MARINE ECOLOGY PROGRESS SERIES Vol. 114: 165-174, 1994 Published November 3 Mar. Ecol. Prog. Ser.
An empirical model for the prediction of secondary production in marine benthic invertebrate populations
Maria L. Tumbiolol, John A. ~owning~l*
'Consiglio Nazionale delle Ricerche, Istituto di Tecnologia della Pesca e del Pescato, Via Luigi Vaccara 51, 1-91026 Mazara del Vallo, Italy 'Universite de Montreal, Departement de Sciences biologiques, CP 6128. Succursale 'A', Montreal, Quebec, Canada H3C 357
ABSTRACT An exlsting marine benthos production model based on population charactenstics, and a freshwater invertebrate production model, based on population charactenstics and temperature, were tested for apphcabihty to manne benthos populations from around the world The freshwater model makes poor predictions of marine secondary production while the manne model makes better predic- tions but errors are correlated with both water temperature and water depth A new manne benthos production model is therefore constructed that accounts for world-wide vanatlon in benthos biomass, individual body mass, water temperature and depth This mult~variateanalysls shows that secondary production nses with blomass (B) as -B1 as others have found and production varies wlth population maximum body mass (W,) as as suggested by allometnc theory The strong effect of tempera- ture ~ndicatesthat the Qloof secondary production is between 2 and 2 5 The effect of depth is strongly negative, suggesting that food quality may be lower at greater depth but the effect of depth is lessened in cold seas Residual analyses accounting for the influences of biomass, body mass, temperature and depth suggest that anthropogenically enriched regions of the sea are more productive than oligo- trophic waters Our results suggest that rare, large animals living in the depths of cold seas support the lowest rates of exploitation and are thus at greatest nsk of extinction from overexploitation
KEYWORDS. ALlometry . Biomass . Depth . Manne resources . Model . Invertebrates . Production . Renewal . Temperature
INTRODUCTION instrument for the evaluation of the trophic potential of the components of each ecosystem. For example, The measurement of secondary production has marine benthic invertebrates represent an important assumed a fundamental role in the quantification of link in the energy flow from primary producers to fish ecosystem dynamics, since production is one of the and in the recycling of sedimented organic matter major pathways of energy flow (Edmondson 1974, (Crisp 1984). Therefore, an understanding of the fac- Waters 1977).The animal and plant biomass produced tors influencing the production of marine benthic per unit time is the most important parameter for esti- invertebrates is of central importance to the compre- mating the sea's total productivity (Greze 1978). The hension of the functioning of marine ecosystems. estimation of secondary production is of basic impor- In spite of the fact that marine invertebrates provide tance to the rational management of natural resources over 3.5 billion kg of food annually worth $10 bilhon (Waters 1977, Downing 1984), because it is the primary (FAO 1993), previous production research has concen- trated primarily on the production of freshwater organ- isms. Many authors (Allen 1951, Hynes & Coleman 'Addressee for correspondence 1968, Hamilton 1969) have developed methods for the
O Inter-Research 1994 Resale of full art~clenot permitted 166 Mar. Ecol. Prog. Ser
estimation of secondary production that can be applied ments and that predicted by the more complex fresh- in marine or freshwater environments. Unfortunately, water models. these methods are expensive and time consuming to There is ample reason to believe that marine benthos apply. A model elucidating global patterns in sec- production is strongly influenced by environmental ondary production that would allow it to be estimated factors such as temperature and depth. In general, pro- without long and costly study would be of obvious im- duction should be greatest where temperature is high- portance to the theory and practice of marine ecology. est, because physiological rates are greater in warm Marine researchers have been estimating secondary ectotherms (Robinson et al. 1983). Because organic production of marine environments since the early matter decomposes as it sinks (Ferrante & Parker 1977, 1970s (e.g. Buchanan & Warwick 1974, Chambers & Urrere & Knauer 1981, Mann 1988), food quality may Milne 1975, Warwick & Price 1975, Carrasco & Arcos decrease with increasing depth (Honjo 1980, Pom- 1980, Josefson 1982, Andersin et al. 1984, Kristensen meroy et al. 1984, Roman & Tenore 1984). Wolff (1977) 1984, Collie 1985, George & Warwick 1985). Unfortu- suggested that differences in food availability to ben- nately, few attempts have been made to discern pat- thic comn~unities may give rise to positive relation- terns