccur relative to tidal height changes, and random physical events, such as damage by logs on rocky shores (Dayton 1971), are not common on mud flats. alternative is A more attractive hypothesis thatrandom events do occur but are unimportant relativeto non-randomeffects. Since Platynereisbicanaliculata extends its tube up into the algae and herbivorous

divingducks are present,at least some P. bicanaliculata individuals are eaten with the algae by such ducks and presumablythis is a random event at a given tidal height. A major non-randomevent that may account for a large percentage of the seasonal variation is reproduction,patch size for this event being less than 0.05 M2. All four species experience mortality afterspawning. Spawning in P. bicanaliculata and Armandia brevis populations occurs within discrete periods. Armandia brevis begins spawning in April and continues to November with settlement 3-4 weeks after each spawning. The juveniles attain reproductive in maturity one and one-halfmonthsand then spawn and die (Hermans 1966). The events are relatively synchronouswithin a population. Marked fluctuations in A. brevis abundance, then, should be expected fromApril to November or December due to adults afterspawning,folmortality overwintered of lowed by settlement, maturation, spawning,and death of two or three new generationsof A. brevis. Such were found (Fig. 5). This does not exfluctuations plain why A. brevis abundance was so much greater in December 1969-February 1970 than in January 1969-February 1969 and December 1970. Nor does it explain the reduction in A. brevis numbers from December 1969 to April 1970 (Fig. 5). Platynereisbicanaliculata die after spawning, and the expected population fluctuationsdue to adult

Spring 1974
200 -

POLYCIIAFTE

ABUND)AN(C
TA3L.Lu

IA'I-PATERNS

179

|VA
_

coefficorrelation 8. Pearson prodUct-nmoment with aLbundances temperaof cients seasonalpolychaete

tLv-eand algal cover

| 100

Species
00 0

Surface- Percent sediment algal Sea water temperature'coverb temperatiure'

+ 0.247 - 0.363 -- 0.0)27
-

Exog.le
B

LI

114i .

I{<1I~1

I'llObrilcris

A .siohtllo

lourei u iolta
ribroilatl

+ 0.458 - 0.276 + 0.258

+ 0.018
10. 9.

+ 0.176
- 0.334 - 0.291

li/aloao A r odlido
JanILMI-a C

hreli.s

0.306 -0.450

.__ .... -. .. .........--------

0.367

- 0.219
-

0.256

1969 to AuLgIlst 1970; N Juc 1969 to December 1970; N P >0.10 tot- all valueILsof r.

300-

to conditionsonlthe mud flatthat were not measured

-

or to conditions in the plankton.

2200

100

rm

such as the population n-uch of the seasonal variation, fluctuations of A. brevisand P. hicanaliculata during

Reproductiveevents,then,can be used to explain

10. . 0 1 L . 0I _
0

the summer,and they probably mask the effectsof random events. Fluctuations that cannot be exevents are the decline in A. plained by reproductive berevisnumbersfrom December 1969 to April 1970, the decline in P. iicanaliculata numbers from Decemiber 1969 to February 1970 and theirsubsequent increase in April 1970 (Fig. 5). Samplingvariability, of course, is another possibility.
Correlation (ofspecies abundance with other species and with physital factors

J 1969

F D 0 DATES SAMPLE

A J 1'70

Abundances of the five dominant polychaete species were examined for correlationwith physicalfacsam-1.2-ftstation.Values fordates on whichreplicate tors found to fluctuateseasonally, i.e., seasonal exare ples weresorted givenas meanswithranges. surface sea temperatures, tremesof surface-sediment (Table 4), and percentalgal cover watertemperatures were observed from (Fig. 4). No significant and juvenile settlement mortality were found (Tacorrelations June to early November (Fig. 5). This does not ex- ble 8). plain the low population numbers in February 1970 Summerlow tides duringhot sunnyweather,howand the subsequent high population level in April ever, do contributeto mortality especially of surface 1970 (Fig. 5). Since P. bicanalicnlata adultsare quite organisms, such as Ophiodlrola us pugettensis-a polysedentary,immigrationis not a serious possibility chaete that spends a large proportion of its time of unless due to shifting algal clumps containingP. crawlingon the surface and often is not in the sedibicanaliculata by tidal action. In addition,this interpretationdoes not explain why the January1969 and stress thermal on December 1969 population levels are so much lower TABILL 9. Individuals surfaceshowing temperatures on JUIly 19, 1970 whenSUrface-sediment 1970 abundances (Fig. 5). than the December reached 28.40 C Both Lunribrineris inflate and Axiothella rubthrocincta reproduce throughoutthe year; variations in Comment Species their abundances may be due to more successful withsurpllgvettteu.sis$ Many dead; number Ophlio(droto)illls periods of settlementor more larvae available for peelingoff face epidermis due to the participationof more adults in Armtandia settlement on Two dead; individuals surb1)er is spawningor increased survivalof larvae (Fig. 5). It escape behaviora face showing was apparentlymore suc- Piityttercis is not clear why settlement on surface showing and P. LAmrintle//ls ,,caltalicullt Individuals cessful some years than others for A. brievis escape behaviora rbtiflat ta la AxitheOtl rulbrocilc tal bicanaliculata (Fig. 5). The increase or decrease in other time dUring low tides SLttC behavior was not seen at success of all four species may be related exccpt wshen a prctlator was present.any settlement

