RIVER RESEARCH AND APPLICATIONS

River. Res. Applic. (2009)

Published online in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/rra.1290

SECONDARY PRODUCTION AS PART OF BIOENERGETIC

THEORY—CONTRIBUTIONS FROM FRESHWATER BENTHIC SCIENCE

ARTHUR C. BENKE*
Department of Biological Sciences, Aquatic Biology Program, The University of Alabama, Tuscaloosa, AL 35487-0206, USA

ABSTRACT
Bioenergetics and energy flow studies have played a prominent role in ecology since the time of Raymond Lindeman’s classic
paper. Several early seminal studies, including Lindeman’s, were on freshwater ecosystems, all of which included benthic
secondary production as an important element. Independently of these energy flow studies, benthic ecologists have played a
major role in developing the methods of population-based secondary production, and produced the majority of all secondary
production studies in ecology. These studies have not only contributed to our understanding of the importance of animals in
ecosystem energy flow, but production is now used to address a wide variety of ecological questions from the construction of
quantitative food webs, to examining predator-prey relationships, to experimental studies of food resource use, to assessing the
effects of nonnative species, pollution and catchment land-use change. Unfortunately, appreciation of the utility of secondary
production is largely restricted to aquatic ecologists, particularly those working in freshwater and marine benthic habitats.
Further, treatment of secondary production is very limited in most general ecology texts. Continued use of secondary production
to address a diversity of ecological questions should result in a greater appreciation of its advantages and cause it to become
better known in the broader ecological community. Copyright # 2009 John Wiley & Sons, Ltd.
key words: benthic invertebrates; ecology; energy flow; marine; methods; population; secondary production; terrestrial

Received 10 October 2008; Revised 13 February 2009; Accepted 21 May 2009

INTRODUCTION
Bioenergetics theory deals with energy transformations within and among organisms, and has played a prominent
role in ecology for more than a century (for a general historical perspective see Golley, 1993; for a stream
perspective see Benke et al., 1988). A major focus of bioenergetic studies has been the flow of energy among
species via consumption along food chains. Raymond Lindeman (1942) first suggested that species could be
grouped into trophic levels and that energy was either transferred or lost as it passed from one level to another
according to ecological transfer efficiencies. Lindeman’s research on Cedar Bog Lake and his characterizations of
Lake Mendota and the Caspian Sea were just the start of several classic illustrations of energy flow in inland waters.
Prominent among subsequent freshwater studies were those on Silver Springs (Odum, 1957), Root Spring (Teal,
1957) and Bear Brook (Fisher and Likens, 1973). These studies of freshwater ecosystems have played a leading role
in our understanding of energy flow for ecology as a whole, and include some of the earliest estimates (although
crude) of benthic secondary production. Thus, benthic secondary production has been a basic component of energy
flow studies for > 60 years.
The main purpose of this paper is to illustrate how contributions from freshwater benthic secondary (animal)
production have contributed not only to bioenergetic theory, but to various other components of ecological theory as
well. This seems necessary because in spite of its historical ties to energy flow and an extensive literature, secondary
production seems largely ignored by much of the ecological community. I suggest three major reasons for this lack
of attention. First, a long-running misconception exists that secondary production is useful only for understanding
trophic level flows and efficiencies, a view perpetuated in most ecological texts. Second, because most secondary
production studies are on aquatic benthic invertebrates, they are largely ignored by those studying other habitats.

*Correspondence to: Arthur C. Benke, Department of Biological Sciences, Aquatic Biology Program, The University of Alabama, Tuscaloosa,
AL 35487-0206, USA. E-mail: abenke@as.ua.edu

Copyright # 2009 John Wiley & Sons, Ltd.

 A. C. BENKE

Third, methods of estimating secondary production are poorly known to the general ecological community, rarely
included in general ecology and population ecology texts, and often may be dismissed as too complicated or tedious
to bother with. A basic premise of this paper is that secondary production analysis is actually a relatively simple
procedure compared to many current ecological analyses, and is closely related to standard methods in population
ecology. Accordingly, secondary production should be considered an essential part of the population ecology
toolbox. Furthermore, its application, primarily through benthic studies, has now addressed many other aspects of
ecological theory outside the trophic level paradigm. Thus, contributions from benthic ecology should form the
foundation on which secondary production can be better integrated into a broader range of ecological studies in all
types of environments.

