Successional status and root foraging forphosphorus in seven tropical tree species

Brent C. Blair and Ivette Perfecto

Abstract: In this study, the impact of localized nutrient patches on above- and belowground growth of tropical treeswas examined. Seedlings of seven tree species (Albizia guachapele Kunth (Dugand), Cedrela odorata L., Ceibapentandra (L.) Gaertn., Cordia alliodora (Ruiz & Pavón) Oken, Dalbergia retusa Hemsl., Gliricidia sepium (Jacq.)Kunth ex Walp., and Swietenia macrophylla King) of varying successional status were used in a greenhouse containerexperiment. Treatments of homogeneous and heterogeneous P fertilization were used to determine each species’ abilityto forage morphologically for P. In each pot, root length density, average root diameter, and root length to shoot ratiowere measured. It was hypothesized that early successional species would be most effective at taking advantage of theheterogeneous soil environment. This prediction was based on studies showing a high degree of soil heterogeneity inearly successional forest environments and the need for plants to take advantage of this variability. The study foundgreat variability in the foraging capacity between species, but the hypothesis that successional status and root foragingability are related was not supported in the species tested. Overall, five of the seven species examined showed some in-dication that they were taking advantage of local nutrient patches. In four of these species, increased root length den-sity was detected in P patches (A. guachapele, C. odorata, G. sepium, and S. macrophylla) and one species haddecreased root width in the P patches (G. sepium). When comparisons were made between homogeneously and hetero-geneously fertilized pots, G. sepium and C. alliodora appeared to take advantage of the heterogeneous resource. Bothof these species increased aboveground growth in the heterogeneous pots and C. alliodora also had a decreased root toshoot ratio.

Résumé : Dans le cadre de cette étude, l’impact de zones localizées de nutriments sur la croissance hypogée et épigéed’arbres tropicaux a été examiné. Les semis de sept espèces d’arbres (Albizia guachapele Kunth (Dugand), Cedrelaodorata L., Ceiba pentandra (L.) Gaertn., Cordia alliodora (Ruiz & Pavón) Oken, Dalbergia retusa Hemsl., Gliricidiasepium (Jacq.) Kunth ex Walp. et Swietenia macrophylla King) associées à différents stades de succession végétale ontété utilizés pour une expérience en contenants réalisée en serre. Des traitements homogènes et hétérogènes de fertiliza-tion au P ont été utilizés pour déterminer la capacité de chaque espèce à fourrager morphologiquement dans le sol pouraccéder au P. Dans chaque pot, la densité linéaire des racines, le diamètre moyen des racines et le rapport de la lon-gueur des racines sur la longueur de la tige ont été mesurés. Nous avons posé comme hypothèse que les espèces pion-nières seraient les plus efficaces à tirer profit d’un sol hétérogène. Cette prédiction était basée sur des études montrantun haut degré d’hétérogénéité du sol en début de succession dans les environnements forestiers et la nécessité pour lesplantes de tirer profit de cette variabilité. L’étude a montré une grande variation parmi les espèces dans leur capacité àfourrager dans le sol mais l’hypothèse voulant que le statut d’une espèce dans la succession végétale et sa capacité ra-cinaire à fourrager soient reliées n’a pas été confirmée chez les espèces testées. Dans l’ensemble, cinq des sept espècesexaminées ont montré des indices qu’elles tiraient profit des zones localizées de nutriments. Chez quatre de ces espèces(A. guachapele, C. odorata, G. sepium et S. macrophylla), une augmentation de la densité linéaire des racines a été dé-tectée dans les zones du sol riches en P et une espèce (G. sepium) a subi une diminution du diamètre des racines dansles zones riches en P. Lorsque des comparaisons ont été faites entre les pots fertilizés de façon homogène et les potsfertilizés de façon hétérogène, G. sepium et C. alliodora semblaient tirer profit des ressources hétérogènes. Les deuxespèces ont augmenté leur croissance épigée dans les traitements hétérogènes et C. alliodora a vu son rapportracine:tige diminuer.

[Traduit par la Rédaction] Blair and Perfecto 1135

Can. J. For. Res. 34: 1128–1135 (2004) doi: 10.1139/X04-004 © 2004 NRC Canada

1128

Received 4 September 2003. Accepted 15 December 2003. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on25 May 2004.

