Morphological distance and inter-nest distance account for intra-specific prey overlap in digger wasps (Hymenoptera: Crabronidae)

ORIGINAL ARTICLE

Morphological distance and inter-nest distance accountfor intra-specific prey overlap in digger wasps(Hymenoptera: Crabronidae)

Carlo Polidori • Yolanda Ballesteros •

Davide Santoro • Jose Tormos • Josep D. Asıs

Received: 3 January 2012 / Accepted: 17 April 2012 / Published online: 4 May 2012

� The Society of Population Ecology and Springer 2012

Abstract Although inter-individual diet variation is

common in predatory wasp populations, the factors

accounting for such variation are still largely unknown.

Here, we asked if paired diet dissimilarity in three species

of digger wasps correlates with morphological distance and

inter-nest distance, two factors previously linked to diet

partitioning in vertebrates. Results sharply differed among

species and generations. All sampled populations showed

significant inter-individual diet variation for prey taxa, but

only in half of the cases for prey size. In one generation of

two species [Bembix zonata Klug and Stizus continuus

(Klug)], similar-sized wasps had similar prey taxonomic

spectra (and for S. continuus also similar prey size spectra),

a phenomenon which probably reduces intra-specific

competition. In addition, B. zonata females nesting closer

to each other had more similar prey taxonomic spectra,

suggesting that distant females probably hunt on different

patches that harbour different prey species. For the females

of a further species (Bembix merceti Parker), pairwise size

difference and inter-nest distance did not affect prey dis-

similarity. Both morphological distance and inter-nest

distance are potentially important in shaping the overlap of

individual resource use in wasps, though probably only in

certain conditions such as a highly clumped distribution of

nests and size-related constraints on prey selection.

Keywords Diet dissimilarity � Intra-specific competition �Nest distribution � Prey size � Wasp size

Introduction

One of the most important findings of the recently renewed

interest in intra-specific trait variation (see Bolnick et al.

2011) is that individual diet specialization is extremely

common in predatory animal populations from disparate

taxa such as amphibians, mammals, fishes, and insects

(e.g., Svanback and Persson 2004; Bolnick et al. 2007;

Quevedo et al. 2009; Polidori et al. 2011). The reasons why

such individual specialization is promoted and maintained

were also recently investigated, and we now know that the

degree of intra-specific niche overlap may for example be

affected by foraging experience (Rendell and Whitehead

2001), sexual dimorphism (Martins et al. 2008), body size

(Bolnick and Paull 2009), cognitive constraints that limit

the use of diverse sets of resources (Bolnick et al. 2003) or

inter- and intra-specific competition (Bolnick 2001; Svan-

back and Bolnick 2007; Bolnick et al. 2010). In practice all

of these studies were carried out on vertebrate predators, so

that factors accounting for diet overlap between individuals

are still not very clear for other taxa. This is the case for

solitary hunting wasps (Hymenoptera: Aculeata). In fact, to

date, studies on diet specialization of solitary hunting

wasps have mostly been done at the species level, and only

rarely at the individual level. For example, we know that in

wasp guilds, mean pairwise overlap in microhabitat utili-

zation can be significantly lower than predicted by null

C. Polidori (&)

Departamento de Biodiversidad y Biologıa Evolutiva,

Museo Nacional de Ciencias Naturales (CSIC),

C/Jose Gutierrez Abascal 2, 28006 Madrid, Spain

e-mail: [email protected]

Y. Ballesteros � J. Tormos � J. D. Asıs

Unidad de Zoologıa, Facultad de Biologıa,

Universidad de Salamanca, 37071 Salamanca, Spain

D. Santoro

School of Biological Sciences, Victoria

University of Wellington, New Kirk Building,

6012 Wellington, New Zealand

123

Popul Ecol (2012) 54:443–454

DOI 10.1007/s10144-012-0322-9

models (Field 1992), but we still have only suggestions that

this pattern applies at the individual level (Polidori et al.

2005). Sympatric Philanthus digger wasp species studied at

a large North American nesting site showed limited dietary

overlap (O’Neill and Evans 1982), and the same trend was

found between females in a single population of a Philanthus

species (Stubblefield et al. 1993). In both cases, however, the

ultimate causes of this resource partitioning were not elu-

cidated. Competition could account for this pattern, as

observed in parasitoid wasps (Shimada 1985). We also

know, both at the species and individual level, that larger

foraging species/females are generally able to select larger

prey, though it is still unclear if this wasp-prey size positive

relationship is also reflected in a significant prey taxa or prey

size segregation, in particular within populations (Field

1992; Polidori et al. 2005, 2009, 2010; Karsai et al. 2006;

Coelho 2011). For instance, although theoretical consider-

ations may predict that, in comparison with smaller preda-

tors, larger ones could be favoured in subduing, handling and

carrying a wider range of prey to the nest, a recent review and

re-analysis of published data largely rejected this hypothesis,

with only three out of ten populations showing smaller

individuals significantly more or less specialized than larger

ones (Polidori et al. 2011). Other factors, such as possible

trade-offs probably related to learning in searching and/or

handling prey, have also been suggested as an explanation

for individual specialization in solitary wasps, but without

supporting evidences (Araujo and Gonzaga 2007).

