distribution of biomass in rocky intertidal communities on the pacific coast of the united states

Distribution of Biomass in Rocky Intertidal Communities on the Pacific Coast of the UnitedStatesAuthor(s): George O. BatzliSource: Journal of Animal Ecology, Vol. 38, No. 3 (Oct., 1969), pp. 531-546Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/3032 .

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531

DISTRIBUTION OF BIOMASS IN ROCKY INTERTIDAL COMMUNITIES ON THE PACIFIC COAST OF THE

UNITED STATES

BY GEORGE 0. BATZLI

Department of Zoology, University of California, Berkeley, California

INTRODUCTION

Community organization can be considered from at least two different aspects. First, the structure can be investigated by studies of species diversity and dispersion. Secondly, the functional relationships between the species can be investigated by studies of food habits, behaviour, population dynamics and energy budgets. This paper reports on the community structure (species diversity) of the rocky intertidal zone on San Juan Island, Washington, and compares it with that of Monterey Bay, California.

Ideally, one would like to know how the biomass of the community is partitioned among all the member species, but practical considerations usually prevent this. Micro- scopic members are often ignored because their evaluation requires special methods, but they are functionally essential and may contribute a significant amount of biomass (Macfadyen 1963). Past workers have concentrated on particular taxonomic groups (King 1964) or particular components of the food web called sub-webs (Paine 1966). While valuable, these approaches are inadequate. Interactions between such groups affect their biomass, and we must know how to fit these sub-systems together to get a picture of the whole system. Rocky intertidal communities lend themselves to more complete studies for several reasons. (1) Since the substratum is hard and compact, it does not harbour such large quantities of microorganisms as most other types. (2) Sampling problems are reduced since many of the animals are sedentary. (3) The taxonomy of the community is manageable. (4) Zonations and the community types are relatively well documented.

While intertidal biological surveys are legion, most merely note the presence or relative abundance of species at particular locations, substratum types or tidal zones. Some work on the Pacific coast of the United States is quantitative and reports the numbers of individuals in each species (Shelford et al. 1935; Hewatt 1937). Mokyevsky (1959) used weights for fauna of the Sea of Japan, but did not say how he got them. The data themselves suggest that they were wet weights. Because species from different taxa come in various sizes and shapes, water contents and inorganic contents, the number of individuals or wet weight per species are unreliable measures of the structural contribution to the community. The dry weight of organic parts gives a more reliable measure because the water content and inorganic content of organisms are expressions of particular adaptations for survival and not of the degree to which a species shares in the biochemical pool of the community. The only rocky intertidal study other than mine that I have found to include information comparable to the dry weight of organic parts is Glynn's (1965) on the Endocladia-Balanus community.



532 Intertidal communities on the Pacific coast of U.S.A.

DESCRIPTION OF STUDY AREA

Six tide pools were chosen as natural units for the measurement of species diversity. These were all within a stretch of 10 miles (16 km) on the south and west shores of San Juan Island on rocky substrata. Surf action is reduced on these shores owing to the protection from the open ocean provided by Vancouver Island. Swift currents develop near the shore in some places, however, as the tide changes. Tidal water plus fresh water from the Frazer River and Puget Sound rush out to sea via the nearby Strait of Juan de Fuca. The resultant mixing produces water with a salinity slightly lower than open ocean water.

Table 1. Conmparison of some physical measurements of the tide pools

Surface area Volume Pool (i2) (104 cm3) Surface/volume

High C 3.8 0.141 0.413 0.341 C 3.3 0-225 0'751 0.300 L 3 5 0-699 2-385 0-293

Low E 0-8 0-398 1240 0-321 D 0 5 0-534 3-600 0.148 L 0.5 2-992 28-865 0.104

Pools were chosen to give two series of three each at high and low intertidal levels. All were inundated daily, and none was shaded. The pools were named after the nearest geographic locations on maps and after their heights in feet above sea level (measured with a transit.) A list of pools follows: Cattle Point 3-8 ft (116 cm), Cattle Point 3-3 ft (101 cm), Limekiln Point 3 5 ft (107 cm), Limekiln Point 0 5 ft (15 cm), Mount Dallas 0-5 ft (15 cm) and Eagle Point 0-8 ft (24 cm).

