Linking aphid honeydew, throughfall, and forest floor

solution chemistry of Norway spruce

AbstractIn a seminatural manipulation experiment with artificial irrigation we followedthroughfall and forest floor solution chemistry collected underneath aphid infestedand uninfested Norway spruce. Solutions underneath infested trees showed significantlyhigher concentrations of dissolved organic carbon (DOC) but lower concentrationsof dissolved organic nitrogen (DON), NO3-N, and NH4-N in throughfall solutionsand of NH4-N in forest floor solutions. Average concentrations were 40.5% (DON),27.5% (NO3-N), and 46.2% lower (NH4-N) underneath infested trees in throughfallsolutions, and 19.5% (DON), 9.4% (NO3-N), and 42.0% (NH4-N) lower in forestfloor solutions. Differences in throughfall were more pronounced than in forest floorleachates. It is likely that honeydew is fuelling the metabolism of micro-organismsand thus critically affects above and below ground nutrient cycles. We emphasize theimportance of linking the biology of herbivores and micro-organisms withgeochemical processes.

KeywordsAphid honeydew, Cinarids, ecosystem processes, forest floor leachates, spatialvartiability, throughfall chemistry

Ecology Letters (1998) 1 : 13±16

I N T R O D U C T I O N

Much of the recent progress in ecosystem ecology is dueto the recognition that ecosystems are not homogenousentities in a stable equilibrium but consist of hetero-geneous patches with gradients between which energy andmatter can flow (Huntly 1991; Manderscheid & Matzner1995; Wu & Loucks 1995). For example, the spatialvariability of different element concentrations in through-fall of Norway spruce ranged between 21% and 164%(expressed as coefficient of variance) (Seiler & Matzner1995). Likewise, the distribution and local abundance ofmany individuals of different species will form patchpopulations that attribute to mosaics of high and lownutrient concentrations or the speed of ecological andbiogeochemical processes (Coleman et al. 1983; Remmert1991). Aphids are an interesting group of herbivores fortesting the relationships between local or temporalabundance and the effects on ecosystem processes, suchas flows of nutrients from the phyllosphere to the forestfloor, because many species excrete large quantities ofhoneydew, e.g. on Norway spruce (Zoebelein 1954;Stadler et al. 1998). Honeydew consists mainly of sugarsof low molecular weight, thus forming a resource that is

easy to consume, e.g. by micro-organisms of the phyllo-sphere (Stadler & MuÈ ller 1996) and soil (Dighton 1978;Grier & Vogt 1990). The nitrogen content is usually low,ranging between 0.2% and 1.8% of the dry mass(Maurizio 1985).

Here, we present the results of an irrigation experimentwith aphid infested and uninfested Norway spruce onnutrient chemistry in throughfall and forest floor leachates.

M A T E R I A L S A N D M E T H O D S

Six 10-year-old spruce trees were used in the experiment,with three trees being artificially infested at the beginningof May with 100 individuals of C. pilicornis (Hartig) and C.costata (Zett.), two of the most abundant aphids on Piceaabies (L.) Karst. in Central Europe (Scheurer 1964). Withthe help of an insect proof net we sheltered the aphidsfrom natural enemies until the beginning of July, butremoved the net afterwards to allow dispersal orpredation. The fluctuation in aphid population densitythus mimiced a field infestation pattern with locally highaphid numbers in spring but declining densities duringsummer. For controlling the quantities of rain we coveredthe trees with a transparent roof (20 m2) and installed an

#1998 Blackwell Science Ltd/CNRS

Bernhard Stadler and Beate

Michalzik

Bayreuth Institute for Terrestrial

Ecosystem Research, University

of Bayreuth, 95440 Bayreuth,

Germany.

