abundance, diversity and temporal variability in a california intertidal nudibranch assemblage

Marine Biology 45, 129-146 (1978) MARINE BIOLOGY �9 by Springer-Verlag t978

Abundance, Diversity and Temporal Variability in a California Intertidal Nudibranch Assemblage

J. Nybakken

Moss Landing Marine Laboratories of the Central California State University and Colleges; Moss Landing, California, USA

Abstract

A 40-month study of a nudibranch assemblage within a 250 m 2 intertidal area at Asilomar State Beach, California, USA, indicated that dominance was shared among 9 species which comprised 87% of the total number of individuals enumerated. These 9 species also showed high frequency of occurrence in the area. The number of nudibranch species counted per month was shown to be independent of weather and tide conditions, but the numbers of individuals and diversity values were correlated with wave action, lower values and numbers being tabulated during times of storms. Cumulative plots of diversity and species number based upon 15 min enumeration times indicated adequate assessment of diversity and species number after 60minof sampling. The number of species and individuals and the diversity varied from month to month over the 40 months, but these variations were shown to be statistically insignificant or to be correlated with weather. Hence, it was concluded that the assemblage was a stable one, structured primarily by the 9 dominant species. No statistically significant seasonal or annual changes were observed in the assemblage. Diversity was found to correlate most highly with species number and less with number of individuals. The average number of species found per month was 13, the average number of individuals I04 r and the average monthly diversity (H) was 1.82. Significant positive and negative correlations between abundances of certain species were found. These were attributed to occurrence of prey items or to synchrony of reproduction. There was no evidence of migration, and resident status for one dominant species was established. Comparison of the present studywithear- liar work suggested that a stable nudibranch assemblage was not merely a local phenomenon.

Introdu~ion studies have been made on single species, such as those on Onchidoris fusca by Potts

Nudibranch mollusks are often conspicuous (1970) , 0. muricata by Thompson (I 961 ) macroscopic members of the intertidal communities along the Central California Coast, primarily due to their gaudy col- ors which contrast with the more somber algal backgrounds. Despite their visi- bility and obvious presence in many areas, extremely little quantitative ecological work has been done on this group. Most information concerning aspects of their ecology is found inciden- tally in papers dealing with other aspects of their biology (Miller, 1961, 1962; Potts, 1970). A few authors (Mil- ler, 1961; Swennen, 1961; Thompson, 1964) have attempted to put this scat- tered information together and to draw more comprehensive pictures of their ecology. In addition, a few ecological

and Archidoris pseudoargus by Thompson (1966).

Perhaps the major reason for the ecological neglect of this conspicuous group has been the prevailing feeling, as Potts (1970) noted, that populations for adequate quantitative analysis are rare.

Another difficulty is due to the short life cycles of most species (Comfort, 1957; Miller, 1962; Thompson, 1964). Nudibranchs can, however, be divided into two ecological groups (Miller, 1962; Clark, 1975; Franz, 1975). The first is characterized by species with several generations per year which feed on seasonally transitory prey and tend to be small in size and often cryptic in color-

0025-3162/78/0045/o129/So3.6o

130 J. Nybakken: California Intertidal Nudibranch Assemblage

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Fig. I. Monterey Peninsula of California showing location of the study site in relation to nearby cities

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BRILLOUIN INDEX

Fig. 3. Relationship between Brillouin index and Shannon index

ation. These nudibranchs are what Franz (1975) terms subannuals with the characteristics of r-strategists, or what Mac- Arthur (1960) terms opportunistic species. These species do not maintain stable populations, and show large fluc-

Fig. 2. Photograph of actual study site on Asi- lomar State Beach. Tide level at time of the photograph was -i.0 ft (-0.3 m)

tuations in abundance over short periods of time. The second group comprises what Franz (1975) terms annual species or K- strategists. These species tend to have one generation per year, feed on encrusting colonial prey animals which maintain stable populations, are of generally large size, and often are colored in striking contrast to their background. In the sense of MacArthur (1960), these are equilibrium species. It is this latter group which is of interest ecologi- cally because, as MacArthur (1960) has noted, it is only this group in which the study of relative abundance has meaning in terms of structural features of the entire community. The present study concentrated on these equilibrium species and considered changes in their abundance and diversity in a small area.

This study attempts to quantitatively analyze a nudibranch assemblage and gen- eralize about the community structure of these mollusks.

Temporal patterns in the abundance and diversity of trophically related sympatric taxa such as nudibranchs, may also reflect other underlying properties of their community, such as variability of the environmental regimen. A temporal pattern in one closely related sympatric taxonomic group may also reflect some fundamental characteristics of species associations within the group.

The basic questions posed in this work were: (I) Is it possible to quantitatively investigate nudibranch mollusk assemblages and, if so, what is their structure? (2) Do nudibranch abundances vary seasonally and/or annually and, if

j. Nybakken: California Intertidal Nudibranch Assemblage 131

so, what is the magnitude of the variation? (3) Can the change in abundance be correlated with biological and/or environmental factors?

Study Area

The study area was located at Asilomar State Beach (Latitude 35 ~ 37' 36" N; Longitude 121 ~ 56' 18" W) within the City of Pacific Grove, California (Fig. I). Sampling was done within an irregular area approximately 50 x 50 m in the lowest zone of the intertidal, Zone 4 of Ricketts and Calvin (1968). This area is uncovered only by tides falling below mean lower low water. The area is open to the Pacific Ocean and is classified in Ricketts-Calvin terminology as ex- posed open coast.

The study area lies on a dissected, granite rocky shore characteristic of most of the Monterey Peninsula. The topography of the intertidal is irregular, containing loose rock, massive rock ridges rising vertically to 2 m and tide pools of varying sizes (Fig. 2).

The study area was defined by several prominent rock ridges on the boundaries and contained in its center a massive rock outcrop rising to 1.5 m. Around this central mass were arranged a number of low-lying areas and tide pools which constituted the actual sampling area.

The area was characterized by a cover of brown algae of which three species, Egregia menziesii, Macrocystis integrifolia and Laminaria dentigera, were the dominant members.

Methods and Biases

The major field method employed was simple and remained the same throughout the study. All sampling was performed during low tides of -0.5 ft (-O.15 m) below mean lower low water or lower. Shortly before the time of low tide, the author and two other observers would enter the sampling area and each would proceed to a different area outlined by prominent features of topography. The coverage of individual observers did not overlap. At the appropriate time, each would begin a search of their sub-area, recording the number of individuals of each species of nudibranch observed.

sity were made. This count was made once a month, except for a few instances dis- cussed below. In all cases, the same observer counted the same sub-area every month.