Table 2. Dry weights of macroscopic flora in the tide pools (g/m2)

Plant genus High pools Low pools C3.8 C3.3 L3.5 E0.8 D0-5 L0.5

Bossiella - - - - 104-1 312.4 Corallina 41-5 14-2 - - 149-6 112-4 Phyllospadix - - - 193.7 - -

Prionitis - - - 0 6 - 8.8 Fucus 18-1 - - - 1.3 - Microcladia - - - - 3.7 Ulva - 0.9 - - 20 - Ceramium - 0-2 - - 05 -

Lethesia - - - 0.7 - Halosaccion - - - - 0.1 -

Polysiphonia - - - - - < 0 1 Lithothamnion (encrusting) - - - + + +

Totals 59 6 15.3 0 194.3 262 0 433.6

Some physical features of the pools are described in Table 1. Measurements of water surface area were made with the aid of a grid placed over the pools. Depth contours were also mapped and used for calculating volume. The pools were irregularly shaped, and their size varied by factors of twenty-one for surface area, seventy for volume, but only three for surface to volume ratio. The surface to volume ratio is probably the most important measure of physical conditions since it suggests the relative rate of change of



GEORGE 0. BATZLI 533

environmental variables within the pools, such as temperature and salinity. The amounts of heat absorbed and water evaporated depend, among other things, upon the area of the pool, but the changes in temperature or salinity depend upon both the surface and volume of the water. Therefore, the higher the surface to volume ratio of the pools, all other things being equal, the more rapidly temperature and salinity will change during low tide.

A second means of describing these habitats is by comparison of their vegetation. The dry weights of the macroscopic flora given in Table 2 are not strictly comparable owing to the carbonate deposits present in the coralline algae (Bossiella, Corallina). Neverthe- less, it is clear that the high pools had few algae, most of which were corallines, while the low pools had considerably more plants, with either corallines or surf grass (Phyllo- spadix) predominating. The differences in the vegetation reflect the position of the pools in different tidal zones as defined for the Pacific coast by several authors (Ricketts & Calvin 1962). The fauna, dealt with later, also reflects this zonation.

METHODS

Error was minimized by collecting the macroscopic fauna of the pools as completely as possible. Animals and plants were removed from the pools by use of hand tools, sorted into higher taxonomic groups and transported in plastic bags to the laboratory. Here they were immediately preserved in 5000 ethyl alcohol. After identification the specimens were sorted by species, counted and dried to constant weight at 60? C. Dry weights were measured on torsion balances accurate to 5 mg. Nomenclature for the animals follows that given in Light et al. (1954) except for some isopods (Hatch 1947) and molluscs (Oldroyd 1927) not given in that reference. Algae were identified to genus from Scagel (1957).

Collections were made from each pool during one low tide. Seasonal variation was minimized by collecting from all pools within 1 week, 4-10 August 1964. With collecting time limited by the tidal cycle, some of the more numerous species could not be completely taken. In several pools the sea anemone Anthopleura elegantissima and the barnacles Balanus glandula and B. cariosus were sampled by transects, taking all of those within 2-5 cm strips across the pools. About 200 were collected to get a weight average for each pool, and the remaining specimens were counted. In the largest pool (Limekiln 0 5) certain other species could only be sampled. All limpets over 1P5 cm long were collected, but those under 1P5 cm were estimated from their proportion in a strip sample of 200 limpets of all sizes. The weight of Dodecaceria concharum, a small polychaete with tubes in an encrusting calcareous mass, was estimated by weighing a sample of 100 and correcting for the other 6700 counted. About 500 crustaceans were floated out of a portion of the algae collected in pool L 0 5, and the total amount present was estimated by correcting for the proportion of algae which had not been examined. All other animals that could be discovered were taken. Since the deepest point in the deepest pool was only 24 cm, relatively few animals (probably less than 50 ) escaped.

Barnacles, mussels and limpets were separated from their shells for determinations of the dry weight of organic parts. Separating the organic parts of chitons and snails re- quired too much labour, so sampling was necessary. Five to ten individuals of each species, spanning the size range of the collected specimens, were prepared, and the total dry weight (with shell) and the dry body weight (without shell) were measured. Graphs (Fig. 1) generally showed a straight line relationship between these two measures for different sized animals. Proportions based on the slopes of these graphs were used to change the




total dry weights to dry body weights for the other members of these species. The internal organs of echinoderms were scraped out and weighed separately from the skeletons. No corrections were made for the skeletal portions of sponges and fish since both of these taxa formed a negligible portion of the community biomass.

