Chapter 1. Assessment of SecondaryProduction: the First Step

JOHN A. DOWNING

1 Introduction

This manual is designed to help freshwater ecologists choose methods for usein the scientific study of secondary productivity. Secondary production has

been defined many times in the literature (e.g. Clarke 1946; Ivlev 1966; Allen1971: Winberg 1971a,b: Waters & Crawford 1973; Edmondson 1974;Cushman et al. 1978; Benke & Wallace 1980) and most definitions are in

agreement. Waters & Crawford (1973) use the term in the sense of Clarke(1946) as 'that amount of tissue elaborated per unit time per unit area,

regardless of its fate'. Other definitions stress that reproductive products andproduction lost to predators and other losses must be included. The tissueelaboration that is usually considered to be 'secondary production' is the

production not only of herbivores but of all freshwater invertebrates (seeMorgan et al. 1980). Therefore, the rate of secondary production can bedefined more specifically for this manual as that amount of tissue elaborated

by freshwater invertebrates per unit time per unit area, regardless of its fate(after Clarke 1946; Waters & Crawford 1973). Many techniques exist for the

study of secondary production in freshwaters, and it is the goal of this bookto help the researcher to choose the appropriate ones to use under differentcircumstances.

Although each author contributing to this handbook has dealt with adifferent set of techniques, one single conclusion has been reachedindependently by each. This common conclusion is that the choice of proper

technique depends upon the question posed or the hypothesis underexamination. Many of the authors have come to a worrying secondconclusion. They believe that few production biologists to date have posed

questions or tested hypotheses; most have simply concerned themselves withthe estimation of single rates of production or its components. Because thechoice of technique depends upon the hypothesis to be tested, it has beendifficult for production ecologists to choose among the many techniques

available. The gravity of this conclusion has been discussed by manyphilosophers of science. For example, F.S.C.Northrop (1947) has writtenthat 'One may have the most rigorous of methods during the later stages of

I

2 Chapter Iinvestigation, but if a false or superficial beginning has been made, rigorlater on will never retrieve the situation.' When questions are only poseda posteriori, we risk the frequent choice of inappropriate methods (cf. LeCren

1972).Because of this problem, this first chapter will review the general reasonswhy ecologists estimate secondary production, and will then provide a

summary of the many interesting hypotheses suggested by the rich literature inthis field.

2 Theoretical Justification for Secondary Production Research

A field of study is usually judged useful if it has a potential for contributing toestablished disciplines or goals. It is the same for the field of secondary

production in freshwaters. Although some production biologists haveestimated productivity of a species in a certain area merely because no suchdata have been published, many others feel that their studies are important

because they address one or more of four main conceptual subject areas.These are:

(1) The elucidation of energy or material transfers within communities andecosystems.(2) The rational management of aquatic resources.(3) The detection of the effects of pollution.(4) The formation of general theories of biological productivity.

Below, I present a brief discussion of the relationship between productionbiology and these general ecological goals.

2.1 Energy or material transfer within ecosystemsG.E.Hutchinson (1942) has written that when Lindeman published his

famous paper The Trophic-Dynamic Aspect of Ecology' (1942), he hopedthat it would serve as a program for future ecological research. This hascertainly been true. Lindeman suggested that if one could reduce the

interactions among components of a community to a common currency (e.g.energy), then one could quantify the interactions and learn to predict changes

such as succession within ecosystems. Lindeman introduced the majorconcept that an organism's success in an environment might be a function of

its ability to fix and retain energy.This concept not only underlies much ofcurrent productivity research, butwas part of the stimulus for the research undertaken in the International

Biological Programme ofwhich this handbook is a result. The elegance of thisconcept is demonstrated by the frequency with which it has been accepted asjustification for research in secondary production (e.g. Kimerle & Anderson

Assessment of Secondary Production: The First Step 31971; Czeczuga & Bobiatyhska-Ksok 1972; Burke & Mann 1974; Nichols1975; Zwick 1975; Benke 1976; Hibbert 1976; Zytkowicz 1976; Waters 1977;Neves 1979; Benke & Wallace 1980; Tonolli 1980). I believe that Edmondson(1974) has expressed it best: i cannot think of secondary production

as a distinct process by itself. Rather it is part of a larger scheme ofthe movement of material through the ecosystem, and this is based on theactivities of individuals and populations of animals.' Much effort has gone

into the quantification of the components of this larger scheme (e.g. Kajak &Hillbricht-Ilkowska 1972). The frustrating aspects are that even the simplestcommunity has many components, there are many different types of possible

interactions among components, almost all individual organisms arebehaviorally plastic, and it is difficult to obtain accurate estimates of even one

rate of transfer under one set of simple circumstances. The result is thatfulfillment of the trophic-dynamic goal of production ecology is a formidabletask.

2.2 Management of aquatic resources

The measurement of secondary production is thought essential to themanagement of aquatic resources, probably due to our trophic-dynamic viewof ecology. The most concrete freshwater resource is, of course, fish. Becausemany fish depend to a high degree upon zooplankton and benthos for food(e.g. Zelinka 1977), a variety of authors have suggested that an understanding

of the production processes of invertebrates will facilitate management offishstocks (Zytkowicz 1976; Waters 1977; Williams c/ al. 1977; Priymachenko etal. 1978) or prediction of rates offish production (Johnson & Brinkhurst 1971;

Moskalenko 1971; Czeczuga & Bobiatyhska-Ksok 1972; Johnson 1974;Zytkowicz 1976). A recent paper by Hanson & Leggett (1982) shows that fishyield is related to the mean standing biomass of macrobenthos in a lake, and

thus suggests that a general relationship probably exists between secondaryproductivity and fish production. This relationship has yet to be describedempirically, however. The importance of secondary producers to the study of

fish dynamics (Hamill et al. 1979) is underscored by their trophic intermediacybetween fish populations and energy sources (Mathias 1971; Dermott et al.

1977). Johnson (1974) has also suggested that enhancement of secondaryproduction may be important to the development of freshwater aquaculture.

