JPE572.fm Page 88 Monday, March 5, 2001 11:48 AM
Journal of Applied Blackwell Science, Ltd Ecology 2001 Living where the food is: web location by linyphiid spiders 38, 88–99 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 to restrict pest population growth, but their populations may be food-limited under current farming regimes. This study aimed to quantify food availability to spiders in winter wheat and to determine whether spider web locations are positively associated with available food resources. 2. Mini-sticky traps (availability rate per 24 h, including prey falling from the crop) and mini-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 sites located randomly up to 30 cm away from each web. A total of 18 546 invertebrates were captured using these methods. 4. Overall, significantly more potential prey were available in web sites than in non-web sites (both on sticky traps and in quadrats). 5. Prey availability in May and July was about a third of that in June (both on sticky traps and in quadrats) and may have been below that known to be necessary for spiders to 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 spiders captured by mini-sticky traps and mini-quadrats increased exponentially as the season progressed. The high capture frequency in relation to population density, and the differential 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 about mate-searching and web site abandonment rates by the Linyphiidae. 7. The combination of techniques described here is recommended for monitoring prey availability in prey-enhancement programmes and may prove useful in quantitative studies of both intra- and interspecific interactions between spiders. Key-words: aggregative responses, Collembola, generalist predators, mini-quadrats, mini-sticky traps. Journal of Applied Ecology (2001) 38, 88–99
because of the associated cumulative problems (such as Introduction pest resistance and environmental pollution) that render In Britain, the area of cereal crops treated with pesti- pesticide-based agriculture unsustainable (Pimentel cide has increased by 24% since 1994, with a concomit- 1995). Biological control is a strong alternative option, ant 16% increase in the amount of active ingredients and for the majority of low-value outdoor European applied ( Thomas, Garthwaite & Banham 1996). Although crops this must be achieved through conservation of chemical pesticides are convenient to use, and often endemic biocontrol agents (i.e. ‘conservation biological efficient and cost-effective in the short term, it is control’; Ehler 1998) rather than by classical biological now appreciated that they are not a long-term option control or rear-and-release methods. Small soft-bodied pests (such as aphids) that are accessible on the vegeta- © 2001 British Correspondence: Dr W.O.C. Symondson (fax 02920 874305; tion and ground surface, are attacked by a range of Ecological Society e-mail [email protected]). natural enemies (pathogens, parasitoids, specialist and
JPE572.fm Page 89 Monday, March 5, 2001 11:48 AM
89 generalist natural enemies) that interact in complex large sticky traps (Kajak 1965; Sunderland, Fraser & Web location by ways (Sunderland et al. 1997). Generalist predators Dixon 1986b) fail to provide density estimates, or seriously linyphiid spiders (e.g. spiders, carabid and staphylinid beetles) have the underestimate density (Sunderland & Topping 1995; valuable attribute of being able to subsist on alternative Sunderland et al. 1995), and lack the spatial precision non-pest prey. They can therefore either simply be needed for this study. present in the field before the pest arrives, performing a To be able ultimately to optimize the spatial dis- lying-in-wait strategy (Murdoch, Chesson & Chesson tribution of within-field diversified prey resource it is 1985; Chang & Kareiva 1999), or build up their popu- necessary to know how efficiently and dynamically lations on alternative foods early in the season and spiders are capable of relocating their webs in relation then impact on the pest population with a favourable to temporal and spatial fluctuations of prey availability. predator : pest ratio during the early phase of pest Some web-building spiders are known to be efficient in population growth (Settle et al. 1996). Manipulative this respect (McNett & Rypstra 1997) but others are field experiments have demonstrated that generalist relatively insensitive to prey availability (Schaefer 1978). predators can often (Edwards, Sunderland & George There are, however, very few such studies of spiders in 1979; Chiverton 1986; Duffield et al. 1996), but not agricultural habitats (Sunderland & Samu 2000). always (Holland & Thomas 1997), contribute to com- In this study we (i) quantified spatial and temporal mercially valuable reductions of aphid populations variation in the availability of potential prey to