Living where the food is: web location by linyphiid spiders in relation ...

Journal of Applied Ecology

2001

38

, 88–99

© 2001 British Ecological Society

Blackwell Science, Ltd

Living where the food is: web location by linyphiid spiders in relation to prey availability in winter wheat

J.D. HARWOOD*†, K.D. SUNDERLAND† and W.O.C. SYMONDSON*

*

School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK; and

†

Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK

Summary

1.

Spiders form a major component of the generalist predator fauna, potentially able torestrict pest population growth, but their populations may be food-limited undercurrent farming regimes. This study aimed to quantify food availability to spiders inwinter wheat and to determine whether spider web locations are positively associatedwith available food resources.

2.

Mini-sticky traps (availability rate per 24 h, including prey falling from the crop) andmini-quadrats (instantaneous density on the ground by day) were used, in combination,to monitor the availability of potential prey to web-building species of money spider(Linyphiidae) in fields of winter wheat in Warwickshire, UK, 1997–98.

3.

These methods were applied to web sites of individual spiders and to non-web siteslocated randomly up to 30 cm away from each web. A total of 18 546 invertebrates werecaptured using these methods.

4.

Overall, significantly more potential prey were available in web sites than in non-websites (both on sticky traps and in quadrats).

5.

Prey availability in May and July was about a third of that in June (both on stickytraps and in quadrats) and may have been below that known to be necessary for spidersto realize their maximum population growth rate.

6.

The peak rate of capture of linyphiid spiders on mini-sticky traps was 0·6 trap

–1

day

–1

at web sites, and approximately half this value at non-web sites. Numbers of spiderscaptured by mini-sticky traps and mini-quadrats increased exponentially as the seasonprogressed. The high capture frequency in relation to population density, and thedifferential between web and non-web sites, points to a dynamic and aggregated dis-tribution of spiders in winter wheat, which is consistent with what is known aboutmate-searching and web site abandonment rates by the Linyphiidae.

7.

The combination of techniques described here is recommended for monitoring preyavailability in prey-enhancement programmes and may prove useful in quantitativestudies of both intra- and interspecific interactions between spiders.

Key-words

: aggregative responses, Collembola, generalist predators, mini-quadrats,mini-sticky traps.


(2001)

38

, 88–99

Introduction

In Britain, the area of cereal crops treated with pesti-cide has increased by 24% since 1994, with a concomit-ant 16% increase in the amount of active ingredientsapplied (Thomas, Garthwaite & Banham 1996). Althoughchemical pesticides are convenient to use, and oftenefficient and cost-effective in the short term, it isnow appreciated that they are not a long-term option

because of the associated cumulative problems (such aspest resistance and environmental pollution) that renderpesticide-based agriculture unsustainable (Pimentel1995). Biological control is a strong alternative option,and for the majority of low-value outdoor Europeancrops this must be achieved through conservation ofendemic biocontrol agents (i.e. ‘conservation biologicalcontrol’; Ehler 1998) rather than by classical biologicalcontrol or rear-and-release methods. Small soft-bodiedpests (such as aphids) that are accessible on the vegeta-tion and ground surface, are attacked by a range ofnatural enemies (pathogens, parasitoids, specialist and

Correspondence: Dr W.O.C. Symondson (fax 02920 874305;e-mail [email protected]).

JPE572.fm Page 88 Monday, March 5, 2001 11:48 AM

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Web location by linyphiid spiders

© 2001 British Ecological Society,


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generalist natural enemies) that interact in complexways (Sunderland

et al

. 1997). Generalist predators(e.g. spiders, carabid and staphylinid beetles) have thevaluable attribute of being able to subsist on alternativenon-pest prey. They can therefore either simply bepresent in the field before the pest arrives, performing alying-in-wait strategy (Murdoch, Chesson & Chesson1985; Chang & Kareiva 1999), or build up their popu-lations on alternative foods early in the season andthen impact on the pest population with a favourablepredator : pest ratio during the early phase of pestpopulation growth (Settle

et al

. 1996). Manipulativefield experiments have demonstrated that generalistpredators can often (Edwards, Sunderland & George1979; Chiverton 1986; Duffield

et al

. 1996), but notalways (Holland & Thomas 1997), contribute to com-mercially valuable reductions of aphid populationson wheat. Web-building species of money spider(Linyphiidae), such as

Lepthyphantes tenuis

(Blackwall)and

Erigone atra

(Blackwall), consume cereal aphids(Sunderland

et al

. 1987) and trap considerable num-bers in their horizontal sheet webs (Sunderland, Fraser& Dixon 1986a; Alderweireldt 1994a), which can coverup to half of the surface area of a wheat field (Sunder-land, Fraser & Dixon 1986b). Death of pests trapped inwebs may contribute to pest control even if the spiderdoes not consume them (Sunderland 1999).

