Behaviour and activity patterns of the scuttle fly Megaselia oxybelorum Schmitz (Diptera: Phoridae)...

Behaviour and activity patterns of the scuttle fly Megaselia

oxybelorum Schmitz (Diptera: Phoridae) at nestaggregations of two host digger wasps (Hymenoptera:Crabronidae)

CARLO POLIDORI1, CRISTINA PAPADIA1, R.H.L. DISNEY2 &

FRANCESCO ANDRIETTI1

1Dipartimento di Biologia, Sezione di Zoologia e Citologia, Universita degli Studi di Milano, Milan,

Italy, and 2Department of Zoology, University of Cambridge, Cambridge, UK

(Accepted 28 September 2006)

AbstractWe report on a field study of the behavioural ecology of Megaselia oxybelorum Schmitz at nestaggregations of its hosts, the digger wasps Philanthus triangulum F. and Cerceris arenaria L.(Hymenoptera: Crabronidae). The flies flew across the P. triangulum nesting site both as singleindividuals and as females and males paired in copula, and the former case was recorded more thantwice as often as the latter, while only single individuals were recorded at the C. arenaria site.Individuals both alone and in copula were seen at the P. triangulum site during the day roughlycoinciding with the host provisioning activity, while at the C. arenaria site the fly’s daily activityfollowed a bimodal trend in contrast to the normal distribution of the host provisioning. Visits of hostnests were frequent at the P. triangulum site and null at the C. arenaria site. Single individuals spentless than 1 min inside a nest, while a female entering while still in copula spent generally 1–3 mininside, males exiting after 1–5 s, showing that only in this second case was an oviposition possible. Thenumber of Megaselia oxybelorum increased with increasing host nest density and decreasing nearestneighbour distances of nests. Behavioural patterns of M. oxybelorum, when compared to otherMegaselia spp. associated with fossorial Hymenoptera, showed differences possibly related to thebiology of the hosts. In addition, some morphological variation within and between host sites arediscussed.

Keywords: Cerceris, kleptoparasitism, Megaselia, nest aggregation, phenology, Philanthus

Introduction

Scuttle flies (Diptera: Phoridae) are a large group of small insects often associated with

Hymenoptera, of which some are parasitoids, kleptoparasites or predators, facultative or

obligate (Disney 1994). Their common name comes from the typical walking behaviour of

adults, based on rapid bursts of movements with short pauses between (Miller 1979).

Correspondence: Carlo Polidori, Dipartimento di Biologia, Sezione di Zoologia e Citologia, Universita degli Studi di Milano, Via

Celoria 26, 20133 Milan, Italy. Email: [email protected]

Published 4 December 2006

Journal of Natural History, 2006; 40(32–34): 1969–1982

ISSN 0022-2933 print/ISSN 1464-5262 online # 2006 Taylor & Francis

DOI: 10.1080/00222930601046527

Generally their detailed biology is poorly known and most published works concern aspects of

their reproductive behaviour (Binns 1980; Miller 1984; Sivinski 1988; Wcislo 1990; Polidori

et al. 2004). In the Hymenoptera, the most commonly reported associations are with ants

(Disney 1994), but some recent studies are increasing our knowledge of associations with

some bees and wasps (e.g. Coville and Griswold 1983, 1984; Wcislo 1990; Disney et al. 2000;

Polidori et al. 2001, 2004; Otterstatter et al. 2002; Boesi et al. in press).

In the family, the large genus Megaselia Rondani is undoubtedly the most diverse and

widespread, but also behaviourally least known (Disney 1994). Of about 1400 known

species (almost half the Phoridae), data on phenology and behaviour are available for very

few species. This genus has dominated the family since at least the Miocene. It is the prime

candidate for the genus of insects possessing a greater diversity of larval habits than any

other. These habits include feeding on micro-organisms in aquatic habitats, dung, and

carrion (including human corpses), and the genus also comprises fungivores, plant feeders,

kleptoparasites, predators, parasitoids, and parasites (Disney 1994; Greenberg and Wells

1998; Lee et al. 2001). Megaselia species were also recently proposed as bioindicators in

disturbed tropical forests (Idris and Saiap 2002).