or regularities in these individual estimates of ships between benthic biomass and surface produc- marine invertebrate production. Robertson (1979) first tivity, and negative relationships between benthic related the production to biomass ratio (P/B) to the life- biomass and depth (Sparck 1935, Rowe 1971).Alterna- span of populations, providing estimates of marine tively, species that live at great depth may be well macrobenthos production for populations of known adapted to low food quality (Lopez & Levinton 1987). biomass and life-span. This model is difficult to apply, Depth may influence production beyond the simple in practice, because field longevity can depend more physiological effect of temperature, however. Food on mortality due to predation than on absolute maxi- quality may also change with depth at different rates in mum life-span. Further, life-span is highly vanable in warm and cold climates (Honjo & Roman 1978, Hobbie temperate multivoltine species that overwinter as lar- & Cole 1984, Amon & Herndl 1991), therefore depth vae or adults (Banse & Mosher 1980).Therefore, Banse may have less effect on production in cold seas than in & Mosher (1980) advanced a simpler model relating warm ones. Depth may have more impact on sec- P/B to adult body mass, which is easier to determine ondary production in marine than freshwaters (cf. and less variable than longevity. The only other Plante & Downing 1989) and the effect of depth may attempt to find patterns in the production of marine vary with water temperature. invertebrates is that of Brey (1990), who considered 2 The objective of this study was to test the efficacy of fundamental population parameters: mean annual the Brey and Plante-Downing models for the predic- biomass (B) and mean individual body mass (W). tion of marine invertebrate production. Because these Brey found that production varies as: logP = -0.4 + 2 models inaccurately account for variation in the pro- 1.007 log B - 0.27 log W. duction of marine invertebrates, a new model was Environmental parameters such as oxygen concen- sought to account for world-wide variations in the pro- tration, food availability and quality, and temperature duction of this important fauna1 group. may influence growth rates. The first model to consider the possible effects of environment on invertebrate productivity was developed by Plante & Downing MATERIALS AND METHODS (1989) (hereafter referred to as the Plante-Downing model) for lentic freshwater invertebrates. This analy- Patterns in production of marine benthos popula- sis showed that secondary production is correlated tions were investigated using estimates of population with mean annual biomass, maximum individual body secondary production collected from the world litera- mass (W,) and annual mean surface water tempera- ture. We wished to consider the widest possible range ture (T,) as: logP = 0.06 + 0.791og B - 0.16log W, + of populations, but concerns about data reliability and 0 05 Ts. Morin & Bourassa (1992) and Benke (1993) measurement consistency led us to consider only esti- have developed similar models for stream inverte- mates denved using classical methods such as the brates. Freshwater production models thus account for increment summation, the removal summation, the the influence of some environmental variables on sec- Allen curve, the instantaneous growth rate and size- ondary production, but marine production models still frequency methods (Allen 1951, Hynes & Coleman only account for simple population parameters. It is 1968, Hamilton 1969). Production rates estimated indi- unknown whether Brey's model can adequately rectly as the product of general PIB ratios and B, and as describe the production of organisms from diverse functions of respiration, were rejected a pnon. environments, or whether there is a difference The annual production, the average annual biomass between secondary production in marine environ- and the maximum individual body mass were deter- Tumbiolo & Downing: Marine secondary production 167
mined for each population. For those populations for values using the Bi-ey (1990) and Plante & Downing which several years of sampling were available, (1989) models and the ambient T,, Tb and Z. The annual means were extracted for each year. Estimates LOWESS procedure, an unbiased estimator of non-lin- calculated on a period less than 12 mo or for which ear trends (Cleveland 1979), was used to assess the some cohorts were excluded from consideration were form of these relationships. not included in our analyses. All the estimates were Stepwise, least-squares multiple regression was converted to common units of g dry mass m-2 for used to explore the relationship between Pand B, W,,, annual mean biomass and mg dry mass for individual Tb, T, and depth [log (Z+l)].All variables except tem- body mass in order to test the Plante-Downing model. perature (Plante & Downing 1989) were transformed