MIYADI AWARD

Hideyuki Doi

Resource productivity and availability impacts for food-chain length

Received: 24 February 2011 / Accepted: 6 March 2012 / Published online: 29 March 2012� The Ecological Society of Japan 2012

Abstract Ecologists have focused on food-chain length(FCL) for the past eight decades as an index of food-webstructure. Here, I review the hypotheses determining FCLwith a focus on resource productivity and availabilityeffects on FCL. First, I introduce the mainstreamhypotheses to explain FCL variations: productivity, eco-system size, anddisturbance. For the existing productivityand productive space hypotheses, I stress the importanceof using resource availability to estimate the productivityeffect on FCL. Using a FCL dataset from 15 ponds, Itested the resource stoichiometry effect on FCL for pondswith between carbon:nitrogen ratio of primary producersand FCL. Moreover, I provide a perspective for studyingresource availability and stoichiometry effects on FCLand of the alternative hypotheses of productive-space andecosystem size. Finally, I suggest the future directions ofthe FCL study: a resource subsidy and climate changeeffects on FCL and food-web structure.

Keywords Food web Æ Primary production Æ Ecosystemsize Æ Subsidy Æ Ecological stoichiometry

Introduction

Food web is a central theme of ecology and has beenwell studied for the past decades (Pimm 1982; Polis et al.

1997; Post 2002). Food webs represent the complextrophic interactions in an ecosystem (Pimm 1982), andinfluence population dynamics, community structure,and ecosystem function (Pimm 1982; Polis et al. 1997).Food chain is a caricature of community that traceslinear trophic pathway from primary producer to toppredator within a complex food web, and food-chainlength (FCL) is defined as the maximum length of foodchains in ecosystem (Elton 1927; Pimm 1982). FCL is acrucial food-web characteristic that influences commu-nity structure, species diversity, and population stabilityby altering the organization of trophic interactions (e.g.,Elton 1927; Pimm 1982; Post et al. 2000; Post 2002).

FCL varies from 3 to 6 (Pimm 1982), and explainingvariation in FCL is a central theme of ecology in the pasteight decades. Elton (1927) speculated that energyavailability ultimately limits the trophic pyramid ofnumbers in ecosystems. His book is the starting point ofthe FCL study, and in the later years, productivityhypothesis of FCL was theoretically established(Hutchinson 1959; Slobodkin 1961). Other factors, suchas ecosystem size and disturbance, have also been pro-posed and tested as determinants of FCL (Power et al.1996; Takimoto et al. 2008; Walters and Post 2008;McHugh et al. 2010; Sabo et al. 2010). Historically,food-chain length has derived from various methods, forexample; connectance web by observations of theinteractions, and energy web to employ a stable isotopetechnique that integrates the assimilation of energy ormass flow through all the trophic pathways leading totop predators (Post 2002). The recent FCL studiesmainly used stable isotope to estimate FCL by maxi-mum trophic position of the top-predator species in thesystem.

Although there is long history of the FCL study afterElton (1927), the hypotheses, including productivity,ecosystem size, productive-space and disturbancehypothesis, are still being debated, because relativeimportance of the mechanisms proposed by thehypotheses to determine FCL has remained unknown. Inthis paper, I firstly review existing hypotheses explaining

Hideyuki Doi is the recipient of the 15th Denzaburo MiyadiAward.

H. DoiInstitute for Chemistry and Biology of the Marine Environment,Carl-von-Ossietzky University Oldenburg, Schleusenstrasse 1,26382 Wilhelmshaven, Germany

H. Doi (&)Institute for Sustainable Sciences and Development, 701-3,ASoM, Hiroshima University, 1-3-1 Kagamiyama,Higashihiroshima 739-8530, JapanE-mail: doih@hiroshima-u.ac.jpTel.: +81-82-4245732Fax: +81-82-4245732

Ecol Res (2012) 27: 521–527DOI 10.1007/s11284-012-0941-9

variations in FCL with related to productivity, ecosystemsize, and disturbance. Using FCL data in the pond (Doiet al. 2009), I then tested resource availability (i.e.,nutrient stoichiometry) effects on FCL. Based on recentevidence, I provide a perspective for studying produc-tivity and resource availability effects on FCL and anintegrated framework to consider productive-space andecosystem size hypotheses along an ecosystem size gra-dient. Finally, I suggest future directions for research onresource subsidy and climate change effects on FCL.