2.3 Detection ofpollution

Because secondary production is a complex process that can be altered byvariations in many variables, it seems logical that variations in rates ofsecondary production could be used to detect pollution (Winberg 1971b; see

review by Waters 1977). For example, Golterman (1972) found that the ratio

4 Chapter 1of production to biomass (P/B) ofzooplankton is higher in thermally pollutedwaters than in control areas. A similar effect is suggested by McNaught&

Fenlon (1972). Many researchers have found that benthos production in lakesis highest near areas of human activity (e.g. Mikulski et at. 1975;Wolnomiejski et a/. 1976; Dermott et al. 1977). Zelinka (1977), on the otherhand, found that human activities (stream bed modification, toxic wastes, etc.)most often have a negative effect on mayfly production. Other authors suggest

that secondary producers could be used in sewage treatment (e.g. Kimerle &Anderson 1971; Waters 1977), or in the self-purification of pollutedecosystems.

2.4 Formation ofgeneral theories of biological productionWinberg(1971a;Tonolli 1980) has stated that the'development of a theory of

biological productivity is one of the central aims ofcontemporary biology...'.Mann (1972) has made a similar statement and suggests that we must 'makeevery effort to improve the accuracy of the observations and the confidence

limits of resulting estimates' in order to help produce a general ecologicaltheory of biological budgets. If we take the term 'theory' in the usual sense,

that is, a construct that makes predictions about nature, then one of the basicreasons for measuring secondary production is to learn how to predict it.

Looking back to Sections 2.1 and 2.2. we can see why it is very important to beable to predict rates of productivity. The trophic dynamic analysis ofecosystems requires the estimation of the secondary production of many

populations of animals. If these values could be predicted accurately under avariety of conditions, then much effort could be saved in the trophic analysisof communities. In addition, general theories of secondary production would

be very useful in the management of aquatic resources.Brylinsky (1980) has written recently that productivity data should beanalyzed 'with a view to identifying those factors most important incontrolling biological production. Once identified, management efforts could

be directed towards manipulation of those factors appearing most important'.Most of the balance of this introductory chapter will be devoted to anexploration of those specific factors which have been suggested as important

in determining the rate of secondary production in fresh waters. It is my hopethat presentation of these hypotheses will help production biologists to definespecific questions for study, and thus indicate appropriate methods foranalysis.

3 Factors Affecting Rates of Secondary ProductionThis section contains a summary of the hypotheses suggested most frequently

by production biologists. Most of these hypotheses have arisen from isolated

Assessment of Secondary Production: The First Step 5observations; only a few have been tested explicitly. It is not my intention tosuggest that these are the only interesting hypotheses or even the hypothesesthat will yield the most or quickest progress in production ecology. I only wish

to demonstrate that we possess a large set of implicit theories. These, or otherhypotheses, if tested explicitly, could not only yield progress in productionbiology, but could make the choice of methods a more tractable problem.

For the sake of organization, I have arranged these hypotheses into fourcategories. I will first discuss how rates of secondary production are affected

by characteristics of the population under study, then I will examinehypotheses that relate to aspects of the environment in which they live.Thirdly, I will present the few hypotheses in the literature that address the

manner in which secondary production is affected by interactions amongpopulations in the same community. Lastly, I will discuss the possible effectsof basin characteristics.

3.1 Effect ofpopulation characteristics

There are certain intrinsic characteristics of populations which dictate themanner in which they live. When one examines an animal population casually,certain elementary questions materialize. Four of these questions are: Howmany are there, and what is their biomass? What is their life history like; howlong do they live, How big are they? What kind of animal are they?

Production biologists feel that each of these questions has a bearing on therate of secondary production that populations are able to attain.

3.1.1 Biomass

The literature contains a number of specific hypotheses regarding therelationship of production (P) to mean biomass (B). First, there are many(e.g. Laville 1971; Gak et ai 1972; Eckblad 1973; Waters & Crawford 1973;Johnson 1974; Lavandier 1975; Mikulski et ai 1975; Wolnomiejski et al.

1976; Waters 1977; Hamill et al. 1979; Makarewicz & Likens 1979; Benke &Wallace 1980; Short & Ward 1980) who have suggested that the ratio P/B is aconstant (c) for a given type of organism. That is:

P/B = c (l.l)If in fact P/B is constant, then production is an increasing linear function ofbiomass with slope c and intercept zero:

P=cB (1.2)

This relationship suggests that P = 0 at B =0, and that P = xc at B = oc. IfP/B is constant then production is not density dependent and is not subject to

6 Chapter 1the normal constraints imposed by the carrying capacity of the environment.A mental Malthusian exercise tells us that this cannot be so. Even though therelationship between P and B may appear linear over a small range of B, theconvenient but inaccurate notion that P/B is constant should be abandoned.

Many have already done this for empirical reasons (e.g. McLaren 1969;Schindler 1972; Paterson & Walker 1974; Jonasson 1975; Pedersen et al.

1976; Janicki & DeCosta 1977; Momot 1978; Pinel-Alloul 1978; Adcock1979; Banse & Mosher 1980; Nauwerck et al. 1980; Uye 1982). Jonasson(1975) has found that it is not even safe to use the same value of P/B for onespecies at one site in successive years. He found that P/B for Chironomusanthacinus was 4 in one year and 0-8 the next. Because the relation between

production and biomass is not linear, there will be a necessary negativerelationship between P/B and B. The danger is that variables correlated with B(e.g. temperature, body size, respiration) may account for statisticallysignificant variation in P/B when they would not account for significantvariation in P beyond the accurately fitted effect of B. This could lead to errors

in both interpretation and predictive ability.

