Spiders (Araneae) in ground covers of pistachio orchards in
South Africa
C R Haddad1*, S vd M Louw1 & A S Dippenaar-Schoeman2
1
Department of Zoology and Entomology, University of the Free State, PO Box 339, Bloemfontein, 9300 South Africa
2
Biosystematics: Arachnology, ARC-Plant Protection Research Institute, Private Bag X134, Queenswood,
0121 South Africa, and Department of Zoology and Entomology, University of Pretoria,
Pretoria, 0002 South Africa
Haddad C R, Louw S vd M & Dippenaar-Schoeman A S 2004. Spiders (Araneae) in ground covers of pistachio
orchards in South Africa. African Plant Protection 10(2): 97–107.
As part of a larger study of arthropod diversity in pistachio orchards under IPM practices in South Africa, spiders
(Araneae) living on ground cover plants were surveyed in two orchards (GVN 1 and GVN 19) at the Green Valley
Nuts Estate and an orchard on the farm Remhoogte (REM) in the Prieska district, Northern Cape Province. Spiders
were sampled from three different ground cover regimes in the orchards to determine their diversity, relative
abundance and prey items of the numerically dominant species. Sampling was undertaken using a sweep net, with
200 sweeps per orchard per month, in July 2001, September 2001 to April 2002, and July 2002. In total, 1760
spiders representing 55 species were collected in the three orchards. Total spider numbers and diversity were
highest at GVN 1 (n = 631, 40 spp.), followed by REM (n = 580, 36 spp.) and GVN 19 (n = 549, 35 spp.). Two species,
Peucetia viridis (Blackwall) and Heliophanus pistaciae Wesolowska, dominated the spider fauna, accounting for
29.3 % and 23.4 % of the total, respectively. Plant composition and orchard age had a significant effect on the
abundance of spiders, but a minimal influence on diversity. Predation events observed in the field for nine common
spider species showed that they preyed on nine orders of insects, including various minor pests. The presence of
spiders in the ground covers may play a role in suppressing populations of minor pests before they reach damaging
levels in pistachio trees.
Key words: Araneae, ground covers, orchards, pistachio, predation, South Africa, spiders.
Ground covers comprise an important structural
component in many orchard ecosystems, influencing natural enemy populations by increasing
overall habitat complexity, providing alternative
food for predators and serving as trap crops for
herbivores with pest potential (Cortesero et al.
2000). All three factors can positively influence
the survival and consequent pest management
effects of natural enemy populations on pest
organisms infesting the main crop.
Ground covers have been shown to increase the
biological control effects on pest populations in
orchards (Bugg & Waddington 1994; Wyss et al.
1995; Brown et al. 1997a). Like field margins, they
also play an important role as overwintering sites
for various natural enemies, ensuring the survival
of the species until the next season when the
agroecosystem can be recolonised (Dennis & Fry
1992; Dennis et al. 1994; Thomas & Marshall
1999). However, they need to be carefully selected
as their composition may influence herbivore
and predator populations in this vegetation, and in
the tree canopies above (Bugg & Dutcher 1989;
Bugg et al. 1991; Kaakeh & Dutcher 1993; Smith
et al. 1994; Rieux et al. 1999). While cover crops
*Author for correspondence: E-mail: haddadcr.sci@mail.uovs.ac.za
and other floor vegetation can play a role in pest
management, they cannot be relied upon to
provide complete control of pests on the main crop
(Costello & Daane 1998a).
Spiders are often the most abundant predators
in various orchard ecosystems (Carroll 1980; Liao
et al. 1984; Nyffeler & Benz 1987; Knight et al.
1997; Costello & Daane 1999), forming an essential
part of the natural enemy complex. They can play
an important role in the natural suppression of pest
organisms, both on the main crop and in ground
covers. Spiders have attributes related to pest
mortality not often encountered in other natural
enemy groups such as parasitoids, e.g. wasteful
killing (unpalatable prey that are killed without
feeding taking place), disturbance effects, positive
responses to high prey densities, and the mortality
of non-consumed pests in webs (Mansour et al.
1981; Samu & Bíró 1993; Riechert 1999; Sunderland 1999; Haddad et al. 2004). In addition, the
different lifestyles or guilds of spiders ensure that a
particular prey species may be captured by different methods (Marc & Canard 1997) and in various
strata of the agroecosystem, a characteristic of
ecosystem functioning known as resource-use
complementarity (Wilby & Thomas 2002). All
life-stages of spiders are predacious and can
98
African Plant Protection vol. 10, no. 2, August 2004
Table 1. Ground cover parameters in three pistachio orchards in the Prieska district, Northern Cape Province, at the
start of the survey in July 2001.
