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Production dynamics of riverine chironomids: extremely high biomass turnover rates of primary consumers.

INTRODUCTION

Primary consumers are those animals that feed upon basal food resources (i.e., plants or detritus) and form the first feeding link in community food webs and trophic structures in all ecosystems. Accurate assessment of these initial consumers, regardless of the ecosystem under consideration, is extremely important if we are to understand the significance of subsequent trophic pathways for food web analysis or energy flow. An essential consideration in the energetics of primary consumers is their production (i.e., secondary production), and this is directly related to their consumption of basal food resources (Benke 1993, Benke and Wallace 1997). Furthermore, the efficiency with which primary consumers convert their food into secondary production determines the potential food available to subsequent links in the food web.

A basic principle of ecological energetics is that production (P) of a population is equally dependent on its biomass (B) and biomass growth rate (g), regardless of where that population is located in the food web; i.e., P = g x B (Benke 1993). Annual production divided by mean annual biomass (P/B) is often used as an index of annual biomass turnover rate, although turnover rates for fast-growing organisms are usually calculated for shorter periods, such as a day. Measurement of biomass is usually a straightforward matter of quantitative sampling. However, determination of growth rate or P/B is difficult when cohorts cannot be followed from field sampling and when there are several generations per year. Unfortunately, without an estimate of biomass turnover rate, measurement of consumer production is not possible, nor can food web links that depend on consumer production be adequately understood.

Secondary production of freshwater benthic invertebrates has been studied for several decades, and most early studies generally suggested that annual P/B rarely exceeded 10 (e.g., Waters 1977). Banse and Mosher (1980) provided the first empirical models of annual P/B as a function of animal body mass, but their data for freshwater benthic animals did not include any P/B values [greater than]5. Thus, there was the perception that annual P/B values for benthic invertebrates were quite low regardless of ecosystem type or taxon. However, scattered studies documenting high growth rates of aquatic insects, particularly midges of the family Chironomidae, suggested that P/B values could be much higher than previously believed. For example, Mackey (1977a) showed that several species of chironomids could complete larval development in [less than]2 wk in the laboratory, and using this information he estimated P/B values of 50-60 in the River Thames, England (Mackey 1977b). The possibility of high P/B values due to short developmental times was particularly significant because chironomids typically have the highest densities and often comprise a large proportion of all invertebrate species present in freshwater benthic communities. Unfortunately, because of their small size, difficulties in identification, and relatively low biomass, the importance of chironomids in benthic food webs has not been widely appreciated.

In a study on the Satilla River, a blackwater Coastal Plain river in the southeastern United States, Benke et al. (1984) estimated chironomid production by assuming short development times based primarily upon the temperature-specific laboratory growth studies by Mackey (1977a). Chironomids from snag habitat (submerged wood) were reported to have annual P/B values of [greater than]65 in all cases, with most estimates [greater than]100. These P/B values were [greater than]10 times higher than many previous estimates for chironomids, and at least twice as high as Mackey (1977b) himself reported for chironomids in the River Thames. Not surprisingly, such high values have generated skepticism among some who believe that high growth rates in the laboratory do not reflect growth of populations in the field (e.g., Soluk 1985, Lindegaard and Mortensen 1988).

The major objective of the current study was to describe the production dynamics and biomass turnover rates of the major components of the chironomid assemblage occurring on the snag habitat of another Coastal Plain river, the Ogeechee River. Particular attention was given to measuring growth rates and determining production dynamics (i.e., temporal patterns). In order to obtain realistic growth rates, riverside studies were conducted that simulated natural food, temperature, and photoperiod (Stites and Benke 1989, Hauer and Benke 1991). The chironomids were grown in a mixed assemblage as they occur in nature, although other invertebrate groups were excluded.

The major questions were: (1) What is the magnitude of chironomid production on the snag habitat? (2) What is the temporal pattern of production and biomass? (3) What do the observed production dynamics suggest about trophic relationships on snags and in stream communities in general? This analysis is part of a total assessment of the production dynamics of the entire snag community. The assessment involved an intensive 2-yr sampling effort (Benke and Parsons 1990, Benke and Jacobi 1994, Benke and Wallace 1997) and the onsite measurement of growth rates for several species (Hauer and Benke 1987, 1991, Stites and Benke 1989, Benke et al. 1992).

