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Distribution of Oligochaetes in Lake Michigan and Comments on Their use as Indices of Pollution
J. Great Lakes Res. 11(1):67-76 Internat. Assoc. Great Lakes Res., 1985
DISTRIBUTION OF OLIGOCHAETES IN LAKE MICHIGAN AND COMMENTS ON THEIR USE AS INDICES OF POLLUTION
Diane D. Lauritsen!, Samuel C. Mozleyl, and David S. White Great Lakes Research Division The University of Michigan Ann Arbor, Michigan 48109 ABSTRA CT. Benthic samples were taken from 286 stations covering all areas of Lake Michigan in 1975 as part of a sedimentological survey of the Great Lakes. From these samples a total of tw~nt]: seven oligochaete species were identified. Stylodrilu~ heringianus was th.e most abu~~a~t spec!e~ m the lake and densities were inversely related to orgamc content of the sediments. Tubif,c,ds exhibited localized concentrations in Green Bay and in the northern and southern basins. Comparison of several methods using oligochaete data to assess water quality showed similar patterns, indicating that Southern Green Bay and parts of the southern and northern basins of the lake are organically enriched environments. With the exception of the northern basin, which had not previously been surveyed, these conclusions are consistent with earlier regional oligochaete surveys of the lake. T.he northern basin of Lake Michigan warrants further study to generate and test hypotheses concernmg tubificid species distributions observed there. ADDITIONAL INDEX WORDS: Great Lakes, Benthos, Eutrophication.
Extensive spatial and temporal information about standing crops of oligochaetes was provided by Alley and Mozley (1975). Their data covered about two-thirds of the lake over a 3-year period, but considered oligochaetes only at the class level. In those instances where oligochaete species distribution and abundance have been examined, the surveys have been restricted to particular regions of the lake. Noteworthy among these oligochaete surveys are Hiltunen's (1967) in the southern basin and Green Bay, Howmiller's (1974) in the central portion of the lake, and an extensive analysis of the fauna of Green Bay by Howmiller and Beeton (1971). Mozley and Howmiller (1977) summarized the knowledge of Lake Michigan Oligochaeta up to 1974, while a more recent review of the literature on Great Lakes oligochaetes is given by Spencer (1980). Our work represents the first complete lake survey of oligochaetes at the species level. Lake Michigan, third largest of the Laurentian Great Lakes, is the largest lake found entirely within the United States (57,800 km2), and has a hydraulic renewal time of 108 years. Most of the major tributaries enter the southeastern quadrant of the lake with the exception of the Fox River, which enters lower Green Bay (Fig. 1). These
INTRODUCTION The composition of the benthic fauna of lakes has long been considered to be a good indicator of water quality, since sedentary benthic organisms form relatively stable communities in the sediments and can integrate changes which reflect characteristics of both the sediments and the water column (e.g., Wiederholm 1980). Among the infauna, oligochaetes are considered one of the best groups to use as indicators of pollution or trophic status of a body of water (Milbrink 1973, Howmiller and Scott 1977). Recent laboratory studies using several common worm species have confirmed that rank order of tolerance to sewage sludge corresponds to trophic indications developed from patterns of distribution in lakes (Chapman et al. 1982a). Early surveys documented the significance of oligochaetes as a component of the benthic fauna of Lake Michigan (Eggleton 1936, Powers and Robertson 1965, Robertson and Alley 1966).
lDepartment of Zoology, North Carolina State University, Raleigh, North Carolina 27695
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LAURITSEN et al.
68
Stralta of Mackinac
Mllwa"a• • WISCONSIN ILLINOIS
MICHIGAN INDIANA
FIG. I. Map of stations for Canada Centre for Inland Waters 1977 survey of Lake Michigan.
larger tributaries are the principal source of certain contaminants to lake sediments, so that accumulation rates of organic matter, organochloride insecticides, and trace elements are greater in the central and eastern parts of the southern basin (Leland et al. 1973). Further information on morphometry, current patterns, and sediments of Lake Michigan can be found in Mortimer (1975) and Mozley and Howmiller (1977). Present results were obtained with samples from a Canada Centre for Inland Waters (C.C.I.W.) regional sedimentological study of the Laurentian Great Lakes (Cahill 1981). The entire lake was sampled within a short period of time, so that comparisons between major morphometric regions of the lake may be made by using distributional maps of important species. The intent of this paper is to focus on offshore water quality using oligochaete species as indicators. But since there is no general
consensus among researchers on the best method for analyzing and presenting oligochaete species data, we have compared several of the more recent approaches. These include the percentage of Limnodrilus hojjmeisteri relative to total oligochaetes (Brinkhurst 1967) and the oligochaete taxocene classification proposed by Mozley and Howmiller (1977). MATERIALS AND METHODS Bottom samples were collected in August, 1975, by personnel of the C.C.I.W. aboard the C.S.S. LIMNOS, using a double Shipek sampler. One of each of the 286 paired samples was used for sediment analysis by C.C.I.W., while the other sample was preserved for benthos identification. The samples were collected at the intersections of a 14- by 14km Universal Transverse Mercator (UTM) grid over most of the lake, with a 7- by 7-km UTM grid being used in Green Bay and in the northeastern corner of the lake (Fig. 1). According to C.C.I.W. staff, benthos samples were washed in the field using a sieve with openings 0.25 mm wide. The residue containing the animals was then fixed with 4070 buffered formalin and the samples were taken to the laboratory, where they were elutriated in a device similar to that described by Worswick and Barbour (1974). The elutriated samples were again preserved in 4% formalin and placed in jars. Some of the samples were sorted into major taxa at C.C.I.W., with the use of a dissecting microscope. Sorted and unsorted samples were brought to the Great Lakes and Marine Waters Center laboratories at the University of Michigan, where sorting was completed and organisms were identified. Oligochaetes were mounted on glass slides using lactophenol and were examined under 40X or greater magnification using the keys of Hiltunen (unpubl. mimeo., now Hiltunen and Klemm 1980) and Brinkhurst and Jamieson (1971). All Naididae, Stylodrilus heringianus, Spirosperma jerox, and Limnodrilus udekemianus could be identified at the species level, while other oligochaetes could be identified to species only when mature; immature specimens were sorted into the categories "with-" or "without hair chaetae." The oligochaete species found at each station were assigned to one of four groups based on the trophic index proposed by Mozley and Howmiller (1977; Table 2). Numbers of worms in each group were totaled and the numerically dominant group determined the trophic classification of the sample station.
69
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN Species distributions were analyzed for depth and regional trends by analysis of variance of log transformed data using the MIDAS computer system at the University of Michigan. RESULTS Sediments Some of the relevant sediment data collected by C.C.I.W. are included here for comparison with oligochaete distributions; a complete report of sediment data can be found in Cahill (1981). Since sediment texture was finest at the deeper offshore stations and displayed the same pattern as percentage organic carbon content of the sediments, we have included only a map of the latter to illustrate the trend. Organic carbon in sediments was highest in Green Bay, the southeastern part of the lake, and in several pockets in the northern basin (Fig. 2). Oligochaete Distributions The lake was· divided into three major basins to facilitate comparisons with earlier oligochaete studies. The southern basin was represented by sample sites south of a line between Milwaukee, Wisconsin, and Grand Haven, Michigan, and the northern basin was separated from the central basin by a line drawn between Manitowoc, Wisconsin, and Ludington, Michigan. Green Bay was considered separately from the northern basin. Twenty-seven species of oligochaetes were identified from the survey, representing 1 Lumbriculidae, 6 Naididae, and 18 Tubificidae (Table 1); none of these were new distributional records. The enchytraeids examined were split into two groups, dependent upon the number of chaetae per bundle. The group referred to as "Species 1" consisted of those individuals having 2-4 chaetae per bundle (this group includes the genus Lumbricillus-J. Hiltunen, personal communication, Great Lakes Fishery Laboratory, U.S. Fish and Wildlife Service, Ann Arbor, Michigan); the "Species 2" group consisted of those having 5 or more chaetae per bundle. Possibly two or more species were represented in each group, but the taxonomy of the family is poorly known in North America and no species names can be attached at this time. Although mean densities of oligochaetes in each basin and Green Bay were quite similar (470 m- 2 in the southern basin, 488 m- 2 in the central basin, 410 m-2 in the northern basin, and 353 m-2 in Green
Organic C. % 0-1
_1-3
_>5
_3-5
FIG. 2. Percentage of organic carbon in sediment samples from the 1977 survey of Lake Michigan.
