Linking Aphid Ecology with Nutrient Fluxes in a Coniferous Forest

Linking Aphid Ecology with Nutrient Fluxes in a Coniferous ForestAuthor(s): Bernhard Stadler, Beate Michalzik and Thomas MullerSource: Ecology, Vol. 79, No. 5 (Jul., 1998), pp. 1514-1525Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/176773 .

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Ecology, 79(5), 1998, pp. 1514-1525 ? 1998 by the Ecological Society of America

LINKING APHID ECOLOGY WITH NUTRIENT FLUXES IN A CONIFEROUS FOREST

BERNHARD STADLER,I BEATE MICHALZIK,' AND THOMAS MULLER2

'Institute for Terrestrial Ecosystem Research, University of Bayreuth, 95440 Bayreuth, Germany 2Centre for Agricultural Landscape and Land Use Research, Miincheberg, Institute of Microbial Ecology and Soil Biology,

14641 Paulinenaue, Germany

Abstract. Flows of dissolved organic carbon (DOC) in throughfall and soil solutions in forest ecosystems vary spatially and temporally. However, the reasons for the variability of DOC flows are unknown. Phytophagous insects such as aphids have not been considered a potential source of organic carbon, even though aphids feeding on trees excrete copious amounts of honeydew. We followed the key processes determining the origin, flow, and path of honeydew from the phyllosphere of a Norway spruce stand to the soil. We analyzed the chemical composition of needle leachates, throughfall, and soil solution to calculate fluxes of DOC and hexose-C in an aphid-infested and an uninfested Norway spruce stand.

At the individual aphid level, the amount of honeydew produced was dependent on temperature, developmental stage, and the nutritional status of spruce. At the population level, colony growth and natural enemies influenced the amount of honeydew available in the phyllosphere. The growth rates of microorganisms on spruce needles were significantly increased when honeydew was available.

This study of the fate of honeydew and associated metabolites within a forest stand shows that the concentrations of DOC and hexose-C in throughfall were reduced on the way to the soil and that there were no differences in the soil solutions from infested and uninfested stands. However, the distribution and abundance of honeydew-producing Ho- moptera had a marked effect on the spatial and temporal variability in the DOC concentrations in throughfall. High DOC concentrations in throughfall during summer are not exclusively due to the leaching of nutrients from leaves, but may also be attributed to the excreta of aphids.

Our results highlight the importance of studying physiological and life history processes in addition to taking the traditional biomass approach to ecosystem studies. We discuss our results with regard to the types of information that are preserved, transformed, or lost when crossing the conceptual border between one scale of observation and another. We emphasize the importance of identifying key processes at different spatiotemporal scales by linking the biology of individuals and populations with flows of energy and matter within an ecosystem, while stressing the need to identify ecosystem changes at different scales of observation.

Key words: aphids; carbon fluxes; dissolved organic carbon; ecosystem analysis; epiphytic microorganisms; forest ecosystems; honeydew; leaching; organic carbon; phyllosphere; Picea abies; spatial heterogeneity.

INTRODUCTION

Analyses of ecosystem processes have traditionally focused on fluxes of energy and matter through a de- fined section of a landscape. Insect herbivores, in con- trast to grazing mammals, are seldom considered to be contributors to such flows, because their biomass tends to be low compared to the biomass of trees or the organic soil body, or to atmospheric deposits into an ecosystem (Seastedt and Crossley 1984, Detling 1988). Only at times of severe infestations do insect herbivores receive greater attention with respect to the behavior of an ecosystem (Romme et al. 1986, Reiners 1988, Myers 1993). The role of microorganisms in eco-

Manuscript received 10 March 1997; revised 26 June 1997; accepted 17 July 1997; final version received 20 August 1997.

system functioning has been equally neglected, although recent work has emphasized the contribution of microorganisms to energy transfer in many ecosystems (Pomeroy et al. 1988, Fokkema 1991, Stadler and Mull- er 1996). Such studies emphasize biomass and the flow of energy while neglecting the specific physiological and ecological properties of species interacting in an ecosystem. Complex interactions are possible between insect herbivores such as aphids, which excrete copious amounts of honeydew, and microorganisms of the phyllosphere and/or soil, which use the honeydew as a source of energy. However, there appear to be no studies on their effects on ecosystem processes, although Macrosiphum liriodendri has received some attention for its effect on the nitrogen cycle of a Liriodendron tulipifera stand (Van Hook et al. 1980).

1514



July 1998 APHID HONEYDEW IN FOREST ECOSYSTEMS 1515

ahI ds . life-history

population dynamics plant quality, life cycle, temperature

honeydew on needles

throughfall honeydew remaining on needles (e.g. crystallizing)

growth of micro- th organisms on needles I

throu~hfall chemistry (DOC, Hexose-C) leaching from

needles

leachate chemistry (Hexose-C)

soil solution chemistry

ri'

(DOC, Hexose-C)

FIG. 1. Overview of major pathways of honeydew through the phyllosphere of Norway spruce. Words in italics highlight biological aspects that are investigated in order to identify sources of variation in the quantities of honeydew ultimately available for carbon fluxes. Horizontal arrows mark the experiments and chemical analyses done in this investigation at different spatiotemporal scales (individuals, populations, forest stand).

