- Email: [email protected]
Acid-iron waste as a factor affecting the distribution and abundance of zooplankton in the New York Bight
Estuarine and Coastal Marine Science (1973) I, 5 1-64
Acid-iron Waste as a Factor Affecting the Distribution and Abundance of Zooplankton in the New York Bight II. Spatial Variations in the Field and Implications Monitoring Studies”
for
Peter H. Wiebe, George D. Grice and Elaine Hoaglandb Woods Hole Oceanographic Institution,
Woods Hole, Mass. 02543, U.S.A.
Reckved 2 May 1972 and in revisedform 10 November 1972
A study was undertaken in the New York Bight in an effort to understand small scale variations of single species populations and coastal zooplankton communities as they relate to the disposal of acid wastes. Two grids of eight locations each, one day and one night station per location, were placed so that one covered the acid grounds and the other a similar area functioning as a control 9 km to the northeast. Thirty-nine taxonomic categories of zooplankton were counted from oblique net tow samples collected at the 32 stations. Biomass was determined from length measurements of individuals of 24 taxa. Species composition of the samples was typical of neritic waters of the north-east Atlantic coast. The spatial distribution of the majority of the species was markedly aggregated, but no trend was observed which would suggest that the acid wastes were an important factor in shaping the distributions. Species did not show collective agreement as to the area in which a higher average abundance for each occurred; and no significant trends in percent similarity or diversity (Simpson’s D and the information theory H’) were evident. Although Vaccaro et al. (1972) found zooplankton biomass to be approximately 30% higher from the control area than from the acid grounds, comparison of the biomass difference between the two areas on a species by species basis showed that 95% of the overall difference was accounted for by only three species, Pseudocalanus sp. and its copepodids, Calanus jinmarchicus copepodids and Temora longicornis. The acid-iron wastes appeared to be a minor factor affecting the distribution and abundance of zooplankton species during the time of this investigation. The laboratory data reported in the preceding paper (Grice et al., 1973) support this conclusion. Empirical measures of the variability of single species populations and community indices presented in the text may be useful guides for future surveys or monitoring studies.
Introduction The coastal waters of developed nations are subject to considerable inputs of solid and liquid wastes resulting from man’s activities. This is particularly true of waters such as those of the New York Bight which are located near areas of heavy industrialization and urbanization. Although ’ Contribution no. 2890 from the Woods Hole Oceanographic Institution Woods Hole, Mass. 02543, U.S.A. This study was supported in part by the National Science Foundation Grants GA 29303 and GB 27405, the Atomic Energy Commission Contract AT(I I-I)3564 (ref. no. NYO-3564-4), and NL Industries, Inc. ’ Present address: Biological Laboratories, Harvard University, Cambridge, Mass. 02138, U.S.A.
52
P. H. Wiebe et al.
the knowledge that some waste products are now severely stressing nearshore ecosystems is increasing, specific quantitative details about the nature of their influence on marine organisms and the mechanisms by which they exert their effect are generally not available. In recognition of this fact, the National Academy of Sciences, and the National Academy of Engineering (1970) jointly prepared a report outlining major problem areas and research requirements related largely to the coastal zone and to a lesser extent the world oceans. Regarding assessment of the biological status of receiving waters, this report emphasizes the need for studies of various parameters such as similarity and dissimilarity coefficients, diversity indices, toxicity bioassays and mortality and physiological response rates. The report also recognizes the need for evaluation of various components of sampling variability with respect to their effects on the above indices and also with respect to the methods of collection and the strategy of sampling. The research design of Vaccaro et al. (1972) which utilized an intensive synoptic field sampling survey of the ‘acid grounds’ and an adjoining control area in the New York Bight in combination with laboratory experiments to examine the ecological consequences of acid-waste disposal, adheres closely to the general design recommended by the above mentioned report. It was largely as a result of this design that Vaccaro et al. (1972) were able to determine that disposal of acid-iron waste in this area appeared to influence the standing crops of zooplankton, phytoplankton and benthos in minor ways. Since only the total biomass of the zooplankton collections was reported by Vaccaro et al. (1972), the possible effects of the waste on individual species collected in the field could not be determined. We have therefore counted the zooplankton in these samples collected in June 1970. Our basic objective was to understand small scale variations of single species populations in coastal zooplankton communities as they relate to disposal of acid-iron wastes and to variations in coastal populations in general. We have also compared the variations in numbers of individuals per species with variations in total biomass and examined the variability of community indices in the light of the considerable variability noted in single species populations. Methods The sampling scheme (Figure I), described in detail by Vaccaro et al. (1972, p. 234), consisted essentially of two grids of stations. One covered the acid grounds and the other a bathymetrically similar area located 9 km to the north-east. At each grid location a day and a night oblique net tow were taken from the bottom to the surface with a 70 cm diameter net (0.239 mm mesh aperture) giving a total of 32 collections. The average volume filtered during a haul was 119 m3 (range 4.4’3 to 166 m”). Samples from the 32 stations were split with a Folsom splitter (McEwan et al., 1954) usually to 1/32; samples with higher plankton concentrations were split further, to 1/64, or in one case to 1/128. Counts of the rare organisms present were made on the entire aliquot. The aliquot was then diluted to a known volume (usually 400 cm3.) Ten cm3 were removed by a piston pipette while the plankton in the aliquot were well-mixed and suspended in the liquid thus providing a 1/40 sub-sample of the aliquot. Abundant species were counted in this fraction. To test reproducibility of the sub-sampling technique, a second IO cm3 subsample was withdrawn from nine aliquots and the organisms of all species combined were counted. The totals for the two subsamples were compared. These values differed by an average of 5.4% (range 1.2 to 10+6~/~).The errors in the counts arising from subsampling the aliquot and from the aliquoting procedure itself (McEwen et al., 1954) appear small in comparison to the observed differences in species abundance between stations and between grids described below. Thirty-nine taxonomic categories were recognized and counted. The majority of organisms were identified to species level. For CuZunusJinmurchicus, Temoru Zongicornis, Tortunus discuudutus,
Acid waste affecting distribution of zooplankton
74000' 73040' Figure I. The New York Bight survey area. Zooplankton grid stations, I to 16 and 22 to 37. The dotted lines within path of a discharging barge during summer and winter.
53
73O20' samples were collected at the the acid-iron grid indicate the
Pseudocalanus sp., Centropages hamatus and C. typicus. copepodids were tallied separately from the adult. Specimens of Pseudocalanus sp. were not identified to species because of unresolved systematic problems in the genus. Although three species of Acartia were present (A. longiremus, A. tansa and A. cl&), they were lumped together as Acartia spp. because they were difficult to identify routinely. Temora longicornis adults varied significantly in size, but no species differences were detected. Sagitta &guns was the only adult chaetognath observed in the samples. It was assumed that all the juveniles were also S. elegant. One type of egg abundantly present in some of the samples contained worm-like embryos. Other identical eggs obtained from plankton tows in the New York Bight area subsequent to the June 1970 sampling, were kept alive and they hatched into chaetognaths. It was thus assumed that the eggs in samples from the grids were also chaetognaths, probably S. elegans. Brachyuran zoeae, and Cancer borealis megalopae were each considered as taxonomic groups, but the remainder of the crustacean larvae were simple grouped as ‘crustacean larvae’. Two amphipods were found, one identified as Monoculodes sp. and the other, very rare in our samples, a gammarid not identified to genus and called ‘amphipod B’. The counts were standardized to numbers per 100 m s. They were transformed to logarithms where statistical testing assumed normalized data and a variance independent of the mean, because standardized data for most species were not normally distributed. A value of I was substituted for o prior to transformation. The logarithmically transformed data did not completely satisfy the testing requirement in all cases; the consequences of this will be discussed below. The biomass contribution of 24 species in the samples was estimated by an indirect method reported by Isaacs et al. (1969) which is based on the average length of a species. Ten individuals of a species were randomly removed from each of several samples. These animals were measured
54
P. H. Wiebeet al.
according to the standard lengths used by Issacs et al. (1969) and an average obtained. The average lengths in mm were converted to their ocular scale units (0.167 mm=r unit). Their Table giving relationships of length (in ocular units) to wet weight was then used to obtain a value for the number of individuals of each species corresponding to I gram wet weight. Interpolation in the Table was done where necessary. For organisms smaller than any in the same category listed in the Table, the value corresponding to the smallest length was used. From values of numbers of individuals per gram, an estimate of the grams wet weight of a species/m3 was calculated. A total estimated wet weight at each station was calculated by summing the individual estimates for the 24 species. The proportional contribution of each species to the total biomass was then determined.