There is thus a need to investigate in greater depth the

role of selected factors in shaping individual resource

overlap in wasp populations. In this study, we partially fill

this gap by testing if two particular factors, namely dis-

tance between individuals’ nests and morphological dis-

tance (size difference) between individuals, account for

pairwise diet overlap in three species of solitary predatory

digger wasps (Hymenoptera: Crabronidae). In particular,

we hypothesize that: (1) morphologically divergent indi-

viduals share few if any prey (Roughgarden 1972;

Ackermann and Doebeli 2004), because an individual

consumer’s phenotype is likely to determine the set of

resources that it is able to use (Roughgarden 1972;

Ackermann and Doebeli 2004; Bolnick and Paull 2009);

and (2) close-nesting individuals forage on similar types of

prey, because, as occurs in some social wasps (Nieh 2009),

they may tend to travel to and feed or hunt prey in locations

where they can see conspecifics preying or because of local

enhancement (the facilitation of learning resulting from an

individual’s attention being drawn to a locale and then

reinforced with a reward, e.g., Brown 1986), or because

close-nesting wasps may have access to the same closer

hunting patch, and patches differ in prey types.

Digger wasps, i.e., aculeate hymenopterans which dig

their nests in the ground and fill them up with paralysed

arthropods in order to feed the offspring reared in the nest

(Evans and O’Neill 2007), seem to be an adequate model to

test for the effect of these two factors on diet partitioning:

firstly, in any given population, body size variance among

individuals is often great enough to appreciate size-related

fitness components, including provisioning (O’Neill 2001;

Evans and O’Neill 2007; Coelho 2011); secondly, the

variance in the distance between pairs of nests is often high

as a result of the common spatially clumped distribution of

nests (e.g., Polidori et al. 2006, 2008); and thirdly, digger

wasps nest in restricted areas and are central-place forag-

ers, allowing researchers to monitor with ease the resource

use of many individuals (e.g., Polidori et al. 2010; Santoro

et al. 2011).

Methods

Studied organisms

Bembix merceti Parker and Bembix zonata Klug are

solitary Diptera-hunting wasps restricted to Southern

Europe or even to the Iberian Peninsula alone (the former

species). The nests of both species are unicellular and

wasps nest in aggregations (Asıs et al. 2004). Despite

many fly families being reported among prey of

B. merceti (Evans and O’Neill 2007), recent studies have

shown that populations may actually be selective in prey

use, with wasps positively selecting families of flies with

greater mean weights even though they are less abundant

(Asıs et al. 2011), and that individual wasps significantly

segregate their diets (individual specialization) (Polidori

et al. 2011). On the other hand, only very limited prey

sampling has been carried out for B. zonata (Asıs et al.

2004), so that details on prey use in this species are

unknown.

Stizus continuus (Klug) is a Mediterranean solitary wasp

whose populations are bivoltine in Southern Europe;

females dig multicellular nests in large aggregations and

hunt for grasshoppers, mainly of the family Acrididae, to

feed their immature offspring (Polidori et al. 2008, 2009).

As for B. merceti, recent studies on S. continuus clearly

showed a selective predation at population-level, females

hunting mainly grasshopper species living on bushes

(though they are less abundant), and high specialization at

individual level (Santoro et al. 2011).

Mapping of nests, wasp size and prey sampling

Two study areas were chosen to carry out the field work,

performed during July and August 2007, 2009 and 2010

(depending on the species, see Table 1). The nest aggre-

gations of B. merceti and B. zonata were located in the

444 Popul Ecol (2012) 54:443–454

123

neighbourhood of Almarail (province of Soria, Spain),

where there is a predominance of cereal crops. The nest

aggregation of S. continuus was located at ‘La Mallada

Larga’ of ‘Dehesa del Saler’ (province of Valencia, Spain),

which is a coastal salt marsh with damp sandy soil. Details

of the two study areas are reported in Asıs et al. (2011) and

Polidori et al. (2008) respectively.

Within each nest aggregation, wasp females and their

associated nests were marked to allow individual identifi-

cation. Each wasp was marked with a unique combination

of two or three colours on the thorax, using marking pens

with fast drying inks (water-based paint), a well-estab-

lished technique in wasp behavioural studies (e.g., Polidori

et al. 2008; Asıs et al. 2011). Nests were individually

marked with a differently coloured stick located close to

the entrance, and their coordinates recorded in a Cartesian

system (see Polidori et al. 2008). We then obtained for each

nest (i.e., wasp) the distances to all the other nests (wasps)

(ND) using Pitagora’s formula. Marked wasps were

weighed in the field to the nearest 1 mg with an electronic

portable balance. The most limiting factor while hunting

and carrying a prey item to the nest is its size (relative to

wasp size) (Coelho 2011), so we did not consider addi-

tional morphological characters.

To obtain prey, marked females returning to the nest

after a foraging trip were re-captured and, once deprived of

the prey, released. Prey were then preserved in 95 % eth-

anol or killed by ether. To reduce problems of small

samples, at least four prey items were collected from each

marked wasp (Santoro et al. 2011) (Table 1). Prey were

weighed to the nearest 1 mg with an electronic balance,

and identified at the species level or separated into mor-

phospecies with the help of specialists (see Acknowl-

edgements) and by comparison with previous collections

(Asıs et al. 2011).