3.1.2 Age, lifespan, and voitinismThe length of life or relative age of individuals in a population also seems toaffect production. The influence of age on production is not clear-cut. Someauthors feel that P/B declines with age (Hibbert 1976; Waters 1977; Banse &

Mosher 1980) but this could simply be due to the non-linear effect of B on P, ifB and age are positively correlated. Others have examined the effect of age ongrowth rate. Johnson (1974) found that the growth rate ofamphipods declinedwith the age of the population, while Coon et al. (1977) found that the

growth rate of mussels increased with age. This contradiction is probably duein part to the sort of growth rate under discussion. Sutcliffe et al. (1981)suggest that specific growth rates (% wet wt. day ~') decrease with increasedage, while absolute growth rate (wet wt. day"1) occurs when the animal's

body size is about one-half of the maximum. Although age and biomass aresometimes confounded, Borkowski (1974) feels that, at least for marine snails,older populations tend to have higher rates of secondary production. The

lifespan of animals has a similar effect, such that longer-lived animals havelower rates of production (Zaika 1970; Waters 1977; review by Banse &

Mosher 1980).The effect of voitinism (number of generations per year) is consistent andcontinuous with the effect of lifespan. All authors who cite this effect (e.g.Johnson 1974: Zytkowicz 1976: Waters 1977: Jonasson 1978; Banse &

Mosher 1980; Benke & Wallace 1980; Wildish & Peer 1981) suggest thatsecondary production and P/B increase with the number of generations

Assessment of Secondary Production: The First Step 7produced per year. Populations that are multivoltine have higher rates ofproduction than those that are univoltine. An analysis presented by Jonasson(1978) suggests that we may have erroneously ascribed causation in thisapparent correlation. He suggests that faster growth in the littoral zone

permits more generations per unit time. Thus, multivoltinism may be an effectof high production rates, not a cause of them.

3.1.3 Body-sizeThe effect of body-size on secondary production is one of the few relationships

that have been tested explicitly. Unfortunately, much of this work hasemployed P/B as a dependent variable and is, therefore, difficult to interpret

mechanistically. The conclusion has been that P/B decreases with increasingbody-size (M) in the population (Janicki & DeCosta 1977; Waters 1977;

Finlay 1978; Banse & Mosher 1980; Benke & Wallace 1980). Banse & Mosher(1980) have shown that P/B varies as a function of M:

P/B = aMb (1.3)where a and b are fitted constants. Because B = NM(N = average population

density) then:

P = aNcM1+b (1.4)where c = 1. This equation suggests that the effect of body-size would be more

accurately determined by a multiple regression employing both populationdensity and mean body-size (see Chapter 8). There appears to be a real effect of

body-size on secondary production, upheld by the experiments of Zelinka(1977) who found that benthos communities made up of larger species had

lower overall rates of secondary production.

3.1.4 Taxonomy and trophic status

A variety of authors have suggested that physiological and ecologicaldifferences among taxonomic units account for differences in secondary

productivity. Jonasson (1978) suggests that similar species have developeddifferent tolerances and efficiencies for dealing with environmental problems,

thus production rates must vary among species. Coon et al. (1977) suggest thesame for mussels. Makarewicz & Likens (1979) suggest that differences in P/Bfor rotifers among lakes are probably due to taxonomic differences. A numberof workers (Mikulski et al. 1975; Pederson et al. 1976; Waters 1977;

Nauwerck et al. 1980) have suggested that cladocerans are more productivethan copepods, which are, in turn, more productive than rotifers. Schindler(1972), however, suggests that P/B is higher for rotifers than for other

8 Chapter 1plankton, thus the apparent low productivity of rotifers could be due toinaccurate biomass estimation. Herbivorous taxa are generally thought to bemore productive than detritivores or carnivores (Waters 1977; Jonasson

1978).

3.2 Effect of environmentalfactors

It is one of the basic tenets of ecology that the success of organisms in aparticular ecosystem is determined in part by the suitability of theenvironment. Among the most obvious aspects of the environment that might

affect animal production are the average temperature, the ability of theecosystem to produce sufficient food of acceptable quality, the character of thesubstrate, and the concentration of respirable oxygen.

3.2.1 Temperature

Temperature has long been known to influence rates of activity from amolecular to an organismal scale. It is not surprising, therefore, that manyproduction ecologists have found that rates of secondary production increasewith temperature (e.g. Neves 1979: Laville 1971; McNaught & Fenlon 1972;

Edmondson 1974; Kititsyna & Pidgaiko 1974; Paterson & Walker 1974;Pederson et al. 1976; Zytkowicz 1976; Iverson & Jesson 1977; Finlay 1978;Selin & Hakkari 1982). P, B also is thought to rise with increased temperature,either as a linear (Winberg et al. 1973; Johnson 1974; Paterson & Walker

1974; Wildish & Peer 1981; Uye 1982) or a curvilinear (Johnson & Brinkhurst1971;Janicki&DeCosta 1977; Waters 1977; Nauwerck etal. 1980) function.Banse & Mosher (1980), on the other hand, show that P/B is not correlatedwith temperature after regression on body-size.

The general positive effect of temperature on secondary production is aresult of the reproductive biology of zooplankton and benthos. A variety ofauthors have suggested that growth rates increase (Johnson 1974; Jonasson

1978: Humpesch 1979; Vijverberg 1980: Marchanl & Hynes 1981; Sutclifle etal. 1981), egg development times decrease (Schindler 1972: Bottrell 1975;

Makarewicz & Likens 1979: Vijverberg 1980), the rate of population increaserises (Armitage et al. 1973), and feeding rates increase (Zimmerman & Wissing

1978; see Chapter 9) with increased temperature. These factors tend toincrease production at high temperature (see Chapter 2). On the other hand,

O'Brien et al. (1973) suggest that average clutch size of Diaptomus leptopusdecreases with temperature, and Aston (1973) suggests that egg production byoligochaetes declines at high temperature. Pidgaiko et al. (1972) conclude thattemperature variation could have either a positive or negative effect onsecondary production, depending upon geographic location and basinmorphometry.