A UNIVERSAL MODEL OF ENERGY FLOW

To provide an initial appreciation of the concept of secondary production, it is helpful to first place it within the
broader context of energy flow. For decades, Eugene Odum championed the energy flow approach (McIntosh,
1985; Golley, 1993) with multiple editions of ‘Fundamentals of Ecology’ (e.g. Odum, 1971). He illustrated the
concept of energy flow with his ‘universal model’ that could be applied to any individual, population, functional
group or trophic level. A modification of this pictorial model is illustrated for a stream insect to more clearly
represent secondary production in Figure 1. The model should make it clear that secondary production is a flow (or
flux) representing the formation of biomass by growth of an individual, or collectively as a population, through
time. For the individual, food is first ingested, a fraction is lost as feces, a fraction is assimilated (or absorbed) and a
fraction of the assimilated energy forms new biomass. We generally think of production as the formation of new
biomass at the population level (somatic or reproductive) which is eventually lost as mortality (e.g. predator
consumption) or emigration (e.g. drift or emergence in the case of stream insects). All losses illustrated in Figure 1
are negative flows that subtract from population biomass, often at the same time biomass is being formed from
production. An essential step in quantifying this model, however, is estimation of production, the formation of
population biomass.

Figure 1. Energy flow model of a stream insect, emphasizing secondary production. Flows are shown with gray arrows and formation of animal
tissue (production) results in an increase of individual biomass. Population biomass is the sum of all individual biomass values for a given area
with units of g dry mass m
2 (historically, the energy units of Kcal m
2 or Kj m
2 have been used). Population production has the units of mass
flow by incorporating a time unit (e.g. g dry mass m
2 y
1). Population biomass is determined by the balance of biomass gains (growth of
individuals) and biomass losses (mortality, particularly predation, and emigration, including emergence of aquatic insects and drift). Biomass
values are typically averaged over some time period (e.g. d, wk, y)

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
DOI: 10.1002/rra
 SECONDARY PRODUCTION—CONTRIBUTIONS FROM BENTHIC SCIENCE

COMMUNITY OR POPULATION APPROACH?

Early work on secondary production treated it as a community-level energy flow that involved formation of trophic
level biomass and its transfer (consumption and assimilation) to succeeding trophic levels (Lindeman, 1942). This
view of secondary production is perpetuated in most ecology texts, both past (e.g. Odum, 1971; Ricklefs, 1973) and
present (e.g. Odum and Barrett, 2005; Begon et al., 2006). Although most texts at least mention secondary
production, its treatment is often brief and usually only within the context of energy flow and trophic-level
efficiencies. We are often left with the misconception that secondary production is somehow estimated at the
trophic-level scale, since there is rarely any indication of how this flow is actually measured. In fairness, there are
notable exceptions. Charles Krebs, in several editions of his text (e.g. Krebs, 2009), demonstrated a basic
population method as applied to an elephant population. Robert Smith, in several editions of his text (e.g. Smith,
1986; Smith and Smith, 2009), provided a reasonably extensive treatment of secondary production, although
presented no methods. Robert Ricklefs, with four editions of his shorter text ‘Economy of Nature’ (e.g. Ricklefs,
1976), provided a good discussion of trophic level efficiencies, but no methods. His 5th edition with ‘data analysis
update’ (Ricklefs, 2006), however, now provides a strong description of estimating population-level secondary
production as applied to aquatic insects. Treatments of secondary production are also commonly found in aquatic
ecology texts and handbooks (Cole, 1994; Valiela, 1995; Moss, 1998; Wetzel, 2001; Hauer and Lamberti, 2006;
Allan and Castillo, 2007; also see Wetzel and Likens, 1991). For the most part, however, secondary production has
received relatively little attention in general ecology texts, with infrequent mention of methods, and usually within
the limited context of energy flow.
In reality, secondary production is almost always estimated using population-based methods. This contrasts with
estimation of primary production, often measured at the primary producer trophic level with 14C uptake or oxygen
change methods (e.g. Benke, 1993; Bott, 2006). Population-based methods have been widely applied to aquatic
invertebrates, fishes and terrestrial animals for more than four decades. The basic method is quite simple and has
been used in all major habitat types. If a population cohort begins with age-zero animals and is followed through
time with quantitative sampling, production is easily calculated between each sampling interval as the product of
mean density (N, individuals m
2) and increase in individual mass (DM, g dry mass):