Field Results Variation
in single species populations
Some basic statistics of the species counted in the samples are given in Table I. The species are listed in order of the average abundance to indicate their relative importance in the survey area. Crustaceans, especially copepods, are numerically dominant. An average of 88% of the individuals in our samples are of two species, Pseudocalanus sp. and Temora longicornis including their copepodids. Although there is considerable variation in the exact rank order of species from station to station, the numerical dominance of a few species is exemplified by the fact that the seven most abundant species were ranked within the top ten at every station. Despite dominance and homogeneity in rank order, there is considerable heterogeneity in spatial distribution of individuals of most species over the area. Two indicators of this heterogeneity are the frequency of occurrence of species at the stations (Table I) and the index of dispersion (Fisher, 1958) which measures the degree of departure from a Poisson random distribution. Only ten species occurred at every station; 16 were present at less than half of them. While there is a strong positive regression (P
Acid waste affecting distribution of zooplankton
TABLE I. Basic statistics of taxonomic
Rank
55
groups counted. Listings
Category
Xl100 m3
I
Pseudocalanussp.’ Temora longieornis copepodids” 3 Pseudocalanussp. copepodids”
345 027 245498 241776
4
211469
2
Temora lo&cow&
5 Centropages typicus” 6 Oitkona s&nilisa 7 Sagitta elegans eggs 8 Tortanus discaudat&’ 9
Calanus ~n~~c~c~
copepodids”
IO Podon polypkemoid~a I I Centropages typicus copepodids” 12 Acartiu spp.’ 13 Sagitta elegant juveniles’ 14 Centropages kamatus” 15 Mono&odes sp” 16 Cancer borealis megalopae” 17 18
19 20 21 22 23
Brachyuran zoea’ Crustacean larvae* Gastropod larvae”
Sagitta elega& Tortanus discaudatus copepodids” Calanus finmarckicus’ Barnacle nauplii
24 Eetadne ~~dmam.a 25
Barnacle cyprids
26 Centropages kamatus copepodids’ 27 28 29 30
3I 32 33
Fish eggs Foraminifera
Neomysisamericana” Fish larvae Pelecypods Medusae Polychaeta
34 Metridia hens 35 36 37 38 39
Amphipod B Cumacea Hermit crab Echinoderm larvae Isopod
48621 38747 13072 IO742 7240 6823 6147 5622 3472
are in order of abundance
Variance W)
1010 10lO
3*0x 2*4x 1.4x 3'2X 2-8x 3*6x
10s
S'OX
IO'
1010 10'0
IO@
8.1 x IO'
52x
IO'
9*8x 108 3'5X 107 6.6 x IO?
2’9 x 106
1468
4.8x
1203
5’0 x 106
845 807 7x2 670 461 452 3'7 I99 123 1x9 1x9
110 81 74 34 28 I5 IO
4 3
2
106
4*6x 10~ r-7x 106 9'5 x IO" 2.6~ IO* 2'0 x 10s 6.4x 10~ 4-8x IO* 7'7X IOP' 1.6~ IO& 3'OX 104 1-6~10~ 2-7x 10~ 2'1
x IO4
32 32 32 32 32 32 32 30 32 13 31 24 32 16 17 32 31 30 20 31 10
31 i
21 3 23 12
x 10s
IO 18
10~
8
IO*
3.7x 2'1
Frequency of occurrence
65x 1-4x
10~
700 160 210 60
2
4 I
I I
50
2 I
20
I
I
IO
I
o Speciesused in biomasscomputation. to avoid capture during the day. It could also indicate that a large fraction of the planktonic populations were migrating down to the bottom during daylight or alternatively that the species were basically benthic with portions of populations which moved into the water column at night. Inspection of the list of species showing significant increase in abundance at night indicates the latter explanation may be appropriate for Monoculodes sp. (an amphipod), Foraminifera and possibly the crustacean larvae and brachyuran zoea, while avoidance would be a more likely explanation for fish larvae. Both factors are probably responsible for the increased abundance of the mysid ~eo~y~ algae at night (Hulbert, 1957; Clutter & Ann&u, 1968). Estimates of the variability to be expected for species in collections from similar coastal areas can be generated, providing that the data for each species are representative of coastal species in general and that these values fit the mathematical model used to develop variance estimates and
56
P. H. Wiebe et al.
TABLE z. Species with differences between means for areas or time of day significant at or P
Acid grounds
Control
area
Centvopages typicus*
Pseudocalanw
Podon palyph~o~des~
Ps~d~a~nus sp. copepodids** Sagitta elegant eggs*
Centropages typicus copepodids** Gastropod larvae* Tortanus discaudatus copopedids* * Barnacle nauplii** Fish eggs*
sp,+
Tortanus discaudatus” CaEanus$nmarchicus copepodids* Acartiu spp.** Sagitta elegans juveniles* Calanusfinmarchicus* Barnacle cyprids* Centropages haemntus copepodids**
Day Centropages typicus copepodids** Centropages hamat~s copepodids**
Night Calanus jinmarchicus copepodids** Mono~ulodes sp.* Brachyuran
zoea*
Crustacean larvae* Gastropod larvae** Foraminifera* Neomysis americana* Fish larvae**
*P
confidence limits. We used a modified form of the classical method introduced by Winsor & Clarke (1940) to determine the 95% limits of a single observation. In this procedure the analysis of variance is used on logarithmically transformed data to separate the components of variation contributing to the total error of a sample. The variance estimates of components appropriate to the error of a single observation are summed and this variance is used to construct confidence limits for the logarithms. Anti-logging provides multiplicative limits for the untransformed data. It was not necessary for us to do a separation of components via the analysis of variance. Error associated with samples from the acid grounds and control area results from large scale variations in abundance between grids, smaller scale variations between station locations within a grid, variations between day and night and variations from other sources such as net handling and counting techniques, All of these components are important to the estimate of variability of a single collection in an area. For the first 30 species in Table I, confidence limits were developed from a variance calculated from the log-transformed data (Table 3). The conversion to logarithms is intended to remove the dependence of the variance on the mean, evident in our data, and to stabilize the variance. However, for a number of species, the transformation was inappropriate and confidence limits based on transformed data were gross overestimates of the variability actually observed. In these cases, only the range of values is given. Vuriations in co~~u~it~ indices Since there was considerable variability in the abundance of species in the survey area, we examined the magnitude of variation of community oriented indices to determine how they are affected. The percent similarity index, S, is widely used to measure differences in species relative proportions between pairs of collections. Using the first 29 species in Table I, this index was computed for all possible pairs of stations. The results are summarized in Table 4. There is a small but discernible increase in similarity of species composition over the time period in which the tows were taken. The mean value for stations I to 8<9 to 16~22 to 29<30 to 37; the maximum
Acid waste aflecting distribution of zooplankton
57
TABLE 3. Confidence limits of a single observation or the range of values observed for a species in the survey area. The range is given in cases where the procedure used to calculate confidence limits was inappropriate and resulted in gross overestimates of the observed variability
95% Limits of single observation
Species
Pseadocalanus sp. Temora tongr*co?~~iscopepodids Pse&oca&?uis sp. copepodids Temora longicornis Centropages typicus Oithona similis Sag&to elegans eggs Sag&a elegans juveniles Cancer borealis megalopae
Range (no./100 ms
Species
37’2-269 %
Tortanus discaudutus
32*9-30+%
Cal~~n~r&~~~
o- 90
21*6-464%
Podon polyphemoides
50780 o- 17.5540
15.3456 % 35.7-280 % 28.9-346 % 39.8-25 1% 27.8360 %
Centropages typkus copepodids Acartia spp.
o- 37 3.50
41y24I
copepodids
%
IOO-
o-
Centropages hamatus Mono&odes sp.
e-
o-
Brachyuran wea Gastropod larvae
Barnacle cyprids Centrogogar hmnatus copepodids Fish eggs Foraminifera
Neomysis americana
stations.
5350
67.50 2030 3300 1470 4880
S” Acid grounds to 8 within day I 9 to 16 within night I I to 16 between day I and night x Control area 30 to 37 within day 2 22 to 29 within night 2 22 to 37 between day 2 and night 2 Between areas I to 8 vs. 30 to 37 between days 9 to 16 vs. 22 to 29 between nights I to 8 vs. 22 to 29 acid day I-control night 2 9 to 16 vs. 30 to 37 acid night I--control day 2
"S=too
x
(I~o-o~sx~
where P,, and P,k are the proportions is the number of species.