A major problem in studying the ecology of organisms as well as ecosystem processes such as throughfall fluxes is a high level of spatial and/or temporal heterogeneity, which obscures many key processes. Re- cent investigations dealing with the spatial or temporal variability in soil solution chemistry and ion fluxes in forest ecosystems have largely attributed the origin of variation in soil solutions to throughfall fluxes (Man- derscheid and Matzner 1995). Stem distance has been identified as a potential parameter influencing throughfall chemistry in a mature Norway spruce stand (Seiler and Matzner 1995), and several other factors such as age of leaves, exposure, type of plant, and temperature are known to affect throughfall chemistry (Tukey 1970). In deciduous forests, leaf leaching or leaf wash- ing is assumed to be the main source of increased levels of dissolved organic carbon (DOC) during the summer (McDowell and Likens 1988, Qualls et al. 1991); the increase in DOC provides microorganisms in the soil with considerable amounts of energy. However, the role of aphids in DOC fluxes has not been investigated.

The objective of the present study is to identify sources of spatial and/or temporal variability in the fluxes of organic carbon compounds in throughfall and soil solutions in the phyllosphere of Norway spruce that result from aphid ecology, i.e., from honeydew production and subsequent processes (Fig. 1).

This study starts by investigating the reproductive

biology of individual aphids of the genus Cinara as influenced by changes in the quality of their host trees and by changes in temperature. The amounts of honeydew produced at different stages in the life cycle of Norway spruce were determined for different aphid instars and for adult aphids. At the population level, the numbers of aphids were followed for three consecutive years. Together with the information from the individual level, this provided an estimate of the amount of honeydew produced per tree as well as per forest stand. The effect of honeydew on the population dynamics of microorganisms in the phyllosphere of Norway spruce was also analyzed. Lastly, at the level of the ecosystem, the effect of honeydew on the carbon concentration in the throughfall and soil solutions was determined by analyzing samples from rain collectors and lysimeters for DOC and hexose-C from aphid-infested and uninfested Norway spruce.

Studies on the life history and population dynamics of aphids, the ecology of microorganisms, and ecosystem carbon fluxes will eventually be integrated in order to develop a more complete picture of the carbon flow in the phyllosphere of a forest stand.

METHODS

Site description

The study site is located in the Fichtelgebirge, north- eastern Bavaria, Germany. It forms part of the Leh- stenbach watershed (418 ha), whose central area lies at an altitude of 800 m a.s.l., and is planted with Nor- way spruce (Picea abies [L.] Karst.) at densities of >300 trees/ha. The trees we used to study the population dynamics of aphids and nutrient fluxes were on a southwestern exposure and ranged in age between 10 and 15 yr. Understory plant species include Calama- grostis villosa, Deschampsia flexuosa, and Vaccinium spp., usually distributed in patches. The climate is con- tinental with short, mild summers and long, cold win- ters. The average monthly precipitation ranges between 15 and 152 mm, with a yearly average of 1100 mm. The monthly average temperature ranges from -100C in winter to +17'C during summer, with an annual mean of 5.60C. For the growth of aphids and microbes, the mean summer temperature, as measured continu- ously 2.5 m above the forest floor, is likely to be more important than the annual average. Over the period May-October 1995 the average temperature was 13.20C.

Soils in the watershed developed from weathered granitic bedrock and are classified as mosaics of Cam- bisols and Cambic Podzols. The soil texture varies from loamy sand to loam, with pH <4.0 (Manderscheid and Matzner 1995). The organic layer varies from moder to raw humus. Mean annual DOC concentrations range from 3.5 to 5.7 mg/L in precipitation and from 10.8 to 15.9 mg/L in throughfall (Manderscheid et al. 1995).



1516 BERNHARD STADLER ET AL. Ecology, Vol. 79, No. 5

Ecology of aphids and microorganisms

Five species of the genus Cinara were recorded at the study site with Cinara pilicornis (Hartig) and Cin- ara pruinosa (Hartig) as the dominant aphids, feeding exclusively on Norway spruce. All species are holo- cyclic, hatching from eggs during early to mid-April. During the growing period, four to five parthenogenetic generations are produced before egg deposition by ovipara starts during September-October. Occasionally, eggs are found as early as June. Although all these species feed on the woody parts of spruce, they deposit their eggs singly or in small patches of two to three eggs, mostly on needles from the current year.

Microorganisms living in the soil are known to re- spond to the presence of honeydew by increasing in number and/or in respiration rate (Dighton 1978). There is also a considerable biomass of microorganisms on leaf or needle surfaces, which could influence element cycling in ecosystems, i.e., the microepiphytes in a canopy of Douglas-firs may reach a standing crop of 38-60 kg/ha (Carroll 1979). Many microorganisms are energy limited (Dommergues et al. 1978); thus, the availability of honeydew sugars in the phyllosphere should promote microbial growth.

Life history of Cinara species

In many ecosystems, aphids may encounter a range of different plant developmental stages or plant qualities at any time. To investigate how an aphid's reproductive schedule is affected by the quality of its host plant, by the intrinsic life cycle of the host, and by temperature, we measured the age-specific survival and reproduction of individuals of C. pruinosa feeding on Norway spruce seedlings subjected to different treatments. Ten seedlings were planted in pots either filled with high-quality soil (5 parts [by volume] compost soil, 2 parts pumice, 2 parts lava, 2 parts peat soil, 1 part less, and 2.5 kg/M3 Osmocote fertilizer) or in sand without nutrients, in which the plants developed marked needle yellowing. These two extreme types of soil were chosen so that aphid performance could be followed on trees of high and low quality, similar to those they are likely to encounter on the study site. After transfer to a greenhouse, each plant was infested with a single newborn aphid (first-instar larva), which was then reared to maturity. On reaching maturity, the number of offspring produced at a particular age and the age-specific survival rates were recorded. In this way three consecutive aphid generations were reared. The first generation developed during bud burst, the second during shoot elongation, and the third after shoot growth ceased. The temperature in the greenhouse was 190 ? 20C, and plants were watered ac- cording to their needs. To compare the effect of varying temperature on the reproduction of aphids relative to plant quality, an identical treatment was set up at the experimental plot at the Institute for Terrestrial Eco-