The particular role of Megaselia flies as natural enemies of fossorial Hymenoptera has

been long underestimated, and only recently associations with digger wasps and bees have

been highlighted (Disney et al. 2000; Polidori et al. 2001). Together with cuckoo bees and

wasps (Halictidae and Chrysididae), velvet ants (Mutillidae), and satellite flies

(Sarcophagidae and Anthomyiidae), Megaselia scuttle flies seem to be a constant

component of the parasite guilds found at nest aggregations of aculeate Hymenoptera

(Polidori et al. 2005b, unpublished data).

To date, the only species of Megaselia known to invade nests of apoid wasps are Megaselia

oxybelorum Schmitz, which was found as a kleptoparasite of Oxybelus uniglumis L. and

Cerceris arenaria (L.) (Chevalier 1925; Schmitz 1928; Polidori et al. 2001), Megaselia

leucozona Schmitz, kleptoparasite of Cerceris rubida Jurine (Polidori et al. 2005a) and

Megaselia aletiae (Comstock), reared from brood cells of the cavity-nesting wasp, Ectemnius

paucimaculatus (Packard) (Hymenoptera: Crabronidae) (Krombein 1967). Undetermined

species of Megaselia were also reared from nests of the digger wasps Philanthus solivagus Say

and Bembix amoena Handlirsch (Hymenoptera: Crabronidae), and from brood cells of the

mud-dauber Sceliphron jamaicense (Fabricius) (Hymenoptera: Sphecidae) (Evans 1966;

Evans and O’Neill 1988; Genaro 1996). Recently Disney (2006) revised and discussed the

complex of species to which M. oxybelorum belongs, concluding that this species has been

misidentified in the past and that only the Western European populations of this species

complex are the true M. oxybelorum.

In this paper we give behavioural and ecological data about M. oxybelorum in association

with two digger wasps, the European beewolf Philanthus triangulum (Fabricius)

(Hymenoptera: Crabronidae) and the weevil-hunting Cerceris arenaria L.

Philanthus triangulum and C. arenaria are solitary wasps which capture exclusively honey

bee workers (Apis mellifera L.) and adult weevils, respectively, to provide food for their

larvae. The detailed biology of these two wasps is well known (e.g. Fabre 1856; Tinbergen

1932), including recent interesting findings on sex allocation and mother–larvae

communication (P. triangulum), nest aggregation dynamics (C. arenaria), and intraspecific

competitive interactions (C. arenaria) (Field and Foster 1995; Strohm and Linsenmair

1995, 2000; Polidori et al. 2006). However, phorid flies have never before been recorded in

association with P. triangulum, and only recently with C. arenaria (Polidori et al. 2001).

Both wasps dig multicellular nests in compact soil where larvae stay until emergence,

1970 C. Polidori et al.

protected from the attack of a set of natural enemies, including Hedychrum cuckoo wasps

and sarcophagid flies (Strohm et al. 2001; C. Polidori et al., unpublished). Our main aim

was to study the activity patterns and the behaviour of M. oxybelorum at two different host

nesting sites in order to find possible variations linked to differences between the different

host nesting biologies.

Materials and methods

The study was conducted at two sites: (1) the Ticino Regional Park (Lombardy, Italy) in

2004 (15–31 July) at a large aggregation (about 150 nests) of the digger wasp P. triangulum

located in the Riserva Orientata ‘‘La Fagiana’’ (Magenta, Milano Province), and (2) the

Adda Sud Regional Park (Lombardy, Italy) during the summer of 2005 (6–26 July) at a

large aggregation (about 200 nests) of the digger wasp C. arenaria.

The nesting area of P. triangulum was characterized by high vegetation coverage (more

than 60% of the wasps nests were located under grass patches), and situated on a trail in the

wood dominated by Quercus robur, Populus nigra, and Ulmus campestris; the whole nesting

area was about 30 m2. Cerceris arenaria established its nests in a dairy farm located in

Catiglione d’Adda (Lodi Province); the aggregation covered about 35 m2 and included 196

nests in 2005, although its dimension has fluctuated considerably in the last 9 years

(Polidori et al. 2006).