Range
I
z o-
1830
o-
470
590 2000 210
No. of observations
75’1 77’8 76.8
88.5-56.5 93.3-56.4 92.2-52.8
83.1 81.7 81.4
94'8-54'1 96.7-52.0
28 28 64
72.6 78.0 74'6 75'5
91.6-50.7 90*0-52.7 89.5~53.4 92.0-56.7
64 64 64 64
94‘1-70'2
P,,-pm
i=I
1830 1870
for all possible pairs of
x
I
8370
o-
4. Summary of percent similarity values (S) calculated Station numbers are chronologically sequenced
Stations
10040
oo-
o-
Fish larvae
29 630
o-
Sagitta ekgans Tortanw discaudatus copepodids oCalanus jinmarchicus oBarnacle nauplii oEvadne normandi o-
TABLE
100
28
28 64
1 I
of the ith species in thejth
and kth samples and n
P. H. Wiebe et al.
difference between means is 8*0~/~.While average similarity values are slightly higher on the control area than on the acid grounds, mean values for comparisons between the two areas arc not lower than those for the acid grounds. The variability in similarity values, as exemplified by the range for each set of comparisons (Table 4) is nearly the same both within and between areas regardless of time of day. In most cases the range of percentages for a data set extends from the low 90’s to the 50’s, excepting the low value for stations 30 to 37 of 70.2%. These ranges of similarity values are relatively large considering the small size (86 kma) of the area enclosed by each grid of stations. Another means of comparing change of community structure within and between areas is through the use of diversity indices. Two indices chosen for use here are Simpson’s index, D, and the information measure of diversity, H’ (Pielou, 1969, p. 223, 224). Both provide a single numerical value incorporating the effects of species list length and the equitability in distribution of individuals among the species. Index values computed for each station using all 39 taxonomic entities are given in Table 5 along with a measure of the equitability, ‘J, described by Pielou (1969, P. 233). Trends in diversity values are opposite to those of the percent similarity values; average diversity for a data set decreaseswith time with either measure. In this case, the mean value for stations I to 8> 9 to 16> 22 to 29> 30 to 37. Related to this sequence, the average diversity of the samples is slightly higher on the acid grounds than on the control area. However, the variability of the values within data sets is so great that a Tukey two-way analysis of variance on values of N (Tukey, 1953) indicates the trend is not significant at P=o*og level. The role each component of diversity (number of species and equitability) plays in determining the index value for a sample is illustrated by the acid grounds H’ data. The average values are essentially the same for the day and night collections. Yet the number of species caught on the average during the day (204) is considerably less than the average caught at night (26.5). This difference is offset by a marked increase in the equitability component in day as compared to night collections. A similar but less intense complementation of components is also seen in the control area. While there is little difference in mean values of either Simpson’s index or the information index between areas, the difference in variability of the values is much larger. Coefficients of variation (s/2) calculated from values of H’ for day and night sets of stations separately are: acid grounds day, 0.083 ; acid grounds night, 0.075; control area day, 0.036; control area night, 0,035. Acid grounds coefficients are approximately twice as large as those of the control area. Variations in biomass
Twenty-four species indicated by a in Table I were used in our biomass computation. S. elegans eggs, which ranked seventh in abundance, and the other species not footnoted were omitted from this analysis because the method of Isaacs et al. (1969) was not extended to these taxonomic entities. The error resulting from these omissions is minor because their biomass contribution is small due to small individual size or rarity in the collections. Regression analysis of the total estimated biomass versus the dry weight measured by Vaccaro et al. (1972) shows a strong positive relationship between these two variables (Po-IO) 1 erences in dry weight and displacement volume were while the observed significant (P
H,=;
;
i=I
~ -‘=I
= J =H’I&..
b
(I
16
13 I4 15
II 12
IO
Night 9
;:
2
~=2’54
x=2.55
2’49 2.30 2.38 2’77
2’44
2.85
2.61
2.47
Where H, 8I=log2n
23 24 25 26 27 28 29
22
Night
30 31 32 33 34 35 36 37
Day
Stations
2=25’s
23 26 25 26 25 26 26 25
X=22.4
20
21
23 23 24 23
22
23
No. species
0.521
2.42 2-57 2.43 2.51 2.29
2'51
Ea.528
0.534 0’553 0.517 0.534 0.493
0.541 0’534
kO.542
0.566 0.525 0.539 0.546 0.539 0.546 0.530 0.548
Equitability .T
2.45 2.51
x=2*46
x=2+4
2’47 2’54 2’47 2’33 2’37
2’44
2.56 2’34
Information index H
of all species and n is the number of species.
x=0*77
0.74 0.77 0.76 0.78 0.79 0.76 0.79 0.74
of the ith species and n is the total number of species.
and n is the number of species
of individuals
0.77 0.73 0.78 0.76 0.75 0.75 0.75 0.77
--h
g=o,76
D=I
Control area Simpson’s index
of the ith species, X is the total number of individuals
i&o.538
0.506 0.604
0.518 0.516
0’539 0.517 0.587 0.519
%o.587
0.558 0.578 0.592 0.607
2.14 2.64 2’53
2.41
0.615 0.539 0.591
Equitability 3
0.612
b
2’73
2.81
2.66 2.47
Where Xi is the number of individuals
%=-o.,,
0.79 0’79 0.84 0.78 0.78 0’73 0.77 0.82
ho.79
Pi log, Pi Where Pi is the proportion
X(X-1)
X,(X,-I)
x=26*5
26 24
22
24 33 29 26 28
z=20.8
18
20
0.79
0.81
22
--h
13
24 27
2
22
20
3 4
D=I
Information index H’
in survey area of New York Bight
Acid grounds Simpson’s index”
of zooplankton
0.82 0.79 0.82 0.83 0’77 0.72
No. species
I
Day
Stations
TABLE 5. Species diversity
60
P. H. Wiebe et al.
of this difficulty, the above procedure used to estimate the biomass of individual species and the total biomass at stations in the survey area is valid at least as a means of determining species most responsible for large scale fluctuations of biomass. Based on the proportional contribution of a species to the total biomass at all stations, nine species were selected as significant contributors to biomass variations in the area (Figure 2). These species accounted for an average of 96.0% of the biomass at our stations (range 87.2 to 99.5%) and multiple linear regression analyses indicated that they explained 99.86% of the variability in total wet weight (P
lo
(a)(b)(c)(d)(e)(f)(a)(h)(i)
I:
Species
Figure 2. Estimated biomass of the nine species contributing most significantly to the total zooplankton biomass in the survey area. For each species average wet weight for the acid grounds and the control area and the difference between them are given. Species are: (a) Pseudocalanus sp., (b) Temora longicornis copepodids, (c) Pseudocalanus sp. copepodids, (d) Temora longicornis, (e) Centropages typicus, (f) Oithona similis, (g) Calanus jinmarchicus copepodids, (h) Tortanus discaudatus, (i) Cancer borealis megalopa. C, Total biomass for nine species.
Acid waste affecting distribution of zooplankton
61
Figure 2. Seven of the nine species contribute towards the higher biomass on the control area. The other two species, T. longicornis copepodids and C. typicus, have a higher average biomass on the acid grounds. One species, Pseudocalanus sp. and its copepodids, accounts for 70.2% of the total biomass difference on the control area; C.finmarchicus copepodids and T. longicornis account for an additional 24’7%. Thus approximately 95% of the biomass difference between the two areas is due to changes in abundance of only three species.
Discussion Eflects of acid-waste on sooplankton The basic finding of the laboratory studies described in the preceding paper by Grice et al. (1973) was that detectable effects of acid-iron waste on copepods occurred only at combinations of concentrations of waste solution and time periods which have been demonstrated not to persist on the acid grounds. In the laboratory tests, the principal cause of copepod mortality appeared to be the acidity of the waste product rather than some toxic component in the material. Thus the laboratory experiments suggest that the mortality of zooplankton resulting from acid waste discharge is negligible because potentially lethal concentrations of low pH do not persist for sufficient time to produce a noticeable effect in the field. The field observations support this conclusion. If disposal of acid wastes was detrimental to zooplankton populations on the acid grounds, this should manifest itself in a decline in numbers or biomass, and/or a change in community indices relative to the control area. Observations of the zooplankton species and the community do not support this presumption. Species do not show a collective agreement as to the area in which a higher average abundance is observed (Table 2). Approximately half of the species show higher average abundance on the acid grounds and half on the control area. While the total wet displacement volume (ems/m*) and dry weight (mg/m*) were found by Vaccaro et al. (1972, p. 241) to be approximately 30% higher on the control area than on the acid grounds, our analysis based on a species by species computation of their biomass contribution to the total shows this difference is almost entirely accounted for by only three species, Pseudocalanus sp. and its copepodids, C.fimnarchicus copepodids, and T. Zongicornis(Figure 2). Population structure in terms of similarity in proportions of species within and between areas is nearly the same (Table 4). In addition, no significant trends of diversity indices (Simpson’s D and the information theory H’) are evident to suggest that acid discharge has been inhibitory to the maintenance of the resident plankton community (Table 3). Thus, acid-waste discharges do not appear to have a systematic effect on zooplankton numbers or biomass which is detectable at this intensity and scale of sampling. Longer term effects on developmental stages of copepods also appear negligible since concentrations of acid waste required to inhibit development do not occur for sufficient time in the receiving waters. A similar conclusion was reached by Rachor (1970) in a report on the initial effects of acid-iron waste disposal on the bottom fauna in a sea area NW of Helgoland, Federal Republic of Germany. Sea-disposal from a TiOs factory in this area began in May 1969 and after one and a half years, it was not possible to demonstrate any harmful effect due to the wastes. Assessmentand monitor&g studies The increasing use of coastal and offshore marine waters for waste disposal will lead to an increasing demand for studies to determine whether a given waste disposal operation is damaging environmental conditions. As outlined in the introduction, the research design of our study is similar in many respects to that suggested for study of biological effects of waste materials in a report