Assessment of Secondary Production: The First Step 93.2.2 Food production, availability, and qualityA community of heterotrophs can fix no more energy than the amount madeavailable to them by primary producers. Edmondson (1974) has reasoned thatthe rate of primary production must set the upper limit for secondaryproduction. Using similar logic, many authors have suggested that rates ofproduction of freshwater benthos and zooplanklon are positively related to

food availability (Miller et al. 1971; Ladle et al. 1972; George & Edwards1974; Prikhod'ko 1975; Martien & Benke 1977; Jonasson 1978: Neves 1979;Benke & Wallace 1980; Nauwerck et al. 1980). Others have found that rates ofzooplankton and benthos production are positively related to rates of primary

production (Patalas 1970, cited by Schindler 1972; Hillbricht-Ilkowska 1972,cited by Pederson et al. 1976; Monokov & Sorokin 1972; Brylinsky & Mann

1973; Johnson 1974; Dermott et al. 1977; Makarewicz & Likens 1979; Smyly1979: Brylinsky 1980; Strayer et al. 1981). Winberg (1971b) has been morespecific, hypothesizing that secondary production (Ps) is about 10% ofprimary production (Pp), on the average. This suggests that:

Ps = a + bPp (1.5)where a = 0 and b = 0-1. A recent analysis by Brylinsky (1980) shows that

phytoplankton primary production is a better predictor of zooplanktonproduction than phytoplankton biomass, but the relationship may not belinear. Equation 1.5 probably overestimates zooplankton production at lowphytoplankton production, and makes underestimates at high phytoplanktonproduction. The relationship between phytoplankton production and

secondary production is probably also responsible for apparent relationshipsbetween secondary production and nutrient conditions (e.g. Stross et al. 1961;Halle/ al. 1970; Wattiez 1981) and alkalinity (Waters 1977; Pinel-Alloul 1978;Neves 1979). It should also be remembered that quality of food is important indetermining the secondary production of both zooplankton (Pederson et al.

1976; Vijverberg 1976, 1980; Makarewicz & Likens 1979; Nauwerck et al.1980), and benthos (Swiss & Johnson 1976; Willoughby & Sutclifle 1976;Zimmerman & Wissing 1978; SutcliflTe et al. 1981).

3.2.3 Oxygen concentrationThe availability of oxygen is thought to be critical, especially to the benthosbecause they often live in areas that are oxygen-poor. Brylinsky (1980),

however, has found that carnivorous zooplankton production in a wide rangeof lakes is also influenced by oxygen concentration in the epilimnion.Jonasson (1978) suggests that sufficient oxygen is important to benthos

production because food cannot be metabolized efficiently at low oxygenlevels. This conclusion has also been reached by Dermott et al. (1977) and

10 Chapter IRosenberg (1977). Aston (1973) suggests that egg production in freshwateroligochaetes is constant with decreasing oxygen concentration until somecritical low level is reached. Pond benthos seem to require >lmgl~1 of

dissolved oxygen in order to maintain positive production (Martien & Benke1977). Laville (1971) suggests that, at least for some benthos, secondaryproduction and oxygen concentration are inversely related (see also regressionanalysis of Brylinsky 1980).

3.2.4 Substrate characteristicsAnother aspect of the environment that has been hypothesized as important tolake and stream benthos is the character and composition of the substrate.Resh (1977), for example, found that the production of stream caddisflies waspositively related to the average size of particle in the substrate. Hamill et al.(1979), working in a large river, found that the production of benthic snailswas highest at intermediate substrate particle size. Similar suggestions have

been made by Mecom (1972), Martien & Benke (1977), and Neves (1979). Forlacustrine benthos, secondary production seems to rely more heavily onorganic matter content than particle composition (e.g. Johnson 1974;

Zytkowicz 1976; Marchant & Williams 1977; Jonasson 1978). In addition,Zytkowicz (1976) feels that benthos production in lakes is a positive functionof the depth to which sediments can be penetrated by benthic organisms.

3.2.5 Miscellaneous environmentalfactorsThree hypotheses have been advanced which do not fit neatly into broadercategories but which are, nonetheless, interesting. An important factor in

streams and rivers seems to be the current velocity. Zelinka (1977), Hamill etal. (1979). and Neves (1979) all suggest that secondary production decreaseswith increasing water flow rate. With respect to lacustrine zooplankton

production, Edmondson (1974), Makarewicz & Likens (1979), and Selin &Hakkari (1982) have suggested a positive relationship with intensity of solarradiation. Finally, Burgis (1971) and Paterson & Walker (1974) suggest that

high zooplankton and benthos production rates should be found in the moststable ecosystems.

3.3 Predation, competition, and diversity

Predation, competition, and diversity are three topics that have generatedmuch interest in ecology, yet production biologists have seldom consideredthem. Current thought regarding the effect of predation upon secondary

production is contradictory. Hall et al. (1970), Zytkowicz (1976), Waters

Assessment of Secondary Production: The First Step 11(1977), and Banse & Mosher (1980) suggest that predation leads to increased

production, presumably because the slow growing organisms are removedfrom the population. Zndanova & Tseyev (1970), Miller et al. (1971),

Prikhod'ko (1975), and Momot (1978) suggest that predation decreasesproduction perhaps due to a decline in growing biomass. Thoughts oncompetition are less contradictory but less well developed. The basic belief is

that competition decreases the production of a population (see George 1975;Benke 1976; Lavandier 1981). Production ecologists have not considered thepossible positive effects of competition on community production (cf.economic theory). The effect of diversity upon secondary production has onlybeen considered (to my knowledge) by Paterson & Walker (1974). Their datasuggest that the low benthos diversity in a saline lake allowed very high rates of

secondary production.

3.4 Lake morphometry, lateral zonation, and allochthonom input

The morphological characteristics of the ecosystem or placement within it alsoseems to affect secondary production. The literature generally suggests that

shallower lakes support higher rates of secondary production (Johnson 1974;Zytkowicz 1976; Matuszek 1978; Brylinsky 1980). Johnson (1974) alsosuggests that the surface area of a lake may be important, since in larger lakesthe profundal zone is less enriched by the littoral zone or allochthonoussources. Other authors have suggested the importance of allochthonousmaterials to secondary production in both lakes and streams (Edmondson

1974; Willoughby & Sutcliffe 1976; Marchant & Williams 1977; Martien &Benke 1977; Waters 1977; Adcock 1979). Possibly due to high primaryproduction in the littoral zone, it is generally believed that secondaryproduction in near-shore areas and macrophyte beds is greater than in allother areas (Mathias 1971; Johnson 1974; Kajak & Dusoge 1975a,b, 1976;

Mikulski et al. 1975; Jonasson 1978; Neveau & Lapchin 1979; Kajak et al.1980). The only contradiction seems to be for some stream ecosystems wherehighest rates of productivity are seen in mid-stream (e.g. Neves 1979).