In contemporary usage, species diversity is a measurable characteristic of a collection or a natural association of organisms which has two components, the number of species or "species richness" and the distribution of individuals among those species or "evenness" (Pielou, 1966a). Several different indices have been suggested to measure diversity in the above sense (Simpson, 1949; Hurlbert, 1971; Fager, 1972), but the two most commonly used are derived from the information theory. The two indices are those of Brillouin (1962) and Shannon and Weaver (1963). They measure the relative unpredictability that the next individual chosen will be of a given species.

The use and validity in ecological studies of diversity indices based on the information theory is controversial (Hurlbert, 1971; Fager, 1972; Peet, 1974; Goodman, 1975). Some authors such as Goodman (1975) deny that the indices have any ecological meaning, while others whilst accepting the indices (McIntosh, 1967; Sanders, 1968; Fager, 1972) have pointed out the flaws of certain indices and proposed changes or new indices. Still others (Pielou, 1966a, b; Sager and Hasler, 1969; Peet, 1974) have iden- tified the conditions under which certain indices increase or decrease in sensitivity or are simply invalid. The latter problem is particularly difficult to resolve. Hence, Pielou (1966a, b) argues for the use of the Brillouin index in cases such as this study, where the "local" diversity is wanted and where a random sample cannot be taken. At the same time, she states that the Brillouin index is better because it is not as responsive to sample size as the Shannon index. However, Peet (1974) has shown just the opposite with respect to sample size and suggests the Brillouin index is not an acceptable measure of diversity. Sager and Hasler (1969) have stated that the Shannon index is not sensitive to rare species, whereas Peet (1974) has shown that it is very responsive to such rare species. Both Shannon and Brillouin indices have been calculated in this

Enumeration was done in 15 min intervals, study and show close correlation (r = At the end of I h (75 min in a few cases) 0.98; 95% CL = 0.96-0.99), suggesting all counting would stop. The results that either would be acceptable, as Loya tabulated by each observer were then (1972) also noted (Fig. 3). I have added together for each 15 min period to chosen to use the Brillouin index because obtain the totals for 15 min, 30 min, of the lack of randomness in the sampling 45 min and 60 min intervals upon which data and because I was not interested in the calculations of abundance and diver- estimating the diversity of a larger


population. Since I was interested only in the "local" diversity of this area and its variation, I have followed Pielou (1966a, b) and others (Lloyd et al., 1968b). I have calculated these indices because they usefully incorporate into a single testable figure the parameters I wish to compare: the number of species and their relative abundance. Since I am mainly interested in comparing relative

~S 1 A r = n ~ !

where A r is the abundance of individuals of the rth rarest species; m is the number of individuals, and n is the number of species. This formula has been criticized by a number of ecologists (Hair- ston, 1959, 1969; King, 1964), primarily because of the conclusion usually drawn from good fits to the model in which

changes in diversity values among season species have been described as having and years (a-level diversity in the sense niches which are non-overlapping but of Whittaker, 1969), at the same place contiguous. It has also been criticized and not absolute values between different communities, the choice of index is not critical.

The formula employed to calculate the Brillouin index was:

I log N I. H= N N I ! N2! ..... Ns[.'

where N = total number of individuals and N I, N 2, N3,...N s are the numbers of individuals of species I, 2, 3,...s. Here, natural logarithms were used. This formula gives a population value for H, not an estimate, and as such, has no variance associated with it. However, if a series of such plot censuses are considered, then an average diversity (H) can be calculated and its variance de- termined as follows:

_ ~H S2 : ~H 2 - (ZH) 2 , N N

N-I

where H'S are the monthly H'S from the plots and N = number of months.

In order to examine the two components of diversity, evenness and richness, it was necessary to calculate the maximum

by Cohen (1968) because it is not the only possible model. Good fits are not evidence of contiguous and non-overlapping niches, and organisms which tend to show good fits share a similar set of life history characteristics (King, 1964). Thus, certain groups of organisms cannot be expected to show good fits, and others can.

This model cannot be used as evidence of niche arrangement, but this does not detract from its usefulness as a simple test for the arrangement of species abundances. Good fits to the model indicate random arrangement of abundances. Since on a empirical basis this was the sus- pected arrangement, and since the dorid nudibranches share most of the characteristics of groups showing good Mac- Arthur fits (see King, 1964), I under- took to make MacArthur plots of abundances. To indicate the closeness of the observed abundances to the expected, I calculated Lloyd and Ghelardi's (1964) "equitability" or s. This equitability is the ratio of the number of hypothe-

diversity for each collection. Evenness tically equitably distributed species could then be calculated from J = H/Hma x. based on a perfect MacArthur fit to the Using the following formula from Pielou number actually observed for the given

(1966a), Hma x was calculated:

= ~ log N! Hmax N {~!}s-r {~+I!] r

Evenness may be calculated in several ways, but here, j : Hma X is used because Sheldon (1969) has shown J to be least influenced by species richness.

Calculation of the Shannon-Weaver index was according to the formula:

H' = pilnpi ,

where Pi was the proportion of the ith species in the sample. Evenness was calculated as J' = H'/Hmax; where Hma x = in s.

observed diversity. Its upper limit is one indicating a perfect fit.

To test for similarity of the composition of the nudibranch fauna among months, I calculated a similarity index for each pair of months using an index based upon summing, for each species, the smaller of two values which was the per- cent of the total number of individuals in each sample, or:

% s = ~ min (a, b,...n),

where a, b,...n are the percentage of the total number of individuals in species a, b,...n (Southwood, 1966).

Early in the study, it became apparent MacArthur (1957) erected several math- that it was not possible to count or

ematical models to predict the relative estimate with any accuracy the numbers abundances of adequately sampled popula- of certain of the nudibranchs. In gen- tions of sympatric species in homogeneous eral, those nudibranchs whi~ could not associations. The most interesting model be accurately counted were the eolids, is that called Model I, the formula for a group which falls into the opportun- which is: istic class of MacArthur (1960). Their

j. Nybakken: California Intertidal Nudibranch Assemblage 133

cryptic coloration and small size were its occurrence did not have a signifi- most responsible for our inaccurate esti- cant effect on the diversity and abun- mates. Hence, these species were omitted from further counts and the study was then generally restricted to the dorid nudibranchs, which were usually larger in size and had a coloration which con- trasted with the background, making them easy to see. These are equilibrium species in the MacArthur (1960) sense. How- ever, one common eolid, Hermissenda crassicornis, which did have contrasting color, was retained. It is very catholic in diet. Two rarer eolids of large size

dance estimated. Two weather conditions were tested: cloudy or foggy versus clear, and calm seas versus rough. In the case of cloudy versus clear, there was no significant difference in the number of nudibranchs counted (Mann-Whitney U test, P >0.2). In the case of cloudy versus clear, there was also no correlation (Mann-Whitney U test, P >O.1) between these conditions and the calculated diversity values (H), but there was a correlation between calm versus rough

were also counted: Aeolidia papillosa, which with respect to calculated diversity val- feeds on long-lived anemones, and Flabel- lina iodinea, which feeds on hydroids; but both nudibranchs were rare in the area.

