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The Loch Eil project: Population fluctuations in the macrobenthos
305
J. exp. mar. Biol. Ecol., 1982, Vol. 56, pp. 305-321
Elsevier Biomedical Press
THE LOCH EIL PROJECT:
POPULATION
FLUCTUATIONS
IN THE MACROBENTHOS
T. H. PEARSON, G. DUNCAN and J. NUTTALL Scottish Marine Biological Association. DunstaSfnage Marine Research Laboratory, Oban, Argyli, Scotland
Abstract: Population fluctuations in the macrobenthic
fauna at three stations in Loch Eil and at a control station in the Lynn of Lorne were followed by monthly sampling over 1 yr. Populations of relatively low density but high species numbers and size range occurred at the control station where the fluctuations over the year were small. In the deep basin of Loch Eil the populations were much less diverse and fluctuated considerably from month to month. These fluctuations followed changes in the carbon input to the Loch and subsequent changes in the chemistry and microbiology of the sediments. A time lag of 46 wk was observed between an increased carbon input to the sediments and a subsequent increase in the numbers of small deposit-feeding annelids. Increases in populations of carnivores took place after a further 8-10 wk and coincided with a decline in deposit-feeding populations. At the head of the Loch where carbon inputs were lower population structure was intermediate between the diverse situation at the control station and the opportunist dominated populations of the deep basin. In this area populations of larger surface deposit-feeding species fluctuated apparently in response to a change in carbon input after an interval of z 12-14 wk.
Population changes in the macrobenthic fauna of Loch Linnhe and Loch Eil have been monitored continuously from 1963 (Pearson 1970; 1971a,b, 1975) with a minimum biannual sampling frequency. Observed changes have been related primarily to fluctuations in the input of effluent material to the loch system from the pulp and paper mill at Annat Point. High input levels have resulted in fauna1 dominance by small rapidly breeding (opportunistic) annelid species in place of the more usual complex communities of molluscs, echinoderms, crustaceans, and annelids with a wide range of size and life history pattern which occur when organic input levels to the sediment are low (Pearson 8z Rosenberg, 1978). Changes in the opportunistic populations of the enriched areas of Loch Eil are rapid and thus not easily assessed from the low frequency sampling maintained for the long-term monitoring survey. Thus, one of the aims of the Loch Eil project was to follow in some detail the rapid fluctuations in the Loch Eil macrobenthic populations. In addition, it was hoped that such demographic changes might be related to effluent input levels and to the changing physical, chemical, and microbiological condition of the sediments and might be placed in their context relative to events in an analogous control area beyond the influence of the effluent inputs.
0022-098l/82/0000-0000/$02.75
0 1982 Elsexier
Biomedical
Press
306
T. H.
PEARSONET
AL.
METHODS Sampling areas and times are as described in Pearson (1981). Three samples were obtained on each sampling occasion by means of a Van Veen grab having a sample area of 0.1 m2, sieved on a l-mm mesh screen, the residues preserved in 4% formaldehyde and returned to the laboratory for examination. In the laboratory the samples were stained with 0.1% Rose Bengal to facilitate the extraction of the animals which were then picked by eye from the residues, identified, and enumerated. The species found have been assigned to a trophic group on the basis of a knowledge of their feeding habits obtained from the present study qualified by the information summarized by Fauchald & Jumars (1979). RESULTS POPULATIONSPRESENTAl- EACHSTATION The total number of species found over the 12-month sampling period and the mean species numbers (S), abundance (A), and biomass (B) of animals found over the year at each of the four sampling stations is shown in Table I. There are TABLE I Basic population
Depth Station
(m)
Total number of species found over 12 months
statistics
Mean number of species found in each month
for the four sampling
stations.
Mean abundance per month
Mean wet wt biomass per month
Mean number of individuals per species
per individual
(A)
(B) (g/m2 )
(A/S)
WA) (w)
(S)
Mean wt
-____ LYI (control)
48
94
37
468
49.3
13
164.0
E24 (head of loch)
42
86
29
1118
69.6
38
62.5
E2 (edge of deep basin)
62
17
1265
13.3
74
10.5
E70 (centre of deep basin)
65
14
2486
26.5
I78
10.6
45
considerable variations in the population structure at each station. Thus, at the control station in the Lynn of Lorne the population is diverse with a relatively low abundance and high species numbers and a biomass of ~50 g/m’ (wet wt).
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
307
In Loch Eil the populations have a low diversity and biomass at Stations E70 and E2 in the deep basin and a relatively high diversity and biomass at Station 24 at the head of the loch. These differences are more easily appreciated by a consideration of two simple comparative statistics i.e. the abundance ratio A/S, and the size ratio B/A. Thus there are 13 individuals per species at the control station, 3 times that number at station E24, 6 times the.number at E2 and >I2 times the number at E70. By way of contrast the mean weight of each individual (B/A) varies from 164 mg at LYI to less than half that at E24 and less than a tenth as much at4he two stations in the deep basin of Loch Eil. Fig. 1 shows the species area curve for each station based on the full year’s sampling of 36 0.1-m’ samples. As can be seen from Table I the largest number of species were found at the control station where >90 species were found after 2 rn? had been sampled. Only a further 4 species were found in the subsequent 10 samples 100
1
E24
E2
E70
0
I
I 2.0
AREA Fig. 1. Cumulative
species-area
SAMPLED
1
I
4.0
m2
curves for the four stations based on all samples taken over the 12-month sampling period.
308
T. H. PEARSON
ETAL.
taken. Progressively fewer species were found at E24, E2, and E70, the species increment added for each additional sample being smaller at each station thus producing successively flatter species-area curves. The 10 numerical dominants at each station are listed in Table II, together with their ranking, the mean numbers found per m2 over the sampling period and the trophic group to which they have been assigned. The percentage of the total fauna comprised by the 10 listed dominants at each station is also given. The two stations
TABLE II Numerically
dominant
species at each sampling station: rankings (R) and mean numbers per m2 over the survey period (N) given; D, subsurface deposit-feeders; SD, surface deposit-feeders; 0, omnivores; C, carnivores.
StatIons E2
E70
E24
LYI
Trophic Species
group
Tubijfcoides brnedeni (Udekem) Pro/odorvilleu
kefersteini (McIntosh)
Caprteila capirata (Fabricius) Scolelepis juliginosa (Clap&de) Prionospio cirrifera Wiren Capitomastus
minimus (Langerhans)
Nematoda sp. indet. Anailides groenlandica (Ousted)
Norris virens San Pholoe minuta (Fabricius) Ophiodromus jlemosus (delle Chiaje) Ophryorrocha puerilis (Claparede and Metschnikow) GI~cera ulba (Miiller) Paraonis gracilis (Tauber) Melinnupalmata (Grube) Thyasiraflexuosa (Montagu) Amphwn chi@i Forbes Chaetoamr sctma Malmgren Goniada moculata Ousted Diplocirrus glaurus (Malmgren) Scoloplos arm@ (Miiller) Lumbrineris hiberma (McIntosh) Nephtys hysrricis (McIntosh) Nucula sulcatu Bronn Abro alba (Wood) Cirratulus sp. indet. Praxillella affinis (Sam) Rhodine loveni Malmgren Noromastus latrricrus San
__-. 10 dominants as a percentage of total abundance
D D D SD SD D 0 C C c C
R
N
R
N
1
698
I
2
671
4
58
3
545
2
326
4
168
3
73
7
21
5
58
5
93
6
91
N
R
N
540
7
60
8
18
8
42
10
15
9
38
IO
I
SD C D SD D 0 SD C D D C C D SD D D D D
R
8
18
6
26
2 I
150 56
10
40
I
I91
3 4 5 6 8 9
143
I0
40
83 69
I
38
7
17
2
36
3
38
4
27
5
24
6
18
67 50 41
7
17
9
15
IO
IO
___. 98
94
86
69
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
309
in the deep basin of Loch Eil are dominated by small deposit-feeding annelid worms with the oligochaete Tubificoides (Peloscolex) benedeni being the most numerous. In this area the only group represented in the list of dominants apart from the anneiids are nematodes, which were quite numerous at E70. At the head of Loch Eil deposit-feeding annelids were still the most numerous species found, but the lamellibranch mollusc Thyasira and the ophiuroid echinoderm Amphiuva were present in relatively high numbers. The latter species was the most numerous animal present at the control station where two species of lamellibranch Nucula and Abra were listed among the 10 dominants in addition to annelid species. These listed dominant species comprised almost the entire fauna in the deep basin of Loch Eil and just over 85% of the total at the head of the loch. At the control station, however, they made up only 707: of the fauna. CHANGES
OCCURRING
DURING
THE SAMPLING
PERIOD
Population statistics Variation in the S A B statistics over the 12-month sampling period is shown in Fig. 2 and changes in the abundance and size ratios calculated from these are E2
d
E70
Fig. 2. Variation in the basic population statistics at each station over the 12-month sampling period: 0, S, the total number of species; A, A, the total abundance (no./m2); 0, B, the total biomass (g wet wt/m’); note the change in scale for each statistic.