B.C. Blair1,2 and I. Perfecto. School of Natural Resources and Environment, University of Michigan, 430 East University, AnnArbor, MI 48105, USA.

1Corresponding author (e-mail: bblair@ucsc.edu).2Present address: Environmental Studies Department, University of California at Santa Cruz, Interdisciplinary Sciences Building,1156 High Street, Santa Cruz, CA 95064, USA.

Introduction

It is widely known that soil nutrients are heterogeneouslydistributed in soil at scales relevant to individual plants(Lechowicz and Bell 1991; Gross et al. 1995; Cain et al.1999; Farley and Fitter 1999). However, it is not generallyunderstood how this characteristic influences plant growthand competition. While it is recognized that roots can re-spond to spatial and temporal patches of nutrients and water,all plants do not share the same capabilities (Campbell et al.1991; Robinson 1994; Finér et al. 1997; Einsmann et al.1999).

Both morphological and physiological methods of forag-ing for edaphic resources exist (review in Robinson 1994).In this study, morphological mechanisms of foraging are em-phasized where changes in the rate and form of root growthallow a plant to take advantage of localized increases innutrient availability. Plants use three methods to morpholog-ically forage for nutrients in nutrient-rich patches: (i) in-creasing rooting density, (ii) increasing the proportion offine roots, and (iii) increasing the rate of fine root turnover.

Root foraging studies are often limited to the common ob-servation of roots growing prolifically into areas of high nu-trient concentration and relatively little into areas that arenutrient poor. This type of foraging is well documented(e.g., Pregitzer et al. 1993; Cain 1994; Einsmann et al. 1999;Wijesinghe et al. 2001), yet it is not universal and someplants show little morphological change in response to in-creased nutrient availability (Jackson and Caldwell 1992;Robinson 1994).

Root width is important because it is believed that youngfine roots are most effective at nutrient absorption and areresponsible for the bulk of nutrient uptake (Nye and Tinker1977; Caldwell and Richards 1983). This characteristic al-lows a second foraging tactic to take place, when plants in-crease the proportion of fine roots grown into an area in thepresence of an increased resource supply. However, becauseyounger, finer roots are most able to absorb nutrients, it maynot be energetically worthwhile for a plant to maintain older,less efficient roots. Thus, fine root turnover may increase ina high-nutrient environment (Brække 1992; Pregitzer et al.1995). This mechanism of root foraging involves an increasein fine root growth in nutrient rich areas but also increasedroot mortality. Root density is not necessarily changed.

In addition to direct observations of changes in root mor-phology, other plant traits can strongly suggest that root for-aging has taken place, although they do not indicate the typeof foraging. For instance, when comparing plants betweenhomogeneous and heterogeneous nutrient environments, in-creased plant size, or a decreased root to shoot ratio in theheterogeneous environment, suggests that roots were able totake advantage of nutrient patches. These indirect secondarymeasures are important because plants can obtain benefitsthrough forms of root foraging that are not easily measuredincluding root architecture (Fitter et al. 1988; Fitter andStrickland 1991) and physiological mechanisms (Robinsonand Rorison 1983; Jackson et al. 1990; Robinson et al.1994).

The secondary traits (i.e., increased plant size and de-creased root to shoot ratio), although not measuring root for-

aging directly, quantify its benefits. Increased abovegroundplant size is one potential outcome of foraging behavior(Anghinoni and Barber 1980). This result suggests thatplants able to absorb needed nutrients more effectively fromthe soil apply a greater proportion of their energy reserves toaboveground growth. In addition to an increase in above-ground biomass, a plant may be able to reduce the total rootlength necessary to obtain a sufficient amount of nutrientsfrom the soil without reducing aboveground growth. In sucha case, plants growing in a heterogeneous soil environmentwill display a decreased root to shoot ratio.

Although all of the parameters outlined above are possibleresponses to a heterogeneous environment, they should notall be expected to occur together in a single species. Somespecies, for instance, may use physiological means to en-hance nutrient uptake (Robinson and Rorison 1983; Jacksonet al. 1990; Robinson et al. 1994) and not display increasedroot length within patches but still have increased above-ground growth or a decreased root to shoot ratio. Similarly, atree that forages for nutrients (morphologically or physiolog-ically) may not display increased aboveground growth in aheterogeneous environment because the extra energy ob-tained is stored.