-w'

A. ok.15 wXf

PLATE 1. Ovipara of Cinara pilicornis with droplets of honeydew on Norway spruce needles.

system Research University of Bayreuth. Aphids that

disappeared before offspring reproduction were not re-

placed, and were not included in the analysis because it could not be determined whether they abandoned the host plant or were lost to natural enemies.

Honeydew production

The excreta that aphids produce per day often exceed their biomass. We measured honeydew production of different instar larvae and adult aphids of C. pruinosa and C pilicornis feeding on 3-yr-old seedlings of P. babies grown in pots filled with compost soil. In order to investigate the influence of the life cycle of spruce on honeydew production, the experiment was started at the time of bud burst and repeated when shoot growth ceased. This was done by transferring a newborn aphid to the shoot of a seedling with a fine camelhair brush, where it was allowed to settle down and feed for 24 h. The following day a small piece of preweighed alu- minum foil was clipped underneath each individual in order to collect the honeydew excreted during the following 24 h. This procedure was repeated every 24 h until the aphid started to reproduce. The pieces of foil

plus honeydew were oven-dried at 40'C for 48 h and




reweighed on a Sartorius microbalance (sensitivity 1 [Lg). The temperature was 22? ? 10C, relative humidity 65%, light intensity 5000 lx, and photoperiod 18:6 h day: night. The honeydew produced by 73 C. pruinosa and 74 C. pilicornis was collected. Honeydew production of adult aphids and colonies comprising >100 individuals of mixed age (8.0-12.1% adults; 10.2-16.9% instars L4-L3; 74.4-81.2% instars L2-L1) was also measured at 10 ? 20C at a relative humidity of 65%. The study of honeydew production was completed by measuring the excretion rates of colonies of aphids on Norway spruce in the field during a 24-h period. These aphids had a similar range of age classes to allow comparison with the laboratory results.

Population dynamics of Cinara on Norway spruce

The population dynamics of Cinara spp. was mon- itored at the study site by recording aphid abundance at 2-wk intervals from April to October from 1994 to 1996. Trees were chosen at random, and at least five twigs per tree were searched for aphids. On each twig we recorded the numbers of aphids found on 1-3-yr- old shoots. No attempt was made to search for aphids on older shoots or on the trunk. The minimum amount of time spent searching for aphids was 2 h.

Sample collection and analyses of microorganisms of the phyllosphere

During the 1995 growing season, 1- and 2-yr-old shoots of P. abies infested with Cinara spp. and uninfested control shoots were collected from 10-15-yr- old Norway spruce trees on the study site. Samples were taken at the end of May, when aphid densities were still low; at the beginning of July, at the time of peak abundance; and at the beginning of September, when aphid numbers were again low. The time the shoots were collected was influenced by weather conditions and was always at least 1 wk after any precipitation, in order to allow honeydew to accumulate and microbial growth to occur on the needles.

For the microbiological analyses, 25 g of needles from each twig were cut off with sterile scissors and mixed with 225 mL distilled water for 2 min (so as to remove microorganisms attached to the surface of the needles without destroying the needles). Immediately afterwards the samples were logarithmically diluted with quarter-strength Ringer's solution and analyzed by spread plating. For growing aerobic heterotrophic bacteria, a Standard II nutrient agar (Merck) was used, supplemented with 0.4 g/L Cycloheximide to inhibit growth of fungi. The pH of the medium was set to 6.5. For yeast and filamentous fungi, Sabouraud-1% dex- trose-1% maltose agar (Merck) was used, with Chlor- amphenicol (Berlin-Chemie, Berlin, Germany) added at 0.4 g/L to suppress bacterial growth. The medium for these microorganisms was adjusted to pH 5.5. All plates were incubated for 5 d at 250C.

Collection of throughfall, soil solution, and needle leachates

In 1996 throughfall from five infested Norway spruce and five uninfested controls was collected in polyethylene rain samplers (diameter = 20 cm, sample volume = 5 L) placed underneath the trees with three twigs above each sampler. Throughfall solutions were collected weekly (during peak aphid abundance) and biweekly (every other week) after aphid populations declined. At each sampling date the number of aphids on 1- and 2-yr-old shoots above the samplers was recorded. This aphid density was assumed to remain constant until the next sample was taken.

Next to each rain sampler a zero-tension lysimeter was gently installed directly beneath the organic layer in order to compare the input to the mineral soil horizon under infested and uninfested trees. Each lysimeter consisted of a polyethylene pot (diameter = 16 cm), the bottom of which sloped so that the solution was collected gravimetrically. This bottom part was con- nected with a polyethylene tube to a polyethylene bot- tle, where the solution was stored. The lysimeter was covered with a polyethylene net (mesh size =1 mm) that prevented organic material from dropping into the solution, but allowed the passage of the soil solution. The soil solutions were collected on the same dates as the throughfall solutions.