Parameter
GVN 1
GVN 19
REM
Orchard age (years)
Orchard size (ha)
Ground cover characteristics
8
16
Mixed herbs, weeds and
few grasses
Moderately dense
Weeds
5
16
Alternate rows of weeds
and grasses
Low
Equal distribution
9
1.5
Mixed herbs and
grasses, few weeds
Dense
Herbs
Vegetation density
Dominant vegetation
impact on pest populations. Many insect predators
are only carnivorous in one life-stage (e.g. larval
lacewings), and with their restricted movement,
are more strongly influenced by prey density,
patch restriction and cannibalism (Kindlmann &
Dixon 1999). Furthermore, spiders are able to
balloon to more suitable feeding sites if prey densities become too low. The most promising option for
utilising the particular predatory nature of spiders
for the biological control of pests is to increase
their density in crops as close to the pest density
as possible (Sunderland & Samu 2000). Smith et
al. (1996) suggested that a high density of spiders
in the ground cover layer often indicates that they
are important predators in the orchard canopy.
Basic faunistic surveys are essential for determining agrobiont species in agroecosystems for
further focused study, as these species are likely
to have the greatest impact on pest populations by
virtue of their abundance in the agroecosystems,
and may also serve as bioindicators of pesticide
residue effects in the ground covers of the crop.
The aim of this study, the first of its kind in South
Africa, was to determine the diversity and abundance of spider species in ground covers of
pistachio (Pistacia vera L.) orchards, seasonal
fluctuations in spider populations, the role of
spiders as predators in this layer, and the effect of
ground cover selection on arboreal populations.
Materials and methods
Study area and period
The study took place in pistachio orchards on
two farms in the Prieska district in the Northern
Cape Province, South Africa. Sampling was done
in two orchards at Green Valley Nuts Estate (GVN,
29.35.18S, 22.56.68E), and an orchard at the farm
Remhoogte (REM, 29.31.92S, 23.00.10E). All
three orchards are managed according to IPM
practices, and the only insecticides applied to the
trees during the study period were endosulfan in
December and parathion in April for the control of
stink-bugs and other hemipterans. Benomyl was
applied to control fungal pathogens in trees, and
glyphosate was applied in the orchard rows to
restrict weed encroachment on the pistachio
trees. The natural vegetation in the area is classified as Orange River Nama Karoo (Hoffman
1996). Orchard parameters and ground cover
composition of the three sampling sites are given
in Table 1.
The spiders inhabiting ground covers in pistachio orchards were studied monthly from July
2001 to July 2002, but no sampling was undertaken in August 2001 and May and June 2002. The
ground covers were mowed in each orchard
during early September, early December and late
March. Ground cover growth is most vigorous from
early spring (September) to late autumn (May),
and during this period the ground covers usually
recovered within a few weeks following mowing.
Sampling methods
Spiders were collected using a sweep net with a
diameter of 40 cm. Two transects of 100 sweeps,
each comprising four 25-sweep sub-samples,
were made in each orchard. Each sweep covered
an arc of 1.0–1.5 m. A total of 200 sweeps were
taken in each orchard per month. All material was
sorted by hand on site and preserved in 70 % ethanol before proceeding with the next sub-sample.
All spiders from each orchard were pooled to
represent each months’ sample. Material was
subsequently sorted quantitatively and qualitatively, and identified, in the laboratory. Specimens
were separated into guilds based on their foraging
strategies. Wandering spiders were divided into
plant wanderers (PW) and ground wanderers
(GW), and web-building spiders into orb-web
Haddad et al.: Spiders in ground covers of pistachio orchards in South Africa
builders (OWB), hackle-web builders (HWB),
gum-foot web builders (GWB) and sheet-web
builders (SWB).
Field observations of spider predation were
made during sampling to determine the prey spectrum of the most common species. All prey capture
events observed while sorting sweep samples
were noted. Additional observations (1–2 hours
per sample date) were made on weedy plants and
in webs of web-building spiders to further determine the prey spectrum of spiders. Spiders and
their prey items were identified in the field by the
collector. Data were not processed quantitatively,
but only in terms of the prey taxa captured by each
spider.
Statistical analysis
Total spider numbers in the three orchards
were subjected to chi-square analysis with Yate’s
correction, at a significance level of 95 %, to determine if ground cover structure and vegetation
density have an effect on total spider abundance.
Species richness was calculated as the number
of species captured in each orchard divided by the
total species collected in the three orchards during
the study. Sørensen’s quotient of similarity was
used to compare the similarity of the spider faunas
of the three orchards. The formula used in this
index is QS = 2j /(a + b), where a and b are the
number of species captured at two particular sites,
and j the number of species common to both
samples (Magurran 1988). A higher value (closer
to 1) indicates that the faunas at the two sites are
more similar, while a value closer to 0 indicates a
more unique fauna in each habitat.
Results
Numbers, diversity and guilds
A total of 1760 spiders representing 55 species
was collected in the three orchards in the ten
months sampled (Table 2). Total spider abundance was highest in GVN 1 (n = 631), followed by
REM (n = 580) and GVN 19 (n = 549). Total spider
abundance was significantly higher (P = 0.0184,
P2 = 5.56, P < 0.05) in GVN 1 than in GVN 19, but
numbers did not differ significantly between GVN 1
and REM, and REM and GVN 19.
