Mycorrhiza (1994) 5:99-103
F. Hiol Hiol 9 R. K. Dixon 9 E. A. Curl
The feeding preference of mycophagousCollembola
varies with the ectomycorrhizal symbiont
Abstract The interactions of the collembolan insect
Proisotoma minuta with ectomycorrhizal and/or pa-
thogenic fungi was examined in three experiments: (1)
in vitro analysis of feeding patterns, (2) in vitro food
preference test, and (3) in situ analysis of ectomycorrhi-
zal colonization in relation to population density. The
ectomycorrhizal fungi Laccaria laccata, Pisolithus tinc-
torius, Suillus luteus, Thelephora terrestris and the pa-
thogenic fungi Rhizoctonia solani were employed in all
experiments. In vitro and in situ experiments revealed
that Pr. minuta consumed all the ectomycorrhizal fungi
tested but the feeding pattern and consumption varied
with each isolate. In a comparative in vitro feeding pre-
ference test, where Pr. minuta was given a choice, R.
solani was grazed more heavily than the ectomycorrhi-
zal fungi. Among the ectomycorrhizal fungi examined,
Pi. tinctorius was consumed significantly less than L.
laccata, S. luteus or T. terrestris in the presence of R.
solani. A 10-week in situ analysis of lobtolly pine (Pin-
us taeda L.) seedling root systems inoculated with Pr.
minuta revealed that ectomycorrhizal colonization was
significantly less than that of control plants (without Pr.
minuta). Collectively, these data suggest that mycopha-
gous Collembola may play a major role in the distribu-
tion and biomass of ectomycorrhizal fungi in the rhizos-
phere of tree seedlings.
Key words Laccaria laccata 9 Pisolithus tinctorius
Proisotoma minuta 9 Rhizoctonia solani 9 Suillus
luteus 9 Thelephora terrestris 9 Collembolan insects
F. Hiol Hiol (lEVI)
Department of Forestry, University of Dschang,
Dschang, Cameroon
R. K. Dixon
Office of Research and Development,
US Environment Protection Agency,
Washington, DC 20460, USA
E. A. Curl
Department of Plant Pathology and Microbiology,
Auburn University, Auburn, AL 36830, USA
9 Springer-Verlag 1994
Introduction
The microarthropods, comprised principally of the Col-
lembola (springtails) and the Acarina (mites), are the
most abundant soil-inhabiting animals after nematodes
and protozoa (Gunn and Cherrett 1993; Curl and
Truelove 1986). Several species of Collembola, includ-
ing the genera Proisotorna (Isotomidae) and Onychiu-
rus (Poduridae), occur in forest and agroecosystems
(Lagerlof and Andren 1991; Wiggins et al. 1979). These
microinsects are reportedly mycophagous, as docu-
mented by feeding habits of the insects and by mycelia
and spores found in the gut contents (Gunn and Cher-
rett 1993; Testerink 1982; Anderson and Healey 1972).
Collembolan insects when present in sufficient numbers
may play an important role in soil fungus ecology, par-
ticularly food webs (Gunn and Cherrett 1993; Lagerlof
and Andren 1991; Testerink 1982). The feeding activi-
ties of collembolan insects may affect the competitive
advantage of fungal pathogens, saprophytes and sym-
bionts at the root surface and influence their relative
efficacy (Gunn and Cherrett 1993; Wiggins and Curl
1979).
Relatively few controlled experiments have consid-
ered the interactions between Collembola and mycorr-
hizal fungi, although a number of field observations
have been recorded (Gunn and Cherrett 1993; Perry et
al. 1987). Shaw (1985) observed the grazing preferences
of Onychiurus armatus for a range of mycorrhizal and
saprophytic fungi of pine (Pinus) plantations and re-
ported some grazing of ectomycorrhizal fungi, but the
insects did not prefer Hebeloma crustiliniforme (Bull.
ex st. Amens), Paxillus involutus (Fr.) Fr., or Rhizopo-
gon luteolus Fr. The interactions between soil microar-
thropods and endomycorrhizal associations of higher
plants have also been surveyed. Finlay (1985) observed
that Collembola population densities were significantly
greater in the rhizospheres of endomycorrhizal plants
than nonmycorrhizal controls, and there was evidence
that the collembolan insects fed on hyphae of the vesic-
ular-arbuscular mycorrhizal fungi.
100
The objectives of this present work were to: 1) quan-
tify the in vitro feeding patterns of one collembolan
species, Proisotorna minuta Tullberg, on four ectomy-
corrhizal fungi, 2) determine the in vitro feeding prefer-
ence of Pr. minuta for ectomycorrhizal versus pathog-
enic fungi, and 3) characterize the ectomycorrhizal col-
onization of loblolly pine (Pinus taeda L.) seedlings
with and without Pr. minuta in the rhizosphere.
Materials and methods
The Collembola species used throughout this study, Proisotoma
rninuta, was extracted from the rhizosphere of a cultivated agroe-
cosystem in Lee County, A1., USA by the modified Tullgren ex-
traction system described by Wiggins and Curl (1979)9 The insects
were maintained and reproduced on potato dextrose agar cul-
tures of Rhizoctonia solani Kuhn (Wiggins et al. 1979)9 Four ecto-
mycorrhizal fungi, Pisolithus tinctorius (Pers.) Coker and Couch,
Suillus luteus (L.:Fr.) S.F. Gray, Telephora terrestris (Ehrh.) Fr.,
Laccaria laccata (Scop.:Fr.), a n d one pathogenic fungus Rhizoc-
tonia solani were employe d in the experiments. The source, isola-
tion date and cultural history 9f the ectomycorrhizal fungi are
9 t i '? 9
documented by Dixon et al. (1993). The isolate of R. solant was
. and Bryan (1975). The inocula were produced in a peat moss-
collected from soil in a Lee County agroecosystem and main-
tained using methods described)by Wiggins and Curl (1979). The
fungi were cultured on modified, Melin-Norkrans medium
(MMN) prior to the three Experiments (Marx 1969). Agar was
added to the MMN formulation ati fi cgncentration of 15 g/1. After
autoclaving, the pH of tl-ie agar substrate was 59149149The ecto-