Bay), highest densities were found in the southeastern part of the lake. The lumbriculid Stylodrilus heringianus was the most abundant oligochaete found in the lake, comprising 73 % of total oligochaetes. It was distributed throughout the lake except for Green Bay and the deepest portions of the northern and southern basins (Fig. 3). Low densities at some deep stations appeared to be inversely related to organic content
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LAURITSEN et al.
TABLE 1. Species list of Oligochaeta collected from 1975 Lake Michigan benthic survey. Enchyt raeidae Lumbriculidae Sty/odr ilus heringianus Naididae Arcteo nais /omond i (Martin) Chaetogaster diaphanus (Gruithuisen) Nais a/pina Sperber N. variabilis Piguet Sty/aria /acustris (Linnaeus) Vejdovskyella intermedia (Bretscher) Tubificidae Au/odd /us pigueti Kowalewski A. p/uriseta (Piguet) I/yodrilus temp/e toni (Southern) Limnod rilus angustipenis Brinkh urst and Cook L. c1aparedeianus Ratzel L. hoffme isteri Clapar ede L. profun dico/a (Verrill) L. spira/is (variant of L. hoffme isteri?) L. udekem ianus Clapar ede Spirosperma ferox (Eisen) S. niko/sk yi (Lastoc hkin adn Sokolskaya) Isochaetides freyi (Brinkhurst) Potamo thrix vejdovs kyi (Hrabe ) P. mo/daviensis Vejdovsky and Mrazek Rhyaco drilus coccineus (Vejdovsky) Tubifex tubifex (Muller) T. kess/eri americanus Brinkh urst and Cook T. superiorensis (Brinkh urst and Cook)
of the sediments, but an ANOVA of S. heringianus distribution versus organic carbon content of the sediments was not statistically significant. Tubificids (including all immature as well as mature individuals) were most abund ant in Green Bay, the northe rnmos t part of the lake west of the Straits of Mackinac, and along the eastern side of the central and southern basins (Fig. 4). This pattern was repeated in the distribution of mature Limnodrilus hoffmeisteri, with the highest densities in the southeastern portio n of the lake (Fig. 5). Limnodrilus profundicola was most abund ant at deeper (greater than 60 m) stations in the central and northe rn basins (max. density 280 m-2). Potamothr ix moldaviensis was found in low densities (max. 160 m-2) exclusively in the southeastern portion of the lake. Spirosperma ferox was also limited in distribution, being found in low densities in Green Bay and in high densities (100-1,200 m-2) at stations west of the Straits of Mackinac in the
FIG. 3. Distrib ution of Stylodrilus heringianus in Lake Michigan, summe r 1977. The first contou r line delineates areas of < 100 S. heringianus om-2; the second contour < 500 om-2; the third contou r < 900 om-2; and the fourth, indicated in black, >900 om-2• Asteris ks indicate areas of < 100 om-2 within higher density areas.
northe rn basin. Tubifex tubifex was the most abund ant tubificid with hair chaetae and was found primarily at deeper stations (max. density 200 m-2). Tubifex kessleri americanus was present in low densities (max. 80 m-2) in the eastern half of the lake. Both enchytraeid taxa were more abund ant in the central and northe rn basins but densities were low (max. density "Species I" -160 m-2; "Species 2" - 240 m-2) and they were found only rarely. Because this survey included few shallow stations
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
71
FIG. 4. Distribution oftotal Tubificidae in Lake Michigan, summer 1977. The first contour line delineates areas of < 100 total tubificids om-2; the second contour < 500 om-2; the third contour < 1,000 om-2; and the fourth, indicated in black, > 1,000 om-2•
FIG. 5. Distribution of Limnodrilus hoffmeisteri in Lake Michigan, summer 1977. The first contour line delineates areas of < 100 L. hoffmeisteri om-2; the second contour, <200 om-2; the third contour <500 om-2; and the fourth, indicated in black, >500 om-2•
(less than 30 m), Naididae were also found infrequently, and comprised less than 1% of total oligochaetes averaged over the whole lake.
basins, with the highest densities at shallower depths (less than 60 m) in the southern basin. However, two-way analysis of variance on log transformed densities using basin and depth as treatments indicated that these differences were not significant (p > .05). Because of the lack of replication, variances were high and often unequal, so that statistically significant inferences were difficult to make with this data set. In the northern basin, tubificids were absent from 40 to 60-m and 80 to tOO-m depths, and in the central
Depth Distributions of Oligochaetes In the southern and central basins, Sty/odri/us densities were highest in the 30- to 50-m depth interval, while in the northern basin the depth distribution was not as pronounced (Fig. 6). There appeared to be a difference in abundance of tubificids between
LAURITSEN et al.
72 6
1200
NORTHERN
3
800
basin densities were highest at the 30 to 40-m and 150 to 200-m depth intervals. Enchytraeids were absent from depths of less than 20 m and greater than 150 m and showed no obvious depth-related trends in any of the basins. Naidids were found almost exclusively in the 10 to 20-m depth interval in the northern and southern basins (there were no shallow sample stations in the central basin; Fig. 6).
Green Bay and Grand Traverse Bay samples were not included in Figure 6; in Green Bay, tubificids were the dominant oligochaetes found (usually > 80% of total oligochaetes) at shallow « 40 m) depths. In Grand Traverse Bay, Stylodrilus was dominant at shallow depths « 50 m) and tubificids were dominant at > 50 m depths.
400
2
CENTRAL 800
....E
oz 400
2
1600
SOUTHERN 1200 5
5 5 400
14 14 5
10
30
50
70
DEPTH
90
150200250
(m)
FIG. 6. Densities of total oligochaetes, averaged by depth intervals in three arbitrarily defined basins of the main body of Lake Michigan, summer 1977. Insets show densities of total Tubificidae (vertically hatched), Stylodrilus (white), total Enchytraeidae (black), and total Naididae (spots). The number of samples is indicated above each depth interval for the three basins.
DISCUSSION Benthic environmental variations in Lake Michigan are strongly related to depth. Typical profundal faunal patterns show increasing densities and species richness in the 20- to 50-m depth interval; with greater depth both variables then decrease. Near the 20-m depth contour, physical and chemical environments change as the effects of wave action on the benthic environment diminish (Mozley and Garcia 1972, Mortimer 1975). Influxes of organic sediments and contaminants to the benthic environment increase rapidly with depth and the proportion of silt and clay in the sediments after 20 m, and regional variations in the 20- to 50-m depth interval are greater because of proximity to major sources of allochthonous material (Mozley and Alley 1973). Thus local pollution should be most evident in oligochaete communities at these depths. Analysis of sediment samples collected on the CCIW cruise of Lake Michigan showed significant differences in trace element content between depositional and non-depositional areas of the lake and between surficial and buried sediments (Cahill 1981). Bromine, chromium, copper, lead, and zinc showed higher enrichment in depositional areas (with finer-grained sediments) and these areas roughly correspond to the areas of higher sediment organic carbon content, shown in Figure 2 (Cahill 1981). Because of the high variability in this data set, no statistically significant differences were found in regional c~mparisons of depth distributions of tubificids and Stylodrilus. The following discussion is based on inferences made from the distribution maps.