Collection of field data on the activity of M. oxybelorum at both sites was performed using

two different methods: behavioural observations close to host nests and patrolling of the

nesting area. The behavioural observations on M. oxybelorum were made, except rainy days,

at different periods of the day to cover the whole activity period of the host wasps (from

06:00 to 20:00 h for P. triangulum and from 08:00 to 20:00 h for C. arenaria) (solar hours).

We started to record a behavioural sequence when a fly or a pair of flies (male and female in

copula) were detected close to one of the nests under observation, and ended when the

specimens flew away from the nests. Observed behaviours were codified and included flying

or walking of individuals alone and in copula, entering and exiting from the host nests by

males, females, and pairs in copula, and formation and separation of the copulating pairs.

Time spent in the host nests by flies was measured to the nearest second.

The daily activity patterns of the scuttle flies were studied through patrolling of the host

nesting sites, which were divided into a number of plots (22 of 1.5 m2 each at P. triangulum

site, 10 of 1 m2 each at C. arenaria site). Every hour (06:00–19:00 h at the P. triangulum

site, 08:00–19:00 h at the C. arenaria site), a 1 min observation was made on each plot to

obtain the following data: (1) number of passages of single individuals of M. oxybelorum; (2)

number of passages of individuals of M. oxybelorum paired in copula; and (3) number of

open host nests. The term ‘‘passage’’ is used meaning every individual or pair’s flight

recorded in the plot during the minute. The provisioning activity (number entering into the

nest with prey) of P. triangulum and C. arenaria was recorded through the observation of a

selected number of nests (39 nests in two plots at P. triangulum site and 65 nests in three

plots at C. arenaria site). Air temperature and air moisture were recorded with a thermo-

hygrometer every hour during the observation period.

At the P. triangulum site, a pair of (X, Y) coordinates were assigned to all the nests

located in the plots.

Response of the host wasp to the presence of the scuttle fly was evaluated at the P.

triangulum site with a simple experiment involving the location of pinned fly specimens at

0.5, 2, and 5 cm from the host nest entrance.

Behaviour of Megaselia oxybelorum 1971

A sample of specimens collected at both sites and some from other sites (R. H. L. Disney

collection) was used for morphological analysis. Wing length was used as an estimate of fly

size, and number of eggs was counted in gravid females.

Statistical analysis included non-parametric tests of correlation (Spearman test), non-

parametric tests for difference of medians (Mann–Whitney test, Kruskall–Wallis test), and

non-parametric test for differences in distributions (Kolgomorov–Smirnov test); parametric

statistics were used to test for differences in average time spent in host nests by flies

(ANOVA test), after testing the homogeneity of variance with Bartlett’s test. The Clark and

Evans test (1954) was used to evaluate the degree of clustering of P. triangulum nests. In the

text, all average numbers are given ¡SD.

Results

Table I presents the main data concerning the host nest aggregations and the investigated

areas, and the corresponding observations.

Temporal and spatial distribution at the host nesting sites

Philanthus triangulum nesting site. Megaselia oxybelorum flights across the wasp nest

aggregation were observed during the whole daytime period of provisioning activity of P.

triangulum, from 06:00 to 20:00 h (Figure 1). Two categories were recognized: flies

patrolling the nesting site alone (not in copula) and flies paired in copula. The daily

distributions of these two categories were significantly different (Kolgomorov–Smirnov

test: D50.57, n15n2514, P50.011) and not linearly correlated (Spearman correlation test

by ranks: r50.49, n514, P50.071, ns). Pairs in copula were recorded, on average, less

frequently than individuals flying alone (1.11¡1.01 and 2.99¡2.17 average passages per

minute per plot, respectively; Mann–Whitney test: U5149.5, n15n2514, P50.017). Both

categories were more abundant between 09:00 and 11:00 h and between 16:00 and

17:00 h; pairs in copula (but not individuals flying alone) were also abundant between

19:00 and 20:00 h, which coincides with the only time of the day when this category was

higher, on average, than the individuals flying alone. Although these distributions roughly

Table I. Main data concerning the host nest aggregations, the investigated areas, and the corresponding

observations.