Reviews of the literature have demonstrated thatspider density is likely to be increased by within-crophabitat diversification (Samu & Sunderland 1999; Sun-derland & Samu 2000). The mechanisms underlyingthis effect are not fully understood but it is probablethat prey diversification is an important factor. Labo-ratory investigations suggest that the value of differentprey types for supporting spider population growthvaries greatly between major taxonomic groups (ordersand families) of prey (Toft 1995; Sunderland

et al

.1996; Beck & Toft 2000; Bilde, Axelsen & Toft 2000)and even between congeneric species [e.g. between thecollembolans

Isotoma anglicana

Lubbock and

Folsomiacandida

Willem (Toft & Nielsen 1997; K.D. Sunderland,J.D. Harwood & W.O.C. Symondson, unpublisheddata) and

Isotoma tigrina

Nicolet (T. Bilde & S. Toft,unpublished data) ]. To guide the future developmentof improved practical techniques aimed at enhancingspider populations and increase their impact on pests,quantitative information (from the field or undersimulated field conditions) will be needed on (i) theabsolute and relative availability of different prey types,(ii) prey preferences, and (iii) diet-related spider popu-lation growth rates. In this paper we address the first ofthese aims and develop the methodology needed toquantify prey availability in the field. For this purposeit is necessary to quantify how many prey are availableclose to the webs of individual spiders, which are to befound on the ground or up to 10 cm above the ground(Sunderland, Fraser & Dixon 1986a). Sampling methodssuch as vacuum insect nets (Potts & Vickerman 1974;Moreby

et al

. 1994), pitfall traps (Nentwig 1982) and

large sticky traps (Kajak 1965; Sunderland, Fraser &Dixon 1986b) fail to provide density estimates, or seriouslyunderestimate density (Sunderland & Topping 1995;Sunderland

et al

. 1995), and lack the spatial precisionneeded for this study.

To be able ultimately to optimize the spatial dis-tribution of within-field diversified prey resource it isnecessary to know how efficiently and dynamicallyspiders are capable of relocating their webs in relationto temporal and spatial fluctuations of prey availability.Some web-building spiders are known to be efficient inthis respect (McNett & Rypstra 1997) but others arerelatively insensitive to prey availability (Schaefer 1978).There are, however, very few such studies of spiders inagricultural habitats (Sunderland & Samu 2000).

In this study we (i) quantified spatial and temporalvariation in the availability of potential prey to web-building linyphiid spiders in fields of winter wheat,using a combination of ‘instantaneous’ and cumulativesampling techniques, and (ii) determined whether weblocation is correlated spatially with the abundance ofpotential prey. As far as we know, this is the first timethat these topics have been investigated in an agricul-tural setting.

Methods

The study sites were winter wheat (cv. ‘Hereward’)fields of approximately 7 ha planted on a predom-inantly sandy loam soil at Horticulture ResearchInternational (HRI), Wellesbourne, Warwickshire,UK (52

°

12.18

′

N, 1

°

36.00

′

W). The fields were farmedaccording to standard farming practice and noinsecticide applications were required during theperiod of investigation. The study sites were sur-rounded by fields of spring barley, winter barley,winter wheat and by hay meadows.

Sampling was carried out from late April until harvest(in late July/early August) in 1997 and 1998. The abun-dance of invertebrates (including potential prey) wasdetermined by two different ground-based samplingmethods: mini-sticky traps and mini-quadrats. Thesemethods were designed to be small and precise enoughto monitor potential prey in the immediate area of aweb without the interference of ‘sampling noise’ frominvertebrates that would never be encountered by thespiders. They also form a complementary pair of methods;the mini-sticky trap is a passive sampling technique thatrelies on activity of the prey, but can sample throughout24 h and catch prey that fall or descend from higherstrata, whereas collection from a mini-quadrat is anactive sampling method, confined to the ground duringa very limited time period (thus providing an ‘instan-taneous’ density estimate). The use of mini-quadrats


90

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,88–99

enables the collection of potential prey that are tem-porarily inactive and hiding under weeds, small stonesand at the bases of cereal stems.

The plastic mini-sticky traps were 7·5 cm

2

(1·5 cm

×

5 cm, 2 mm thick), which is of comparable area towebs constructed by the common erigonid spiders

E. atra

and

Erigone dentipalpis

(Wider) (Sunderland,Fraser & Dixon 1986a; Alderweireldt 1994a). The trapswere coloured with black acrylic paint (to minimizevisual attraction by merging in colour with the groundsurface) and were covered on the upper side with athin acetate sheet coated with Oecotak A5, a non-toxicpolybutene-based adhesive (Oecos, Kimpton, UK).The black traps were unlikely to absorb much addi-tional heat from sunlight because they were placed onthe ground surface, and were therefore shaded by thewinter wheat. After traps were removed from the field,the detachable acetate sheet was placed in a bath ofwhite spirit to dissolve the Oecotak, enabling recoveryof trapped invertebrates into alcohol for storage andlater identification. The mini-quadrats were circularsampling areas (diameter 10 cm, area approximately78·5 cm

2

) defined by a template. These were placedon the ground, surrounding the web or non-web site.All invertebrates were collected from within the mini-quadrat by pooter, searching under loose soil andvegetation.