Two major difficulties in the method had to be dealt with before any conclusions could be reached from the results. One was to estimate the contribution to the variability of the data contributed through biases from weather conditions, tidal conditions, time of day and dif-

ues (Mann-Whitney U test, P <0.02) and the numbers counted (Mann-Whitney U test, P <0.05). This was anticipated because, under conditions of heavy seas, the counting area was subjected to considerable inundation even at low tide, making it difficult for the observers to count. In addition, any nudibranchs counted on rough days tended to be better hidden from view. As a result, those nudibranchs

ferent observers. The second was to esti- counted tended to be the larger and more mate how accurately the sampling re- conspicuous ones. flected the true abundances and diversi- To ascertain how accurately our sam- ties. pling reflected the true diversity and

The bias due to the differential abundance, a type of replicate sampling powers of observation of different people was attempted. Since the I h counting could not ultimately be overcome. It was time did not allow us to recount the reduced, however, by having the same area again before the flooding tide made people count the same sub-area and by counting impossible, it was necessary to the fortunate circumstance that, through- sample on a set of successive days with out the 40 months of work, only one major similar tides and consider the samples change in personnel occurred. At no time as replicates. On February 6, 7 and 8, was an observer active for less than I 1971, the tide fell to exactly the same year. I remained as an observer through- level and we sampled on those three suc- out the entire study, cessive days. The results were tested

On the California coast, the two daily with a Kruskal-Wallis one-way ANOVA, low tides are unequal and over the year which showed no significant difference do not occur at the same time of day. The lowest tide of the day, the one upon which we were dependent, occurs in the afternoon hours during the fall and winter and in the morning during the spring and summer. The month of September is usually without daylight tides of -0.5 ft and lower, and hence it is absent from our data.

In an attempt to ascertain if the tide level or the time of day that the tide occurred were correlated with the numbers of individuals counted or the diversity, regression analyses were run and correlation coefficients (r) calculated. In all cases, correlations were not significant (r = 0.06, P >O.1, tide height versus number of individuals; r = -O.21, P >O.1, tide height versus H; r = -0.09, P >>O.1, time of tide versus H; r

between successive samples (P >0.2), in dicating that our counts were statistically consistent (i.e., could have been drawn from the same population).

Pielou ~1966a) has shown that plotting cumulative numbers of sampling units against cumulative diversity (H or H') results in a curve in which H initially fluctuates and then eventually levels off. The point where the leveling-off of H occurs is the number of sampling units necessary to give a good estimate of the true diversity ("H pop" of Pielou). Since the area of our sampling was fixed, a modification of Pielou's method was attempted to ascertain if our diversity values were accurately reflecting true values. The modification was to randomly choose one of the four 15 min counting intervals, calculate the diversity (Bril-

= O.124, P >0.1, time versus number of louin H), then randomly select a second individuals; r = 0.3, P >0.05, time versus 15 min interval and combine it with the number of species counted), indicating first and recalculate the diversity, that the height of tide and the time of then do the same for three combined in-


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tervals and finally for all four intervals.

The results of this analysis, repre- senting average values based on 5 random combinations of intervals for 5 sampling dates, are given in Fig. 4 and suggest that 60 min is adequate. Because of the incoming tide, it is not feasible to carry out the sampling beyond about 75 min and, hence, we did not have the op- tion of sampling further in time to determine if any further change might have occurred with longer sampling.

A similar plot of the cumulative number of species per 15 min interval also shows leveling off at 60 min (Fig. 5).

R e s u l t s

Relative Abundance and Species Structure of the Nudibranch Assemblage

A total of 40 months of sampling has I I I i been analyzed, from October 1969 to July

1.00 15 30 45 60 1973; however, only data for the years TIME IN MINUTES 1970 through 1973 were employed for eval-

Fig. 4. Cumulative Brillouin diversity per 15 rain uating seasonal trends. The early months time interval for 5 selected sampling dates of sampling in 1969 were discarded be-

cause of loss of some months and ques-

18-

16-

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tionable early identifications. During )ct1972 the 40 months, a total of 4,162 indivi-

duals of 31 species of countable nudi- ]une1973 branchs were enumerated (Table I).

A few species were the most abundant and were present during all or nearly all 40 months of sampling. They had a high fidelity to the sampling area or high frequency (Fager, 1963).

)ec1972 On the basis of abundance and of high ~pr.1973 frequency of occurrence (80%) or fidelity

to the system, the following 9 species :eb.1973 were dominant: Triopha maculata, Doriopsilla

albopunctata, Triopha carpenteri, Rostanga pulchra, Hermissenda crassicornis, Archidoris montereyensis, Anisodoris nobilis, Discodoris heathi and Diaulula sandiegensis. All but H. crassicornis are large dorids.

Because of the presumed transitory nature of many nudibranchs, because of dependence of certain diversity indices on the knowledge of the total number of species present in a system (Pie!ou, 1966a; Lloyd et al., 1968a) and because of an interest in the total number of species that could be expected in the area, the cumulative number of species was plotted against the cumulative number of individuals counted (Fig. 6). Cumulative total numbers of individuals counted is the same as cumulative time and would give the same results. Since we sampled a single defined area rather than randomly distributed areas, this curve is the equivalent of a species- area curve which would normally be con-

/ /

I I I I 15 3 0 45 6 0 TIME IN MINUTES

Fig. 5. Cumulative number of species recorded per 15 min time interval for 5 selected sampling dates

Table i. List of species recorded during 40 months of sampling with total number counted in that period and frequency of occurrence during months of counting

Species

3 0

Total no. Frequency Species counted of occur-

rence (%)

Total no. Frequency counted of occur-

rence (%)

Triopha maculata 990

Doriopsilla albopunctata 752

Triopha carpenteri 541

Rostanga pulchra 471

Hermissenda crassicornis 302

Archidoris montereyensis 143

Anisodoris nobilis 141

Discodoris heathi 155

Diaulula sandiegensis ~37

Cadlina modesta iO1

C. flavomaculata 79

Dirona picta 77

Hopkinsia rosacea 78

Ancula pacifica 42

Dendronotus albus 34

ioo Aegires albopunctatus 36 30

100 Cadlina luteomarginata 15 23

93 C. sparsa iO 8

95 Laila cockerelli ii 23

IOO Aeolidia papillosa 9 15

93 Aldisa sanguinea 8 20

85 Antiopella barbarensis 7 13

73 Tritonia festiva 7 15

88 Onchidoris hystricina 5 13

60 Dirona albolineata 3 8

60 Phidiana nigra 2 5

58 Acanthodoris hudsoni 2 5

60 Polycera atra 1 3

40 Onchidoris muricata i 3

30 Ancula lentiginosa i 3

Hallaxa chani i 3

Total 4,162

structed by accumulating successive quadrats. The result (Fig. 6) is a typical curve which becomes asymptotic between 28 and 29 species and suggests that we have, in fact, recorded most of the species present in the system. If the x axis were to be changed to time rather than individuals, this point would have been reached after the first 18 months of sampling. That this takes more than 1 year indicates that some of the less common species have definite < seasons when they are present in the community and/or that some of the rare m

o dorids are very sporadic in occurrence.