4 Concluding CommentsThe preceding paragraphs indicate that many variables are involved in the richvariety of hypotheses regarding secondary productivity. In some cases, it isdifficult to extricate real effects from artefacts. For this reason tests of

hypotheses should take one of two courses. Either we should test for the effectofcertain factors under conditions that control all other variables, or we mustpose multivariate hypotheses that account for simultaneous covariation inmore than two variables. I believe that the former approach is currently more

12 Chapter 1popular because it is conceptually simple; while the latter approach is moreuseful, because it is difficult to control circumstances without altering them.

What is really important, though, is that production ecologists defineproblems before seeking methods for their examination. To quote again from

Northrop (1947): 'It is like a ship leaving port for a distant destination. A veryslight erroneous deviation in taking one's bearings at the beginning may result

in entirely missing one's mark at the end regafdless of the sturdiness of one'scraft or the excellence of one's subsequent seamanship.' This first chapter hasexamined the range of production hypotheses currently under considerationby production biologists. The chapters that follow strive to supply methods

that can be used to test these and other production hypotheses.

5 References

Adcock J.A. (1979) Energetics of a population of the isopod Asellus aquaticus: lifehistory and production. Freshw. Bioi, 9, 343-355.Allen K.R. (1971) Relation between production and biomass. J. Fish. Res. Board Can.,

28, 1573-1581.Armitage K.B., Saxena B. & Angino E.E. (1973) Population dynamics of pond

zooplankton, I. Diaptomus pallidus Herrick. Hydrobiologia, 42, 295-333.Aston R.J. (1973) Field and experimental studies on the effects of a power station

effluent on Tubificidae (Oligochaeta, Annelida). Hydrobiologia, 42, 225-242.Banse K. & Mosher S. (1980) Adult body mass and annual production/biomass

relationships of field populations. Ecol. Monogr., 50, 355-379.Benke A.C. (1976) Dragonfly production and prey turnover. Ecology, 57, 915-927.

Benke A.C. & Wallace J.B. (1980) Trophic basis of production among net-spinningcaddisflies in a southern Appalachian stream. Ecology, 61, 108-118.Borkowski T.V. (1974) Growth, mortality and productivity of south Floridian

Littorinidae (Gastropoda: Prosobranchia). Bull. Mar. Sci., 24, 409-438.Bottrell H.H. (1975) The relationship between temperature and duration of egg

development in some epiphytic Cladocera and Copepoda from the River Thames,Reading, with a discussion of temperature functions. Oecologia, 18, 63-84.Brylinsky M. (1980) Estimating the productivity of lakes and reservoirs. In

E.D.LeCren & R.H.Lowe-McConnell (eds.), The Functioning of FreshwaterEcosystems. IBP 22. Cambridge: Cambridge University Press.Brylinsky M. & Mann K.H. (1973) An analysis of factors governing productivity in

lakes and reservoirs. Limnol. Oceanogr., 18, 1-14.Burgis M.J. (1971) The ecology and production of copepods, particularly

Thermocyclops hyalinus, in the tropical Lake George, Uganda. Freshw. Biol., 1,169-192.Burke M.V. & Mann K.H. (1974) Productivity and production to biomass ratios of

bivalve and gastropod populations in an eastern Canadian estuary. J. Fish. Res.Board Can., 31, 167-177.Clarke G.L. (1946) Dynamics of production in a marine area. Ecol. Monogr., 16,

321-335.Coon T.G., Eckblad J.W. & Trygstad P.M. (1977) Relative abundance and growth of

Assessment of Secondary Production: The First Step 13mussels (Mollusca: Eulamellibranchia) in pools 8, 9 and 10 of the Mississippi.

Freshw. Biol., 7, 279-285.Cushman R.M., Shugart H.H., Jr., Hildebrand S.G. & Elwood J.W. (1978) The effect

of growth curve and sampling regime on instantaneous-growth, removal-summation, and Hynes/Hamilton estimates of aquatic insect production: acomputer simulation. Limnol. Oceanogr., 23, 184-189.Czeczuga B. & Bobiatynska-Ksok E. (1972) The extent of consumption of the energy

contained in the food suspension by Ceriodaphnia reticulata(Jur\ne). In Z.Kajak &A.Hillbricht-Ilkowska (eds.), Productivity Problems in Freshwaters. Proceedings

ofthelBP-UNESCO Symposium on Productivity in Freshwaters. Krakow: PolishScientific Publishers.Dermott R.M., KalfT J., Leggett W.C. & Spence J. (1977) Production of Chironomus,

Procladius, and Chaoborus at different levels of phytoplankton biomass in LakeMemphremagog, Quebec-Vermont. J. Fish. Res. Board Can., 34, 2001-2007.Eckblad J.W. (1973) Population studies of three aquatic gastropods in an intermittent

backwater. Hydrobiologia, 41, 199-219.Edmondson W.T. (1974) Secondary production. Mitt. Int. Ver. Theor. Angew.