Existing hypotheses for FCL

Numerous hypotheses have been proposed and widelycited. Recently, three mainstream hypotheses regardingproductivity, ecosystem size, and disturbance (Fig. 1)have been examined empirically (Power et al. 1996;Vander Zanden et al. 1999; Post et al. 2000; Thompsonand Townsend 2005; Post 2007; Vander Zanden andFetzer 2007; Takimoto et al. 2008; Walters and Post2008; Doi et al. 2009; McHugh et al. 2010; Sabo et al.2010).

Productivity hypothesis

This hypothesis predicts that greater productivity (i.e.,per-unit-size resource availability) of an ecosystemlengthens FCL (Slobodkin 1961; Pimm 1982). This isbecause, due to limited efficiency in energy transferacross trophic steps, available energy diminishes athigher trophic levels, and through several trophic stepsthere remains insufficient energy to support higher tro-phic levels.

Ecosystem size hypothesis

This hypothesis predicts that FCL increases withincreasing ecosystem size, such as lake volume and

island area (Cohen and Newman 1992; Post et al. 2000;Takimoto et al. 2008). There are multiple (not mutuallyexclusive) mechanisms underlying this hypothesis,including species–area relationships (Cohen and New-man 1992), meta-population dynamics (Holt 1996), andstabilization of predator–prey interactions (Spencer andWarren 1996; Holt 2002).

Productive-space hypothesis

This hypothesis is a combination of the productivity andecosystem size hypotheses. This argues that total eco-system productivity (per-unit-size productivity · eco-system size) reflects the capability of the ecosystem tosupport higher trophic levels (Schoener 1989). Per-unit-size productivity is often expressed as carbon productionper unit space per unit time. Animals may forage over awider area in low productivity habitats to meet theirenergy requirements (Pimm 1982). Unlike the produc-tivity hypothesis, the productive-space hypothesisexplicitly includes a spatial component to accuratelyestimate the total resource availability for higher trophiclevels. This hypothesis postulates that per-unit-sizeproductivity and ecosystem size should have comple-mentary effects on FCL (Schoener 1989; Fig. 1) becauselog (per-unit-size productivity · ecosystem size) is equalto the sum of log (per-unit-size productivity) and log(ecosystem size).

Disturbance hypothesis

The dynamic stability hypothesis argues that the localstability of dynamics controls FCL because longer foodchains are potentially unstable (Pimm and Lawton 1977;Jenkins et al. 1992). In the dynamic constraintshypothesis, more frequent or more intense disturbancein ecosystems would shorten FCL, because simple the-oretical models suggest that longer chains are less resil-ient, and thus unlikely to persist in disturbed habitats

(a) Productivity

Foo

d-ch

ain

leng

th

(b) Ecosystem size (c) Productive-space

Ecosy

stem

size

Productivity(or resource availability)

Fig. 1 Conceptual illustrations of relationships among food-chain length (FCL), productivity (or resource availability), and ecosystemsize (log-transformed values) based on the three mainstream hypotheses

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(Pimm and Lawton 1977, but see Sterner et al. 1997 forthe theoretical absence of the evidence). This hypothesiswas supported in some streams (Power et al. 1996;Thompson and Townsend 2005; McHugh et al. 2010),but not the experimental streams (Walters and Post2008) and in island (Takimoto et al. 2008).

Productivity hypothesis for FCL

Productivity is often expressed as primary production byautotrophs in an ecosystem and represents the potentialenergy available to higher trophic levels. It is well ac-cepted that energy availability plays an important role inecological systems, as Lawton (1999) suggested that thisis one of the general patterns in ecology. For the lastdecades, many studies have been conducted to under-stand how productivity influences ecosystems and howecosystem properties, such as food-web structure andbiodiversity, influence productivity (e.g., Tilman 1996;Hillebrand and Matthiesen 2009).

Some previous studies with smaller ecosystem sizeand in the laboratory experiments have supported theproductivity hypothesis (e.g., Jenkins et al. 1992;Kaunzinger and Morin 1998). For example, Thompsonand Townsend (2005) showed that the carbon produc-tivity of benthic algae predicts the FCL of streams.However, in natural ecosystems, the hypothesis is notgenerally supported. Recently, Sabo et al. (2009) re-viewed >30 papers in freshwater systems and summa-rized that approximately one-third of the reviewedstudies supported the productivity hypothesis. Post(2002) reported in his review that ecosystem size is animportant factor to determine FCLs in lake ecosystems.However, in smaller ecosystems, productivity would stillbe one of the most important determinants of FCL infreshwater systems. To my knowledge, there is no evi-dence for the productivity hypothesis in terrestrial eco-systems, as most FCL studies have been done infreshwater ecosystems (see arguments of Takimoto et al.2008; Sabo et al. 2009). Further study is needed to testthe productivity hypotheses in terrestrial systems.