The number of species and the number of individuals recorded each month varied considerably (Figs. 7 and 8). The average number of species counted each month was 13.18, and the 95% confidence limits were 12.3 and 14.1. The fewest number of species recorded was 7 (April, 1970) and the largest number 19 (October, 1972). The average number of individuals counted each month was 104 and the 95% confidence limits were 88.8 and 119.2. The fewest was 36 (May, 1970) and the largest was 200 (October, 1972).

On an empirical basis, the abundances of most nudibranch species appeared to

J If) ILl

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J. Nybakken: California Intertidal Nudibranch Assemblage 135

I I I

I 0 0 0 2 0 0 0 3 0 0 0 C U M U L A T I V E No, I N D I V I D U A L S

Fiq. 6. Cumulative number of species recorded as a function of cumulative number of individuals counted

were found in the same spot several months in succession. Even after 3 years of sampling, it was not possible to predict where in the area one would expect to encounter a given species, except for

be randomly distributed within the count- juvenile Triopha maculata, which were al- ing area during most counting months, ways found under rocks. This was not always the case for single To test for random arrangement of individuals of a species, a few of which species abundance, observed abundances


2O

16

14

0 12 W

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J M M J S N J M M J S N J M M J S N J M M J 1970 1971 1972 1973

Fig. 7. Total number of nudibranch species recorded in each month of sampling

200 d

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Fig. 8. Total number of individuals of all nudibranch species recorded in each month of sampling

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Fig. 9. Relative abundance (numbers) of nudibranchs per month in study area. Dashed lines: observed abundance; solid lines: calculated abundance from MacArthur model I. Ordinate is abundance, and abscissa is species rank by numerical abundance. Data from the year 1972

were compared with those expected on the basis of MacArthur Model I (MacArthur, 1957). In most months, the nudibranchs showed a qood fit to the model (Fig. 9). In those months where the fit was not

good (February, March, May, November and December), the common species was always far more common than the model predicted. This was almost always due to the occurrence in these months of large numbers


2.50 2.25 2.00 /

H 1.75 1.50 1.25

1.00 ' ' ' , ' , , , , , ' , , , , , , , , , , , , n i l , , , , , , L , , , , , , M M J S N J M M J S N J M M 4 S N J M M J

1970 197l 1972 1973

Fig. iO. Variation in Brillouin diversity (H) from month to month over the period of study

�9 90 f .85

d 75 t .70 .65!, .60

. . . . , , . , . , . , . , . , , , , , , , , , , , , , . , , , . ,

�9 5 5 MM d S N d M M d S N d M M d S N d M M J 1970 1971 1972 1973

Fig. 11. Variation in "evenness" (J) from month to month over the period of study

of small juvenile Triophamaculata. It thus appeared that the abundances of dorid nudibranches were randomly distributed in time. Present knowledge of food and substrate preferences is inadequate for conclusions regarding niche arrangement.

Di versi t y

Since there were rather large monthly fluctuations in both diversity (H) and evenness (J), it became of interest to determine whether species richness or total numbers of individuals accounted for more of the variability. Spearman rank tests (r s) correlating H with number of individuals and of species were both significant (r s = 0.38 for H versus individuals, P <0.05; r s = 0.63 for H versus species number, P <<O.O1). The correlation was much stronger for species and diversity, indicating that the number of species counted per month was a better indicator of diversity than the number of individuals. This was due to the fact that, when high numbers of individuals were counted, it was the result of inclusion in the sample of large numbers of Triopha maculata (r = -O.51, P <<O.OO1 for number of T. maculata versus J; r = 0.58, P <O.O1 for number of g. maculata versus total number of individuals.

Evenness (J) was not correlated with the total number of individuals counted (r = 0.06, P >>O.1) nor with the total number of species recorded (r = 0.09, P >>O.1) but was, as expected, correlated with diversity (r = 0.66, P <0.O01). This means that high diversity in nudibranchs usually indicates high evenness values and is independent of the numbers of species and individuals recorded. It is here a measure of numerical dominance, with high J values indicating a lack of dominance and vice versa.

Lack of correlation of evenness with total numbers of individuals counted was probably due to the fact that, when large numbers were counted, it was usually due to the increased abundance of one or two of the common species, notably griopha maculata or Doriopsilla albopunctata, which was also reflected in decreased diversity values (r = -0.76, P <<0.001). This is also suggested as the reason for the lack of correlation with number of species because, when counts of individuals are high, the few individuals of new species added do not affect the evenness component as much as the abundant species.

The correlation between the species richness and the number of individuals counted was strong (r = 0.67, P <<O.O01), indicating that the more nudibranchs enumerated, the greater was the probability of obtaining additional species. This correlation was not reflected in

Diversity (H) and evenness (J) calculated the correlation between diversity and monthly for 1970-1973 are given in Figs. total number or between evenness and to- 10 and 11. The average diversity over 31 tal number, because these measures were months of sampling was H = 1.80, the vari- responsive to the distribution of indi- ance was O.51, the 95% confidence limits viduals as well, and high numbers usual- were 1.80 • and the range was 1.1 to ly mean disproportionate numbers of the 2.45. common species.


To recapitulate, there was a highly significant correlation between diversity and species richness (r = O.71), but months with greater numbers counted tended to have more species (r = 0.67), which yielded the significant, but weaker, correlation (r = 0.46) between

Since Sager and Hasler (1969) dealt with phytoplankton, it seems likely that they had large numbers of individuals and, as shown here, when large numbers are available, the rare species have little or no effect on the Shannon formula. Sager and Hasler (1969) note this

diversity and total number of individuals by saying that, after the first 10 to 15 enumerated, because more individuals of the common species were added.