Limnol., 20, 229-272.Finlay B.J. (1978) Community production and respiration by ciliated protozoa in the

benthos of a small eutrophic loch. Freshw. Biol., 8, 327-341.Gak D.Z., Gurvich V.V., Korelyakova I.L., Kastikova L.E., Konstantinova N.A.,

Olivari G.A., Priimachenko A.D., Tseeb Y.Y., Vladimirova K.S. &Zimbalevskaya L.N. (1972) Productivity of aquatic organism communities ofdifferent trophic levels in Kiev Reservoir. In Z.Kajak & A.Hillbricht-Ilkowska(eds.), Productivity Problems in Freshwaters. Proceedings of the IBP-UNESCO

Symposium on Productivity in Freshwaters. Krakow: Polish Scientific Publishers.George D.G. (1975) Life cycles and production of Cyclops vicinus in a shallow

eutrophic reservoir. Oikos, 26, 101-110.George D.G. & Edwards R.W. (1974) Population dynamics and production of

Daphnia hyalina in a eutrophic reservoir. Freshw. Biol., 4, 445-465.Golterman H.L. (1972) Report of the working group 'Production studies as a help in

dealing with man-made changes in waters (eutrophication, pollution, self-purification).' In Z. Kajak & A. Hillbricht-Ilkowska (eds.), Productivity Problems

in Freshwaters. Proceedings of the IBP-UNESCO Symposium on Productivity inFreshwaters. Krakow: Polish Scientific Publishers.Hall, D.J., Cooper W.E. & Werner E.E. (1970) An experimental approach to the

production, dynamics, and structure of freshwater animal communities. Limnol.Oceanogr, 15, 839-928.Hamill S.E., Qadri S.U. & Mackie G.L. (1979) Production and turnover ratio of

Pisidium casertanum (Pelecypoda: Sphaeriidae) in the Ottawa River near Ottawa-Hull, Canada. Hydrobiologia, 62, 225-230.Hanson J.M. & Leggett W.C. (1982) Empirical prediction offish biomass and yield.

Can. J. Fish Aquat. Sci., 39, 257-263.Hibbert C.J. (1976) Biomass and production of a bivalve community on an intertidal

mud-flat. J. Exp.Mar. Biol. Ecoi, 25, 249-261.Humpesch U.H. (1979) Life cycles and growth rates of Baetis spp. (Ephemeroptera:

Baetidae) in the laboratory and in two stony streams in Austria. Freshw. Biol 9467-479.

14 Chapter 1Hutchinson G.E. (1942) Addendum to R.L.Lindeman's The trophic-dynamic aspect

of ecology'. Ecology, 23, 418.Iverson T.M. & Jesson J. (1977) Life-cycle, drift, and production of Gammarus pulex

L. (Amphipoda) in a Danish spring. Freshw. BioL, 7, 287-296.Ivlev V.S. (1966) The biological productivity of waters. J. Fish. Res. Board Can., 23,

1727-1759.Janicki A.J. & DeCosta J. (1977) The effect of temperature and age structure on P/B for

Bosmina longirostris in a small impoundment. Hydrobiologia, 56, 11-66.Johnson M.G. (1974) Production and productivity. In R.O.Brinkhurst (ed.), The

Benthos of Lakes. London: Macmillan Press.Johnson M.G. & Brinkhurst R.O. (1971) Production of benthic macroinvertebrates of

Bay of Quinte and Lake Ontario. J. Fish Res. Board Can., 28, 1699-1714.Jonasson P.M. (1975) Population ecology and production of benthic detritivores.

Verh. Int. Verein. LimnoL, 19, 1066-1072.Jonasson P.M. (1978) Zoobenthos of lakes. Verh. Int. Verein. LimnoL, 20, 13-37.

Kajak Z. & Dusoge K. (1975a) Macrobenthos of Lake Taltowisko. Ekol. Pol., 23,295-316.Kajak Z. & Dusoge K. (1975b) Macrobenthos of Mikolajskie Lake. Ekol. Pol., 23,

437-457.Kajak Z. & Dusoge K. (1976) Benthos of Lake Sniardwy as compared to benthos of

Mikolajskie Lake and Lake Taltowisko. Ekol. Pol., 24, 77-101.Kajak Z. & Hillbricht-Ilkowska A. (eds.) (1972) Productivity Problems in Freshwaters.

Proceedings of the IBP-UNESCO Symposium on Productivity in Freshwaters.Krakow: Polish Scientific Publishers.Kajak, Z., Bretschko G., Schiemer F. & Leveque C. (1980) Secondary production:

zoobenthos. In E.D.LeCren & R.H.Lowe-McConnell (eds.) The Functioning ofFreshwater Ecosystems. IBP 22. Cambridge: Cambridge University Press.Kimerle R.A. & Anderson N.H. (1971) Production and bioenergetic role of the midge

Glyptotendipes barbipes (Staeger) in a waste stabilization lagoon. LimnoLOceanogr., 16, 646-659.Kititsyna L.A. & Pidgaiko M.L. (1974) Production of Pontogammarus robustoides in

the cooling pond of the Kurakhovka thermal power plant. Hydrobiol. J., 10(4),20-26.Ladle M., Bass J.A.B. & Jenkins W.R. (1972) Studies on production and food

consumption by the larval Simuliidae(Diptera) of a chalk stream. Hydrobiologia,39, 429-448.Lavandier P. (1975) Cycle biologique et production de Capnioneura brachyptera D.

(Plecopteres) dans un ruisseau d'altitude des Pyreneescentrales. Ann. LimnoL, 11,145-156.Lavandier P. (1981) Cycle biologique, croissance et production de Rhithrogena

loyolaea Navas (Ephemeroptera) dans un torrent Pyreneen de haute montagne.Ann. LimnoL, 17, 163-179.Laville H. (1971) Recherche sur les chironomides lacustre du Massif de Neouville

(Hautes-Pyrenees) 2. Communautes et production benthique. Ann. LimnoL, 7,335-414.LeCren E.D. (1972) Report ofworking group on 'Secondary production and efficiency

of its utilization including fish production'. In Z. Kajak & A. Hillbricht-Ilkowska

Assessment of Secondary Production: The First Step 15(eds.), Productivity Problems in Freshwaters. Proceedings of the IBP-UNESCO

Symposium on Productivity in Freshwaters. Krakow: Polish Scientific Publishers.Lindeman R. L. (1942) The trophic-dynamic aspect of ecology. Ecology, 23,399-418.