web- on wheat. Web-building species of money spider building linyphiid spiders in fields of winter wheat, (Linyphiidae), such as Lepthyphantes tenuis (Blackwall) using a combination of ‘instantaneous’ and cumulative and Erigone atra (Blackwall), consume cereal aphids sampling techniques, and (ii) determined whether web (Sunderland et al. 1987) and trap considerable num- location is correlated spatially with the abundance of bers in their horizontal sheet webs (Sunderland, Fraser potential prey. As far as we know, this is the first time & Dixon 1986a; Alderweireldt 1994a), which can cover that these topics have been investigated in an agricul- up to half of the surface area of a wheat field (Sunder- tural setting. land, Fraser & Dixon 1986b). Death of pests trapped in webs may contribute to pest control even if the spider Methods does not consume them (Sunderland 1999). Reviews of the literature have demonstrated that spider density is likely to be increased by within-crop habitat diversification (Samu & Sunderland 1999; Sun- The study sites were winter wheat (cv. ‘Hereward’) derland & Samu 2000). The mechanisms underlying fields of approximately 7 ha planted on a predom- this effect are not fully understood but it is probable inantly sandy loam soil at Horticulture Research that prey diversification is an important factor. Labo- International (HRI), Wellesbourne, Warwickshire, ratory investigations suggest that the value of different UK (52°12.18′ N, 1°36.00′ W). The fields were farmed prey types for supporting spider population growth according to standard farming practice and no varies greatly between major taxonomic groups (orders insecticide applications were required during the and families) of prey (Toft 1995; Sunderland et al. period of investigation. The study sites were sur- 1996; Beck & Toft 2000; Bilde, Axelsen & Toft 2000) rounded by fields of spring barley, winter barley, and even between congeneric species [e.g. between the winter wheat and by hay meadows. collembolans Isotoma anglicana Lubbock and Folsomia candida Willem (Toft & Nielsen 1997; K.D. Sunderland, J.D. Harwood & W.O.C. Symondson, unpublished data) and Isotoma tigrina Nicolet (T. Bilde & S. Toft, Sampling was carried out from late April until harvest unpublished data)]. To guide the future development (in late July/early August) in 1997 and 1998. The abun- of improved practical techniques aimed at enhancing dance of invertebrates (including potential prey) was spider populations and increase their impact on pests, determined by two different ground-based sampling quantitative information (from the field or under methods: mini-sticky traps and mini-quadrats. These simulated field conditions) will be needed on (i) the methods were designed to be small and precise enough absolute and relative availability of different prey types, to monitor potential prey in the immediate area of a (ii) prey preferences, and (iii) diet-related spider popu- web without the interference of ‘sampling noise’ from lation growth rates. In this paper we address the first of invertebrates that would never be encountered by the these aims and develop the methodology needed to spiders. They also form a complementary pair of methods; quantify prey availability in the field. For this purpose the mini-sticky trap is a passive sampling technique that it is necessary to quantify how many prey are available relies on activity of the prey, but can sample throughout close to the webs of individual spiders, which are to be 24 h and catch prey that fall or descend from higher © 2001 British found on the ground or up to 10 cm above the ground strata, whereas collection from a mini-quadrat is an Ecological Society, Journal of Applied (Sunderland, Fraser & Dixon 1986a). Sampling methods active sampling method, confined to the ground during Ecology, 38, such as vacuum insect nets (Potts & Vickerman 1974; a very limited time period (thus providing an ‘instan- 88–99 Moreby et al. 1994), pitfall traps (Nentwig 1982) and taneous’ density estimate). The use of mini-quadrats
JPE572.fm Page 90 Monday, March 5, 2001 11:48 AM
90 enables the collection of potential prey that are tem- Comparisons between web-centred and non-web- J.D. Harwood, porarily inactive and hiding under weeds, small stones centred mini-sticky traps were made from mid-June to K.D. Sunderland & and at the bases of cereal stems. mid-July in 1997 (n = 120 paired samples), and a more W.O.C. Symondson The plastic mini-sticky traps were 7·5 cm2 (1·5 cm extensive monitoring programme performed in 1998 at × 5 cm, 2 mm thick), which is of comparable area to regular intervals from late April until harvest (n = 250). webs constructed by the common erigonid spiders Mini-quadrats were used to sample the abundance of E. atra and Erigone dentipalpis (Wider) (Sunderland, potential prey during July 1997 (n = 52) and from late Fraser & Dixon 1986a; Alderweireldt 1994a). The traps April until harvest in 1998 (n = 271). No comparisons were coloured with black acrylic paint (to minimize were made for quadrat catches between the two years visual attraction by merging in colour with the ground due to the different sampling dates. surface) and were covered on the upper side with a thin acetate sheet coated with Oecotak A5, a non-toxic polybutene-based adhesive (Oecos, Kimpton, UK). The black traps were unlikely to absorb much addi- Meteorological data (maximum and minimum air tem- tional heat from sunlight because they were placed on peratures; soil temperature; rainfall; hours of sunshine; the ground surface, and were therefore shaded by the wind speed; rate of evaporation; relative humidity) winter wheat. After traps were removed from the field, were obtained from the weather station located at HRI the detachable acetate sheet was placed in a bath of Wellesbourne, which was within 1200 m of all field sites. white spirit to dissolve the Oecotak, enabling recovery of trapped invertebrates into alcohol for storage and later identification. The mini-quadrats were circular sampling areas (diameter 10 cm, area approximately To stabilize variances, all sample data were transformed 2 78·5 cm ) defined by a template. These were placed (log10 (x + 1)) prior to analyses. For the purposes of on the ground, surrounding the web or non-web site. making direct comparisons between mini-sticky traps All invertebrates were collected from within the mini- and mini-quadrats, data were converted into standard quadrat by pooter, searching under loose soil and unit areas (per cm2). Analysis of variance () was vegetation. used to analyse potential prey populations captured by Sheet webs were located at random within the study mini-sticky traps and mini-quadrats. Catches of potential fields, and linyphiid spiders present within these webs prey were pooled over time for comparisons of web vs. were captured and preserved for subsequent identifica- non-web sites, and mini-sticky traps verses mini-quadrats. tion. Vacant webs were not categorized as web sites A non-parametric Mann–Whitney U-test was used because spiders are known to leave their webs in active where the assumptions of could not be met, and pursuit of prey (Alderweireldt 1994a; Schütt 1995) or paired sample t-tests were used to compare numbers abandon their web sites (Samu et al. 1996) in search of of individual prey taxa captured by web and non-web more profitable hunting grounds (Vollrath 1985; Gillespie traps. Where less common prey taxa were analysed, & Caraco 1987). Therefore, only webs in which linyphiid data were grouped into means per sampling session spiders were present were included in the analysis. The and the analysis was performed on mean numbers webs were removed because spiders are known to be captured per session. attracted by the presence of silk (Leborgne & Pasquet Potential prey items in the samples were separated 1987; Hodge & Storfer-Isser 1997). This also minimized from other invertebrates on the basis of size (the any potential interference with the traps. One mini-sticky linyphiid species found in winter wheat are rarely able trap was centred horizontally on the ground at the to capture and kill prey > 5 mm long) and in relation position from which a web was removed, and another to information from the published literature for prey placed at a random non-web site nearby (up to 30 cm of linyphiids in European arable crops (Sunderland, away). Sampling was always carried out in pairs, to Fraser & Dixon 1986a; De Keer & Maelfait 1987a, enable direct comparisons between each set of traps, 1988; Nyffeler & Benz 1988; Alderweireldt 1994a; which were left in situ for 24 h. Great care was taken Jmhasly & Nentwig 1995; Toft 1995) and the results of not to disturb surrounding vegetation and dislodge laboratory prey acceptability trials (K.D. Sunderland, arthropods onto the traps during placement and unpublished data). collection. When sampling by mini-quadrat, the same pair- Results wise sampling procedure was used as described above for mini-sticky traps. The ground within the mini- Data for web sites of all Linyphiidae were pooled and quadrat was searched thoroughly, and all arthropods analysed collectively. Table 1 shows the numbers of present were transferred immediately into alcohol. each species/genus/subfamily of spider captured at web © 2001 British No attempt was made to collect arthropods from the sites prior to sampling by mini-sticky traps and quadrats Ecological Society, Journal of Applied crop vegetation above the mini-quadrat. Samples (i.e. the web owners). The total numbers of linyphiids Ecology, 38, were taken during the daytime between 08.00 hours recorded exceeded the number of web sites because, 88–99 and 16.00 hours. occasionally, more than one spider was present in a web.