0-5 I- 0 Littorino sitchono

o A A 0 03 A L. scutu/lto/

0 03 ? 002- OA

0-2 OA _ 0 OA

001 _ A A

A A Thols cono/icUllot OQA A A r lome//osa

0 2 4 6 8 0 01 02

> 0' 0 _ I I c 0 01 _002 0-03 0A04

I 0~~~~

02 2 SeoresIa 4 0 Oafferina o A 0010

A C8 Aiostomo a Le*doc1/1onc ?

013 0 3I A 0 008

0~~~~

A~~~~

0 -- 2 - - -0 1 5

Total dry weight (g)1

FIG. 1. Graphs comparing the dry weights of some molluscs with and without their shells. Lepidochitona is the smaller of the two chitons shown in the lower right-hand graph.

RESULTS

Tide pool communities Seventy-two species of animals were collected in the six tide pools. Of these twenty-

seven appeared in all of the high pools or all of the low pools or both and can be considered constant. Their distribution among the pools is given in Table 3. Eight species were ubiquitous, of which five were among the top five species by weight in at least one pool, but none was a major dominant (Table 4). The major high pool dominants, the anemone Anthopleura elegantissima and the barnacle Balanus cariosus, occurred in all of the high pools and some of the low pools. The major low pool dominant, the chiton Katherina tunicata, occurred in all of the low pools but none of the high pools. Eight other species




Table 3. Distribution of twenty-seven species which occurred regularly in the tide pools

In all high pools In all low pools

But no low And some low But no high And some high Taxon In all pools pools pools pools pools

Anemones Anthopleura elegantissima

Polyclads Freemania litoricola

Polychaetes Nereis procera Nereis vexillosa Syllis sp.

Chitons Lepidochitona sp. Cyanoplax Katherina tunicata hartwegii Tonicella lineata

Gastropods Acmaea pelta Acmaea digitalis Searlesia dira A. testudinalis Acmaea sp. Littorina scutulata L. sitchana

Pelecypods Mytilus sp. Barnacles Balanus cariosus

B. glandula Isopods Dynamene sheareri Pseudione giardi Idothea

wosnesenskii Decapods Hemigrapsus nudus Pagurus

Pagurus hirsutiusculus granosimanus Asteroids Leptasterias

aequalis Fish Oligocottus

maculosus

Table 4. Dry weight (g/m2) of organic parts of the five most abundant species in each tide pool

Rank

Pool 1 2 3 4 5

C 3-8 Anthopleura Balanus cariosus Littorina Acmaea pelta Acmaea elegantissima (23 8) scutulata (9 9) testudinalis

(135-1) (12-5) (8 5) C 3-3 A. elegantissima B. cariosus Hemigrapsus Littorina Mytilus

(348 9) (63.2) nudus scutulata californianus (36 2) (16-9) (3 8)

L 3-5 A. elegantissima B. cariosus Mytilus Hemigrapsus Littorina (169-0) (31V6) californianus nudus scutulata

(12-2) (1 9) (1-8) E 0-8 Katherina Searlesia dira Pagurus Acmaea Hemigrapsus

tunicata (274) granosimanus testudinalis nudus (276) (67) (5 3) (3 5)

D 0 5 K. tunicata Thais Thais lamellosa Pagurus Searlesia dira (32 0) canaliculata (1 9) hirsutiusculus (4 2)

(16-0) (9 6)

L 0-5 K. tunicata Anthopleura Acmaea Acmaea pelta Pagurus (28 2) elegantissima testudinalis (3 6) hirsutiusculus

(27 4) (5 9) (3-1)




occurred only in the three low pools. Cyanoplax hartwegii, a small chiton usually found in the interstices between barnacles, was the only species which occurred only in the three high pools. The number of species in the low pools ranged between thirty-five and fifty-one, whereas the high pools contained eighteen to twenty-two species. Lower intertidal species tended to drop out of the fauna under the more rigorous conditions of the upper intertidal zone.

As previously noted, the high pools contained few macroscopic plants (0-60 g/m2). Sessile animals, which filter or capture small particles or organisms from the water, covered most of the rock surfaces. The dry weight of organic matter contributed by the fauna ranged between 213 and 480 g/m2 (Table 5), considerably higher than that contributed by the flora. Anthopleura and Balanus always ranked first and second; Littorina scutulata, a snail, always ranked in the top five; and the crab Hemigrapsis nudus and the mussel Mytilus californianus ranked in the top five in two of the three pools (Table 4). These pools fit into Zone 2 of the intertidal scheme of Ricketts & Calvin (1962).