Philanthus triangulum Cerceris arenaria

Period 15–31 July 2004 6–26 July 2005

Extent of nest aggregation (m2) 33 34.4

Total number of nests 157 196

Area used for patrolling plots (m2) 33 10

Number of observed nests 39 65

Average nest density (per m2) (whole aggregation) 4.7 5.7

Average prey per day per nest (average of n selected nests) 2.9 (n539) 4.3 (n565)

Area of plots (m2) 1.5 1

Number of plots 22 10

Number of observed isolated fly individuals passages (per

min per plot)

2.99¡2.17 (n5387) 0.23¡0.08 (n5272)

Number of observed flies in copula passages (per min per

plot)

1.11¡1.01 (n5111) 0


overlapped the daily distribution of provisioning activity of P. triangulum (Figure 1), neither

pair frequency nor individual frequency was correlated with host wasp frequency

(Spearman correlation test by ranks: pairs versus host: r50.37, n514, P50.177, ns;

individual versus host: r520.14, n514, P50.611, ns), not even combining pairs’ and

individuals’ passages (i.e. M. oxybelorum totals) (r50.20, n514, P50.45, ns).

Philanthus triangulum nest density varied in the 22 plots from 0 (one plot) to 10.6 nests

per m2, with an average of 4.7¡3.5 nests per m2 (total number of nests5157). Nearest

neighbour distances of nests varied from 13.9 to 82 cm, with an average of 27.5¡16.8 cm,

and the corresponding degree of clustering of nests (Rn value of Clark and Evans formula,

1954) varied from 0.53 to 1.34, with an average of 0.94¡0.22. This means that on the

whole nests in the aggregation were clustered (Clark and Evans test: c53.43, P,0.01).

The total number of M. oxybelorum passages correlated positively with the host nests

density per plot (Spearman correlation test by ranks: singles: r50.94, n522, P,0.001;

pairs: r50.95, n522, P,0.001) and negatively with the average nest’s nearest neighbour

distance per plot (Spearman correlation test by ranks: singles: r520.68, n521, P50.002;

pairs: r520.65, n521, P50.003). There was no correlation between M. oxybelorum

passages and the Rn value (clustering degree) per plot (Spearman correlation test by ranks:

singles: r50.33, n521, P50.13, ns; pairs: r50.38, n521, P50.088, ns) (Figure 2).

Air temperature and air moisture were not correlated with frequency of passages of M.

oxybelorum pairs, individuals, or with both categories combined (Spearman correlation test

by ranks: temperature versus pairs: r50.41, n514, P50.13, ns; temperature versus

individuals: r50.51, n514, P50.06, ns; temperature versus categories combined: r50.34,

n514, P50.21, ns; moisture versus singles: r520.52, n514, P50.06, ns; moisture versus

pairs: r50.34, n514, P50.81, ns; moisture versus categories combined: r520.30, n514,

P50.27, ns). Philanthus triangulum provisioning activity was also not correlated with

weather parameters (temperature: r520.29, n514, P50.23, ns; moisture: r50.42, n514,

P50.12, ns).

Figure 1. Daily distribution of Megaselia oxybelorum passages (per minute per plot) and daily provisioning activity

of their host wasps (number of trips per hour). (a, b) Philanthus triangulum nesting site; (c, d) Cerceris arenaria

nesting site.


Cerceris arenaria nesting site. At this site, M. oxybelorum was less abundant than at the P.

triangulum site (0.23¡0.08 average passages per minute per plot). Instead, nest density was

comparable to that of P. triangulum, varying in the 10 plots from 4.5 to 33 nests per m2,

with an average of 15.2¡9.8 nests per m2. At this site, no copulating pairs were recorded,

and the frequency of flying individuals was negatively correlated to that of the host

provisioning flights per hour (Spearman correlation test by ranks: r520.60, n512,

P50.043) (Figure 1). The total number of M. oxybelorum passages at the C. arenaria site

correlated positively with the host nests density per plot (Spearman correlation test by

ranks: singles: r50.67, n510, P50.042) (Figure 2).

Air temperature and air moisture were not correlated with frequency of passages of M.

oxybelorum at the C. arenaria site (Spearman correlation test by ranks: temperature:

r520.01, n512, P50.9, ns; humidity: r50.21, n512, P50.48, ns), and these parameters

were not correlated to C. arenaria activity (Spearman correlation test by ranks:

temperature: r520.06, n512, P50.81, ns; humidity: r520.06, n512, P50.98, ns).