JPE572.fm Page 91 Monday, March 5, 2001 11:48 AM
91 Table 1. Number of each species/genus/subfamily caught in web sites prior to sampling by mini-sticky traps (MS) and mini- Web location by quadrats (MQ) during 1997 and 1998 linyphiid spiders Species/genus/subfamily 1997 MS 1997 MQ 1998 MS 1998 MQ
Erigone atra (Blackwall) 25 5 54 76 Erigone dentipalpis (Wider) 18 4 32 34 Milleriana inerrans (O.P.-Cambridge) 3 1 – – Oedothorax spp. 2 2 6 19 Lepthyphantes tenuis (Blackwall) 25 25 103 113 Bathyphantes gracilis (Blackwall) – 1 37 23 Meioneta rurestris (C.L. Koch) 39 6 8 11 Porrhomma errans (Blackwall) – – 1 – Micrargus subaequalis (Westring) 1 – – – Pachygnatha degeeri Sundevall 1 – 1 – Erigoninae juveniles 10 5 12 10 Linyphiinae juveniles 9 7 9 9 Total 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 within web 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.
per cm2, than were found in mini-quadrats (instanta- © 2001 British neous sampling during the day) (F = 5·67, P < 0·001). Ecological Society, 1,340 Journal of Applied However, comparisons between individual prey taxa Ecology, 38, In 1997, web-centred mini-sticky traps (cumulative were not possible due to the small number of sampling 88–99 sampling over 24 h) caught more potential prey items, dates (n = 4 for both mini-sticky traps and mini-quadrats).
JPE572.fm Page 92 Monday, March 5, 2001 11:48 AM
92 J.D. Harwood, K.D. Sunderland & W.O.C. Symondson
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 traps from May to July 1998. Bars are ± SE.
Similarly in 1998, significantly more potential prey monitored by both mini-sticky traps (F1,480 = 96·69, 2 items were captured, per cm , by web-centred mini-sticky P < 0·001) and mini-quadrats (F1,520 = 75·51, P < 0·001).
traps than by web-centred mini-quadrats (F1,1038 = 1199·43, The temporal abundance of potential prey in 1998 was
P < 0·001). There were also large differences between found to be highly variable (F9,480 = 28·45, P < 0·001) the two methods in the numbers of certain invertebrate (Fig. 2a). taxa captured during both 1997 and 1998 (Fig. 1). Collembola, which constituted > 60% of all poten-
Significantly more Collembola (F1,1038 = 532·05, P < tial prey items captured by web-centred mini-sticky 0·001), Diptera (Mann–Whitney, U = 0·0, n = 35, traps during 1998, were significantly more abundant in P < 0·001), Hymenoptera (U = 64·0, n = 35, P < 0·01) web sites (mean per cm2 = 0·60 ± 0·04) than in non-web 2 ± and Araneae (U = 77·5, n = 35, P < 0·05) were caught sites (mean per cm = 0·26 0·02) (F1,480 = 109·02, by web-centred mini-sticky traps than were sampled by P < 0·001). Similar distribution patterns were also web-centred mini-quadrats. There were large differ- evident when individual species of Collembola were ences in the ratio of individual prey taxa captured, per analysed. The two most abundant isotomid collembolans, cm2, between the two sampling methodologies (Fig. 1). I. anglicana (sensu. Fjellberg 1980) and Isotomurus The small dipterans that were classified as potential palustris Müller, were present in greater densities on prey were especially diverse, with representatives web-centred, than on non-web, mini-sticky traps (I.