62
P. H. Wiebe et al.
entitled ‘Waste Management Concepts for the Coastal Zone’, (National Academy of Sciences, 1970, pp. 61-66). Thus, it may serve as a model for similar projects where the strategy of sampling requires employing a comparison of a receiving areas with a control area subsequently integrated with laboratory toxicity studies. Our data provide an assessmentof methods of zooplankton collection in terms of expected variability of individuals in single species populations and variability of community related indices. These empirical measures of variability should be helpful for planning research in coastal areas as large or larger than the acid grounds and control area (N 174 km2). According to our data, differences of less than a factor of 5 or IO in the abundance of a population between stations in coastal waters, when based on single observations, can be caused by sampling error. The 95% limits typical of species for which the abundance data do not deviate significantly from a log-normal distribution (Table 3) range from approximately 1/3 to 3 times to 1/6 to 6 times a single observation. For a species such as T. Zongicorniswhose 95% limits are 41.5 to 241%, a single observation of IOO individuals would yield a lower limit of 41.5 individuals and an upper limit of 241, and another observation would have to be less than the lower limit or greater than the upper limit to be considered significantly different from it. In general, the ranges given in Table 3 vary about the mean by more than a factor of six (the mean divided into the maximum observed value). Extreme values in some cases produce factors as great as 25 (for example P. polyphemoides, barnacle nauplii and N. americana). It should be emphasized that these error estimates include errors resulting from large scale differences between grids, small scale differences between stations, differences between day and night and variations from other sources such as net handling and laboratory procedures. For most species, the confidence limits are quite similar to those for oceanic and neritic zooplankton summarized by Wiebe and Holland (1968, p. 319-320). If, as suggested by Wiebe (1971, p. 37), most field sampling error results from small scale patchiness of zooplankton and if the error associated with a single tow has been minimized by optimizing net size and tow length, further reductions in error to permit detection of small differences in populations would appear possible only through replication of tows at each station. Similarity values which range in most data sets (Table 4) from the low SO’Sto the 90’s show that large fluctuations in proportions of the more numerically dominant species are common within this restricted area. Since the variations in similarity between grids are not measureably larger than within those grids, the observed variability must result from small spatial inhomogeneities in species composition over the survey area rather than from differences between the two grids. Thus, where comparison between station pairs requires an index value for discriminating between areas of high and low similarity, these data suggest an index value equal to or less than 50% would be considered a conservative level indicating significant dissimilarity in species composition. This level is considerably lower than the lowest value (79%) selected by Miller (1970, p. 733) to indicate differences in species composition. However, the levels he selected were based on a Monte Carlo computer study of the theoretical levels of variability to be expected in replicate subsample counts of a sample when the subsample size is varied. The study did not take into consideration variations resulting from patchiness of zooplankton (Wiebe, 1970). The downward bias introduced by subsampling coupled with the error resulting from patchiness (Wiebe, 1971) quite possibly explains the greater variability observed in our similarity data. Although conceptual aspects of diversity measures have been criticized (Hurlbert, I~I), their use here has been simply as another means of comparing the species composition of the acid grounds and the control area. Since species composition in our samples is similar to that of other areas in this region during winter, spring and perhaps early summer, coefficients of variation (s/X) for Simpson’s index (0.039) and the information index (0.062) may be useful empirical guides to variability expected at other shelf locations. All 32 values in Table 5 were used in the
Acid waste affecting distribution of zooplankton
63
calculation of the coefficients for each index. Confidence limits of a single observation can be calculated with these coefficients in a manner similar to that described by Wiebe (1971, p. 33). Comparison with other studies Species encountered in our samples are typical of continental shelf zooplankton communities along the eastern United States from Cape Hatteras to Cape Cod. Copepods, the most abundant group in collections from the acid grounds and control area, were the dominant group in collections from shelf waters of Block Island Sound (Deevey, Iqjza,b), off Long Island (Grice & Hart, 1962, p. 305) and Delaware Bay (Deevey, 1960). The copepod species composition in our samples was also quite similar to that of other studies. Most of the four numerically important species listed in Table I, Pseudocalanus sp., Temora longicornis, Centropages typicus and Oithona similis, were cited by the above authors and Van Engel and Eng-Chow Tan (1965, p. 184) as principal components of their collections during one or more seasons. The occurrence of Pseudocalanus sp. in the summer of 1970 as the most abundant species in our collections is a deviation from its pattern of seasonal importance as described by Deevey (1952a,b; 1960), Cronin et al. (1962) and Van Engel & Eng-Chow Tan (1965). Usually it predominates in the winter and spring becoming much less abundant or absent in the summer, especially in estuaries. However, in their July shelf samples collected off New York in depths comparable to those of the acid grounds, Grice & Hart (1962, p. 295) also found Pseudocalanus minutus was the most abundant species, particularly at inshore neritic stations. It probably occurs in the colder deeper water which is characteristic of the entire area off the New York coast in summer. Notably absent from our list of species are species such as those given by Grice & Hart (1962, p. 305) which are considered to be indicators of the penetration of slope and oceanic water into the neritic environment in late summer. The absence of these species suggests offshore water has not yet transgressed onto the acid grounds at the time of this study. According to Bumpus & Lauzier (1965), the penetration of offshore waters usually begins south of Cape Cod during the late spring and early summer. Acknowledgements We acknowledge, with pleasure, the following persons for checking our species determinations in the indicated taxa: Drs Thomas E. Bowman (Axnphipoda); Arkela Sastry (Cancer borealis); Angeles Alvarino (Chaetognatha). Mr Thomas L. Lawson provided considerable assistance with the laboratory experiments. We also wish to thank Drs Bostwick Ketchum, James Cox, Richard H. Backus and Mr Ralph Vaccaro for reading and criticizing the manuscript. References Bumpus, D. F. & Lauzier, L. M. 1965 Surface circulation on the Continental Shelf off Eastern North America between Newfoundland and Florida. Serial Atlas of the Marine Environment Folio 7 American Geographic Society. Clutter, R. I. & Anraku, M. 1968 Avoidance of Samplers. In Zooplankton Sampling 57-76 (Tranter, D. J., ed.) UNESCO Monographs on Oceanographic Methodology (2) p. 174. Cronin, L. E., Daiber, J. C. & Hulbert, E. M. 1962 Quantitative seasonal aspects of zooplankton in the Delaware River Estuary. Chesapeake Science 3, 63-93. Deevey, G. B. 1952~ A survey of the zooplankton of Block Island Sound 1943-1946. Bulletin of the Bingham Oceanographic Collection Yale University 13, 65-119. Deevey, G. B. 19526 Quantity and composition of the zooplankton of Block Island Sound, 1949. Bulletin of the Bingham Oceanographic Collection, Yale University 13, 120-164. Deevey, G. B. 1960 The zooplankton of the surface waters of the Delaware Bay region. Bulletin of the Binghum Oceanographic Collection, Yale University 17, 5-53. Fisher, R. A. 1958 Statistical Methodsfor Research Workers Hafner Publ. Co. New York, 13th edition, 356 pp.
P. H. Wiebe et al.
64
Grice, G. D. & Hart, A. D. 1962 The abundance, seasonal occurrence and distribution of the epizooplankton between New York and Bermuda. Ecological Monographs 32, 287-309. Grice, G. D., Wiebe, P. H. & Hoagland, E. 1973 Acid-iron waste as a factor affecting the distribution and abundance of zooplankton in the New York Bight. I. Laboratory studies on the effects of acid wastes on copepods. Estuarine and Coastal Marine Science I, 45-50, Hulbert, E. M. 1957 The distribution of Neomysis americana in the estuary of the Delaware River. Limnology and Oceanography 2, I- I I. Hurlbert, S. H. 1971 The nonconcept of species diversity: a critique and alternative parameters. Ecology 52, 577-586.
Isaacs, J. D., Fleminger, A. & Miller, J. K. 1969 Distributional Atlas of Zooplankton Biomass in the California Current Region: Spring and Fall 19.j-1959. CalCOFI Atlas No. IO V-XXV, I--252. McEwen, G. F., Johnson, M. W. & Folsom, T. R. 1954 A statistical analysis of the Folsom sample splitter based upon test observations. Archivfikt Meteorologie Geophysik und Bioklimatologie, Series A. G, 502-527. Miller, C. B. 1970 Some environmental consequence of vertical migration in marine zooplankton. Limnology and Oceanography 15, 727-741. National Academy of Sciences and National Academy of Engineering. 1970 Waste management concepts for the coastal zone, requirements for research and investigation. Washington, D.C. p. 126. Pielou, E. C. 1969 An introduction to Mathematical Ecology Wiley-Interscience, New York. p. 286. Rachor, E. 1970 On the influence of industrial waste containing H.&SO4 and FeSO, on the bottom fauna off Helgoland (German Bight). Paper presented to the FAO Technical Conference on Marine Pollution, Rome. Vaccaro, R. F., Grice, G. D., Rowe, G. T. & Wiebe, P. H. 1972 Acid-iron waste and the summer distribution of standing crops in the New York Bight. Water Resenrch 6, 231-256. Van Engel, W. A. & Tan, Eng-Chow. 1965 Investigations of inner continental shelf waters off lower Chesapeake Bay. Part VI. The Copepods. CheAnpeake Science 6, 183-189. Wiebe, P. H. 1970 Small scale spatial distribution in oceanic zooplankton. Limnology and Oceanography 15, 205-217.
Wiebe, P. H. 1971 A computer model study of zooplankton patchiness and its effects on sampling error. Limnology and Oceanography 16,29-38. Wiebe, P. H. & Holland, W. R. 1968 Plankton patchiness: effects on repeated net tows. Limnology and OceanogrOP~YI3~3I5-32I.