This study examines the foraging ability of seven tropicalforest tree species of differing successional status. The studyfollows other work in this area that has explored the ideathat foraging ability is related to successional status (Bauhusand Messier 1999; Campbell et al. 1991; Grime and Mackey2002; Einsmann et al. 1999). While not examining this ideadirectly, Huante et al.’s (1998) study of trees indigenous toMexico, like the present experiment, examined the foragingstatus of tropical trees.

Here, a greenhouse experiment is used to focus on treesindigenous to Nicaragua. In Nicaragua and elsewhere, geo-statistical studies have shown that natural disturbance in-creases the patchiness of belowground resources (B.C. Blair,unpublished data; Dali et al. 2002; Gross et al. 1995; Hirobeet al. 2003). It is the early successional tree species that ex-perience this more variable environment directly. For thisreason, it is hypothesized that early successional tree specieswill be most effective at taking advantage of heterogeneoussoil resources. Root foraging will be measured directlythrough root density measurements as well as by examiningindirect indicators of a species’ relative advantage in hetero-geneous environments (e.g., decreased root to shoot ratioand reduced root width).

Methods

SpeciesSeven tropical forest species were used that represent a

range of successional types (Table 1). Three species havebeen classified as early successional (Ceiba pentandra (L.)Gaertn., Cedrela odorata L., and Cordia alliodora (Ruiz &Pavón) Oken) and three as late successional (Dalbergiaretusa Hemsl., Gliricidia sepium (Jacq.) Kunth ex Walp.,and Swietenia macrophylla King) (see Table 1 for refer-ences). An additional species, Albizia guachapele (Kunth)Dugand, has, to the authors’ knowledge, not been classifiedinto a successional type. Propagation was done using seeds

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collected in Nicaragua that were purchased from the Bancode Semillas Forestales located in Leon, Nicaragua, and sub-sequently transported to the University of Michigan. All spe-cies with the exception of A. guachapele and S. macrophyllaare found in Nicaragua’s wet tropical forests on the easterncoast as well as in the dry forests to the west. Albiziaguachapele’s range in Nicaragua is limited to Pacific dryforests, while S. macrophylla is found only in the wetter re-gions to the east.

Experimental designHeterogeneous fertilization treatments were used to create

variable soil environments in which the only difference be-tween patches was P content. Seeds from each of the sevenspecies were planted individually in standard 21-cm-diameter plastic pots in two soil environments: a homoge-neous fertilization treatment and a heterogeneous fertiliza-tion treatment.

Soil consisted of a 1:1 by volume mixture of rinsed puresilica sand and potting soil (Sunshine Mix® 4, Sun Gro Hor-ticultural). This mixture was used to assure a low-P environ-ment in the P-free area of the heterogeneous fertilizationtreatment. All pots were saturated once every 2 weeks with a50% modified Hoagland nutrient solution (without P)(Hoagland 1938) to prevent nutrient deficiencies of other nu-trients. The soil was kept near field capacity at all times.

Every pot was fertilized at a rate of 100 mg P/kg soil(500 mg P/pot) for a fertilization rate of 110 kg P/ha. How-ever, the distribution of P varied between treatments. To cre-ate the homogeneous fertilization treatment, 100 mg of Pwas added to every kilogram of soil mixture. After thor-oughly mixing, each pot was filled with 5 kg of this homo-geneously fertilized soil. To create the heterogeneousfertilization treatment, pots were filled with 5 kg of the un-fertilized soil mixture. Using a 6-cm aluminum core (14% ofpot volume), a soil core was taken 2 cm from the pot’s edge.The soil from the core was put in a bucket and mixed with

500 mg of P. This P-enriched soil was then put back into thecoring hole to create a cylindrical fertilizer patch. A smallstake was placed in the middle of each patch for later identi-fication. All P was added in the form of CaH4(PO4)2.

This study was carried out on greenhouse benches at theMathai Botanical Gardens in Ann Arbor, Michigan, from20 May to 13 September 2000. Greenhouse temperatures av-eraged between 23 and 27 °C. Similarly, temperatures inNicaragua averaged between 25 and 27 °C during this5-month period. Photoperiod was comparable, with daylengths ranging from 12 to 15 h in Ann Arbor and from 12to 13 h in Nicaragua.