There is controversy concerning whether the Shannon index is responsive to the presence of rare species. Sager and Hasler (1969) have criticized the index as insensitive to rare species, while Peet (1974) demonstrates mathematically that it is most sensitive to rare species. Calculations in the present study suggest that this sensitivity may be a function of numbers of individuals. When the total number of nudibranchs counted over the 40 month study, apportioned in- to species {Table I), is used to calculate H', the value is 2.361. If, however, the 10 rarest species are removed and the index recalculated, the value is 2.342, which is not significantly different from that calculated for 31 species. In this case, the index is not sensitive to rare species. The correlation between H' and number of species for each of the 40 months is highly significant (r s = 0.63, P <<O.O1). In all these months, however, no month had more than 200 individuals enumerated. It thus appears that the Shannon formula is sensitive to rare species when the number of individuals counted is low, but is not when the number of individuals is high. The point or area of significant change here is not known, but it certainly is more than 200 and less than 4,000. For our monthly examples, the Shannon formula should be sensitive to

dominant species have been enumerated, the remainder added have little effect. In the present study, however, the correlation of H' with species number was highly significant (r s = 0.63, P <<O.01), and this was undoubtedly due to the small numbers of individuals enumerated per sampling interval, which made H' sensitive to the less abundant species. In this study, H' was also significantly correlated with the number of individuals (rs = 0.38, P <0.05), which again was probably due to the fact that as more individuals were enumerated, rare species were encountered faster than individuals were added to abundant species. Sager and Hasler (1969) also reported no correlation between number of species and J' or evenness, and suggested that this was due to the fact that the equitability was established by the first 10 to 15 abundant species, after which additional species did not have any significant in- fluence. In the present study, there was no significant correlation of J' with either species number (r = 0.09, P >>O.1) or number of individuals (r = -0.06, P >>0.1). This suggests that, even though the index is sensitive to species at these low numbers, the evenness component is not influenced by it so much as it is by how the numbers are apportioned among the dominant species. Or, alternatively, at these low numbers, the addition of new, rare species and addition of more individuals to the dominant species as sample size increased reinforced each

rare species. Sensitivity to rare species other. at low numbers of individuals is more pronounced where there is a high concen- tration of individuals in the dominant species (which counteracts the low evenness component).

Sager and Hasler (1969) and others (Pielou, 1966b) have noted that there is a problem in estimating the diversity of a community where number of species is unknown and a sample large enough to hold them unreasonable. After 40 months, 31 species had been found, but calcu- lating diversity on the basis of these 31 using total abundance gives a value not significantly different from one using 21 species. It appears unnecessary to have all rare species to estimate community diversity, provided one goes beyond a certain critical level, as Sa- ger and Hasler (1969) have noted.

Temporal Variability and Species Interactions

As was anticipated, the number of species counted, the number of individuals counted and the diversity values showed considerable fluctuations over the 40 months of study ~Figs. 6, 7, 10). Where- as a portion of this temporal variability can be explained by the aforementioned significant correlation between wave action and number of nudibranchs, it is not an explanation of all fluctuations. It is of interest to determine if the observed fluctuations were indicative of temporal or seasonal changes or cycles or were merely due to random error.

To answer this question, a one-way analysis of variance was first run with


2 .50r 3 0 0

2.25

2.00 " r

>- 1.75 I'- ( / 3 r r

t.u 1,50 > a

z 1.25 : : ) 0 _1

l.OO n,, o3

075

i

4

T

•

J F M A M J J A S 0 N D MONTHS

Fig. 12. Average monthly Brillouin diversity over 40 month period. Solid dots are means and lines represent 95% confidence limits

250

2OO <{

E 3

N is0

Z

u_ I 0 0 0

6 z 5 0

0

I I I

I I I I i l 1 | I i |

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

MONTHS Fig. 13. Mean number of individuals collected per month over 40 month period. Solid dots are means and lines represent 95% confidence limits

the months as treatments and the years as replicates. One such ANOVA was run for each of the following: the diversity values, the number of individuals, the number of species. Secondly, the mean values for each of the three parameters 20 for each month were calculated and are presented in Figs. 12, 13 and 14, respec- J8 tively, where the monthly means and 95% confidence limits are displayed. In order 16 to make all pair-wise comparisons, I w employed the Tukey w-procedure (simul- ~ 14 taneous test procedure) which adjusts W probability levels in multiple compari- ~ 12 sons.

The results of the Tukey w-procedure O showed that, in all cases, diversity, 6 I0 numbers of individuals and numbers of Z species did not differ significantly 8 (P >0.05) among months from that expected by chance. The few low mean values ob- 6 served, November and March, when checked turn out to have resulted from the inclusion in these means of sampling times when wave action was particularly severe. Since, as I have shown before, there is a positive correlation with weather, this is the reason for the low values.

Because there are no significant differences between months for diversity, numbers counted, or species recorded, and because 9 species (Table I) showed

I

- '1'

m

]

i I I 1 I i I i I J

J F M A M J d A S O N O

MONTHS

Fig. 14. Mean number of species collected per month over 40 month period. Solid dots are means and lines are 95% confidence limits


such high fidelity to the area throughout 40 months, I conclude that the nudibranch assemblage is stable in terms of these parameters. It would appear that the 9 dominant species, accounting for 87% of all counted individuals, are the most important in characterizing the assemblage. Declines in the abundance of one species are compensated for by in- creases in the abundance of other species such that fluctuations in diversity values and in numbers of individuals re- main relatively constant within the limits of sampling error.

Results of one-way ANOVA indicate that the diversity did not change significantly over the years 1970-1973 (P >0.05), nor did the numbers of individuals counted (P >0.05); but the number of species did (P <0.05) (Table 2), with more species enumerated in 1972 and 1973 than in 1970. Since the 9 dominant species remained abundant throughout this period and since the numbers of rare species counted was not significantly different among years (ANOVA, P >0.05), this may be due to increased competence of the team. This significant trend was probably also responsible for the nearly significant change in diversity over the years, because, as we have seen, diversity was strongly correlated with species

richness. Similarity among months or seasons

within years in the composition of the nudibranch fauna was examined; the results of this similarity analysis are given in Table 3. Adjacent months showed high similarity and, in general, there was low similarity with more distant months. Trends or seasonal groupings were not apparent, suggesting that the nudibranch species structure was relatively constant and changed slowly within limits. There were no large fluctuations in species from month to month, due to rapid appearances and disappear- ances of individuals. Again, this can be attributed to the high fidelity of the 9 dominant species.