Winsor, C. P. & Clarke, G. L. Ma&e Research 3, 1-34.
1940
A statistical
study of variation
in the catch of plankton
nets. Journal
of
Acid-iron Waste as a Factor Affecting the Distribution and Abundance of Zooplankton in the New York Bight II. Spatial Variations in the Field and Implications Monitoring Studies”
for
Peter H. Wiebe, George D. Grice and Elaine Hoaglandb Woods Hole Oceanographic Institution,
Woods Hole, Mass. 02543, U.S.A.
Reckved 2 May 1972 and in revisedform 10 November 1972
A study was undertaken in the New York Bight in an effort to understand small scale variations of single species populations and coastal zooplankton communities as they relate to the disposal of acid wastes. Two grids of eight locations each, one day and one night station per location, were placed so that one covered the acid grounds and the other a similar area functioning as a control 9 km to the northeast. Thirty-nine taxonomic categories of zooplankton were counted from oblique net tow samples collected at the 32 stations. Biomass was determined from length measurements of individuals of 24 taxa. Species composition of the samples was typical of neritic waters of the north-east Atlantic coast. The spatial distribution of the majority of the species was markedly aggregated, but no trend was observed which would suggest that the acid wastes were an important factor in shaping the distributions. Species did not show collective agreement as to the area in which a higher average abundance for each occurred; and no significant trends in percent similarity or diversity (Simpson’s D and the information theory H’) were evident. Although Vaccaro et al. (1972) found zooplankton biomass to be approximately 30% higher from the control area than from the acid grounds, comparison of the biomass difference between the two areas on a species by species basis showed that 95% of the overall difference was accounted for by only three species, Pseudocalanus sp. and its copepodids, Calanus jinmarchicus copepodids and Temora longicornis. The acid-iron wastes appeared to be a minor factor affecting the distribution and abundance of zooplankton species during the time of this investigation. The laboratory data reported in the preceding paper (Grice et al., 1973) support this conclusion. Empirical measures of the variability of single species populations and community indices presented in the text may be useful guides for future surveys or monitoring studies.
Introduction The coastal waters of developed nations are subject to considerable inputs of solid and liquid wastes resulting from man’s activities. This is particularly true of waters such as those of the New York Bight which are located near areas of heavy industrialization and urbanization. Although ’ Contribution no. 2890 from the Woods Hole Oceanographic Institution Woods Hole, Mass. 02543, U.S.A. This study was supported in part by the National Science Foundation Grants GA 29303 and GB 27405, the Atomic Energy Commission Contract AT(I I-I)3564 (ref. no. NYO-3564-4), and NL Industries, Inc. ’ Present address: Biological Laboratories, Harvard University, Cambridge, Mass. 02138, U.S.A.
52
P. H. Wiebe et al.
the knowledge that some waste products are now severely stressing nearshore ecosystems is increasing, specific quantitative details about the nature of their influence on marine organisms and the mechanisms by which they exert their effect are generally not available. In recognition of this fact, the National Academy of Sciences, and the National Academy of Engineering (1970) jointly prepared a report outlining major problem areas and research requirements related largely to the coastal zone and to a lesser extent the world oceans. Regarding assessment of the biological status of receiving waters, this report emphasizes the need for studies of various parameters such as similarity and dissimilarity coefficients, diversity indices, toxicity bioassays and mortality and physiological response rates. The report also recognizes the need for evaluation of various components of sampling variability with respect to their effects on the above indices and also with respect to the methods of collection and the strategy of sampling. The research design of Vaccaro et al. (1972) which utilized an intensive synoptic field sampling survey of the ‘acid grounds’ and an adjoining control area in the New York Bight in combination with laboratory experiments to examine the ecological consequences of acid-waste disposal, adheres closely to the general design recommended by the above mentioned report. It was largely as a result of this design that Vaccaro et al. (1972) were able to determine that disposal of acid-iron waste in this area appeared to influence the standing crops of zooplankton, phytoplankton and benthos in minor ways. Since only the total biomass of the zooplankton collections was reported by Vaccaro et al. (1972), the possible effects of the waste on individual species collected in the field could not be determined. We have therefore counted the zooplankton in these samples collected in June 1970. Our basic objective was to understand small scale variations of single species populations in coastal zooplankton communities as they relate to disposal of acid-iron wastes and to variations in coastal populations in general. We have also compared the variations in numbers of individuals per species with variations in total biomass and examined the variability of community indices in the light of the considerable variability noted in single species populations. Methods The sampling scheme (Figure I), described in detail by Vaccaro et al. (1972, p. 234), consisted essentially of two grids of stations. One covered the acid grounds and the other a bathymetrically similar area located 9 km to the north-east. At each grid location a day and a night oblique net tow were taken from the bottom to the surface with a 70 cm diameter net (0.239 mm mesh aperture) giving a total of 32 collections. The average volume filtered during a haul was 119 m3 (range 4.4’3 to 166 m”). Samples from the 32 stations were split with a Folsom splitter (McEwan et al., 1954) usually to 1/32; samples with higher plankton concentrations were split further, to 1/64, or in one case to 1/128. Counts of the rare organisms present were made on the entire aliquot. The aliquot was then diluted to a known volume (usually 400 cm3.) Ten cm3 were removed by a piston pipette while the plankton in the aliquot were well-mixed and suspended in the liquid thus providing a 1/40 sub-sample of the aliquot. Abundant species were counted in this fraction. To test reproducibility of the sub-sampling technique, a second IO cm3 subsample was withdrawn from nine aliquots and the organisms of all species combined were counted. The totals for the two subsamples were compared. These values differed by an average of 5.4% (range 1.2 to 10+6~/~).The errors in the counts arising from subsampling the aliquot and from the aliquoting procedure itself (McEwen et al., 1954) appear small in comparison to the observed differences in species abundance between stations and between grids described below. Thirty-nine taxonomic categories were recognized and counted. The majority of organisms were identified to species level. For CuZunusJinmurchicus, Temoru Zongicornis, Tortunus discuudutus,
Acid waste affecting distribution of zooplankton
74000' 73040' Figure I. The New York Bight survey area. Zooplankton grid stations, I to 16 and 22 to 37. The dotted lines within path of a discharging barge during summer and winter.
53
73O20' samples were collected at the the acid-iron grid indicate the
Pseudocalanus sp., Centropages hamatus and C. typicus. copepodids were tallied separately from the adult. Specimens of Pseudocalanus sp. were not identified to species because of unresolved systematic problems in the genus. Although three species of Acartia were present (A. longiremus, A. tansa and A. cl&), they were lumped together as Acartia spp. because they were difficult to identify routinely. Temora longicornis adults varied significantly in size, but no species differences were detected. Sagitta &guns was the only adult chaetognath observed in the samples. It was assumed that all the juveniles were also S. elegant. One type of egg abundantly present in some of the samples contained worm-like embryos. Other identical eggs obtained from plankton tows in the New York Bight area subsequent to the June 1970 sampling, were kept alive and they hatched into chaetognaths. It was thus assumed that the eggs in samples from the grids were also chaetognaths, probably S. elegans. Brachyuran zoeae, and Cancer borealis megalopae were each considered as taxonomic groups, but the remainder of the crustacean larvae were simple grouped as ‘crustacean larvae’. Two amphipods were found, one identified as Monoculodes sp. and the other, very rare in our samples, a gammarid not identified to genus and called ‘amphipod B’. The counts were standardized to numbers per 100 m s. They were transformed to logarithms where statistical testing assumed normalized data and a variance independent of the mean, because standardized data for most species were not normally distributed. A value of I was substituted for o prior to transformation. The logarithmically transformed data did not completely satisfy the testing requirement in all cases; the consequences of this will be discussed below. The biomass contribution of 24 species in the samples was estimated by an indirect method reported by Isaacs et al. (1969) which is based on the average length of a species. Ten individuals of a species were randomly removed from each of several samples. These animals were measured
54
P. H. Wiebeet al.
according to the standard lengths used by Issacs et al. (1969) and an average obtained. The average lengths in mm were converted to their ocular scale units (0.167 mm=r unit). Their Table giving relationships of length (in ocular units) to wet weight was then used to obtain a value for the number of individuals of each species corresponding to I gram wet weight. Interpolation in the Table was done where necessary. For organisms smaller than any in the same category listed in the Table, the value corresponding to the smallest length was used. From values of numbers of individuals per gram, an estimate of the grams wet weight of a species/m3 was calculated. A total estimated wet weight at each station was calculated by summing the individual estimates for the 24 species. The proportional contribution of each species to the total biomass was then determined.