P ¼ NDM

Such calculations can be summed for a year to estimate annual production or divided by the number of days in
each time interval to obtain mean daily production. Other conceptually-related approaches exist for both cohort and
non-cohort populations (e.g. Waters, 1977; Benke, 1984, 1993; Benke and Huryn, 2006).
With this simple approach it is possible to obtain extremely detailed population-specific production estimates
that can be measured over days, weeks or years. Population estimates of multiple species can be combined to obtain
production of taxonomic or functional feeding groups, depending on the purpose of the study. I suspect the high
level of possible detail, as sometimes illustrated with hundreds of production estimates in a single paper (e.g.
Wallace et al., 1999), is far greater than ever imagined by Lindeman (1942) and other early energy-flow ecologists.
If secondary production is envisioned as a population level process, several ecological properties (variables) can
be considered to influence or contribute to it (Figure 2). As indicated above, mean density, when combined with
individual growth over some time interval (e.g. DM) provides a direct measure of production (P ¼ NDM). However,
biomass is the product of mean individual body mass and density (B ¼ M  N), and the product of biomass and
individual growth rate (g) is another simple way to estimate production (P ¼ B  g). Furthermore, individual
growth rate is roughly related to length of life (commonly called the cohort production interval, or CPI, in benthic
studies) as (g  5/CPI), length of life is roughly related to body size (CPI a M0.25) and temperature (CPI a T
1),
fecundity is influenced by body size, density is determined by fecundity and mortality, and so forth (e.g. Benke,
1993; Huryn and Benke, 2007). It should be apparent from Figure 2 that production is the most comprehensive
measure of ‘success’ for a population because it is a combination of several other variables that themselves have
been considered measures of success or fitness: density, biomass, individual growth rate, fecundity, survivorship,
body size and life span (Benke, 1993). In spite of the apparent importance of production, one might wonder why the
vast majority of ecological field experiments instead use the static properties of density or biomass as the major
response variables (see my suggested reasons above). It is interesting to note that some studies using biomass as a

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
DOI: 10.1002/rra
 A. C. BENKE

Figure 2. Ecological variables (abiotic and biotic) that influence or contribute to secondary production. Note that Production (P) is the product
of growth rate (g) and biomass (B) (i.e. P ¼ g  B), biomass is the product of mean body size (M) and density (N) (i.e. B ¼ M  N), and length of
life (cohort production interval, CPI) is influenced by temperature, body size and food quality/quantity. For discussion of these relationships, see
Benke, 1993; Huryn and Benke, 2007)

response variable suggest it as a surrogate for production, when in fact that is not necessarily the case (e.g. Grosholz
and Gallo, 2006; O’Gorman et al., 2008).

NINETY YEARS OF POPULATION-BASED SECONDARY PRODUCTION ANALYSIS

Although the first population-based method of estimating secondary production appeared about 90 years ago
(Boysen-Jensen, 1919) and the earliest subsequent work was published in the Russian literature (Winberg, 1971),
population-based methods started appearing more frequently in the English-language literature in a variety of
habitats from the 1940s through the 1960s. During this time, work was conducted on terrestrial insects (Smalley,
1960; Wiegert, 1964, 1965) and mammals (Petrides and Swank, 1966), and on freshwater fishes (Ricker, 1946;
Allen, 1949; Waters, 1977) and invertebrates (Waters, 1966; Negus, 1966). The International Biological Program
(IBP) in the 1960s spawned several handbooks on animal production for freshwater fishes (Ricker, 1968),
freshwater invertebrates (Edmondson and Winberg, 1971), marine invertebrates (Holme and McIntyre, 1971) and
terrestrial animals (Petrusewicz and Macfadyen, 1970). Thus, widespread applications of population approaches to
secondary production go back > 40 years in all major habitats.
Spurred by the IBP handbooks, secondary production studies became even more popular in the 1970s,
particularly in inland waters (see review by Waters, 1977). Given the momentum created during this time, it seems
appropriate to ask at least two major questions: (1) To what extent has this interest in animal production continued
in more recent decades and for what habitats and taxonomic groups? (2) to what extent has secondary production
expanded beyond trophic level questions of energy flow; i.e. how has it been used to address other aspects of
ecological theory?
To investigate the current state of animal secondary production work, I conducted a Web-of-Science literature
search using the key word combination ‘secondary production’. The search covered publications from
January 1998 through August 2008 (almost 11 years). Abstracts of all ‘hits’ were closely examined to ensure that
papers actually dealt with an important aspect of animal secondary production. Furthermore, each paper was
categorized by habitat (terrestrial, marine, stream/river, and lake/wetland), animal type (benthic invertebrate,
zooplankton and vertebrate) and basic versus applied research. Such a search strategy will miss some relevant
papers (e.g. book chapters or papers that did not include the term secondary production in the title, abstract or
keyword list), but it should be a reasonably accurate indicator of publication patterns.
A total of 332 animal secondary production papers were found over this time period, indicating an active area of
study (Table I). For perspective, approximately twice as many basic research papers have been published on animal
production as on life tables (non-human) during the last 4 years. Life table analysis, of course, has been described in