Two species, the lynx spider Peucetia viridis
(Blackwall) and jumping spider Heliophanus
pistaciae Wesolowska, dominated the spider
fauna. They accounted for 29.3 % and 23.4 % of
99
the total number of spiders collected, respectively
(Table 2). The only other species representing
more than 5 % of the total were the crab spider
Thomisus stenningi Pocock (6.5 %) and the jumping spider Phlegra sp. (5.8 %).
Species richness was highest in GVN 1 (0.727,
40 spp.), followed by GVN 19 (0.655, 36 spp.) and
REM (0.636, 35 spp.) (Table 2). Sørensen’s
quotient values (Table 3) were highest (0.789) for
the GVN 19-REM combination. This indicated
that the two orchards with the most contrasting
vegetation densities and compositions had the
most similar fauna, and suggests that ground
cover composition has a minimal influence on
the diversity of spiders. When similarity was
compared at guild level a similar pattern emerged.
Sørensen’s quotient values were only slightly
higher for the plant-wandering guild in the GVN
1-GVN 19 combination (0.824) than for the
GVN 19-REM combination (0.778). Ground
wanderers and the various guilds of web-dwellers
also displayed the most similar diversity between
the orchards GVN 19 and REM. The reason for
this pattern is not known, since the plant compositions of the two orchards are markedly different.
Perhaps the presence of grasses in both orchards,
while being scarce at GVN 1, could account for the
greater similarity between GVN 19 and REM.
Sixteen of the 17 species that represented more
than 1 % or more of the total fauna were found in
all three orchards. Plant wanderers dominated the
spider fauna dwelling on ground cover plants in
terms of diversity and abundance (Fig. 1), comprising 76.7 % of the spiders and 38.2 % of the
species present. Although ground wanderers
were also diverse (29.1 % of all the species), they
formed a comparatively small part of the total
number collected (8.9 %). This pattern could be
expected since sampling was conducted only by
sweep-netting. Apart from the sheet-weavers,
which comprised 7.1 % of the total (9.1 % of the
species), most of the remaining guilds represented only a minor part of the spider population.
These groups included hackle-web builders
(3.0 %, and 1.8 % of the species), orb-weavers
(2.7 %, and 9.1 % of the species) and gum-foot
web builders (1.6 %, and 12.7 % of the species).
Seasonal abundance patterns
The seasonal fluctuation of spider populations in
the three orchards followed a variable pattern
(Fig. 2). Numbers were low in the winter, with a
100
African Plant Protection vol. 10, no. 2, August 2004
Table 2. Species diversity and abundance of spiders collected from ground covers in three pistachio orchards in the
Prieska district, Northern Cape Province, from July 2001 to July 2002.
a
Family/species
Guild
ARANEIDAE
Argiope australis (Walckenaer, 1805)
Neoscona blondeli (Simon, 1885)
Neoscona subfusca (C L Koch, 1837)
Prasonica sp.
OWB
OWB
OWB
OWB
CORINNIDAE
Austrachelas sp.
Castianeira sp. 1
Castianeira sp. 2
Trachelas pusillus Lessert, 1923
GW
GW
GW
PW
DICTYNIDAE
Archaeodictyna sp.
HWB
GNAPHOSIDAE
Aneplasa nigra Tucker, 1923
Camillina cordifera (Tullgren, 1910)
Echemus sp.
Micaria sp.
Pterotricha auris (Tucker, 1923)
Setaphis subtilis (Simon, 1897)
GW
GW
GW
GW
GW
GW
LINYPHIIDAE
Eperigone fradeorum (Berland, 1932)
Meioneta habra Locket, 1968
Meioneta sp.
Microlinyphia sterilis (Pavesi, 1883)
Ostearius melanopygius (O P-Cambridge, 1879)
SWB
SWB
SWB
SWB
SWB
LYCOSIDAE
Pardosa crassipalpis Purcell, 1903
Lycosinae sp.
GVN 1
10
6
GVN 19
1
6
8
REM
Total
% of total
10
4
2
1
26
18
2
0.06
1.47
1.02
0.11
1
1
2
3
2
0.06
0.11
0.17
0.11
1
2
3
1
12
19
21
52
2.95
3
2
4
1
6
4
1
2
2
1
0.34
0.23
0.06
0.11
0.11
0.06
1
4
23
12
9
3
5
28
80
0.51
0.17
0.28
1.59
4.55
1
2
2
1
2
1
7
1
1
5
51
17
GW
GW
2
6
12
5
20
5
1.14
0.28
MITURGIDAE
Cheiracanthium furculatum Karsch, 1879
PW
6
2
12
20
1.14
OXYOPIDAE
Peucetia viridis (Blackwall, 1858)
Oxyopes bothai Lessert, 1915
Oxyopes hoggi Lessert, 1915
PW
PW
PW
185
8
1
156
18
1
176
1
517
27
2
29.34
1.53
0.11
PHILODROMIDAE
Hirriusa arenacea (Lawrence, 1927)
Philodromus sp.