mycorrhizal fungi were passed thro,ugh loblolly pine seedlings and
maintained on MMN medium prior to initiation of the experi-
ments (Marx and Bryan 1975). The in vitro cultures of the test
fungi and Pr. minuta were maintained in darkness at 28-30~ C at
> 90% relative humidity unless stated otherwise.
In vitro Collembola feeding pattern analysis
The feeding pattern(s) of Pr. minuta on petri dish cultures of four
ectomycorrhizal fungi were examined in a 5 x 4 x 2 factorial ex-
perimental design. The experiment included five replicates x four
test fungi x two Pr. minu:ta tseatments (with and without Pr. min-
uta). Mycelial discs (8 trim di~ameter) of the ectomycorrhizal fungi
on MMN were extracted from the periphery of 3-week-old cul-
tures and placed on the center surface of MMN medium in a 110-
mm petri dish. Cultures of Pr. minuta were passed over a dry
short-term funnel with an attached capillary tube that had been
calibrated volumetrically (Wiggins and Curl 1979). By this meth-
od, 300 insects were placed in petri dishes containing 2-week-old
ectomycorrhizal fungi colonies on MMN medium. Observations
were made after 1, 2 and 5 days of the experiment to determine
feeding patterns of the insects and consumption of the test fun-
gus. At each observation, the colony diameters of the test fungi
were measured and the density of the fungal hyphae was ranked
into one of four categories: 1, fungal hyphae totally consumed; 2,
up to two-thirds of hyphae consumed by grazing; 3, up to one-
third of hyphae consumed by grazing; 4, no apparent consump-
tion by grazing. The feeding patterns of Pr. rninuta on the test
fungi were also recorded with photographs.
In vitro Collembola x fungi preference test
This 5 x 3 • factorial experiment was designed to determine
which of the following ectomycorrhizae and pathogenic fungi Pr.
minuta would prefer in a controlled environment: Pi. tinctorius,
R. solani or S. luteus. Mycelial discs (8 mm diameter) from each
of the ectomycorrhizal fungi were applied to the MMN agar sur-
face 10 mm from the edge of the petri dish. Rhizoctonia solani is
very fast growing compared to the ectomycorrhizal fungi (Wig-
gins and Curl 1979). Therefore, a R. solani mycelial disc was in-
troduced to the petri dish after the ectomycorrhizal fungi had
reached an average colony diameter of 70 mm. Approximately 40
insects were then added with a calibrated capillary tube, as de-
scribed previously, in the center of the petri dish at an equal dis-
tance between the two colonies. After 1, 24 and 48 h of incuba-
tion, the insect distribution pattern in relation to test fungi was
determined by enumerating the insects on each food source and
by recording their positions in the petri dishes. The first observa-
tion was completed by examining the Pr. minuta and fungi cul-
tures under a light microscope. For the second observation (after
24 h), the petri dish cultures were cooled (0~ for 10 rain) to
deactivate the insects and then examined under a microscope.
The 48-h petri dish observation was made after killing the insects
with chloroform9
In situ analyses of Collembola grazing
Vegetative mycelial inocula of L. laccata, Pi. tinctorius, S. luteus,
and T. terrestris were produced using methods described by Marx
vermiculite matrix containing MMN solution in 2-1 jars for 14
weeks and thoroughly leached before adding to the growth me-
dium of seedling containers. The vegetative mycelial inoculum
was mixed into the growing medium at a ratio of 1 : 25 (v/v) (Marx
and Bryan 1975).
Seedlings of loblolly pine were grown in 2-1 plastic pots con-
taining a sandy loam soil using methods described by Dixon and
Hiol Hiol (1992). The 5 x 4 x 2 experimental design was a factorial
arrangement of four fungi treatments with and without the insect
Pr. minuta, replicated in five blocks on greenhouse benches. The
growth medium (soil) pH was 4.8-5.0, with a cation exchange ca-
pacity of 3.45 meg/100 g, an organic matter content of 1.5%, and
P, NO3, NH4, Fe, Mn, Zn, B, Mo and Cu contents of 6, 2, 6, 3, 1,
0.3, 0.04, 0.01 and 0.1 ppm, respectively9
The study was implemented in a glasshouse with environmen-
tal features described by Dixon and Hiol Hiol (1992). Daily pho-
toperiod and photosynthetically active radiation were 14 h and
800 ixEm 2 s 1, respectively. Ambient temperature and relative hu-
midity ranged from 22 to 32~ C and from 45 to 90%, respectively.
Seedlings received deionized water to achieve field capacity daily
and were fertilized with half-strength Hoagland nutrient solution
weekly (Hoagland and Arnon 1950). The insect Pr. minuta was
introduced to the soil surface of pots with loblolly pine seedlings
using methods described by Wiggins et al. (1979). Approximately
Pr. minuta were added to each pot. Populations of Collembola at
the time of seedling establishment were determined by the modif-
ied Tullgren method (Wiggins and Curl 1979).
The study was terminated after 10 weeks and plants were har-
vested. Seedling root and shoot weight were measured after oven
drying (75 ~ C, 72 h). Ectomycorrhizal colonization of seedling pri-
mary lateral roots was quantified using methods described by
Dixon et al. (1981). The percentage of ectomycorrhizal inocula-
tion was computed as a ratio of the colonized lateral roots to total
lateral roots (Dixon and Hiol Hiol 1992). The presence of a Har-
rig net was confirmed following microscopic examination of ecto-
mycorrhizal short roots excised from seedling lateral roots. Col-
lembola insects were extracted from a soil core sample of the see-
dling rhizosphere and enumerated to determine relative popula-
tion densities (Wiggins et al. 1979).
Where appropriate, data from the three studies were sub-
jected to analysis of variance, least significant difference test or
t-test (P=0.05) (Steel and Torrie 1980).
 101