from the families Cecidomyiidae, Lonchopteridae, anglicana: F1,480 = 39·69, P < 0·001; I. palustris: F1,18 = Phoridae, Sciaridae, Mycetophilidae, Drosophilidae 6·41, P < 0·05) and in mini-quadrats (I. anglicana:
and Dolichopodidae. F1,520 = 29·59, P < 0·001; I. palustris: F1,520 = 22·54, P < 0·001). The temporal capture frequencies of these species, and of Collembola as a whole, on mini-sticky traps varied significantly throughout the monitoring
In 1997, significantly more potential prey items were period (Fig. 2b–d) (all Collembola: F9,480 = 45·56, P < captured in sites where Linyphiidae had constructed 0·001; I. anglicana: F = 55·60, P < 0·001; I. palustris: © 2001 British 9,480 their webs than in non-web sites, as monitored by F = 17·22, P < 0·001). Similar significant differences Ecological Society, 9,480 Journal of Applied both mini-sticky traps (F1,238 = 6·80, P < 0·01) and between numbers captured over time were recorded by Ecology, 38, mini-quadrats (F1,102 = 12·22, P < 0·01). Similar results mini-quadrat sampling (all Collembola: F10,520 = 59·67,
88–99 were found in 1998, on different fields, again when P < 0·001; I. anglicana: F10,520 = 99·30, P < 0·001;
JPE572.fm Page 93 Monday, March 5, 2001 11:48 AM
93 Web location by linyphiid spiders
Fig. 3. Mean number of entomobryid collembolans (Lepidocyrtus cyaneus and Entomobrya multifasciata) captured per cm2 by
web-centred mini-sticky traps and mini-quadrats during 1998. Points are log10 (means) for individual sampling occasions. 2 Mini-sticky trap regression: log10 y = 0·00648x – 0·117, r = 0·80, t14 = 7·10, P < 0·001. Mini-quadrat regression: log10 y = 0·00862x 2 – 0·164, r = 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 of a mini-sticky trap (7·5 cm2) is approximately a tenth that of a mini-quadrat (78·5 cm2). Mean number of Araneae captured per web-centred mini-quadrat are presented as (x + 1) to account for the web owner
Mean per web Mean per non-web Ratio web/ Variable t d.f. P site ± SE site ± SE non-web
(a) Mini-sticky traps Collembola 7·52 14 < 0·001 4·48 ± 0·31 1·93 ± 0·18 2·32 Diptera 1·02 14 0·326 0·29 ± 0·04 0·25 ± 0·03 1·16 Hymenoptera 1·32 14 0·209 0·14 ± 0·03 0·08 ± 0·02 1·75 Coleoptera 2·02 14 0·063 0·12 ± 0·02 0·06 ± 0·01 2·00 Aphididae 1·49 14 0·157 0·20 ± 0·04 0·11 ± 0·02 1·81 Araneae 4·26 14 0·001 0·30 ± 0·04 0·08 ± 0·02 3·75 (b) Mini-quadrats Collembola 10·85 19 < 0·001 27·66 ± 1·81 13·66 ± 1·12 2·02 Diptera 3·24 19 0·004 0·20 ± 0·03 0·08 ± 0·02 2·50 Hymenoptera 3·94 19 0·001 0·08 ± 0·02 0·04 ± 0·01 2·00 Coleoptera 5·25 19 < 0·001 0·75 ± 0·07 0·34 ± 0·04 2·21 Aphididae 1·40 19 0·117 0·21 ± 0·04 0·16 ± 0·03 1·31 Araneae 32·47 19 < 0·001 1·78 ± 0·08 0·19 ± 0·04 9·37
I. palustris: F10,520 = 77·06, P < 0·001). However, despite catches between the two years due to the different samp- this temporal variability, more Collembola (total and ling dates. However, during 1998 the density of Entom- isotomid) were captured on all dates at web-centred obryidae increased logarithmically as the season sites, regardless of sampling method. progressed (Fig. 3). Analysis of covariance indicated The entomobryid collembolans Lepidocyrtus cyaneus that there was no significant difference between the
Tullberg and Entomobrya multifasciata (Tullberg) slopes for mini-sticky traps and quadrats (F1,31 = 0·40,
constituted 25·4% of total potential prey items on P > 0·05) or the y-axis intercepts (F1,31 = 0·52, P > 0·05). mini-sticky traps and 57·6% in mini-quadrats in 1997, Linyphiidae were significantly more abundant in although this difference was not significant. They were web than non-web sites both on mini-sticky traps and relatively less dominant in 1998 (5·6% for mini-sticky in mini-quadrats, and Diptera, Hymenoptera and traps and 14·3% for mini-quadrats), with no significant Coleoptera were more abundant in web than non-web © 2001 British difference between the two sampling methods, although sites within mini-quadrats (Table 2). The sex ratio of Ecological Society, Journal of Applied there was a significant difference in numbers captured spiders captured also varied considerably. Male linyph- Ecology, 38, by mini-sticky traps between the two years (U = 6198·5, iids were captured on significantly more occasions than 88–99 n = 240, P < 0·05). No comparison was made for quadrat females on mini-sticky traps in web sites (U = 56·5, JPE572.fm Page 94 Monday, March 5, 2001 11:48 AM