Seeds were initially planted in silica sand on trays and in-dividually transplanted within a week of their emergenceinto the previously prepared pots. Seedlings were planted inthe center of pots. When planted in the heterogeneous fertil-ization treatment, seedlings were at least 2 cm away fromthe enriched patch. Each fertilization treatment was repli-cated 10 times for each species. The exception to this wasS. macrophylla, which because of germination problems hadsufficient seedlings for only the heterogeneous fertilizationtreatment. This resulted in a total of 130 pots. Four potswere removed over the course of the experiment because ofdamage from insects or transplant shock. These includedthree C. alliodora pots, two from the homogeneous fertiliza-tion and one from the heterogeneous fertilization treatment,and one S. macrophylla pot from the heterogeneous fertiliza-tion treatment.

At harvest, tree seedlings were cut at soil level and soilcores were taken for root analysis. Aboveground biomasswas dried at 70 °C and weighed. In the heterogeneous fertil-ization treatment, two 6-cm soil cores were taken, one fromdirectly over the fertilizer patch and a second, a control, onthe opposite side of the pot at a point equidistant from thepot edge as the fertilized core. In the homogeneously fertil-ized pots, just one core was taken 2 cm from the pot edge.Roots were removed from soil cores through a combination

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1130 Can. J. For. Res. Vol. 34, 2004

Species (family) Abbreviation Common name Transplant date Harvest dateDays ofgrowth

Reference(s) forsuccessional status

Early successional speciesCordia alliodora

(Borraginaceae)CA Laurel 24 June 2000 13 Sept. 2000 82 Opler and Janzen 1983;

Strauss-Debenedetti andBazzaz 1996

Cedrela odorata (Meliaceae) CO Cedro Real 10 June 2000 21 Aug. 2000 73 Ramos and Grace 1990;Strauss-Debenedetti andBazzaz 1996

Ceiba pentandra(Bombacaceae)

CP Ceiba 10 June 2000 21 Aug. 2000 73 Baker 1983; Agyeman etal. 1999

Late successional speciesDalbergia retusa (Fabaceae) DR Granadillo 10 June 2000 29 Aug. 2000 81 Hartshorn 1983Gliricidia sepium (Fabaceae) GS Madero Negro 10 June 2000 21 Aug. 2000 73 Janzen 1983Swietenia macrophylla

(Meliaceae)SM Caoba 24 June 2000 13 Sept. 2000 82 Whitmore 1983; Strauss-

Debenedetti and Bazzaz1996

Unknown classificationAlbizia guachapele

(Mimosaceae)AG Gavilan 10 June 2000 21 Aug. 2000 73 None

Table 1. Species used in the study and their successional status and growth period.

of wet sieving (2-mm mesh) and visual inspection andstored in a 30% alcohol solution until analysis. Before siev-ing, six soil subsamples (approximately 10 g each) weretaken for P analysis from each of the three potential P re-gimes (nutrient patch, control patch, and homogeneouslyfertilized soil) for a total of 18 subsamples (6 samples × 3treatments).

Binary root images were obtained using a desktop scannerand light bank system (Richner et al. 2000). These imageswere examined using the program ROOTEDGE (Kasper andEwing 1997), which estimates root length and diameter us-ing the edge chord algorithm (Ewing and Kasper 1995).

Analysis

NutrientsEach soil sample was tested for available P to determine if

P remained localized at the end of the experiment. Analyseswere done on air-dried soil. Soil P was determined using2.5-g subsamples extracted with 50 mL of Olsen’s solution(Olsen and Sommers 1982) and automated colorometry(Quickchem 8000 FIA+; Lachat Instruments, Milwaukee,Wis.).

Rooting patternRoot length density (RLD) (centimetres per cubic centi-

metre), width (millimetres), and a statistic of foraging preci-sion were used to analyze differences in rooting patterns.RLD was calculated in pots by core and on a per pot basisfor later comparisons. Core RLD was determined by takingthe total root length (centimetres) in each core and dividingit by core volume (770 cm3). Estimated average RLD per potwas determined in the homogenous pots by using the RLDfound in the single core. In the heterogeneous pots, theweighted average of the two cores (patch and even) was cal-culated (fertilized core = 14% of pot volume). Similarly, es-timates of average root width by core and per pot were

calculated. Foraging precision was calculated by taking thedifference between the RLD of the P and control patches di-vided by the RLD of the control patch ((RLD enrichedpatch – RLD control patch)/RLD control patch) (Farley andFitter 1999). Here, a value above zero indicates increasedroot proliferation in the P patches.