Table 5. Comparison of the distribution of biomass of animals in the tide pools

No. of dominant species Dry weight . - - - A_

Pools No. of species (g/m2) 75%, biomass 95% biomass

High C 3.8 22 213'5 2 (9%) 8 (36%) C 3'3 22 480-0 2 (9%) 4(18%) L 3.5 18 223'5 1 (6%) 3 (17%,)

Range 18-22 213-480 6-9% 17-36%

Low E 0'8 41 87.9 4 (10') 13 (32%) D 0'5 35 92'5 5 (14%) 14 (40%) L 0'5 51 85-3 3 (6%) 16 (31%)

Range 35-51 85-92 6-14% 31-40%

The low pools contained more plant biomass than the high pools (194-434 g/m2) and a greater variety of plants. The biomass contributed by the fauna ranged between 85 and 92 g/m2 (Table 5), considerably less than that for either the high pool animals or the low pool plants. Katherina, a grazing indicator of Zone 3 of Ricketts and Calvin, always ranked first in biomass. The other ranks were variable, but a member of the scavenging hermit crab genus Pagurus always occurred in the top five species. The grazing limpet Acmaea testudinalis and the carnivorous snail Searlesia dira ranked in the top five in two of the three pools (Table 4). Predatory stenoglossid snails, Thais and Searlesia, sometimes move with the tidal level and are therefore considered transient and eliminated from community analyses (Glynn 1965). If they are eliminated from the low pool data, members of the grazing genus Acmaea rank in the top five species consistently.

The results in Table 5 show that a relatively small proportion of the species contribute the bulk of the biomass. Between 5 and 1500 of the species contribute at least 75', of the biomass in both the high and low pools. Between 15 and 40?/ of the species contribute at least 95'% of the biomass, with the high pools tending to show dominance by a smaller proportion of species. When biomass is plotted against species rank on an arithmetic graph, these distributions show J-shaped curves for all pools. Since most of the species are at the bottom of the curves, little resolution of the relative abundance of most of the species is possible. Plotting the log of biomass transforms the J-shaped curves into



GEoRGE 0. BATZLI 537

100 * X.

10 -x _

xx^x * *

XX*.we"

1a Mb}AX

'xx '

0- - '

00)LOWPQQ1s:*,LO*5, M$D ,A, ( L<XX XXC ; A a

O-i AML x' 00 | *)

AAA~~(x 0AX

; < 9 3 \ 564

(a) ~~~AAAMA . (b) Ax

0 10 20 30 40 50 0 10 20 Species rank

FioG 2. The relative abundance of species in tide pools of San Juan Island, Washington. (a)Lowpools., a Lr05; xD DO S LA, EOS. (b)Highpools:, L 35; x,C 38; O,C C 33.

7g3

2-

A*

(a) (b)

2-

(c) '.(d)

0t L II ~ 2 34 56 7 89 1 23 4 56

Species rank

FsG. 3. The relative abundance of species in some tide pool components compared to that predicted by MacArthur's model ( .Relative biomass units (the mean for each component) are used. (a) Sedentary L O-5, E =O020; (b) acmaeids L 0-5, E =O072;

(c) grazers L 3-5, E =1'05; (d) acmaeids L 3-5, E = 2-05.




sigmoid curves whose slope depends on the number of species ranked (Fig. 2). Such curves are called 'type b' by Whittaker (1965), and represent communities with a small group of dominants, a larger group of moderately important species and a small group of rare species. When such communities involve a greater number of species than those present here (more moderate slope to the curve), they fit the lognormal distribution of Preston (1948).

Another yardstick to which biomass distributions may be compared is MacArthur's 'broken stick' model (1957). Although the model was only meant to predict relative abundance for equilibrium species populations of similar body size and physiology residing in homogeneous biotopes, this need not prevent its use as a standard distribution with which to compare field populations. Lloyd & Ghelardi (1964) have devised a measure of equitability (E) which compares the distribution of abundances of field populations with that predicted by MacArthur's model. Other measures of goodness of fit have been proposed, but E is relatively easy to calculate and gives results consistent with the others (King 1964).