Table 1 In vitro hyphae colony diameter (mm) of four ectomy-

Results corrhizal fungi with (+) and without ( - ) Proisotoma minuta

In vitro Collembola feeding pattern analysis Day Ectomycorrhizal fungi

Suillus Pisolithus Thelephora Laccaria
P r o i s o t o m a minuta was attracted to all the ectomycorr- luteus tinctorius terrestris laccata
hizal fungi evaluated but the feeding patterns varied
- + - + - + - +
between day 1 and 7 (Table 1). Significant differences
in the colony diameter of Pi. tinctorius and S. luteus
1 67* 66 32 33 18 18 16 16
were observed on days 2 and 5. The colony diameter 2 75* 73 40* 34 19 20 18 18
growth of all test fungi was significantly reduced by day 5 78 77 44* 38 21 22 19 19
7. Without other food choices, Pr. minuta significantly 7 81" 79 59* 45 27* 24 23* 20
reduced the colony diameter of Pi. tinctorius growing in
* Pairs of means are significantly different (P=0.05)
the petri dishes.
Grazing of the ectomycorrhizal fungi by Pr. m i n u t a
was intense but the consumption of the hyphae varied
with the isolate (Table 2). The insects grazed in an er- consumed by Pr. minuta in petri dishes containing L.
ratic, unpredictable manner but sometimes established laccata, S. luteus, and T. terrestris. Of the four test fungi,
feeding galleries within juvenile and mature hyphae the hyphal density of Pi. tinctorius was least reduced by
(Figs. 1, 2). By day 5, two-thirds of the hyphae were Pr. minuta.