Sheet webs were located at random within the studyfields, and linyphiid spiders present within these webswere captured and preserved for subsequent identifica-tion. Vacant webs were not categorized as web sitesbecause spiders are known to leave their webs in activepursuit of prey (Alderweireldt 1994a; Schütt 1995) orabandon their web sites (Samu

et al

. 1996) in search ofmore profitable hunting grounds (Vollrath 1985; Gillespie& Caraco 1987). Therefore, only webs in which linyphiidspiders were present were included in the analysis. Thewebs were removed because spiders are known to beattracted by the presence of silk (Leborgne & Pasquet1987; Hodge & Storfer-Isser 1997). This also minimizedany potential interference with the traps. One mini-stickytrap was centred horizontally on the ground at theposition from which a web was removed, and anotherplaced at a random non-web site nearby (up to 30 cmaway). Sampling was always carried out in pairs, toenable direct comparisons between each set of traps,which were left

in situ

for 24 h. Great care was takennot to disturb surrounding vegetation and dislodgearthropods onto the traps during placement andcollection.

When sampling by mini-quadrat, the same pair-wise sampling procedure was used as described abovefor mini-sticky traps. The ground within the mini-quadrat was searched thoroughly, and all arthropodspresent were transferred immediately into alcohol.No attempt was made to collect arthropods from thecrop vegetation above the mini-quadrat. Sampleswere taken during the daytime between 08.00 hoursand 16.00 hours.

Comparisons between web-centred and non-web-centred mini-sticky traps were made from mid-June tomid-July in 1997 (

n

= 120 paired samples), and a moreextensive monitoring programme performed in 1998 atregular intervals from late April until harvest (

n

= 250).Mini-quadrats were used to sample the abundance ofpotential prey during July 1997 (

n

= 52) and from lateApril until harvest in 1998 (

n

= 271). No comparisonswere made for quadrat catches between the two yearsdue to the different sampling dates.

Meteorological data (maximum and minimum air tem-peratures; soil temperature; rainfall; hours of sunshine;wind speed; rate of evaporation; relative humidity)were obtained from the weather station located at HRIWellesbourne, which was within 1200 m of all field sites.

To stabilize variances, all sample data were transformed(log

10

(

x

+ 1)) prior to analyses. For the purposes ofmaking direct comparisons between mini-sticky trapsand mini-quadrats, data were converted into standardunit areas (per cm

2

). Analysis of variance (

) wasused to analyse potential prey populations captured bymini-sticky traps and mini-quadrats. Catches of potentialprey were pooled over time for comparisons of web vs.non-web sites, and mini-sticky traps verses mini-quadrats.A non-parametric Mann–Whitney

U

-test was usedwhere the assumptions of

could not be met, andpaired sample

t

-tests were used to compare numbersof individual prey taxa captured by web and non-webtraps. Where less common prey taxa were analysed,data were grouped into means per sampling sessionand the analysis was performed on mean numberscaptured per session.

Potential prey items in the samples were separatedfrom other invertebrates on the basis of size (thelinyphiid species found in winter wheat are rarely ableto capture and kill prey > 5 mm long) and in relationto information from the published literature for preyof linyphiids in European arable crops (Sunderland,Fraser & Dixon 1986a; De Keer & Maelfait 1987a,1988; Nyffeler & Benz 1988; Alderweireldt 1994a;Jmhasly & Nentwig 1995; Toft 1995) and the results oflaboratory prey acceptability trials (K.D. Sunderland,unpublished data).

Results

Data for web sites of all Linyphiidae were pooled andanalysed collectively. Table 1 shows the numbers ofeach species/genus/subfamily of spider captured at websites prior to sampling by mini-sticky traps and quadrats(i.e. the web owners). The total numbers of linyphiidsrecorded exceeded the number of web sites because,occasionally, more than one spider was present in a web.


91




,

38

,88–99

In 1997, web-centred mini-sticky traps (cumulativesampling over 24 h) caught more potential prey items,

per cm

2

, than were found in mini-quadrats (instanta-neous sampling during the day) (

F

1,340

= 5·67,

P

< 0·001).However, comparisons between individual prey taxawere not possible due to the small number of samplingdates (

n

= 4 for both mini-sticky traps and mini-quadrats).

Table 1. Number of each species/genus/subfamily caught in web sites prior to sampling by mini-sticky traps (MS) and mini-quadrats (MQ) during 1997 and 1998

Species/genus/subfamily 1997 MS 1997 MQ 1998 MS 1998 MQ

Erigone atra (Blackwall) 25 5 54 76Erigone dentipalpis (Wider) 18 4 32 34Milleriana inerrans (O.P.-Cambridge) 3 1 – –Oedothorax spp. 2 2 6 19Lepthyphantes tenuis (Blackwall) 25 25 103 113Bathyphantes gracilis (Blackwall) – 1 37 23Meioneta rurestris (C.L. Koch) 39 6 8 11Porrhomma errans (Blackwall) – – 1 –Micrargus subaequalis (Westring) 1 – – –Pachygnatha degeeri Sundevall 1 – 1 –Erigoninae juveniles 10 5 12 10Linyphiinae juveniles 9 7 9 9Total captured 133 56 263 295

Fig. 1. Mean number of potential prey, non-prey and spiders captured (per cm2) by mini-sticky traps and mini-quadrats withinweb sites during (a) 1997 and (b) 1998. Bars are ± SE. Numbers above columns are the ratios of numbers of prey captured by mini-sticky trap/mini-quadrat.


