SPATIAL ASSOCIATION BETWEEN A SPIDER WASP AND ITS HOST IN FRAGMENTED DUNE HABITATS

2005·9 MB·English

by  Dries Bonte

2005. The Journal of Arachnology 33:222-229
SPATIAL ASSOCIATION BETWEEN A SPIDER WASP AND
ITS HOST IN FRAGMENTED DUNE HABITATS
Dries Bonte^ and Jean-Pierre MaelfaiP’^: *Ghent University, Dep. Biology, Research
group Terrestrial Ecology, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium. E-mail:
[email protected]; ^Institute of Nature Conservation, Kliniekstraat 25, B-1070
Brussels, Belgium
ABSTRACT, In patchily distributed habitats, species potentially occur whereverconditions are suitable
or show arestricted distribution, influenced by patch quality, geometry andconfiguration. Ifpatchisolation
appears to be the main determinant of the species’ distribution then dispersal ability is supposed to be
limited. Although only scarce literature is available, dispersal limitation seems to be an important factor
in determining the spatial population structure in spiders. In this paper, we document on the spatial
population structure of the rare wolf spiderAlopecosafabrilis, restricted to fragmented grey dunes along
the Flemish coast (Belgium) and ask whether its distribution appears to be affected by aspects of patch
configuration. Simultaneously, we investigated whether the local distribution of its main parasitoid, the
spider wasp Arachnospila nifa (Hymenoptera, Pompilidae) was associated with its host. Our results in-
dicate that A. fabrilis shows an aggregative population structure, which is determined by the distance to
nearest occupied patch, indicating that spatially correlated habitat quality probably determine its occur-
rence. Although spider wasps are generally characterized as non-specialists, the almost complete covari-
ation between its spatial occurrence and that of A. fabrilis, indicates that spider hunting wasps may, at
least temporally and locally, show a restricted host-range. As a result, the presence of a rather generalist
parasitoid is a good predictor for the presence of nocturnal and burrowing dune wolf spider.
Keywords: Alopecosafabrilis, Lycosidae, Arachnospila rufa, Pompilidae, metapopulations
In fragmented habitats, species live either odology to study dispersal abilities or
in patchy populations or in metapopulations populations viability with respect to popula-
(Harrison 1991; Hanski 1999). In patchy pop- tion size (patch size) resulting from historical
ulations, individuals move freely among hab- habitat fragmentation and population dynam-
itat patches, while in metapopulations, most ics. As shown for a coastal dune wolf spider,
individuals stay in a single patch during their living in fragmented grassland habitats, patch
entire life, but dispersing individuals enhance occupancy patterns may depend both on as-
strong colonization-extinction dynamics. This pects ofhabitat quality and on differentmodes
results in a population structure in which some of dispersal through the surrounding matrix
suitable patches remain vacant. Besides the (Bonte et al. 2003a). For spiders in general,
colonization abilities, changes in habitat qual- cursorial dispersal and ballooning induce dif-
ity can also attribute to local extinction dy- ferent colonization and extinction patterns, de-
namics, as demonstrated for specialized but- pendent on the species' mobility, its niche
terflies (e.g. Thomas et al. 1992; Ravenscroft breadth and its propensity for aerial dispersal
1994; Moilanen & Hanski 1998; Bergman (Bonte et al. 2003a, 2004b). Especially bal-
1999) and backswimmers of the genus Noto- looning dispersal appears to be important for
&
necta (Briers Warren 2000). Therefore, occupancy patterns at extended temporal and
studying the spatial structure of populations spatial scales (Bonte et al. 2003a, 2004a),
during successive years by considering as- while cursorial dispersal induces short-term
pects of patch geometry, quality and config- colonization events at small spatial and tem-
uration enables us to assess actual dispersal poral scales (Bonte et al. 2003a). For spiders,
limitation and population dynamics in an in- direct estimates of realized dispersal are rare
direct way. Snapshots of patch-occupancy in- and indicate dispersal distances up to few-
cidences provide an alternative indirect meth- hundred meters within suitable habitat (Krei-
222
BONTE & MAELFAIT—ASSOCIATION BETWEEN SPIDER WASP AND HOST 223
ter & Wise 2001; Bonte et aL 2003a; Samu et oid could be an indicator for the presence of
al. 2003) but restricted dispersal up to few me- populations of a nocturnal, fossorial spider.