Effects of resource availability and stoichiometry on FCL

The previous studies of FCL have focused on totalproductivity (e.g., carbon production rate, total phos-phorus, and Secchi transparency) (Vander Zanden et al.1999; Post et al. 2000; Thompson and Townsend 2005;McHugh et al. 2010), and impacts of resource avail-ability on FCL remain largely unexamined. Originally,the productivity and productive-space hypotheses pre-dict that ‘‘resource availability’’ limits FCL. Recently,Sabo et al. (2009) suggested that we should call ‘‘re-source-availability’’ hypothesis instead of productivityor productive-space hypothesis. The resource availabil-ity is not only determined by total production as well asedibility and resource stoichiometric balance. Doi et al.

(2009) conducted to test three of the mainstreamhypotheses (Fig. 1) by considering resource availabilityin terms of edibility of algal species in 15 ponds. Thestudy used nitrogen stable isotopes to measure FCL.The results showed that FCL was not correlated withalgal biomass (Chlorophyll), Secchi depth, and totalphosphorous of the pond water as primary productionindices to determine FCL of ponds. However, bothedible carbon concentration (as an index of resourceavailability) and ecosystem size are positively correlatedwith FCL (Fig. 2, there is not significant collinearlybetween edible carbon and ecosystem size). The resultsof Doi et al. (2009) provide a new measurement to testproductivity and productive-space hypothesis using re-source edibility.

Productivity and productive-space hypotheses assumelimited energy transfer efficiency from primary producersto top-predator species in an ecosystem. Importantly,energy transfer efficiency is largely determined by stoi-chiometric match/mismatching between prey (or re-source) and predator (or consumer) (Sterner and Elser2002). Numerous studies have suggested that carbon (C):nitrogen (N): phosphorous (P) ratio of primary produc-ers influence resource-use efficiency, population size, andgrowth rate of consumer species in food webs (Sternerand Elser 2002; Urabe et al. 2002; Doi et al. 2010).Therefore, it has been hypothesized that food-chainefficiency (FCE) (defined as energy transfer efficiencyacross multiple trophic levels) is constrained by the effi-ciency at which herbivores use plant energy and thatFCE depends on plant nutritional quality. Recently,using field experiment manipulating light intensity,nutrient availability, and presence or absence of highertrophic levels, Dickman et al. (2008) showed that FCE isconstrained by C:N:P stoichiometry of primary produc-ers and resource-use efficiencies of consumer and pred-ator species are higher when the food web has longer

Fig. 2 Three-dimensional plot between food-chain length (FCL),resource availability (edible carbon concentration), and ecosystemsize (pond volume). The graph is from Doi et al. (2009)

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FCL than that with shorter FCL. Their results suggestedthat FCE is strongly constrained by stoichiometry ofprimary producer and FCL. In the study, they suggesteddecreasing of FCL increased FCE of the system, indi-cating that the food web with longer FCL have limitedFCE even if the same resource availability and stoichi-ometry. The experiment is short period, but when longerFCL limited FCE in the field, longer FCL can be pre-dicted to be consequently shortened energy and materialsfor the top-predator species. Thus, I suggest that C:N:Pstoichiometry of primary producers would limit FCL, ifresource availability is also important to determine FCL(i.e., ‘‘stoichiometry hypothesis’’).

Using the data of Doi et al. (2009) and Doi et al.(2011), I test how FCL of the ponds are related to C:Nratio of seston (consisting mainly of phytoplankton,primary producer). FCL and seston C:N ratio were notsignificantly correlated (Fig. 3), indicating the C:Nstoichiometry of primary production did not signifi-cantly determine FCL in the ponds, despite the observedeffects of edible carbon in Fig. 2.

In aquatic ecosystems, P is more limited than C and Nin the food webs (Sterner and Elser 2002), thus P transferin the food web is more important to determine FCL.However, other stoichiometric indices, for example, C:PandN:P ratios, have not been tested here. Further studiesneed to test the ‘‘stoichiometry hypothesis’’ of FCL toconsider resource availability effect on FCL.

The framework for productive-space and ecosystem sizehypotheses

Strong evidence for the productivity and productive-space hypothesis is currently available only from small

ecosystems (streams, ponds, and microcosms) (Jenkinset al. 1992; Kaunzinger and Morin 1998; Thompson andTownsend 2005; Doi et al. 2009), although weak evi-dence comes from various sizes of aquatic ecosystems(e.g., stream, ponds, wetland) (Sabo et al. 2009). Doiet al. (2009) supported the productive-space hypothesisin ponds, while microcosm experiments strongly sup-ported the productivity hypothesis (Jenkins et al. 1992;Kaunzinger and Morin 1998). In contrast, Post et al.(2000) rejected the productive-space hypothesis for thedataset of large lakes including the Great Lakes. If theproductivity and productive-space hypotheses are cor-rect only in small ecosystems, the productive-space andecosystem size hypotheses might be alternatives whenconsidering FCL along a wide range of ecosystem size.Indeed, for larger ecosystems, productivity may not beimportant to determine FCL, because large ecosystemscan have high total productivity even if the per-unit-sizeproductivity is very low.