92

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,

38

,88–99

Similarly in 1998, significantly more potential preyitems were captured, per cm

2

, by web-centred mini-stickytraps than by web-centred mini-quadrats (

F

1,1038

= 1199·43,

P

< 0·001). There were also large differences betweenthe two methods in the numbers of certain invertebratetaxa captured during both 1997 and 1998 (Fig. 1).Significantly more Collembola (

F

1,1038

= 532·05,

P

<0·001), Diptera (Mann–Whitney,

U

= 0·0,

n

= 35,

P

< 0·001), Hymenoptera (

U

= 64·0,

n

= 35,

P

< 0·01)and Araneae (

U

= 77·5,

n

= 35,

P

< 0·05) were caughtby web-centred mini-sticky traps than were sampled byweb-centred mini-quadrats. There were large differ-ences in the ratio of individual prey taxa captured, percm

2

, between the two sampling methodologies (Fig. 1).The small dipterans that were classified as potentialprey were especially diverse, with representativesfrom the families Cecidomyiidae, Lonchopteridae,Phoridae, Sciaridae, Mycetophilidae, Drosophilidaeand Dolichopodidae.

In 1997, significantly more potential prey items werecaptured in sites where Linyphiidae had constructedtheir webs than in non-web sites, as monitored byboth mini-sticky traps (

F

1,238

= 6·80,

P

< 0·01) andmini-quadrats (

F

1,102

= 12·22,

P

< 0·01). Similar resultswere found in 1998, on different fields, again when

monitored by both mini-sticky traps (

F

1,480

= 96·69,

P

< 0·001) and mini-quadrats (

F

1,520

= 75·51,

P

< 0·001).The temporal abundance of potential prey in 1998 wasfound to be highly variable (

F

9,480

= 28·45,

P

< 0·001)(Fig. 2a).

Collembola, which constituted > 60% of all poten-tial prey items captured by web-centred mini-stickytraps during 1998, were significantly more abundant inweb sites (mean per cm

2

= 0·60

±

0·04) than in non-websites (mean per cm

2

= 0·26

±

0·02) (

F

1,480

= 109·02,

P

< 0·001). Similar distribution patterns were alsoevident when individual species of Collembola wereanalysed. The two most abundant isotomid collembolans,

I. anglicana

(

sensu

. Fjellberg 1980) and

Isotomuruspalustris

Müller, were present in greater densities onweb-centred, than on non-web, mini-sticky traps (

I.anglicana

:

F

1,480

= 39·69,

P

< 0·001;

I. palustris

:

F

1,18

=6·41,

P

< 0·05) and in mini-quadrats (

I. anglicana

:

F

1,520

= 29·59,

P

< 0·001;

I. palustris

:

F

1,520

= 22·54,

P

<0·001). The temporal capture frequencies of thesespecies, and of Collembola as a whole, on mini-stickytraps varied significantly throughout the monitoringperiod (Fig. 2b–d) (all Collembola:

F

9,480

= 45·56,

P

<0·001;

I. anglicana

:

F

9,480

= 55·60,

P

< 0·001;

I. palustris

:

F

9,480

= 17·22,

P

< 0·001). Similar significant differencesbetween numbers captured over time were recorded bymini-quadrat sampling (all Collembola:

F

10,520

= 59·67,

P

< 0·001;

I. anglicana

:

F

10,520

= 99·30,

P

< 0·001;

Fig. 2. Mean number (per trap per day) of (a) total potential prey, (b) all Collembola, (c) Isotoma anglicana (Collembola) and (d)Isotomurus palustris (Collembola) captured by web-centred (filled circles) and non-web-centred (empty circles) mini-sticky trapsfrom May to July 1998. Bars are ± SE.


93


© 2001 British Ecological Society, Journal of Applied Ecology, 38,88–99

I. palustris: F10,520 = 77·06, P < 0·001). However, despitethis temporal variability, more Collembola (total andisotomid) were captured on all dates at web-centredsites, regardless of sampling method.

The entomobryid collembolans Lepidocyrtus cyaneusTullberg and Entomobrya multifasciata (Tullberg)constituted 25·4% of total potential prey items onmini-sticky traps and 57·6% in mini-quadrats in 1997,although this difference was not significant. They wererelatively less dominant in 1998 (5·6% for mini-stickytraps and 14·3% for mini-quadrats), with no significantdifference between the two sampling methods, althoughthere was a significant difference in numbers capturedby mini-sticky traps between the two years (U = 6198·5,n = 240, P < 0·05). No comparison was made for quadrat

catches between the two years due to the different samp-ling dates. However, during 1998 the density of Entom-obryidae increased logarithmically as the seasonprogressed (Fig. 3). Analysis of covariance indicatedthat there was no significant difference between theslopes for mini-sticky traps and quadrats (F1,31 = 0·40,P > 0·05) or the y-axis intercepts (F1,31 = 0·52, P > 0·05).