Measures of individual diet specialization

Individual diet specialization was calculated as the pro-

portional similarity between the diet of the individual i and

the diet of the generation (intra-specific overlap in prey

taxa) (Bolnick et al. 2002), i.e.,

PSi ¼ 1� 0:5X

j

pij � qj

����

where pij is the proportion of the jth prey species in indi-

vidual i’s diet, and qj is proportion of the jth prey species in

the whole species/generation’s prey spectrum.

The mean value of PSi (IS) expresses the average indi-

vidual specialization for a species/generation. IS varies

from near 0 (maximum individual specialization) to 1 (no

individual specialization). However, we used the more

intuitive V (i.e., 1 - IS), so that higher values indicated

higher individual specialization (see Bolnick et al. 2007).

To measure individual specialization for prey weight we

used Roughgarden’s Index (R’s I) (Roughgarden 1974) for

continuous data (Bolnick et al. 2002). The index is based

on the within-individual component (WIC) and the

between-individual component (BIC) of the total niche

width (TNW), i.e.,

R0sI ¼ WIC

TNW¼

E Var xij ij� �� �

VarðxijÞ

where xij = weight of the jth prey item in individual i’s

diet. Also, this index decreases with specialization, so we

used the more intuitive W (i.e., 1 - R’sI) (higher values

indicate higher individual specialization).

The indices of individual specialization (PSi and R’s I)

were calculated with the IndSpec1 program (Bolnick et al.

2002). IndSpec1 uses a non-parametric Monte Carlo pro-

cedure to generate replicate null diet matrices drawn from

the population distribution, from which P values can be

computed (Bolnick et al. 2002). Ten thousand replicates in

Monte Carlo bootstrap simulations were performed.

Measures of pairwise diet dissimilarity

We performed a series of Pearson correlation tests (for

n [ 10; correlation coefficient r) or Spearman correlation

tests (for n \ 10; correlation coefficient q) to test if larger

Table 1 Sample size, wasps’ and prey body mass and inter-nest distance (ND) for each of the studied species/periods

Species and period Wasp body mass (mg) Prey body mass (mg) ND (cm)

Bembix merceti 2009 (12, 156, 19) 95 ± 17 (66–123) 14.14 ± 9.6 (6–89) 1384.8 ± 1089.8 (17–3475.6)

Bembix merceti 2010 (12, 141, 18) 100 ± 20 (63–140) 15.9 ± 11 (4–56) 234.3 ± 124.3 (15.2–583.4)

Bembix zonata 2009 (13, 113, 17) 109 ± 10 (92–129) 22 ± 16 (4–124) 7180 ± 6477.7 (71.8–15401.8)

Bembix zonata 2010 (8, 70, 13) 115 ± 20 (74–132) 16 ± 13 (4–91) 586.8 ± 271.9 (128.3–1216.1)

Stizus continuus 2007-I (16, 201, 7) 172 ± 40 (92–226) 70 ± 33 (22–240) 268.6 ± 147.4 (34.9–648)

Stizus continuus 2007-II (19, 138, 6) 182 ± 38 (122–258) 152 ± 86 (22–422) 257 ± 151.6 (26–750.4)

For each parameter, mean ± SD precedes min–max values (in brackets). In brackets, after the species/periods, there is, in the following order,

the number of females (and nests), number of prey items, and number of prey species (or morphospecies)

Popul Ecol (2012) 54:443–454 445

123

wasps hunt for larger prey, using the ln-transformed data to

meet normality assumptions.

We calculated the pairwise taxonomic diet dissimilarity

(the complement of the diet similarity PS; Bolnick and

Paull 2009) between each pair of individuals i and j as:

PDSij ¼ 1�Xn

k¼1

minðpik; pjkÞ

where pik and pjk are the proportions of the kth prey type in

individual i’s and j’s diet, respectively (Ingram et al. 2011).

PDSij ranges from zero, when individuals consume the

same prey in identical proportions, up to 1, when the

individuals share no prey taxa in common. The diet simi-

larity PSij was calculated with IndSpec1, which also pro-

vided a matrix of diet similarity, i.e., a matrix including all

the pairwise PSij values between individuals; we then used

the complementary values PDSij to build the dissimilarity

matrix (PDS matrix). The mean value of PDSij across all

pairs of individuals (ET) represents the overall level of prey

taxa variation within the population (Ingram et al. 2011).

We calculated the pairwise prey size dissimilarity

(SDSij) between each pair of individuals i and j with the

following formula that we developed for the present study:

SDSij ¼

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiPmi � Pmj

� �þ Pcvi � Pcvj

� �

Pmi þ Pmj

����

����

s

where Pm is the mean prey size of the individual and Pcv is

the coefficient of variation (SD/mean) in prey size of the

individual. The index ranges from 0 (completely over-

lapped prey size) to &1 (extremely divergent prey size);

note that the index takes into account both the size dif-

ference and the difference in the relative variance in prey

size, so that, if the mean prey size is exactly the same for

the two individuals, SDSij increases with increasing dif-

ference in relative variance. We then built the dissimilarity

matrix (SDS matrix). Note also that, because this index is

based on a continuous variable (e.g., a linear measure or a

mass), the upper extreme never reaches 1, but becomes

asymptotic to 1 above a certain (very high) difference in

mean prey size between the two individuals (SDSij is[0.99

when the ratio of the larger mean to the smaller mean is

[100). The mean value of SDSij across all pairs of indi-

viduals (ES) represents the overall level of prey size vari-

ation within the population.