ECOLOGY Letters, (1998) 1 : 13±16

L E T T E R

AhedBhedChedDhedRef markerFig markerTable mar-kerRef endRef start

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irrigation system. We standardized plant quality, theamount of rain applied onto the trees, rain chemicalcomposition [10.03 mg/L NH4-N, 10.18 mg/L NO3-N,11.33 mg/L K2SO4, 3.55 mg/L Na2 SO4, 4.93 mg/LMgSO467H2O, 7.33 mg/L CaCl2, and 286.2 mg/L (1N)H2SO4 with pH 3.61 and conductivity of 161 mS/cm], andthe irrigation schedule to allow comparisons betweentreatments. Underneath each tree two throughfall sam-plers (diameter 15 cm) and forest floor lysimeters(diameter 17 cm) were placed to measure input to thelysimeters and output from forest floor leachates. Theforest floor (Ol±Oh horizon) was carefully cut out fromthe Waldstein site/Fichtelgebirge, Germany, and trans-ferred undisturbed into the lysimeters 1 week before theexperiment started in June. Details on the study area aredescribed in a companion paper (Stadler et al. 1998) and inother papers from ongoing studies in the field (Mander-scheid & GoÈ ttlein 1995; Stadler & MuÈ ller 1996).

Chemical analyses

Forest floor solutions were filtered with a cellulose-acetatemembrane filter, Sartorius (0.45 mm). DOC was deter-mined as CO2 after persulphate-UV-oxidation (FossHaereus, liqui TOC). NH4-N and NO3-N were measuredby ionchromatography. DON was calculated by subtract-ing NH4-N and NO3-N from total dissolved nitrogen.Total nitrogen was measured after thermo-oxidation at700 8C as NOx (Abimed: TN-05).

We provide a descriptive summary of the main resultsin a condensed form by showing differences in concentra-tions between the control and the infested treatments.

R E S U L T S

The population dynamics of aphids above throughfallsampler and soil lysimeters showed the highest numbersfrom the beginning to mid-July, whereas the populationdeclined rapidly after the insect nets were removed due toaphid dispersal and predation through natural enemies(Fig. 1). In late August no more aphids were feeding onthe trees. The high standard errors were largely due to thefact that the aphids showed a high degree of mobility(especially during early season) or due to local extinctionby natural enemies.

Differences in concentrations of throughfall and forestfloor solution chemistry between controls and infestedtrees are given in Fig. 2. DOC concentrations inthroughfall of infested trees quickly responded to thepresence of aphids and reflected the population dynamicsof the Cinarids. Nitrogen concentrations of throughfalland floor leachates were negatively affected underneathinfested trees as controls tended to have higher concen-

trations of DON, NO3-N, and NH4-N, particularlyduring peak aphid abundance. During July throughfall,concentrations of DOC and DON significantly differedbetween control and infested trees (Mann±Whitney test: P5 0.001) but not in forest floor leachates. NO3-N andNH4-N concentrations in throughfall were significantlydifferent in June (Mann±Whitney test: P 5 0.001) butfloor leachates only differed significantly with respect toNH4-N in July (Mann±Whitney test: P 5 0.05). Averageconcentrations of nitrogen compounds in throughfall andforest floor solution were always higher underneath

#1998 Blackwell Science Ltd/CNRS

14 B. Stadler and B. Michalzik

Figure 1 Seasonal dynamics in the number of aphids above soillysimeters (., ÐÐ) and throughfall samplers (&, - - - -)underneath Norway spruce (means+ SE). The arrow indicatesthe time when the insect net was removed.

Figure 2 Differences in concentrations between unaffected(cont.) and honeydew affected (aphid) solutions. Throughfallsolution (&, - - - -) and forest floor leachates (*, ÐÐ) werecollected underneath Norway spruce from June to August(means+ SE). Arrows indicate the time when the insect net wasremoved.

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uninfested trees compared with aphid infested spruce[throughfall, 40.5% (DON), 27.5% (NO3-N), and 46.2%(NH4-N) higher; floor leachate, 19.5% (DON), 9.4%(NO3-N), and 42.0% (NH4-N) higher]. Thus, differencesbetween treatments appeared more pronounced inthroughfall compared with floor leachates, which mightindicate a buffering effect of the forest floor.