Linyphiidae were significantly more abundant inweb than non-web sites both on mini-sticky traps andin mini-quadrats, and Diptera, Hymenoptera andColeoptera were more abundant in web than non-websites within mini-quadrats (Table 2). The sex ratio ofspiders captured also varied considerably. Male linyph-iids were captured on significantly more occasions thanfemales on mini-sticky traps in web sites (U = 56·5,

Fig. 3. Mean number of entomobryid collembolans (Lepidocyrtus cyaneus and Entomobrya multifasciata) captured per cm2 byweb-centred mini-sticky traps and mini-quadrats during 1998. Points are log10 (means) for individual sampling occasions.Mini-sticky trap regression: log10 y = 0·00648x – 0·117, r 2 = 0·80, t14 = 7·10, P < 0·001. Mini-quadrat regression: log10 y = 0·00862x– 0·164, r2 = 0·42, t19 = 3·64, P < 0·01.

Table 2. Differences between web and non-web sites in numbers of potential prey (Diptera, Hymenoptera, Coleoptera,Aphididae) and spiders (Araneae) captured by (a) mini-sticky traps and (b) mini-quadrats, in winter wheat in 1998. The area ofa mini-sticky trap (7·5 cm2) is approximately a tenth that of a mini-quadrat (78·5 cm2). Mean number of Araneae captured perweb-centred mini-quadrat are presented as (x + 1) to account for the web owner

Variable t d.f. PMean per web site ± SE

Mean per non-web site ± SE

Ratio web/non-web

(a) Mini-sticky trapsCollembola 7·52 14 < 0·001 4·48 ± 0·31 1·93 ± 0·18 2·32Diptera 1·02 14 0·326 0·29 ± 0·04 0·25 ± 0·03 1·16Hymenoptera 1·32 14 0·209 0·14 ± 0·03 0·08 ± 0·02 1·75Coleoptera 2·02 14 0·063 0·12 ± 0·02 0·06 ± 0·01 2·00Aphididae 1·49 14 0·157 0·20 ± 0·04 0·11 ± 0·02 1·81Araneae 4·26 14 0·001 0·30 ± 0·04 0·08 ± 0·02 3·75

(b) Mini-quadratsCollembola 10·85 19 < 0·001 27·66 ± 1·81 13·66 ± 1·12 2·02Diptera 3·24 19 0·004 0·20 ± 0·03 0·08 ± 0·02 2·50Hymenoptera 3·94 19 0·001 0·08 ± 0·02 0·04 ± 0·01 2·00Coleoptera 5·25 19 < 0·001 0·75 ± 0·07 0·34 ± 0·04 2·21Aphididae 1·40 19 0·117 0·21 ± 0·04 0·16 ± 0·03 1·31Araneae 32·47 19 < 0·001 1·78 ± 0·08 0·19 ± 0·04 9·37


94J.D. Harwood, K.D. Sunderland & W.O.C. Symondson


n = 30, P < 0·01); 3·3 times more male than femalespiders were also collected in non-web traps, althoughthese differences were not statistically significant.

Linyphiid density, monitored by mini-quadratsampling, increased logarithmically with time (Fig. 4).Analysis of covariance indicated a significant differencebetween the slopes of the web and non-web regressions(F1,36 = 7·17, P < 0·05) and the y-axis intercepts (F1,36 =76·51, P < 0·001), showing that linyphiid density wasincreasing more rapidly at web sites. The number oflinyphiids captured by mini-sticky traps (both web andnon-web) showed a similar pattern (Fig. 5) but analysisof covariance indicated no significant difference betweenthe two slopes (F1,26 = 1·57, P > 0·05) or y-axis intercepts(F1,26 = 0·32, P > 0·05), but the two slopes are signific-antly different from zero (F1,26 = 14·28, P < 0·01). Thelog10 number of spiders captured by these methods

within web sites also increased when regressed againstmaximum air temperature (mini-sticky traps: r2 = 0·27,t14 = 2·18, P < 0·05; mini-quadrats: r2 = 0·57, t19 = 4·91,P < 0·001) and soil temperature (mini-quadrats:r2 = 0·53, t19 = 4·47, P < 0·001).

A negative relationship was found to exist betweenthe number of Linyphiidae and Collembola capturedby web-centred mini-sticky traps (log10 Linyphiidae =–0·721 log10 Collembola + 0·636, r2 = 0·40, t14 = 2·97,P < 0·05). No such relationship was found using datafrom mini-quadrats.

-

From the comparison of 4 consecutive weeks (mid-Juneto mid-July) of mini-sticky trap data collected during

Fig. 4. Mean number of Linyphiidae sampled by web and non-web-centred mini-quadrats during 1998. Data for web quadratsare presented as log10(x + 1) to account for the web owner. Web regression: log10y = 0·00621x – 0·080, r 2 = 0·72, t19 = 6·78,P < 0·001. Non-web regression: log10y = 0·00330x – 0·360, r2 = 0·64, t19 = 5·63, P < 0·001.