Particular care was taken with molluscan masses in to their logarithms to linearize responses and reduce order that they be conlparable with other organisms' heteroscedasticity. Depth was transformed to log (Z+l) masses. We therefore retained only molluscan bio- because many intertidal populations (Z = 0 m) were mass, production and individual body mass values included in the data set. The interaction term (TbZ) which were obtained by dissolving shells with HCl was used to assess whether temperature effects were prior to weighing. A conversion factor (Brey et al. 1988) constant with depth. Only variables with partial ef- was sometimes used to convert ash-free dry masses fects significant at the p < 0.001 level were retained, (AFDM) to dry masses without shells. The Brey model and insignificant variables were eliminated using for- was created using AFDM, not simple dry masses, so ward selection (Hocking 1976). Tukey's Studentized dry mass data were converted to g AFDM m-' using range test was used to compare the estimated produc- published conversion factors (Waters 1977, Brey et al. tion for different taxonomic groups, zones and envi- 1988),where necessary, to test this model. ronments. The maximum individual body mass (W,, mg dry mass) was read from size-frequency histograms, from mean length of the largest size class, or from age:body RESULTS mass relationship using 1ength:weight relationships provided by authors. In 1 case, body mass was deter- The data collected include 125 populations of mined from data on a close congener. marine benthic invertebrates, drawn from 34 differ- The annual mean bottom (Tb)and surface (T,) water ent sites, covering 16 amphipod species, 17 bivalves, temperatures ("C) were either obtained from the 1 harpacticoid copepod, 3 decapods, 3 echinoderms, authors of specific production studies or were calcu- 3 gastropods, 3 isopods, 1 leptostrac and 13 poly- lated from published, site-specific temporal trends in chaetes. Data were collected from a broad range of water temperature. In 27 % of the cases, T, was taken geographical regions (Fig. 1). Body mass varied from from an Atlas of World Temperature (U.S. Navy 1955). as little as 10 g dry mass in Canuella perplexa in the Although these data were collected several years ago, Scadovari lagoon, Italy (Ceccherelli & Mistri 1991) to average annual ocean temperatures are time-stable 62 g in Leptogorgia hebes in the soft bottom out of (Tait 1981) and have changed little over this century Mobile Bay, Alabama, USA (Mitchell et al. 1992). (Bethoux et al. 1990). Daily and annual variations in temperature are known to influence the physiological demands on Ns-th .r,,;, benthic organisms (Kinne 1970, Aarset & 5d 80 --=c;--? - w----..-ea=-f-f~--- ,--aw.-h,:& Aunas 1990), but temperature variation 1 60- ,S$- ,<-S, ,.. -7 , p-LA could not be considered because of the ,,< -m 40 - wT rarity of such detailed, site-specific infor- 'L p L- 20 - . l,' ,,, -*,, mation. Depth (Z) was expressed in \$&.,, p,d 0 '!W-.,. 'L-.> 'L< ,, meters, assigning a value of 0 m to all in O- ./ L, '\,, ( ' %%$c. C, intertidal sampling stations. C 20 . , ,' .:) 'L ,I_, . '?".l The adequacy of existing production 1,-.l \ ,'C! --v> 40 - models (Plante & Downing 1989, Brey a i -.,' 1990) was examined by testing the 60 hypothesis that the relationship between SCJ~IIII80 1511 100 21) 0 observed and predicted points is 1:l (t- 50 100 150 c 3 4 U,lsl test). Statistical lack of fit attributable to I)cg~.c(,sof' 1,oilgiIudc environmental conditions was deter- mined by examining the relationship Fig. 1. Map showing sampling sites for which reliable data were found on between the residuals of the predicted the secondary production of marine benthic invertebrates Mar. Ecol. Prog. Ser. 114: 165-174, 1994
5 studied at the bottom of the Baltic Sea (Tb = -0.5 "C, T, Marine Model 0. , .' = 6.1 "C; Highsmith & Coyle 1991), and very high in a This study coastal sampling station off the coast of Florida, USA - - -- LOWESS (Tb = TS = 22.6"C; Mitchell et al. 1991). The biomass .... 1 :l turnover rate or PIB varied from as little as 0.17 to as - much as 23. The full data set and list of sources is available on request from the authors. The marine production model of Brey (1990) fits the - data well while the freshwater model of Plante & Downing (1989) underestimates marine production. The Brey model fits the data with no systematic lack of - fit (Fig. 2A) The slope of the relationship between loglop predicted using Brey's model and the logloP 2 observed in the field was not significantly different - 9' r =0.78 p
- . Anthozoa Bivolvia Amphipodo Polychaeto Others
5 10 15 20 25 Surface Temperature ("C)
loglo Estimated Production
Fig. 4. Relationship between the observed production in 125 populations of benthic invertebrates and the production predicted by Eq. (2)