Field Results Variation
in single species populations
Some basic statistics of the species counted in the samples are given in Table I. The species are listed in order of the average abundance to indicate their relative importance in the survey area. Crustaceans, especially copepods, are numerically dominant. An average of 88% of the individuals in our samples are of two species, Pseudocalanus sp. and Temora longicornis including their copepodids. Although there is considerable variation in the exact rank order of species from station to station, the numerical dominance of a few species is exemplified by the fact that the seven most abundant species were ranked within the top ten at every station. Despite dominance and homogeneity in rank order, there is considerable heterogeneity in spatial distribution of individuals of most species over the area. Two indicators of this heterogeneity are the frequency of occurrence of species at the stations (Table I) and the index of dispersion (Fisher, 1958) which measures the degree of departure from a Poisson random distribution. Only ten species occurred at every station; 16 were present at less than half of them. While there is a strong positive regression (P
Acid waste affecting distribution of zooplankton
TABLE I. Basic statistics of taxonomic
Rank
55
groups counted. Listings
Category
Xl100 m3
I
Pseudocalanussp.’ Temora longieornis copepodids” 3 Pseudocalanussp. copepodids”
345 027 245498 241776
4
211469
2
Temora lo&cow&
5 Centropages typicus” 6 Oitkona s&nilisa 7 Sagitta elegans eggs 8 Tortanus discaudat&’ 9
Calanus ~n~~c~c~
copepodids”
IO Podon polypkemoid~a I I Centropages typicus copepodids” 12 Acartiu spp.’ 13 Sagitta elegant juveniles’ 14 Centropages kamatus” 15 Mono&odes sp” 16 Cancer borealis megalopae” 17 18
19 20 21 22 23
Brachyuran zoea’ Crustacean larvae* Gastropod larvae”
Sagitta elega& Tortanus discaudatus copepodids” Calanus finmarckicus’ Barnacle nauplii
24 Eetadne ~~dmam.a 25
Barnacle cyprids
26 Centropages kamatus copepodids’ 27 28 29 30
3I 32 33
Fish eggs Foraminifera
Neomysisamericana” Fish larvae Pelecypods Medusae Polychaeta
34 Metridia hens 35 36 37 38 39
Amphipod B Cumacea Hermit crab Echinoderm larvae Isopod
48621 38747 13072 IO742 7240 6823 6147 5622 3472
are in order of abundance
Variance W)
1010 10lO
3*0x 2*4x 1.4x 3'2X 2-8x 3*6x
10s
S'OX
IO'
1010 10'0
IO@
8.1 x IO'
52x
IO'
9*8x 108 3'5X 107 6.6 x IO?
2’9 x 106
1468
4.8x
1203
5’0 x 106
845 807 7x2 670 461 452 3'7 I99 123 1x9 1x9
110 81 74 34 28 I5 IO
4 3
2
106
4*6x 10~ r-7x 106 9'5 x IO" 2.6~ IO* 2'0 x 10s 6.4x 10~ 4-8x IO* 7'7X IOP' 1.6~ IO& 3'OX 104 1-6~10~ 2-7x 10~ 2'1
x IO4
32 32 32 32 32 32 32 30 32 13 31 24 32 16 17 32 31 30 20 31 10
31 i
21 3 23 12
x 10s
IO 18
10~
8
IO*
3.7x 2'1
Frequency of occurrence
65x 1-4x
10~
700 160 210 60
2
4 I
I I
50
2 I
20
I
I
IO
I
o Speciesused in biomasscomputation. to avoid capture during the day. It could also indicate that a large fraction of the planktonic populations were migrating down to the bottom during daylight or alternatively that the species were basically benthic with portions of populations which moved into the water column at night. Inspection of the list of species showing significant increase in abundance at night indicates the latter explanation may be appropriate for Monoculodes sp. (an amphipod), Foraminifera and possibly the crustacean larvae and brachyuran zoea, while avoidance would be a more likely explanation for fish larvae. Both factors are probably responsible for the increased abundance of the mysid ~eo~y~ algae at night (Hulbert, 1957; Clutter & Ann&u, 1968). Estimates of the variability to be expected for species in collections from similar coastal areas can be generated, providing that the data for each species are representative of coastal species in general and that these values fit the mathematical model used to develop variance estimates and
56
P. H. Wiebe et al.
TABLE z. Species with differences between means for areas or time of day significant at or P
Acid grounds
Control
area
Centvopages typicus*
Pseudocalanw
Podon palyph~o~des~
Ps~d~a~nus sp. copepodids** Sagitta elegant eggs*
Centropages typicus copepodids** Gastropod larvae* Tortanus discaudatus copopedids* * Barnacle nauplii** Fish eggs*
sp,+
Tortanus discaudatus” CaEanus$nmarchicus copepodids* Acartiu spp.** Sagitta elegans juveniles* Calanusfinmarchicus* Barnacle cyprids* Centropages haemntus copepodids**
Day Centropages typicus copepodids** Centropages hamat~s copepodids**
Night Calanus jinmarchicus copepodids** Mono~ulodes sp.* Brachyuran
zoea*
Crustacean larvae* Gastropod larvae** Foraminifera* Neomysis americana* Fish larvae**
*P
confidence limits. We used a modified form of the classical method introduced by Winsor & Clarke (1940) to determine the 95% limits of a single observation. In this procedure the analysis of variance is used on logarithmically transformed data to separate the components of variation contributing to the total error of a sample. The variance estimates of components appropriate to the error of a single observation are summed and this variance is used to construct confidence limits for the logarithms. Anti-logging provides multiplicative limits for the untransformed data. It was not necessary for us to do a separation of components via the analysis of variance. Error associated with samples from the acid grounds and control area results from large scale variations in abundance between grids, smaller scale variations between station locations within a grid, variations between day and night and variations from other sources such as net handling and counting techniques, All of these components are important to the estimate of variability of a single collection in an area. For the first 30 species in Table I, confidence limits were developed from a variance calculated from the log-transformed data (Table 3). The conversion to logarithms is intended to remove the dependence of the variance on the mean, evident in our data, and to stabilize the variance. However, for a number of species, the transformation was inappropriate and confidence limits based on transformed data were gross overestimates of the variability actually observed. In these cases, only the range of values is given. Vuriations in co~~u~it~ indices Since there was considerable variability in the abundance of species in the survey area, we examined the magnitude of variation of community oriented indices to determine how they are affected. The percent similarity index, S, is widely used to measure differences in species relative proportions between pairs of collections. Using the first 29 species in Table I, this index was computed for all possible pairs of stations. The results are summarized in Table 4. There is a small but discernible increase in similarity of species composition over the time period in which the tows were taken. The mean value for stations I to 8<9 to 16~22 to 29<30 to 37; the maximum
Acid waste aflecting distribution of zooplankton
57
TABLE 3. Confidence limits of a single observation or the range of values observed for a species in the survey area. The range is given in cases where the procedure used to calculate confidence limits was inappropriate and resulted in gross overestimates of the observed variability
95% Limits of single observation
Species
Pseadocalanus sp. Temora tongr*co?~~iscopepodids Pse&oca&?uis sp. copepodids Temora longicornis Centropages typicus Oithona similis Sag&to elegans eggs Sag&a elegans juveniles Cancer borealis megalopae
Range (no./100 ms
Species
37’2-269 %
Tortanus discaudutus
32*9-30+%
Cal~~n~r&~~~
o- 90
21*6-464%
Podon polyphemoides
50780 o- 17.5540
15.3456 % 35.7-280 % 28.9-346 % 39.8-25 1% 27.8360 %
Centropages typkus copepodids Acartia spp.
o- 37 3.50
41y24I
copepodids
%
IOO-
o-
Centropages hamatus Mono&odes sp.
e-
o-
Brachyuran wea Gastropod larvae
Barnacle cyprids Centrogogar hmnatus copepodids Fish eggs Foraminifera
Neomysis americana
stations.
5350
67.50 2030 3300 1470 4880
S” Acid grounds to 8 within day I 9 to 16 within night I I to 16 between day I and night x Control area 30 to 37 within day 2 22 to 29 within night 2 22 to 37 between day 2 and night 2 Between areas I to 8 vs. 30 to 37 between days 9 to 16 vs. 22 to 29 between nights I to 8 vs. 22 to 29 acid day I-control night 2 9 to 16 vs. 30 to 37 acid night I--control day 2
"S=too
x
(I~o-o~sx~
where P,, and P,k are the proportions is the number of species.
Range
I
z o-
1830
o-
470
590 2000 210
No. of observations
75’1 77’8 76.8
88.5-56.5 93.3-56.4 92.2-52.8
83.1 81.7 81.4
94'8-54'1 96.7-52.0
28 28 64
72.6 78.0 74'6 75'5
91.6-50.7 90*0-52.7 89.5~53.4 92.0-56.7
64 64 64 64
94‘1-70'2
P,,-pm
i=I
1830 1870
for all possible pairs of
x
I
8370
o-
4. Summary of percent similarity values (S) calculated Station numbers are chronologically sequenced
Stations
10040
oo-
o-
Fish larvae
29 630
o-
Sagitta ekgans Tortanw discaudatus copepodids oCalanus jinmarchicus oBarnacle nauplii oEvadne normandi o-