Makarewicz J.C. & Likens G. E. (1979) Structure and function of the zooplanktoncommunity of Mirror Lake, New Hampshire. Ecol. Monogr., 49, 109-127.Mann K.H. (1972) Report ofworking group on 'Biological budgets ofwater bodies'. In

Z. Kajak & A. Hillbricht-Ilkowska (eds.), Productivity Problems in Freshwaters.Proceedings of the IBP-UNESCO Symposium on Productivity in Freshwaters.Krakow: Polish Scientific Publishers.Marchant R. & Hynes H.B.N. (1981) The distribution and production of Gammarus

pseudolimnaeus (Crustacea: Amphipoda) along a reach of the Credit River,Ontario. Freshw. Biol., 11, 169-182.Marchant R. & Williams W.D. (1977) Population dynamics and production of a brine

shrimp Parartemia zietziana Sayce (Crustacea: Anostraca) in two salt lakes inWestern Victoria, Australia. Austr. J. Mar. Freshwat. Res., 28, 417-438.MartienR.F. &BenkeA.C.( 1977) Distribution and production oftwo crustaceans in a

wetland pond. Am. Midi. Nat., 98, 162-175.Mathias J.A. (1971) Energy flow and secondary production of amphipods Hyallela

azteca and Crangonyx richmondensis occidentalis in Marion Lake, BritishColumbia. J. Fish. Res. Board Can., 28, 711-726.Matuszek J.E. (1978) Empirical predictions of fish yields of large North American

lakes. Trans. Am. Fish. Soc, 107, 385-394.McLaren I.A. (1969) Population and production ecology of zooplankton in Ogac

Lake, a landlocked fiord on Baffin Island. J. Fish. Res. Board Can., 26,1485-1559.McNaught D.C. & Fenlon M.W. (1972) The effects of thermal effluents upon

secondary production. Verh. Int. Verein. Limnol., 18, 204-212.Mecom J.D. (1972) Productivity and distribution of Trichoptera larvae in a Colorado

mountain stream. Hydrobiologia, 40, 151-176.Mikulski J.S., Adanczak B., Bittel L., Bohr R., Bronisz D., Donderski W., Giziriski A.,

Luscinska M., Rejewski M., Strzelczyk E., Wolnomiejski N., Zawislak W. &Zytowicz R. (1975) Basic regularities of productive processes in the Ilawa lakes andthe Golpo Lake from the point of view of utility values of the water. Pol. Arch.Hydrobiol., 22, 101-122.Miller R.J., Mann K.H. & Scarrat D.J. (1971) Production potential of a seaweed-

lobster community in eastern Canada. J. Fish. Res. Board Can., 28, 1733-1738.Momot W.T. (1978) Annual production and production/biomass ratios of the

crayfish, Oronectes virilis, in two northern Ontario lakes. Trans. Am. Fish. Soc,107, 776-784.Monokov A.V. & Sorokin Yu.I. (1972) Some results on investigations on nutrition of

water animals. In Z.Kajak & A.Hillbricht-Ilkowska (eds.), Productivity Problemsin Freshwaters. Proceedings of the IBP-UNESCO Symposium on Productivity inFreshwaters. Krakow: Polish Scientific Publishers.Morgan N.C., Backiel T., Bretschko G., Duncan A., Hillbricht-Ilkowska A., Kajak

Z., Kitchell J.F., Larsson P., LevequeC, Nauwerck A., Schiemer F. & Thorpe J.E.(1980) Secondary production. In E.D.LeCren &R.H.Lowe-McConnell(eds.), The

Functioning ofFreshwater Ecosystems. IB P 22. Cambridge: Cambridge UniversityPress.

16 Chapter IMoskalenko B.K. (1971) The biological productivity of Lake Baykal. Hydrobiol. J.,

7(5), 1-8.Nauwerck A., Duncan A., Hillbricht-Ilkowska A. & Larsson P. (1980) Secondary

production: zooplankton. In E.D.LeCren & R.H.Lowe-McConnell (eds.), TheFunctioning ofFreshwater Ecosystems. IBP 22. Cambridge: Cambridge University

Press.Neveau A. & Lapchin L. (1979) Ecologie des principaux invertebres filtreurs de la

basse nivelle (Pyrenes-Atlantiques) 1. Simuliidae (Diptera, Nematocera). Ann.LimnoL, 14, 225-244.Neves R.J. (1979) Secondary production of epilithic fauna in a woodland stream. Am.

Midi. Nat., 102, 209-224.Nichols F.H. (1975) Dynamics and energetics of three deposit-feeding benthic

invertebrate populations in Puget Sound, Washington. Ecoi Monogr., 45, 57-82.Northrop F.S.C. (1947) The Logic of the Sciences and the Humanities. New York:

World Publishing.O'Brien F.I., Winner J.M. & Krochak D.K. (1973) Ecology of Diaptomus leptopuss.a.

Forbes 1882 (Copepoda: Calanoidea) under temporary pond conditions.Hydrobiologia, 43, 137-155.Paterson C.G. & Walker K..F. (1974) Seasonal dynamics and productivity of

Tanytarsus barbitarsis Freeman (Diptera: Chironomidae) in the benthos of ashallow, saline lake. Aust. J. mar. Freshwat. Res., 25, 151-165.Pederson G.L., Welch E.B. & Litt A.H. (1976) Plankton secondary productivity and

biomass: their relation to lake trophic status. Hydrobiologia, 50, 129-144.Pidgaiko M.L., Grin V.G., Kititsina L.A., Lenchina L.G., Polivannaya M.F., Sergeva

O.A. & Vinogradskaya T.A. (1972) Biological productivity of Kurakhov's powerstation cooling reservoir. In Z.Kajak & A.Hillbricht-Ilkowska (eds.), Productivity

Problems in Freshwaters. Proceedings of the IBP-UNESCO Symposium onProductivity in Freshwaters. Krakow: Polish Scientific Publishers.Pinel-Alloul B. (1978) Ecologie des populations de Lymnaea catascopium

(Mollusques, Gasteropodes, Pulmonees) du Lac St-Louis, pres de Montreal,Quebec. Verh. Int. Verein. LimnoL, 20, 2412-2426.Prikhod'ko T.I. (1975) A mathematical model of the production ofDaphnia longiremis