Behaviour at the host nests

Philanthus triangulum nesting site. A total of 255 behavioural sequences of M. oxybelorum

were recorded close to the nest entrance of the host wasp. Megaselia oxybelorum was

Figure 2. Relationships of host nest density, host nest nearest neighbour, and host nest clustering degree (Rn) with

the total number of Megaselia oxybelorum passages. (a–c) Philanthus triangulum nesting site; (d) Cerceris arenaria

nesting site.


observed to fly across the wasp nests close to the soil surface, stopping sometimes on the

ground, walking for a while and then flying again, sometimes visiting the host nests. The

typical searching behaviour of the scuttle fly at the moment of entering a nest is represented

in Figure 3, including the following basic, more frequent, sequence: (1) female and male

enter the nest in copula; (2) male exits (after 1–5 s) the nest before the female; (3) female

exits from the nest. Thus separation of pairs in copula usually occurred inside the nest. In

fewer cases, single individuals were seen to enter the nest alone, and very rarely a male and

a female entered and exited together in copula.

We observed the following three kinds of patterns: a single fly enters (A); a pair enters,

then the female exits after the male (B); a pair enters and exits in copula (C), differing in

two main aspects, i.e. number of visits and time spent in the nest (Figure 4). On average,

event A was that most frequently recorded (13.2¡14.7 visits per day), followed by B

(8.8¡10.0 visits per day) and C (1.3¡2.0 visits per day). Corresponding medians (7, 5.5,

and 0, respectively) differed significantly (Kruskall–Wallis test: x257.58, df52, P50.022).

Time spent in the nest by flies was longer in case B (106¡46 s), followed by A (46¡18 s)

and C (20¡20 s). These average times were significantly different (Bartlett test for

homogeneity of variance: df52, statistic value58.35, P50.015; ANOVA: df52, F515.4,

P,0.001). In case B, the average time spent in the nest differed over the day (Bartlett test

for homogeneity of variance: df58, statistic value537.7, P,0.001; ANOVA: df58,

F52.68, P50.009), while the average time per hour did not differ in the other two cases (A:

Bartlett test for homogeneity of variance: df59, statistic value542.9, P,0.001; ANOVA:

df59, F50.88, P50.53, ns; for case C no test was possible due to the small sample size).

Philanthus triangulum appeared to detect the scuttle fly only if it was very close (0.5 cm)

from the nest entrance. In this case, the wasp attacked the fly protruding its head from the

nest and snapping with its mandibles. The fly generally escaped, but sometimes stopped a

few cemtimetres away from the nest entrance, trying repeatedly to enter a few seconds later.

Figure 3. Ethogram of Megaselia oxybelorum pairs close to host nest entrances (Philanthus triangulum nesting site).

Dashed lines show events that occurred at a low percentage (,5%), grey lines show events not directly observed,

but obviously occurred. Numbers close to arrows are the frequencies (%) of observed behaviours.


Cerceris arenaria nesting site. Megaselia oxybelorum behaved differently at the C. arenaria

nesting aggregation. No pairs in copula were observed, no entering of nests was recorded,

and in general the flies moved across the nesting site more frequently by walking rather than

flying.

Morphological variation within and between sites

Megaselia oxybelorum is sexually dimorphic, females being larger than males (F test:

F511.4, P,0.01; Student t test: t52.32, n1514, n257, P50.031).

Although few individuals were collected (two in 2001 at C. arenaria site and 21 in 2004 at

the P. triangulum site), morphology of M. oxybelorum seemed to vary greatly with respect to

wing length and egg batch size (Table II includes also specimens collected in other sites,

from the R. H. L. Disney collection). At the P. triangulum site, female wing lengths varied

from 0.975 to 1.59 mm and male wings from 1.02 to 1.18 mm, a variation greater than

Figure 4. Daily distribution of time spent in the host nests and daily distribution of visits in the host nests by

Megaselia oxybelorum (Philanthus triangulum nesting site). (a) Single individuals entered the nest alone (not in

copula); (b) pairs entered the nest, males exited after 1–5 s, and females exited alone; (c) pairs entered the nest and

exited still in copula.