TABLE
100
28
28 64
1 I
of the ith species in thejth
and kth samples and n
P. H. Wiebe et al.
difference between means is 8*0~/~.While average similarity values are slightly higher on the control area than on the acid grounds, mean values for comparisons between the two areas arc not lower than those for the acid grounds. The variability in similarity values, as exemplified by the range for each set of comparisons (Table 4) is nearly the same both within and between areas regardless of time of day. In most cases the range of percentages for a data set extends from the low 90’s to the 50’s, excepting the low value for stations 30 to 37 of 70.2%. These ranges of similarity values are relatively large considering the small size (86 kma) of the area enclosed by each grid of stations. Another means of comparing change of community structure within and between areas is through the use of diversity indices. Two indices chosen for use here are Simpson’s index, D, and the information measure of diversity, H’ (Pielou, 1969, p. 223, 224). Both provide a single numerical value incorporating the effects of species list length and the equitability in distribution of individuals among the species. Index values computed for each station using all 39 taxonomic entities are given in Table 5 along with a measure of the equitability, ‘J, described by Pielou (1969, P. 233). Trends in diversity values are opposite to those of the percent similarity values; average diversity for a data set decreaseswith time with either measure. In this case, the mean value for stations I to 8> 9 to 16> 22 to 29> 30 to 37. Related to this sequence, the average diversity of the samples is slightly higher on the acid grounds than on the control area. However, the variability of the values within data sets is so great that a Tukey two-way analysis of variance on values of N (Tukey, 1953) indicates the trend is not significant at P=o*og level. The role each component of diversity (number of species and equitability) plays in determining the index value for a sample is illustrated by the acid grounds H’ data. The average values are essentially the same for the day and night collections. Yet the number of species caught on the average during the day (204) is considerably less than the average caught at night (26.5). This difference is offset by a marked increase in the equitability component in day as compared to night collections. A similar but less intense complementation of components is also seen in the control area. While there is little difference in mean values of either Simpson’s index or the information index between areas, the difference in variability of the values is much larger. Coefficients of variation (s/2) calculated from values of H’ for day and night sets of stations separately are: acid grounds day, 0.083 ; acid grounds night, 0.075; control area day, 0.036; control area night, 0,035. Acid grounds coefficients are approximately twice as large as those of the control area. Variations in biomass
Twenty-four species indicated by a in Table I were used in our biomass computation. S. elegans eggs, which ranked seventh in abundance, and the other species not footnoted were omitted from this analysis because the method of Isaacs et al. (1969) was not extended to these taxonomic entities. The error resulting from these omissions is minor because their biomass contribution is small due to small individual size or rarity in the collections. Regression analysis of the total estimated biomass versus the dry weight measured by Vaccaro et al. (1972) shows a strong positive relationship between these two variables (P
H,=;
;
i=I
~ -‘=I
= J =H’I&..
b
(I
16
13 I4 15
II 12
IO
Night 9
;:
2
~=2’54
x=2.55
2’49 2.30 2.38 2’77
2’44
2.85
2.61
2.47
Where H, 8I=log2n
23 24 25 26 27 28 29
22
Night
30 31 32 33 34 35 36 37
Day
Stations
2=25’s
23 26 25 26 25 26 26 25
X=22.4
20
21
23 23 24 23
22
23
No. species
0.521
2.42 2-57 2.43 2.51 2.29
2'51
Ea.528
0.534 0’553 0.517 0.534 0.493
0.541 0’534
kO.542
0.566 0.525 0.539 0.546 0.539 0.546 0.530 0.548
Equitability .T
2.45 2.51
x=2*46
x=2+4
2’47 2’54 2’47 2’33 2’37
2’44
2.56 2’34
Information index H
of all species and n is the number of species.
x=0*77
0.74 0.77 0.76 0.78 0.79 0.76 0.79 0.74
of the ith species and n is the total number of species.
and n is the number of species
of individuals
0.77 0.73 0.78 0.76 0.75 0.75 0.75 0.77
--h
g=o,76
D=I
Control area Simpson’s index
of the ith species, X is the total number of individuals
i&o.538
0.506 0.604
0.518 0.516
0’539 0.517 0.587 0.519
%o.587
0.558 0.578 0.592 0.607
2.14 2.64 2’53
2.41
0.615 0.539 0.591
Equitability 3
0.612
b
2’73
2.81
2.66 2.47
Where Xi is the number of individuals
%=-o.,,
0.79 0’79 0.84 0.78 0.78 0’73 0.77 0.82
ho.79
Pi log, Pi Where Pi is the proportion
X(X-1)
X,(X,-I)
x=26*5
26 24
22
24 33 29 26 28
z=20.8
18
20
0.79
0.81
22
--h
13
24 27
2
22
20
3 4
D=I
Information index H’
in survey area of New York Bight
Acid grounds Simpson’s index”
of zooplankton
0.82 0.79 0.82 0.83 0’77 0.72
No. species
I
Day
Stations
TABLE 5. Species diversity
60
P. H. Wiebe et al.
of this difficulty, the above procedure used to estimate the biomass of individual species and the total biomass at stations in the survey area is valid at least as a means of determining species most responsible for large scale fluctuations of biomass. Based on the proportional contribution of a species to the total biomass at all stations, nine species were selected as significant contributors to biomass variations in the area (Figure 2). These species accounted for an average of 96.0% of the biomass at our stations (range 87.2 to 99.5%) and multiple linear regression analyses indicated that they explained 99.86% of the variability in total wet weight (P
lo
(a)(b)(c)(d)(e)(f)(a)(h)(i)
I:
Species
Figure 2. Estimated biomass of the nine species contributing most significantly to the total zooplankton biomass in the survey area. For each species average wet weight for the acid grounds and the control area and the difference between them are given. Species are: (a) Pseudocalanus sp., (b) Temora longicornis copepodids, (c) Pseudocalanus sp. copepodids, (d) Temora longicornis, (e) Centropages typicus, (f) Oithona similis, (g) Calanus jinmarchicus copepodids, (h) Tortanus discaudatus, (i) Cancer borealis megalopa. C, Total biomass for nine species.
Acid waste affecting distribution of zooplankton
61
Figure 2. Seven of the nine species contribute towards the higher biomass on the control area. The other two species, T. longicornis copepodids and C. typicus, have a higher average biomass on the acid grounds. One species, Pseudocalanus sp. and its copepodids, accounts for 70.2% of the total biomass difference on the control area; C.finmarchicus copepodids and T. longicornis account for an additional 24’7%. Thus approximately 95% of the biomass difference between the two areas is due to changes in abundance of only three species.
Discussion Eflects of acid-waste on sooplankton The basic finding of the laboratory studies described in the preceding paper by Grice et al. (1973) was that detectable effects of acid-iron waste on copepods occurred only at combinations of concentrations of waste solution and time periods which have been demonstrated not to persist on the acid grounds. In the laboratory tests, the principal cause of copepod mortality appeared to be the acidity of the waste product rather than some toxic component in the material. Thus the laboratory experiments suggest that the mortality of zooplankton resulting from acid waste discharge is negligible because potentially lethal concentrations of low pH do not persist for sufficient time to produce a noticeable effect in the field. The field observations support this conclusion. If disposal of acid wastes was detrimental to zooplankton populations on the acid grounds, this should manifest itself in a decline in numbers or biomass, and/or a change in community indices relative to the control area. Observations of the zooplankton species and the community do not support this presumption. Species do not show a collective agreement as to the area in which a higher average abundance is observed (Table 2). Approximately half of the species show higher average abundance on the acid grounds and half on the control area. While the total wet displacement volume (ems/m*) and dry weight (mg/m*) were found by Vaccaro et al. (1972, p. 241) to be approximately 30% higher on the control area than on the acid grounds, our analysis based on a species by species computation of their biomass contribution to the total shows this difference is almost entirely accounted for by only three species, Pseudocalanus sp. and its copepodids, C.fimnarchicus copepodids, and T. Zongicornis(Figure 2). Population structure in terms of similarity in proportions of species within and between areas is nearly the same (Table 4). In addition, no significant trends of diversity indices (Simpson’s D and the information theory H’) are evident to suggest that acid discharge has been inhibitory to the maintenance of the resident plankton community (Table 3). Thus, acid-waste discharges do not appear to have a systematic effect on zooplankton numbers or biomass which is detectable at this intensity and scale of sampling. Longer term effects on developmental stages of copepods also appear negligible since concentrations of acid waste required to inhibit development do not occur for sufficient time in the receiving waters. A similar conclusion was reached by Rachor (1970) in a report on the initial effects of acid-iron waste disposal on the bottom fauna in a sea area NW of Helgoland, Federal Republic of Germany. Sea-disposal from a TiOs factory in this area began in May 1969 and after one and a half years, it was not possible to demonstrate any harmful effect due to the wastes. Assessmentand monitor&g studies The increasing use of coastal and offshore marine waters for waste disposal will lead to an increasing demand for studies to determine whether a given waste disposal operation is damaging environmental conditions. As outlined in the introduction, the research design of our study is similar in many respects to that suggested for study of biological effects of waste materials in a report