Fig. 5. Mean number of Linyphiidae captured by web and non-web-centred mini-sticky traps during 1998. Web regression:log10y = 0·00388x – 0·395, r2 = 0·37, t14 = 2·73, P < 0·05. Non-web regression: log10y = 0·00195x – 0·250, r2 = 0·45, t14 = 3·25,P < 0·01.


95Web location by linyphiid spiders


1997 (mean number of total potential prey capturedper web site = 3·12 ± 0·22, non-web site = 2·38 ± 0·20)with a data set for the same calendar period during1998 (mean number per web site = 5·69 ± 0·50, non-website = 3·95 ± 0·27), the mean number of arthropodscaptured during the second year was significantly greater(F1,476 = 20·55, P < 0·001).

-

Despite the large variation in the numbers of arthro-pods captured between years, there was no evidence tosuggest that meteorological factors were responsiblefor such variability. Comparisons of data from 1997and 1998 indicated that no category of meteorologicaldata varied significantly in the 4 weeks prior to sam-pling, or during the months in which the study wasundertaken (Table 3).

Discussion

Quadrats (Bilsing 1920; Edgar 1969) and sticky traps(Kajak 1965; Sunderland, Fraser & Dixon 1986b;Riechert 1991; Bradley 1993; Gillespie & Tabashnik1994; Marshall 1997) have been used previously tomonitor the potential prey of spiders, but very few ofthese studies were in agricultural habitats. This appearsto be the first study where both methods were appliedsimultaneously to individual web sites to obtain abalanced and spatially precise assessment of theavailability of potential prey. Overall, it revealed thatCollembola were the most abundant group of potentialprey. Biomass of prey items was not recorded in thisstudy, but it is likely that Diptera, Hymenoptera,Coleoptera and Aphididae would increase in relativeimportance if biomass were to be taken into account.Densities of potential prey (per cm2) were usually greateron mini-sticky traps than in mini-quadrats. This is, inpart, because the latter offer an instantaneous measureof prey availability, whereas the former represent anavailability rate (per 24 h in this case). It is, however,also likely that the cumulative differences are relatedto diel cycles in availability of prey to spiders in webson and near the ground (Vickerman & Sunderland1975; Leathwick & Winterbourn 1984; Sunderland

1996). Nocturnal prey availability could be animportant aspect of the trophic biology of agriculturallinyphiids because many species are particularly activeat night (Thornhill 1983; De Keer & Maelfait 1987b;Alderweireldt 1994b). The ratio of aerial species,such as Diptera and Hymenoptera, sampled by mini-sticky traps in relation to mini-quadrats was particu-larly high, indicating the likelihood of underestimatingthe presence of such species if quadrat sampling is usedalone. The ratio of Aphididae captured by mini-stickytraps in relation to quadrats was also relatively high,probably due to the presence of alate aphids descend-ing into the crop, and the high frequency with whichaphids are known to fall from the crop (Sunderland,Fraser & Dixon 1986b; Sopp, Sunderland & Coombes1987). It is clear, therefore, that use of daytime mini-quadrats alone would have seriously underestimatedthe abundance and diversity of prey available to spiders.

There was considerable temporal variation in preyavailability. Less than four prey items were available permini-sticky trap per day (c. 0·5 cm–2) in web sites duringMay and July. This is approximately equivalent to fouritems per day entering the 8-cm2 web of an adult femaleErigoninae spider (e.g. E. atra). If the 74-cm2 webs ofadult female Linyphiinae spiders (e.g. L. tenuis) wereon the ground they would receive a mean of 37 itemsper day, but as they are located up to 10 cm aboveground they will receive only falling prey, and thereforefail to benefit from the traffic of ground-active prey.This does not necessarily mean that these linyphiidswould receive less than this number of prey items,because their location may allow them to intercept andcapture more flying species than they would at groundlevel. Solid horizontal sticky traps at 10 cm aboveground caught half as many potential prey per unitarea as traps placed on the ground (Sunderland, Fraser& Dixon 1986a), but solid traps might not be appro-priate in an aerial location. Immature Linyphiidae,which constitute the vast majority of spiders during thegrowing season (Sunderland & Topping 1993; Topping& Sunderland 1998), have much smaller webs (16 cm2

for Linyphiinae and 3 cm2 for Erigoninae; Sunderland,Fraser & Dixon 1986a) and so will receive commen-surately fewer prey. In laboratory studies, immatureE. atra that received approximately one collembolan per

Table 3. Mean daily meteorological values (± SE) for climatic conditions in the months May, June and July during 1997 and 1998