310
T. H. PEARSON ET AL.
illustrated in Fig. 3. An initial comparison of the fluctuation in these statistics at the control Station LYl with the changes at the Loch Eil stations suggests that in general the populations at the control station were much more stable than the loch E2
A/S x 100 WA
Fig. 3.
Variationin the abundance ratio, the mean number of individuals per species (A/S) in each month (Cl) and the size ratio, the mean weight of each individual (B/I+) in any month (m).
populations. Thus, there were only two periods during the year’s sampling when major fluctuations occurred at LY 1. Abundance, species numbers, and biomass all increased markedly in December-January but then declined to fluctuate around their original levels until Au~st-September when there was a further sharp rise in biomass. A subsequent decline in all three factors took place at the end of the sampling period in October. These changes are reflected in the changes in the size ratio (B/A) which shows increases in February and in August-September, whereas the abundance ratio (A/S) showed a uniformly low level throughout the sampling period. At Station E24 at the head of Loch Eil there was a general decline in all three SA B factors from November to April interrupted by a brief rise in January. An increase in biomass occurred from April to August followed by a decline to low levels in September and October. Species numbers increased from June to August, whereas abundances remained low during the summer but showed a slight increase in August. These changes did not produce any marked fluctuations in the abundance ratio, which remained relatively low and uniform throughout the year, but the size ratio increased during the summer months from a low point in March to a peak in July to be followed by a decline to the end of the sampling period in October.
POPULATION
FLUCTUATIONS
311
IN MACROBENTHOS
E2, the station on the edge of the worst affected areas of the deep basin of Loch Eil showed marked fluctuations in all three population statistics throughout the sampling period. All three showed a slight peak in January and both B and S rose sharply in April. Biomass rose again in June and September and species numbers in July and October. Abundances rose sharply from May to July, declined in August and September and rose again in October. These latter changes are reflected in the abundance ratio which peaked sharply in June and started rising again in October. The size ratio showed a small rise in April and another in September, but otherwise remained low and uniform. In the centre of the deep basin at Station E70 the most notable fluctuation was the enormous increase in abundance between March and May. This was followed by a large rise in biomass in July and August which came after a period of relatively low biomass levels from the beginning of the year. Species numbers were low at the beginning and end of the year but peaked slightly in March before a fall in April. The size ratio reflects these trends, being uniformly low from January to July during the period of large population increases but rising from June to September when the biomass increases were recorded. The abundance ratio reflects the high abundance figures faithfully, being high in April, May and October. Dominants
as a percentage
qf’the
total.fkna
There was little significant change in the proportion of the total fauna made up by the 10 most numerous species at each station throughout the year’s sampling (Fig. 4). At Station LYl the proportion fell to or below 50% between January and
Fig. 4. The
10 dominant
(most numerous) species at each station on each percentage of the total fauna in each month.
sampling
occasion
as a
312
T. H. PEARSON
ETAL.
Fig. 5. Fluctuations in the abundance of the 10 most numerous species at each sampling station: for comparative purposes species are assigned to major trophic groups and histograms of the total number of species (5’) total abundances (A) (no./m2) and biomass (B) (g/m’) are also shown; note the variable scale for each factor plotted, and the scale variation between diagrams; Station LYl (abundance scale x IO*); Station E24 (abundance scale x IO’); Station E2 (abundance scale x 10’); Station E70 (abundance scale x 103); subsurface deposit-feeders, heavy stippling; surface deposit-feeders, square hatching; omnivores, light stippling; carnivores, dark shading; total number of species, vertically hatched histogram; total abundance, blank histogram; biomass (g/m’), horizontally hatched histogram;
POPULATION FLUCTUATlONS
IN MACROBENTHOS
313
Ab, Abra alba; Nu, Nucula sulcata; Am, Amphiura chiajei; Lu, Lumbrinereis hibernica; Np, Nephtys hystricis; Rh, Rhodine lovewi; PI, Praxillela offinis; Ci, Cirratulus sp. ; Di, Diplocirrus glaucus; No, Noromastus Iatericeus; Pa, Paraonis gracifis; MI, Mehnna palmata; Th, Thyasira flexuosa; GI, Glycera alba; Go, Goniada maculata; Pr, Prionospio cirrifera; Ch, Chaetozone setosa; Tu, Tubijicoides benedeni; Ca, Capitella capitata; IV, Protodorvillea kefersteini; SC, Scolelepis filiginosa; Nr, Nereis virens; PO, Phofoe minuta; Ne, Nematoda sp. ; Op. Ophiotrocha puerilis; Of, Ophiodromus flexuosus; Ph, Anaitides groenlandiea.
314
T. H. PEARSON
May but thereafter varied
between
deep basin
between
80 and 90% until
stations
except for January Population
fluctuated
the dominants
ETAL
55 and 65:;.
September comprised
At Station
when it declined
E24 the proportion a little. At the two
over 95% of the fauna
and April when the proportion
fell slightly at Station
consistently E2.
changes in the dominant species
The fluctuations in the abundance of the ten most numerous species at each of the sampling stations are illustrated in Fig. 5. Histograms of the total numbers of species, total abundances and biomass for each month are also shown on the diagrams. At Station LYl (Fig. 5) the overall abundance and biomass increases in December and January are seen to be largely due to increases in the numbers of the lamellibranchs Abra and Nucula. No great changes in the numbers of the various dominants took place between February and June when all maintained fairly low populations, but the numbers of Abra rose sharply again in July, and there were small rises in the numbers of Amphiura, Lumbrinereis, Nephtys, Rhodine, and Praxillela in August to September. In general numbers remained low throughout the year in comparison with the populations in Loch Eil. Fig. 5 shows the population fluctuations taking place at Station E24 drawn to the same scale thus demonstrating the much higher abundances in the Loch. At this station the small deposit-feeding polychaete Paraonis and the much larger surface deposit-feeding ampharetid polychaete Melinna maintained relatively high populations until September when the numbers of Melinna dropped markedly. The deposit-feeding lamellibranch mollusc Thyasira was present in relatively large numbers at the beginning and end of the sampling period but was absent in May and June. The numbers of the carnivorous polychaetes GIycera and Goniada and of the brittle star Amphiura and the polychaete Scoloplos did not fluctuate greatly throughout the year, but populations of the surface deposit-feeding Chaetozone, and Diplocirrus were high from November The deposit-feeding considerably reduced thereafter.
polychaetes Prionospio, to February although capitellid polychaete
Capitomastus followed a similar pattern. The large rise in overall biomass from April to August at this station thus seems attributable principally to the increase in the numbers of Melinna at this time. Population changes at the two stations (E2 and E70) in the deep basin of Loch Eil are shown in Fig. 5, where the scale to which the abundanceslare drawn is an order of magnitude greater than in the previous two diagrams in order to represent the much higher populations present. At Station E2 large increases in the numbers of deposit-feeding polychaetes Capitella took place in May and June together with smaller increases in Protodorvillea and Scolelepis. The greatest population increases were in the oligochaete Tubificoides whose numbers reached over 2500/m2 in July. The numbers of all these species declined in August and September but there were smaller increases in Tubfkiodes and Capitella in October.