Interactions between species such as the abundance of one species affecting the presence, absence or abundance of another species were also examined. Due

Table 2. Analysis of variance comparing diversity, numbers of individuals and number of species among years

Source SS DF MS F P

Diversity

Years 0.435 2 O.217 3.42

Error 1.714 27 0.063

P >0.05

Number of individuals

Years 8545 2 4272

Error 43167 28 1541

2.77 P >O.1

Number of species

Years 55.0 2 27.5

Error 150.5 28 5.4

5.12 P <O.O5

Archidoris montereyensis, Diaulula sandiegensis and Discodoris heathi which, among themselves, account for half the significant correlations. This may be fortuitous due to the seasonal presence of special- ized food organisms, but this seems unlikely, since sponges appear to be present all year. Since the correlations were positive, these species probably do not compete for the same food. Indeed, Cook ( 19 62) reports Archidoris montereyensis to feed on Halichondria panicea, Diaulula sandiegensis on Haliclona sp. and Rostanga pulchra mainly on Ophilitaspongia sp. (but on others as well). Similarly, McBeth (I 971 ) reports Anisodoris nobilis tO feed on the sponges Myxilla agennes, Parasperella psila, Zygerphe hyaloderma and Mycale macgini- tiei. The food of Discodoris heathi is unknown at present, but is probably also sponges.

A more likely explanation for the positive correlations may be synchrony of the reproductive seasons or a long, extended reproductive season among these species. Unfortunately, little is known of the reproductive cycle of Pacific coast nudibranchs. McFarland (1966) reports egg laying in July for Discodoris

to the lack of available information on heathi, and Costello (1938) notes the ap- resource utilization for the 9 most abun- pearance of eggs of m. heathi in labora- dant species, only a series of statisti- tory aquaria in January. For Archidoris

cal correlations on the relative abundances from the counting area were possible. The abundances of the 9 most common species were correlated with each other using a Spearman rank correlation

montereyensis, Marcus (1961) reports spawning at Monterey from November to March, as does Costello (1938) for laboratory individuals, while Hurst (1967) reports egg masses of A. montereyensis at

test (Table 4). any time of the year. Ricketts and Cal- A large number of significant positive vin (1968) say that miaulula sandiegensis

correlations was found among the sponge eggs may also be found almost throughout feeders Rostanga pulchra, Anisodoris nobilis, the year, but Costello (1938) noted


Table 3. Trellis for comparison of similarity of months. * = 35-50%,

�9 ** = 66-80%

** = 51-65%,

1970 Feb. Apr. May June July Aug. Sep. Oct. Nov. Dec.

Feb. ** * * *** ** *** * * **

Apr. 55.5 *** ** ** ** ** *** ** **

May 49.6 73.1 *** ** ** ** *** * **

June 46.5 59.4 66.3 * * * ** * *

July 74.7 60.5 58.9 42.4 *** ** ** * **

Aug. 65.0 65.5 56.5 40.2 77.5 *** ** * **

Sep. 70.1 54.1 53.7 40.6 58.9 68.3 *** *** ***

Oct. 45.4 68.3 66.4 56,4 51.7 62.6 76.7 *** ***

Nov. 32.8 55.3 48.1 38.0 41.9 49.9 74.2 68.9 ***

Dec. 58.4 60.7 53.4 44.6 60.7 64.3 82.6 79.6 72.7

Average similarity = ~ = 58.9

1971 Jan. Feb. Mar. Apr. May June July Aug. Oct. Nov. Dec.

Jan. *** ** * * * * * * * *

Feb. 75.8 *** ** ** ** ** * ** * **

Mar. 52.1 70.8 ** ** ** * * * * *

Apr. 44.0 62.2 60.8 *** ** ** ** ** ** ***

May 42.7 63.6 53.6 79.9 *** *** ** *** *** ***

June 44.2 51.0 55.3 59.6 68.2 *** *** *** *** ***

July 33.9 54.0 42.7 59.8 66.7 76.0 *** ** ** **

Aug. 34.8 36.1 42.6 53.2 65.5 69.2 70.1 *** ** ***

Oct. 42.0 56.2 48.0 64.2 78.5 70.3 64.6 78.8 *** ***

Nov. 36.5 48.6 35.7 63.3 72.3 66.0 62.8 61.4 78.4 ***

Dec. 46.9 57.3 46.3 68.0 78.9 71.7 62.2 67.6 77.0 80.3

= 59.5

1972 Jan. Feb. Mar. Apr. May June July Aug. Oct. Nov. Dec.

Jan. *** *** *** *** ** *** ** *** ** **

Feb. 66.0 *** *** ** ** * * ** *** ***

Mar. 66.4 75.8 *** *** *** ** * ** *** ***

Apr. 76.5 73.1 82.2 *** *** ** ** ** ** **

May 75.0 59.9 72.8 76.9 *** ** ** ** ** *

June 62.0 58.9 69.7 73.8 81.0 *** *** *** ** *

July 67.7 43.5 63.6 61.1 65.2 74.1 *** *** * *

Aug. 59.2 38.0 49.7 55.3 61.7 73.0 76.3 ** * *

Oct. 74.8 55.7 58.O 62.8 55.3 69.7 70.4 59.4 ** **

Nov. 59.1 79.6 72.1 65.0 51.1 55.2 40.6 34.5 52.3 ***

Dec. 56.5 78.9 69.3 55.9 47.5 43.1 44.7 35.2 57.6 75.6

= 62.5


Table 4. Matrix of Spearman rank values (r s) for 9 most abundant species, April 1970- June 1973

Triopha maculata

Doriopsilla albopunctata

Triopha carpenteri

Rostanga pulchra

Hermissenda crassicornis

Archidoris montereyensis

Anisodoris nobilis

Discodoris heathi

Diaulula sandiegensis

~ ~ ~ 0 0 ~ "-I

.06 - . 0 5 -.07 -.002 +.02 +.25 +.03 - .05 +. [0

+.47 +.ll +.25 +.50 +.47

. . . . . . . . ~ 7 -.05 +.47 +.62 +.36

* -- ** . . . . ~"-~.~. 13 +.33 +.39 +.64

. . . . . . . . . . . . ~ 8 +.34 +.25

-- = P >0.05; * = P <0.05; ** = P <O.01.

reproduction in laboratory individuals of D. sandiegensis from November to March and in tidepools during both winter and summer. The egg ribbons of Anisodoris nobilis have been reported from Monterey tidepoo!s in March and in laboratory individuals from November to March and in June and July (Costello, 1938). Hurst (1967) found Rostanga pulchra egg masses in Puget Sound only during summer, while Costello (1938) reported laboratory individuals spawning at Monterey from November to March. Several authors (Costello, 1938; Marcus, 1961) here noted that time of breeding varies at different localities along the coast. Based on available evidence, it seems

The significant positive correlations of Triopha carpenteri with the sponge feeders Diaulula sandiegensis and Discodoris heathi and with the eolid Hermissenda crassicornis are more difficult to explain. Presumably, there is no food overlap; hence, these correlations may be due to other reasons such as synchrony of breeding season or season of maximal occurrence. Coexistence may also be due to spatial relationships. No reason is evi- dent why H. crassicornis should have significant positive correlations with the sponge feeders Anisodoris nobilis Diaulula sandiegensis and Discodoris heathi.