of FIG. 5. Abundances Lumnihrineris iflatal (A) thella rubrocincta (B), Platyiiereis bicbal(Ilicul(It(I (C), and Armandia breies (D) fromJan. 1969 to Dec. 1970 at

Axio-

180
TABLE

SARAH ANN WOODIN

Ecological

Vol. 44, No. 2

Monographs

10. Pearson product-moment correlation coefficientsof infaunal albundances from January 1969 to December 1970 and the significanceof the correlation coefficients

L. vsaviiiivi Leptoclelia SO i'igy Exogoile lourei Lumhri/ieris itIflata A-xioti/llarbtbroc inctti Plbtaviiereis bicaiiablicidlbtia: Arnaclidia hre'i~s
* *

E. lourei +0.618

L. jiuflaita +0.648 +0.578

A. ruhroti-bwta P. hicoooiliclo1ta A. brevis +0.916 +0.668 +0.710 n.s. +0.821 +0.493 +0.550 +0.524 n.s. +0.175 +0.099 +0.282 +0.206 +0.466

n.s.

n.s.

n.s.

n.s.

0.1 > P > 0.o5. 11.05> P > 1.0(11. n.s. P> 0.1. ;I Abundances of L. savigtiyi were only available N =8.

for January 1969, AuLguIst 1969. Deceoiber

1969, and April 1970 to December

1970;

mentbut only under the algae duringlow tides. For example, on July 19, 1970, mortalityattributedto heat stressdid occur (Table 9). Such mortality has been observedin the fieldonly when surface-sediment temperaturesexceeded 270 C. Laboratory experimentswith0. pugettensis observedunder a dissecting microscope in sea water in heated watch glasses confirmed that temperaturesin excess of 27? C are lethal. Thus, the insulationprovided by algal cover (Fig. 3) could affect0. pugettensissurvival during hot periods of tidal exposure. Since mostwormsotherthan 0. pugettensis not are on the surfaceduringlow tide,and since the sediment providesan excellent insulatinglayer (Fig. 3), mortalitydue to thermalstresswas rarely observed presumably because the temperature the deeper sediof mentlevels rarelyexceeded infaunaltolerance limits. 0. pugettensis the only species for which mortality is was observed more than once. Other species, however, do experience thermal stress, if not mortality (Table 9) even thoughtheirseasonal abundances do not correlatewith seasonal temperatures (Table 8). Abundances of the same five species were examined for correlation with one another by Pearson product-moment correlationcoefficients (Table 10). Positive significant nearly significant correlations or were found between all species except Armandia brevis (Table 10). Since the reproductivecycles of Exogone lourei, Lumbrinerisinflata, Axiothella rubicanaliculatadiffer(Table and Platynereis brocincta, cannot be explained on thatbasis. 6), the correlations All four species are tube dwellers while A. brevisthe one uncorrelatedspecies-is a burrower (Table 6). Fhe numericallydominant tanaid, Leptochelia savignyi, is a tube dweller and its abundances are positively correlated with three of the four tubedwelling polychaetes but not with the burrower (Table 10).

The year to year changes may possiblybe due to poor success or poor survival of larvae in the settlement plankton for some unknown reason. The seasonal changes in population levels of the five dominant with seapolychaetes do not correlate significantly and algal cover (Table sonal changes in temperature polychaete species show 8). All four tube-dwelling correlations or positive significant nearly significant of theirseasonal abundances, and the abundances of three of these species correlate positivelywith those tanaid (Table 10). The burrowof the tube-dwelling ing species' abundances do not correlatesignificantly with the tube builders' abundances. Conditions that favor one tube dweller, then, seem to favor all five such species, but do not affectthe burrowereither positivelyor negatively. The data do not indicate what these conditionsare.
EXPERIMENTAL MANIPULATION