- 1.5 log P = 0.18 + 0.97 log B - 0.22 log W,,, + 0.04 Tb 0 5 10 15 20 25 0.014Tblog (Z+l) (2) Bottom Temperature ("C) - (n = 123; R2= 0.86; F= 194; p < 0.0001), where all van- ables are listed in decreasing order of their partial sig- nificance (all have p < 0.001). Analysis of covariance showed that the production of benthic populations in different types of environments differed significantly (p < 0.05). Residual analysis of Eqs. (1 & 2) shows that there was no significant differ- ence between the production of intertidal and soft-bot- tom populations, but there was a significant difference (p < 0.05) between production rates of benthic popula- tions found in shallow seagrass beds and those living in intertidal or soft-bottom environments (Table 1).The Tukey test reveals that there was no significant (p 0.05) difference in the production of estuarine and
Fig 3. Relationships between the residuals of the Brey (1990) model of marine invertebrate secondary production (Fig. 2A) Table 1. Fit to the trend in Eq (2) of populations living on dif- and (A) the sea-surface temperature, (B) the water tempera- ferent substrata. Fit is measured by the residuals from Eq. (2), ture at the bottom where the benthic organisms were living, considering the effects of b~omass,body mass, bottom tem- and (C) the depth (Z; in m) of the water at each study site. perature and depth. n: number of populations; SD: standard Solid lines: least-squares linear relationships between the 2 deviation of the mean residual. The vertical line indicates variables no significant difference (p < 0.05) between the residuals of Eq. (2) for the bracketed categories sure of the average temperature climate inhabited by populations, and is therefore much simpler to interpret Substratum Mean res~dual n SD than the surface temperature (see 'Discussion' in Intertidal -0.067 36 Plante & Downing 1989). For the sake of biological Soft bottom -0.024 74 0.072O2Ij4 1 interpretability, we also fit a multivariate equation Seagrass 0.347 11 0,132 including Tb and its interaction with depth: 170 Mar. Ecol. Prog. Ser. 114: 165-174, 1994
Table 2. Fit to the trend in Eq. (2) of populations livlng in estu- tions of equivalent body mass under similar environ- aries and open seas. Other: includes some pecullar environ- mental conditions. ments such as hypersaline lagoons and fjords. Fit is measured Body mass is the second most important variable for by the residual from Eq. (2), considering the effects of bio- mass, body mass, bottom temperature and depth. n: number determining marine secondary production. Our analy- of populations; SD: standard deviation of the mean residual. sis confirms that the production of marine inverte- The vertical line indicates no significant difference (p < 0.05) brates is negatively related to body mass as between the residuals of Eq. (2) for the bracketed categories where B is statistically held constant. This exponent is not significantly different (p < 0.05) from -0.25, the I Substratum Mean residual n value suggested by general allometric theory (Peters SD I 1983).The observed value also agrees with the expo- Estuarine 0.015 62 0.349 Sea -0.008 57 0.220 nent of -0.27 found by Brey (1990),and is statistically Other 0.497 6 0.080 indistinguishable from the exponent found in the Plante-Downing freshwater model (w,,,-'.'~). Our re- sult, however, contrasts with Banse & Mosher's (1980) Table 3. Fit to the trend in Eq. (2)of populations of different finding that production varies as W,,,-037. The differ- taxa. Fit is measured by the residual from Eq. (2),considering ences among the exponents may arise from statistical the effects of biomass, body mass, bottom temperature and fits that are influenced by variables that are unac- depth. n: number of populations; SD: standard devlation of counted for in other models. For example, if we were to the mean residual; p: t-test probability associated with the null hypothesis that the mean residuals of each group do not fit the bivariate relationship between production and differ from zero; ns: p > 0.05 body mass without considering W,,,, Tor Z, we would find an exponent of -0.16. Perhaps these apparent dif- Taxon Mean residual n ferences among exponents of production models are due less to real differences among the data sets than to Gastropoda statistical artifacts due to unexplained variation. Anthozoa P/Bcan be considered an indicator of the maximum Harpacticoidea limit of sustainable exploitation of populations. Be- Amphipoda Bivalvia cause P/Bdeclines with W, (Fig. 5), small species can Polychaeta be exploited at greater rates than large ones, since Echinodermata their renewal rates are high and they can replace their Decapoda Leptostraca Isopoda
marine benthic species, once differences in biomass, body mass, temperature and depth had been accounted for (Table 2). Further, of the 10 taxonomic groups which were present in the data set, only a few populations of gastropods departed significantly from the general trend described by Eqs. (1 & 2) (Table 3).