Length and width averages were examined to see ifsignificant treatment differences existed between the hetero-geneous and homogeneous P treatments or within het-erogeneous pots. Differences between heterogeneous andhomogeneous pots were determined using one-way ANOVA.Within the heterogeneous pots, differences between the Pand control cores were analyzed using paired sample t tests.Root data were log transformed before analysis to meet as-sumptions of normality.

Aboveground biomassAboveground dry biomass (grams) and the root length

density to shoot ratio (RLD/S) (cm·cm–3·g–1) were deter-mined for each pot. The root length to shoot ratio was calcu-lated using the estimated average RLD and aboveground drybiomass. These secondary parameters were used to deter-mine if roots were able to take advantage of the heteroge-neous soil environments. Comparisons between treatmentswere made using one-way ANOVA. Aboveground biomassdata were log transformed before analysis to meet the as-sumptions of normality.

Results

NutrientsNutrient analysis revealed that there was greater P avail-

ability in cores taken from fertilized cores in heterogeneousnutrient pots than in those from the unfertilized surroundingarea. The hierarchy of P availability within cores was as ex-pected: inside patch (79.41 ± 7.79 mg/kg) > homogeneous

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SpeciesCorelocation

RLD(cm/cm3)

Root width(mm) n

Albizia guachapele Patch 0.39±0.06* 0.51±0.01 10Control 0.28±0.09 0.52±0.02 10

Cordia alliodora Patch 0.64±0.19 0.40±0.03 9Control 0.36±0.05 0.40±0.02 9

Cedrela odorata Patch 0.65±0.08* 0.50±0.02 10Control 0.54±0.10 0.50±0.01 10

Ceiba pentandra Patch 0.45±0.06 0.50±0.02 10Control 0.43±0.08 0.46±0.02 10

Dalbergia retusa Patch 0.40±0.03 0.45±0.01 10Control 0.37±0.04 0.42±0.01 10

Gliricidia sepium Patch 0.89±0.12* 0.45±0.02* 10Control 0.57±0.06 0.48±0.02 10

Swietenia macrophylla Patch 0.25±0.04* 0.60±0.04 9Control 0.09±0.02 0.54±0.02 9

Note: All values are core means (±SE). Asterisks indicate significant differences (paired sam-ple t test, P < 0.05) within a species between treatments. RLD was significantly greater in thefertilized cores than in the unfertilized control cores in four species (A. guachapele: t = 2.29,P = 0.048; C. odorata: t = 2.51, P = 0.033; G. sepium: t = 2.92, P = 0.017; S. macrophylla: t =2.65, P = 0.029) and root width was significantly thinner in the fertilized cores in one species(G. sepium: t = 6.53, P < 0.001).

Table 2. Mean root length density (RLD) and mean root width by species in theheterogeneous fertilization treatment.

fertilization (8.47 ± 0.65 mg/kg) > outside patch (3.28 ±0.26 mg/kg).

Foraging behaviorIn the heterogeneous fertilizer treatment, there was a trend

in all species to increase RLD in the fertilized cores (Ta-ble 2). When species are grouped, this trend was significant(t = 4.53, df = 67, P < 0.001). Separately, in four of theseven species examined (A. guachapele, C. odorata, G. se-pium, and S. macrophylla), root proliferation as measured byaverage RLD was significantly greater in the fertilized coresthan in the unfertilized control cores (Table 2). Foraging pre-cision was positive in all cases but there was a 15-fold dif-ference between the lowest species (C. pentandra andD. retusa) and highest species (A. guachapele and S. macro-phylla) (<0.2 to >3) (Fig. 1). No trend existed between rootwidths of the fertilized and control cores and G. sepium wasthe only species where shifts in root width between coretypes was significant. Here, root width significantly de-creased in P-enriched patches (Table 2).

When comparing whole pots, few differences were de-tected between the heterogeneous and homogeneous treat-ments. No species tested significantly changed their RLD inresponse to the heterogeneity of the soil P environment (Ta-ble 3). Root width was significantly affected in onlyC. alliodora, which decreased root width in response to theheterogeneous nutrient treatment (Table 3). Cordia alliodoraand G. sepium increased their aboveground dry mass in theheterogeneous soil environment (Table 3). Cordia alliodoradecreased its RLD/S in the heterogeneous P treatment (F =16.45, df = 1, 15, P = 0.001) (Fig. 2).