Fig. 1 In vitro hyphae density

of Suillus luteus without (left)
and with (right) Proisotoma
minuta

Fig. 2 In vitro density of Lac-

carla laccata with (left) and
without (right) Pr. rninuta
102

Table 2 In vitro hyphae density of four ectomycorrhizal fungi In vitro Collembola x fungi preference test
with Pr, minuta. Hyphae density categories: 1 fungal hyphae total-
ly consumed, 2 up to two-thirds of hyphae consumed by grazing, 3
up to one-third of hyphae consumed by grazing, 4 no apparent In the feeding preference test Pr. m i n u t a initially (after
consumption by grazing, Within a row, means followed by a com- 1 h) migrated m o r e to Pi. tinctorius and S. luteus than
mon letter are not significantly different (P=0.05) to R. solani (Table 3). As the ectomycorrhizal fungi
were partially grazed after 24 h, Pr. m i n u t a increasingly
Day E~omycorrhizalNngi migrated to R. solani. A f t e r 24 h, the insects preferred
S.~Wus Pi, nncmrius ~terrestr~ L.~ccam R. solani over Pi. tinctorius. The R. solani was com-
pletely c o n s u m e d after 48 h (Table 4). In contrast, large
1 3b 4a 3b 3b patches of Pi. tinctorius and S. luteus hyphae r e m a i n e d
2 3a 3a 3a 3a in the petri dishes after 48 h.
5 2b 3a 2b 2b
7 2b 3a 2b 2b
In situ analyses of Collembola grazing

T h e loblolly pine seedlings were uniform in biomass

Table 3 Percentage of Pr. minuta (% of the total number intro- (300 + 15 rag) and were colonized by the ectomycorrhi-
duced) on three combinations of fungi colonies and in the center
of the petri dish at three observation periods. Within a fungi zal fungi introduced into the soil culture. Seedlings in
treatment and sample time, row means followed by a common the absence of Pr. m i n u t a developed adequate ectomy-
letter are not significantly different (P=0.05). Sl S. luteus, Pt Pi. corrhizal associations after 10 weeks (Table 5). The in-
tinctorius, Rs Rhizoctonia solani, C center of dish) troduction of Pr. m i n u t a into the loblolly pine pot cul-
Time Ectomycorrhizal fungi ture significantly reduced ectomycorrhizat colonization
(h) by L. laccata and T. terrestris relative to the control
S1+ Pt S1+ Rs Pt + Rs plants without Pr. minuta. T h e population of Pr. m i n u t a
at harvest (after 10 weeks) was low relative to the num-
SI Pt C S1 Rs C Pt Rs C ber of insects introduced. The fate of the insects, pre-
1 50a 5 c 15b 43a 27b 30b 49a 34b 17c s u m e d dead, could not be discerned f r o m the soil sam-
24 80a i c 19b 36b 60a 4b lb 94a 5b pies.
48 100 a 0 b 0 b 0 0 0a 0 0 0"
a All fungal hyphae were consumed after 48 h and Pr. minuta
were distributed randomly Discussion