Introductionto tile hypothesisthatspace is limiting The tube-building activities of polychaetes and to tanaids give structure the upper 4 cm of sediment. The tubes intertwine and often the majorityof the surfacesedimentseems to be composed of tube structures and fecal pellets. Since the animals require access to the surfaceforfood (e.g. green algae) and/or of fullutilization surfacespace oxygen,the apparently that surface space is by tubes suggeststhe hypothesis species and a limiting resourceboth for tube-building burrowingspecies. Tube-buildingspecies in general need at least one tube extensionto the surface; thus, theirneed for surface space is continuous over time species need acif the tube is permanent. Burrowing cess to the surface and/or the shallow oxygenated The hypothesis layer beneath it only intermittently. further predictsthatif the abundance of tube builders decreases, the sedimentvolume available for burrowing will increase thus increasingease of access to the surface layers. With this increase in space availabilSummaryof sampling information ity, more burrowingindividuals should occur. One The majorityof the seasonal changes in the abun- means of testingthis hypothesisis to remove all or the dance levels of the four large dominant polychaetes some of the tube builderswithoutdisturbing sediremoves theirtubes since unin can be interpreted terms of reproductiveevents. ment. This effectively

Spring 1974

POLYCHAETE

ABUNDANCE
TABLE

PATTERNS

181

occupied tubes were found to degrade withinseveral days. However, no method of removingtube builders withoutdisturbing sedimenthas been reported the previously. Manipulation of abundances of infauna In the field, the surfaces of enclosures (Fig. 2) became covered with diatoms almost immediately. The larvae of Armandia brevis,a burrowingspecies, responded to this layer as a sedimentlayer and burrowed through thustheyreached the enclosed sediit; ment. Larvae of tube-building species, such as Platynereis bicanaliculata, also reacted to the diatom growthas a sedimentlayer and built tubes in it; thus theydid not reach the enclosed sedimentbelow. The abundances of tube-buildingspecies, then, can be reduced by placing cages in the field prior to periods of settlement the larvae of tube-building by species. Given variable diatom growthon the cage surfaces, the reductionin the abundance of tube-building species should be directly related to the amount of diatom cover. If the hypothesisis correct that burrowingspecies are competingwith tube-building species for access to the surface sediment,one should find an increase in the volume or numbers of the burrowing species with reduction of tube-building species abundance or volume. Since thesepolychaetes are relatively sedentary, one would not expect to observe immigration rathera response in the form but of either increased settlementsuccess or increased growth or both. Obviously the response is not restricted the burrowing to species, since already settled tube-building species are presentand can respond by growthto the increase in available space. Among the tube builders, Platynereis bicanaliculata is the easiest one to manipulate since its major spawning period is in August and is quite discrete, and settlementis usually completed by the end of October. The other large, numerically important polychaete tube builders, Lumbrineris inflata and Axiothella rubrocincta, reproduce throughout the year. Armandia brevis, the numerically important finishessettlement November and thus burrower, in has larvae available to respond to increased space vacated by P. bicanaliculata adults, which die after spawning. The space is not filled by P. bicanaliculata juveniles as theyare kept out by the presence of cages. The first experimentalcages were placed at the -1.2-ft stationin August 1970, and the enclosed sedimentwas sampled in November and December 1970. The four month interval encompassed the major spawningand settlement periods of P. bicanaliculata and A. brevisbut only a fractionof the reproductive periodsof L. inflataand A. rubrocincta. As Table 1 I shows, P. bicanaliculata abundances were reduced

11. Abundancesof three tube-building species and one burrowing species within 0.05 m2caged and uncagedareas at -1.2-fttidal elevation after4 months
Tube-buildingspecies
L. inflata A. rubro- P. bicanacincta liculata Total

Burrowing species
A. brevis

Without cage With cage

*168 92 168 132 113 64 -0.098a

n.s.

123 158 136 153 141 104 -0.089a

n.s.

358 313 47 25 19 54
-0.974a *

649 563 351 310 273 222 -0.920 t

**

47 52 143 160 129 139

n.s. P > 0.05. **0.01 >P>0.00l. a Correlationwith A. brevis abundance; Pearson product-moment correlationcoefficient.
***

0.001 > P.