POPULATION FLUCTUATIONS
IN MACROBENTHOS
315
Only small changes occurred in the number of the dominant carnivorous polychaetes Ophiodromus, Nereis, and Phyllodoce at this station. In the centre of the deep basin at Station E70 abundance fluctuations were much greater. Populations of Protodovillea and Tubijkoides started to rise in February, reached numbers of >4000/m’ and 6000/m*, respectively, in April, but declined sharply in subsequent months before slight rises were again recorded in October. Capitomastus followed a similar pattern but at much lower levels. Capitella populations rose in March, fell sharply in April, reached high levels again in June and July only to decline once more in August and September before reaching a final peak in October. Numbers ofbhe small carnivorous polychaete Pholoe rose in April and May but were low in subsequent months. The larger polychaete carnivores Nereis and Anaitides reached high populations towards the end of the sampling period, Nereis in July to September and Anaitides in September. The high overall biomass figures of the later months are associated with the increase in these carnivorous species whereas the high abundance figures of April and May are attributable to the small deposit-feeding Protodorvillea and Tubtfkoides. Fluctuations in trophic groups
Some indication of changes in the trophic status of populations throughout the sampling period has been given in the preceding discussion where the feeding habits of the dominants have been mentioned. Species have been assigned to one of the following five general trophic groups: subsurface deposit-feeders (D), surface deposit-feeders (SD), carnivores (C), omnivores (0), and filter-feeders (F). The changes in these groups summed over the whole population summarize any general changes in the feeding habits of the community which may have occurred during the years sampling. Fig. 6 illustrates these changes. Filter-feeders were present only at the control Station LYI where they represented between 5 and 17”/, of the population. In this area all five groups showed considerable stability throughout the year, the only notable change being an increase in surface deposit-feeders in July at the expense of filter-feeders and omnivores. At Station E24 there was a marked decrease in the proportion of surface deposit-feeders from February to May accompanied by a corresponding increase in subsurface deposit-feeders, carnivores and latterly omnivores. Subsurface deposit-feeders reached a peak in May, declined in the following 2 months, increased again in August, declined in September, and finally reached their highest proportion in October when they comprised nearly 60% of the fauna. From May onwards omnivores and carnivores fluctuated at between 10 and 25% of the fauna. Surface deposit-feeders increased again in June but then decreased in the following three months to reach their lowest level in September when they made up < 10% of the fauna. In the deep basin deposit-feeders were predominant through most of the year at both stations. At the start of sampling in November and December surface deposit-feeders were the most important group
316
T. H. PEARSON ETAL.
at both Stations
E70 and E2 but thereafter
greater part of the fauna
in all months
subsurface
but February,
deposit-feeders when omnivores
formed
the
were briefly
Fig. 6. Fluctuations in the proportions of trophic groups found at each station: D, subsurface depositfeeders, heavy stippling; SD, surface deposit-feeders, squared hatching; 0. omnivores, light hatching; C. carnivores. dark shading; F, filter-feeders, vertical hatching.
important
at Station
2, and in September
when carnivores
were prominent
at both
stations. DISCUSSION FLUCTUATION
IN POPULATION
STATISTICS
Pearson & Rosenberg (1978) described benthic population changes and succession along a gradient of increasing organic pollution and showed that the SA B statistics defining such changes varied along the gradient in a characteristic manner. The four sampling stations chosen for the present study may be placed relative to their position on such a gradient by reference to the range of their SA B statistics derived
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
317
from the year’s sampling data (Fig. 7). Thus, the control Station LYl falls well to the low organic input end of the gradient and deviated little from such a position during the year. The station at the head of Loch Eil (E24) is placed near the centre of the gradient with the S A B values tending to the low input end in December 1975 to April 1976 and again in September and to the high input end in other months. 6
A x103 B
XIO
-INCREASING
-OF
GRADIENT ORGANIC
-
DECREASING
__)
,NP”T
Fig. 7. The range of changes in the basic population statistics at each station related to the changing pattern of such statistics along a hypothetical gradient of organic input to marine sediments (after Pearson & Rosenberg. 1978): months in which the statistics reflected changes towards either the upper or lower end of the gradient are listed; S, number of species; A. total abundance; B. total biomass.
Both the stations in the deep basin of Loch Eil lie towards the high input end of the gradient but the range of SA B values at Station E70 covers a wider range than at E2. Thus, at E70 the values tended to approach the extreme upper end of the gradient from March to May and again in October and tended to the middle range of the gradient overlapping with the E2 values from November to February and again from June to September. The SA B values at E2 tended to lie in the middle to upper areas of the gradient but showed less consistent tendencies than the other stations. The values tended, however, towards the uppermost end of the gradient from May to July. These results strongly suggest that the population fluctuations observed in Loch
318
T. H. PEARSON
Eil are related
to the recorded
changes
a comparison
with the variations
ET AL.
in the organic
in effluent
input
input to the Loch, and indeed reveals
some analogous
trends.
Thus, inputs were relatively high from September to December 1975 (13-15 tonnes/ day), low in January 1976 (7 tonnes/day), very high in February (19 tonnes/day) and remained high at between 15 and 16 tonnes/day. Thereafter they declined in May to as low as 6 tonnes/day in June, but were again high from July to September. reaching a peak of 26 tonnes/day in August (see Pearson, 1981). If it is assumed that the SA B statistics are fluctuating in response to these changing organic inputs then it seems that the high inputs in February were followed by a corresponding change in the populations at Station E70 in March, but that similar changes did not take place until May at Stations E2 and E24. Similarly, the low inputs in June are followed by down gradient population changes at E70 the next month but not until 2 months later at E2 and only in September at E24. The high inputs in July to September are apparently reflected in the up-gradient SA B changes in October at E70 and also, in this instance, at E2. The corresponding changes at E24 presumably occurred in November-December i.e. beyond the end of the sampling period. It is assumed
that the control
Station
LYI lay well beyond
any influence
of the
effluent, thus any fluctuations observed in the populations in that area are attributable to natural causes. Indeed the populations at the station remained relatively constant throughout the year in marked contrast to the instability observed in the Loch Eil populations. Notable increases in all three population statistics were observed, however, in January, and a biomass increase was apparent in August and September. The former increases are rather inexplicable but the autumn biomass increase probably arises from the normal seasonal growth of annual benthic species and thus corresponds to an expected seasonal trend in this factor. It may be that the biomass increases observed at E70 and E24 in July and August could be partially due to a like seasonal increase, but their association with fluctuations in abundance seasonal
and biomass
in the preceding
months
(see Fig. 2) suggests
that
the
factor, if any, is small.
FLUCTUATIONS
IN DOMINANT
SPECIES
Although there were considerable fluctuations in the individual numbers of the 10 dominapt (most numerous) species at each station, the proportion of these dominants to the rest of the fauna did not change much during the year at any of the stations, implying the presence of an underlying stability to the benthic community structure at each station. At the control Station, LY 1, the changes observed in the numbers of the various dominant species were relatively small and showed no discernible pattern but at the stations in Loch Eil the fluctuations in most of the dominants were large and can be interpreted in relation to fluctuation in the organic input to the loch. The relationship is most clearly seen at Station E70
POPULATION
(Fig. 5) where
FLUCTUATIONS
the large increases
in the numbers
and Capitellu from March
to May appear
effluent
Numbers
input
subsequently
in February. declined
of Tubiji’coides, Protodorvillea,
to be a direct response
of Pvotodorvillea reached
Tubtficoides also peaked
sharply.