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
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 SECONDARY PRODUCTION—CONTRIBUTIONS FROM BENTHIC SCIENCE

Table I. Distribution of secondary production papers (N ¼ 332) among habitats/animal groups and applied/basic, January 1998
though August 2008 from Web of Science. Some papers included in more than one category (e.g. benthic and zooplankton)

No. of papers Percentage

Terrestrial invertebrates 3 0.9

Terrestrial vertebrates 1 0.3
Marine zooplankton 47 14.2
Freshwater zooplankton 12 3.6
Marine vertebrates 9 2.7
Freshwater vertebrates 10 3.0
Marine benthic invertebrates 118 35.5
Stream/river benthic invertebrates 111 33.4
Lake/wetland benthic invertebrates 30 9.0
Applied research 32 9.6
Basic research 300 90.4
Total terrestrial studies 4 1.2
Total marine studies 172 51.8
Total freshwater studies 154 46.4

detail in most general and population ecology texts of the last half century and is frequently seen in General Biology
texts. It is clearly evident from Table I that the great majority (> 98%) of secondary production studies over the past
decade has occurred in aquatic environments. I suspect this pattern has been the same for at least 3 decades.
Although there have been some excellent terrestrial production studies since the early 1970s, such as on snails (e.g.
Staikou et al., 1988; Staikou and Lazaridoudimitriadou, 1990) and grasshoppers (e.g. Duke and Crossley, 1975;
Meyer et al., 2002), secondary production studies have never really taken hold in terrestrial ecology. It is also
apparent that the majority (almost 80%) of aquatic studies focused on benthic invertebrates, 54% in freshwater
(principally in streams and rivers) and 46% in marine. Considering all animal types, there were slightly more
marine than freshwater studies because of a greater emphasis on marine than freshwater zooplankton production. It
was surprising that so few studies (19) have been done on aquatic vertebrates (mostly fishes) in the past decade,
which may represent a decline from the 1970s (Waters, 1977). Interesting, however, is that more work is now being
done on amphibians (e.g. Regester et al., 2008). The major conclusion from this almost 11-year assessment of the
literature is that freshwater and marine benthic scientists have been the leaders in field studies of secondary
production and this has probably been the case for several decades. The paucity of work on vertebrates in any
environment, on terrestrial invertebrates and on freshwater zooplankton is noteworthy.
This brings me to my second major question: to what extent has secondary production expanded beyond trophic
level questions and been used to address other aspects of ecological theory? If secondary production analysis has
remained useful only for trophic level studies, its application is clearly somewhat limited. To investigate this
question, Alex Huryn and I (Benke and Huryn, in press) reviewed applications of freshwater secondary production
over the past 3 decades, and documented its use in addressing a wide variety of ecological questions of which
energy flow studies represent a small fraction. Several of these categories represent other facets of ecological theory
and others are applied areas of research. In most applications, there is either a relatively extensive or a growing
literature. I briefly list eight of these categories:
 Niche overlap and competition
 Effects of pollution
 Effects of catchment land use change
 Chemical flows and stoichiometry
 Predator–prey relationships
 Experimental studies of food resource use
 Quantitative food webs
 Effects of nonnative species.

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
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 A. C. BENKE