The significant negative correlation between Doriopsilla albogunctata and Triopha

likely that breeding extends over a large carpenteri is most interesting. Since one proportion of the year, particularly in this area, where variations in sea tem- peratures are minimal throughout the year. Comparison of the abundance of these 5 nudibranchs among the different months {Tukey w-procedure, P <0.05, all combinations) revealed no significant

feeds on bryozoans and the other on sponges (Ghiselin, 1964), they cannot compete for food. The correlation could, however, be due to reproductive asyn- chrony, as g. carpenteri breeds primarily in the summer (Costello, 1938), whereas D. albopunctata apparently breeds through-

differences in abundances among any pairs out the year (Costello, 1938; McFarland, of months. Hence, there are no pulses in 1966). Clearly, more data are needed to the population abundances; these species resolve these correlations. are equally abundant all year.

The two species of Triopha both feed on bryozoans (McBeth, 1971; Nybakken and Eastman, 1977). The lack of any significant correlation of abundances between them suggests that they do not compete, as was found by Nybakken and Eastman (1977).

Less Abundant Species

I have already shown (Nybakken, 1974) that the smaller eolid, arminacean and dendronotacean nudibranchs occur seasonally at Asilomar, and a similar sit-


uation might prevail among the rarer samples is 0.57, and it is from a large dorids. To test this hypothesis, the sample (N= 187). number of rarer dorid species and individuals observed each month from February 1970 to July 1973 were compiled, and the GeneralDi~ussionandConclusions means calculated for each month and for each year. Analysis of variance and the Tukey w-procedure showed no significant differences among months (P >0.05), either for the number of species observed or the numbers of individuals, suggesting that there was no seasonality in their appearance in the enumeration area. Similar tests between years also showed no significant difference (P >0.05).

Despite the lack of statistical sig- nificance among months, the data show, with one exception, high values of both species and individuals of the rarer dorids in the fall and early winter months (October - December). This trend might have been significant had not November of 1972 had the worst weather of the entire 40 months of counting, with counts for that month of but 2 species and 2 individuals. October of that year produced counts of 10 species and 48 individuals and December 8 species and 31 individuals. Since there was a significant correlation between weather and number of individuals and diversity measurements, it seems possible that this stormy month may have masked a real trend. It is possible that the dorids really peak in fall and winter, whereas eolids peak in spring (Nybakken, 1974), but the present data are insufficient to establish seasonality for the less abundant dorids.

Lloyd and Ghelardi (1.964) and Fager (1972) have noted that small samples tend to contain a higher proportion of rare species than occurs in the whole population. Since there did not appear to be a significant correlation between season and occurrence of the rarer species, the proportion of rare species in

Whenever ecological studies of nudibranchs have been done in the intertidal zone, and especially when considering, as in the present situation, long-term studies of what are presumed to be resident populations, the question of migration arises. Earlier authors (Garstang, 1890; Hecht, 1895; Balch, 1908; Eliot, 1910; Crozier, 1917; Costello, 1938; Thompson, 1957) have suggested that the sudden appearance or disappearance of nudibranchs in the intertidal either does or could result from migration from subtidal population centers. If this were so in the present case, surely the results could not be interpreted as reflecting temporal variation in a stable community.

Migration in nudibranchs has been attributed to various aspects of spawning (Hecht, 1895; Balch, 1908), action of currents and wave action, or other cli- matic factors (Crozier, 1917; Chambers, 1934) and changes in post-larval behavior and food (Garstang, 1890; Thompson, 1957).

The literature on migration has re- ceived an extensive review by Miller (1962), who concluded that migration did not occur, and both he and Thompson (1964) indicate that populations of nudibranchs are established in regions through settlement of veliger larvae.

During the course of the present study, no evidence was obtained suggesting that migration occurred in any of the numerically dominant nudibranch species. The best evidence for a resident population was obtained for Triopha macu-

lata. In this species, both very tiny individuals and mature, large individuals were found in the counting area. In T.

the samples was examined. A Spearman rank maculata, the small individuals appeared correlation analysis of the total number during the winter months, followed by of nudibranchs counted with the proportion of rare species present, i.e., all those species except the dominant nine, indicated a significant positive correlation (r s = +0.57; P <O.O1). This suggests exactly the opposite; i.e., the larger the sample size, the greater the proportion of rare species. If the total number of species collected over 38 months is taken as the true species number, it is 31. Of this 31, nine are here

progressively large individuals and cul- minating in large adults in late fall (Fig. 15). This is a typical progression expected in an annual species, as noted by Thompson (1964). The small individuals of T. maculata were found under rocks, whereas the adults were found conspicu- ously crawling in the open. A similar situation has been reported by Potts (1970) for Onchidoris fusca, and suggests that one reason for the sudden appearance

designated as numerically dominant, of certain species on the shore is the leaving 22 in the "rare" or less abundant change from cryptic under-rock habits to category and giving a proportion of rare surface habitation. Certainly, the pres- species for the population of 0.71. The ence of all sizes of T. maculata in the only value which approaches this in the counting area strongly suggests that they


--Si7E NUMBER not seem logical for these small animals i~[ ~ to undertake migrations when their basic I | ~ II ]I~O food supply is present at all times.

i~ ~ II II | The species Triopha carpenteri and Doriopsilla albopunctata are Numbers 2 and

E l I I I Ill /lie o J 3 in total abundance, respectively, with ~--J Jl I A/I I ~ ~ ~ extremely high fidelity to the area

(Table I). However, extremely few small individuals were encountered during the

~0 l 80 ~ entire study. When present, the individ- ___ uals were always large or mature. It is

~ [9 / ~ I~_6 l /160 possible that the small ones were over- ~_~ F looked, that they inhabited the under-

8 ~\ / k F ~ ~ sides of large rocks which were inacces- sible to observation, and were cryptic

40 ~ in color, but it seems unlikely that in ~I~;~\~;/~ ~ ~ ~ I ~ 40 months of careful work, we would not

have found at least some, if they had ~u ~0 been present. No egg masses were found

for either species during this time. ~.l ~i, J L, J L,, :,~a ~, ~ Ij ,, ~,~, ,!I Whereas this suggests the possibility of

5 } ~ 0 migration the fact that they were pres- J FMAMJ JAOND J FMAMJ J AONDJFMAMJ

197J 1972 1973 ant virtually all the time suggests that,

Fig. 15. Triopha maculata. Number and average size (arbitrary units) per month for 28 month period

do not migrate. The sudden disappearance of most large individuals of T. maculata late in the year probably is due to their death following breeding, as has been noted for other nudibranchs by Com- fort (1957). That not all die is veri- fied by the finding of a few adults of large size at other seasons and hence, death is not certain following spawning, a situation noted also by Miller (1962).