319
IN MACROBENTHOS
to the increased
a peak in May and
in May
but maintained
relatively high numbers into June. Capitella after increasing in March declined in April, but reached its maximum numbers in June and July in association with the large spionid Scolelepis. These observations support the suggestion put forward by Pearson (in press) that Tub(fi’coide.s and Protodorvillea alternate with Capitellu and Scolelepis as the most important dominants in two competing groups of opportunist species which may replace each other in organically enriched areas. The sequence observed in this instance suggests that Tuh$coides and Protodorvillea developed large populations most rapidly following the high effluent inputs in February and that Capitella and Scolelepis reached high numbers as the other two species declined. Increases in both Capitella and Tub$coides were again recorded in October
following
further
high
effluent
inputs
in August
and
sampling stopped before these changes could be followed similar changes in the various dominant species were recorded
September,
in detail. at Station
but
Essentially E2 (Fig. 5)
with Capitella and Tub(ficoides reaching peaks in June. At this station Protodorvillea and Scolelepis were present in lower numbers, and the alternate species groupings noted at E70 were not observed. It seems that the populations at the edge of the deep basin although identical in species composition with those in the centre of the basin, were affected to a slightly lesser extent by the effluent input fluctuations in that the variations in individual species numbers were less pronounced. At the head of the Loch (Station E24) significant changes in individual species were also observed from March onwards following the effluent input increases in February. Thus the surface deposit-feeding polychaetes Chaetozone and Prionospio declined from relatively high numbers in February to very low numbers in May. The deposit-feeding lamellibranch Thyusira vanished completely from the April, May, and June samples although at the beginning of the sampling period it was one of the
most
numerous
species,
and
the
numbers
of the
surface
deposit-feeding
ampharetid polychaete Melinna fell sharply in April. Melinna populations recovered again in May and remained high until September when they again declined, possibly in response to the higher effluent inputs in that month. Thyzsira populations recovered in July but also declined again in September, while populations of Clzaetozone and Prionospio remained at fairly low levels for the rest of the sampling period.
FLUCTUATIONS
IN TROPHIC
GROUPS
The composite trends of the various changes observed in the individual species discussed above are to a large extent summarized in the trophic group changes. Thus, an increase in effluent input appears initially to favour subsurface deposit-
320
T.H.PEARSON ETAL.
feeding species at the expense of surface deposit-feeders. Some 12-16 wk after the largest population increases in deposit-feeders an increase in carnivores was recorded, presumably representing a response to the increased number of prey species. The carnivorous species, however, declined rapidly again following a further increase in effluent inputs at the end of the sampling period, thus suggesting that they were more sensitive to the consequent changes in the chemical conditions of the sediment than their prey.
CONCLUSIONS
Information presented elsewhere in this series of papers (Stanley rt al., 1981; Vance et al., 1982; Blake et al., 1982) show that the changes in effluent input discussed above brought about a series of consequential changes in the chemistry and microbiology of the sediments at the various sampling stations, most notably increases in the populations of cellulose-digesting and aerobic heterotrophic bacteria in the weeks immediately following an increase in effluent input to the Loch. At the same time significant increases in the populations of ciliates in the sediments took place (Wyatt & Pearson, 1982) and there was some evidence that meiofaunal abundance also increased simultaneously. The greatest changes recorded in the macrofauna took place between 4-8 wk after the microfaunal changes and it seems reasonable to suggest that the events are causally linked. The increasing bacterial populations must represent an abundant food source to those animals. primarily the subsurface deposit-feeders, which are adapted for their exploitation. Thus, those deposit-feeders, which are capable of surviving in the relatively low oxygen tensions and high sulphide levels of the sediment which accompany the increasing bacterial populations as carbon input to the sediments increases, must be assured of a rapid population growth, particularly as the sedimentary conditions apparently preclude the immediate build-up of predator populations. Copitella, Tub(ficoides, and Protodorvillea would appear to be in this category whereas the deposit-feeding lamellibranch Thyasira declines in numbers under these conditions. As carbon input levels decrease then populations of predatory polychaetes such as Glyccru, Goniada, and Pholoe build-up, presumably at the expense of the opportunistic deposit-feeders whose numbers decline at this stage. The time scale of these changes is relatively short. The increase in deposit-feeder populations, particularly of the small polychaetes is rapid, taking place within 46 wk of the chemical and microbiological changes of the sediment in the deep basin. The larger species of surface deposit-feeders, e.g. Melinna, in the sediments at the head of the Loch and the carnivorous polychaetes in the deep basin appear to respond within 12-14 wk of a major change in sedimentary conditions. Obviously, such response times will be a function not only of food availability but of reproductive period and interspecific competition for space. Elucidation of these
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
321
aspects will require further detailed autecological studies of the dominant species in the system. Further consideration of the synecological aspects of this study is given in Pearson (1982).
REFERENCES
BLAKE, D., J.W.
LEFTLEY & C.M. BROWN, 1981. The Loch Eil Project: the bacterial flora and heterotrophic nitrogen fixation in sediments of Loch Eil. J. “up. mar. Biol. Ecol., Vol. 56, pp. 115-122. FAUCHALD, K. & P. A. JUMARS, 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Ann. Rev., Vol. 17, pp. 193-284. PEARSON, T. H., 1970. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. I. The physical environment and distribution of the macrobenthic fauna. J. exp. mar. Biol. Ecol., Vol. 5, pp. l-34. PEARSON, T. H., 197la. Studies on the ecology of the macrobenthic fauna of Lochs Linnhe and Eil, west coast of Scotland. II. Analysis of the macrobenthic fauna by comparison of feeding groups. Vie Milieu, Suppl. No. 22, pp. 53-91. PEARSON, T. H., 197lb. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. III. The effect on the benthic fauna of the introduction of pulp mill effluent. J. exp. mar. Biol. Ecol.. Vol. 6, pp. 211-233. PEARSON, T. H.. 1975. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. IV. Changes in the benthic fauna attributable to organic enrichment. J. up. mar. Biol. Ecol.. Vol. 20. pp. l-41. PEARSON, T. H.. 1981. The Loch Eil Project: introduction and rationale. J. exp. mar. Biol. Ecol.. Vol. 55. pp. 93-102. PF~KSON. T. H., 1982. The Loch Eil Project: assessment and synthesis with a discussion of certain biological questions arising from a study of the orgamc pollution of sediments. J. e.~p. mclr. Bid. Ecol., Vol. 37, in press. PEARSON, T. H., in press. Stress and catastrophe in benthic ecosystems. In. Stress qffectson naturul ecosystems. edited by G. W. Barrett & R. Rosenberg, John Wiley & Sons, New York. PF~~RSON,T. H. & R. ROSENBERG, 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Ann. Rev.. Vol. 16. pp. 229-31 I. ST,~IULEY. S.O.. J.W. LEyrLEv, A. LIGH~FOO~. N. Roat.~r~oh. I.M. STANLEY & I. V~hct, 1981. The Loch Eil Project: sediment chemistry, sedimentation and the chemistry of. the overlying water in Loch Eil. J. exp. mar. Biol. Ecol., Vol. 55, pp. 299-313. VAKF, I., S. 0. STANLEY & C. M. BROWN, 1982. The Loch Eil Project: cellulose-degrading bacteria in the sediments of Loch Eil and the Lynn of Lorne. J. exp. mar. Biol. Ecol., Vol. 56, pp. 2677278. WYATT. C. E. & T. H. PEARSON, 1982. The Loch Eil Project: population characteristics of ciliate protozoans from organically enriched sea-loch sediments. J. exp. mar. Biol. Ecol., Vol. 56. pp. 279-303.