Suemus sp.
Thanatus sp.
GW
PW
GW
GW
1
3
6
17
19
1
1
32
6
1
21
57
7
0.06
1.19
3.24
0.40
PISAURIDAE
Rothus vittatus Simon, 1898
PW
17
17
0.97
SALTICIDAE
Heliophanus charlesi Wesolowska, 2003
Heliophanus pistaciae Wesolowska, 2003
Natta horizontalis Karsch, 1879
Pellenes sp.
Phlegra sp.
PW
PW
GW
GW
GW
2
191
1
1
5
15
411
2
3
102
0.85
23.35
0.11
0.17
5.80
7
168
1
55
6
52
1
1
42
Continued on p. 101
Haddad et al.: Spiders in ground covers of pistachio orchards in South Africa
101
Table 2 (continued )
a
Family/species
Guild
Pseudicius sp.
Thyene aperta (Peckham & Peckham, 1903)
Thyene inflata (Gerstaecker, 1873)
PW
PW
PW
THERIDIIDAE
Enoplognatha sp.
Euryopis sp.
Latrodectus geometricus C L Koch, 1841
Latrodectus indistinctus O P-Cambridge, 1904
Theridion sp. 1
Theridion sp. 2
Tidarren sp.
GWB
GWB
GWB
GWB
GWB
GWB
GWB
THOMISIDAE
Diaea puncta Karsch, 1884
Heriaeus sp.
Misumenops rubrodecoratus Millot, 1941
Monaeses austrinus Simon, 1910
Runcinia depressa Simon, 1906
Thomisus machadoi Comellini, 1959
Thomisus stenningi Pocock, 1900
Xysticus sp.
PW
PW
PW
PW
PW
PW
PW
GW
ULOBORIDAE
Uloborus plumipes Lucas, 1846
OWB
GVN 1
GVN 19
4
1
1
5
2
REM
Total
2
1
1
1
1
1
7
0.06
0.06
1.40
2
5
1
1
1
4
6
5
8
3
1
0.06
0.23
0.34
0.28
0.46
0.17
0.06
1
3
5
1
23
12
8
1
2
15
2
34
74
11
1
10
114
1
0.11
1.93
4.21
0.63
0.06
0.57
6.48
0.06
8
92
1
10
549
580
1760
100.00
1
9
47
3
1
1
12
1
1
TOTAL SPECIMENS
631
TOTAL SPECIES
SPECIES RICHNESS
% of total
1
0.06
40
36
35
55
–
0.727
0.655
0.636
–
–
a
GW = ground wanderers, GWB = gum-foot web builders, HWB = hackle-web builders, OWB = orb-web builders, PW = plant
wanderers, SWB = sheet-web builders.
slight (GVN 19 and REM) and a sharp (GVN 1)
increase in abundance in spring. This is a
consequence of recovery of the ground cover
growth due to increased rainfall in the spring and
summer months, with an accompanying response
by insect and spider populations. Numbers in all
orchards peaked in summer (December–February),
before decreasing markedly in March (probably
due to further mechanical cutting of the ground
cover and pistachio nut harvesting). Numbers
recovered somewhat in April before decreasing to
a low in July.
Seasonal abundance patterns of the two dominant
species (Fig. 3) followed a similar pattern to that of
the total spider catch, described above. This could
be expected, as the two species together comprised
nearly 53 % of the spiders collected in the ground
covers. However, there was a noticeable difference
in the population structure of the two species.
Almost all P. viridis collected were immatures,
while the H. pistaciae population comprised only
65 % immatures. H. pistaciae also displayed more
steady patterns of increase or decrease than
P. viridis throughout the season.
Table 3. Sørensen’s quotient values for spider populations and guilds collected in three pistachio orchards in
the Prieska district, Northern Cape Province.
Guilda
Total population
PW
GW
OWB
HWB
GWB
SWB
a
GVN 1/GVN 19
0.684
0.824
0.421
0.667
1.000
0.444
0.750
GVN 19/REM GVN 1/REM
0.789
0.778
0.667
0.667
1.000
0.857
0.750
0.667
0.632
0.556
0.667
1.000
0.500
0.750
GW = ground wanderers, GWB = gum-foot web builders, HWB =
hackle-web builders, OWB = orb-web builders, PW = plant wanderers, SWB = sheet-web builders.
102
African Plant Protection vol. 10, no. 2, August 2004
Fig. 1. Guild composition of spider populations in ground covers of pistachio orchards in the Prieska district, Northern
Cape Province, with reference to percentage diversity and abundance. GW = ground wanderers, GWB = gum-foot
web builders, HWB = hackle-web builders, OWB = orb-web builders, PW = plant wanderers, SWB = sheet-web
builders.