We tested for differences in PDSij, SDSij and ND distri-

butions between the two generations for each population

with a two-sample Kolgomorov–Smirnov test. We tested

for differences in wasp mass and prey mass between gen-

erations with an unpaired Student’s t test, applied to the ln-

transformed data to meet normality assumptions. An

Aspin–Welch test was used instead of the Student’s t test in

the case of non-homogeneity of variance (significant F test).

Correlating pairwise wasp trait differences with prey

dissimilarity measures

Because prey taxonomic overlap and prey size overlap can

be inter-correlated, we first plotted the SDS matrix with the

PDS matrix. A positive correlation between the SDS matrix

and the PDS matrix would suggest that prey species differ

in size enough to allow taxonomic and size differences to

be highly related, i.e., that wasps hunting for more diverse

prey species actually also hunted for prey with more var-

iable size. We tested for a significant positive or negative

slope of this relationship with a two-tailed Mantel test,

whose statistical significance was assessed by 10000 rep-

licate permutations (Bolnick and Paull 2009).

From the body mass values of the individual wasps, we built

a matrix based on the absolute pairwise difference of body

mass between females (wasp_MASS matrix). To obtain a

value between 0 and 1, as for PDS and SDS, we calculated such

paired size differences as massi �massj

�� ���maxðmassi;jÞ, so

that the difference is expressed as a proportional mass increase

of the larger wasp relative to the smaller one. If body size

difference affects the level of prey (taxa and/or size) dissimi-

larity, the wasp_MASS matrix and the PDS matrix and/or the

SDS matrix would be correlated (Mantel test).

We built a matrix with the distances between each nest

and all the others (ND) (NEST matrix). If pairwise inter-

nest distance explains the degree of prey taxa dissimilarity,

the NEST matrix and the PDS matrix would be correlated.

These correlations were also tested with a Mantel test. Note

that we did not analyse the relationship between inter-nest

distance and SDS, because there is no reason to expect

wasps to be partitioning their prey size in relation to nest

distance to conspecifics.

Results

Wasp traits

The populations studied varied considerably in body mass

(weight) (Table 1). Within the studied cases, S. continuus

females, B. merceti females in 2010 and B. zonata females in

2010 appeared to be more variable in size (coefficient of

variation approximately 0.2) than B. merceti in 2009 and

B. zonata in 2009 (coefficient of variation approximately

0.07) (Table 1). Wasp body mass did not differ between gene-

rations in any species (B. merceti: F = 1.38, P = 0.29, t =

-0.55, df = 22, P = 0.58; B. zonata: F = 4.8, P = 0.02,

Aspin–Welch’s t = -0.67, df = 8.82, P = 0.51; S. con-

tinuus: F = 1.54, P = 0.18, t = -0.79, df = 33, P = 0.43).

The populations studied varied considerably in mean

nest distance (ND) (Table 1). Bembix zonata in 2009 was

446 Popul Ecol (2012) 54:443–454

123

the population which nested in the largest area, and thus the

distance between its nests had the widest range, with nests

being approximately 40 cm to 150 m apart (Table 1). This

nest aggregation was in fact composed of two well-sepa-

rated (about 100 m) clusters of nests. At the other extreme,

nests of S. continuus in the first generation of 2007 were

only 35–650 cm apart (Table 1). ND distribution did not

differ between generations in S. continuus (Kolgomorov–

Smirnov test: D = 0.09, n1 = 120, n2 = 172, P = 0.58),

but it differed between generations in the other two species

(though only marginally in B. zonata) (Kolgomorov–

Smirnov test, B. merceti: D = 0.71, n1 = 66, n2 = 66,

P \ 0.0001; B. zonata, D = 0.56, n1 = 78, n2 = 28,

P = 0.06).

Overall prey spectrum and individual specialization

Fly prey of B. merceti and B. zonata consisted mainly of

Bombyliidae and Syrphidae, in both 2009 and 2010

(Table 2). For both species, a few other fly families, such

as Calliphoridae and Stratiomyidae, were also included in

the diet at appreciable frequencies (Table 2).

Orthopteran prey of S. continuus in the first generation

of 2007 belonged to three families, with Acrididae being

the most hunted. In the second generation of 2007 Acrid-

idae was again the most hunted family (Table 2).

Prey size was highly variable within the studied cases: in

each, the smaller prey item weighed at least approximately

10 times less than the largest prey item, and sometimes

even approximately 20 times less (B. zonata 2010,

S. continuus 2007-II) (Table 1). Prey size did not differ

between generations in B. merceti (F = 1.77, P = 0.0003,

Aspin–Welch’s t = -0.96, df = 258.3, P = 0.33), but did

in B. zonata (F = 1.02, P = 0.47, t = 3.5, df = 181,

P = 0.0005) and in S. continuus (F = 2.46, P \ 0.0001,

Aspin–Welch’s t = -12.1, df = 212.5, P \ 0.001).

All the populations and generations showed significant

prey taxa partitioning among individuals (Table 3), while

prey size partitioning was detected in both S. continuus

generations and in B. merceti in 2010, but not in the other

Bembix populations/periods (Table 3).