J. exp. mar. Biol. Ecol., 1982, Vol. 56, pp. 305-321
Elsevier Biomedical Press
THE LOCH EIL PROJECT:
POPULATION
FLUCTUATIONS
IN THE MACROBENTHOS
T. H. PEARSON, G. DUNCAN and J. NUTTALL Scottish Marine Biological Association. DunstaSfnage Marine Research Laboratory, Oban, Argyli, Scotland
Abstract: Population fluctuations in the macrobenthic
fauna at three stations in Loch Eil and at a control station in the Lynn of Lorne were followed by monthly sampling over 1 yr. Populations of relatively low density but high species numbers and size range occurred at the control station where the fluctuations over the year were small. In the deep basin of Loch Eil the populations were much less diverse and fluctuated considerably from month to month. These fluctuations followed changes in the carbon input to the Loch and subsequent changes in the chemistry and microbiology of the sediments. A time lag of 46 wk was observed between an increased carbon input to the sediments and a subsequent increase in the numbers of small deposit-feeding annelids. Increases in populations of carnivores took place after a further 8-10 wk and coincided with a decline in deposit-feeding populations. At the head of the Loch where carbon inputs were lower population structure was intermediate between the diverse situation at the control station and the opportunist dominated populations of the deep basin. In this area populations of larger surface deposit-feeding species fluctuated apparently in response to a change in carbon input after an interval of z 12-14 wk.
Population changes in the macrobenthic fauna of Loch Linnhe and Loch Eil have been monitored continuously from 1963 (Pearson 1970; 1971a,b, 1975) with a minimum biannual sampling frequency. Observed changes have been related primarily to fluctuations in the input of effluent material to the loch system from the pulp and paper mill at Annat Point. High input levels have resulted in fauna1 dominance by small rapidly breeding (opportunistic) annelid species in place of the more usual complex communities of molluscs, echinoderms, crustaceans, and annelids with a wide range of size and life history pattern which occur when organic input levels to the sediment are low (Pearson 8z Rosenberg, 1978). Changes in the opportunistic populations of the enriched areas of Loch Eil are rapid and thus not easily assessed from the low frequency sampling maintained for the long-term monitoring survey. Thus, one of the aims of the Loch Eil project was to follow in some detail the rapid fluctuations in the Loch Eil macrobenthic populations. In addition, it was hoped that such demographic changes might be related to effluent input levels and to the changing physical, chemical, and microbiological condition of the sediments and might be placed in their context relative to events in an analogous control area beyond the influence of the effluent inputs.
0022-098l/82/0000-0000/$02.75
0 1982 Elsexier
Biomedical
Press
306
T. H.
PEARSONET
AL.
METHODS Sampling areas and times are as described in Pearson (1981). Three samples were obtained on each sampling occasion by means of a Van Veen grab having a sample area of 0.1 m2, sieved on a l-mm mesh screen, the residues preserved in 4% formaldehyde and returned to the laboratory for examination. In the laboratory the samples were stained with 0.1% Rose Bengal to facilitate the extraction of the animals which were then picked by eye from the residues, identified, and enumerated. The species found have been assigned to a trophic group on the basis of a knowledge of their feeding habits obtained from the present study qualified by the information summarized by Fauchald & Jumars (1979). RESULTS POPULATIONSPRESENTAl- EACHSTATION The total number of species found over the 12-month sampling period and the mean species numbers (S), abundance (A), and biomass (B) of animals found over the year at each of the four sampling stations is shown in Table I. There are TABLE I Basic population
Depth Station
(m)
Total number of species found over 12 months
statistics
Mean number of species found in each month
for the four sampling
stations.
Mean abundance per month
Mean wet wt biomass per month
Mean number of individuals per species
per individual
(A)
(B) (g/m2 )
(A/S)
WA) (w)
(S)
Mean wt
-____ LYI (control)
48
94
37
468
49.3
13
164.0
E24 (head of loch)
42
86
29
1118
69.6
38
62.5
E2 (edge of deep basin)
62
17
1265
13.3
74
10.5
E70 (centre of deep basin)
65
14
2486
26.5
I78
10.6
45
considerable variations in the population structure at each station. Thus, at the control station in the Lynn of Lorne the population is diverse with a relatively low abundance and high species numbers and a biomass of ~50 g/m’ (wet wt).
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
307
In Loch Eil the populations have a low diversity and biomass at Stations E70 and E2 in the deep basin and a relatively high diversity and biomass at Station 24 at the head of the loch. These differences are more easily appreciated by a consideration of two simple comparative statistics i.e. the abundance ratio A/S, and the size ratio B/A. Thus there are 13 individuals per species at the control station, 3 times that number at station E24, 6 times the.number at E2 and >I2 times the number at E70. By way of contrast the mean weight of each individual (B/A) varies from 164 mg at LYI to less than half that at E24 and less than a tenth as much at4he two stations in the deep basin of Loch Eil. Fig. 1 shows the species area curve for each station based on the full year’s sampling of 36 0.1-m’ samples. As can be seen from Table I the largest number of species were found at the control station where >90 species were found after 2 rn? had been sampled. Only a further 4 species were found in the subsequent 10 samples 100
1
E24
E2
E70
0
I
I 2.0
AREA Fig. 1. Cumulative
species-area
SAMPLED
1
I
4.0
m2
curves for the four stations based on all samples taken over the 12-month sampling period.
308
T. H. PEARSON
ETAL.
taken. Progressively fewer species were found at E24, E2, and E70, the species increment added for each additional sample being smaller at each station thus producing successively flatter species-area curves. The 10 numerical dominants at each station are listed in Table II, together with their ranking, the mean numbers found per m2 over the sampling period and the trophic group to which they have been assigned. The percentage of the total fauna comprised by the 10 listed dominants at each station is also given. The two stations
TABLE II Numerically
dominant
species at each sampling station: rankings (R) and mean numbers per m2 over the survey period (N) given; D, subsurface deposit-feeders; SD, surface deposit-feeders; 0, omnivores; C, carnivores.
StatIons E2
E70
E24
LYI
Trophic Species
group
Tubijfcoides brnedeni (Udekem) Pro/odorvilleu
kefersteini (McIntosh)
Caprteila capirata (Fabricius) Scolelepis juliginosa (Clap&de) Prionospio cirrifera Wiren Capitomastus
minimus (Langerhans)
Nematoda sp. indet. Anailides groenlandica (Ousted)
Norris virens San Pholoe minuta (Fabricius) Ophiodromus jlemosus (delle Chiaje) Ophryorrocha puerilis (Claparede and Metschnikow) GI~cera ulba (Miiller) Paraonis gracilis (Tauber) Melinnupalmata (Grube) Thyasiraflexuosa (Montagu) Amphwn chi@i Forbes Chaetoamr sctma Malmgren Goniada moculata Ousted Diplocirrus glaurus (Malmgren) Scoloplos arm@ (Miiller) Lumbrineris hiberma (McIntosh) Nephtys hysrricis (McIntosh) Nucula sulcatu Bronn Abro alba (Wood) Cirratulus sp. indet. Praxillella affinis (Sam) Rhodine loveni Malmgren Noromastus latrricrus San
__-. 10 dominants as a percentage of total abundance
D D D SD SD D 0 C C c C
R
N
R
N
1
698
I
2
671
4
58
3
545
2
326
4
168
3
73
7
21
5
58
5
93
6
91
N
R
N
540
7
60
8
18
8
42
10
15
9
38
IO
I
SD C D SD D 0 SD C D D C C D SD D D D D
R
8
18
6
26
2 I
150 56
10
40
I
I91
3 4 5 6 8 9
143
I0
40
83 69
I
38
7
17
2
36
3
38
4
27
5
24
6
18
67 50 41
7
17
9
15
IO
IO
___. 98
94
86
69
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
309
in the deep basin of Loch Eil are dominated by small deposit-feeding annelid worms with the oligochaete Tubificoides (Peloscolex) benedeni being the most numerous. In this area the only group represented in the list of dominants apart from the anneiids are nematodes, which were quite numerous at E70. At the head of Loch Eil deposit-feeding annelids were still the most numerous species found, but the lamellibranch mollusc Thyasira and the ophiuroid echinoderm Amphiuva were present in relatively high numbers. The latter species was the most numerous animal present at the control station where two species of lamellibranch Nucula and Abra were listed among the 10 dominants in addition to annelid species. These listed dominant species comprised almost the entire fauna in the deep basin of Loch Eil and just over 85% of the total at the head of the loch. At the control station, however, they made up only 707: of the fauna. CHANGES
OCCURRING
DURING
THE SAMPLING
PERIOD
Population statistics Variation in the S A B statistics over the 12-month sampling period is shown in Fig. 2 and changes in the abundance and size ratios calculated from these are E2
d
E70
Fig. 2. Variation in the basic population statistics at each station over the 12-month sampling period: 0, S, the total number of species; A, A, the total abundance (no./m2); 0, B, the total biomass (g wet wt/m’); note the change in scale for each statistic.