Influence of vegetation structure
The percentage representation of the five
dominant agrobiont species varied between
orchards (Fig. 4), indicating some degree of preference by individual species for different vegetation
structures. P. viridis was equally abundant in the
three orchards and seemed to concentrate on any
available vegetation, but particularly herbs and
weeds. The jumping spiders H. pistaciae and
Phlegra sp. showed distinct preferences for particular plant compositions and densities. The former
species preferred dense and moderately dense
plantings where movement between plant foliage
is easier, as in the predominantly mixed planting
orchards (GVN 1 and REM). The latter is largely
surface-active, but occasionally wandered onto
plants, and was more abundant in the orchards
with at least some space between plants (GVN 1
and GVN 19). Since these three species were
among the most commonly found, providing ground
covers of similar composition to GVN 1 may yield
the greatest benefits for increasing their populations.
T. stenningi and other crab spiders were most
Fig. 2. Seasonal fluctuations of spider populations in ground covers in three pistachio orchards in the Prieska district,
Northern Cape Province, over a period of a year.
Haddad et al.: Spiders in ground covers of pistachio orchards in South Africa
103
Fig. 3. Seasonal fluctuations of Peucetia viridis and Heliophanus pistaciae in ground covers of three pistachio
orchards in the Prieska district, Northern Cape Province, over a period of a year.
abundant at GVN 19, which could be attributed to
the presence of alternate rows of grasses and
weeds. This mixed vegetation complex provided a
greater variety of niches to be occupied by this
group. Included were typical grass-dwelling species
( T. stenningi, Thomisus machadoi Comellini
Misumenops rubrodecoratus Millot and Heriaeus
sp.), as well as flower-dwelling species (primarily
Thomisus spp.).
The dominant web-building spider in the ground
covers, Ostearius melanopygius (O P-Cambridge),
while not strongly dominant (4.6 % of the total),
was more prevalent at GVN 1 than at GVN 19 and
REM. This may have been due the vegetation
structure at GVN 1, comprising mostly herbs and
short weeds, providing suitable web sites close to
the ground at the base of vegetation, and/or to the
strong colonisation ability of this species from
wheat (Triticum aestivum L.) and maize (Zea mays
L.) fields adjacent to the orchard.
Predation events
Although spiders were found preying on nine
orders of insect prey, namely Collembola, Orthoptera, Thysanoptera, Hemiptera, Homoptera,
Coleoptera, Diptera, Lepidoptera and Hymenoptera,
and also other spiders, only data on the eight taxa
most frequently observed in the chelicerae of
spiders are presented here (Table 4).
Spiders were found to prey on a variety of minor
pests, as well as on certain taxa of beneficial
arthropods. At least six spider species were
observed preying on minor pest thrips (Thysanoptera: Phlaeothripidae), leafhoppers (Homoptera: Cicadellidae), aphids (Homoptera: Aphididae) and false chinch bugs (Nysius natalensis
104
African Plant Protection vol. 10, no. 2, August 2004
Fig. 4. Relative abundance of five numerically dominant spider species in the ground cover layer of three pistachio
orchards in the Prieska district, Northern Cape Province.
Evans, Hemiptera: Lygaeidae). In addition,
spiders were occasionally also observed preying
on leaf beetles and flies.
The most frequently attacked natural enemies
were parasitoids (Hymenoptera: Chalcidoidea).
Four spider species were seen capturing small
immature thomisids and philodromids (Table 4).
On two occasions, H. pistaciae and Philodromus
sp. were also seen feeding on the small ladybird
species Scymnus levaillanti Mulsant (Coleoptera:
Coccinellidae). Since most predation events
observed were on pest species, the impact of
spiders on other natural enemies may be minimal.mm
Discussion
This study has shown spiders to be a diverse and
abundant arthropod group in ground cover layers
in the pistachio orchards surveyed. Dominant
species responded differently to vegetation type,
although a preference for weedy and herbal
vegetation was apparent. It is known that the
nature and density of ground covers affect spider
phenology differently. More complex habitats
provide a greater diversity of structures for
web-building spiders to construct webs (Wyss et
al. 1995). This was reflected in the greater
abundance and diversity of spiders at GVN 1, an
orchard dominated by weedy and herbal growth,
which creates the most complex habitat structure.
This, in turn, may be related to more luscious
vegetation, which supports a greater diversity of
herbivorous and saprophagous insects. Flowering
plants attract large numbers of insects that provide
a variety of prey for spiders, hence increasing their
rate of survival (Costello & Daane 1998b).
Mowing of ground covers is likely to affect
populations of spider groups differently. Howell
& Pienkowski (1971) found no differences in
numbers of orb-web builders (Tetragnathidae) and
nocturnal wolf spider species (Lycosidae) following the cutting of lucerne (Medicago sativa L.).