due to the presence of cages (settled individualswere found on the cage surfaces), while as predicted by the hypothesisthat space is limiting, the abundance of the burrowingspecies was increased. A possible complication,the fillingof the vacated space by increased growthof organismsenclosed initially, such as L. inflataand A. rubrocincta adults,apparently did not occur. The correlationof the total abundance of L. inflata,A. rubrocincta, and P. bicanaliculata with the abundance of A. brevis is highlysignificantby Pearson product-momentcorrelation (0.01 > P > 0.001), and 85% of the variance in A. brevis abundance is explained by the relationshipbetween tube builder and A. brevisdensity. To test the hypothesisfurther, cages were maintained at the -1.7-ft stationfor six monthsfromAusucgust 1970 to January1971 so thatthe settlement cess of Lumbrineris inflataand Axiothellarubrocincta would be reduced as well as that of Platynereisbicanaliculata. Since all three species experience morsuctalityafterspawning,with decreased settlement cess the population abundances are reduced. Due to the longer time, however, the possibilityof growth effects by already settled individuals is increased. since both L. inflata and A. rubroUnfortunately, cincta fragmenteasily during fixation, no volume measurementswere made. A gradient in settlement success of L. inflata and A. rubrocinctawas found forthesefiveexperimental areas, while the abundance of P. bicanaliculata,settledover a much shortertime, was reduced in all areas. The diatom cover varied over the 6-mo period,thusthe larvae of L. inflataand A. rubrocinctathatsettledover the entire6 mo were exposed to a wide varietyof diatom cover, while the larvae of P. bicanaliculata that settled over a much shorter period were not (e.g. Fig. 6). If the hypothesis of space limitation correct,the abundance of A. is brevis should follow the gradientof increasingspace

182

SARAH ANN WOODIN

Ecological Monographs Vol. 44, No. 2

10.~~~~~~~~~~~~~~~~~~'

FIG

Photographs

of

c'ige surfa.es

ifter

three

months

(A,

C,

and

E)

and

four

months

(B,

D,

and

F).

FIG.

6. Photographs cage surfaces of after threemonths(A, C, and E) and fourmonths D, and F). (B. not sampled for 5 mo after removal of the cages (August 1971 to April 1972) at the -1.2-ft station showed the same result (Table 13). The correlation coefficient is significant (0.025 > P> 0.01), and 79'/ of the variation in A. brevis abundance is explained by the relationshipbetween A. brevis and tube-builder density. The abundance of the burrowing species,Armandia

availability,i.e., the reverseof the gradientof abundance of tube-building species. As Table 12 shows, this is the case. This correlationof number of A. brevis with total numbersof the three tube-huilding species is significant (0.05 > P > 0.025), explaining 70% of the variationin A. breviis abundancc. Another long-term experimentin which the cages were maintainedfor four monthsbut the .areas were

Spring 1974 TABLE

POLYCHAETE

ABUNDANCE
TABLE

PATTERNS

183

12. Abundancesof three tube-building species and one burrowing specieswithin0.05 m2caged and uncagedareas at -1.7-ft tidalelevation after months 6
Tube-buildingspecies
L. inflata A. rubro- P. bicanacincta liculata Total

14. Seasonal variationsin the abundances of threetube-building species and a burrowing species, tidalelevation 0.05 m' samplesat -1.2-ft
Tube-building species Date L. inflata 135 37 104 38 A. rubro- P. bicanaLincta liculata 158 49 79 93 72 143 69 160 Total 365 229 252 291 Burrowing species A. brevis 55 99 77 49

Burrowing species
A. brevis

Withoutcage
With cage

309
263 163 171 60 -0.712 n.s.
t

65
37 54 20

101
12 23 24 20 -0.403a n.s.

475
312 240 215

45
49 41 39 101

October 1969 December 1969 February 1970 April 1970a

148

159
88

86

8
-0.766t

a Mean of two replicates.

n.s.

-0.8341 *

n.s. P> t).05. *0.05 > P >0.025. Correlationof tube-building species abundances in caged areas with A. brevis abundances; Pearson product-moment correlation coefficients.

Laboratory experiments An obvious corollaryof the hypothesis thatspace is limiting that therewill be intraspecific is competition for space. To test this in the laboratory,measured individualsof Armandia brevis were introducedinto containersof sediment. The sedimenthad been collected a maximum of 2 days previously from the -1.2-ft station; the grain size was less than 1.0 mm. A. brevis numbers declined due to the inabilityof some individualsto maintain themselvesin the sediment. These appeared on the sedimentsurfacewithin the initial3 days. In all six experiments stabilization of the population levels occurred withinthree days, afterwhich therewas no further reduction in numbers even after48 days. The data indicatea constant relationship betweenthe volume of the sedimentand the final total volume of A. brevis specimens (Table 15). Individual A. brevis,therefore, affectother A. brevis negatively, and given a volume of sediment,a certainabundance of A. brevisof a given size can be maintainedwithinit. In nature,the volume of sediment available to A. brevis is determinedby the abundances of tube builders (Tables 11, 12, and 13) whose tubes remove sedimentfromthe volume available for burrowing. Several attemptswere made to controlthe possibility food limitationof A. brevis of abundance using the same experimentaldesign but with sterile sediment. A. brevis, however, will not burrow into such sediment; thus, food cannot be completelyeliminatedas a limitingfactor, although of 15. Relationship Arinandia breviisvolumeto in sediment volumein containers the laboratory
Final mean A. brei's no. A. brevis