To analyze the effect of honeydew on needle leaching, 15 infested and uninfested shoots (1 and 2 yr old) were collected from Norway spruce at the study site at the end of June and July and at the beginning of September. The cut surfaces of the shoots were sealed with Parafilm to prevent contamination of the needle surfaces with xylem sap, and the shoots were trans- ferred to a cooled box for transportation to the laboratory.

Sample preparation and chemical analysis

All field samples (throughfall, soil solution) were filtered (0.45 Vlm, cellulose-acetate membrane filters, Sartorius) within 24 h of collection and stored at 20C. Chemical analysis was carried out within 5 d, or samples were frozen to prevent them from oxidizing and degrading.

Needle leachates were determined within 6 h of collection by weighing and transferring the needles to a polyethylene bag to which distilled H20 was added. The leaching volume depended on the wet mass of each twig; 5 mL of distilled H20 was added per gram of twig. Each bag was tied 2 cm above the cut end of a twig. The leaching period was 60 min at room temperature, and the bags were turned over every 15 min in order to moisten the needles repeatedly. At the end of the leaching period the twigs were removed and the leachates filtered (0.45 [lm) immediately.

DOC was determined as CO2 after persulfate UV oxidation using a DOC analyzer, liqui TOC (Foss Haer-




TABLE 1. Intrinsic rate of increase (r, ) of C. pruinosa in three consecutive generations (GI, G2, G3) either on high- or low-quality Norway spruce trees and at different developmental stages (bud burst, shoot extension, end of shoot growth).

Greenhouse Field

Attribute GI G2 G3 GI G2 G3

High-quality treatment n 9 9 8 5 5 5 Shoot growth (cm) -4.5 3.5 1.0 3.0 7.5 2.0 r,, (mean t 95% cI)t 0.19 ? 0.01 0.15 ? 0.01 0.12 ? 0.02 0.15 ? 0.01 0.13 + 0.01 0.13 ? 0.01

NS ** ** NS ** **

Low-quality treatment n 9 5 5 5 5 5 Shoot growth (cm) 1.0 1.0 0.5 1.0 1.5 0.5 r,,, (mean ? 95% cI)t 0.16 ? 0.02 0.07 + 0.04 0.07 +? 0.02 0.12 ? 0.03 0.09 + 0.01 0.08 ? 0.01 ** P < 0.01. t 95% confidence intervals (ci) were calculated with the jackknife procedure.

eus, Hanau, Germany). Hexose-C was measured col- orimetrically by the anthrone method (Jermyn 1975) at a wavelength of 630 nm.

Calculation of honeydew and concentrations of throughfall and soil solution

The average dry mass of honeydew excreted per aphid per day was estimated by collecting honeydew from colonies of C. pilicornis and C. pruinosa and dividing the amount of honeydew collected by the total number of aphids comprising each colony. In this way we calculated the amount of honeydew excreted by any member of a colony at 10C under field conditions both at bud burst and at the end of shoot growth (Table 2). Using data from colonies was considered more accurate than integrating larval instars and adult aphids because the former method includes the effects of any interactions between aphids (if present) (Way and Cammell 1970). To calculate the amount of honeydew excreted on infested trees between June and August during 1994-1996, the mean number of infested twigs per tree and the mean colony sizes during that period were used.

Total fluxes of DOC and hexose-C in throughfall and soil solutions were measured on the experimental trees. The total volume of water collected in the throughfall samplers was used to calculate DOC and hexose-C fluxes, measured in milligrams per square meter per 6-wk period. Measurements were made over the period of aphid abundance, from the end of May to mid-July, when the most honeydew was present in the phyllosphere.

Statistical procedures

The intrinsic rate of increase (rm) for each aphid generation on plants in each treatment was calculated using the Lotka-Euler equation

E mJle-= 1

where lx age-specific survival rate and mx = age- specific reproduction. The 95% confidence intervals were determined using a jackknife method (Tukey 1958, Meyer et al. 1986). For calculating statistical

differences between rm values of aphids feeding on plants of different qualities, we followed Sachs (1984). Otherwise, we compared differences between treatment means using procedures in Sokal and Rohlf (1995).

RESULTS

Effects of plant quality and temperature on aphid life history

In Table 1 the rm values and length of shoot growth (an indicator of plant developmental state) are given for two treatments. In the greenhouse, rm values were highest at the time of bud burst and then declined. On low-quality plants, the highest values were also recorded for the first generation of aphids on actively growing buds. Statistically significant differences between r1, values for aphids feeding on high- and low- quality plants were only observed in the second and third generations (both greenhouse and field treatments), indicating that the decline in host quality oc- curs more quickly on seedlings that had a low nutritional supply. In the field the effect of deteriorating plant quality, associated with the endogenic cycle of the host plant, was alleviated by the higher temperatures prevailing in summer. Therefore, the main reason for the lack of any pronounced seasonal decline in fitness in the field is temperature, because aphids from the third generation started to reproduce one week earlier than aphids from the first two generations. How- ever, aphids feeding on low-quality plants had significantly lower rin values than those feeding on high- quality plants in generations two and three. Therefore, it appears that the population dynamics of Cinarids and ultimately honeydew production will be affected most severely by plant quality (nutritional supply of the host tree), and by temperature, which blurred the endogenic seasonal change in host plant quality.