The value of ET was variable across the study cases, and

sometimes very variable between generations of a given

species (Table 3). In all the populations, at least one pair of

individuals showed a complete absence of prey overlap

(PDSij = 1), while only in S. continuus were there also

pairs of individuals completely sharing their prey spectrum

(PDSij = 0), giving a clear bimodal distribution of PDSij in

one of the generations (2007-I) (Table 2; Fig. 1). PDSij

distribution did not differ between generations in B. mer-

ceti (Kolgomorov–Smirnov test: D = 0.21, n1 = 66,

n2 = 66, P = 0.08), but it differed between generations

in the other two species (Kolgomorov–Smirnov test,

B. zonata, D = 0.45, n1 = 78, n2 = 28, P = 0.0003;

S. continuus: D = 0.56, n1 = 120, n2 = 172, P \ 0.001).

Variation in the distribution of the SDSij values was also

observed (Table 3; Fig. 2), which led to variable values of

ES. Cases of SDSij = 0 (total overlap in prey size) occurred

only in S. continuus in one generation, while, on the other

hand, no values of SDSij \ 0.1 were recorded in one gen-

eration of B. zonata (Table 2; Fig. 2). SDSij distribution did

not differ between generations in B. merceti (Kolgomorov–

Smirnov test: D = 0.19, n1 = 66, n2 = 66, P = 0.13) and

in B. zonata (Kolgomorov–Smirnov test, D = 0.25,

n1 = 78, n2 = 28, P = 0.12), but did in S. continuus:

D = 0.33, n1 = 120, n2 = 172, P \ 0.001).

Relationships between prey taxonomic spectra and prey

size spectra

A positive correlation between the SDS matrix and the PDS

matrix was found in five of the six studied cases,

Table 2 Relative frequencies (%) of prey families hunted by female wasps in the three studied species

Species and period Asi Bom Cal Sar Str Syr Tac Tab The

Diptera

B. merceti 2009 – 26.3 (8) 8.3 (1) 1.9 (3) 15.4 (1) 51.9 (3) 3.2 (3) – –

B. merceti 2010 – 44.7 (11) 2.1 (2) 0.7 (1) – 50.4 (1) 1.4 (1) 1.4 (2) –

B. zonata 2009 2.7 (2) 61.1 (6) – 0.9 (1) – 32.7 (4) 1.8 (1) – 0.9 (1)

B. zonata 2010 2.9 (2) 28.6 (8) 65.7 (3)

Acr Pyr Gry

Orthoptera

S. continuus 2007-I 96.3 (5) 3.1 (1) 0.6 (1)

S. continuus 2007-II 78.8 (5) 21.2 (1) –

In brackets there are the number of species (or morphospecies) identified in each family

Asi Asilidae, Bom Bombyliidae, Cal Calliphoridae, Sar Sarcophagidae, Str Stratiomyidae, Syr Syrphidae, Tac Tachinidae, Tab Tabanidae, TheTherevidae, Acr Acrididae, Pyr Pyrgomorphidae, Gry Gryllidae

Popul Ecol (2012) 54:443–454 447

123

suggesting that wasps hunting for more diverse prey spe-

cies actually also hunted for prey with more variable size

(Mantel test: B. merceti 2009: r(PDS matrix, SDS matrix) =

0.31, P \ 0.0001; B. merceti 2010: r(PDS matrix, SDS matrix) =

0.34, P \ 0.0001; B. zonata 2009: r(PDS matrix, SDS matrix)

= -0.11, P = 0.18; B. zonata 2010: r(PDS matrix, SDS matrix)

= 0.94, P \ 0.0001; S. continuus 2007-I: r(PDS matrix, SDS

matrix) = 0.47, P \ 0.0001; S. continuus 2007-II: r(PDS

matrix, SDS matrix) = 0.58, P \ 0.0001).

Do similar-size wasps overlap more or less their prey

spectra?

In all but one case (S. continuus 2007-II: Pearson test,

r = 0.74, n = 19, P = 0.0002) larger wasps did not hunt,

on average, for larger prey (B. merceti 2009: r = 0.38,

n = 12, P = 0.22; B. merceti 2010: r = 0.32, n = 12,

P = 0.30; B. zonata 2009: r = -0.27, n = 13, P = 0.37;

B. zonata 2010: q = 0.15, n = 8, P = 0.68; S. continuus

2007-I: r = 0.24, n = 16, P = 0.36).

Increasing morphological distance (body mass) between

pairs of wasps did not correspond to an increase or

decrease of pairwise prey taxonomic dissimilarity in B.

merceti in 2009 (Mantel test: r(wasp_MASS matrix, PDS matrix)

= -0.12, P = 0.29), B. merceti in 2010 (Mantel

test: r(wasp_MASS matrix, PDS matrix) = -0.006, P = 0.61),

B. zonata in 2010 (Mantel test: r(wasp_MASS matrix, PDS

matrix) = -0.18, P = 0.33), and in S. continuus 2007-I

(Mantel test: r(wasp_MASS matrix, PDS matrix) = -0.08, P =

0.35) (Fig. 3). However, a positive association between

pairwise size distance and pairwise prey taxonomic dis-

similarity was found marginally in B. zonata in 2009

(Mantel test: r(wasp_MASS matrix, PDS matrix) = 0.22,

P = 0.055) and more strongly in S. continuus 2007-II

(Mantel test: r(wasp_MASS matrix, PDS matrix) = 0.20,

P = 0.008) (Fig. 3), i.e., wasps with similar body mass

shared more of their prey taxonomic spectra.