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
Sty/odri/us heringianus was the most common oligochaete in all but the shallowest depths of the lake and its distribution illustrates the depth pattern described by Mozley and Alley (1973) for total oligochaetes in each basin of the lake. A number of studies have indicated that S. heringianus is most abundant where sediment organic content is low, but we could not make a significant correlation using this data set. Tubificids were more common at mid-depths of 20-60 m in the southern basin. This trend has been observed by other researchers (Mozley and Howmiller 1977) and is generally attributed to higher rates of sedimentation of organic matter at these depths (Mozley and Alley 1973). But in the northern basin, tubificid densities were greatest at shallower depths of 10-40 m, and many areas of highest tubificid density did not have organically enriched sediments. Brinkhurst and Jamieson (1971) have noted that where careful analyses have been made, few clear correlations between the variations of total organic matter and the distribution and abundance of worms have been demonstrated. Recent work indicates that tubificid sediment preferences are a result of the bacterial abundance in the sediments (McMurtry et a/. 1983) and there may be no correlation between the quantity of bacteria and the organic content of the sediments (e.g., Drabkova 1983). Enchytraeid densities exhibit a distribution pattern similar to that of Sty/odri/us. As with naidids, these small worms are easily lost when sieving benthic samples and were probably underrepresented in this survey. Total oligochaete densities were lower than previously reported for comparable areas of the lake (e.g., Howmiller 1974, Hiltunen 1967, Howmiller and Beeton 1971) and this is probably attributable to the inefficiency of the Shipek sampler (Flannagan 1970). This inefficiency is most pronounced at depths less than 60 m (N. Watson, personal communication, Canada Centre for Inland Waters, Burlington, Ontario), where the greatest· oligochaete densities are found in Lake Michigan. Early studies in Lake Michigan have included the ratio of amphipods to oligochaetes (Powers and Robertson 1965, Ayers and Huang 1967), and density of oligochaetes (Mozley and Alley 1973) as benthic indices of pollution. However, because they are numerical criteria, results are dependent upon type of grab sampler used and mesh size of sieves used to wash samples so that comparisons between data sets are often difficult to make.
73
Much better assessment may be achieved with information on relative densities of particular species. For example, a high relative abundance of Sty/odri/us heringianus is usually accepted as evidence that an area receives little organic enrichment (Howmiller and Beeton 1971, Milbrink 1973). Upward of 80010 S. heringianus were found in deeper portions of the lake where organic carbon content of the sediments was not high. Brinkhurst (1967) suggested that the percentage of the tubificid Limnodrilus hoffmeistri in relation to other oligochaetes may be a useful index of organic pollution, with a higher relative abundance indicating more enriched areas. Combining all immature tubificids without hair chaetae to total numbers of mature L. hoffmeisteri gave high percentages (80-100%) in the southern basin, the lower two-thirds of Green Bay, and the northernmost portion of the lake. These results reflect the distribution pattern of the species shown in Figure 5, and with the exception of the northern area, are similar to the known or expected patterns of organic enrichment of sediments in the lake, suggesting that extensive areas of Lake Michigan are enriched or polluted. Oligochaete communities,· or taxocenes, have been widely used in recent years as indicators of pollution, particularly by European biologists working on large inland lakes (Milbrink 1980, Lang and Lang-Dobler 1980). This approach depends upon differences among oligochaete species in physiological tolerance of direct or indirect effects of sediment pollution. As pollution increases, species replace each other and the com..; position of the taxocene shifts. Species have been generally characterized by their distribution patterns in areas with known or suspected pollution or enrichment (Brinkhurst et a/. 1968), and laboratory testing of common species has verified these field observations (Chapman et a/. 1982a). This can be explained by the relative abilities of the species to live anaerobically when oxygen is depleted, but oligotrophic species can be more tolerant of certain heavy metals, pesticides, and industrial wastes than eutrophic species (Chapman et a/. 1982a). Therefore, the established taxocene-based assessments must refer primarily to pollution by readily degradable organic matter. Higher temperature can affect oligochaete behavior and/or physiology, increasing toxic reactions so that the same level of organic pollution would have a greater influence on taxocene composition in warmer, shallower habitats.
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LAURITSEN et al.
In the Great Lakes, analysis of oligochaete taxocene structure and classification according to pollution tolerance has centered around Howmiller's studies of Green Bay (Howmiller and Scott 1977, Mozley and Howmiller 1977). Howmiller's first system divides common Great Lakes species into four groups according to degree of tolerance to enrichment of the benthic environment (Table 2; Mozley and Howmiller 1977). This classification was later modified and reduced to three categories and included all naidid oligochaetes in the mesotrophic category (Howmiller and Scott 1977). We feel that the earlier, four-category classification is more precise, and that because of their life histories and feeding behaviors, naidids should not be grouped as mesotrophic indicators. When stations were assigned to one of four categories based on the numerically dominant species group, the only area of the lake to show gross organic enrichment was southern Green Bay (Fig. 7); this corresponds with observations made by Howmiller and Beeton (1970). Areas of slight and extreme enrichment are scattered around the lake,
TABLE 2. Classification of common Oligochaetes according to the degree of organic enrichment of the environment (Type I-oligotrophic; Type II- mesotrophic; Type III- saprophilic; Type IV- saprobionts; from Mozley and Howmiller 1977, with permission). Environment Type Species
Sty/odTi/us heringianus Spirosperma niko/skyi Limnodrilus profundico/a Tubifex superiorensis Tubifex kess/eTi Rhyacodrilus montana Rhyacodrilus coccineus Spirosperma ferox Isochaetides freyi Ilyodrilus temp/etoni Potamothrix mo/daviensis Potamothrix vejdovskyi Au/odrilus spp. Limnodrilus hoffmeisteri Limnodrilus udekemianus Limnodrilus angustipenis Tubifex tubifex Limnodrilus cervix Limnodrilus claparedeianus Limnodrilus maumeensis Quistadrilus multisetosus
II
III
•
•
•• TYPE I-OLIGOTROPHIC •
TYPE II-MESOTROPHIC
•
TYPE III-SAPROPHILIC
•
TYPE IV-SAPROBIONTS
FIG. 7. Oligochaete species groups (taxocenes) according to environment type (cf. Table 1) based on densities from the summer 1977 survey of Lake Michigan.