P r o i s o t o m a m i n u t a grazed all of the ectomycorrhizal

Table 4 In vitro hyphae density of three combinations of fungi fungi tested, but the preference, pattern and a m o u n t of
colonies at three observation periods. Hyphae density categories hyphae consumed varied significantly in vitro and in
as in Table 2. Abbreviations as in Table 3 situ. The m y c o p h a g o u s activity of Pr. rninuta was ob-
Time (h) Ectomycorrhizal fungi served earlier in soils of forest ( G u n n and Cherrett
1993; Finlay 1985; Shaw 1985) and agroecosystems (La-
S1+ Pt S1+ Rs Pt + Rs gerlof and A n d r e n 1991; Curl et al. 1985; Wiggins et al.
1979). Because Collembola consumes a wide diversity
S1 Pt SI Rs Pt Rs
of food, these insects are sometimes referred to as un-
1 3 4* 3 3 3 3 specialized feeders. H o w e v e r , as observed in this ex-
24 3* 2 2 2 2 3* periment, Pr. m i n u t a can exhibit a feeding preference
48 3* 2 2* 1 2* 1 for selected fungi. Curl (1979) found that Pr. m i n u t a
* Means within a fungat pair and time period are significantly dif- preferred R solani over T r i c h o d e r m a species in a feed-
ferent (P=0,05) ing experiment. Wiggins and Curl (1979) d e m o n s t r a t e d

Table 5 In situ ectomycorrhizal colonization by four test fungi minuta, + with Pr. minuta. Means within a test fungus (row) fol-
and Pr. rninuta population density in the rhizosphere of loblolly lowed by a common letter are not significantly different
pine seedlings after 10 weeks in a greenhouse. - Without Pr. (P =0.05)
Ectomycorrhizal fungi
L. laccata Pi. tinctorius S. luteus T. terrestris
-- + -- + -- + -- +

Ectomycorrhizal roots (%) 37 a 22 b 41 a 30 b 19 a 16 a 47 a 16 b

Proisotoma minuta population/1 soil 8a 10 a 12 a 9a 14 a 7b 6a 9a

that two coUembolan species, Onychiurus encarpatus
Denis and Pr. minuta consumed more Fusarium oxy-
sporum f. relative to cultures of Aspergillus, Penicil-
lium, Pythiurn and Trichoderma, indicating that the lat-
ter were not preferred.
Feeding preferences observed in this study may be
attributable to the morphology or texture of the fungi
tested. However, the hyphae morphology (e.g., diam-
eter) of the ectomycorrhizal and pathogenic fungi
tested in vitro were similar at a given age. It has been
observed that Collembola prefer juvenile over mature
fungal hyphae (Wiggins and Curl 1979; Anderson and
Healey 1972). The feeding galleries observed in the in
vitro experiments tend not to support this hypothesis,
as both mature and juvenile hyphae were consumed in
large sections or "galleries" of the hyphal mats. Pr.
minuta did not prefer juvenile or mature mycelium of
Pi. tinctorius or S. luteus to a lesser degree when given
other choices of food, suggesting other factors in-
fluenced feeding patterns of the insects.
In this study, Pr. minuta fed on Pi. tinctorius, but the
insects did not especially prefer this fungus when
placed in a petri dish along with S. luteus or R. solani.
Moreover, in situ experiments revealed that ectomy-
corrhizal Pi. tinctorius was grazed less than L. laccata,
S. luteus or T. terrestris in pot cultures of loblolly pine.
This consistent food preference response in two con-
trasting environments, together with the observation
that fungal hyphae morphology did not significantly in-
fluence grazing patterns, suggests selected fungi may
have biochemical or metabolic features that influence
feeding preferences by soil insects such as Pr. minuta.
Pi. tinctorius has biochemical features that deter pa-
thogenic fungi (Marx 1972; Marx 1969) and this fungus
may have similar metabolic attributes that deter the in-
sects ( G u n n and Cherrett 1993; Lagerlof and A n d r e n
1991; Tan et al. 1978). The presence of another fungus
(S. luteus or R. solani) along with Pi. tinctorius may in-
duce biochemical features that repel the insects (Lager-
lof and Andren 1991; Harley and Smith 1983).
In situ ectomycorrhizal colonization of loblolly pine
was reduced by Pr. minuta in this study. However, ecto-
mycorrhizal colonization can only be considered an in-
direct measure of Collembola feeding activity, as the
total volume of extramatrical fungi relative to soil vol-
ume was not measured or computed in this analysis.
More elaborate experimental methods are n e e d e d to
observe and quantify the in situ role of Collembola in
the mycorrhizal relations of woody plants. Collectively,
the in situ and in vitro observations in the three experi-
ments of this study, together with the field and labora-
tory observations of others ( G u n n and Cherrett 1993;
Lagerlof and A n d r e n 1991; Shaw 1985), suggest Pr.
minuta and other springtails may play a major role in
the ecology of ectomycorrhizal fungi.
Acknowledgement This research was supported by the Came-
roon Forestry Education Project, which is sponsored by the US
Agency for International Development.
103
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