ters in unsuitable, often densely vegetated METHODS
habitat (Bonte et al. 2003a). Indirect estimates —
of dispersal, estimated by population genetic Study Area, Study Species. Fieldwork
analyses, are more common (e.g. Boulton et was conducted in the Flemish coastal dunes,
al. 1998; Ramirez & Fandino 1996; Ramirez located between the cities of De Panne (Bel-
& Haakonsen 1999; Gurdebeke et al. 2000). gium) and Bray-Dunes, France (51°05'N,
In contrast to the latter, studies on occupancy 2°32'E) consisting of 52 discrete grey dune
incidences, ideally conducted during several patches, varying between 0.05 and 27.6 ha
successive years, reveal indirect estimates of (Fig. i). Grey dunes, known as “Fixed coastal
dispersal that are independent of historical dunes” are most readily defined using plant
bottlenecks and selectionpressures in spatially communities. Vegetation includes Atlantic
structured habitats (Peterson et al. 2001; Bon- moss dominated dunes (mainly Tortula rur-
te et al. 2003a). alis) as well as dune grassland (with a distinct
In addition to earlier studies on the mobile organic soil layer) belonging to the Cladonio-
wolf spider Pardosa monticola (Clerck 1757), Koelerietalia syntaxon in case of lime rich
we here report on the population structure in grey dune, and to the Trifolio-Festucetaliaovi-
coastal dune habitats of the specialized fos- nae syntaxon in case ofdecalcified grey dunes
sorial wolf spider Alopecosa fabrilis (Clerck (Provoost et al. 2002). In this study, only grey
1757) with limited aerial dispersal abilities dunes without substantial soil development
(Bonte et al. 2003b) and of its main (winged) were surveyed since they are the habitat of
parasitoid, Arachnospila rufa (Haupt 1927) both study species (see further). Ecologically
(Hymenoptera, Pompilidae), knowing to host it is merely the dry component of the
on larger Alopecosa wolf spiders (Koomen & “stressed dune landscape”. The main differ-
Peeters 1993; Peelers et al. 1994). According entiating processes are related to dune fixa-
to theoretical work, host-parasitoid metapo- tion, soil formation and vegetation develop-
pulations dynamics strongly interfere and oc- ment (Provoost et al. 2002). At present, rough
cupancy patterns should strongly overlap in grass and scrub encroachment result in a se-
case of limited host interpatch dispersal abil- vere fragmentation within a matrix of dense
ities and relatively low infection rates and par- dune vegetation (shrubs, dense grassland). In
asitoid survival rates (Hassel et al. 1991; an earlier paper, we identified typical spider
Comins et al. 1992; White et al. 1996; Hanski species for this habitat (Bonte et al. 2002).
1999). One of the most habitat-specific species is A/-
The population structure of parasitoid and opecosafabrilis, although its overall Indicator
host were investigated in the Flemish coastal Value was low, hence, indicating a relative
dunes, where grey dune habitats, being the op- low occupancy rate.
timal habitat for both A. fabrilis and A. rufa, Alopecosafabrilis is used as model organ-
are truly fragmented since the Second World ism in this study. It is the largest lycosid spe-
War (see e.g. Bonte et al. 2003a; Provoost & cies, living in self-made burrows in dry sandy
Bonte 2004). This was done in order to test habitats from temperate regions in Europe
the following hypotheses: (i) A. fabrilis has (males: 10-12 mm; females: 13-16 mm; Rob-
limited dispersal abilities, resulting in an iso- erts 1998). The species has a nocturnal life
lation-dependent population structure, (ii) A. style in which especially males leave their
fabrilis, having low population densities only burrow in search for mating partners during
occupies larger habitat patches and (iii) local autumn, with a peak activity during Septem-
and temporal host-parasitoid association result ber (Roberts 1998; Bonte, unpub. data.). Fe-
in similar distribution patterns, although Pom- males are active during autumn, but especially
pilidae have better dispersal abilities and are during late winter and early spring. The spe-
believed to be rather generalistic in prey cies occurs in low densities, has a biannual
choice according to prey species (Finch 1997). life cycle (Bonte et al. unpub. data) and does
Additionally, as A. fabrilis is nocturnal while not perform ballooning dispersal under labo-
its parasitoid is diurnally active, we asked ratory conditions (Bonte et al. 2003b).