Table II. Wing length and egg batch size in Megaselia oxybelorum individuals collected at our study sites and at

other sites.

Site of collection

Female wing length

(mm)

Male wing length

(mm)

Egg batch size (no. of eggs

in gravid females)

Philanthus triangulum site 1.28¡0.21

[n514; range: 0.97–1.59]

1.09¡0.06

[n57; range: 1.02–1.18]

3.71¡2.42

[n57; range: 2–7]

Cerceris arenaria site 1.51 [n51] 0.99 [n51] 16 [n51]

Canary Islands 1.20¡0.18

[n52; range: 1.07–1.33]

1.10¡0.03

[n53; range: 1.07–1.13]

2 [n51]

Peninsular Spain 1.38 [n51] 1.06 [n51] 10 [n51]


expected for a single species in the features used in literature on this complex of species.

Moreover, the female collected in Castiglione d’Adda in 2001 had one of the longest wings

(1.51 mm) and the male at the same site had the shortest wing (0.996 mm) recorded in the

two sites as well as in other sites of collection. Egg batch size also varied greatly, the number

of eggs ranging from two to seven at the P. triangulum site and 16 in the only female at the

C. arenaria site.

Discussion

The observed mating system (frequent pairs in copula searching for a suitable host nest)

recorded at the P. triangulum site seems to be widespread in scuttle flies associated with

fossorial bees and wasps. Frequent matings were observed by Wcislo (1990) for

Phalacrotophora halictorum (Melander and Brues) at a nesting aggregation of the bee

Lasioglossum figueresi Wcislo. Pairs in copula, in addition to those reported in the present

study, were observed for two additional Megaselia spp. (Table III). The scarcity of the

scuttle fly at the C. arenaria nest aggregation (and the corresponding absence of copulae)

already assessed in Polidori et al. (2001), could confirm the hypothesis that the typical

reproductive behaviour of this parasitic fly is a density-dependent recordable phenomenon

that depends neither on the size nor on the density of the host populations which are

comparable in the two sites (Table I; Figure 2).

The apparently lower reproductive success of the scuttle fly at the C. arenaria site should

not be attributed to the recent formation of the host population, which has been established

since at least 1996 (Polidori et al. 2006), and together with the scuttle fly at least since 2001

(Polidori et al. 2001). Hence, the small number of flies recorded at the C. arenaria site

might depend on other, perhaps behavioural, factors. However, both host wasps leave their

nests open during provisioning activity, which should give the scuttle flies the same

opportunities to enter the host nests during the day. On the contrary, C. arenaria females,

contrary to those of P. triangulum, frequently compete for a nest, usurping each other’s

burrows, as a consequence of the lack of new nest-digging behaviour (Polidori et al. 2006).

During a usurpation attempt, C. arenaria nests are often closed from the inside by the

usurping females (Field and Foster 1995; Polidori et al. 2006). This would reduce the

probability, for M. oxybelorum, of encountering an open nest. In C. arenaria, on average, a

nest is closed 0.8 times per day in addition to the overnight closure (data from a 1997 field

research on the same wasp population; Polidori et al. 2006), and could be one of the

reasons for the lower number of scuttle flies recorded at the C. arenaria site. A second

reason could be related to the higher frequency of provisioning by this wasp (Table I;

Figure 1), which would produce a higher frequency of encounters with the flies.

Competition with other natural enemies could also explain the difference, although on

both nesting sites the other major kleptoparasite was a Hedychrum cuckoo wasp (H. nobile

(Scopoli) at the C. arenaria site and H. rutilans Dahlbom at the P. triangulum site), which

appeared to be similarly abundant (C. Polidori et al., unpublished data).

One may suppose that the influence of the host on scuttle fly activity is mediated by two

opposing factors: (1) an indication of an actively foraged nest, working in synergy with the

presence of a certain number of nests (nest density); (2) a possible defensive behaviour of

the host with regard to the parasite (effectively observed only in P. triangulum). The

possible result might depend on the balance between these two factors: when the host

provisioning activity is moderate, as in the case of P. triangulum, the first mechanism would

predominate, giving rise to a positive correlation (Figure 1a, b). On the contrary, for a


Table

III.