Honeydew production

The amount of honeydew produced by an aphid is dependent on species, instar, plant growth stage, and temperature (Table 2). Adult aphids may excrete 10




TABLE 2. Honeydew production by the various instars (L1-L4) and adults feeding isolated or in colonies of two species of Cinara on Norway spruce. Data are separated for the time at bud burst and end of shoot growth and for different temperatures. Results are expressed as milligrams dry mass excreted per aphid per day (means ? 1 SD). P values indicate the level of significance of the differences between the excreta produced by aphids on the two plant developmental stages (Mann- Whitney U statistic); NS P > 0.05.

Developmental Bud burst End of shoot growth stage!

Species colony Excreta n Excreta n P

Cinara pruinosa (220C) LI 0.07 + 0.06 5 0.12t ? 0.05 6 NS L2 0.II+t 0.06 6 0.17t t 0.05 6 NS L3 .OIt ? 0.09 9 0.20t ? 0.07 6 0.036 L4 0.13t ? 0.06 3 0.42t ? 0.13 6 0.024 adult 0.43t ? 0.04 6 0.61t ? 0.14 10 0.011

Cinara pilicornis (22?C) LI 0.06t ? 0.07 7 0.08T + 0.05 6 NS L2 0.II+t 0.03 6 0.22t + 0.06 6 0.004 L3 0.16t ? 0.09 10 0.27T ? 0.02 5 0.013 L4 0.37t + 0.05 5 0.53t + 0.11 5 0.016 adult 0.66t ? 0.12 7 0.97t ? 0.18 6 0.008

Cinara pruinosa (100C) adult 0.19t ? 0.06 5 0.23t ? 0.07 5 0.003 colony 0.12t _ 0.05 135 0.13t _ 0.06 196 NS

Cinara pilicornis (100C) adult 0.20t _ 0.10 6 0.27T _ 0.15 5 0.020 colony 0.13t ? 0.07 271 0.16t ? 0.34 98 0.043

Cinara pilicornis (field min./max.) adult 0.41t _ 0.18 8 0.58t + 0.13 12 0.015 (9.5--25.8?C) colony 0.19t + 0.12 830 0.20t ? 0.13 719 NS

Notes: "Bud burst" marks the beginning of the shoot elongation period; "end of shoot growth" marks the end of the shoot growth period.

t Aphids were feeding on shoots developed in the previous year. T Aphids were feeding on shoots of the current year.

times more honeydew than first-instar larvae. However, early instars excrete more honeydew per unit body mass than do older instar or adult aphids. The amount of honeydew excreted was significantly influenced by the developmental stage of the host. First and second instars of C. pruinosa feeding on shoots that had ceased growing excreted similar amounts of honeydew to L3 and L4 instars feeding on the shoots at time of bud burst. Cinara pilicornis, which changes its feeding site from the shoots of the previous year to newly devel- oping shoots, showed a similar trend and excreted at the highest rate at the end of shoot elongation. Thus, although aphids were smaller after plant growth ceased, they produced larger quantities of honeydew both in absolute and relative terms (per unit body mass). Adults reared at 100C excreted less honeydew than did aphids reared at 22TC. Growing colonies consisted mainly of young aphids, and the quantity of honeydew excreted by these colonies reflected the proportion of young aphids in a colony. However, if the competitive abilities of different instars are affected during colony growth it is possible that feeding within a colony may stimulate or reduce the phloem uptake and excretion of different aphid growth stages, and thus within-colony feeding rates may differ quantitatively from those recorded for isolated aphids. As a workable value, the grand mean of honeydew produced is 0.165 mg honeydew per aphid per day (dry mass) (n = 28). This value averages the amount of honeydew excreted by any aphid feeding in a colony in the field irrespective of its age, the temperature, species, or the plant developmental stage. In the field the average fresh mass of an individual from a growing colony ranged from 1.1 0.7 mg (n = 830)

in spring to 0.6 ? 0.2 mg in summer (n = 2045 individuals; mean ? 1 SD), with the largest proportion of individuals belonging to the first and second instars. Thus, the amount of honeydew produced during the lifetime of an aphid usually will greatly exceed its biomass and may amount to as much as 20 mg dry mass during its entire lifetime.

Population dynamics of Cinara spp. on Norway spruce

The population dynamics of Cinara spp., expressed as the proportion of infested trees and of infested twigs per tree, typically showed a single peak in June-July with 80-100% of all trees and 70-80% of all twigs of infested trees colonized (Fig. 2a). A critical parameter influencing aphid population development is the number of eggs hatching in spring and colonization by alates in June. In 1994 eggs were found on >30% of trees (Fig. 2a) and the aphids became very abundant, whereas in the following years only 2-3% of all trees were infested with eggs, which delayed population increase. The high infestation rates (100%) in 1995 and 1996 resulted from a massive colonization by alates. Aphid populations declined at the beginning of July as a result of three factors: (1) heavy predation by Coc- cinellids, Chrysopids, and Syrphids; (2) dispersal; and (3) deterioration in plant quality associated with host plant development, which caused a decrease in the rates of reproduction and survival of the aphids (see Aphid life history, above, for details).

Despite the fairly constant incidence in the percentage of trees or twigs infested during 1994-1996, the number of aphids in a colony varied considerably (Fig.




a 1994 1995 1996

100 l - 100

80[- A - 80 60 14 -60

40 - 4

20 --20 SO i 0L9

AMJJASON AMJJASON AMJJASON

.29 300 -

b 4 250 -

1994 200-

2 150 -

U 100 _ 0 ~~~~~~~~1995

50 -

April May June July August September October

FIG. 2. (a) Mean percentage of trees (dashed line) and twigs (solid line) of Norway spruce infested with Cinara spp. at the study site from 1994 to 1996. The black diamond rep- resents the proportion of trees with eggs. (b) Mean colony size of aphids infesting twigs of Norway spruce from 1994 to 1996.