Increasing morphological distance (body mass) between

pairs of wasps did not correspond to an increase or

decrease of pairwise prey size dissimilarity in B. merceti

in 2009 (Mantel test: r(wasp_MASS matrix, SDS matrix) =

-0.035, P = 0.76), B. merceti in 2010 (Mantel test:

r(wasp_MASS matrix, SDS matrix) = -0.14, P = 0.24), B. zonata

in 2009 (Mantel test: r(wasp_MASS matrix, SDS matrix) = 0.06,

P = 0.59), B. zonata in 2010 (Mantel test: r(wasp_MASS

matrix, SDS matrix) = -0.12, P = 0.54), and S. continuus

2007-I (Mantel test: r(wasp_MASS matrix, SDS matrix) = -0.11,

P = 0.22) (Fig. 4). However, a positive association was

found for size distance between pairs of wasps and pair-

wise prey size dissimilarity in S. continuus 2007-II (Mantel

Table 3 Individual diet specialization and pairwise diet dissimilarity between females for each species/period studied

Species and period Individual specialization for

prey taxa (V)

Individual specialization

for prey size (W)

Pairwise prey taxonomic

dissimilarity

Pairwise prey size

dissimilarity

B. merceti 2009 0.531 ± 0.202, P \ 0.0001 0.164, ns PDSij = 0.246–1,

ET = 0.704 ± 0.253

SDSij = 0.094–0.807,

ES = 0.395 ± 0.197

B. merceti 2010 0.412 ± 0.178, P \ 0.0013 0.384, P \ 0.0001 PDSij = 0.142–1,

ET = 0.621 ± 0.344

SDSij = 0.040–0.756,

ES = 0.426 ± 0.162

B. zonata 2009 0.514 ± 0.185, P \ 0.0001 0.174, ns PDSij = 0.142–1,

ET = 0.654 ± 0.283

SDSij = 0.054–0.719,

ES = 0.384 ± 0.154

B. zonata 2010 0.391 ± 0.127, P \ 0.0049 0.066, ns PDSij = 0.076–0.75,

ET = 0.460 ± 0.196

SDSij = 0.149–0.664,

ES = 0.436 ± 0.155

S. continuus 2007-I 0.336 ± 0.259, P \ 0.0001 0.341, P \ 0.0001 PDSij = 0–1,

ET = 0.389 ± 0.423

SDSij = 0.007–0.801,

ES = 0.352 ± 0.221

S. continuus 2007-II 0.567 ± 0.152, P \ 0.0001 0.494, P \ 0.0001 PDSij = 0–1,

ET = 0.695 ± 0.315

SDSij = 0.041–0.756,

ES = 0.447 ± 0.169

For each parameter, min–max range precedes mean ± SD

1

2

3

4

5

6

7

B. merceti

2009

ln(m

ass)

(m

g)

waspprey

B. zonata S. continuus

2009 2007-II2007-I20102010

Fig. 1 Box plots showing averages (crosses), outliers (circles), and

with whiskers showing minimum–maximum values and 1st and 3rd

quartiles of ln-transformed wasp size and prey size in the six studied

species/periods

448 Popul Ecol (2012) 54:443–454

123

test: r(wasp_MASS matrix, SDS matrix) = 0.38, P \ 0.0001)

(Fig. 4), i.e., wasps with similar body mass hunted for

similarly large prey.

Do wasps nesting more closely overlap more or less

their prey spectra?

Increasing distance between pairs of nests did not

correspond to an increase or decrease of pairwise prey taxa

dissimilarity in B. merceti in 2009 (Mantel test: r(NEST matrix,

PDS matrix) = -0.09, P = 0.43), B. merceti in 2010 (Mantel

test: r(NEST matrix, PDS matrix) = 0.11, P = 0.37), S. continuus

2007-I (Mantel test: r(NEST matrix, PDS matrix) = -0.06,

P = 0.46), S. continuus 2007-II (Mantel test: r(NEST matrix,

PDS matrix) = 0.07, P = 0.36), and B. zonata in 2010 (Mantel

test: r(NEST matrix, PDS matrix) = 0.21, P = 0.29). However, a

strongly positive association was found between inter-

nest distances and pairwise prey taxonomic dissimilar-

ity in B. zonata in 2009 (Mantel test: r(NEST matrix, PDS matrix)

= 0.55, P \ 0.0001) (Fig. 3c), i.e., more closely nesting

wasps shared more of their prey taxonomic spectra (Fig. 4).

Discussion

All the studied populations showed significant prey taxa

partitioning among individuals. This pattern confirms what

has previously been shown for B. merceti and S. continuus

e

c

0.00

0.05

0.10

0.15

0.20

0.25

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

0.00

0.05

0.10

0.15

0.20

0.25

0.00

0.05

0.10

0.15

0.20

0.25

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0.00.00

0.05

0.10

0.15

0.20

0.25

0.30

0.35

Rel

ativ

e fr

eque

ncy

Pairwise prey taxa dissimilarity (PDS )

B. merceti 2009 B. merceti 2010

B. zonata 2009 B. zonata 2010

S. continuus 2007-I S. continuus 2007-II

a b

d

f

1.00.5 0.0 1.00.5

0.0 1.00.50.0 1.00.5

0.0 1.00.50.0 1.00.5

ij

Fig. 2 Histograms showing the

frequency distributions of the

observed pairwise prey

taxonomic dissimilarity

between all pairs of individuals

(PDSij) for the six studied cases.

a, b B. merceti (2009 and 2010

respectively); c, d B. zonata(2009 and 2010 respectively);

e, f S. continuus (2007-I and

2007-II respectively). Note that

the scales of vertical axes differ

among panels

Popul Ecol (2012) 54:443–454 449

123

(Asıs et al. 2011; Santoro et al. 2011), and is reported here for

the first time in B. zonata, increasing the number of predatory

wasp species in which individual specialization occurs to

about 15 species (Polidori et al. 2011 and unpublished data).