brevis,responds to the abundances of all threelarge tube-building polychaete species. The form of the response varies temporally. Armandia brevis abundances fluctuatefromlate April to November due to reproductive events (Fig. 5 and Table 6). In November the final settlementoccurs, and if larvae and space are available, settlementsuccess should be good. Thus, in the fall the responseto available space is in the form of settlement success or failure. Armandia breviscan respond only to vacated space between November and April by growth. If competitionfor space increasesbetweenNovember and April due to increased growthof tube-building species or due to increasingL. inflataand A. rubrocinctaabundances (P. bicanaliculata settlement does not occur duringthis time), A. brevis numbersshould decline due to mortality emigrationof its settledindividor uals. A population decline of this type apparently occurredfromDecember 1969 to April 1970 (Fig. 5 and Table 14). As was mentionedearlier,thisdecline can not be interpreted termsof reproductive in events.
TABLE

13. Abundancesof three tube-building species and one burrowing 0.05 rrn specieswithin caged areas at -1.2-ft tidalelevation after months 9 (cage was pres4 entonlyduring first months) the
Tube-buildingspecies Burrowing species
Total 357 310 234 209 129 A. brevis 90 73 152 125 175 A. rubrocincta 174 133 109 71 40 P. bicanalicualata 46 36 34 9 21

TABL-E

L. inflata 137 141 91 129 68

Total

Sediment
volume

individual
A. brevis

volume
volume

(cm)

initialfinal 10 10 4 4 4 4 5 4 1 1 1 1

volume(cm3) 0.17 0.16 0.16 0.16 0.16 0.16

sediment 0.004 0.005 0.004 0.004 0.004 0.004

-0.947 t
*

-0.7931 o n.s.

-0.503a
n.s.

-0.890;

correlationcoefficients.

*).01 > P >0.005. * 0.025 > P > 0.t 1. n.s. P >0.05. t Correlationwith A. brevis abundance; Pearson prodtuct-moroent

228.9 121.5 42.9 42.9 42.9 42.9

184
TABLE

SARAH ANN WOODIN

TABLE

Ecological Monographs Vol. 44, No. 2

16. Axiothella rubrocincta abundancerelative to areas maintained percentalgal cover in manipulated fromAugust 1970 to January1971 at -1.7-ft tidal elevation Manipulation type A. rubrocincta no./ 0.05 m' sample 157 138 65 15
10

by of 18. Estimates thearea defended Platynereis tidalelevation at bicanaliculata -1.2-ft

April 1969 April 1970 June 1970 cm 8 cm2 cm2 December 1970 1.7 cm 358 520 cm2 500 cm2 length)2,r.

Algae removed Control: natural algal cover Algae added"

Topless and sideless cages that retained algae.

Mean P. bicanaliculata length P. bicanaliculata abundance Estimates of area defended, Area available (P. bicanaliculata

3.5 2.3 cm 2.2 cm 28 165 67 cm2 445 cm2 49 500 cm2 500 cm2 500

abundance)(0.4

mean P. bicanaliculata

given the rapidityof the response and the size of the sedimentvolume, it seems unlikelyto be one. Algal cover Animals that cannot survive anaerobically must possess eithera tube openingon the surfaceor access to the oxygenated-surface layers. When algal cover is present,the situation is more complex since the animals mustthen extendtheirtubes or access routes up throughseveral layers of algae. Most polychaetes do, but Axiothella rubrocinctadoes not and is incapable of emigration;thus, individualsof A. rubrocincta musteitherbe able to withstand anoxia or die. Comparison of data from topless and sideless cages that retained algae and from areas that were kept clear of algae shows that A. rubrocinctaabundances are negativelyaffectedby the continued presence of algae, presumablydue to an inabilityto withstand anoxia and the failure to move and/or to extend its tube up through the algae (Table 16). No obvious relationship exists between seasonal abundances of A. rubrocincta and percentalgal cover (Table 8). The majorityof the algae is loose; so, the relationshipmay be masked by the variabilityof the algal cover (Fig. 4).