62
P. H. Wiebe et al.
entitled ‘Waste Management Concepts for the Coastal Zone’, (National Academy of Sciences, 1970, pp. 61-66). Thus, it may serve as a model for similar projects where the strategy of sampling requires employing a comparison of a receiving areas with a control area subsequently integrated with laboratory toxicity studies. Our data provide an assessmentof methods of zooplankton collection in terms of expected variability of individuals in single species populations and variability of community related indices. These empirical measures of variability should be helpful for planning research in coastal areas as large or larger than the acid grounds and control area (N 174 km2). According to our data, differences of less than a factor of 5 or IO in the abundance of a population between stations in coastal waters, when based on single observations, can be caused by sampling error. The 95% limits typical of species for which the abundance data do not deviate significantly from a log-normal distribution (Table 3) range from approximately 1/3 to 3 times to 1/6 to 6 times a single observation. For a species such as T. Zongicorniswhose 95% limits are 41.5 to 241%, a single observation of IOO individuals would yield a lower limit of 41.5 individuals and an upper limit of 241, and another observation would have to be less than the lower limit or greater than the upper limit to be considered significantly different from it. In general, the ranges given in Table 3 vary about the mean by more than a factor of six (the mean divided into the maximum observed value). Extreme values in some cases produce factors as great as 25 (for example P. polyphemoides, barnacle nauplii and N. americana). It should be emphasized that these error estimates include errors resulting from large scale differences between grids, small scale differences between stations, differences between day and night and variations from other sources such as net handling and laboratory procedures. For most species, the confidence limits are quite similar to those for oceanic and neritic zooplankton summarized by Wiebe and Holland (1968, p. 319-320). If, as suggested by Wiebe (1971, p. 37), most field sampling error results from small scale patchiness of zooplankton and if the error associated with a single tow has been minimized by optimizing net size and tow length, further reductions in error to permit detection of small differences in populations would appear possible only through replication of tows at each station. Similarity values which range in most data sets (Table 4) from the low SO’Sto the 90’s show that large fluctuations in proportions of the more numerically dominant species are common within this restricted area. Since the variations in similarity between grids are not measureably larger than within those grids, the observed variability must result from small spatial inhomogeneities in species composition over the survey area rather than from differences between the two grids. Thus, where comparison between station pairs requires an index value for discriminating between areas of high and low similarity, these data suggest an index value equal to or less than 50% would be considered a conservative level indicating significant dissimilarity in species composition. This level is considerably lower than the lowest value (79%) selected by Miller (1970, p. 733) to indicate differences in species composition. However, the levels he selected were based on a Monte Carlo computer study of the theoretical levels of variability to be expected in replicate subsample counts of a sample when the subsample size is varied. The study did not take into consideration variations resulting from patchiness of zooplankton (Wiebe, 1970). The downward bias introduced by subsampling coupled with the error resulting from patchiness (Wiebe, 1971) quite possibly explains the greater variability observed in our similarity data. Although conceptual aspects of diversity measures have been criticized (Hurlbert, I~I), their use here has been simply as another means of comparing the species composition of the acid grounds and the control area. Since species composition in our samples is similar to that of other areas in this region during winter, spring and perhaps early summer, coefficients of variation (s/X) for Simpson’s index (0.039) and the information index (0.062) may be useful empirical guides to variability expected at other shelf locations. All 32 values in Table 5 were used in the
Acid waste affecting distribution of zooplankton
63
calculation of the coefficients for each index. Confidence limits of a single observation can be calculated with these coefficients in a manner similar to that described by Wiebe (1971, p. 33). Comparison with other studies Species encountered in our samples are typical of continental shelf zooplankton communities along the eastern United States from Cape Hatteras to Cape Cod. Copepods, the most abundant group in collections from the acid grounds and control area, were the dominant group in collections from shelf waters of Block Island Sound (Deevey, Iqjza,b), off Long Island (Grice & Hart, 1962, p. 305) and Delaware Bay (Deevey, 1960). The copepod species composition in our samples was also quite similar to that of other studies. Most of the four numerically important species listed in Table I, Pseudocalanus sp., Temora longicornis, Centropages typicus and Oithona similis, were cited by the above authors and Van Engel and Eng-Chow Tan (1965, p. 184) as principal components of their collections during one or more seasons. The occurrence of Pseudocalanus sp. in the summer of 1970 as the most abundant species in our collections is a deviation from its pattern of seasonal importance as described by Deevey (1952a,b; 1960), Cronin et al. (1962) and Van Engel & Eng-Chow Tan (1965). Usually it predominates in the winter and spring becoming much less abundant or absent in the summer, especially in estuaries. However, in their July shelf samples collected off New York in depths comparable to those of the acid grounds, Grice & Hart (1962, p. 295) also found Pseudocalanus minutus was the most abundant species, particularly at inshore neritic stations. It probably occurs in the colder deeper water which is characteristic of the entire area off the New York coast in summer. Notably absent from our list of species are species such as those given by Grice & Hart (1962, p. 305) which are considered to be indicators of the penetration of slope and oceanic water into the neritic environment in late summer. The absence of these species suggests offshore water has not yet transgressed onto the acid grounds at the time of this study. According to Bumpus & Lauzier (1965), the penetration of offshore waters usually begins south of Cape Cod during the late spring and early summer. Acknowledgements We acknowledge, with pleasure, the following persons for checking our species determinations in the indicated taxa: Drs Thomas E. Bowman (Axnphipoda); Arkela Sastry (Cancer borealis); Angeles Alvarino (Chaetognatha). Mr Thomas L. Lawson provided considerable assistance with the laboratory experiments. We also wish to thank Drs Bostwick Ketchum, James Cox, Richard H. Backus and Mr Ralph Vaccaro for reading and criticizing the manuscript. References Bumpus, D. F. & Lauzier, L. M. 1965 Surface circulation on the Continental Shelf off Eastern North America between Newfoundland and Florida. Serial Atlas of the Marine Environment Folio 7 American Geographic Society. Clutter, R. I. & Anraku, M. 1968 Avoidance of Samplers. In Zooplankton Sampling 57-76 (Tranter, D. J., ed.) UNESCO Monographs on Oceanographic Methodology (2) p. 174. Cronin, L. E., Daiber, J. C. & Hulbert, E. M. 1962 Quantitative seasonal aspects of zooplankton in the Delaware River Estuary. Chesapeake Science 3, 63-93. Deevey, G. B. 1952~ A survey of the zooplankton of Block Island Sound 1943-1946. Bulletin of the Bingham Oceanographic Collection Yale University 13, 65-119. Deevey, G. B. 19526 Quantity and composition of the zooplankton of Block Island Sound, 1949. Bulletin of the Bingham Oceanographic Collection, Yale University 13, 120-164. Deevey, G. B. 1960 The zooplankton of the surface waters of the Delaware Bay region. Bulletin of the Binghum Oceanographic Collection, Yale University 17, 5-53. Fisher, R. A. 1958 Statistical Methodsfor Research Workers Hafner Publ. Co. New York, 13th edition, 356 pp.
P. H. Wiebe et al.
64
Grice, G. D. & Hart, A. D. 1962 The abundance, seasonal occurrence and distribution of the epizooplankton between New York and Bermuda. Ecological Monographs 32, 287-309. Grice, G. D., Wiebe, P. H. & Hoagland, E. 1973 Acid-iron waste as a factor affecting the distribution and abundance of zooplankton in the New York Bight. I. Laboratory studies on the effects of acid wastes on copepods. Estuarine and Coastal Marine Science I, 45-50, Hulbert, E. M. 1957 The distribution of Neomysis americana in the estuary of the Delaware River. Limnology and Oceanography 2, I- I I. Hurlbert, S. H. 1971 The nonconcept of species diversity: a critique and alternative parameters. Ecology 52, 577-586.
Isaacs, J. D., Fleminger, A. & Miller, J. K. 1969 Distributional Atlas of Zooplankton Biomass in the California Current Region: Spring and Fall 19.j-1959. CalCOFI Atlas No. IO V-XXV, I--252. McEwen, G. F., Johnson, M. W. & Folsom, T. R. 1954 A statistical analysis of the Folsom sample splitter based upon test observations. Archivfikt Meteorologie Geophysik und Bioklimatologie, Series A. G, 502-527. Miller, C. B. 1970 Some environmental consequence of vertical migration in marine zooplankton. Limnology and Oceanography 15, 727-741. National Academy of Sciences and National Academy of Engineering. 1970 Waste management concepts for the coastal zone, requirements for research and investigation. Washington, D.C. p. 126. Pielou, E. C. 1969 An introduction to Mathematical Ecology Wiley-Interscience, New York. p. 286. Rachor, E. 1970 On the influence of industrial waste containing H.&SO4 and FeSO, on the bottom fauna off Helgoland (German Bight). Paper presented to the FAO Technical Conference on Marine Pollution, Rome. Vaccaro, R. F., Grice, G. D., Rowe, G. T. & Wiebe, P. H. 1972 Acid-iron waste and the summer distribution of standing crops in the New York Bight. Water Resenrch 6, 231-256. Van Engel, W. A. & Tan, Eng-Chow. 1965 Investigations of inner continental shelf waters off lower Chesapeake Bay. Part VI. The Copepods. CheAnpeake Science 6, 183-189. Wiebe, P. H. 1970 Small scale spatial distribution in oceanic zooplankton. Limnology and Oceanography 15, 205-217.
Wiebe, P. H. 1971 A computer model study of zooplankton patchiness and its effects on sampling error. Limnology and Oceanography 16,29-38. Wiebe, P. H. & Holland, W. R. 1968 Plankton patchiness: effects on repeated net tows. Limnology and OceanogrOP~YI3~3I5-32I.
Winsor, C. P. & Clarke, G. L. Ma&e Research 3, 1-34.
1940
A statistical
study of variation
in the catch of plankton
nets. Journal
of