Weather variable

Mean per day

1997 1998 F P

Maximum air temperature (°C) 18·23 ± 0·40 17·52 ± 0·40 1·47 0·227Minimum air temperature (°C) 7·76 ± 0·42 8·34 ± 0·35 1·07 0·302Soil temperature at 10 cm (°C) 14·85 ± 0·34 14·22 ± 0·37 1·55 0·214Rainfall (mm) 1·95 ± 0·34 2·17 ± 0·60 0·10 0·747Sunshine (h) 5·85 ± 0·40 4·83 ± 0·36 3·65 0·057Wind speed (m.p.h.) 8·50 ± 0·45 8·35 ± 0·39 0·07 0·795Rate of evaporation 2·60 ± 0·16 2·32 ± 0·16 1·63 0·203Relative humidity 75·93 ± 1·09 78·41 ± 0·99 2·83 0·094




day at 20 °C had markedly slower development ratesthan those that received an ad libitum supply (De Keer& Maelfait 1988). Immature E. atra in the currentstudy are estimated to have received approximately 1·5prey items per day in May and July, and so their devel-opment is likely to have been food-limited. De Keer &Maelfait (1988) also showed that adult female E. atrareceiving less that three adult Drosophila melanogasterMeigen (Diptera) per day at 20 °C produced fewer eggsthan those provisioned at higher rates. In May and July,adult female E. atra in our study would have receivedabout four prey items per day, which were mostly smallCollembola. The biomass of prey available was probablytherefore less than the equivalent of three Drosophilaand reproduction is likely to have been suboptimal. Thesituation was different in June, when prey availabilityincreased to 12 prey items per trap per day (c. 1·6 cm–2).The seasonal pattern of prey availability recorded inthis study matches the seasonal pattern of hungerassayed by Bilde & Toft (1998) for the linyphiid spiderOedothorax apicatus (Blackwall) in a Danish winterwheat field. They recorded hunger equivalent to 7 daysof starvation at 20 °C in May and July, but a value of 3–4 days starvation during June. These results suggestthat spiders are unlikely to exhibit prey preferences inMay and July, when they may need to capture whateverthey encounter in order to survive. In June, however,when prey availability is higher, it is possible that theywill reject cereal aphids (which were found to be less-preferred prey in laboratory trials; Toft 1995; Beck &Toft 2000) in favour of alternative prey.

The number of potential prey caught per trap duringa 4-week period was significantly greater in 1998 thanin 1997 and this difference did not appear to be directlydue to weather. However, different fields were invest-igated in the two years and so interfield variability mayexplain the observed differences. A full study of inter-field variation of potential prey availability (using themethods developed here) would be worthwhile, as itmight point to farming practices that are favourableand others that are deleterious in relation to fosteringthe alternative prey of generalist predators. This couldinclude a comparison of winter and spring cereals,as plant taxa that are important food resources forarthropod herbivores (= potential prey for generalistpredators) occur at greater densities in spring cereals(Hald 1999).

The linyphiid spiders at our study sites were notlocating their webs randomly with respect to the spatialdistribution of their food. This was true for all fieldsand sampling methods in 1997 and 1998. More poten-tial prey were available in the web sites of spiders thanin random non-web sites located up to 30 cm awayfrom the web. We do not have information at this stageto determine whether Linyphiidae are respondingdirectly to food availability or whether their aggrega-tion in prey-rich patches is a secondary outcome of aresponse to other microhabitat variables such as highhumidity and structural complexity of the vegetation.

Further studies would be useful, matching web andnon-web sites within crop rows and within spaces betweenrows, for example. It is possible that linyphiids weresimply responding passively to a lack of prey, relocat-ing at random until they reached areas of high preyavailability, where further movements were arrested. Infact, if Linyphiidae were selecting sites on the basis ofquality, the results suggest that their efficiency in select-ing high-quality web sites improved with progressionof season. Our results justify a full study of the deter-minants of microhabitat selection by linyphiid spidersin winter wheat. There are examples in the literature ofmicrohabitat selection being primarily driven by food, ormicroclimate, or physical structure of the microhabitat,or avoidance of conspecifics and enemies; the primedeterminant varies with habitat and species of spider(Samu & Sunderland 1999; Sunderland & Samu 2000).The fine-grain variation in the distribution of linyphiidsand their prey described in this study indicates thatmini-sampling techniques can be valuable for invest-igating spatial dynamics and predator–prey interactionsin agro-ecosystems, especially for small ‘sit-and-wait’strategist predators. There are a growing number ofstudies of the spatial dynamics of predators and prey inagro-ecosystems that employ nested sampling grids ata range of degrees of resolution, suitable for analysis bynew techniques such as Spatial Analysis by DistributionIndices (Perry 1995, 1998). For large, highly mobile,carabid beetles, grid scales ranging from 16 m downto 0·25 m have been demonstrated to be appropriate(Bohan et al. 2000). Our study suggests that for smaller,less-mobile, predators important information will belost unless finer scales are also included. Therefore, thescale should be chosen according to the species beinginvestigated.