For illustration, I will briefly discuss the last two applications and follow that with some additional illustrations of
how production analyses are either essential or superior to density or biomass in addressing several ecological
questions. Benke and Wallace (1997) combined secondary production analysis with gut-content analyses to build a
detailed quantitative food web for snag (wood) dwelling caddisflies in the Ogeechee River, Georgia (Figure 3).
Among other things, we demonstrated that ingestion flows between individual taxa (rather than between trophic
levels) varied by four orders of magnitude and showed how a simple connectivity web using tropho-species can be
very misleading. Other investigators have used this approach to address how quantitative food web flows can be
altered when food resources are reduced (Hall et al., 2000), when streams are nutrient-enriched (Cross et al., 2007),
and when multi-site comparison are made along a river continuum (Rosi-Marshall and Wallace, 2002). Several
other examples of quantitative food webs are found in Benke and Huryn (in press); Woodward et al. (2005) have
compared this with other approaches to food web theory.
Anderson and Rosemond (2007) used secondary production to illustrate the effect of nonnative beavers on
stream function in a Chilean stream. Although diversity was only half that in ponds created by beaver
dams compared to forested streams, ecosystem function as reflected by secondary production was increased
by 3–5 times. Other studies have also considered the influence of nonnative species on stream ecosystem function
using secondary production analysis. Huryn (1998) used production analyses to demonstrate the long-term
influence of a native stream salmonid compared to a nonnative salmonid in a New Zealand stream, and Hall et al.
(2006) demonstrated how a nonnative snail can totally dominate secondary production and nitrogen cycling in a
western US stream.
A valid question is whether density and biomass (which are easier to measure) would have served just as well as
secondary production in addressing the ecological questions listed above. One might argue that anytime one uses
production instead of numbers, biomass or richness as a response variable, one is measuring a functional rather than
a structural variable and is valuable from that standpoint alone. Furthermore, in many cases the production response
might be different than, say, the biomass response. For example, Bruce Wallace and colleagues (Lugthart et al.,
1990; Lugthart and Wallace, 1992; Chung et al., 1993; Whiles and Wallace, 1995) examined effects of the pesticide

Figure 3. Quantitative food web for the major caddisfly taxa on the snag habitat, Ogeechee River. Line thickness indicates magnitude of
ingestion fluxes (flows). Actual ingestion values are presented in Table 4 of Benke and Wallace (1997). Abbreviations: Ephemer-
op. ¼ Ephemeroptera, Lepto. ¼ Leptoceridae, Limneph. ¼ Limnephilidae. Figure from Benke and Wallace (1997), with permission

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
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 SECONDARY PRODUCTION—CONTRIBUTIONS FROM BENTHIC SCIENCE

methoxychlor on species and functional-group production and found this gave a more complete picture of
disturbance and recovery than abundance or diversity. But there are several topics that cannot even be addressed
with only density or biomass, such as in the quantification of food webs as described above. Similarly,
quantification of the role of animals in ecosystem chemical flows through use of production (e.g. Hall et al., 2003;
Cross et al., 2007) is not possible with biomass data alone. An important contribution to predator-prey theory is the
observation from several stream studies that predators typically consume > 80% of prey production, information
that cannot be shown from numbers or biomass and is typically ignored in the interpretation of most predator-prey
experiments (e.g. Wallace et al., 1997; Benke and Huryn, in press). These are just a few of the many examples
demonstrating the benefit and often the necessity of using production in addressing various aspects of general
ecological theory (Benke and Huryn, in press).
Broader recognition of the utility of secondary production analysis seems needed among ecologists. Although
primarily used in benthic studies, many untapped opportunities to apply production techniques in other
environments exist. As secondary production is repeatedly shown to be useful in all environments, it should catch
the attention of more textbook authors. The basic methods are easy to explain and understand, such as with the
simple equation presented above. They can be described as an extension of life tables (Krebs, 2009) or as part of
energy flow analysis (Ricklefs, 2006, data analysis update). Benthic ecologists have led the way in providing many
applications of secondary production in addressing ecological theory.

CONCLUSIONS
Benthic secondary production has been a part of energy flow studies since Lindeman (1942), and the majority of
seminal papers on energy flow originate from freshwater environments. It may therefore be no surprise that both
freshwater and marine benthic ecologists have been the leaders in secondary production analysis. Today many more
stand-alone production studies are being conducted than complete energy flow studies and applications have
expanded to a far wider range of questions addressing other facets of ecological theory. Unfortunately, this
approach is greatly under-utilized in non-benthic habitats, and not widely recognized in the non-benthic literature
or in ecology texts. Continued leadership by benthic ecologists in this area will hopefully cause secondary
production to be rediscovered by terrestrial and pelagic scientists and be recognized as an appropriate response
variable for many ecological questions. Methods and applications of secondary production will (or should)
eventually become a common topic in ecology texts.

ACKNOWLEDGEMENTS

This paper is based on a presentation in a special session on contributions of benthic science to general ecological
theory at the 2008 meeting of the North American Benthological Society. I thank the organizers, Sandy Milner and
Klement Tockner, for the invitation to participate and to prepare this paper. Thanks also to Alex Huryn for review of
an early draft of this manuscript, and to Sandy Milner, Matt Whiles, and two anonymous reviewers whose
suggestions improved the final version.

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Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. (2009)
DOI: 10.1002/rra