Small and large individuals of Rostan- ga pulchra, Anidodoris nobilis, Archidoris montereyensis, Diaulula sandiegensis and Hermis- senda crassicornis were found in the study area, suggesting that migration was not responsible for these populations. This is further reinforced by the knowledge that, with the exception of H. crassicor- his, all the above feed on encrusting sponges (Cook, 1962; McBeth, 1971), which are present year-around in the area making migration for food unnecessary.

Although it has been suggested (Cos- tello, 1938) that migration may also be affected by currents or wave action, these dominant species <Table I) are present year-around, including times of severe wave action~ Although low abundances during times of stormy weather may be due both to individuals seeking shelter in crevices and under rocks, where they were not observed, and to being washed out of the area, I do not believe it is due to migration. It does

if migration does occur, it must be a continuing process at a low level. Re- cently, close examination of the under- sides of very large rocks, rocks not normally moved in our studies, has revealed small D. albopunctata. Hence, I do not believe migration occurs in these species either.

Unfortunately, no other quantitative long-term studies exist for nudibranch assemblages on the Pacific coast. The only study of nudibranch populations close to this is that of Bertsch et el. (1972) on the nudibranchs of the San Mateo coast, an area some 30 to 40 miles north of the present study. Their study was not quantitative, and reported results of haphazard samplings at various different areas and months over a 5 year period. It is thus not possible to make statistical comparisons of the data. It is, however, of value to compare the relative abundances of species, based on 5 year totals, with the present data. In Bertsch et el. (1972), the dominant 9 species in decreasing order of abundance were: Triopha carpenteri, Diaulula sandiegensis, Rostanga pulchra, Acanthodoris lutea, Anisodoris nobilis, Cadlina luteomariginata, Archidoris montereyensis, Aegires albopunctatus and Cad- line modesta. It should be noted, however, that Bertsch et el. list a "Triopha sp. " category and a Triopha macu!ata category. it is quite likely that the "Triopha sp. ~' were juvenile T. maculata showing the different color pattern typical of the ju- veniles. If this is so, then combining these two categories would give T. macu- late a relative abundance position tied with Archidoris montereyensis. This means that of my 9 dominant species, 6 were also among the most abundant on the San Mateo coast, suggesting that stable nudi-


branch populations dominated by a few species is more than just a local phenomenon.

The major dominant in my studies, which is present but does not appear to be dominant in San Mateo, is Doriopsilla albopunctata. Triophacarpenteri was the most abundant nudibranch in San Mateo, and at Asilomar Beach there is a highly significant negative correlation between T. carpenteri and D. albopunctata, a relation which may explain the lower abundance of the latter to the north.

Bertsch et al. (1972) also calculated diversity indices, but the validity of these indices is questionable due to variation in sampling times, area and effort. They also calculated their index over all nudibranchs, including the smaller opportunistic eolids which I have noted (Nybakken, 1974) were not present at all times nor could be accurately counted. Despite these problems, Bertsch et al. (1972) concluded that, during their 5 years of study, the species diversity did not fluctuate seasonally, a conclusion supported by this study. They also state that the "greatest absolute abundance of opisthobranch species and speci- mens occurred during the summer months" As I have noted, my data do not suggest this (Mann-Whitney U test, P >0.05 for all months compared among themselves). Bertsch etal., however, did not make a distinction between the opportunistic and equilibrium species, counting all. As I have noted (Nybakken, 1974), the opportunists as a group tend to cycle in species numbers, the largest numbers occurring in the spring and early summer. If the number of species of opportunists

of San Mateo County, California. Veliger 14, 302-311 (1972)

Brillouin. L.: Science and information theory, 2nd ed. 169 pp. New York: Academic Press 1962

Chambers, L.A.: Studies on the organs of reproduction in the nudibranchiate mollusks, with special reference to Embletonia fuseata Gould. Bull. Am. Mus. nat. Hist. 66, 599-641 (1934)

Clark, K.B.: Nudibranch life cycles in the North- west Atlantic and their relationship to the ecology of fouling communities. Helgol6nder wiss. Meeresunters. 27, 28-69 (1975)

Cohen, J.: Alternate derivations of a species- abundance relation. Am. Nat. 102, 165-172 (1968)

Comfort, A.: The duration of life in molluscs. Proc. malac. Soc. Lond. 32, 219-241 (1957)

Cook, E.: A study of food choice of two opisthobranchs, Rostanga puichra McFarland and Archi- doris montereyensis (Cooper). Veliger 4, 194- 196 (1962)

Costello, D.P.: Notes on the breeding habits of the nudibranchs of Monterey Bay and vicinity. J. Morph. 63, 319-343 (1938)

Crozier, W.J.: On a periodic shoreward migration of tropical nudibranchs. Am. Nat. 51, 377-382 (1917)

Eliot, C.: A monograph of the British nudibranchiate Mollusca, Part VIII (Supplement), 198 pp. London: Ray Society 1910

Fager, E.W.: Communities of organisms. In: The seas, Vol. 2. pp 415-437. Ed. by M.N. Hill. New York. Interscience 1963

- Diversity: a sampling study. Am. Nat. 106, 293-310 (1972)

Franz, D.R.: An ecological interpretation of nudibranch distribution in the northwest At- lantic. Veliger 18, 79-83 (1975)

Garstang, W.: A complete list of the opisthobranchiate Mollusca found at Plymouth. J. mar. biol. Ass. U.K. 1, 399-457 (1890)

observed is added to the present data for Ghiselin, M.T.: Feeding of Dendrodoris (Doriop- equilibrium species, then large numbers of species occur in both spring-summer and fall. However, even with that, there are no significant differences among the months (Tukey w-procedure, p >0.05). Hence, I conclude that, except for the aforementioned eolids, the number of species present does not vary seasonally.

Acknowledgements. I owe a debt of gratitude to my students R. Ajeska, G. McDonald, D. Shon- man, S. Anderson and G. Anderson, who helped me in the field work, particularly the monthly counting.

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Hecht, E.: Contributions a l'etude des nudibranches. M~m. Soc. zool. Fr. 8, 539-711 ( 1 8 9 5 ) '

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14@ J. Nybakken: California Intertidal Nudibranch Assemblage

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Professor J. Nybakken Moss Landing Marine Laboratories

P.O. Box 223 Moss Landing, California 95039

USA

Date of final manuscrlpt acceptance: July i, 1977. Communicated by J.S. Pearse, Santa Cruz

abundance, diversity and temporal variability in a california intertidal nudibranch assemblage

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