STUDY SITE

The Ogeechee River is a 6th-order blackwater system located in the Coastal Plain of the southeastern USA. Detailed descriptions of the physical and chemical characteristics of the river during the two years of the study are presented elsewhere (Benke and Parsons 1990, Meyer 1992). Briefly, mean discharge was 50.7 [m.sup.3]/s during the 1st yr of sampling (1982) and 79.1 [m.sup.3]/s during the 2nd yr (1983), compared to the long-term mean of 66.8 [m.sup.3]/s (Benke and Parsons 1990). Mean water temperature was 19.5 [degrees] C (range: 2.0 [degrees]-28.7 [degrees] C) in 1982 and 19.2 [degrees] C (range: 4.4 [degrees]-30.8 [degrees] C) in 1983 (see temporal patterns below).

The snag habitat is extremely important in the Ogeechee River, as it is in all Coastal Plain rivers, supporting a richer and denser concentration of invertebrates than any other habitat in the river (e.g., Benke et al. 1984, Benke and Jacobi 1994, Benke and Wallace 1997). Snag surfaces are typically 20-50% that of true benthic surfaces (Wallace and Benke 1984), and they are the only stable substratum in the main river channel. Although chironomids are extremely abundant on the snag habitat, they are also common in the sandy benthic habitat covering most of the river bottom (Stites 1986).

METHODS

Snag samples were collected by hand, usually from a small boat, with the aid of a cylindrically shaped sieve (Benke et al. 1984). Twenty samples were collected monthly during the first year (December 1981 to November 1982) and 10 samples/mo in the 2nd yr (December 1982 to November 1983), as described for black flies (Benke and Parsons 1990), mayflies (Benke and Jacobi 1994), and caddisflies (Benke and Wallace 1997). All samples were processed as described in an earlier study by Benke et al. (1984) so that densities and biomass could be estimated per square meter of snag surface. Sample surface area was usually [approximately]250 [cm.sup.2].

During the 1st yr of sampling, chironomid larvae usually were identified to the generic level before measurement of their length. Length-frequency histograms were constructed for the major taxa to determine whether cohort structure could be recognized from samples taken through time. Lengths were converted to mass using volumetric approximations based on the mean diameter and length of each individual taxon and assuming a volume-to-dry-mass conversion of 0.2 (Benke et al. 1984, Stites and Benke 1989, Hauer and Benke 1991). During the 2nd yr of sampling, chironomids were only identified to the family level (i.e., all chironomids combined) to reduce processing time.

The instantaneous growth method was used to estimate mean daily production between sampling dates. Daily growth rate (g) for a given sampling interval was calculated from equations predicting growth rate from temperature (Hauer and Benke 1991). The equations were developed from chironomids grown in riverside mesocosms throughout most of the year. The mesocosms contained river water that was exchanged daily (with the only food source being natural seston) and simulating natural conditions under ambient and experimentally altered temperature regimes. Due to taxonomic uncertainties in the identification of early instars used at the initiation of growth trials, growth calculations could only be made at the tribe (Chironomini and Tanytarsini) or subfamily (Orthocladiinae) level. Growth rate was also determined at the family level (all Chironomidae).

Growth rate was weakly, but significantly, related to temperature for Chironomini, Tanytarsini, and all Chironomidae according to the following equations (Hauer and Benke 1991):

Chironomini: g = -0.687 + 0.115T - [0.0024T.sup.2] (P [less than] 0.01, N = 36, [R.sup.2] = 0.28)

Tanytarsini: g = -0.669 + 0.119T - [0.0029T.sup.2] (P [less than] 0.01, N = 37, [R.sup.2] = 0.24)

Chironomidae: g = -0.725 + 0.122T - [0.0028T.sup.2] (P [less than] 0.01, N = 40, [R.sup.2] = 0.25)

where T is mean temperature during the growth measurements ([degrees]C).