An advantage of E is that its value not only measures the goodness of fit but also suggests the shape of the empirical curve (Fig. 3). A value of 1 indicates a good fit. As values decrease from 1 the fit becomes poorer, and the empirical curve is too high for the topmost ranks and too low for the middle and low ranks. As values increase from 1 the fit becomes poorer, and the empirical curve is too low for the topmost ranks and too high for the middle and low ranks. The same pattern can be found in the graphs given by King (1964) though he gave no results with an E more than 1.

E is a ratio whose numerator is taken from Table 1 of Lloyd & Ghelardi (1964) and whose denominator is the number of species in the community being analysed. The table contains the information content for distributions of different numbers of species whose relative abundances were determined by the MacArthur model. The proper numerator is selected by taking the number of species in the table whose information content matches that calculated from the empirical data for the community. The numerator must be greater than 1, so the minimum possible value of E increases as the number of species in the community decreases. Therefore, one might expect smaller groups of species to have higher Es than larger groups. I have used E to compare the biomass distributions within several components of the several tide pools. Since the various components have different numbers of species and different Es, it is important to know if differences in E result from differences in biomass distribution or simply from differences in the number of species involved. A scattergram of E and the number of species in the component (Fig. 4) shows a tendency for higher Es to be associated with fewer species, but within any component there is no such tendency. The same trends held for components not shown. These results suggest that the values of E, even for small numbers of species, depend mostly on the biomass distribution of the component and not the number of species in the component.

Dr Joseph Connell (personal communication) has suggested that E might automatically increase when a community is divided into components. This would result from reductions in the differences of body weights among the species in the components as compared to those in the whole community. Differences in E would then reflect only the relative sizes of species within the components and not a different pattern of population biomass distribution resulting from ecological processes. If this were so, there would be a negative correlation between the difference in body weights of the largest and smallest species in a component and the E of that component. A scattergram of these two variables (Fig. 5)




shows no such correlation. Apparently the numbers of individuals in the populations for which E was calculated compensated for any effects of body size.

When comparing the Es of pools or components, it is desirable to determine whether or not they are statistically different. The value of E depends on a great many variables and may vary from sample to sample with a normal distribution of frequencies. To test this

20 _ X

x

- X

a) A

4-

cr _X X A

O0 10 20 30 0 50

No. species FIG. 4. A scattergram of the measure of equitability (E) and the number of species for several communities and components. 0, Whole community; A, top 950 ; x, acmaeids.

20

2o - 3 05

Ic 8

6-

14 -

>, 1%2

0 0.0

A

06 .

0.4 1A A A

02 A

l l I , l , , I 0 02 04 06 08 10 12 14 16

Difference in body weights (g)

FIG. 5. A scattergram of the measure of equitability (E) and the difference in body weight between the largest and smallest species for several communities and components in the

tide pools. *, High pools; A, low pools.




assumption I plotted on probability paper the distributions of E for those components which were unimodal. The resultant distributions could be fitted reasonably well by a straight line, and a scattergram of log mean and log variance showed no simple relationship. Means and standard errors are therefore used to compare Es.

For each tide pool Es were calculated for the following groups of species: the whole community (all species), the top-ranking species composing at least 950% of the biomass, sedentary species which take food from the water (anemones, barnacles, mussels and tube worms), mobile grazers (snails, acmaeids and chitons) and acmaeids alone. Additional components in which a sufficient number of species (at least three) occurred in the low pools were also treated. The means for the high and low pools are compared in Fig. 6.

Index of equitability ( E)

0 1 0203040506 070809 10 12 14 16 18 20 22

Top 95% Y 1 I iT 1 1 1 I

All species

Less stenoglossids -4-

Sedentary . .

Grazers +t

Acmoeids IL o

Chitons + + Hghpools Gatrpds____ _4-I + Low pools

Gastropodsll

Stenoglossids .-- Algal crustaceans --I

Amphipods -1-

Isopods

Decapods

Pdycyhoetes I I

Mobile .

Sedentary I I

FIG. 6. A comparison of the equitability (E) for various components of high and low tide pool communities. Vertical lines are means and horizontal lines represent two standard

errors (N = 3).