2b). In 1994, aphid population density peaked in mid- June with a mean of >250 individuals per colony. Most likely this was a result of the high numbers of eggs in that year (see Fig. 2a). In 1995 and 1996 a mean of only 70 individuals was found per infested twig. How- ever, for ecosystem processes a measurement other than the mean colony size is needed. The relative frequency of size classes during 1994-1996 at the time of highest aphid abundance (usually from mid-June to the end of June) is shown in Fig. 3. In 1994, colony size classes were almost evenly distributed, with the largest colonies (comprising thousands of individuals) often cov- ering large areas of the twigs. In 1995 and 1996 most

colonies consisted of <50 individuals; however, on some twigs and trees aphids formed large colonies ("hot spots").

From the population dynamics of aphids we can infer the amount of honeydew produced on infested trees (Fig. 2a, b; Table 2) for any period of time and for any degree of infestation. Over a period of 60 d the excreta (dry mass) on 10-15-yr-old Norway spruce accumu- lated to 66.8 g in 1994, 28.5 g in 1995, and 32.1 g in 1996.

Microorganisms as consumers of honeydew

Microorganisms on the needles of Norway spruce benefited from the presence of honeydew. Significantly more bacteria, yeast, and molds (expressed as number of colony-forming units) were found at the beginning of July (Fig. 4), when aphids were most abundant in 1995 (see Fig. 2b), but not in May, a time of low aphid abundance. In September, yeast and molds were still more abundant on aphid-infested twigs than on control twigs without aphids.

Throughfall chemistry and needle leachates

The relationship between aphid density and DOC/ hexose-C concentrations in throughfall solutions is shown in Fig. 5. For both organic C fractions the correlation is significant (rDOC = 0.728, P < 0.0001, n = 30; rhexose-c = 0.596, P < 0.001, n = 30). The variation in concentrations increased with growing aphid density, which might reflect the difficulty of dissolving and collecting excreta in throughfall from large colonies in the rain samplers.

Seasonal changes were observed in the concentrations of carbon compounds in throughfall collected from beneath infested and uninfested trees (Fig. 6). At the end of June, when aphids were most abundant, the highest concentrations of DOC and hexose-C occurred in throughfall from infested trees. The concentrations of DOC and hexose-C in throughfall declined along with the decline in aphid density. Mean concentrations

70 -

60-

50-

40- FIG. 3. Relative frequency of colony size |

classes of Cinara spp. at the time of peak abun- 0 30 - dance in 1994 (solid columns), 1995 (shaded ; columns), and 1996 (open columns). a 20

10

0 . I 1-50 51-100 101-150 151-200 201-250 251-300 >300

Colony size classes




bacteria yeast molds

1000xx * II

*, 10Ox 10

FIG. 4. Number of colony-forming units per t lox 10* gram fresh mass of needles. Samples originated e

from 1- and 2-yr-old twigs of Norway spruce uninfested (open columns) or infested with Cin- 1 x l0 . ara spp. (shaded columns). Sample dates: 1, 9 29

0

U 0.1 X104*

0.01 X 10-4 1 2 3 1 2 3 1 2 3

Sampling dates

in the throughfall collected from uninfested trees ranged from 4.0 to 7.2 mg/L of DOC, while hexose-C was often undetectable. For 1996, mean DOC and hexose-C throughfall fluxes over 6 wk were 2.4 g DOC/ m2 and 1.2 g hexose-C/m2 from infested trees, vs. 1.3 g DOC/m2 and 0.6 g hexose-C/m2 from uninfested trees. Thus, fluxes of organic carbon through the twigs above each sampler were about twice as high on infested compared to uninfested trees.

Because of low volumes in the needle leachates, the chemical analyses were restricted to hexose-C. How- ever, previous analyses showed that roughly 60% of the organic carbon in aphid honeydew consisted of sugars. Needle leachates showed a significant correlation with aphid density at the end of June (Fig. 7, r = 0.704, n = 29, P < 0.0001). That is, the leachate from shoots that were infested with aphids contained more sugar than did uninfested controls. There was no seasonal trend in the sugar content of the leachates from unin-

50 -

40 -

0 -E 30 -

30 -0~~~~~~~~~~~~~ 20 -

U *U

10 '

0''; 0 0 8 ? 0 0 0

0 100 200 300 400 500

Aphid density

FIG. 5. Relationship between aphid density and DOC (black squares) and hexose-C (open circles) concentrations in throughfall samples collected under infested Norway spruce.

fested controls, with values ranging from 0.2 to 1.3 mg hexose-C/L.

Soil solution chemistry

Concentrations of DOC and hexose-C in soil solutions are given in Table 3. There were no statistically significant differences in the concentrations of DOC

40 a

30 -

20 T

10 I

~b0 D 40 b u

30

20

10

25 2 9 23 6 20 Jun Jul Jul Jul Aug Aug

FIG. 6. Seasonal change in the concentrations of DOC (black squares) and hexose-C (open circles) in throughfall collected from (a) aphid-infested and (b) uninfested Norway spruce in 1996 (means ? 1 SE).