Examination of the data suggested that the low [R.sup.2] values were due primarily to considerable variation among data collected when discharge was [less than]20 [m.sup.3]/s. A regression determined for values when discharge was [greater than]20 [m.sup.3]/s showed that growth rate was more strongly related to temperature for each of the three groupings than when data from all discharge levels were included (Hauer and Benke 1991):

Chironomini: g = -0.609 + 0.111T - [0.0020T.sup.2] (P [less than] 0.01, N = 10, [R.sup.2] = 0.88),

Tanytarsini: g = -0.746 + 0.155T - [0.0039T.sup.2] (P [less than] 0.01, N = 10, [R.sup.2] = 0.62),

Chironomidae: g = -0.710 + 0.138T - [0.0031T.sup.2] (P [less than] 0.01, N = 10, [R.sup.2] = 0.86).

Growth rate was not significantly related to temperature for the Orthocladiinae at any discharge level, and a constant growth rate of 0.44 [d.sup.-1] (SE = 0.04, N = 32) was assumed for this subfamily, regardless of temperature (Hauer and Benke 1991).

When discharge was [less than]20 [m.sup.3]/s, there was no significant relationship between growth rate and temperature for any of the groupings. However, rather than assuming a constant mean value for growth rate when discharge was [less than]20 [m.sup.3]/s, equations developed from all growth trials at all discharge levels were used for values [less than]20 [m.sup.3]/s. Because the statistically significant curve for all discharge values was very similar to the nonsignificant curve for discharge [less than]20 [m.sup.3]/s (Hauer and Benke 1991), I felt this approach was more realistic than assuming a constant growth rate, particularly at low temperatures ([less than]10 [degrees] C). Although growth rates were still quite high at low discharge, the high variability in their values may be due to more variable food quality at such times.

Because most of the Chironomini used in the trials were in the genus Polypedilum, the Chironomini equation can safely be applied to field populations of this genus. However, because information on individual growth rates was not available for other Chironomini taxa (e.g., Dicrotendipes and Stenochironomus), their production was not calculated. Most of the Tanytarsini used in the growth experiments were in the genus Rheotanytarsus and almost all of the Tanytarsini from field samples were Rheotanytarsus. Thus, in applying the Tanytarsini equation to the field data, all Tanytarsini were assumed to be Rheotanytarsus. Furthermore, the mean growth rate of 0.44 [d.sup.-1] for Orthocladiinae was applied to Rheocricotopus, which represented 87% of subfamily biomass, but was not applied on an individual basis to the other orthoclads. Finally, the general chironomid equation was applied to the Tanypodinae. This seemed justified because their growth rate was not significantly different from other fast-growing snag midges during summer months (Stites and Benke 1989). Although the Tanypodinae are often considered to be predators, they are included in this analysis because they also function as collector-gatherers (Merritt and Cummins 1996), and our own limited gut analysis suggested they consumed amorphous detritus (Wallace et al. 1987).

Mean daily production between sampling dates was calculated as the mean daily growth rate (g) multiplied by the linear mean of biomass on the two consecutive sampling dates (e.g., Benke and Parsons 1990, Benke 1993). Mean daily growth rate was estimated as the mean of growth rates on sample dates within an interval, each of which was based on mean daily temperature.

Production values are presented using two units: production per surface area of snag habitat and production per area of river channel bottom. The first was estimated by measuring snag surface area after animals were removed (Benke et al. 1984). The second was estimated by multiplying snag values by a conversion factor that accounts for surface area of snag as a function of river height (Wallace and Benke 1984). This approach has been used for black flies, mayflies, and caddisflies from these same snags (Benke and Parsons 1990, Benke and Jacobi 1994, Benke and Wallace 1997). Production estimated on the basis of snag surface area represents a measure of production intensity on a specific habitat. However, production per area of channel bottom accounts for relative abundance of habitats and represents an ecosystem-level measurement. Production of snag chironomids can be added directly to production of chironomids from the sandy benthic habitat to obtain total chironomid production.