DISCUSSION
Biomass is the most important variable explaining world-wide variation in marine secondary production. It alone is responsible for 77 % of the explained varia- tion in Eq. (1).The coefficient associated with biomass is 0.96, which is not significantly different from 1, indi- log,o Wm (mg dry mass) cating that there is no demonstrable density-depen- dence of biomass turnover rate in this fauna. The same result was indicated by the analyses of Banse & Fig. 5. Relationship between the biomass turnover rate (PIB) and the average body mass of the individuals in the largest Mosher (1980), Brey (1990) and Morin & Bourassa size class of each population. Solid line: the least-squares lin- (1992).The finding of a coefficient close to unity sug- ear relationship between these 2 variables [log,,,(P/B) = 0.504 gests that the P/B ratio is constant with B for popula- - 0.18810g,~U',,,; r2 = 0.27, n = 126, p < 0.0011 Tumbiolo & Downing: Marine secondary production 171
biomass in a short time. This characteristic also allows small species to be more resilient to environmental perturbations and consequently to be more successful at counterbalancing overexploitation. On the other hand, larger species of invertebrates such as some species of bivalves, decapods or echinoderms show a lower PIB, which indicates less capacity to survive overexploitation. This consideration is of obvious importance when the species considered represents a source of human food. Further, this analysis predicts that marine biodiversity will first be lost in the largest organisms when communities are perturbed or envi- ronmental conditions degraded. This result agrees with the general concept that severe reduction in num- bers constitutes a greater problem for larger bodied vertebrates due to their lower intrinsic population growth rates (Belovsky 1987, Godman 1987, Pimm et a1 1988), which leads them to be extremely vulnerable to extinction (Fenchel 1993) and to rebound slowly after a Annual Mean Temperature ("C) catastrophic decline (Peters 1983). Ours is the first study to seek general patterns in the Fig. 6. Contour plot showing the general relationship combined effects of biological and environmental between water depth, bottom temperature and secondary characteristics on the secondary production of a broad product~onfound by multiple regression and shown in Eq. (2). Predictions are for a population of average biomass (B = 19 g variety of populations of marine invertebrates. Since m-2),and maximum individual bodymass (W,,, = 1162 mg dry production is the result of metabolic processes, it is not mass], shown over the range of environmental conditions surprising that temperature has an influence on it. where data coverage was most dense. The extreme upper left Ecologists have known for many years that tempera- and lower right corners are extrapolated ture influences biological activities (Downing 1984). For example, increased temperature can decrease egg temperature, has significantly lower production if it developnlent time, and increase voltinism, rates of lives in a deeper habitat. This may be due to the fact population growth and feeding The aggregate effect that a much greater proportion of primary production of these factors is to augment growth and reproduc- reaches the bottom in shallow coastal waters than in tion, leading to increased production. The effect deep oceans (Mann 1988). Benthic organisms at deep of temperature on production that we found is not sites depend primarily on low-quality food such as significantly different from that found in analyses of fecal pellets, crustacean exuviae, organic detritus with freshwater invertebrate production. Neither of the a scarce phytoplanktonic component that is degraded coefficients in Eqs. (1 & 2) (0.03, 0.04) are, in fact, sig- during sedimentation (Ferrante & Parker 1977, Urrere nificantly different from 0.05 (Plante & Downing 19891, & Knauer 1981) and thus decreases in quantity and showing that the temperature dependences of produc- quality with increased depth (Honjo 1980, Pomeroy et tion of marine and freshwater organisms are substan- al. 1984, Roman & Tenore 1984). This interpretation is tially similar. The Q,, indicated by the fitted coeffi- bolstered by the significant interaction term in Eq. (2), cients in Eqs. (1 & 2) are between 2 and 2.5, very close which shows that production decreases much more to the standard Qlo found for many physiological rates rapidly with increasing depth in warm waters (Fig. 61, (Hardy 1973). This finding suggests that the influence where the breakdown of sedimented organic matter of temperature on secondary production may be the would be most rapid. result of increased physiological