Com

pari

son

of

beh

avio

ura

ltr

ait

sb

etw

een

Meg

ase

lia

spp

.ass

oci

ate

dw

ith

foss

ori

al

Hym

enop

tera

.

Meg

ase

lia

sp.

Host

Host

nes

tin

g

bio

logy

Ob

serv

ed

pair

sin

cop

ula

Pair

sin

copu

la

ente

rin

g

host

nes

t

Sex

of

ind

ivid

uals

ente

rin

gth

eh

ost

nes

talo

ne

Aver

age

tim

e

spen

tin

the

host

nes

t(s

)

Beh

avio

ur

of

male

saft

ersp

lit

of

the

cop

ula

Pre

sen

ce/

ab

sen

ceof

mati

ng

balls

Ref

eren

ces

M.

andre

nae

Andre

na

agi

liss

ima

Com

mu

nal

Yes

No

Male

s241.4

Wait

ing

ou

tsid

e

the

nes

t

Yes

,ou

tsid

e

nes

t

Dis

ney

etal.

2000;

Polid

ori

etal.

2004

M.

leuco

zon

aL

asi

oglo

ssum

mala

churu

m

Eu

soci

al

Yes

Rare

lyM

ale

s6.6

Fly

ing

aw

ay

No

Polid

ori

etal.

2005a

Halict

us

scabi

osae

Eu

soci

al

Yes

Yes

Male

s7.8

Fly

ing

aw

ay

No

Polid

ori

etal.

2005a

Cer

ceri

sru

bida

Com

mu

nal

Yes

Yes

Male

s2.5

–N

oP

olid

ori

etal.

2005a,

un

pu

blish

ed

data

M.

oxyb

elor

um

Oxybe

lus

unig

lum

isS

olita

ry–

––

––

–C

hev

alier

1925;

Sch

mit

z1928

Philanth

us

tria

ngu

lum

Solita

ryY

esY

esP

robab

lym

ale

s76

Fly

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higher host activity, the second mechanism would generate a negative correlation, as

observed for C. arenaria (Figure 1c, d). However, the suggested mechanims are rather

speculative and far from being clearly understood.

Pairs of M. oxybelorum in copula and single individuals flying alone seem to follow a

similar trend during the day, but the frequency of observations was much lower in the former

case (Table I). Individuals probably spend most of their time in search of a partner, joined in

copula, and seeking a suitable host nest. Evidently, not all the time spent paired coincides

with that of the actual copulation (sperm transfer), that perhaps occurs only close to (or

inside) the host nest. In fact, studies on other Megaselia spp. revealed that sperm transfer

lasts a few seconds (about 30 s; Benner 1991), so we may suppose that the reason why males

search for a host nest while paired is to prevent females obtaining other matings. This

suggestion is in accordance with what happens to the males of the scuttle fly Puliciphora

boriquenensis, which airlift the apterous females to the oviposition site (Miller 1984).

Nest density and nearest neighbour distance of nests affect the spatial distribution of M.

oxybelorum. This means that nest entrance holes probably represent another important cue

for the scuttle fly. A similar correlation with nest density was observed for Megaselia

andrenae Disney, a kleptoparasite of the fossorial bee Andrena agilissima Scopoli (Polidori

et al. 2005b).

We cannot exclude the involvement of chemical cues in host searching and acceptance.

For example, in some ant-attacking phorid flies chemical cues (host pheromones) are used

to locate hosts (Feener et al. 1996) and Megaselia opacicornis Schmitz locates the beetle host

using its defensive secretions as a cue (Zvereva and Rank 2004).

The much longer time spent in the nest by females which entered together with rapidly

exiting males (B) suggests that parasitism of the host brood provisions is possible only in this

case at the Philanthus site. We assume that a copulation persists only briefly inside the host

burrow, allowing the female to enter a brood cell to oviposit. Females and males in copula

were rarely seen to enter a nest and to exit quickly still paired (C), suggesting that these

events represent failed attempted parasitic ovipositions. The third case recorded concerns

single individuals entering and exiting from the nests (A). Although it was impossible, due to

the fly’s very small size, to attribute a sex to every single individual in the field, we may

suppose that these events are mostly related to males only, since: (1) the time spent in the

nest by single flies was short, probably insufficient to reach a brood cell and to oviposit; (2)