RESULTS

Size-frequency patterns

The three dominant taxa found on the snag habitat were the filtering collector, Rheotanytarsus spp., and the gathering collectors, Rheocricotopus spp. and Polypedilum spp. Each genus had mixed size distributions on all dates with little suggestion of any cohort structure that might be followed through time [ILLUSTRATION FOR FIGURE 1 OMITTED]. Because each generic grouping probably was composed of several species, it is possible that true cohorts may have been hidden. However, the growth rates resulting from the equations shown above (Hauer and Benke 1991) and from Stites and Benke (1989) result in potential larval development times of [less than]2 wk for most of the year, only about half the length of the sampling interval. Thus, we would not expect to be able to follow a cohort through time, unless extremely cold weather ([less than]10 [degrees] C) occurred over a several-month period, and this did not take place. The most important conclusion to be gained from these size-frequency distributions is that during the winter there was no tendency for all animals to accumulate in the final size class, an indication that emergence occurs throughout the year.

Production dynamics

Daily growth rates predicted from the temperature-dependent growth equations were extremely high for individual tribes [ILLUSTRATION FOR FIGURE (2 OMITTED], 1st yr only) and for Chironomidae as a group [ILLUSTRATION FOR FIGURE (3 OMITTED], two consecutive years) throughout most of either year. Growth rates were usually at least 0.4 [d.sup.-1] and sometimes exceeded 0.8 [d.sup.-1]. Such high growth rates throughout the year were the result of water temperatures that were [greater than or equal to] 15 [degrees] C throughout much of the year [ILLUSTRATION FOR FIGURE 3 OMITTED]. Only for short durations in midwinter did temperatures drop below 10 [degrees] C and growth rates fall to zero [ILLUSTRATION FOR FIGURES 2 AND 3 OMITTED].

Tanytarsini (Rheotanytarsus) growth rates were highest from March through May when temperatures generally fluctuated between 15 [degrees] and 20 [degrees] C, and declined somewhat during the summer as temperatures increased [ILLUSTRATION FOR FIGURES 2 AND 3 OMITTED]. On the other hand, growth rates for Chironomini (specifically Polypedilum) were highest during the warmest months of the year when mean daily temperatures were between 24 [degrees] and 30 [degrees] C. For the composite estimation of growth rate, values were usually high ([greater than]0.75 [d.sup.-1]) from March through November of both years [ILLUSTRATION FOR FIGURE 3 OMITTED]. The sharp short-term drops and increases in growth rate (e.g., 0.7 to 0.5 [d.sup.-1]) during the summer months occurred when discharge fell below 20 [m.sup.3]/s, causing a shift in the equation used to predict growth rate. These sudden shifts are undoubtedly artifacts caused by the change in regression equations. In reality, the pattern is likely to be smoother, but the mean daily growth rate calculated between sampling dates should be little affected. Nonetheless, except during December and January, the composite growth rate was almost always [greater than]0.5 [d.sup.-1] [ILLUSTRATION FOR FIGURE 3 OMITTED].

Production dynamics for Polypedilum and Rheotanytarsus showed that biomass and production were particularly low during the first winter, but rose during the summer and peaked in the fall [ILLUSTRATION FOR FIGURE 2 OMITTED]. Rheocricotopus biomass and production were moderately high early in the winter, but declined to low levels during late winter and rose during the summer and fall like the other two taxa. Production for total Chironomidae over two consecutive years suggested that daily production was relatively high ([greater than]0.2 g[center dot][m.sup.-2][center dot][d.sup.-1] for surface area of snag) throughout most of the year, with peak values ([greater than]0.4 g[center dot][m.sup.-2][center dot][d.sup.-1]) occurring either in mid or late summer [ILLUSTRATION FOR FIGURE 3 OMITTED]. The period of lowest production was in early to midwinter and resulted from the combination of low biomass and low temperature.