Numbers of both spiders and Entomobryidae(Collembola), captured by mini-sticky traps andmini-quadrats, increased logarithmically as the seasonprogressed. At the same time, trap capture frequenciesof isotomid Collembola (Fig. 2c,d) showed a sharpdecline in July, when spider activity density was at amaximum. While it is possible that predation by spiders(and other natural enemies) was affecting populationdensities of isotomid Collembola (see below) this doesnot explain why capture frequencies of the Entomobry-idae continued to increase. One possible explanation isthat the Entomobryidae have powerful protectionmechanisms against predators (Bauer & Pfeiffer 1991).Figure 3 clearly indicates that entomobryid activitymust have been very low, with relatively few encounteringwebs, because the cumulative capture rates (mini-stickytraps) over time were not significantly different fromthe instantaneous densities (mini-quadrats). This toocould contribute to lower levels of predation. Altern-atively, Entomobryidae could be a non-preferredprey item, as the nutritive value of different speciesof Collembola is known to vary (Toft & Nielsen 1997).However, a number of other factors could be responsiblefor the differential trends in capture rates for the

JPE572.fm 6 Monday, March 5, 2001 11:48 AM



different groups of Collembola, including responsesto changing climatic conditions, or some species ofCollembola locating to different microhabitats suchas the large cracks which appear in the soil late in theseason. The negative relationship between numbers ofspiders and Collembola captured by mini-sticky trapsindicates that, as Collembola density decreases, spideractivity density increases. Increases in predator activity,in response to reduced prey availability, have been foundamongst other generalist predators such as carabid beetles(Chiverton 1984). However, increasing spider densitymay also be a factor. Although it is possible that theassociations between Collembola and linyphiid numberswere in part a result of predation, quantitative immuno-logical studies would be needed to confirm such a link inthe field (Symondson et al. 1996; Bohan et al. 2000).

A surprisingly large number of linyphiid spiders wascaptured on the mini-sticky traps. These were not theoriginal web owners returning to the web site becausewe removed and killed them as a routine part of thesampling protocol. Peak linyphiid densities (includingimmatures) in winter wheat are typically about 100 m–2

(Dinter & Poehling 1992; Sunderland & Topping 1993;Volkmar et al. 1994), which is equal to one spider per100 cm2, or 0·08 spiders per trap. The actual capturerate per trap peaked at 0·6 linyphiids day–1 (web sitesin July), which implies that either these spiders areextremely active throughout the field, or their activityis lower and concentrated in areas that they find attract-ive. Support for the latter hypothesis comes from thefact that peak capture rate on non-web mini-sticky trapswas only 0·3 trap–1 day–1. Thus, the sampling programmehas detected the aggregated and dynamic nature ofspider distribution in winter wheat. The dynamic aspectis likely to be due to males searching for females, andfemales searching for new web sites. Male linyphiids areknown to be, in general, more active than females, e.g.sex ratios in pitfall traps are strongly biased towardsmales (Sunderland 1987; Topping & Sunderland 1992),and they can be attracted to sex pheromones secretedonto web silk by the female (Watson 1986). Adult femalelinyphiids, such as L. tenuis, compete strongly fordesirable web sites, a larger female being able to evict asmaller one. Web site abandonment from this and othercauses results in the mean duration of an individualL. tenuis in a web site being less than 2 days (Samu et al.1996). These mechanisms probably contributed to thehigh capture rate on mini-sticky traps and are alsolikely to have caused a fairly high encounter rate betweenindividual spiders. Although, in general, spiders arehighly cannibalistic (Edgar 1969; Wise 1993), it is knownthat web-weavers (including Linyphiidae) are muchless so than hunters such as Lycosidae, Salticidae andThomisidae (Nyffeler 1999), and so the encountersimplied by the results from this study probably did notresult in high rates of mortality. We suggest, however,that mini-sticky traps could, more generally, be a usefultool for quantitative arachnological investigations ofintra- and interspecific interactions.

This study has shown that money spiders locate theirwebs in prey-rich areas of winter wheat fields. In spiteof this behaviour, which enables them to maximizetheir access to food, it seems likely that prey availabilityin May and July is not sufficiently great for them torealize fully their potential population growth rate.Studies are needed to find practical modifications tocurrent farming practice that will achieve enhancedprey availability, especially at times of year whenprey densities are low. The mini-sampling techniquesdeveloped here, especially when used in combination,will enable prey availability to be monitored moreefficiently in such prey-enhancement studies.

There is no certainty, however, that increased preyand spider density will always translate into improvedpest control (Sunderland & Samu 2000). Indeed, theincreased availability of high-quality alternative foodcould, to some extent, divert spiders from feeding onpests. Clearly, there is a need for manipulative fieldstudies to investigate rigorously the interactions betweenspiders, pests and alternative prey before sound recom-mendations can be made to optimize the spiderpredation component of pest control.

Acknowledgements

We are very grateful to John Fenlon (HRI) for statisticaladvice, Sally Mann (HRI) for meteorological data, andJørgen Axelsen (National Environmental ResearchInstitute, Silkeborg, Denmark) for Collembola identi-fication. J.D. Harwood was funded by a joint CardiffUniversity and HRI studentship, and K.D. Sunderlandby the UK Ministry of Agriculture Fisheries and Food.

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Received 9 October 1999; revision received 6 June 2000


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