(Table 16), and the presence of algae can prevent access. Nereid "gardening" behavior influencesthe permanenceof the algal cover; thusthe physicaleffect is biologicallymediated.
PREDATION AND CANNIBALISM

No estimate of fish predation was made because were observed only three times in over 150 flatfish hours of diving, no evidence of siphon predation eitherin theformof evasive feedingbehavior(Hughes (Trevallion et al. 1970) 1969) or siphonregeneration was found in the bivalve population,and the only fish consistently seen on the flat was a cottid,Oligocottus maculosus, which ate copepods as it followed the incomingtide edge (Table 17). Bird predationwas observed but only on one species, Clinocardium nuttalli,a surface bivalve. Both ravens and gulls ate thisspecies by pickingindividuals off the surface at low tide and cracking their shells by droppingthemonto rocks. Gulls also occasionally ate individualsof Nereis vexillosa,which is active just beforethe mud flat is covered by water. Herbivorous ducks were frequentlyseen diving in the bay, and along with pieces of green algae they probably consumed various infaunal species, in particular those that build permanenttubes in the algae, e.g. Platyof nereisbicanaliculata. The activity such birdscould in part account for the patchinessof the algal cover. Fewer than ten shorebirdswere seen on the flat. Summaryof manipulation data peregrina,a Roe ( 1971) showed thatParanemertes Tables I I to 15 show the importanceof space and predatory nemertean, ate Platynereis bicanaliculata the effect tube buildingon the accessibility sedi- and accounted in part forthe reductionin P. bicanaliof of mentvolume to burrowing species. Access to the sur- culata abundances after settlement. However, P. for face is important at least one tube dweller as well peregrinadoes not account entirely thisreduction for since individualsof P. bicanaliculataare lost to diving ducks and stormswhen theirtubes are in the algae. TABLE 17. Diet of Oligocottus ilnculosuIs as determined In addition,P. bicanaliculata is aggressive(Reish and byfecalpelletanalysis Alosi 1968). Observationsmade both in the laboratory and field showed that P. bicanaliculata defends Frequency of prey type in diet No. of the area in frontof its tube. It feeds in this area, No. P. food Other which has a radius one-thirdto one-half its body of hicanaL. crustaorganisms Copefish counted liculata pods ceans inflata length. It will attack and eat other P. bicanaliculata 21 665 (0.98 0.02 0.002 0.0 that trespass within this territory. 2(0 1574 0.91 0.09 0.001 0.001 Calculationsof P. bicanaliculatasize and abundance 28 3455 0.94 0.06 ().001 0.0 23 (December 1970) and in 1963 show that aftersettlement 0.96 0).03 0.001 0.0 22 1711 0.99 0.0 0.0 ().(I the spring before spawning mortalityand after a

Spring 1974 TABLE

POLYCHAETE

ABUNDANCE
TABLE

PATTERNS

185

19. Mortalityof Nereis i'exillosa juveniles in containers with and withoutPlatynereis bicanaliculata and Ophiodromnus pugettensisadults

20. Infaunal abundances in 0.05 m2 caged areas with and withoutCancer magisterat -1.2-ft tidal elevation after4 months With 140 43 27 lII 597 113 141 Without 531 64 104 737 132 153 949 168 136

Density of Nereis vexillosa juveniles Controls" A Day 1 Day 19 B 500 500 151 223 With 5 P. hicanaliculata C D 500 0 500 500 0 0 With 5 0. pugettensi.s