Mean annual density, biomass, and production are shown for each of the major taxa per area of snag surface area and per area of river bottom (Table 1). Rheocricotopus was clearly the dominant genus of the Orthocladiinae, although densities of Thienemanniella were quite high. The Chironomini were dominated by Polypedilum, but biomass of Stenochironomus, a large wood-boring midge, was also high. The Tanytarsini (almost all Rheotanytarsus) had the highest density, biomass, and production among all the taxa. The Tanypodinae were relatively low in all production statistics. Production estimates per area of river bottom were roughly one-third of the values per surface area of snag (see values in parentheses, Table 1). Total chironomid production from summation of individual estimates made using taxon-specific growth equations (65 362 mg[center dot][m.sup.-2][center dot][yr.sup.-1]) was quite close to the estimate using the family-level equation (69 917 mg[center dot][m.sup.-2][center dot][yr.sup.-1]) for the 1st yr (Table 1). Density, biomass, and production for total Chironomidae were very similar between years, with mean densities [greater than]70 000/[m.sup.2], biomass [greater than]0.3 g/[m.sup.2], and production from [approximately]70 to 82 g[center dot][m.sup.-2][center dot][yr.sup.-1] (for snag surface and using the family-level estimates).

Annual biomass turnover, as represented by annual P/B, was extremely high for all taxa, whether calculated on a snag surface area or river bottom basis (Table 1). Values were 157-159 for the Orthocladiinae, 196-198 for Tanytarsini, and 255-258 for the Chironomini. For the latter, this represented a biomass turnover rate of almost once per day. For the family as a whole, annual P/B was 202-235.

DISCUSSION

This study has shown that chironomid production can be extremely high on the snag habitat of Coastal Plain rivers, and this high production was due to extremely high daily and annual P/B values. Furthermore, high levels of production and turnover were sustained throughout most of the year, even during winter. These findings raise several issues concerning the role and characteristics of primary consumers in Coastal Plain rivers, as well as in other aquatic ecosystems: (1) Are such high P/B values realistic for natural populations of primary consumers, and what conditions in Coastal Plain rivers make them possible? (2) How do these high production and P/B values compare with estimates for primary consumers from other systems and how widespread are such high turnover rates? (3) What is the trophic significance of such high P/B values for primary consumers, and what are the implications for their predators?

Extremely high P/B in Coastal Plain rivers

The high P/B values of chironomids in the Ogeechee River were in agreement with estimates of similar populations from the Satilla River (Table 2). Values for Polypedilum, Rheocricotopus, and Rheotanytarsus in the Ogeechee were slightly higher than estimated for the same or closely related taxa in the Satilla, where the latter were based on published laboratory growth studies (Mackey 1977a). Although it is impossible to totally duplicate the natural environment and still be able to measure growth, the approximation of natural [TABULAR DATA FOR TABLE 1 OMITTED] food, temperature, and photoperiod in streamside growth chambers is a realistic compromise (Stites and Benke 1989, Hauer and Benke 1991). Thus, the high P/B values found for Ogeechee River chironomids appear to be real.

It might be argued that even though chironomids continue growing in winter when temperatures usually fluctuate between 10 [degrees] and 16 [degrees] C [ILLUSTRATION FOR FIGURE 3 OMITTED], they might not emerge until temperature increases in the spring. Individuals might remain in the final instar for an extended period of time, resulting in a lowering of annual P/B. However, examination of the size-frequency distributions of the three major taxa showed little evidence of this happening, as mixed size classes were present on almost every date [ILLUSTRATION FOR FIGURE 1 OMITTED]. Furthermore, adult chironomids were commonly observed during warm winter days (i.e., in December and January), and Soponis (1980, 1983) reported that pupal exuvia comprised more than half of the chironomids drifting in a north Florida stream in February when water temperatures were [approximately]12 [degrees] C.

It is possible that application of a single growth rate to population biomass might overestimate production and P/B, because large size classes, whose growth rate is lower than the average growth rate, often compose much of the population biomass (Huryn 1990). However, I believe this effect will be minimal in the Ogeechee because there was not an accumulation in large size classes and total development time was so short (Hauer and Benke 1991).