Here, I provide a perspective by integrating the pro-ductive-space and ecosystem size hypotheses (Fig. 4). Isuggest that the threshold of ecosystem size may dis-criminate the hypotheses and that the productive-spacehypothesis changes to the ecosystem size hypothesisabove the threshold (arrow on y-axis in Fig. 4). Scho-ener (1989) suggested that the productive-spacehypothesis relies on individual behaviors within re-source-limited food webs and the ecosystem size re-quired to support a single individual of a particularspecies depends on the per-unit-size resource availabil-ity. Thus, the ecosystem-size threshold discriminatingthe productive-space and ecosystem size hypothesesmight be related to individual performance of top-predator species in a food web (e.g., minimum habitatsize to harbor the population of top-predator species inponds, Doi et al. 2009; hunting and migration rangeof top-predator). Finding what ecosystem size is the

Fig. 4 Conceptual illustration for productive-space and ecosystemsize hypotheses along with productivity (or resource availability)and ecosystem size. The arrow on the y-axis indicates the ecosystemsize threshold for discriminating the hypotheses

5 10 15 20

3.5

4.0

4.5

5.0

C:N ratio of seston

FC

L

Fig. 3 Relationship between food-chain length (FCL, mean chainlengths) and atomic C:N ratio of seston (mainly phytoplankton)from Doi et al. (2009, 2011). The correlation is not significant(p = 0.16, r = 0.17, n = 15, Pearson’s correlation coefficient)

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threshold of the alternative hypotheses would be a fu-ture theme of food-web ecology and can connect theproductive-space and ecosystem size hypotheses of FCL.

Future directions

Here, I provide some new ideas for the FCL hypotheses;the resource availability effect, stoichiometry effect, andintegrated framework of productive-space and ecosys-tem size. Further study is needed to test these hypothesesin both aquatic and terrestrial systems. For futuredirections of the FCL study, I provide two additionalimportant themes.

Resource subsidy effect on FCL

To consider productivity or resource availability effectson FCL, the previous studies have ignored ‘‘subsidy’’into ecosystems. Subsidy of resources into ecosystemsdetermines food-web and community structures (e.g.,Polis et al. 1997; Nakano and Murakami 2001; Doi et al.2008). If the per-unit-size productivity or total resourceavailability determine FCL, then the amount of subsidyinto the food web would also be important as an addi-tional force to lengthen FCL. However, resource subsidyeffect on FCL was not considered to test productivityhypothesis. As I suggested above, FCL in small eco-systems are closely related to productivity, thus subsidyeffects on FCL would be higher in smaller ecosystemsthan in larger ecosystems. It should also be noted thatthe relative impact of subsidy would increase withdecreasing ecosystem size due to increasing the bound-ary: ecosystem size ratio (Doi 2009). In addition, theadaptive foraging of top predator shapes FCL (Kondohand Ninomiya 2009), and adaptive foraging for subsi-dized resources have been observed in top-predatorspecies (e.g., Nakano and Murakami 2001). Thus,adaptive foraging between local and subsidized re-sources would also shape FCL. Testing the hypothesiswould improve our understanding of FCL. Post et al.(2007) suggested that we should consider the boundaryof ecosystems to test FCL hypotheses. In mountain-stream ecosystems, which gain higher resource subsidyfrom forest, the ecosystem size of the stream should beconsider as watershed area or other indices rather thanstream width. Thus, to test resource subsidy effect onFCL, we should consider the ecosystem size as well totest ecosystem size and productive-space hypotheses.

Some effects should be considered to estimate theeffect of subsidy on FCL; (1) Connectedness to the do-nor system and the ecosystem types would influence theamount of subsidy (e.g., Marczak et al. 2007), andwould consequently influence FCL. To test the subsidyeffect on FCL, connectedness should be considered withthe other factors such as ecosystem size. (2) Amountof subsidy is influenced by ecosystem size, namely,

increasing of lake ecosystem size would decrease amountof subsidy (Doi 2009). Thus, ecosystem size would berelated with subsidy effect on FCL. To fully consider thesubsidy effect on FCL, ecosystem size should be con-sidered to estimate, since the ecosystem boundaryshould be defined by the area where provide the subsidy.