IV
x X X X X X X X X X X X X
X X X
X X X X X
including most of Green Bay, much of the northernmost part of the lake, and nearshore areas in the southern basin. The results of the taxocene classification show the same general patterns as the percentage L. hoffmeisteri index, but the former has an advantage in that it is not dependent upon the presence of only one oligochaete species. However, uncertainty still remains regarding the environmental responses of certain oligochaete species included in the taxocene classification. For example, Tubifex tubifex can be quite abundant in polluted areas and also in deeper areas of lakes where there are few other oligochaete species present, indicating that it may be sensitive to competition (Milbrink 1973). But it is also highly tolerant of sewage sludge (Chapman et al. 1982a). Milbrink (1983) has suggested that T. tubifex be given a dual ecological ranking - as a eutrophic
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
indicator when it is found in association with Limnodrilus hoffmeisteri, and as an oligotrophic indicator when it is found in association with other oligotrophic species. Potamothrix vejdovskyi is considered a mesotrophic indicator by Mozley and Howmiller (1977), while Milbrink (1973) suggested that it does best in polluted conditions. It may be an opportunistic species-for example, Nalepa and Thomas (1976) reported very high densities of P. vejdovskyi near the Niagara River inflow into Lake Ontario. Spirosperma ferox (as Peloscolex) has long been considered as an oligotrophic indicator in European lakes (Milbrink 1980). Not all European biologists agree with that claim however; Lang (1978) believed that S. ferox indicates eutrophic conditions. In laboratory tests, it was less tolerant of sewage sludge than any other species tested (Chapman et al. 1982a). Mozley and Howmiller (1977) considered this species to be a mesotrophic indicator in the Great Lakes. Because of the interactions between biotic and abiotic factors, we are not yet able to predict precisely the responses of species in situ to specific environmental conditions or toxins. For example, sediments often serve to ameliorate the effects of toxic substances (Chapman et al. 1982a), as can biological interactions between oligochaete species (Chapman et al. 1982b). Further experimental research on species responses to pollutants should help to refine the oligochaete taxocene classification system, and allow us to make better use of benthic invertebrates as indicators of water quality. The present work is the first lake-wide survey of Lake Michigan in which oligochaetes were identified to the species level. Since it was based solely on a systematic sampling design, it has statistical disadvantages, but provides a strong basis for rational design of future surveys and hypothesisoriented research. The data (available on magnetic tape from the U.S. Environmental Protection Agency or the Great Lakes and Marine Waters Center, University of Michigan) will support analysis of sampling design efficiency, definition of appropriate spatial strata, and future regional or whole-lake surveillance for temporal trends in water quality. CONCLUSIONS
Although oligochaete densities from the present survey were lower than have been previously reported for the lake, the general patterns of species' distributions (Stylodrilus heringianus domi-
75
nant at greater depths; eutrophic species such as Limnodrilus hoffmeisteri abundant in Green Bay and nearshore areas in the southern part of the lake) were consistent with earlier regional studies. An exception was the previously unsampled northern portion of the lake which contained a majority of eutrophic species, in contrast with what might be expected given the distance from major sources of nutrient or organic loading. Certainly more sampling is warranted to elucidate patterns of species distributions and causal factors in this part of the lake. Use of taxocene classifications (such as Mozley and Howmiller 1977) can aid in making comparisons between different areas in a body of water; additional experimental toxicity testing including the other common oligochaete species of the region should help to refine such indices and broaden their usefulness. ACKNOWLEDGMENTS
This research was supported by the U.S. Environmental Protection Agency, grant number R805333010. We would like to thank Z. BatacCatalan, C. Millenbach, M. Wiley, and M. Winnell for assistance with data handling. This manuscript has been improved by suggestions from a number of people, including P. Bradbury, L. Crowder, T. Nalepa, T. Wentworth, and an anonymous reviewer. Contribution number 404, Great Lakes Research Division, The University of Michigan. Paper No. 9601 of the Journal Series of the North Carolina Agricultural Research Service, Raleigh, NC 27695-7601. REFERENCES Alley, W. P., and Mozley, S. C. 1975. Seasonal abundance and spatial distribution of Lake Michigan macrobenthos, 1964-67. University of Michigan, Great Lakes Research Division Special Report #54. Ayers,J. C.,andHuang,J. C. K.1967.StudiesofMilwaukee Harbor and embayment. In Studies on the Environment and Eutrophication of Lake Michigan, ed. J. C. Ayers and D. C. Chandler, pp. 372-394. University of Michigan Great Lakes Research Division Special Report #30. Brinkhurst, R. O. 1967. The distribution of aquatic oligochaetes in Saginaw Bay, Lake Huron. Limnol. Oceanogr. 12:137-143. ' ____ , and Jamieson, B. G. M. 1971. Aquatic Oligochaeta of the World. Edinburgh: Oliver and Boyd. ____ , Hamilton, A. L., and Herrington, H. B. 1968. Components of the bottom fauna of the St. Lawrence Great Lakes. Univ. Toronto Great Lakes Inst. No. PR 33:1-49.
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Cahill, R. A. 1981. Geochemistry ofrecent Lake Michigan sediments. Ill. State Geol. Survey Div. Circ. #517. Chapman, P. M., Farrell, M. A. and Brinkhurst, R. O. 1982a. Relative tolerances of selected aquatic oligochaetes to individual pollutants and environmental factors. Aquat. Toxicol. 2:47-67. ____ , Farrell, M. A., and Brinkhurst, R. O. 1982b. Effects of species interactions on the survival and respiration of Limnodrilus hoffmeisteri and Tubifex tubifex (Oligochaeta, Tubificidae) exposed to various pollutants and environmental factors. Water Res. 16:1405-1408. Drabkova, V. G. 1983. Bacterial decomposition of organic matter in lacustrine sediments. Hydrobiol. 103:99-102. Eggleton, F. E. 1936. The deep water bottom fauna of Lake Michigan. Pap. Mich. A cad. Sci. Arts Lett. 22:593-611. Flannagan, J. F. 1970. Efficiencies of various grabs and corers in sampling freshwater benthos. J. Fish. Res. Board Can. 27:1691-1700. Hiltunen, J. K. 1967. Some oligochaetes from Lake Michigan. Trans. A mer. Microsc. Soc. 86:433-454. ____ , and Klemm, D. J. 1980. A guide to the Naididae (Annelida: Clitellata: Oligochaeta) of North America. U.S. Environmental Protection Agency Report No. EPA-6oo/4-80-031, Office of Research and Development. Howmiller, R. P. 1974. Composition of the oligochaete fauna of central Lake Michigan. In Proceedings 17th Conf. Great Lakes Res., pp. 589-592. Internat. Assoc. Great Lakes Res. ____ , and Beeton, A. M. 1970. The oligochaete fauna of Green Bay, Lake Michigan. In Proceedings 13th Conf. Great Lakes Res., pp. 15-46. Internat. Assoc. Great Lakes Res. ____ , and Scott, M. A. 1977. An environmental index based on relative abundance of oligochaete species. J. Water Poll. Cont. Fed. 49:809-815. Lang, C. 1978. Factorial correspondence analysis of Oligochaeta communities according to eutrophical level. Hydrobiol. 57:241-247. ____ , and Lang-Dobler, B. 1980. Structure of tubificid and lumbriculid worm communities, and three indices of trophy based upon these communities as descriptors of eutrophication level of Lake Geneva (Switzerland). In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 457-470. New York: Plenum Press. Leland, H. V., Shukla, S. S., and Shimp, N. F. 1973. Factors affecting disribution of lead and other trace elements in sediments of southern Lake Michigan. In Trace Metals and Metal-organic Interactions in Natural Waters, ed. P. C. Singer, pp. 89-129. Ann Arbor: Ann Arbor Science Pub I.
McMurty, M. J., Rapport, D. J., and Chua, K. E. 1983. Substrate selection by tubificid oligochaetes. Can. J. Fish. Aquat. Sci. 40:1639-1646. Milbrink, G. 1973. On the use of indicator communities of Tubificidae and some Lumbriculidae in the assessment of water pollution in Swedish lakes. Zoon. 1:125-139. ____ .1980. Oligochaete communities in pollution biology: The European situation with special reference to lakes in Scandinavia. In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 433-455. New York: Plenum Press. ____ . 1983. An improved environmental index based on the relative abundance of oligochaete species. Hydrobiol. 102:89-97. Mortimer, C. H. 1975. Environmental status of the Lake Michigan region: Physical limnology of Lake Michigan. Argonne National Lab. Report No. ANL/ ES-40, Vol. 2, U.S. Energy Research and Development Administration. Mozley, S. C., and Alley, W. P. 1973. Distribution of benthic invertebrates in the south end of Lake Michigan. In Proceedings 16th Conf. Great Lakes Res., pp. 87-96. Internat. Assoc. Great Lakes Res. ____ , and Garcia, L. C. 1972. Benthic macrofauna in the coastal zone of Southeastern Lake Michigan. In Proc. 15th Conf. Great Lakes Res., pp. 102-116. Internat. Assoc. Great Lakes Res. ____ , and Howmiller, R. P. 1977. Environmental status of the Lake Michigan region: Zoobenthos of Lake Michigan. Argonne National Lab. Report No. ANL/ES-40, Vol. 6, U.S. Energy Research and Development Administration. Nalepa, T. F., and Thomas, N. A. 1976. Distribution of macrobenthic species in Lake Ontario in relation to source of pollution and sediment parameters J. Great Lakes Res. 2:150-163. Powers, C. F., and Robertson, A. 1965. Some quantitative aspects of the macrobenthos of Lake Michigan. In Proceedings 8th Conf. Great Lakes Res., pp. 153-159. University of Michigan, Great Lakes Research Division Publ. #13. Robertson, A., and Alley, W. P. 1966. A comparative study of Lake Michigan macrobenthos. Limnol. Oceanogr. 11:576-583. Spencer, D. R. 1980. The aquatic Oligochaeta of the St. Lawrence Great Lakes region. In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 115-164. New York: Plenum Press. Wiederholm, T. 1980. Use of benthos in lake monitoring. J. Water Poll. Cont. Fed. 52:537-547. Worswick, J. M., and Barbour, M. T. 1974. An elutriation apparatus for macroinvertebrates. Limnol. Oceanogr. 19:538-540.