310
T. H. PEARSON ET AL.
illustrated in Fig. 3. An initial comparison of the fluctuation in these statistics at the control Station LYl with the changes at the Loch Eil stations suggests that in general the populations at the control station were much more stable than the loch E2
A/S x 100 WA
Fig. 3.
Variationin the abundance ratio, the mean number of individuals per species (A/S) in each month (Cl) and the size ratio, the mean weight of each individual (B/I+) in any month (m).
populations. Thus, there were only two periods during the year’s sampling when major fluctuations occurred at LY 1. Abundance, species numbers, and biomass all increased markedly in December-January but then declined to fluctuate around their original levels until Au~st-September when there was a further sharp rise in biomass. A subsequent decline in all three factors took place at the end of the sampling period in October. These changes are reflected in the changes in the size ratio (B/A) which shows increases in February and in August-September, whereas the abundance ratio (A/S) showed a uniformly low level throughout the sampling period. At Station E24 at the head of Loch Eil there was a general decline in all three SA B factors from November to April interrupted by a brief rise in January. An increase in biomass occurred from April to August followed by a decline to low levels in September and October. Species numbers increased from June to August, whereas abundances remained low during the summer but showed a slight increase in August. These changes did not produce any marked fluctuations in the abundance ratio, which remained relatively low and uniform throughout the year, but the size ratio increased during the summer months from a low point in March to a peak in July to be followed by a decline to the end of the sampling period in October.
POPULATION
FLUCTUATIONS
311
IN MACROBENTHOS
E2, the station on the edge of the worst affected areas of the deep basin of Loch Eil showed marked fluctuations in all three population statistics throughout the sampling period. All three showed a slight peak in January and both B and S rose sharply in April. Biomass rose again in June and September and species numbers in July and October. Abundances rose sharply from May to July, declined in August and September and rose again in October. These latter changes are reflected in the abundance ratio which peaked sharply in June and started rising again in October. The size ratio showed a small rise in April and another in September, but otherwise remained low and uniform. In the centre of the deep basin at Station E70 the most notable fluctuation was the enormous increase in abundance between March and May. This was followed by a large rise in biomass in July and August which came after a period of relatively low biomass levels from the beginning of the year. Species numbers were low at the beginning and end of the year but peaked slightly in March before a fall in April. The size ratio reflects these trends, being uniformly low from January to July during the period of large population increases but rising from June to September when the biomass increases were recorded. The abundance ratio reflects the high abundance figures faithfully, being high in April, May and October. Dominants
as a percentage
qf’the
total.fkna
There was little significant change in the proportion of the total fauna made up by the 10 most numerous species at each station throughout the year’s sampling (Fig. 4). At Station LYl the proportion fell to or below 50% between January and
Fig. 4. The
10 dominant
(most numerous) species at each station on each percentage of the total fauna in each month.
sampling
occasion
as a
312
T. H. PEARSON
ETAL.
Fig. 5. Fluctuations in the abundance of the 10 most numerous species at each sampling station: for comparative purposes species are assigned to major trophic groups and histograms of the total number of species (5’) total abundances (A) (no./m2) and biomass (B) (g/m’) are also shown; note the variable scale for each factor plotted, and the scale variation between diagrams; Station LYl (abundance scale x IO*); Station E24 (abundance scale x IO’); Station E2 (abundance scale x 10’); Station E70 (abundance scale x 103); subsurface deposit-feeders, heavy stippling; surface deposit-feeders, square hatching; omnivores, light stippling; carnivores, dark shading; total number of species, vertically hatched histogram; total abundance, blank histogram; biomass (g/m’), horizontally hatched histogram;
POPULATION FLUCTUATlONS
IN MACROBENTHOS
313
Ab, Abra alba; Nu, Nucula sulcata; Am, Amphiura chiajei; Lu, Lumbrinereis hibernica; Np, Nephtys hystricis; Rh, Rhodine lovewi; PI, Praxillela offinis; Ci, Cirratulus sp. ; Di, Diplocirrus glaucus; No, Noromastus Iatericeus; Pa, Paraonis gracifis; MI, Mehnna palmata; Th, Thyasira flexuosa; GI, Glycera alba; Go, Goniada maculata; Pr, Prionospio cirrifera; Ch, Chaetozone setosa; Tu, Tubijicoides benedeni; Ca, Capitella capitata; IV, Protodorvillea kefersteini; SC, Scolelepis filiginosa; Nr, Nereis virens; PO, Phofoe minuta; Ne, Nematoda sp. ; Op. Ophiotrocha puerilis; Of, Ophiodromus flexuosus; Ph, Anaitides groenlandiea.
314
T. H. PEARSON
May but thereafter varied
between
deep basin
between
80 and 90% until
stations
except for January Population
fluctuated
the dominants
ETAL
55 and 65:;.
September comprised
At Station
when it declined
E24 the proportion a little. At the two
over 95% of the fauna
and April when the proportion
fell slightly at Station
consistently E2.
changes in the dominant species
The fluctuations in the abundance of the ten most numerous species at each of the sampling stations are illustrated in Fig. 5. Histograms of the total numbers of species, total abundances and biomass for each month are also shown on the diagrams. At Station LYl (Fig. 5) the overall abundance and biomass increases in December and January are seen to be largely due to increases in the numbers of the lamellibranchs Abra and Nucula. No great changes in the numbers of the various dominants took place between February and June when all maintained fairly low populations, but the numbers of Abra rose sharply again in July, and there were small rises in the numbers of Amphiura, Lumbrinereis, Nephtys, Rhodine, and Praxillela in August to September. In general numbers remained low throughout the year in comparison with the populations in Loch Eil. Fig. 5 shows the population fluctuations taking place at Station E24 drawn to the same scale thus demonstrating the much higher abundances in the Loch. At this station the small deposit-feeding polychaete Paraonis and the much larger surface deposit-feeding ampharetid polychaete Melinna maintained relatively high populations until September when the numbers of Melinna dropped markedly. The deposit-feeding lamellibranch mollusc Thyasira was present in relatively large numbers at the beginning and end of the sampling period but was absent in May and June. The numbers of the carnivorous polychaetes GIycera and Goniada and of the brittle star Amphiura and the polychaete Scoloplos did not fluctuate greatly throughout the year, but populations of the surface deposit-feeding Chaetozone, and Diplocirrus were high from November The deposit-feeding considerably reduced thereafter.
polychaetes Prionospio, to February although capitellid polychaete
Capitomastus followed a similar pattern. The large rise in overall biomass from April to August at this station thus seems attributable principally to the increase in the numbers of Melinna at this time. Population changes at the two stations (E2 and E70) in the deep basin of Loch Eil are shown in Fig. 5, where the scale to which the abundanceslare drawn is an order of magnitude greater than in the previous two diagrams in order to represent the much higher populations present. At Station E2 large increases in the numbers of deposit-feeding polychaetes Capitella took place in May and June together with smaller increases in Protodorvillea and Scolelepis. The greatest population increases were in the oligochaete Tubificoides whose numbers reached over 2500/m2 in July. The numbers of all these species declined in August and September but there were smaller increases in Tubfkiodes and Capitella in October.