High biomass turnover of snag chironomids is consistent with results for several other insect populations in the Ogeechee River. Annual P/B of certain mayfly taxa, such as Baetis spp., was close to 70 or higher (Benke and Jacobi 1994), and values for black flies were 37 to 47 (Benke and Parsons 1990). In the sandy benthic habitat, several chironomid taxa had annual P/B values close to or greater than 100 (Stites 1986). In each case of high annual P/B values (midges, mayflies, and black flies), they were based on growth rates determined in riverside mesocosms simulating natural conditions (Benke and Jacobi 1986, Hauer and Benke 1987, 1991, Stites and Benke 1989, Benke et al. 1992). Likewise, water lily beetles found on leaves of Nuphar luteum in backwater habitats of the Ogeechee River had an annual P/B of 195 (Wallace and O'Hop 1985).

Part of the reason for high annual production and P/B is that most of the consumer groups are productive throughout all seasons, with water temperatures rarely falling below 10 [degrees] C ([ILLUSTRATION FOR FIGURES 2 AND 3 OMITTED]; also see Benke and Parsons 1990, Benke and Jacobi 1994, Benke and Wallace 1997). This is in contrast to many studies in north temperate zones in which production greatly declines during the winter when water temperatures are below 10 [degrees] C for long periods of time (e.g., Mackey 1977b). If daily P/B is extremely low for several months in the winter, annual P/B will necessarily be lower than is possible in a warmwater system.

The other major reason for unusually high production and turnover appears to be the quantity and quality of food available in the form of amorphous detritus in the seston. Originating from river-channel sediments and the floodplain (e.g., Wainright et al. 1992, Carlough 1994), amorphous detritus provides the major food for all primary consumers of the snag community (Wallace et al. 1987). Cudney and Wallace (1980) pointed out that high invertebrate production in streams is often represented by filter-feeders (e.g., Rheotanytarsus, Table 1) because they are able to exploit food that is produced elsewhere (i.e., an energy subsidy). However, seston also rapidly accumulates on snags and is consumed by gathering collectors as well as filter-feeders. This amorphous detritus is rich in bacteria (Carlough and Meyer 1989) and especially nutritious for aquatic [TABULAR DATA FOR TABLE 2 OMITTED] insects (Edwards 1987, Edwards and Meyer 1987, 1990). Furthermore, an extracellular polysaccharide produced by bacteria serves as a nutritious food source for black flies from the Ogeechee River, and may be useful to other primary consumers such as chironomids (Couch et al. 1996). Previous calculations to determine the fraction of seston removed by filter-feeders have shown that depletion of the food resource is highly unlikely, and that food does not limit growth and production (Benke and Parsons 1990, Stites et al. 1995, Benke and Wallace 1997). Thus, relatively warm temperatures and abundant high-quality food create conditions under which chironomids can maintain high biomass turnover and production.

Comparisons of production and P/B among freshwater organisms

Production estimates of snag-dwelling chironomids in the Ogeechee River are among the highest for this group in any freshwater system. Tokeshi (1995) reviewed the literature on chironomid production from both lentic and lotic systems and suggested that production values of 8-32 g[center dot][m.sup.-2][center dot][yr.sup.-1] be considered as high productivity (eutrophy) and those [greater than]32 g[center dot][m.sup.-2][center dot][yr.sup.-1] be considered as extremely productive situations (hypereutrophy). Chironomid production of 65 g[center dot][m.sup.-2][center dot][yr.sup.-1] for snag surfaces is thus well above the minimum for extremely high production, and even after conversion to a channel bottom basis ([greater than]20 g[center dot][m.sup.-2][center dot][yr.sup.-1]), values are still high. Incorporating chironomid production from the sandy benthic habitat (4.7 g[center dot][m.sup.-2][center dot][yr.sup.-1], Stites 1986) raises total chironomid production to [approximately]25 g[center dot][m.sup.-2][center dot][yr.sup.-1].