400

300

-) 200

o

X 100 0@

0.-~~~~~~~- ~ 0 100 200 300 400

Aphid density

FIG. 7. Hexose-C in needle leachates collected from infested (filled circles) and uninfested (open circles) Norway spruce in relation to the number of aphids on 1- and 2-yr-old shoots. Leachates from uninfested shoots often did not con- tain any hexose-C.

and hexose-C between soil solutions collected under infested and uninfested Norway spruce. At the end of June and during the beginning of July only small quantities of rain reached the lysimeters, which limited any comparison between trees. It is likely that the sugars that reached the soil in throughfall were metabolized by microorganisms of the rhizosphere.

DISCUSSION

We need to understand the ecology of individuals within ecosystems in order to understand patterns in the processes that produce them (Levin 1992, Grimm 1995). However, combining the results of investigations on different scales ranging from the individual to the ecosystem scale has proved notoriously difficult. This study is an attempt to carry out a cross-scale investigation and aims to identify the information that needs to be passed from the fine scale to the broad scale.

Aphid ecology

The interaction between aphids and their host plants showed that the fitness of aphids is dependent on the quality and developmental stage of their host plant, and on the temperature prevailing during reproduction (Ta- ble 1). Aphids are very sensitive to changes in host plant quality, as shown in the greenhouse treatment,

where the nutritional supply to the plant and its stage of development influenced the rm values. In the field, however, temperature trends counteracted those in the endogenic cycle of host plant quality. Thus, temperature and the nutritional status of the host plant are the most important parameters determining the abundance of aphids and ultimately the availability of honeydew.

Honeydew production is dependent on aphid age, plant developmental stage, and temperature. The average amount of honeydew produced by aphids on a 10-15-yr-old tree ranged from 28 to 67 g dry mass during 1994-1996. For 70-80-yr-old trees, substantially larger amounts of honeydew were recorded for Cinarids, with a total of 400-700 kg fresh mass-ha-1lyr-1 (ZwOlfer 1952, Zoebelein 1954, Eckloff 1972). Muller (1956) reports 30-60 kg honeydew tree-1-yr-1 when conditions are favorable. How- ever, the study site is comparatively cold, with the growing period at least 3-4 wk shorter than that of forest sites at lower elevations.

The population dynamics of the Cinarids at the study site reflects their reproductive biology in terms of population growth rate, which is highest in June, when their host plants are actively growing. The rapid decline in the number of infested trees and of colony size during July-August can be explained in terms of deteriorating plant quality (end of shoot extension stage) and a subsequently stronger effect of natural enemies, because aphids were unable to compensate for losses on hosts of low quality (Stadler 1997). Tree-induced changes in nymphal mortality are also assumed to be important factors affecting population growth, e.g., that of Cinara pinea (Mordv.) on pine (Kidd 1985, Kidd et al. 1990). When analyzing ecosystem effects it is important to recognize that aphid populations are initially clustered in patches on several trees, but that after mi- gration almost all trees and many of their twigs are infested with aphids, thus forming an almost uniform distribution. Locally this might produce very large amounts of honeydew and subsequent flows of nutrients in the phyllosphere, especially during springtime. Our investigation were restricted to trees that were moderately infested by aphids (as were most trees), but the data enable the calculation of the amounts of honeydew excreted for any degree of infestation. Differ-

TABLE 3. Concentrations of DOC and hexose-C (mg/L) in soil solutions collected under aphid-infested and uninfested Norway spruce (means + 1 SD). Values in parentheses indicate the number of samples collected on a particular date. Because of low precipitation no soil solutions could be collected in certain periods. No pair of trees differed significantly in DOC or hexose-C concentrations at any sampling date.

25 June 2 July 9 July 23 July 6 August 20 August

DOC Infested 26.6 (1) 21.3 + 10.4 (3) 17.2 + 5.6 (4) 12.3 + 2.2 (3) 14.5 + 6.9 (4) 12.9 + 2.6 (4) Control (0) 25.6 (2) 8.9 1 3.5 (5) 9.6 1 2.0 (3) 11.9 + 3.7 (5) 11.4 + 6.0 (5)

Hexose-C Infested 1.1 (1) 1.4 1 1.4 (3) 0.5 10.3 (4) 0.1 10.0 (3) 0.2 10.1 (4) 0.3 10.1 (4) Control (0) 0.6 (2) 0.2 + 0.4 (5) 0.1 1 0.1 (3) 0.4 1 0.2 (5) 0.4 + 0.2 (5)




ences in aphid numbers between successive years can also be substantial and thus influence carbon availability.

Honeydew is known to be consumed by >250 different species of insects (Zoebelein 1956), and microorganisms in the phyllosphere substantially benefit from the presence of honeydew, which can result in an increase of two to three orders of magnitude in their population densities (Fig. 4). Because such microorganisms are able to metabolize inorganic nitrogen sources from atmospheric deposition (Stadler and Muller 1996), they could substantially influence nutrient cycles. Aphid honeydew is also known to enhance the growth of soil microorganisms (Dighton 1978), which could lead to a significant reduction in the availability of soil nitrogen, nitrogen mineralization rates, and nitrogen uptake rates, as demonstrated for Alnus rubra Bong (Grier and Vogt 1990). Therefore, flows of carbon might also affect flows of nitrogen via the activity of microorganisms.