POPULATION FLUCTUATIONS
IN MACROBENTHOS
315
Only small changes occurred in the number of the dominant carnivorous polychaetes Ophiodromus, Nereis, and Phyllodoce at this station. In the centre of the deep basin at Station E70 abundance fluctuations were much greater. Populations of Protodovillea and Tubijkoides started to rise in February, reached numbers of >4000/m’ and 6000/m*, respectively, in April, but declined sharply in subsequent months before slight rises were again recorded in October. Capitomastus followed a similar pattern but at much lower levels. Capitella populations rose in March, fell sharply in April, reached high levels again in June and July only to decline once more in August and September before reaching a final peak in October. Numbers ofbhe small carnivorous polychaete Pholoe rose in April and May but were low in subsequent months. The larger polychaete carnivores Nereis and Anaitides reached high populations towards the end of the sampling period, Nereis in July to September and Anaitides in September. The high overall biomass figures of the later months are associated with the increase in these carnivorous species whereas the high abundance figures of April and May are attributable to the small deposit-feeding Protodorvillea and Tubtfkoides. Fluctuations in trophic groups
Some indication of changes in the trophic status of populations throughout the sampling period has been given in the preceding discussion where the feeding habits of the dominants have been mentioned. Species have been assigned to one of the following five general trophic groups: subsurface deposit-feeders (D), surface deposit-feeders (SD), carnivores (C), omnivores (0), and filter-feeders (F). The changes in these groups summed over the whole population summarize any general changes in the feeding habits of the community which may have occurred during the years sampling. Fig. 6 illustrates these changes. Filter-feeders were present only at the control Station LYI where they represented between 5 and 17”/, of the population. In this area all five groups showed considerable stability throughout the year, the only notable change being an increase in surface deposit-feeders in July at the expense of filter-feeders and omnivores. At Station E24 there was a marked decrease in the proportion of surface deposit-feeders from February to May accompanied by a corresponding increase in subsurface deposit-feeders, carnivores and latterly omnivores. Subsurface deposit-feeders reached a peak in May, declined in the following 2 months, increased again in August, declined in September, and finally reached their highest proportion in October when they comprised nearly 60% of the fauna. From May onwards omnivores and carnivores fluctuated at between 10 and 25% of the fauna. Surface deposit-feeders increased again in June but then decreased in the following three months to reach their lowest level in September when they made up < 10% of the fauna. In the deep basin deposit-feeders were predominant through most of the year at both stations. At the start of sampling in November and December surface deposit-feeders were the most important group
316
T. H. PEARSON ETAL.
at both Stations
E70 and E2 but thereafter
greater part of the fauna
in all months
subsurface
but February,
deposit-feeders when omnivores
formed
the
were briefly
Fig. 6. Fluctuations in the proportions of trophic groups found at each station: D, subsurface depositfeeders, heavy stippling; SD, surface deposit-feeders, squared hatching; 0. omnivores, light hatching; C. carnivores. dark shading; F, filter-feeders, vertical hatching.
important
at Station
2, and in September
when carnivores
were prominent
at both
stations. DISCUSSION FLUCTUATION
IN POPULATION
STATISTICS
Pearson & Rosenberg (1978) described benthic population changes and succession along a gradient of increasing organic pollution and showed that the SA B statistics defining such changes varied along the gradient in a characteristic manner. The four sampling stations chosen for the present study may be placed relative to their position on such a gradient by reference to the range of their SA B statistics derived
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
317
from the year’s sampling data (Fig. 7). Thus, the control Station LYl falls well to the low organic input end of the gradient and deviated little from such a position during the year. The station at the head of Loch Eil (E24) is placed near the centre of the gradient with the S A B values tending to the low input end in December 1975 to April 1976 and again in September and to the high input end in other months. 6
A x103 B
XIO
-INCREASING
-OF
GRADIENT ORGANIC
-
DECREASING
__)
,NP”T
Fig. 7. The range of changes in the basic population statistics at each station related to the changing pattern of such statistics along a hypothetical gradient of organic input to marine sediments (after Pearson & Rosenberg. 1978): months in which the statistics reflected changes towards either the upper or lower end of the gradient are listed; S, number of species; A. total abundance; B. total biomass.
Both the stations in the deep basin of Loch Eil lie towards the high input end of the gradient but the range of SA B values at Station E70 covers a wider range than at E2. Thus, at E70 the values tended to approach the extreme upper end of the gradient from March to May and again in October and tended to the middle range of the gradient overlapping with the E2 values from November to February and again from June to September. The SA B values at E2 tended to lie in the middle to upper areas of the gradient but showed less consistent tendencies than the other stations. The values tended, however, towards the uppermost end of the gradient from May to July. These results strongly suggest that the population fluctuations observed in Loch
318
T. H. PEARSON
Eil are related
to the recorded
changes
a comparison
with the variations
ET AL.
in the organic
in effluent
input
input to the Loch, and indeed reveals
some analogous
trends.
Thus, inputs were relatively high from September to December 1975 (13-15 tonnes/ day), low in January 1976 (7 tonnes/day), very high in February (19 tonnes/day) and remained high at between 15 and 16 tonnes/day. Thereafter they declined in May to as low as 6 tonnes/day in June, but were again high from July to September. reaching a peak of 26 tonnes/day in August (see Pearson, 1981). If it is assumed that the SA B statistics are fluctuating in response to these changing organic inputs then it seems that the high inputs in February were followed by a corresponding change in the populations at Station E70 in March, but that similar changes did not take place until May at Stations E2 and E24. Similarly, the low inputs in June are followed by down gradient population changes at E70 the next month but not until 2 months later at E2 and only in September at E24. The high inputs in July to September are apparently reflected in the up-gradient SA B changes in October at E70 and also, in this instance, at E2. The corresponding changes at E24 presumably occurred in November-December i.e. beyond the end of the sampling period. It is assumed
that the control
Station
LYI lay well beyond
any influence
of the
effluent, thus any fluctuations observed in the populations in that area are attributable to natural causes. Indeed the populations at the station remained relatively constant throughout the year in marked contrast to the instability observed in the Loch Eil populations. Notable increases in all three population statistics were observed, however, in January, and a biomass increase was apparent in August and September. The former increases are rather inexplicable but the autumn biomass increase probably arises from the normal seasonal growth of annual benthic species and thus corresponds to an expected seasonal trend in this factor. It may be that the biomass increases observed at E70 and E24 in July and August could be partially due to a like seasonal increase, but their association with fluctuations in abundance seasonal
and biomass
in the preceding
months
(see Fig. 2) suggests
that
the
factor, if any, is small.
FLUCTUATIONS
IN DOMINANT
SPECIES
Although there were considerable fluctuations in the individual numbers of the 10 dominapt (most numerous) species at each station, the proportion of these dominants to the rest of the fauna did not change much during the year at any of the stations, implying the presence of an underlying stability to the benthic community structure at each station. At the control Station, LY 1, the changes observed in the numbers of the various dominant species were relatively small and showed no discernible pattern but at the stations in Loch Eil the fluctuations in most of the dominants were large and can be interpreted in relation to fluctuation in the organic input to the loch. The relationship is most clearly seen at Station E70
POPULATION
(Fig. 5) where
FLUCTUATIONS
the large increases
in the numbers
and Capitellu from March
to May appear
effluent
Numbers
input
subsequently
in February. declined
of Tubiji’coides, Protodorvillea,
to be a direct response
of Pvotodorvillea reached
Tubtficoides also peaked
sharply.