On the contrary, prey size inter-individual variation was not

significant in half of the cases, so it seems overall to be a rarer

occurrence in wasps. Newer and more intriguing results arose

from our analysis of the factors that possibly account for such

inter-individual variation of diet. The influence of the two

factors is discussed in detail below.

Morphological distance and diet dissimilarity

In two cases (B. zonata 2009 and S. continuus 2007-II) we

found a positive correlation between wasp size difference

and prey taxonomic dissimilarity, that is, wasps with sim-

ilar size shared an important proportion of prey taxa,

according to our hypothesis. A similar result has also

recently been found by Bolnick and Paull (2009), using the

same type of statistical approach for a predatory fish, the

threespine stickleback (Gasterosteus aculeatus), but to date

never in invertebrates. Interestingly, both paired body size

and trophic morphology differences in the stickleback

explained only a small percentage of the variance in diet

overlap (about 0.3–0.9 % at best, depending on the mor-

phological trait being considered) compared to our findings

(about 4 % in both wasp species) (Bolnick and Paull 2009;

Ingram et al. 2011).

Though this relationship was clearly tested here for the

first time in wasps, some previous information already

c

e

Pairwise prey size dissimilarity (SDSij)

Rel

ativ

e fr

eque

ncy

B. merceti 2009 B. merceti 2010

B. zonata 2009 B. zonata 2010

S. continuus 2007-I S. continuus 2007-II

a b

d

f

0.0 1.00.5 0.0 1.00.5

0.0 1.00.50.0 1.00.5

0.0 1.00.50.0 1.00.50.00

0.02

0.04

0.06

0.08

0.12

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.08

0.00

0.02

0.04

0.08

0.10

0.12

0.00

0.02

0.04

0.06

0.10

0.12

0.00

0.02

0.04

0.16

0.08

0.10

0.12

0.00

0.02

0.04

0.10

0.06

0.08

0.10

0.12

0.06

Fig. 3 Histograms showing the

frequency distributions of the

observed pairwise prey size

dissimilarity (SDSij) between all

pairs of individuals for the six

studied cases. a, b B. merceti(2009 and 2010 respectively); c,d B. zonata (2009 and 2010

respectively); e, f, S. continuus(2007-I and 2007-II

respectively). Note that the

scales of vertical axes differ

among panels

450 Popul Ecol (2012) 54:443–454

123

suggested that this phenomenon might occur. For example,

in the digger wasps Cerceris arenaria L. and Sphecius

speciosus Drury, dietary segregation is largely due to size-

specific selection, given the great size difference between

small prey species (hunted by small wasps) and large prey

species (hunted by large wasps) (Polidori et al. 2005)

which moreover, at least for C. arenaria, inhabit different

microhabitats. In the beetle-hunting Cerceris rubida Jurine,

the relationship between the size of the female and that of

its prey also suggests that individual diet specialization is at

least partially due to size-constraints, though differences in

microhabitats exploited by individual females, being

essentially the same, would not account for diet segregation

(Polidori et al. 2010). In the cricket-hunting Palmodes la-

eviventris (Cresson), larger females take larger prey, and

size selection may further explain the strong bias towards

female prey (Gwynne and Dodson 1983).

Interestingly, in our sample the relationship between

wasp size and prey size was found to be significantly

positive only in S. continuus, contrasting with the general

trend observed in apoid wasps (e.g., Gwynne and Dodson

1983; Polidori et al. 2005, 2010; Grant 2006; see Polidori

et al. 2011 for a review). However, it is also true that in

Bembix species larger females usually do not discard

small prey, somehow destroying the correlation (see Asıs

et al. 2011). Moreover, Bembix wasps typically maintain a

‘‘margin’’ between the maximum prey mass they can lift

and the mass of the heaviest carried prey (Asıs et al. 2011;

Coelho 2011), possibly due to environmental scarcity of

prey matching the maximum theoretical load, or in order to

retain high manoeuvrability under parasitic pressure (Asıs

et al. 2011; Coelho 2011). In S. continuus, in contrast,

wasps tend to, on average, maximize the prey load (Santoro

et al. 2011). The tendency to maximize prey load (i.e.,

when loaded prey decreases the flight muscle ratio just

above the marginal flight muscle ratio) is not very wide-

spread in wasps and is generally imprecise, since loaded

prey mass, apart from wasp mass, is also greatly influenced

by available prey sizes, by the prey stealing behaviour of

conspecifics or by the location of their nests (review in

Coelho 2011). According in part to this positive relation-

ship between wasp size and mean prey size found in S.

continuus 2007-II, we found a significant relationship

between wasp size distance and prey size overlap in this

case. Such a double relationship (wasp size distance vs.