Populations of diurnal wandering spiders (Salticidae, Thomisidae), however, decreased whereas
sheet-weavers (Linyphiidae) increased after
cutting. In the present study the entire spider population showed a marked decrease following
ground cover mowing in March, but recovered
somewhat in April. Horton (1999) found that spider
and parasitoid populations were increased
arboreally in pear (Pyrus communis L.) trees by
decreasing mowing frequency, but this also resulted
in an increase in arboreal spider mite populations.
Attention should therefore be given to the timing
and frequency of mowing to restrict negative
effects on spiders and avoid pest proliferation. An
effective management strategy (presently in place
at GVN) that maintains a clear space, free of any
ground cover vegetation, beneath the trees is also
important as encroachment by understorey vegetation may reduce yield and vigour of the trees (Brown
et al. 1997b; Costello & Daane 1997).
+
+
+
+
+
+
+
+
+
+
+
Archaeodictyna sp.
Cheiracanthium furculatum
Heliophanus pistaciae
Neoscona subfusca
Peucetia viridis
Pardosa crassipalpis
Philodromus spp.
Phlegra sp.
Thomisus spp.
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Other Araneae
Hymenoptera:
Chalcidoidea
Diptera:
Ephydroidea
Coleoptera:
Chrysomelidae
Homoptera:
Cicadellidae
Thysanoptera:
Phlaeothripidae
Hemiptera:
Lygaeidae
Homoptera:
Aphididae
Insect prey
Spider species
Table 4. Most frequently encountered field observations of predation events involving spiders inhabiting ground covers in pistachio orchards in the Prieska district,
Northern Cape Province.
Haddad et al.: Spiders in ground covers of pistachio orchards in South Africa
105
There is conflicting evidence regarding the
relationship between faunas of ground covers and
tree canopies. Spider species composition of
ground covers and canopies in orchards may differ
considerably (Samu et al. 1997; Costello & Daane
1998b), or there may be a large degree of overlap
(Bogya et al. 1999, 2000; Pekár 1999; Rieux et al.
1999; Miliczky et al. 2000). Bogya et al. (1999,
2000) suggested that the presence or absence of
ground covers does not significantly influence the
abundance or species richness of spiders
arboreally. However, 87.3 % of the spider species
collected from ground covers in the present study
were also present in the tree canopies (Haddad
2003), with H. pistaciae accounting for 23.4 % of
the spiders in the ground covers and 53.8 % of the
canopy fauna. Considering the degree of species
overlap, it appears that ground covers in pistachio
orchards in South Africa may play an important
role in supplementing the arboreal spider fauna,
hence assisting in the recovery of arboreal populations depleted by chemical treatments (Rieux et al.
1999; Bogya et al. 2000). This is supported by the
decrease in populations of H. pistaciae in the ground
covers at GVN 1 and REM following a peak in
December/January, and subsequent increase in
H. pistaciae numbers in the tree canopies to
a peak in March–April (Haddad 2003). Other
scenarios, besides the above overlap between
arboreal and ground cover populations of H.
pistaciae, that could be deduced regarding the
correlation between ground cover and arboreal
spider faunas (Haddad 2003) in pistachio
orchards include the following: (i) distinct dominance in ground covers, while being scarce in the
tree layer, e.g. P. viridis, (ii) rare in ground covers
but common in tree tops, e.g. Cheiracanthium
furculatum Karsch, (iii) scarce in both ground
covers and tree layers, e.g. Rothus vittatus Simon,
and (iv) scarce in either the ground cover or tree
layer, and absent in the other layer, e.g. Argiope
australis (Walckenaer) and Pelecopsis janus
Jocqué, respectively.
All the minor pests observed in the study were
also present in most of the pistachio trees sampled
(Haddad 2003) and have the potential to attain key
pest status if measures to control them are inadequate. Thrips, aphids and leafhoppers can cause
extensive leaf damage (abrasion and wilting),
thereby reducing the photosynthetic capacity of
the plants and, consequently, nutrient conversion
and growth. Species such as N. natalensis further-
106
African Plant Protection vol. 10, no. 2, August 2004
more serves as a vector for fungal pathogens of
pistachio (Swart 2002). While not particularly
abundant in the tree canopies, N. natalensis is
very common in ground covers of most orchards,
especially when weedy plants such as Conyza
bonariensis (L.) Cronq. are present. Field trials
indicated that a mean of 1.05 N. natalensis are
killed by H. pistaciae (n = 20) per 24 hours,
whereas laboratory experiments suggest that
H. pistaciae kills N. natalensis without feeding
on it (Haddad et al. 2004), which is a form of
wasteful killing (Sunderland 1999). As part of a
greater natural enemy complex in the ground
cover layer, spiders may therefore play an important role in the suppression of minor pests in this
stratum.