DISTRIBUTION OF OLIGOCHAETES IN LAKE MICHIGAN AND COMMENTS ON THEIR USE AS INDICES OF POLLUTION
Diane D. Lauritsen!, Samuel C. Mozleyl, and David S. White Great Lakes Research Division The University of Michigan Ann Arbor, Michigan 48109 ABSTRA CT. Benthic samples were taken from 286 stations covering all areas of Lake Michigan in 1975 as part of a sedimentological survey of the Great Lakes. From these samples a total of tw~nt]: seven oligochaete species were identified. Stylodrilu~ heringianus was th.e most abu~~a~t spec!e~ m the lake and densities were inversely related to orgamc content of the sediments. Tubif,c,ds exhibited localized concentrations in Green Bay and in the northern and southern basins. Comparison of several methods using oligochaete data to assess water quality showed similar patterns, indicating that Southern Green Bay and parts of the southern and northern basins of the lake are organically enriched environments. With the exception of the northern basin, which had not previously been surveyed, these conclusions are consistent with earlier regional oligochaete surveys of the lake. T.he northern basin of Lake Michigan warrants further study to generate and test hypotheses concernmg tubificid species distributions observed there. ADDITIONAL INDEX WORDS: Great Lakes, Benthos, Eutrophication.
Extensive spatial and temporal information about standing crops of oligochaetes was provided by Alley and Mozley (1975). Their data covered about two-thirds of the lake over a 3-year period, but considered oligochaetes only at the class level. In those instances where oligochaete species distribution and abundance have been examined, the surveys have been restricted to particular regions of the lake. Noteworthy among these oligochaete surveys are Hiltunen's (1967) in the southern basin and Green Bay, Howmiller's (1974) in the central portion of the lake, and an extensive analysis of the fauna of Green Bay by Howmiller and Beeton (1971). Mozley and Howmiller (1977) summarized the knowledge of Lake Michigan Oligochaeta up to 1974, while a more recent review of the literature on Great Lakes oligochaetes is given by Spencer (1980). Our work represents the first complete lake survey of oligochaetes at the species level. Lake Michigan, third largest of the Laurentian Great Lakes, is the largest lake found entirely within the United States (57,800 km2), and has a hydraulic renewal time of 108 years. Most of the major tributaries enter the southeastern quadrant of the lake with the exception of the Fox River, which enters lower Green Bay (Fig. 1). These
INTRODUCTION The composition of the benthic fauna of lakes has long been considered to be a good indicator of water quality, since sedentary benthic organisms form relatively stable communities in the sediments and can integrate changes which reflect characteristics of both the sediments and the water column (e.g., Wiederholm 1980). Among the infauna, oligochaetes are considered one of the best groups to use as indicators of pollution or trophic status of a body of water (Milbrink 1973, Howmiller and Scott 1977). Recent laboratory studies using several common worm species have confirmed that rank order of tolerance to sewage sludge corresponds to trophic indications developed from patterns of distribution in lakes (Chapman et al. 1982a). Early surveys documented the significance of oligochaetes as a component of the benthic fauna of Lake Michigan (Eggleton 1936, Powers and Robertson 1965, Robertson and Alley 1966).
lDepartment of Zoology, North Carolina State University, Raleigh, North Carolina 27695
67
LAURITSEN et al.
68
Stralta of Mackinac
Mllwa"a• • WISCONSIN ILLINOIS
MICHIGAN INDIANA
FIG. I. Map of stations for Canada Centre for Inland Waters 1977 survey of Lake Michigan.
larger tributaries are the principal source of certain contaminants to lake sediments, so that accumulation rates of organic matter, organochloride insecticides, and trace elements are greater in the central and eastern parts of the southern basin (Leland et al. 1973). Further information on morphometry, current patterns, and sediments of Lake Michigan can be found in Mortimer (1975) and Mozley and Howmiller (1977). Present results were obtained with samples from a Canada Centre for Inland Waters (C.C.I.W.) regional sedimentological study of the Laurentian Great Lakes (Cahill 1981). The entire lake was sampled within a short period of time, so that comparisons between major morphometric regions of the lake may be made by using distributional maps of important species. The intent of this paper is to focus on offshore water quality using oligochaete species as indicators. But since there is no general
consensus among researchers on the best method for analyzing and presenting oligochaete species data, we have compared several of the more recent approaches. These include the percentage of Limnodrilus hojjmeisteri relative to total oligochaetes (Brinkhurst 1967) and the oligochaete taxocene classification proposed by Mozley and Howmiller (1977). MATERIALS AND METHODS Bottom samples were collected in August, 1975, by personnel of the C.C.I.W. aboard the C.S.S. LIMNOS, using a double Shipek sampler. One of each of the 286 paired samples was used for sediment analysis by C.C.I.W., while the other sample was preserved for benthos identification. The samples were collected at the intersections of a 14- by 14km Universal Transverse Mercator (UTM) grid over most of the lake, with a 7- by 7-km UTM grid being used in Green Bay and in the northeastern corner of the lake (Fig. 1). According to C.C.I.W. staff, benthos samples were washed in the field using a sieve with openings 0.25 mm wide. The residue containing the animals was then fixed with 4070 buffered formalin and the samples were taken to the laboratory, where they were elutriated in a device similar to that described by Worswick and Barbour (1974). The elutriated samples were again preserved in 4% formalin and placed in jars. Some of the samples were sorted into major taxa at C.C.I.W., with the use of a dissecting microscope. Sorted and unsorted samples were brought to the Great Lakes and Marine Waters Center laboratories at the University of Michigan, where sorting was completed and organisms were identified. Oligochaetes were mounted on glass slides using lactophenol and were examined under 40X or greater magnification using the keys of Hiltunen (unpubl. mimeo., now Hiltunen and Klemm 1980) and Brinkhurst and Jamieson (1971). All Naididae, Stylodrilus heringianus, Spirosperma jerox, and Limnodrilus udekemianus could be identified at the species level, while other oligochaetes could be identified to species only when mature; immature specimens were sorted into the categories "with-" or "without hair chaetae." The oligochaete species found at each station were assigned to one of four groups based on the trophic index proposed by Mozley and Howmiller (1977; Table 2). Numbers of worms in each group were totaled and the numerically dominant group determined the trophic classification of the sample station.
69
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN Species distributions were analyzed for depth and regional trends by analysis of variance of log transformed data using the MIDAS computer system at the University of Michigan. RESULTS Sediments Some of the relevant sediment data collected by C.C.I.W. are included here for comparison with oligochaete distributions; a complete report of sediment data can be found in Cahill (1981). Since sediment texture was finest at the deeper offshore stations and displayed the same pattern as percentage organic carbon content of the sediments, we have included only a map of the latter to illustrate the trend. Organic carbon in sediments was highest in Green Bay, the southeastern part of the lake, and in several pockets in the northern basin (Fig. 2). Oligochaete Distributions The lake was· divided into three major basins to facilitate comparisons with earlier oligochaete studies. The southern basin was represented by sample sites south of a line between Milwaukee, Wisconsin, and Grand Haven, Michigan, and the northern basin was separated from the central basin by a line drawn between Manitowoc, Wisconsin, and Ludington, Michigan. Green Bay was considered separately from the northern basin. Twenty-seven species of oligochaetes were identified from the survey, representing 1 Lumbriculidae, 6 Naididae, and 18 Tubificidae (Table 1); none of these were new distributional records. The enchytraeids examined were split into two groups, dependent upon the number of chaetae per bundle. The group referred to as "Species 1" consisted of those individuals having 2-4 chaetae per bundle (this group includes the genus Lumbricillus-J. Hiltunen, personal communication, Great Lakes Fishery Laboratory, U.S. Fish and Wildlife Service, Ann Arbor, Michigan); the "Species 2" group consisted of those having 5 or more chaetae per bundle. Possibly two or more species were represented in each group, but the taxonomy of the family is poorly known in North America and no species names can be attached at this time. Although mean densities of oligochaetes in each basin and Green Bay were quite similar (470 m- 2 in the southern basin, 488 m- 2 in the central basin, 410 m-2 in the northern basin, and 353 m-2 in Green
Organic C. % 0-1
_1-3
_>5
_3-5
FIG. 2. Percentage of organic carbon in sediment samples from the 1977 survey of Lake Michigan.