whether the presence of a day-active parasit- During its period of activity, the spider
224 THE JOURNAL OF ARACHNOLOGY
—
Figure 1. Map of the surveyed grey dune habitat patches in the coastal dunes of De Panne-Bray
Dunes, Belgium. Black: patches occupied by Alopecosafahrilis', white: unoccupied patches. Circles in-
dicate patches not occupied by Arachnospila rufci.
hunting wasp (Hymenoptera, Pompilidae) Ar- tergent solution). In each of the 52 grey dune
achnospila rufa has been observed to be the patches, at least five traps were randomly
main predator (Koomen & Peeters 1993; Pee- placed, depending on the patch area. Patches
ters et al. 2004; Bonte, pers. obs.; Nieuwen- were digitized from aerial orthophotographs
huijsen, pers. comm.). Alopecosa schmidti with a Geographic Information System
(Hahn 1834) has been recorded as prey in (Arcview 3.1) and discrimination of vegeta-
Middle-Europe (Schljachtenok 1996). Female tion types was based on vegetation-specific
pompilids provide each cell of their nest be- red (RED) and near-infrared (NIR) reflectance
low the sand surface with only a single par- values (Provoost et al. 2002). Because of its
alyzed spider, on which one egg is laid. Ar- high activity during this season, the use ofpit-
achnospila rufa is large (body size up to 18 fall traps have been shown to be very useful
mm) and common in sandy regions of Bel- in catching this typical spider species living
gium and the Netherlands. It reaches adult- within this habitat (Bonte et al. 2004c). The
hood from June-October (Peeters et al. 2004; presence of the hunting wasp was recorded in
Nieuwenhuijsen in press). More detailed in- the same pitfall traps, but completed with de-
formation about its ecology and life history is tailed field surveys during sunny days. Al-
unfortunately not available. Voucher speci- though not all observed specimens were col-
mens of both Alopecosa fabrilis and Arach- lected to confirm identification, individuals
nospila rufa are deposited at the Royal Bel- could be identified in the field by their large
gian Institute for Natural Sciences. — size and distinct abdominal coloration. From
Field Survey & StatisticalAnalyses. Oc- GIS, we measured patch area, the distances to
cupancy patterns ofA. fabrilis were recorded the nearest suitable patch, as a measure of
from 25 August-7 October 2003 using pitfall patch isolation and distance to the nearest oc-
traps (diameter 9 cm, 6% formaldehyde-de- cupied patch (nearest-neighbor distance) as
BONTE & MAELFAIT—ASSOCIATION BETWEEN SPIDER WASP AND HOST 225
measurement of population isolation. For A. ney U-test: Z = 2.74; P = 0.006; Fig. 2). Ar-
rufa, we did not use the latter isolation mea- achnospila rufa was not recorded in patches
surement because its presence was only re- without A. fabrilis populations.
corded during September, hence ignoring pos-
DISCUSSION
sible different distribution patterns during the
previous summer-period. —Population structure ofAlopecosafabril-
Patch occupancy patterns forA. fabrilis (0: is, Our results demonstrate that the distance
vacant; 1: occupied) were analyzed by logistic to the nearest occupied patch contributed sig-
models for binomial data and logit-link with nificantly to the patch-occupancy model,
backward elimination of the non-significant whereas the overall habitat structure (i.e. ge-
parameters (SAS 9.2). Patch area, patch iso- ometry and configuration of all available
lation and the interaction between both were patches) did not. As a result, the population
included as independentvariables. ForA. rufa, structure seems not to be affected by local po-
the occupancy status of the patch by A. fa- tential population sizes (related to local pop-
brilis was used as an additional categorical ulation viability; Hanski 1999) and distant dis-
variable. persal abilities by ballooning. The latter is in
agreement with the absence ofaerial dispersal
RESULTS
under laboratory conditions (Bonte et al.