Discussion

Foraging abilityThe data suggest that root foraging occurred in five of the

seven species tested. Only two species, C. pentandra and

D. retusa, showed no direct or indirect evidence that theywere taking advantage of localized nutrient resources. Infour of these species, average RLD increased in P patches(Table 2). This was the most common way that foraging wasdetected. In contrast, reducing root width was not commonand occurred in only one instance (G. sepium) when com-paring nutrient with nonnutrient patches (Table 2).

In a previous study with C. alliodora, this species in-creased root proliferation in the presence of a NPK nutrient

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1132 Can. J. For. Res. Vol. 34, 2004

Fig. 1. Average foraging precision ((root length (RLD) enrichedpatch – RLD control patch)/RLD control patch) in heterogeneousfertilization treatment by species. Error bars represent ±SE. SeeTable 1 for species abbreviations.

SpeciesFertilizationtreatment

Abovegrounddry mass (g)

RLD(cm/cm3)

Root width(mm) n

Albizia guachapele Heterogeneous 5.11±0.95 0.30±0.08 0.52±0.02 10Homogeneous 7.10±1.08 0.51±0.09 0.55±0.01 10

Cordia alliodora Heterogeneous 8.43±1.34* 0.40±0.07 0.39±0.02* 9Homogeneous 4.72±0.65 0.42±0.09 0.49±0.03 8

Cedrela odorata Heterogeneous 6.72±0.39 0.56±0.09 0.50±0.01 10Homogeneous 5.25±0.71 0.44±0.10 0.48±0.01 10

Ceiba pentandra Heterogeneous 7.38±0.72 0.44±0.07 0.46±0.01 10Homogeneous 8.32±1.23 0.42±0.08 0.48±0.02 10

Dalbergia retusa Heterogeneous 4.15±0.22 0.38±0.04 0.43±0.01 10Homogeneous 4.15±0.47 0.39±0.08 0.39±0.01 10

Gliricidia sepium Heterogeneous 6.73±0.50* 0.62±0.06 0.48±0.02 10Homogeneous 4.83±0.50 0.48±0.07 0.44±0.01 10

Swietenia macrophylla Heterogeneous 5.30±0.27 0.12±0.02 0.55±0.01 9Homogeneous na na na na

Note: Comparisons are between whole pots. All values are pot means (±SE). na, not applicable. As-terisks indicate significant differences (ANOVA, P < 0.05) within a species between treatments. Above-ground dry mass was significantly greater in the heterogeneously fertilized pots in two species(C. alliodora: F = 8.72, P = 0.009; G. sepium: F = 7.58, P = 0.013). Root width was thinner in theheterogeneously fertilized pots in one species (C. alliodora: F = 7.76, P = 0.014).

Table 3. Seedling aboveground dry mass, root length density (RLD), and mean root widthby species.

patch (Huante et al. 1998). The current study did not revealsignificant increased rooting density, although there was anonsignificant trend in this direction. It is possible that thedifference in supplied nutrients in the patch (P versus NPK)caused the discrepancy between the two studies, as speciesoften have a nutrient-specific ability to forage (Robinson1994). However, other indications that C. alliodora was tak-ing advantage of the P patches were found. This species dis-played an increased aboveground dry mass and a decreasedRLD/S in the heterogeneous pots (Fig. 2; Table 3). To-gether, this evidence strongly suggests that this species wastaking advantage of nutrient heterogeneity in this study.

Some studies suggest that inherently faster growing spe-cies have a greater ability to morphologically forage for nu-trients than species that grow more slowly (Crick and Grime1987; Robinson and van Vuren 1998; Fransen et al. 1998).However, recent work has shown that this relationship is notuniversal (Fransen et al. 1999a, 1999b). The current studyfound no correlation between a species’ above- or below-ground growth and its ability to morphologically forage fornutrients.