94 J.D. Harwood, K.D. Sunderland & W.O.C. Symondson
Fig. 4. Mean number of Linyphiidae sampled by web and non-web-centred mini-quadrats during 1998. Data for web quadrats 2 are presented as log10(x + 1) to account for the web owner. Web regression: log10y = 0·00621x – 0·080, r = 0·72, t19 = 6·78, 2 P < 0·001. Non-web regression: log10y = 0·00330x – 0·360, r = 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: 2 2 log10y = 0·00388x – 0·395, r = 0·37, t14 = 2·73, P < 0·05. Non-web regression: log10y = 0·00195x – 0·250, r = 0·45, t14 = 3·25, P < 0·01.
n = 30, P < 0·01); 3·3 times more male than female within web sites also increased when regressed against spiders were also collected in non-web traps, although maximum air temperature (mini-sticky traps: r2 = 0·27, 2 these differences were not statistically significant. t14 = 2·18, P < 0·05; mini-quadrats: r = 0·57, t19 = 4·91, Linyphiid density, monitored by mini-quadrat P < 0·001) and soil temperature (mini-quadrats: 2 sampling, increased logarithmically with time (Fig. 4). r = 0·53, t19 = 4·47, P < 0·001). Analysis of covariance indicated a significant difference A negative relationship was found to exist between between the slopes of the web and non-web regressions the number of Linyphiidae and Collembola captured
(F1,36 = 7·17, P < 0·05) and the y-axis intercepts (F1,36 = by web-centred mini-sticky traps (log10 Linyphiidae = 2 76·51, P < 0·001), showing that linyphiid density was –0·721 log10 Collembola + 0·636, r = 0·40, t14 = 2·97, increasing more rapidly at web sites. The number of P < 0·05). No such relationship was found using data linyphiids captured by mini-sticky traps (both web and from mini-quadrats. non-web) showed a similar pattern (Fig. 5) but analysis of covariance indicated no significant difference between © 2001 British - the two slopes (F = 1·57, P > 0·05) or y-axis intercepts Ecological Society, 1,26 Journal of Applied (F1,26 = 0·32, P > 0·05), but the two slopes are signific- Ecology, 38, antly different from zero (F1,26 = 14·28, P < 0·01). The From the comparison of 4 consecutive weeks (mid-June
88–99 log10 number of spiders captured by these methods to mid-July) of mini-sticky trap data collected during JPE572.fm Page 95 Monday, March 5, 2001 11:48 AM
95 Table 3. Mean daily meteorological values (± SE) for climatic conditions in the months May, June and July during 1997 and 1998 Web location by linyphiid spiders Mean per day Weather variable 1997 1998 FP
Maximum air temperature (°C) 18·23 ± 0·40 17·52 ± 0·40 1·47 0·227 Minimum air temperature (°C) 7·76 ± 0·42 8·34 ± 0·35 1·07 0·302 Soil temperature at 10 cm (°C) 14·85 ± 0·34 14·22 ± 0·37 1·55 0·214 Rainfall (mm) 1·95 ± 0·34 2·17 ± 0·60 0·10 0·747 Sunshine (h) 5·85 ± 0·40 4·83 ± 0·36 3·65 0·057 Wind speed (m.p.h.) 8·50 ± 0·45 8·35 ± 0·39 0·07 0·795 Rate of evaporation 2·60 ± 0·16 2·32 ± 0·16 1·63 0·203 Relative humidity 75·93 ± 1·09 78·41 ± 0·99 2·83 0·094
1997 (mean number of total potential prey captured 1996). Nocturnal prey availability could be an per web site = 3·12 ± 0·22, non-web site = 2·38 ± 0·20) important aspect of the trophic biology of agricultural with a data set for the same calendar period during linyphiids because many species are particularly active 1998 (mean number per web site = 5·69 ± 0·50, non-web at night (Thornhill 1983; De Keer & Maelfait 1987b; site = 3·95 ± 0·27), the mean number of arthropods Alderweireldt 1994b). The ratio of aerial species, captured during the second year was significantly greater such as Diptera and Hymenoptera, sampled by mini-