319
IN MACROBENTHOS
to the increased
a peak in May and
in May
but maintained
relatively high numbers into June. Capitella after increasing in March declined in April, but reached its maximum numbers in June and July in association with the large spionid Scolelepis. These observations support the suggestion put forward by Pearson (in press) that Tub(fi’coide.s and Protodorvillea alternate with Capitellu and Scolelepis as the most important dominants in two competing groups of opportunist species which may replace each other in organically enriched areas. The sequence observed in this instance suggests that Tuh$coides and Protodorvillea developed large populations most rapidly following the high effluent inputs in February and that Capitella and Scolelepis reached high numbers as the other two species declined. Increases in both Capitella and Tub$coides were again recorded in October
following
further
high
effluent
inputs
in August
and
sampling stopped before these changes could be followed similar changes in the various dominant species were recorded
September,
in detail. at Station
but
Essentially E2 (Fig. 5)
with Capitella and Tub(ficoides reaching peaks in June. At this station Protodorvillea and Scolelepis were present in lower numbers, and the alternate species groupings noted at E70 were not observed. It seems that the populations at the edge of the deep basin although identical in species composition with those in the centre of the basin, were affected to a slightly lesser extent by the effluent input fluctuations in that the variations in individual species numbers were less pronounced. At the head of the Loch (Station E24) significant changes in individual species were also observed from March onwards following the effluent input increases in February. Thus the surface deposit-feeding polychaetes Chaetozone and Prionospio declined from relatively high numbers in February to very low numbers in May. The deposit-feeding lamellibranch Thyusira vanished completely from the April, May, and June samples although at the beginning of the sampling period it was one of the
most
numerous
species,
and
the
numbers
of the
surface
deposit-feeding
ampharetid polychaete Melinna fell sharply in April. Melinna populations recovered again in May and remained high until September when they again declined, possibly in response to the higher effluent inputs in that month. Thyzsira populations recovered in July but also declined again in September, while populations of Clzaetozone and Prionospio remained at fairly low levels for the rest of the sampling period.
FLUCTUATIONS
IN TROPHIC
GROUPS
The composite trends of the various changes observed in the individual species discussed above are to a large extent summarized in the trophic group changes. Thus, an increase in effluent input appears initially to favour subsurface deposit-
320
T.H.PEARSON ETAL.
feeding species at the expense of surface deposit-feeders. Some 12-16 wk after the largest population increases in deposit-feeders an increase in carnivores was recorded, presumably representing a response to the increased number of prey species. The carnivorous species, however, declined rapidly again following a further increase in effluent inputs at the end of the sampling period, thus suggesting that they were more sensitive to the consequent changes in the chemical conditions of the sediment than their prey.
CONCLUSIONS
Information presented elsewhere in this series of papers (Stanley rt al., 1981; Vance et al., 1982; Blake et al., 1982) show that the changes in effluent input discussed above brought about a series of consequential changes in the chemistry and microbiology of the sediments at the various sampling stations, most notably increases in the populations of cellulose-digesting and aerobic heterotrophic bacteria in the weeks immediately following an increase in effluent input to the Loch. At the same time significant increases in the populations of ciliates in the sediments took place (Wyatt & Pearson, 1982) and there was some evidence that meiofaunal abundance also increased simultaneously. The greatest changes recorded in the macrofauna took place between 4-8 wk after the microfaunal changes and it seems reasonable to suggest that the events are causally linked. The increasing bacterial populations must represent an abundant food source to those animals. primarily the subsurface deposit-feeders, which are adapted for their exploitation. Thus, those deposit-feeders, which are capable of surviving in the relatively low oxygen tensions and high sulphide levels of the sediment which accompany the increasing bacterial populations as carbon input to the sediments increases, must be assured of a rapid population growth, particularly as the sedimentary conditions apparently preclude the immediate build-up of predator populations. Copitella, Tub(ficoides, and Protodorvillea would appear to be in this category whereas the deposit-feeding lamellibranch Thyasira declines in numbers under these conditions. As carbon input levels decrease then populations of predatory polychaetes such as Glyccru, Goniada, and Pholoe build-up, presumably at the expense of the opportunistic deposit-feeders whose numbers decline at this stage. The time scale of these changes is relatively short. The increase in deposit-feeder populations, particularly of the small polychaetes is rapid, taking place within 46 wk of the chemical and microbiological changes of the sediment in the deep basin. The larger species of surface deposit-feeders, e.g. Melinna, in the sediments at the head of the Loch and the carnivorous polychaetes in the deep basin appear to respond within 12-14 wk of a major change in sedimentary conditions. Obviously, such response times will be a function not only of food availability but of reproductive period and interspecific competition for space. Elucidation of these
POPULATION
FLUCTUATIONS
IN MACROBENTHOS
321
aspects will require further detailed autecological studies of the dominant species in the system. Further consideration of the synecological aspects of this study is given in Pearson (1982).
REFERENCES
BLAKE, D., J.W.
LEFTLEY & C.M. BROWN, 1981. The Loch Eil Project: the bacterial flora and heterotrophic nitrogen fixation in sediments of Loch Eil. J. “up. mar. Biol. Ecol., Vol. 56, pp. 115-122. FAUCHALD, K. & P. A. JUMARS, 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Ann. Rev., Vol. 17, pp. 193-284. PEARSON, T. H., 1970. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. I. The physical environment and distribution of the macrobenthic fauna. J. exp. mar. Biol. Ecol., Vol. 5, pp. l-34. PEARSON, T. H., 197la. Studies on the ecology of the macrobenthic fauna of Lochs Linnhe and Eil, west coast of Scotland. II. Analysis of the macrobenthic fauna by comparison of feeding groups. Vie Milieu, Suppl. No. 22, pp. 53-91. PEARSON, T. H., 197lb. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. III. The effect on the benthic fauna of the introduction of pulp mill effluent. J. exp. mar. Biol. Ecol.. Vol. 6, pp. 211-233. PEARSON, T. H.. 1975. The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. IV. Changes in the benthic fauna attributable to organic enrichment. J. up. mar. Biol. Ecol.. Vol. 20. pp. l-41. PEARSON, T. H.. 1981. The Loch Eil Project: introduction and rationale. J. exp. mar. Biol. Ecol.. Vol. 55. pp. 93-102. PF~KSON. T. H., 1982. The Loch Eil Project: assessment and synthesis with a discussion of certain biological questions arising from a study of the orgamc pollution of sediments. J. e.~p. mclr. Bid. Ecol., Vol. 37, in press. PEARSON, T. H., in press. Stress and catastrophe in benthic ecosystems. In. Stress qffectson naturul ecosystems. edited by G. W. Barrett & R. Rosenberg, John Wiley & Sons, New York. PF~~RSON,T. H. & R. ROSENBERG, 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Ann. Rev.. Vol. 16. pp. 229-31 I. ST,~IULEY. S.O.. J.W. LEyrLEv, A. LIGH~FOO~. N. Roat.~r~oh. I.M. STANLEY & I. V~hct, 1981. The Loch Eil Project: sediment chemistry, sedimentation and the chemistry of. the overlying water in Loch Eil. J. exp. mar. Biol. Ecol., Vol. 55, pp. 299-313. VAKF, I., S. 0. STANLEY & C. M. BROWN, 1982. The Loch Eil Project: cellulose-degrading bacteria in the sediments of Loch Eil and the Lynn of Lorne. J. exp. mar. Biol. Ecol., Vol. 56, pp. 2677278. WYATT. C. E. & T. H. PEARSON, 1982. The Loch Eil Project: population characteristics of ciliate protozoans from organically enriched sea-loch sediments. J. exp. mar. Biol. Ecol., Vol. 56. pp. 279-303.