The only difference between pool levels is that E is lower for the grazers and acmaeids in the low pools (t-tests; 005>P>002 and OlO>P>0-5, respectively). The distribution of all species in the low pools agrees closely with that for all species omitting the stenoglossid snails. Considering these possible transients as members of the community does not distort the structure as revealed by relative biomass. Grouping the species in the top 9500 or those with a particular mode of feeding raised E above that for all species. The acmaeids had an E greater than that for the grazers as a whole. Two standard errors of the means for the high pool grazers, low pool acmaeids, stenoglossids, isopods and decapods overlapped the value predicted by MacArthur's model. All of these components had relatively high variability.

Endocladia-Balanus community This analysis of the Endocladia-Balanus community utilizes data gathered by Glynn

(1965) at Monterey Bay, California. The community occurs on rock surfaces of the upper




intertidal (Zone 2 of Ricketts & Calvin) as did the San Juan Island high pools. Glynn reported the dry weight of nitrogen for species collected in a series of twelve quadrats of 400 cm2 each. Thus the data should be comparable to the dry weight of organic parts so far as relative abundance is concerned. Though Glynn eliminated what he considered transient snails (stenoglossids and Tegula) from the community, he reported data from which I could calculate their nitrogen contribution.

Based on averages for the twelve quadrats, the major algal components of the community (Endocladia and Gigartina) contributed considerably less nitrogen (9 4 g/m2) than did the animal components (15-6 g/m2). The five most important animal species were Balanus glandula (12-0 g/m2), Littorina scutulata (141 g/m2), Lassaea cistula (0.9 g/m2),

Acmaea digitalis (0 4 g/m2) and Chthamalus sp. (0 3 g/m2). The first-, third- and fifth- ranking species are sedentary and take their food from the water. Thus the same functional component dominated this community and the high pools at San Juan Island.

Index of equitability (E)

0.1 02 03 0.4 0 5 06 0*7 0 8 09 1[0

Top 95% I I

All species -

Sedentary -

Grazers t_ _ _I

Acmaeids + Summer I + Winter I

Carnivores 1-_ _

Polychaetes .

Syllids

FIG. 7. A comparison of equitability (E) for summer and winter samples of the Endocladia- Balanus community. Vertical lines are means and horizontal lines represent two standard

errors (N 6).

E was calculated for the following groups of each quadrat: all species, top 95?4, sedentary, grazers, acmaeids, carnivores (stenoglossids, predatory polychaetes and nemerteans), polychaetes and syllid polychaetes. Since Glynn's samples were spread over 12 months, I checked for seasonal effects by computing means for seasonal groups of three quadrats each. No differences were found between spring and summer nor between autumn and winter, so means were calculated for two seasonal groups of six quadrats each, the warm, dry season (summer) and the cool, wet season (winter). As shown in Fig. 7 the only seasonal differences were a lower E for the top 95?4 in winter and a lower E for the grazers in summer (t-tests; 005>P>0.02 and 0.10>P>0-05, respectively). All component groups show a higher E than that for the whole community. The E for acmaeids is higher than for summer grazers but not winter grazers. The values of all the means are lower than that predicted by MacArthur's model.

Fig. 8 compares Glynn's quadrats to my pools. Data for components which showed no differences between tidal levels or seasons in previous figures have been lumped for the




calculation of new means for these components. The biomass distributions for all species, sedentary species and polychaetes were the same for both sets of data. The top 95XO of the tide pools showed the same distribution as the top 950 of the summer Endocladia- Balanus community. The biomass of the Endocladia-Balanus community acmaeids was distributed like that of the low pool acmaeids. The most variable results are those for the grazers. Winter data for the Endocladia-Balanus community are similar to those for the high pools, but the summer data fall in between the high and low pools.

Index of equitability (E)

01 02 03 04 05 06 07 0809 10 12 14 16 18 1~~ ~ I 1 1

6 + I * Tide pools Top 95% 6 TI + Endoc/ada-Ba/anus 6 - Summer I

Winter I 6--

All species 12 -f-

Sedentary 12 Tit High

Low t I 3 4 Grazers 6 + I

6 Summer I Winter High

3 Low I High Acmaeids 3 L _ 214

12 + I Low

Polychoetes 13 t I

FIG. 8. A comparison of equitability (E) for tide pool and Endocladia-Balanus community components. Vertical lines are means and horizontal lines represent two standard errors.

The numbers after each component name are the N for each mean.