(F1,476 = 20·55, P < 0·001). sticky traps in relation to mini-quadrats was particu- larly high, indicating the likelihood of underestimating the presence of such species if quadrat sampling is used - alone. The ratio of Aphididae captured by mini-sticky Despite the large variation in the numbers of arthro- traps in relation to quadrats was also relatively high, pods captured between years, there was no evidence to probably due to the presence of alate aphids descend- suggest that meteorological factors were responsible ing into the crop, and the high frequency with which for such variability. Comparisons of data from 1997 aphids are known to fall from the crop (Sunderland, and 1998 indicated that no category of meteorological Fraser & Dixon 1986b; Sopp, Sunderland & Coombes data varied significantly in the 4 weeks prior to sam- 1987). It is clear, therefore, that use of daytime mini- pling, or during the months in which the study was quadrats alone would have seriously underestimated undertaken (Table 3). the abundance and diversity of prey available to spiders. There was considerable temporal variation in prey availability. Less than four prey items were available per Discussion mini-sticky trap per day (c. 0·5 cm–2) in web sites during Quadrats (Bilsing 1920; Edgar 1969) and sticky traps May and July. This is approximately equivalent to four (Kajak 1965; Sunderland, Fraser & Dixon 1986b; items per day entering the 8-cm2 web of an adult female Riechert 1991; Bradley 1993; Gillespie & Tabashnik Erigoninae spider (e.g. E. atra). If the 74-cm2 webs of 1994; Marshall 1997) have been used previously to adult female Linyphiinae spiders (e.g. L. tenuis) were monitor the potential prey of spiders, but very few of on the ground they would receive a mean of 37 items these studies were in agricultural habitats. This appears per day, but as they are located up to 10 cm above to be the first study where both methods were applied ground they will receive only falling prey, and therefore simultaneously to individual web sites to obtain a fail to benefit from the traffic of ground-active prey. balanced and spatially precise assessment of the This does not necessarily mean that these linyphiids availability of potential prey. Overall, it revealed that would receive less than this number of prey items, Collembola were the most abundant group of potential because their location may allow them to intercept and prey. Biomass of prey items was not recorded in this capture more flying species than they would at ground study, but it is likely that Diptera, Hymenoptera, level. Solid horizontal sticky traps at 10 cm above Coleoptera and Aphididae would increase in relative ground caught half as many potential prey per unit importance if biomass were to be taken into account. area as traps placed on the ground (Sunderland, Fraser Densities of potential prey (per cm2) were usually greater & Dixon 1986a), but solid traps might not be appro- on mini-sticky traps than in mini-quadrats. This is, in priate in an aerial location. Immature Linyphiidae, part, because the latter offer an instantaneous measure which constitute the vast majority of spiders during the of prey availability, whereas the former represent an growing season (Sunderland & Topping 1993; Topping availability rate (per 24 h in this case). It is, however, & Sunderland 1998), have much smaller webs (16 cm2 © 2001 British also likely that the cumulative differences are related for Linyphiinae and 3 cm2 for Erigoninae; Sunderland, Ecological Society, Journal of Applied to diel cycles in availability of prey to spiders in webs Fraser & Dixon 1986a) and so will receive commen- Ecology, 38, on and near the ground (Vickerman & Sunderland surately fewer prey. In laboratory studies, immature 88–99 1975; Leathwick & Winterbourn 1984; Sunderland E. atra that received approximately one collembolan per JPE572.fm Page 96 Monday, March 5, 2001 11:48 AM