D I S C U S S I O N

All ecological systems and the organisms living within anecosystem show heterogeneity and patchiness on a broadrange of scales. Patchiness is a fundamental property ofmany insect populations and biogeochemical processesthat affect element cycling. As a scientific concept it couldtherefore provide a common ground for populationbiologists and ecosystem scientists (Levin 1992). We didnot show any results on the population dynamics ofaphids in the field because there exists a wealth ofinformation on this subject (e.g., Scheurer 1964; Kidd1990; Stadler et al. 1998), indicating that aphids areparadigmatic for testing consequences of extreme spatio-temporal fluctuations in abundance for its effect on flowsof nutrients in an ecosystem. The aphid populationsreared in the experiment covered the whole range of thenatural dynamics from high to low infestation periods(Fig. 1). Therefore, our results should have a close bearingfor addressing ecosystem processes from a patch point ofview and for stressing the potential importance of thepopulation dynamics of herbivores for flows of energyand matter through an ecosystem.

Micro-organisms are likely to profit from the presenceof honeydew as a source of energy (Dighton 1978; Stadler& MuÈ ller 1996). Consequently, trophic interactionsbetween Spruce, aphids, and micro-organisms of thephyllosphere and soil are likely to become important for arapid transformation of nutrients from the phyllospheredown to the soil. Underneath infested trees throughfallconcentrations of NH4-N, NO3-N, and DON were lowerthan in throughfall of control trees. Thus, as morenutrients enter the forest floor underneath uninfested treesthe expectation is that nitrogen concentrations of forestfloor leachates should be increased by the higher inputunderneath these trees. There does not seem to exist sucha simple relationship between input and output, however,because soil leachate concentrations mostly showed aunimodal distribution indicating seasonal effects. It ismore likely that the response of the soil biota to the inputof honeydew gradually starts to affect nutrient chemistry,because large differences in throughfall concentrations ofNO3-N and NH4-N in June did not correspond todifferences between treatments in the respective concen-trations of forest floor leachates. Large amounts of sugars

reached the forest floor in June/July when aphidpopulations peaked (Fig. 1), but no difference in theDOC concentrations of the forest floor leachates waspresent between treatments (Fig. 2), supporting acomplete and rapid consumption of the energy by soilmicro-organisms. NH4-N is often the preferred N sourcefor mirco-organisms (Brock & Madigan 1991). Thus,similarly to the phyllosphere, if energy becomes availablethe uptake of this compound by micro-organisms may beenhanced. As a result, differences in throughfall and forestfloor nutrient concentrations underneath infested anduninfested Norway spruce may develop. The populationdynamics of aphids, their excreta, micro-organismgrowth/metabolism, and their combined effects onthroughfall or forest floor leachate chemistry formcomplex interactions. Linking the ecology of herbivoresand micro-organisms with geochemical processes istherefore likely to further our understanding of spatialpatterns of ecosystem processes.

A C K N O W L E D G E M E N T S

Egbert Matzner kindly commented on an earlier draft ofthe manuscript. A. Glaûer, K. Moser, B. Popp, and C.StoÈ cker helped with the chemical analyses. Financialsupport was given by the German Ministry for Researchand Technology (FoÈ rdernummer: BMBF No. PT BEO51±0339476B).

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Manderscheid, B. & GoÈ ttlein, A. (1995). WassereinzugsgebietLehstenbach±das BitoÈ k Untersuchungsgebiet am Waldstein(Fichtelgebirge, NO-Bayern). Bayreuther Forum OÈkologie, 18, 1±86.

Manderscheid, B. & Matzner, E. (1995). Spatial and temporalvariation of soil solution chemistry and ion fluxes through thesoil in a mature Norway spruce (Picea abies (L.) Karst.) stand.Biogeochemistry, 30, 99±114.

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Maurizio, A. (1985). Honigtau±Honigtauhonig. In Waldtrachtund Waldhonig in der Imkerei. eds Kloft W.J., Maurizio A. &Kunkel H., pp. 268±295. Munich: Ehrenwirth.

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Stadler, B., Michalzik, B. & MuÈ ller, T. (1998). Linking aphidecology and ecosystem processes: the effect of spatial andtemporal variability in aphid abundance on nutrient fluxes in aconiferous forest. Ecology, in press.

Stadler, B. & MuÈ ller, T. (1996). Aphid honeydew and its effecton the phyllosphere microflora of Picea abies (L.) Karst.Oecologia, 108, 771±776.

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16 B. Stadler and B. Michalzik

B I O S K E T C H

Bernard Stadler's research interests focus at the interface ofpopulation and ecosystem ecology, the life-history strategiesof phytophageous insects and the evolution of aphid±ant interactions.

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