While not included in this study, the presence ofmycorrhyzae could alter the nutrient absorbing capacity ofthe species tested by increasing the spatial range from whichthey can obtain nutrients. Mycorrhyzae are particularly ef-fective at obtaining P (Reed 1991) and it is well establishedthat they can morphologically forage for nutrients (Olsson etal. 2002). This makes mycorrhyzae in addition to physiolog-ical and morphological root changes a third method thatplants can use to forage for nutrients.

Successional statusThe two species that showed no indications of taking ad-

vantage of the heterogeneous environment are at oppositeends of the successional gradient. While D. retusa is a latesuccessional species found primarily in Nicaragua’s matureforests, C. pentandra is a pioneer species that is common indisturbed forests and pastures. From the small subset ofspecies examined, there is no evidence that species of a par-

ticular successional status take greater advantage ofheterogeneously distributed P.

Huante et al. (1998) had similar results in work examiningthe responses of Mexican tree species to a heterogeneoussoil environment. In their study, two late successional spe-cies (Caesalpinia platyloba and Celaenodendron mexi-canum) and two early successional species (Cordia alliodoraand Heliocarpus pallidus) were used. All species increasedRLD except C. platyloba, which was unable to reach the nu-trient patch before harvest. The authors suggested that if nu-trient patches are time limited, slower growing, latesuccessional species may not be able to take full advantageof them. Instead, these species may dedicate more energy tomaintaining root systems once established than their fastergrowing competitors do (Grime et al. 1986; Huante et al.1998).

This idea suggests that the limitation of late successionalspecies in early successional environments is not their in-ability to forage for nutrients but is their slower relativegrowth rate. A seedling or sapling facing a soil resourcefilled with ephemeral nutrient patches will be at a disadvan-tage if its root relative growth rate is slower than that of itscompetitors. However, this may not be a limitation for anadult tree with an extensive root system. In an early suc-cessional environment where the average tree size and rootmass is small, late successional species may not be able toexplore the soil at a fast enough rate to take advantage of en-vironmental heterogeneity.

This study did not test this potential limitation, and allspecies tested had sufficient time to reach nutrient patches.Two of the three late successional species tested were amongthe slowest growing above and below ground (D. retusa andS. macrophylla) (Table 3). However, the third (G. sepium)had a higher than average aboveground dry mass (heteroge-neous fertilization) and RLD (homogeneous and heteroge-neous fertilization) at the end of the experiment (Table 3).This species may be an anomaly, however, as it is generallyaccepted that late successional species are slower growingthan their early successional counterparts (Huante et al.1995).

Campbell et al. (1991) suggested, based on an examina-tion of eight herbaceous species, that there is a trade-off be-tween the size of a plant’s root system (scale) and itsprecision in root foraging. Two subsequent studies found asimilar negative correlation lending support to this idea(Wijesinghe et al. 2001; Grime and Mackey 2002). We alsofound a negative correlation between scale and precision(r = –0.71), although not a statistically significant one owingto a small sample size (n = 7). However, other studies sug-gest that the scale–precision relationship is not universal(Einsmann et al. 1999; Farley and Fitter 1999; Bliss et al.2002). Einsmann et al. (1999), for example, found a positiverelationship among the six herbaceous species examined intheir study. However, the scale of soil heterogeneity greatlyinfluences species’ ability to perceive nutrient-rich patchesand their capacity to respond to them (Wijesinghe andHutchings 1997, 1999; Einsmann et al. 1999; Farley and Fit-ter 1999; Wiens 2000). Ideally, studies should match experi-mental patch size with the scale of heterogeneity found in aspecies’ natural environment. However, in a temporallychanging habitat (e.g., during ecological succession), this

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Fig. 2. Root length density to shoot ratio (RLD/S) (cm·cm–3·g–1)between heterogeneous fertilization and homogeneous fertiliza-tion pots. The asterisk represents a significant difference betweentreatments (P < 0.001). Error bars represent ±SE. See Table 1for species abbreviations.

may be difficult, as multiple scales would be needed.Matching the scale of heterogeneity with that of the naturalenvironment is rarely attempted and may be a cause of thecontrasting conclusions found in the literature.

Acknowledgements

We would like to thank John Vandermeer for his sugges-tions on the experimental design of this study. MichaelPalmer and Jim Dickenson of the Mathaei Botanical Gardengreenhouses helped make the day-to-day operation of thisstudy go smoothly. Finally, we appreciate the assistanceof L.D. Potter who spent many hours harvesting plants at theend of the experiment.

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