DISCUSSION

The number of species present in the tide pools seemed to be more a function of tidal height than of pool size. High pools had about half as many species as the low pools even though the largest high pool, L 3 5, was larger than two low pools (Table 5). Thus a greater amount of biomass was associated with a fewer number of species. This trend agrees with that usually reported for macroinvertebrates in streams polluted with organic effluents (Wilhm & Dorris 1966; Hynes 1960) and supports the common observ- ation, e.g. Odum (1959), that communities in more stringent environments often have fewer species but greater abundance per species. The larger animal biomass of the high pools may be due to increased production by the sessile species because algae are not taking up living space and/or to decreased population turnover owing to a lack of predation during exposure. Margalef (1963) links greater complexity and greater biomass to more stable communities, but these results point out that increased complexity and increased biomass need not always go together. Indeed, Leigh (1965) has suggested that increased biomass at a given level of productivity will increase community stability whereas increased numbers of species may not.

The biomass distribution within the communities considered here is strikingly similar, the ranked abundance of the species on a log scale produces the sigmoid curve expected if the underlying frequency distribution is lognormal. Whittaker (1965, Fig. 3) found a more variable distribution of annual production for plants communities. Perhaps this is because




of the few species in some of Whittaker's samples and/or the greater range of environmental conditions represented by his data. Alternatively, it may be that the distribution of productivity (a functional attribute) is different from biomass distribution (and structural attribute), and the two should be considered separately.

If the species not in the topmost 95?/ of biomass are eliminated, the August collections from the San Juan Island pools show the same distribution of biomass as the summer Endocladia-Balanus community. Such consistency suggests that consideration of the dominants may be sufficient for characterization of community biomass composition. In the Monterey Bay community the dominance of Balanus was greater in the winter (7500 of total nitrogen) than in the summer (60% of total nitrogen), and this produced a lower E in the winter. The relative change of Balanus resulted not only from lower summer totals of its own biomass but also from higher summer totals of biomass for the second and third dominant species, Littorina and Lasaea. The average abundances of these species were similar, and together they contribute about 25% as much biomass as Balanus in the summer and about 1000 as much in the winter. These important changes were revealed only when the many moderate and rare species were eliminated from the biomass distribution. Which species compose the top 9500 cannot be decided objectively unless all species are collected, so separate consideration of the dominants' biomass distribution should supplement the analysis of the whole community and not substitute for it.

The only component which showed different distributions for both tidal heights and season was the grazers. The trend seemed to be that a few species showed greater dominance when the grazing component formed a larger part of the community. Grazers were dominant in the low pools and had a lower E there than in the high pools where sedentary species dominated. Grazers formed a larger part of the Endocladia-Balanus community in the summer (200%) than in the winter (100%) and had a lower E in the summer. The increase of summer grazers was largely due to the increase of Littorina which became more dominant within the component.

The whole communities and most of the components had Es of less than 1, the dominant species being more abundant than MacArthur's model would predict. Other analyses have produced similar distributions (King 1964) which have been called 'type IV' by Hutchinson (1961). Both taxonomic components and functional components had higher Es than whole communities, but not higher than the dominants considered separately. Just as adding rare species to the community emphasizes the relative dominance of the common species, so does lumping the components. I previously pointed out that neither differences in the number of species nor in the relative sizes of the species in the components account for the differences in E. The alternative explanation is that groups of species more taxonomically or functionally similar tend to have more similar population bio- masses owing to ecological processes.

Whether taxonomy or function is more important is difficult to determine since more closely related animals often have similar functions in the community. It is clear, however, that increasing taxonomic affinityper se does not result in greater values of E. The biomass distribution of syllids was no different than that for polychaetes as a whole, nor was the distribution of stenoglossids significantly different from that of gastropods as a whole. The components with E not significantly different from 1, whether taxonomic or functional, all share the character of similar feeding habits within the component and may be said to represent groups of functionally similar species. However, some groups of functionally similar species, viz. sedentary and grazing, had Es lower than some functionally diverse taxonomic groups, viz. gastropods and polychaetes (Fig. 6).




A major ecological question remaining unanswered is why biological communities should have biomass distributions dominated by a few species. In general the underlying frequency distribution of species abundance seems to be the lognormal of Preston (1948) although deviations from this distribution are to be expected when too few species are considered. Williams (1953) has concluded that the lognormal fits some species-abundance data better than the logarithmic series whose applications he has developed, and he discusses these and other distributions in more detail in a recent book (Williams 1964). Further, Clark, Eckstrom & Linden (1964) have shown that a logarithmic series can be produced by non-random sampling of a lognormal distribution, and many of Williams's examples of logarithmic series come from non-random samples.