Because the high production values for chironomids from the Ogeechee depend heavily on high P/B values, one might ask whether such high P/B values occur in many other systems. Empirical models incorporating the results of several studies simultaneously have predicted annual P/B from body size and mean annual temperature (Morin and Bourassa 1992, Benke 1993). Such models tend to provide conservative estimates for annual P/B due to underestimation of P/B values in previously published studies (Benke 1993). For example, these models would estimate annual P/B values of 11 (Morin and Bourassa 1992) and 39 (Benke 1993) for Polypedilum at a mean temperature of 19.5 [degrees] C, when its measured value was actually 258 (Table 1). Thus, one must turn to individual field studies to consider the generality of high P/B.

Clearly, there are many good studies of chironomid production, but most are in north temperate or arctic areas where annual P/B values for chironomids may be low because of temperature alone (e.g., Butler 1982). In other cases, low growth may be due to low food quality or quantity, or intrinsically low growth rates (e.g., Ward and Cummins 1979). Even when there are multivoltine populations, annual P/B values may [TABULAR DATA FOR TABLE 3 OMITTED] not exceed 15 (e.g., Lindegaard and Mortensen 1988, Huryn 1990). However, it seems likely that many other estimates of chironomid production have been underestimated based on conservative assumptions or interpretations of life histories (such as those based on length-frequency histograms) that were longer than actually occurred.

Studies documenting high annual P/B values for chironomids primarily are based on either laboratory or field estimates of growth rates or development times (Table 2, also see review by Tokeshi 1995). For example, other investigators besides Mackey (1977b) and Benke et al. (1984) have used Mackey's (1977a) growth rates to estimate high annual P/B for chironomids. Annual P/B values [greater than]100 have been reported in Lake Norman (USA) (Wilda 1984), and from 3 to 82 in various Polish rivers (Grzybkowska 1989, Grzybkowska and Witczak 1990, Grzybkowska et al. 1990). Studies employing field-derived growth rates such as those in a warm desert stream (Gray 1981, Fisher and Gray 1983, Jackson and Fisher 1986), in a cool mountain stream (Huryn and Wallace 1986), and in the present study provide even stronger documentation that high P/B values exist in diverse systems (Table 2). Furthermore, recent growth studies have found chironomid development times of only 4-6 wk in both tropical (Jackson and Sweeney 1995) and north temperate streams (Nolte and Hoffman 1992). Thus, while growth rates of chironomids can vary by [greater than]200-fold, the incidence of high P/B appears to be more widespread than previously believed.

Such reports of rapid growth rates and high P/B values among chironomid populations prompts a comparison with other aquatic organisms previously considered to turn over more rapidly than benthic invertebrates (Table 3). Maximum annual P/B values for benthic invertebrates have long been thought to be lower (i.e., 12-25) than the maximum values found among zooplankton of 20 to 44 (Waters 1977, Wetzel 1983). Although recent studies have shown that zooplankton can achieve annual P/B values around 100, and that daily P/B values [greater than]1 are possible (Table 3), the highest P/B values found among most microcrustacean zooplankton, even in tropical lakes, are only 0.1-0.2 [d.sup.-1] (e.g., Saunders and Lewis 1988). Furthermore, the highest annual P/B values for benthic microcrustaceans do not appear to be any higher than for their planktonic counterparts (Robertson 1995). Thus, biomass turnover rates for chironomids can be at least as high as microcrustaceans and potentially higher.

Early studies also suggested that annual P/B values for benthic invertebrates were lower than for microbes (Table 3). Annual P/B values for marine bacterioplankton have ranged from 100 to 400 (Valiela 1995), and for freshwater bacterioplankton from 73 to 237 (Wetzel 1983). Recently, daily growth rates from 0.2 to 2.6 [d.sup.-1] have been reported for bacterioplankton, and values [greater than]1.0 [d.sup.-1] for protists (Table 3). Thus, our current estimates for chironomid annual P/B ([greater than]200) and maximum daily P/B (0.8) suggest that metazoan primary consumers sometimes may have biomass turnover rates as high as or higher than aquatic microbes in their natural environments.