Sars in Lake Dal'neye. Hydrobiol. J., 11(4), 20-26.Priymachenko A.D., Mikhaylinko L.Y., Gusynskaya S.L. & Nebrat A.A. (1978) The

productivity of plankton associations at differing trophic levels in KremenchugReservoir. Hydrobiol. J., 14(4), 1-9.Resh V.H. (1977) Habitat and substrate influences on population and production

dynamics of a stream caddisfly, Ceraclea ancylus (Leptoceridae). Freshw. BioL, 7,261-277.Rosenberg R. (1977) Benthic macrofaunal dynamics, production and dispersion in an

oxygen-deficient estuary of west Sweden. J. Exp. Mar. BioL Ecoi, 26, 107-133.Schindler D.W. (1972) Production of phytoplankton and zooplankton in Canadian

Shield lakes. In Z.Kajak & A.Hillbricht-Ilkowska (eds.), Productivity Problems inFreshwaters. Proceedings of the IBP-UNESCO Symposium on Productivity inFreshwaters. Krakow: Polish Scientific Publishers.Selin P. & Hakkari L. (1982) The diversity, biomass and production ofzooplankton in

Lake Inarijarvi. Hydrobiologia, 86, 55-59.Short R.A. & Ward J.V. (1980) Life cycle and production ofSkwalaparallela (Frison)

Assessment of Secondary Production: The First Step 17(Plecoptera: Perlodidae) in a Colorado montane stream. Hydrobiologia, 69,

273-275.Smyly W.J.P. (1979) Population dynamics of Daphnia hyalina Leydig (Crustacea:

Cladocera) in a productive and an unproductive lake in the English Lake District.Hydrobiologia, 64, 269-278.Strayer D.L., Cole J.L., Likens G.E. & Buso D.C. (1981) Biomass and annual

production of the freshwater mussel Eliptio complanaia in an oligotrophicsoftwater lake. Freshw. Biol.. 11, 435-440.Stross R.G., Neess J.C. & Hasler A.D. (1961) Turnover time and production of

planktonic Crustacea in limed and reference portion of a bog lake. Ecology, 42,237-245.Sutclitfe D.W., Carrier T.R. & Willoughby L.G. (1981) Effects of diet, body size, age

and temperature on growth rates in the amphipod Gammaruspulex. Freshw. Biol.,11, 183-214.Swiss J.J. & Johnson M.G. (1976) Energy dynamics of two benthic crustaceans in

relation to diet. J. Fish. Res. Board Can., 33, 2544-2550.Tonolli, L. (1980) Introduction. In E.D.LeCren & R.H.Lowe-McConnell (eds.). The

Functioning ofFreshwater Ecosystems. IBP 22. Cambridge: Cambridge UniversityPress.Uye S.-I. (1982) Population dynamics and production of Acartia clausi Giesbrecht

(Copepoda: Calanoida) in inlet waters. J. Exp. Mar. Biol. Ecol., 57, 55-83.Vijverberg J. (1976) The effect of food quantity and quality on the growth, birth-rate

and longevity of Daphnia hyalina Leydig. Hydrobiologia, 51, 99-108.Vijverberg J. (1980) Effect of temperature in laboratory studies on development and

growth of Cladocera and Copepoda from Tjeukemeer, The Netherlands. Freshw.Biol., 10,317-340.Waters T.F. (1977) Secondary production in inland waters. Adv. Ecol. Res., 10,

91-164.Waters T.F. & Crawford G.W. (1973) Annual production of a stream mayfly

population: a comparison of methods. Limnol. Oceanogr., 18, 286-296.Wattiez C. (1981) Biomasse du zooplancton et productivity des cladoceres d'eaux de

degre trophique different. Ann. Limnol., 17, 219-236.Wildish D.J. & Peer D. (1981) Methods for estimating secondary production in marine

Amphipoda. Can. J. Fish. Aquat. Sci., 38, 1019-1026.Williams D.D., Mundie J.H. & Mounce D.E. (1977) Some aspects of benthic

production in a Salmonid rearing channel. J. Fish. Res. Board Can.. 34,2133-2141.Willoughby L.G. & Sutclifie D.W. (1976) Experiments on feeding and growth of the

amphipod Gammarus pulex (L.) related to its distribution in the River Duddon.Freshw. Biol., 6, 577-586.Winberg G.G. (ed.) (1971a) Methods for the Estimation of Production of Aquatic

Animals. (Translated by A.Duncan) London: Academic Press.Winberg G .G. (1971 b) Some results of studies on lake productivity in the Soviet Union

conducted as part of the International Biological Programme. Hvdrobiol. J., 7(1),1-12.Winberg G.G., Alimov A.F., Boullion V.V., Ivanova M.B., Korobtzova E.V.,

Kuzmitzkaya N.K., Nikulina V.N., Finogenova N.P. & Fursenko M.V. (1973)Biological productivity of two subarctic lakes. Freshw. Biol., 3, 177-197.

18 Chapter IWolnomiejski N., Giziriski A. & Jermolowicz M. (1976) The production of the

macrobenthos in the psammolittoral of Lake Jeziorak. Acta Univ. NicolaiCopernici Nauk. Matem.-Przyrod., 38, 17-26.Zaika V. E. (1970) Rapports entre la productivity des mollusques aquatiques et la duree

de leur vie. Cah. Biol. Mar., 11, 99-108.Zelinka M. (1977) The production of Ephemeroptera in running waters.

Hydrobiologia, 56, 121-125.Zimmerman M.L. & Wissing T.E. (1978) Effects of temperature on gut-loading and

gut-clearance times of the burrowing mayfly, Hexagenia limbata. Freshw. Biol., 8,269-277.Zndanova G.A. & Tseyev Y.Y. (1970) Biology and productivity of mass species of

Cladocera in the Kiev Reservoir. Hydrobiol. J., 6(1), 33-38.Zwick P. (1975) Critical notes on a proposed method to estimate production. Freshw.

Biol., 5, 65-70.Zytkowicz R. (1976) Production of macrobenthos in Lake Tynwald. Acta Univ.

Nicolai Copernici Nauk. Matem.-Przyrod., 38, 75-97.