Bay), highest densities were found in the southeastern part of the lake. The lumbriculid Stylodrilus heringianus was the most abundant oligochaete found in the lake, comprising 73 % of total oligochaetes. It was distributed throughout the lake except for Green Bay and the deepest portions of the northern and southern basins (Fig. 3). Low densities at some deep stations appeared to be inversely related to organic content
70
LAURITSEN et al.
TABLE 1. Species list of Oligochaeta collected from 1975 Lake Michigan benthic survey. Enchyt raeidae Lumbriculidae Sty/odr ilus heringianus Naididae Arcteo nais /omond i (Martin) Chaetogaster diaphanus (Gruithuisen) Nais a/pina Sperber N. variabilis Piguet Sty/aria /acustris (Linnaeus) Vejdovskyella intermedia (Bretscher) Tubificidae Au/odd /us pigueti Kowalewski A. p/uriseta (Piguet) I/yodrilus temp/e toni (Southern) Limnod rilus angustipenis Brinkh urst and Cook L. c1aparedeianus Ratzel L. hoffme isteri Clapar ede L. profun dico/a (Verrill) L. spira/is (variant of L. hoffme isteri?) L. udekem ianus Clapar ede Spirosperma ferox (Eisen) S. niko/sk yi (Lastoc hkin adn Sokolskaya) Isochaetides freyi (Brinkhurst) Potamo thrix vejdovs kyi (Hrabe ) P. mo/daviensis Vejdovsky and Mrazek Rhyaco drilus coccineus (Vejdovsky) Tubifex tubifex (Muller) T. kess/eri americanus Brinkh urst and Cook T. superiorensis (Brinkh urst and Cook)
of the sediments, but an ANOVA of S. heringianus distribution versus organic carbon content of the sediments was not statistically significant. Tubificids (including all immature as well as mature individuals) were most abund ant in Green Bay, the northe rnmos t part of the lake west of the Straits of Mackinac, and along the eastern side of the central and southern basins (Fig. 4). This pattern was repeated in the distribution of mature Limnodrilus hoffmeisteri, with the highest densities in the southeastern portio n of the lake (Fig. 5). Limnodrilus profundicola was most abund ant at deeper (greater than 60 m) stations in the central and northe rn basins (max. density 280 m-2). Potamothr ix moldaviensis was found in low densities (max. 160 m-2) exclusively in the southeastern portion of the lake. Spirosperma ferox was also limited in distribution, being found in low densities in Green Bay and in high densities (100-1,200 m-2) at stations west of the Straits of Mackinac in the
FIG. 3. Distrib ution of Stylodrilus heringianus in Lake Michigan, summe r 1977. The first contou r line delineates areas of < 100 S. heringianus om-2; the second contour < 500 om-2; the third contou r < 900 om-2; and the fourth, indicated in black, >900 om-2• Asteris ks indicate areas of < 100 om-2 within higher density areas.
northe rn basin. Tubifex tubifex was the most abund ant tubificid with hair chaetae and was found primarily at deeper stations (max. density 200 m-2). Tubifex kessleri americanus was present in low densities (max. 80 m-2) in the eastern half of the lake. Both enchytraeid taxa were more abund ant in the central and northe rn basins but densities were low (max. density "Species I" -160 m-2; "Species 2" - 240 m-2) and they were found only rarely. Because this survey included few shallow stations
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
71
FIG. 4. Distribution oftotal Tubificidae in Lake Michigan, summer 1977. The first contour line delineates areas of < 100 total tubificids om-2; the second contour < 500 om-2; the third contour < 1,000 om-2; and the fourth, indicated in black, > 1,000 om-2•
FIG. 5. Distribution of Limnodrilus hoffmeisteri in Lake Michigan, summer 1977. The first contour line delineates areas of < 100 L. hoffmeisteri om-2; the second contour, <200 om-2; the third contour <500 om-2; and the fourth, indicated in black, >500 om-2•
(less than 30 m), Naididae were also found infrequently, and comprised less than 1% of total oligochaetes averaged over the whole lake.
basins, with the highest densities at shallower depths (less than 60 m) in the southern basin. However, two-way analysis of variance on log transformed densities using basin and depth as treatments indicated that these differences were not significant (p > .05). Because of the lack of replication, variances were high and often unequal, so that statistically significant inferences were difficult to make with this data set. In the northern basin, tubificids were absent from 40 to 60-m and 80 to tOO-m depths, and in the central
Depth Distributions of Oligochaetes In the southern and central basins, Sty/odri/us densities were highest in the 30- to 50-m depth interval, while in the northern basin the depth distribution was not as pronounced (Fig. 6). There appeared to be a difference in abundance of tubificids between
LAURITSEN et al.
72 6
1200
NORTHERN
3
800
basin densities were highest at the 30 to 40-m and 150 to 200-m depth intervals. Enchytraeids were absent from depths of less than 20 m and greater than 150 m and showed no obvious depth-related trends in any of the basins. Naidids were found almost exclusively in the 10 to 20-m depth interval in the northern and southern basins (there were no shallow sample stations in the central basin; Fig. 6).
Green Bay and Grand Traverse Bay samples were not included in Figure 6; in Green Bay, tubificids were the dominant oligochaetes found (usually > 80% of total oligochaetes) at shallow « 40 m) depths. In Grand Traverse Bay, Stylodrilus was dominant at shallow depths « 50 m) and tubificids were dominant at > 50 m depths.
400
2
CENTRAL 800
....E
oz 400
2
1600
SOUTHERN 1200 5
5 5 400
14 14 5
10
30
50
70
DEPTH
90
150200250
(m)
FIG. 6. Densities of total oligochaetes, averaged by depth intervals in three arbitrarily defined basins of the main body of Lake Michigan, summer 1977. Insets show densities of total Tubificidae (vertically hatched), Stylodrilus (white), total Enchytraeidae (black), and total Naididae (spots). The number of samples is indicated above each depth interval for the three basins.
DISCUSSION Benthic environmental variations in Lake Michigan are strongly related to depth. Typical profundal faunal patterns show increasing densities and species richness in the 20- to 50-m depth interval; with greater depth both variables then decrease. Near the 20-m depth contour, physical and chemical environments change as the effects of wave action on the benthic environment diminish (Mozley and Garcia 1972, Mortimer 1975). Influxes of organic sediments and contaminants to the benthic environment increase rapidly with depth and the proportion of silt and clay in the sediments after 20 m, and regional variations in the 20- to 50-m depth interval are greater because of proximity to major sources of allochthonous material (Mozley and Alley 1973). Thus local pollution should be most evident in oligochaete communities at these depths. Analysis of sediment samples collected on the CCIW cruise of Lake Michigan showed significant differences in trace element content between depositional and non-depositional areas of the lake and between surficial and buried sediments (Cahill 1981). Bromine, chromium, copper, lead, and zinc showed higher enrichment in depositional areas (with finer-grained sediments) and these areas roughly correspond to the areas of higher sediment organic carbon content, shown in Figure 2 (Cahill 1981). Because of the high variability in this data set, no statistically significant differences were found in regional c~mparisons of depth distributions of tubificids and Stylodrilus. The following discussion is based on inferences made from the distribution maps.