In the Ogeechee River, daily turnover rates of sestonic bacteria are lower (usually [less than]0.2 [d.sup.-1], Edwards and Meyer 1986, Edwards et al. 1990) than that of the chironomids that feed on seston (Table 3). In fact, the bacterial growth rates in the seston are insufficient to account for their high density and biomass, which must be replenished by large fluxes from both the sediments and floodplain (e.g., Meyer 1988, Wainright et al. 1992). Most of the bacteria and amorphous detritus on the snags appears to represent accumulations from seston because bacterial production on the snag habitat is much lower ([less than]1 g dry mass[center dot][m.sup.-2][center dot][yr.sup.-1], Edwards et al. 1990) than invertebrate production. Thus, invertebrate production on snags seems highly dependent on the capture of seston, or its accumulation on snags. While in many systems it is expected that the biomass turnover of microbes, particularly bacteria and protists, will be much higher than that of their metazoan consumers, just the opposite seems to occur in the Ogeechee River. This appears possible because the microbes and associated detritus are far more plentiful than the metazoans and provide a seemingly inexhaustible food supply.

Significance of high P/B to predators and food webs

Determination of production can be critical for accurate assessment of food web structure and function, particularly for the primary consumers. Biomass of chironomids is often low in comparison to many other primary consumers (e.g., mayflies) and their contributions to food webs are easily underestimated without consideration of potentially high turnover rates. Even though chironomids make up only a small fraction of invertebrate biomass on Ogeechee River snags ([less than]10%, A. C. Benke, unpublished data), they have a higher production than any other group and form the energetic foundation for higher trophic levels (Benke and Wallace 1997).

The importance of incorporating production and turnover rates into trophic transfers (predator-prey relationships) is well illustrated by consideration of hydropsychid caddisflies. These filter-feeders are highly productive omnivores that occur on the Ogeechee snag habitat and are major predators of chironomids (Benke and Wallace 1997). Their biomass is roughly 10 times that of chironomids, an apparent illustration of the Allen (1951) paradox, in which there appears to be insufficient prey to satisfy the energetic requirements of predators. Furthermore, their consumption of animal food has been estimated to be [approximately]28 g[center dot][m.sup.-2][center dot][yr.sup.-1], a value that is almost identical to the combined production of snag-dwelling midges and mayflies. Although high chironomid P/B is necessary to explain this inverted biomass pyramid, it also suggests that virtually all the production of these two consumer groups could be consumed by the caddisflies alone. However, the situation is not this simple, because caddisflies capture drifting invertebrates that may originate from nonsnag habitats (Benke et al. 1986, 1991), and predaceous stoneflies, dragonflies, hellgrammites, and fish also consume snag chironomids (Benke et al. 1985; J. B. Wallace and A. C. Benke, unpublished data). While it is difficult to make such comparisons between production and consumption, high biomass turnover among chironomids is very consistent with the consumption demands of their predators.

All aquatic systems certainly will not have the same conditions of food and temperature that allow such high biomass turnover of chironomids in the Ogeechee River. Nonetheless, high turnover can be found in other types of streams (Table 2), and investigators need to be aware of this possibility. Such high turnover among primary consumers has profound implications for both energy flow and food web analysis. For example, it suggests that great caution must be exercised in using relative biomass as a means of comparing organisms at different trophic levels or positions in the food web. The importance of organisms with low biomass and high turnover will be greatly underestimated by comparisons using biomass. Production rather than biomass is far more critical in understanding the capacity of a population's consumption potential. Similarly, production is much more appropriate than biomass in assessing the consumption pressure by predators. Reliance on presence/absence, density, or biomass can easily lead to incorrect interpretations of predator-prey or food web relationships (e.g., Benke and Wallace 1997).

ACKNOWLEDGMENTS

Keith Parsons, David Jacobi, David Stites, and David Gillespie provided valuable assistance with all field sampling, Special thanks to Keith Parsons for supervising most of the laboratory processing and Richard Hauer for conducting the growth studies employed in this study. Thanks to Bruce Wallace, David Dudgeon, Nancy Grimm, and an anonymous reviewer for providing several useful suggestions on the manuscript. The research was supported by grants from the National Science Foundation (DEB-8104427, BSR-8406630, and BSR 8408188). Contribution number 241 from the University of Alabama Aquatic Biology Program.

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