Megaselia spp. males were recorded in other studies to be more abundant than females on

the host nesting sites (Polidori et al. 2004, 2005a); and (3) females generally enter the host

nests with males in copula (Polidori et al. 2004; present study). Males probably visit the host

nests to increase the probability of meeting a female and possibly to mate. This differs from

the technique adopted by the males of M. andrenae, which typically wait outside the nests of

the host bee, after the separation of the previous copulation and the entry of the female

(Polidori et al. 2004). The fact that males often enter the host nests alone (sometimes more

than once on a single occasion), suggests even the possible presence of ‘‘mating balls’’

(a number of males flying clumped around a female) occurring, for M. oxybelorum, inside the

host nest, as observed for M. andrenae outside them (Polidori et al. 2004).

We may speculate that the different techniques used by pairs at the moment of nest

entering by M. oxybelorum and M. andrenae could be related to the nesting biology of the

hosts. Differently from P. triangulum, A. agilissima females are not solitary, but share nest

entrances with several conspecifics (Giovanetti et al. 2003). From this point of view, males

and females could not easily enter the host nest in copula, because they are likely to be more

detectable by many incoming and departing bees from the nest; in contrast, the probability


of encountering a P. triangulum female in its burrow is lower, because of the greater time

spent by the wasp foraging for its brood, with the burrow left open and with no other wasps

inside. This hypothesis could also be supported by preliminary observations on M.

leucozona, another scuttle fly associated with social digger bees and wasps (two halictid bees

and the digger wasp Cerceris rubida Jurine; see Table III). In this case, the time spent by the

flies inside was very short (from 2.5 to 7.8 s, according to the different sites; see Table III).

In all the three host species, a guard is permanently located at the nest entrance, probably

not permitting mating to be completed inside the nests. In this case, single individuals

entering nests were males (they were collected and determined, at least for Lasioglossum

malachurum Kirby and Halictus scabiosae Rossi; see Table III). The influence of the host

presence on successful parasitism is supported by the time spent in the nest for M.

oxybelorum: 129.5 s at the C. arenaria site (Polidori et al. 2001), 76 s at the P. triangulum site

(Table II). However, the longest average time in a host nest was recorded for M. andrenae

(.200 s), which attacks pollen stores of a communal bee (Table III). This could be due to

the fact that no A. agilissima females act as guards to the nest and, on the other hand, the

nest of this bee is a very complex structure of crossing burrows (Giovanetti et al. 1999) that

could result in a longer time needed for the fly to reach a brood cell.

By contrast, at the C. arenaria nesting site, the single M. oxybelorum individuals which

entered the nests were females (collected and determined; see Table III). In fact, it seems

that there is a continuous range of possibilities (Table III), from cases when mating pairs

enter the nest (M. leucozona; M. oxybelorum at P. triangulum site), to those when they

separate immediately before entering (M. andrenae), to that of a more remote place of

copulae formation (possibly M. oxybelorum at C. arenaria site).

In conclusion, although the present study confirms the non-specificity in host use by

some Megaselia scuttle flies (contrasting with parasitoid phorid genera such as Pseudacteon,

closely associated with Solenopsis fire ants; Porter et al. 1995), it seems that a restricted

group of species obtain resources by acting as kleptoparasites of aculeate, fossorial bees and

wasps, and that the activity patterns and behavioural traits may vary according to the host

biology, not only within species, but also within different populations of a single species.

The observed variation in wing length and egg batch size requires further attention in

future investigations, since if this broad variability is confirmed, one might be led to suspect

the presence of sibling species, as an explanation of some behavioural differences recorded

in the two sites. However, further morphological observations would be likely to benefit

from parallel molecular analysis, which recently was used to solve similar problems in

phorid flies (Cook and Mostovski 2002).

Acknowledgements

Thanks are due to the Parco Regionale della Valle del Ticino for support and to Ivan

Frigerio and Roberto Fumagalli for help in collecting field data. Part of the present work

was supported by a 3-year grant (FIRB (Fondo per gli Investimenti della Ricerca di Base),

RBAU019H94-001, 2001). R.H.L.D.’s studies of Phoridae are funded by the Professor

Hering Memorial Research Fund (British Entomological and Natural History Society).

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