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
Sty/odri/us heringianus was the most common oligochaete in all but the shallowest depths of the lake and its distribution illustrates the depth pattern described by Mozley and Alley (1973) for total oligochaetes in each basin of the lake. A number of studies have indicated that S. heringianus is most abundant where sediment organic content is low, but we could not make a significant correlation using this data set. Tubificids were more common at mid-depths of 20-60 m in the southern basin. This trend has been observed by other researchers (Mozley and Howmiller 1977) and is generally attributed to higher rates of sedimentation of organic matter at these depths (Mozley and Alley 1973). But in the northern basin, tubificid densities were greatest at shallower depths of 10-40 m, and many areas of highest tubificid density did not have organically enriched sediments. Brinkhurst and Jamieson (1971) have noted that where careful analyses have been made, few clear correlations between the variations of total organic matter and the distribution and abundance of worms have been demonstrated. Recent work indicates that tubificid sediment preferences are a result of the bacterial abundance in the sediments (McMurtry et a/. 1983) and there may be no correlation between the quantity of bacteria and the organic content of the sediments (e.g., Drabkova 1983). Enchytraeid densities exhibit a distribution pattern similar to that of Sty/odri/us. As with naidids, these small worms are easily lost when sieving benthic samples and were probably underrepresented in this survey. Total oligochaete densities were lower than previously reported for comparable areas of the lake (e.g., Howmiller 1974, Hiltunen 1967, Howmiller and Beeton 1971) and this is probably attributable to the inefficiency of the Shipek sampler (Flannagan 1970). This inefficiency is most pronounced at depths less than 60 m (N. Watson, personal communication, Canada Centre for Inland Waters, Burlington, Ontario), where the greatest· oligochaete densities are found in Lake Michigan. Early studies in Lake Michigan have included the ratio of amphipods to oligochaetes (Powers and Robertson 1965, Ayers and Huang 1967), and density of oligochaetes (Mozley and Alley 1973) as benthic indices of pollution. However, because they are numerical criteria, results are dependent upon type of grab sampler used and mesh size of sieves used to wash samples so that comparisons between data sets are often difficult to make.
73
Much better assessment may be achieved with information on relative densities of particular species. For example, a high relative abundance of Sty/odri/us heringianus is usually accepted as evidence that an area receives little organic enrichment (Howmiller and Beeton 1971, Milbrink 1973). Upward of 80010 S. heringianus were found in deeper portions of the lake where organic carbon content of the sediments was not high. Brinkhurst (1967) suggested that the percentage of the tubificid Limnodrilus hoffmeistri in relation to other oligochaetes may be a useful index of organic pollution, with a higher relative abundance indicating more enriched areas. Combining all immature tubificids without hair chaetae to total numbers of mature L. hoffmeisteri gave high percentages (80-100%) in the southern basin, the lower two-thirds of Green Bay, and the northernmost portion of the lake. These results reflect the distribution pattern of the species shown in Figure 5, and with the exception of the northern area, are similar to the known or expected patterns of organic enrichment of sediments in the lake, suggesting that extensive areas of Lake Michigan are enriched or polluted. Oligochaete communities,· or taxocenes, have been widely used in recent years as indicators of pollution, particularly by European biologists working on large inland lakes (Milbrink 1980, Lang and Lang-Dobler 1980). This approach depends upon differences among oligochaete species in physiological tolerance of direct or indirect effects of sediment pollution. As pollution increases, species replace each other and the com..; position of the taxocene shifts. Species have been generally characterized by their distribution patterns in areas with known or suspected pollution or enrichment (Brinkhurst et a/. 1968), and laboratory testing of common species has verified these field observations (Chapman et a/. 1982a). This can be explained by the relative abilities of the species to live anaerobically when oxygen is depleted, but oligotrophic species can be more tolerant of certain heavy metals, pesticides, and industrial wastes than eutrophic species (Chapman et a/. 1982a). Therefore, the established taxocene-based assessments must refer primarily to pollution by readily degradable organic matter. Higher temperature can affect oligochaete behavior and/or physiology, increasing toxic reactions so that the same level of organic pollution would have a greater influence on taxocene composition in warmer, shallower habitats.
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LAURITSEN et al.
In the Great Lakes, analysis of oligochaete taxocene structure and classification according to pollution tolerance has centered around Howmiller's studies of Green Bay (Howmiller and Scott 1977, Mozley and Howmiller 1977). Howmiller's first system divides common Great Lakes species into four groups according to degree of tolerance to enrichment of the benthic environment (Table 2; Mozley and Howmiller 1977). This classification was later modified and reduced to three categories and included all naidid oligochaetes in the mesotrophic category (Howmiller and Scott 1977). We feel that the earlier, four-category classification is more precise, and that because of their life histories and feeding behaviors, naidids should not be grouped as mesotrophic indicators. When stations were assigned to one of four categories based on the numerically dominant species group, the only area of the lake to show gross organic enrichment was southern Green Bay (Fig. 7); this corresponds with observations made by Howmiller and Beeton (1970). Areas of slight and extreme enrichment are scattered around the lake,
TABLE 2. Classification of common Oligochaetes according to the degree of organic enrichment of the environment (Type I-oligotrophic; Type II- mesotrophic; Type III- saprophilic; Type IV- saprobionts; from Mozley and Howmiller 1977, with permission). Environment Type Species
Sty/odTi/us heringianus Spirosperma niko/skyi Limnodrilus profundico/a Tubifex superiorensis Tubifex kess/eTi Rhyacodrilus montana Rhyacodrilus coccineus Spirosperma ferox Isochaetides freyi Ilyodrilus temp/etoni Potamothrix mo/daviensis Potamothrix vejdovskyi Au/odrilus spp. Limnodrilus hoffmeisteri Limnodrilus udekemianus Limnodrilus angustipenis Tubifex tubifex Limnodrilus cervix Limnodrilus claparedeianus Limnodrilus maumeensis Quistadrilus multisetosus
II
III
•
•
•• TYPE I-OLIGOTROPHIC •
TYPE II-MESOTROPHIC
•
TYPE III-SAPROPHILIC
•
TYPE IV-SAPROBIONTS
FIG. 7. Oligochaete species groups (taxocenes) according to environment type (cf. Table 1) based on densities from the summer 1977 survey of Lake Michigan.
IV
x X X X X X X X X X X X X
X X X
X X X X X
including most of Green Bay, much of the northernmost part of the lake, and nearshore areas in the southern basin. The results of the taxocene classification show the same general patterns as the percentage L. hoffmeisteri index, but the former has an advantage in that it is not dependent upon the presence of only one oligochaete species. However, uncertainty still remains regarding the environmental responses of certain oligochaete species included in the taxocene classification. For example, Tubifex tubifex can be quite abundant in polluted areas and also in deeper areas of lakes where there are few other oligochaete species present, indicating that it may be sensitive to competition (Milbrink 1973). But it is also highly tolerant of sewage sludge (Chapman et al. 1982a). Milbrink (1983) has suggested that T. tubifex be given a dual ecological ranking - as a eutrophic
OLIGOCHAETE DISTRIBUTIONS IN LAKE MICHIGAN