Odum, Cantlon & Kornicker (1960) have suggested that a hierarchical organization of species niches (analogous to that of human occupations) would produce a logarithmic series of species abundance. There are two major difficulties with this explanation. (1) We probably are not dealing with a simple logarithmic series. (2) The only hierarchical community organization which has been well investigated, that of energy transfer or trophic level organization, has been difficult to elucidate because so many species parti- cipate in more than one level (Engelmann 1966).

A more tenable explanation, in my opinion, can be derived from a consideration of the distribution of organisms along environmental gradients, either vegetational (Curtis & McIntosh 1951) or physical (Whittaker 1956). McIntosh (1963) has reviewed such patterns as found in both animal and plant communities. Though there is much overlap, each species has a different distribution of abundance along the continuum, and the maxima are spread along the continuum. Many physical and biotic factors determine the suitability of a habitat for organisms, and these factors change along continua with varying steepness. Superimposing these continua in a two-dimensional array produces a patchwork or mosaic of different environmental types on several size scales. The bound- aries of the patches are defined by regions of steep gradients for one or several factors. A three-dimensional array can be constructed for communities whose location is specified by three spatial dimensions, e.g. plankton. The different adaptations of the species to physical and biotic conditions of varying commonness in the mosaic produce species with different distributions of abundance. The abundance of each species varies in response to the environmental gradients. Different species reach maximal abundance at different locations, and only a few are common in any one place owing to the wide variety of sites, the large number of highly adapted species and competitive exclusion.

Clark et al. (1964) have generated a lognormal curve by multiplying numbers taken randomly from normal distributions. Now if the biomass distributions of each species over each of the various mosaic types in my model are normal, and if the distribution of the amount of habitat represented by each mosaic type is normal, then the community biomass distribution generated by multiplying the biomass of each species per mosaic unit by the amount of that type present could be lognormal. Thus the lognormal biomass distribution of a community could be simply a result of the gradient organization of the environment and the individual responses of the species. A major advantage of this kind of conceptual model is that it explains in terms of ecological attributes of the species and their environment which can be checked and manipulated.

Many of the specific properties of this model remain to be demonstrated. The sufficiency of the model and the necessary restrictions on the number, size and distribution of mosaic types and the number, abundance and distribution of species can probably be evaluated best by using computer simulations. Such simulations would determine the consequences




of changes in the input variables, suggest experiments and provide output which could be compared with data from natural communities.

While analysis of data in this paper reveals some patterns of community biomass distribution, these results must be confirmed and extended by more intensive investig- ations. Ideally, such studies should be done in the same community for several years, and data should be gathered by means of replicated samples taken throughout the year.

ACKNOWLEDGMENTS

The original data given in this paper were gathered during the author's tenure as a National Science Foundation Predoctoral Summer Fellow at Friday Harbor Laboratories, University of Washington. I am grateful to Dr Paul Illg and Dr Erik Dahl for their encouragement and aid in identification of specimens and to Mr Pierre Peterson for help with the collecting. My thanks also go to Dr Joseph Connell, Dr Oscar Paris, and Dr Frank Pitelka for helpful criticisms of the manuscript.

SUMMARY

(1) The structural organization of three intertidal community types was analysed on the basis of relative biomass of the species populations. Original data for upper and lower tide pools on San Juan Island, Washington, and Glynn's (1965) data for the Endocladia- Balanus community of Monterey Bay, California, were used. Lloyd & Ghelardi's (1964) measure of equitability was used with limited success as an index of the distribution of relative abundances for comparison of communities.

(2) Results showed consistent structural patterns for all community types examined. On a logarithmic scale, community biomass was divided among a few dominant species, greater numbers of moderately abundant species and a few rare species. These results are as expected if the underlying frequency distribution is lognormal.

(3) Groups of similar species, defined either by taxonomic or functional criteria, tended to have higher equitability indices than groups of dissimilar species. The higher indices indicated relatively less dominance by the common species.

(4) A general scheme of animal distribution based on environmental gradient concepts was proposed as an explanatory model for the low equitability indices and the lognormal biomass distributions of whole communities.

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(Received 2 July 1968)



distribution of biomass in rocky intertidal communities on the pacific coast of the united states

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