rates in warmer Likewise, there are apparently differences in the waters. secondary production of different types of marine envi- The negative coefficient associated with depth in ronments. The data suggest that seagrass beds support Eq. (1) indicates that production is highest near the sea higher production than soft bottoms and intertidal surface and decreases rapidly in deeper waters. Since zones (Table 1). The average residual in logarithmic Eq. (2) adjusts statistically for the influence of bottom form for soft bottoms and intertidal zones is -0.0381 temperature, the effect of depth on secondary produc- while it is 0.347 for seagrass beds. This suggests that tion is not simply due to lower temperatures at great for a given biomass, body mass, temperature and depth. In fact, Eqs. (1 & 2) show that a given biomass of depth, secondary production in seagrass beds is on a population of a given body mass, living at any given average 10"~~~times, or 2.4-fold, that found in other Mar. Ecol. Prog. Ser. 114: 165-174, 1994
environments. This conclusion is, however, based on structure and interspecific competition (Sarvala 1986), only 11 observations In seagrass beds and, thus, must which may assume differential importance depending be interpreted with caution. This agrees with Phi1 upon trophic level and feeding behaviour. Others (e.g. (1986), however, who found secondary production to Robertson 1979) have hypothesized that population be greater in vegetated areas than in unvegetated structure may also play a role, and that production may areas of the Swedish west coast, probably due to be influenced by the numerical dominance of young or greater food availability in seagrass beds (Virnstein et senescent individuals. Our analysis underscores the al. 1983). importance of considering both environmental and Our analyses predict that biomass-specific produc- population characteristics in studies of the secondary tion levels for animals of a given body mass decrease production of marine benthic invertebrates. systematically from low latitudes through subarctic zones, and decrease, regardless of latitude, from shal- Acknowledgements. This research was supported by an oper- low waters to the ocean depths (Fig. 6). The effect of ating grant to J.A.D. from the Natural Sciences and Engineer- ing Research Council of Canada (NSERC), a team grant from temperature is strongest in shallow waters and the Ministry of Education of the Province of Quebec, and a becomes progressively weaker as depth increases. Our generous travel grant to M.L.T. from the Consiglio Nazionale analyses therefore predict a stronger effect of depth in delle Ricerche of Italy (protocol no. 052976). We are grateful warm waters at low latitudes and subtropical zones. to T. Brey, A. B. Josefson, R. Diaz, J. C. Dauvin, J. Collie and Biomass-specific production rates appear to be highest R. M. Warwick who supplied unpublished data, and to A. Cat- taneo, M. Silva and 3 anonymous referees who provided help- in those populations with small individual body mass ful comments on the manuscript. living in shallow, warm waters, and lowest in popula- tions with large individual body mass living in cold, deep waters. This result leads us to speculate that dras- LlTERATURE CITED tic changes in population biomass levels could endan- ger the viability of species and populations with high Aarset, A. V., Aunaas, T. (1990). Metabolic responses of the individual body mass living in deep, subarctic areas. sympagic amphipods Gammarus wilkitzlui and Onisimus glacialis to acute temperature variations. Mar. Biol. 107: Average mass-specific renewal rates (PIB)vary from 433-438 > 10 in small animals living in warm, shallow environ- Allen, K.R. (1951).The Horowiki Stream. N.Z.mar. Dept Flsh. ments (biomass renewed 10 times annually), to <0.3in Bull. 10: 1-238 large resource organisms like Arctica islandica living Amon, R. M. W., Herndl, G. J. (1991). Deposit feedlng and in cold, deep environments. Fishing mortality should sediment: 11. Decomposition of fecal pellets of Holothuna tubulosa (Holothuroidea, Echinodermata). P.S.Z N I. Mar. therefore be carefully adjusted according to renewal Eco~.12: 175-184 rates in order to avoid resource depletion and extinc- Andersin, A.-B., Lassig, J., Sladler, H. (1984).On the b~ology tion. Large species living in deep, cold environments and production of Pontoporeja affinis Lindstr. in the Gulf therefore appear to be the most vulnerable species, of Bothnia. Limnologica 15: 395-401 Banse, K., Mosher, S. (1980). 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This article was submitted to the editor Manuscript first received: December 30, 1993 Revised version accepted: August 12, 1994