Tube-building species: Exogone lourei Lumbrinerisinflata Axiothella rubrocincta

(2 P. bicanaliculata added to A) Day 24 1 179

'13 Setigerindividuals; just settling.
b

Leptochelia savignyi Burrowingspecies: Armandia brevis

bicanaliculata 2 Platynerei~s
112

2619 1736 2010 3163 129 139 160

19

54

25

47

143

organisms common obviouslywould favor burrowing organisms. This leads at the expense of tube-building periodof growth(April 1970), the areas theoretically to the predictionthat in areas where C. magisteris defended by the populations are close to those en- abundant, the infaunal communityshould be domiclosed by the sample (Table 18). With spawning nated by burrowingorganisms rather than by the superior tube builders. and severe winterstorm damage and per- competitively mortality haps poor settlement initially etc., the abundances are GENERAL DISCUSSION reduced so that the areas defended are much less thanthe area available (April 1969), as is trueduring large important The abundances of the numerically the spawning season before settlement has occurred polychaete species (Lumbrineris inflata, Axiothella but afterreproductive bicanaliculata,and Armandia mortality Platynereis (June 1970) (Table rubrocincta, 18). brevis) were foundto be quite variable (Fig. 5). The in The area defendedby P. bicanaliculata was calcu- majorityof the fluctuationscould be interpreted after events,such as mortality lated by multiplying bicanaliculata abundance by termsof reproductive P. the area of a circle whose radius was taken to be 0.4 spawning and differences in settlement success. times the mean body length,since the radius of the Abundance levels of thesespecies and Exogone lourei withpercentalgal cover circle P. bicanaliculata defends ranges from 0.33 to did not correlatesignificantly water of (Fig. 4) or with temperatures the overlying 0.5 timesthe body lengthof the individual. This is a crude estimatebecause the defended zone really has or the sedimentsurface (Tables 4 and 8). Abundances of the four numerically important threedimensions not two. polychaetes (Exogone lourei, LumbriPolychaetesare important predatorson otherpoly- tube-building chaetes as well. If juvenile Nereis vexillosaare placed neris inflata,Axiothella rubrocincta,and Platynereis in a dish with approximately cm of sedimentand bicanaliculata) did correlate positively with one 0.5 allowed to build tubes, and then adult Platynereis another (P < 0.01; Table 10). The abundance of tanaidLeptochelia savignyi, important bicanaliculata and/or Ophiodromus pugettensisare thenumerically correlatedwiththreeof all introduced, the N. vexillosa are eaten. Their setae a tube builder,was positively polychaetes. The abundances of appear in the feces of P. bicanaliculata and 0. puget- these tube-building burrowing polychaete,Artensis. Numerous N. vexillosa in identical dishes the numericallyimportant withoutP. bicanaliculata and/or 0. pugettensissur- mandia brevis, did not correlate with those of the vive althoughthey experience mortality(Table 19). species (Table 10). If no other data tube-building The cause of thismortality may be cannibalismof the were available, a possible hypothesismight be that of type described above for P. bicanaliculata since Roe conditions(the characteristics which are unknown) that favor one tube-buildingspecies favor all such (1971) has observedit forN. vexillosa. Although the crab Cancer magisteris rarely seen species but do not affect burrowingspecies either on the flat,it is an important or predatoron species with positively negatively. A corollaryis that the abuntubes thatopen onto the surface. A small C. magister dances of tube builders affectone anotheronly posiintroduced itselfinto an experimental cage in Septem- tivelyand do not affectthe abundances of burrowing ber afterthe cage had been in position one monthat species (Table 10). The way tube-buildingspecies the -1.2-ft station. When the cage was sampled in affect one another could be a synergisticphysical November, the abundances of tube-dwellingspecies effecton the sedimentfor example. This impliesthat had been greatlyreduced while the abundance of the competition for limiting resources,such as space and between tube builders or tube burrowing species, Armandia brevis,was no different food, is not important than in the control caged areas withoutC. magister builders and burrowers. Observations on one tube-buildingspecies, Platy(Table 20). The presence of C. magisterif it were
Dishes without P. bicanaliculata or 0. pugettensis initially.

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Ecological Monographs Vol. 44, No. 2

nereis bicanaliculata, revealed the presence of strong intraspecific competitionfor surface space in which P. bicanaliculata feeds (Table 18). In addition, experimentalmanipulationof the abundances of three tube-building polychaetes(Lunihibrineris inflata,A xiothellarubrocincta, P. bicanaliculata)demonstrated and that their total abundance negatively affected the abundance of the burrowing species,Armandia brevis (Tables 11 to 13). The expected resultof correlation analysis in light of these data would have been a negativecorrelation the seasonal abundances of the of tube-building species with that of the burrowingspecies. This result was not found (Table 10). One possibility thattemporalevents (probably primarily is reproductive)mask the relationship.An obvious implicationis thatone should interpret such correlations very cautiouslywhen no other data are available. The experimental results(Tables 1I to 13), laboratorystudies (Table 15) and abundance data (Tables 14 and 18) demonstratethe presence of biological interactions, including interspecific and intraspecific competitionfor space. These data show that such are important biological interactions determinants of polychaete infaunal species abundance patterns in soft-sediment environments.Additionalscatteredevidence of biological interactions existsin the literature, such as sharp areal boundaries between species (for example, Sanders et al. 1962), between deposit-feeding and suspension-feeding organisms (Rhoads and Young 1970) and the spacing of Tellina tenuis, a bivalve, to avoid siphon overlap (Holme 1950). The significance the experimental of manipulations of natural populations is that such evidence is much stronger than correlative evidence and may contradict the facile conclusions of correlations. Further,they demonstratethe population effects which observations on small numbersof animals do not. Physical factorsare also important (Tables 9 and 16) but perhaps not as important biological interactions. as None of the species discussed are confined to the intertidal (Hartman 1968 and Lie 1968). Thus, one would expect to findsuch interactions deeper softin sedimentenvironments well. My observationson as P. bicanaliculata in subtidal areas, for example, revealed the same intraspecific aggressivebehavior seen in the intertidal.Since the amplitude of the fluctuations of physical factors is greater in the intertidal than in the bordering subtidal,one would predictthat would be even more important biological interactions in the subtidal. In 1968 and 1969 Sanders proposed the stabilitytimehypothesis explain patternsof diversity the to in soft-sediment marine benthos. He demonstrateda for infaunal polychaetes and bipatternof diversity valves from soft-sediment environments with boreal shallow water and estuarine assemblages having low