Ecosystem processes: DOC and hexose-C concentrations in throughfall

Ecosystem parameters such as concentrations of DOC or hexose-C in throughfall are markedly affected when trees are infested with aphids. There were significant relationships between aphid numbers on trees above the throughfall samplers and the concentrations of the carbon fractions in the samplers (Fig. 5). Of the dry mass of honeydew, 40-50% is DOC. Thus, during a 6-wk infestation period, the infested trees in this study yielded 30.1 g DOC in 1994, 12.8 g in 1995, and 14.4 g in 1996. In forest ecosystems in which the annual excreta amount to 400-700 kg fresh mass/ha (Zoebel- ein 1954), 23-41 kg DOC-ha-1 yr-1 can be expected to originate from aphids. There is also a clear seasonal trend in DOC and hexose-C concentrations in the throughfall collected under infested trees (Fig. 6), dem- onstrating the importance of aphids in ecosystem processes such as fluxes of organic material through the phyllosphere. A number of studies have shown that the concentrations of DOC and other carbon compounds in throughfall range between 10 and >60 mg/L under different tree species such as maple or hemlock (Mc- Dowell and Likens 1988, Qualls et al. 1991, Guggen- berger 1992). The explanations offered unanimously favor leaf leaching. However, the seasonal variation in the DOC concentrations in throughfall collected under different tree species indicates the need to consider further sources such as aphids and their excreta. There are several species of aphids on maple that diapause in summer and resume reproduction in autumn (Dixon 1985), which could account for the increase in DOC in throughfall collected in June and October by Mc- Dowell and Likens (1988). The energy and nutrient drain of Drepanosiphum plantanoides (Schr.) feeding on Acer pseudoplantanus (L.) may reduce leaf size by 42% and wood formation by up to 62% (Dixon 197 la).

Eucallipterus tiliae (L.) feeding on Tilia vulgaris Hayne may excrete up to 50 kg dry mass of honeydew per tree per year (Heimbach 1986), and infested leaves are shed earlier and with higher nitrogen contents than uninfested leaves (Dixon 1971b). Thus, heavy aphid infestations of trees must have profound effects on woodland ecosystems.

Needle leachates from infested twigs also showed a significant correlation between concentrations of hexose-C and aphid density, while very little hexose-C could be detected in the leachates from uninfested twigs. Thus, it seems that the large proportion of organic compounds found in throughfall is not exclusively attributable to leaf leaching, as previously claimed (McDowell and Likens 1988, Qualls et al. 1991), but might be traced back to the excreta of Ho- moptera and possibly other honeydew-producing insects such as coccids.

Similar concentrations of DOC were found in throughfall and soil solutions when aphid densities were between 100 and 200 individuals/. Based on yearly averages, Qualls et al. (1991) and Guggenberger and Zech (1993) showed that DOC concentrations in Oa horizons were about three times as high as in throughfall. However, the results presented here indicate that relatively moderate aphid infestations led to substantial increases in the carbon availability in the phyllosphere and accelerated the growth of microorganisms. In the leachates from infested shoots even larger concentrations were found, indicating that (1) honeydew is metabolized in the phyllosphere and (2) honeydew is an important source of the spatial and temporal variability in throughfall concentrations. Thus, variation in the availability of an energy-rich source is not simply a statistical detail, but a biologi- cally important quantity. Aphids and microorganisms are highly efficient in exploiting resources that are only available for a limited period of time. However, their physiological and ecological properties influence the passage of organic carbon from the phyllosphere to the soil.

To summarize, the reproductive biology of aphids determines their population dynamics, which in turn determines the amount of honeydew available in a forest stand. Honeydew is an important source of energy that fuels biotic interactions and ecosystem processes in the phyllosphere. Consequently, the spatial distribution and population dynamics of aphids on their host plants and within a habitat are important components of spatial and temporal heterogeneity in nutrient fluxes.

Conclusions

DOC and hexose-C pass from the phyllosphere to the soil. As a result, no difference was found in soil solution chemistry under infested and uninfested trees, which seems to indicate that variability at the ecological scale will average out at the ecosystem scale. How- ever, such a coarse-grained view neglects short-term




responses such as the increased growth of microorganisms, which is likely to buffer changes in the environ- ment, and in the spatial and temporal heterogeneity in throughflow fluxes. Considerable differences in the overall numbers of aphids were recorded at our site between years and trees, which is likely to affect the path of sugars. Variability is not an absolute dimension, but gains meaning relative to a particular scale of observation. A key to understanding the processes within an ecosystem is to understand how variability is produced, filtered, or reduced across different scales. Hon- eydew is a key element promoting microorganismic growth in the phyllosphere and creating interactions with insects such as ants. The availability of honeydew depended on several parameters, with temperature and plant quality possibly the most influential. The results clearly show that it is not enough to focus mainly on biomass and subsequent fluxes of material and energy, because the amount of honeydew produced by aphids exceeds their body mass by several orders of magnitude. Physiological and life history properties of individuals as well as their effects on the macroscale need to be understood. Thus, we support the view that there is no single correct scale at which to view ecosystems (Wiens 1989, Levin 1992) and no single mechanism that explains patterns at all scales. Linking the ecology of species with fluxes of energy and matter could be the key that would enable us to connect processes at different spatial and temporal scales and to evaluate their relative contribution to ecosystem behavior.

ACKNOWLEDGMENTS

We gratefully acknowledge valuable comments and sug- gestions on earlier versions of the paper by Egbert Matzner and Tony Dixon. Two anonymous reviewers substantially helped to focus the subject. Financial support was provided by the German Ministry for Research and Technology (BMBF Number PT BEO 51-0339476B).

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Linking Aphid Ecology with Nutrient Fluxes in a Coniferous Forest