Conclusion
The benefits that spider communities have as a
predatory complex include the diverse lifestyles of
individual species, utilisation of a greater number
of niches (resulting in a greater pest control effect
in various strata), and the ability to consume all
life stages of a pest (Nyffeler et al. 1994; Marc &
Canard 1997; Sunderland 1999). Structurally
complex ground cover regimes, which have a
variety of strata, will provide refuge for different
species of predators, thereby minimising the role
of intraguild predation (predation of one predator
species on another) and maximising the predation
impact on commonly utilised herbivorous prey
species (Finke & Denno 2002). This implies that
pest control effects at ground level would be maximised in orchards with a complex structure, i.e. a
mixture of herbs, weeds and grasses, such as
GVN 1 and REM in this study.
However, a greater diversity of plant species at
ground level could support a greater diversity of
herbivorous insects, increasing the risk of nonpest herbivores reaching pest status on the main
crop. Such a situation needs to be more closely
scrutinised by comparing minor pest populations
in pistachio tree canopies in orchards with different
ground cover structures.
Acknowledgements
This study formed part of a MSc study by the
senior author on spider ecology in pistachio
orchards in South Africa. The National Research
Foundation of South Africa is thanked for providing
a bursary to fund this project. The staff of the
Green Valley Nuts estate are thanked for their
hospitality and assistance with the field work,
especially A Müller and K Snyman. A Dean and
S Pekár provided useful comments and discussion on earlier versions of the script. J van Niekerk
and D Chikobvu provided assistance and advice
with the statistical analyses.
References
Bogya S, Markó V & Szinetár C 1999. Comparison of
pome fruit orchard inhabiting spider assemblages at
different geographical scales. Agricultural and Forest
Entomology 1: 261–270.
Bogya S, Markó V & Szinetár C 2000. Effect of pest
management systems on foliage- and grass-dwelling
spider communities in an apple orchard in Hungary.
International Journal of Pest Management 46:
241–250.
Brown M W, Niemczyk E, Baicu T, Balázs K, Jarosik
4
V, Jenser G, Kocourek F, Olszak R, Serboiu A &
Van Der Zwet T 1997a. Enhanced biological control
in apple orchards using ground covers and selective
insecticides: an international study. Zahradnictví –
Horticultural Science (Prague) 24: 35–37.
Brown M W, Van Der Zwet T & Glenn D M 1997b.
Impact of ground cover plants on pest management
in West Virginia, USA, apple orchards. Zahradnictví –
Horticultural Science (Prague) 24: 39–44.
Bugg R L & Dutcher J D 1989. Warm-season cover
crops for pecan orchards: horticultural and entomological implications. Biological Agriculture and
Horticulture 6: 123–148.
Bugg R L, Dutcher J D & McNeill P J 1991.
Cool-season cover crops in the pecan orchard
understory: effects on Coccinellidae (Coleoptera)
and pecan aphids (Homoptera: Aphididae). Biological Control 1: 8–15.
Bugg R L & Waddington C 1994. Using cover crops to
manage arthropod pests of orchards: a review. Agriculture, Ecosystems and Environment 50: 11–28.
Carroll D P 1980. Biological notes on the spiders of
some citrus groves in central and southern California.
Entomological News 91: 147–154.
Cortesero A M, Stapel J O & Lewis W J 2000.
Understanding and manipulating plant attributes to
enhance biological control. Biological Control 17:
35–49.
Costello M J & Daane K M 1997. Cover crops affect vine
growth and vineyard microclimate. Grape Grower 29:
22–25.
Costello M J & Daane K M 1998a. Arthropods. In: Cover
cropping in vineyards: a grower’s handbook, 93–106
(Eds C A Ingels, R L Bugg, G Mcgourty & L P
Christensen). Division of Agriculture and Natural
Resources Publication 3338. University of California,
Oakland, California.
Costello M J & Daane K M 1998b. Influence of ground
cover on spider populations in a table grape vineyard.
Ecological Entomology 23: 33–40.
Costello M J & Daane K M 1999. Abundance of spiders
and insect predators on grapes in central California.
Haddad et al.: Spiders in ground covers of pistachio orchards in South Africa
Journal of Arachnology 27: 531–538.
Dennis P & Fry G L A 1992. Field margins: can they
enhance natural enemy population densities and
general arthropod diversity on farmland? Agriculture,
Ecosystems and Environment 40: 95–115.
Dennis P, Thomas M B & Sotherton N W 1994. Structural features of field boundaries which influence the
overwintering densities of beneficial arthropod
predators. Journal of Applied Ecology 32: 361–370.
Finke D L & Denno R 2002. Intraguild predation diminished in complex-structured vegetation: implications
for prey suppression. Ecology 83: 643–652.
Haddad C R 2003. Spider ecology in pistachio orchards
in South Africa. MSc dissertation, University of the
Free State, Bloemfontein.
Haddad C R, Louw S vd M & Dippenaar-Schoeman
A S 2004. An assessment of the biological control
potential of Heliophanus pistaciae (Araneae: Salticidae) on Nysius natalensis (Hemiptera: Lygaeidae), a
pest of pistachio nuts. Biological Control 31: 83–90.