Patch occupancy ofAlopecosafabrilis was 2003b). As only the nearest-neighbor distance
not significantly influenced by patch area (x? contributed significantly to the patch-occupan-
= 2.255; P = 0.133). The distance to the near- cy model, the population structure of A. fa-
est suitable habitat (x? = 1.168; P = 0.280) brilis seems to be clearly aggregative, indi-
and the interaction between both (x? = 0.208; cating low abilities to disperse (and penetrate)
P = 0.648) did not contribute significantly. If cursorially through the hostile matrix or a pre-
the nearest-neighbor distance was taken into dominant role of habitat quality. Our data,
account, a significant negative relationship however, only result from a short term survey.
was found between isolation and patch occu- But preliminary data on patch occupancy pat-
pation (estimated slope:-0.035 ± 0.014; x? ^ terns from 2004 show similar distribution pat-
6.322; P = 0.012; Fig. 2). Other parameters terns (Bonte et al. unpub. results), indicating
remained non-significant. Although the model the absence of strong turn-over dynamics at
describes patch occupancy patterns in a sig- extended, though still rather short time spans.
nificant way, 32.7% of the cases were mis- The fact that patch area (related to local pop-
classified. Mainly patches near the inner dune ulation size) does not explain occupancy
front were occupied (Fig. 1). If only patches patterns seems to indicate that the spatial pop-
at the inner dune front were used for analysis, ulation structure is more likely to be deter-
neither distance to the nearest patch (x? = mined by random extinction-colonization dy-
0.028; P = 0.865), distance to the nearest oc- namics within aggregative clusters of closely
cupied patch (xi == 1.144; P — 0.285) or area connected suitable habitat remnants, which
(Xi = 0.476; P = 0.490) explaineddistribution appear to be situated nearthe innerdune front.
patterns. As the interaction between patch size and
After backward elimination of non-signifi- patch isolation does not explain occupancy
cant parameters, the occupancy of Arachnos- patterns, a rescue effect resulting from source-
pila rufa was only determined by the presence sink dynamics is unlikely (Dias & Blondel
of Alopecosa fabrilis (x? — 34.41; P < 1996).
0.0001). No other lycosid species were re- The aggregated pattern may result from dis-
corded during the survey period. Landscape persal limitation afterhistorical population dy-
geometry appears to be unimportant during namics or from spatially correlated habitat
this season since the explanatory power of characteristics, related to habitat quality, as
both patch area and patch isolation are ex- experienced by the species. Although both are
tremely low (all variables and interactions: x^ possible, the second seems to be more prob-
< 1.29; P > 0.256). Patches occupied by A. able as especially patches near the inner dune
fabrilis but not by A. rufa {n = 4) during this front were occupied. In coastal dunes, char-
period were significantly smaller than those (n acterized by a successive ontogenesis, grey
= 11) occupied by both species (Mann-Whit- dunes, although structurally similar may show
226 THE JOURNAL OF ARACHNOLOGY
—
Figure 2. Relation between patch area, nearest-neighbor distance and occupancy incidence for A,
fabrilis populations. Arrows indicate patches occupied by A.fabrilis, but not by its predatorA. rufa.
extensive spatial correlation in environmental conditions and, possibly, the reason for the
characteristics related to microclimate, soil observed clustered occurrence. Also, the ab-
properties and aeolic dynamics (sand over- sence ofA.fabrilis in large patches moreclose
blowing). The fact that considerable non-spa- to the sea, in which large populations should
tial correlated variation in habitat quality af- be able to persist, provides more likely evi-
fects spatial structural patterns has already dence for a reaction towards spatially corre-
been demonstrated by e.g. Briers & Warren lated environmental properties and optimal
(2000) and Bonte et al. (2003a). For a fosso- habitat quality in older grey dunes, situated
rial species likeA.fabrilis, it is not impossible near the inner dune front. In this case, dis-
that e.g., grain size properties, soil water re- persal limitation is of inferior importance, as
tention, soil formation and the intensity of illustrated by the model in which only patches
sand overblowing strongly determine burrow- near the inner dune front were included.
ing ability and the sustainability of created Host-parasitoid association^^Spatially
burrows. In the same coastal dune landscape, explicit host-parasitoid metapopulation mod-
the grassland inhabiting wolf spider P. mon- els generate spatially correlated abundance
ticola shows a habitat-quality dependent pop- and, hence, occupancy patterns in host and
ulation structure in which both patch area and parasitoid (Hanski, 1999). Arachnopsila rufa
patch connectivity determined occupancy pat- and related spider hunting wasps, however,
terns (Bonte et ah 2003a), although not in an appear to be more generalist parasitoids on
aggregative way. As vegetation structure is (larger) lycosid species (Koomen & Peeters
alike in ail investigated grey dune patches, 1993; Endo & Endo 1994; Finch 1997; Pee-
similarity in habitat quality for A. fabrilis is ters et al. 2004), The almost complete match
probably more related to pedological (possibly between occupancy incidences of host and
soil stability or differences in grain size near parasitoid indicate that, at least in the Flemish
the inner dune front) or microclimatological coastal dunes and during the survey period,A.