96 day at 20 °C had markedly slower development rates Further studies would be useful, matching web and J.D. Harwood, than those that received an ad libitum supply (De Keer non-web sites within crop rows and within spaces between K.D. Sunderland & & Maelfait 1988). Immature E. atra in the current rows, for example. It is possible that linyphiids were W.O.C. Symondson study are estimated to have received approximately 1·5 simply responding passively to a lack of prey, relocat- prey items per day in May and July, and so their devel- ing at random until they reached areas of high prey opment is likely to have been food-limited. De Keer & availability, where further movements were arrested. In Maelfait (1988) also showed that adult female E. atra fact, if Linyphiidae were selecting sites on the basis of receiving less that three adult Drosophila melanogaster quality, the results suggest that their efficiency in select- Meigen (Diptera) per day at 20 °C produced fewer eggs ing high-quality web sites improved with progression than those provisioned at higher rates. In May and July, of season. Our results justify a full study of the deter- adult female E. atra in our study would have received minants of microhabitat selection by linyphiid spiders about four prey items per day, which were mostly small in winter wheat. There are examples in the literature of Collembola. The biomass of prey available was probably microhabitat selection being primarily driven by food, or therefore less than the equivalent of three Drosophila microclimate, or physical structure of the microhabitat, and reproduction is likely to have been suboptimal. The or avoidance of conspecifics and enemies; the prime situation was different in June, when prey availability determinant varies with habitat and species of spider increased to 12 prey items per trap per day (c. 1·6 cm–2). (Samu & Sunderland 1999; Sunderland & Samu 2000). The seasonal pattern of prey availability recorded in The fine-grain variation in the distribution of linyphiids this study matches the seasonal pattern of hunger and their prey described in this study indicates that assayed by Bilde & Toft (1998) for the linyphiid spider mini-sampling techniques can be valuable for invest- Oedothorax apicatus (Blackwall) in a Danish winter igating spatial dynamics and predator–prey interactions wheat field. They recorded hunger equivalent to 7 days in agro-ecosystems, especially for small ‘sit-and-wait’ of starvation at 20 °C in May and July, but a value of 3– strategist predators. There are a growing number of 4 days starvation during June. These results suggest studies of the spatial dynamics of predators and prey in that spiders are unlikely to exhibit prey preferences in agro-ecosystems that employ nested sampling grids at May and July, when they may need to capture whatever a range of degrees of resolution, suitable for analysis by they encounter in order to survive. In June, however, new techniques such as Spatial Analysis by Distribution when prey availability is higher, it is possible that they Indices (Perry 1995, 1998). For large, highly mobile, will reject cereal aphids (which were found to be less- carabid beetles, grid scales ranging from 16 m down preferred prey in laboratory trials; Toft 1995; Beck & to 0·25 m have been demonstrated to be appropriate Toft 2000) in favour of alternative prey. (Bohan et al. 2000). Our study suggests that for smaller, The number of potential prey caught per trap during less-mobile, predators important information will be a 4-week period was significantly greater in 1998 than lost unless finer scales are also included. Therefore, the in 1997 and this difference did not appear to be directly scale should be chosen according to the species being due to weather. Howev