Hoffman M T 1996. Orange River Nama Karoo. In:
Vegetation of South Africa, Lesotho and Swaziland,
1st edition, 71–72 (Eds A B Low & A G Rebelo).
Department of Environmental Affairs and Tourism,
Pretoria.
Horton D R 1999. Enhancing biological control in mating
disruption and organic pear orchards by understory
management. Organic Farming Research Foundation Report No. 98–06.
Howell J O & Pienkowski R L 1971. Spider populations
in alfalfa, with notes on spider prey and effect of harvest. Journal of Economic Entomology 64: 163–168.
Kaakeh W & Dutcher J D 1993. Rates of increase and
probing behavior of Acyrthosiphon pisum (Homoptera:
Aphididae) on preferred and nonpreferred host
cover crops. Environmental Entomology 22: 1016–
1021.
Kindlmann P & Dixon A F G 1999. Generation time
ratios – determinants of prey abundance in insect
predator-prey interactions. Biological Control 16:
133–138.
Knight A L, Turner J E & Brachula B 1997. Predation
on eggs of codling moth (Lepidoptera: Tortricidae) in
mating disrupted and conventional orchards in
Washington. Journal of the Entomological Society of
British Columbia 94: 67–74.
Liao H-T, Harris M K, Gilstrap F E, Dean D A, Agnew C
W, Michels G J & Mansour F 1984. Natural enemies
and other factors affecting seasonal abundance of
the blackmargined aphid on pecan. Southwestern
Entomologist 9: 404–420.
Magurran A E 1988. Ecological diversity and its measurement. Princeton University Press, Princeton, NJ.
Mansour F A, Rosen D & Shulov A 1981. Disturbing
effect of a spider on larval aggregations of
Spodoptera littoralis. Entomologia Experimentalis et
Applicata 29: 234–237.
Marc P & Canard A 1997. Maintaining spider diversity in
agroecosystems as a tool in pest control. Agriculture,
Ecosystems and Environment 62: 229–235.
Miliczky E R, Calkins C O & Horton D R 2000. Spider
107
abundance and diversity in apple orchards under
three pest management programmes in Washington
State, U.S.A. Agricultural and Forest Entomology 2:
203–215.
Nyffeler M & Benz G 1987. Spiders in natural pest
control: a review. Journal of Applied Entomology 103:
321–339.
Nyffeler M, Sterling W L & Dean D A 1994. How spiders
make a living. Environmental Entomology 23: 1357–
1367.
Pekár S 1999. Effect of IPM practices and conventional
spraying on spider population dynamics in an apple
orchard. Agriculture, Ecosystems and Environment
73: 155–166.
Riechert S E 1999. The hows and whys of successful
pest suppression by spiders: insights from case
studies. Journal of Arachnology 27: 387–396.
Rieux R, Simon S & Defrance H 1999. Role of
hedgerows and ground-cover management on
arthropod populations in pear orchards. Agriculture,
Ecosystems and Environment 73: 119–127.
Samu F & Bíró Z 1993. Functional response, multiple
feeding and wasteful killing in a wolf spider (Araneae:
Lycosidae). European Journal of Entomology 90:
471–476.
Samu F, Rácz V, Erdélyi C & Balázs K 1997. Spiders of
the foliage and herbaceous layer of an IPM apple
orchard in Kecskemét-Szarkás, Hungary. Biological
and Agricultural Horticulture 15: 131–140.
Smith M W, Eikenbary R D, Arnold D C, Landgraf B S,
Taylor G G, Barlow G E, Carroll B L, Cheary B S,
Rice N R & Knight R 1994. Screening cool-season
legume cover crops for pecan orchards. American
Journal of Alternative Agriculture 9: 127–135.
Smith M W, Arnold D C, Eikenbary R D, Rice N R,
Shiferaw A, Cheary B S & Carroll B L 1996.
Influence of ground cover on beneficial arthropods in
pecan. Biological Control 6: 164–176.
Sunderland K D 1999. Mechanisms underlying the
effects of spiders on pest populations. Journal of
Arachnology 27: 308–316.
Sunderland K D & Samu F 2000. Effects of agricultural
diversification on the abundance, distribution, and
pest control potential of spiders: a review. Entomologia
Experimentalis et Applicata 95: 1–13.
Swart V R 2002. Insect–fungal ecology on selected new
crops in South Africa. MSc dissertation, University of
the Free State, Bloemfontein.
Thomas C F G & Marshall E J P 1999. Arthropod
abundance and diversity in differently vegetated
margins of arable fields. Agriculture, Ecosystems and
Environment 72: 131–144.
Wilby A & Thomas M B 2002. Are the ecological
concepts of assembly and function of biodiversity
useful frameworks for understanding natural pest
control? Agricultural and Forest Entomology 4:
237–243.
Wyss E, Niggli U & Nentwig W 1995. The impact of
spiders on aphid populations in a strip-managed
apple orchard. Journal of Applied Entomology 119:
473–478.
Accepted 30 June 2004
Associated Editor was E van den Berg