(less buffered temperatures far from the sea) rufa behaves as a specialized parasitoid on A.
BONTE & MAELFAIT—ASSOCIATION BETWEEN SPIDER WASP AND HOST 227
fabrilis. This indicates that at least one species ciation. Assuming that our findings are not
of pompilid wasp may behave as a host-spe- due to sampling artifacts, parasitoid absence
cialist during some periods of its adult life. in small populations indicates low dispersal
According to White et aL (1996), spatial pop- abilities or at least low dispersal motivation in
ulation patterns in which both host and para- spider wasp within spatially structured suit-
sitoid occur in the same patches are only static able habitat surrounded by hostile matrix veg-
in case of low host dispersal and low parasit- etation.
oid survival. Certainly the first assumption Also, since both juvenile and adult A. fa-
seems to be fulfilled in our study. However, brilis stay in their burrow during day, prey
A. rufa is already adult earlier in the season, selection by A. rufa has probably to rely on
and should, as a result, behave more flexibly olfactory and not on visual cues because bur-
in prey selection. As predicted by optimal for- row entrances are not visible, as also observed
aging theory, prey size selection should be op- in spider hunting wasps preying on day-active
timized in relation to the species’ load-carry- wolf spiders (e.g., Pompilus cinereus (Fabri-
&
ing capacity (Evans 1962; Coelho Ladage cius 1775); Bonte pers. obs.) and in sphecid
1999). The latter authors indeed found that wasps (although only at short distance after
large female wasps searched for prey that visual detection; Anton & Gnatzy 1998).
matched their owe body mass and lift capac- In fragmented coastal dune habitats, host
ity. As a result, A. rufa should prey on simi- and parasitoid show, at least temporally and
larly large-bodied lycosid species or show be- locally, a similar aggregative spatial popula-
havioural flexibility according to the available tion structure, indicating the importance of
prey spectrum. Taking into account the need (lack of) dispersal and possibly spatially cor-
for sandy habitats for prey burrowing, A. rufa related habitat characteristics in structuring
seems to be restricted to dynamic dune habi- patch occupancy patterns. Additionally, the
tats in which soil development is poor and spider hunting waspA. rufa appears to behave
bare sand sufficiently available. Female A.fa- as a specialized parasitoid during the main ac-
brilis disappear from the population in late tivity period ofits optimal prey with restricted
winter and early spring and are not available dispersal motivation. During this period, the
as host during the early beginning ofthe hunt- presence of an assumed generalist parasitoid
er wasp’s adulthood (Bonte, unpub. data). is a good predictor for the presence of noc-
Other large-bodied lycosid species, occurring turnal and burrowing dune wolfspider in larg-
in these habitats include only Alopecosa cu- er habitat patches in the Flemish coastal
neata (Clerck 1757) andA. barbipes (Suedev- dunes.
all 1833) (Bonte et al. 2002), also having a
ACKNOWLEDGMENTS
spring activity, and are as a result neither
available during summer. Possibly, A. rufa The author would like to thank the Ministry
uses smaller lycosids as host during early ofthe Flemish Community (Aminal, Afdeling
summer {Arctosa perita (Latreille 1799) or Natuur) and the Conseil General du Nord for
subadult A. fabrilis), potentially resulting in granting access to their field sites. The senior
different spatial distribution patterns. author is a Postdoctoral—Fellow of the Fund
The fact that A. rufa was only absent from for Scie—ntific Research Flanders (Belgium)
small patches, inhabited by A. fabrilis seems (F.W.O. Vlaanderen). One anonymous ref-
to provide evidence that higher trophic levels eree gave very valuable suggestions with re-
require larger habitats (Holt 1996; Holt et al. spect to species-area relationships and trophic
1999), but may also be an artifact in our sam- rank, opening new insights for further re-
pling strategy if smaller patches are only ac-
search.
cidentally visited by the spider wasp, hence
reducing encounter chances in the field. Ac- LITERATURE CITED
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