values, and tropicalshallow water and deepdiversity values (Sanders sea assemblageshavinghighdiversity 1968). The formerassemblages were called physically controlledand the latter"biologicallyaccommodated." If the polychaeteand bivalve data presented in Table 5 are analyzed accordingto Sanders' rarefaction technique (Sanders 1968, Fager 1972 contains a critical evaluation of this method), the values fall withinthose given by Sanders (1968 and 1969) for boreal shallow water assemblages i.e., physically controlledcommunities. Physical factorswere demonstratedto have some impact on population levels data (Tables I I to (Table 16), but the experimental 13 and 15) and abundance data (Tables 14 and 18) the presentedin thiswork demonstrate importanceof of to biological interactions the determination species abundance patternswithinone habitat, an intertidal marine environment. soft-sediment
ACKNOWLEDGMENTS

and the I wish to thankmy fellowgraduatestudents of facultyof the Departmentof Zoology, University whichconfor discussions Washington, manystimulating to of tributed the development my ideas. Particular thanksare due to Alan J. Kohn whose encouragement, were ever presand criticism moral support constructive ent,to RobertT. Paine who spentmanyhoursdiscussing the problemwithme and to Karl Banse who read my of of The facilities the University Washingdissertation. made availton FridayHarborLaboratories werekindly able by the Director,Robert L. Fernald. Carl F. Nyof blade and Pamela Roe helpedin collection fielddata. H. Karl Banse and Frederic Nichols aided in polychaete who thanks due to myparents are Finally, identification. without for and refuge the weary, troutfishing provided whichthiswork would not have been completed.This an workwas supported partby an NDEA fellowship, in of and fellowship, the University WashNSF predoctoral NSF GrantNo. GB-20978. ington
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Fager, E. W. 1972. Diversity: a sampling study. Am. Nat. 106:293-3 10. Gray, J. S. 1966. The attractive factor of intertidal sands to Protodrilus symbioticus. J. Mar. Biol. Assoc. U. K. 46:627-645. Hartman, 0. 1968. Atlas of the errantiate polychaetous annelids from California. Univ. Southern California Press, Los Angeles. 828 p. 1969. Atlas of the sedentariata polychaetous annelids from California. Univ. Southern California Press, Los Angeles. 812 p. Hermans, C. 0. 1964. The reproductive and developmental biology of the opheliid polychaete, Armandia brevis (Moore). Masters Thesis. Univ. Washington, Seattle. 131 p. 1966. The natural historyand larval anatomy of Armandia brevis (Polychaeta: Opheliidae). Ph.D. Thesis. Univ. Washington,Seattle. 175 p. Holme, N. A. 1950. Population dispersion in Tellina tenuis DaCosta. J. Mar. Biol. Assoc. U. K. 29:267280. Hughes, R. N. 1969. A study of feeding in Scrobicularia plana. J. Mar. Biol. Assoc. U. K. 49:805-823. Inman, D. L. 1952. Measures for describing the size distributionof sediments. J. Sediment. Petrol. 22(3): 125-145. Jansson,B. 0. 1967. The availability of oxygen for the interstitial fauna of sandy beaches. J. Exp. Mar. Biol. Ecol. 1:122-143. Johnson,R. G. 1965. Temperature variation in the infaunal environmentof a sand flat. Limnol. Oceanogr. 10:114-120. 1967. Salinity of interstitial water in a sandy beach. Ibid. 12:1-7. Jones, M. L. 1961. A quantitative evaluation of the benthic fauna off Point Richmond, California. Univ. Calif. Publ. Zool. 67:219-320. Khailov, K. M., and Z. P. Burlakova. 1969. Release of dissolved organic matter by marine sea weeds and distribution theirtotal organic production to inshore of communities. Limnol. Oceanogr. 14:521-527. Kozloff, E., and G. Lambert. 1969. Key to the polychaete species. In Marine Fauna of the San Juan Archipelago. Friday Harbor Laboratories, Friday Harbor, Wash. Krumbein, W. C., and F. J. Pettijohn. 1938. Manual of sedimentarypetiography. Appleton-Century-Crofts, Inc., New York. 549 p. Levins, R. 1968. Evolution in changing environments. Princeton Univ. Press, Princeton. 120 p. Lewis, J. R. 1964. The Ecology of Rocky Shores. English UniversitiesPress Ltd., London. 323 p. Lie, U. 1968. A quantitative study of benthic infauna in Puget Sound, Washington, U.S.A., in 1963-1964. Fiskeridir. Skr. Ser. Havunders. 14:229-556. Looman, J., and J. B. Campbell. 1960. Adaptation of S0renson's K (1948) for estimating unit affinities in prairie vegetation. Ecology 41:409-416. Newell, R. C. 1970. Biology of Intertidal Animals. American Elsevier Publishing Co., Inc., New York. 555 p.

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