Climate change effect on FCL

The Intergovernmental Panel on Climate Change (2007)reported that global air and water temperature areincreasing, and in the future global warming would beaccelerated with increasing greenhouse gas. Here, Ipredicted the three main effects on FCL induced byglobal climate change; changing of primary production,disturbance by extreme weather, and species extinction.

Increasing temperature would affect productivity ofecosystems (IPCC 2007; Boyce et al. 2010; Brown et al.2010). In terrestrial ecosystems, the primary productionwould be increased by global warming (e.g., Melilloet al. 1993; IPCC 2007). The increase of primary pro-ductivity in terrestrial would increase FCL, if the FCL inthe terrestrial ecosystem is determined by productivityor productive-space hypothesis (but the testing is verylimited, as noted in the Introduction). In aquatic eco-systems, however, primary productivity has decreased inthe past decades and temperature warming would halveproductivity in some lakes and areas of ocean (e.g.,O’Reilly et al. 2003; Boyce et al. 2010), although theproductivity has increased due to nutrient loading fromwatershed and atmosphere in the lakes (e.g., Wetzel2001; Elser et al. 2009). Such reductions in productivitywould shorten FCL, if the FCL in the systems is deter-mined by productivity or productive-space hypothesis.

IPCC (2007) also predicted that extreme weather suchas storms and drought would increase due to the globalclimate change. From the disturbance hypothesis onFCL, the increase of disturbance by such extremeweather would influence FCL. The disturbancehypothesis is mainly supported in stream ecosystems(e.g., McHugh et al. 2010; Sabo et al. 2010), and streamflow would be changed by changes in precipitation dueto climate change (Milly et al. 2005). Therefore, I predictthat the climate change effect on FCL throughoutincreasing of disturbance would be mainly shown instream ecosystems.

IPCC (2007) also suggested that about 30 % ofknown species worldwide will be threatened with only a2 �C increase in air temperature. Resulting immigration/extinction of top-predator species and changes in com-munity structure would influence the whole food-webstructure and FCL. The extinction of top-predatorwould shorten FCL, but immigration of top-predatorfrom other habitat would enhance FCL. Also, theextinctions of the consumers with middle trophic posi-tions would alter FCL. The species extinction andmigration have the alternative effects to enhance/shorten

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FCL. A decrease of species is predicted by the modeling,but did not appear in the field with the current climatecondition. The immigration/extinction of species andalteration of community structure would change FCLbut the effect on FCL is still largely unknown.

Some experiments have suggested climate effects on apart of the food-web structure (but not on FCL) (e.g.,Kishi et al. 2005; Barton et al. 2009; Barton and Schmitz2009; Brown et al. 2010). Moreover, other climate im-pacts, such as changes in the amount and phenology ofprecipitation, would also change FCL by changingecosystem size (especially in aquatic systems) and dis-turbance level (Sabo et al. 2009). Because climate changeis ongoing and would drastically influence ecosystems inthe near future, direct testing of climate effects on FCLis urgently needed.

Conclusions

In this review, I reviewed the FCL hypotheses withconsidering resource availability and productivity andan integrated framework to connect the hypotheses ofproductive-space and ecosystem size. Furthermore, Iprovide a new idea for future studies; subsidy and cli-mate change affects FCL. Such frontier area for food-web ecology is still remaining. FCL study in terrestrialsystems is limited compared to that in aquatic systems(Takimoto et al. 2008). Recently, some studies estimatedFCL in terrestrial systems (Arim et al. 2007a, b;Takimoto et al. 2008; Ayal and Groner 2009), but weshould consider the similarity and differences in FCLtheories in aquatic and terrestrial systems. Food-webecology will develop for the applied ecology to considerclimate change effect on ecosystems and also for thegeneral ecology to understand population, community,and ecosystem dynamics.

Acknowledgments This paper is based on the awarded lecture forthe 14th Denzaburo Miyadi Award at the 58th Annual Meeting ofthe Ecological Society of Japan, March 18, 2010. I appreciate theassistance of all advisors and colleagues for my previous studies. Iwant to especially mention my supervisor and advisors; HelmutHillebrand, Eisuke Kikuchi, Shin-ichi Nakano, Daniel E. Schin-dler, and Yasuhiro Takemon. I thank Helmut Hillebrand andTakafumi Nakazawa, and Gaku Takimoto for their comments onan early version of the manuscript. The study supported by theJapan Society for the Promotion of Science Postdoctoral Fellow-ship for Research Abroad.

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