indicator when it is found in association with Limnodrilus hoffmeisteri, and as an oligotrophic indicator when it is found in association with other oligotrophic species. Potamothrix vejdovskyi is considered a mesotrophic indicator by Mozley and Howmiller (1977), while Milbrink (1973) suggested that it does best in polluted conditions. It may be an opportunistic species-for example, Nalepa and Thomas (1976) reported very high densities of P. vejdovskyi near the Niagara River inflow into Lake Ontario. Spirosperma ferox (as Peloscolex) has long been considered as an oligotrophic indicator in European lakes (Milbrink 1980). Not all European biologists agree with that claim however; Lang (1978) believed that S. ferox indicates eutrophic conditions. In laboratory tests, it was less tolerant of sewage sludge than any other species tested (Chapman et al. 1982a). Mozley and Howmiller (1977) considered this species to be a mesotrophic indicator in the Great Lakes. Because of the interactions between biotic and abiotic factors, we are not yet able to predict precisely the responses of species in situ to specific environmental conditions or toxins. For example, sediments often serve to ameliorate the effects of toxic substances (Chapman et al. 1982a), as can biological interactions between oligochaete species (Chapman et al. 1982b). Further experimental research on species responses to pollutants should help to refine the oligochaete taxocene classification system, and allow us to make better use of benthic invertebrates as indicators of water quality. The present work is the first lake-wide survey of Lake Michigan in which oligochaetes were identified to the species level. Since it was based solely on a systematic sampling design, it has statistical disadvantages, but provides a strong basis for rational design of future surveys and hypothesisoriented research. The data (available on magnetic tape from the U.S. Environmental Protection Agency or the Great Lakes and Marine Waters Center, University of Michigan) will support analysis of sampling design efficiency, definition of appropriate spatial strata, and future regional or whole-lake surveillance for temporal trends in water quality. CONCLUSIONS
Although oligochaete densities from the present survey were lower than have been previously reported for the lake, the general patterns of species' distributions (Stylodrilus heringianus domi-
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nant at greater depths; eutrophic species such as Limnodrilus hoffmeisteri abundant in Green Bay and nearshore areas in the southern part of the lake) were consistent with earlier regional studies. An exception was the previously unsampled northern portion of the lake which contained a majority of eutrophic species, in contrast with what might be expected given the distance from major sources of nutrient or organic loading. Certainly more sampling is warranted to elucidate patterns of species distributions and causal factors in this part of the lake. Use of taxocene classifications (such as Mozley and Howmiller 1977) can aid in making comparisons between different areas in a body of water; additional experimental toxicity testing including the other common oligochaete species of the region should help to refine such indices and broaden their usefulness. ACKNOWLEDGMENTS
This research was supported by the U.S. Environmental Protection Agency, grant number R805333010. We would like to thank Z. BatacCatalan, C. Millenbach, M. Wiley, and M. Winnell for assistance with data handling. This manuscript has been improved by suggestions from a number of people, including P. Bradbury, L. Crowder, T. Nalepa, T. Wentworth, and an anonymous reviewer. Contribution number 404, Great Lakes Research Division, The University of Michigan. Paper No. 9601 of the Journal Series of the North Carolina Agricultural Research Service, Raleigh, NC 27695-7601. REFERENCES Alley, W. P., and Mozley, S. C. 1975. Seasonal abundance and spatial distribution of Lake Michigan macrobenthos, 1964-67. University of Michigan, Great Lakes Research Division Special Report #54. Ayers,J. C.,andHuang,J. C. K.1967.StudiesofMilwaukee Harbor and embayment. In Studies on the Environment and Eutrophication of Lake Michigan, ed. J. C. Ayers and D. C. Chandler, pp. 372-394. University of Michigan Great Lakes Research Division Special Report #30. Brinkhurst, R. O. 1967. The distribution of aquatic oligochaetes in Saginaw Bay, Lake Huron. Limnol. Oceanogr. 12:137-143. ' ____ , and Jamieson, B. G. M. 1971. Aquatic Oligochaeta of the World. Edinburgh: Oliver and Boyd. ____ , Hamilton, A. L., and Herrington, H. B. 1968. Components of the bottom fauna of the St. Lawrence Great Lakes. Univ. Toronto Great Lakes Inst. No. PR 33:1-49.
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Cahill, R. A. 1981. Geochemistry ofrecent Lake Michigan sediments. Ill. State Geol. Survey Div. Circ. #517. Chapman, P. M., Farrell, M. A. and Brinkhurst, R. O. 1982a. Relative tolerances of selected aquatic oligochaetes to individual pollutants and environmental factors. Aquat. Toxicol. 2:47-67. ____ , Farrell, M. A., and Brinkhurst, R. O. 1982b. Effects of species interactions on the survival and respiration of Limnodrilus hoffmeisteri and Tubifex tubifex (Oligochaeta, Tubificidae) exposed to various pollutants and environmental factors. Water Res. 16:1405-1408. Drabkova, V. G. 1983. Bacterial decomposition of organic matter in lacustrine sediments. Hydrobiol. 103:99-102. Eggleton, F. E. 1936. The deep water bottom fauna of Lake Michigan. Pap. Mich. A cad. Sci. Arts Lett. 22:593-611. Flannagan, J. F. 1970. Efficiencies of various grabs and corers in sampling freshwater benthos. J. Fish. Res. Board Can. 27:1691-1700. Hiltunen, J. K. 1967. Some oligochaetes from Lake Michigan. Trans. A mer. Microsc. Soc. 86:433-454. ____ , and Klemm, D. J. 1980. A guide to the Naididae (Annelida: Clitellata: Oligochaeta) of North America. U.S. Environmental Protection Agency Report No. EPA-6oo/4-80-031, Office of Research and Development. Howmiller, R. P. 1974. Composition of the oligochaete fauna of central Lake Michigan. In Proceedings 17th Conf. Great Lakes Res., pp. 589-592. Internat. Assoc. Great Lakes Res. ____ , and Beeton, A. M. 1970. The oligochaete fauna of Green Bay, Lake Michigan. In Proceedings 13th Conf. Great Lakes Res., pp. 15-46. Internat. Assoc. Great Lakes Res. ____ , and Scott, M. A. 1977. An environmental index based on relative abundance of oligochaete species. J. Water Poll. Cont. Fed. 49:809-815. Lang, C. 1978. Factorial correspondence analysis of Oligochaeta communities according to eutrophical level. Hydrobiol. 57:241-247. ____ , and Lang-Dobler, B. 1980. Structure of tubificid and lumbriculid worm communities, and three indices of trophy based upon these communities as descriptors of eutrophication level of Lake Geneva (Switzerland). In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 457-470. New York: Plenum Press. Leland, H. V., Shukla, S. S., and Shimp, N. F. 1973. Factors affecting disribution of lead and other trace elements in sediments of southern Lake Michigan. In Trace Metals and Metal-organic Interactions in Natural Waters, ed. P. C. Singer, pp. 89-129. Ann Arbor: Ann Arbor Science Pub I.
McMurty, M. J., Rapport, D. J., and Chua, K. E. 1983. Substrate selection by tubificid oligochaetes. Can. J. Fish. Aquat. Sci. 40:1639-1646. Milbrink, G. 1973. On the use of indicator communities of Tubificidae and some Lumbriculidae in the assessment of water pollution in Swedish lakes. Zoon. 1:125-139. ____ .1980. Oligochaete communities in pollution biology: The European situation with special reference to lakes in Scandinavia. In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 433-455. New York: Plenum Press. ____ . 1983. An improved environmental index based on the relative abundance of oligochaete species. Hydrobiol. 102:89-97. Mortimer, C. H. 1975. Environmental status of the Lake Michigan region: Physical limnology of Lake Michigan. Argonne National Lab. Report No. ANL/ ES-40, Vol. 2, U.S. Energy Research and Development Administration. Mozley, S. C., and Alley, W. P. 1973. Distribution of benthic invertebrates in the south end of Lake Michigan. In Proceedings 16th Conf. Great Lakes Res., pp. 87-96. Internat. Assoc. Great Lakes Res. ____ , and Garcia, L. C. 1972. Benthic macrofauna in the coastal zone of Southeastern Lake Michigan. In Proc. 15th Conf. Great Lakes Res., pp. 102-116. Internat. Assoc. Great Lakes Res. ____ , and Howmiller, R. P. 1977. Environmental status of the Lake Michigan region: Zoobenthos of Lake Michigan. Argonne National Lab. Report No. ANL/ES-40, Vol. 6, U.S. Energy Research and Development Administration. Nalepa, T. F., and Thomas, N. A. 1976. Distribution of macrobenthic species in Lake Ontario in relation to source of pollution and sediment parameters J. Great Lakes Res. 2:150-163. Powers, C. F., and Robertson, A. 1965. Some quantitative aspects of the macrobenthos of Lake Michigan. In Proceedings 8th Conf. Great Lakes Res., pp. 153-159. University of Michigan, Great Lakes Research Division Publ. #13. Robertson, A., and Alley, W. P. 1966. A comparative study of Lake Michigan macrobenthos. Limnol. Oceanogr. 11:576-583. Spencer, D. R. 1980. The aquatic Oligochaeta of the St. Lawrence Great Lakes region. In Aquatic Oligochaete Biology, ed. R. O. Brinkhurst and D. G. Cook, pp. 115-164. New York: Plenum Press. Wiederholm, T. 1980. Use of benthos in lake monitoring. J. Water Poll. Cont. Fed. 52:537-547. Worswick, J. M., and Barbour, M. T. 1974. An elutriation apparatus for macroinvertebrates. Limnol. Oceanogr. 19:538-540.