both prey taxa and prey size dissimilarity) is probably due

to the fact that the PDSij matrix and the SDSij matrix were

highly correlated, i.e., that different prey species also had a

different prey size. Furthermore, the trend observed in S.

continuus in the second generation of 2007 was not found

in the first generation. In the latter, wasp size and mean

prey size were not correlated, and the distributions of PDSij

Pre

y ta

xa d

issi

mila

rity

(PD

S )

Pre

y si

ze d

issi

mila

rity

(SD

S )

0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

Wasp size distance Wasp size distance

Nest-nest distance (cm)

0.0

0.2

0.4

0.6

0.8

1.0

0.0

Pre

y ta

xa d

issi

mila

rity

(PD

S )

Wasp size distance

B. zonata 2009

S. continuus 2007-II

B. zonata 2009

S. continuus 2007-II

a b

c d

0.0

0.2

0.4

0.6

0.8

0.0

0.2

0.4

0.6

0.8

1.0

0.2 0.4 10000 20000

0.2 0.4 0.6 0.0 0.2 0.4 0.6

ijijij

Pre

y ta

xa d

issi

mila

rity

(PD

S ) ij

Fig. 4 Significant relationships

observed between a pairwise

wasp size distance and pairwise

prey taxa dissimilarity of S.continuus 2007-II (P = 0.008),

b pairwise wasp size distance

and pairwise prey size

dissimilarity of S. continuus2007-II (P \ 0.0001),

c pairwise wasp size distance

and pairwise prey taxa

dissimilarity of B. zonata 2009

(P = 0.055), and d pairwise

inter-nest distance and pairwise

prey taxa dissimilarity of

B. zonata 2009 (P \ 0.0001), as

calculated with a two-tailed

Mantel test. The linear least

squares lines for the observed

regressions of diet dissimilarity

functions (i.e., PDSij and SDSij)

are shown. Note that the scales

of both vertical and horizontal

axes differ among panels

Popul Ecol (2012) 54:443–454 451

123

showed a clear bimodal trend, with most individuals

sharing all or no prey taxa. The combination of these two

traits in the first generation probably accounts for the

absence of an effect of size difference on diet dissimilarity.

Because grasshoppers grow during the nesting season of

wasps, size-constraints were probably stronger in the sec-

ond generation (Santoro et al. 2011). The lack of wasp-prey

size correlation in Bembix, on the other hand, agrees with

the lack of significant prey size partitioning among indi-

viduals in all but one case. In fact, for B. zonata 2009,

wasps of similar size shared more prey taxa but did not

hunt for prey items of similar size.

Interestingly, our results can be theoretically linked to

intra-specific competition pressure. In fact, many evolu-

tionary and speciation models assume that competition is

strongest between morphologically identical individuals

(Roughgarden 1972; Dieckmann and Doebeli 1999;

Ackermann and Doebeli 2004). Roughly assuming com-

petition is positively correlated to dietary overlap (Abrams

et al. 2008), our results suggested that in B. zonata and

S. continuus, at least in one generation each, the females

may actually be under a reduced competition stress.

Inter-nest distance and diet dissimilarity

We found a significant effect of inter-nest distance on prey

taxonomic overlap in one case (B. zonata 2009), according

to our hypothesis. In this case, closer-nesting females had

more similar prey spectra, though with the present data it is

not possible to identify the reasons for such a pattern.

Hypothetically, wasps could be activated by the informa-

tion received (at the nest) from successful foragers (Nieh

2009) and would tend to travel to and hunt for prey in

locations where they can see conspecifics preying or

because of local enhancement (e.g., Brown 1986). Such a

phenomenon is known in social wasps (Nieh 2009) but,

although it could also be possible in solitary wasps, which

typically nest in dense and clumped aggregations (e.g.,

Polidori et al. 2006, 2008), it should be tested experi-

mentally. The easiest hypothesis would be that wasps

simply hunt in the closer prey patches, with patches asso-

ciated to the two clusters of nests (about 100 m apart)

harbouring different prey species. Many bombyliid flies

and syrphid flies, the main prey of B. zonata in 2009, are

known to be quite specialist in floral choice (Toft 1983;

Haslett 1989), thus potentially creating patches. Note that

the individual hunting areas of wasps could potentially

overlap, since the distance between nest clusters was cer-

tainly shorter than the maximum foraging distance of

wasps, given that we sporadically observed marked wasps

hunting at more than 500 m from their nests, and also

given the maximum distance reported for bees of similar

size ([1 km) (Greenleaf et al. 2007). Furthermore, the prey

families hunted by B. zonata in 2009 were also abundantly

hunted by B. zonata in 2010 and by B. merceti, thus pro-

viding apparently the same conditions of patch-dependent

prey diversity. The fact that in all the other studied cases

the relationship between inter-nest distance and prey tax-

onomic dissimilarity was not significant suggests that

the spatial distribution of nests, extremely clumped in

B. zonata in 2009, may be the crucial condition favouring

the observed trend in this case. Interestingly, in three

species of desert ants (Ryti and Case 1984) and in the

bumblebee Bombus ardens (Munidasa and Toquenaga

2010), dietary overlap between colonies was positively

(and not negatively as in B. zonata) correlated to the mean

nearest neighbour distance, suggesting that competition for

food regulates the inter-colony distance. However, in B.

zonata in 2009 competition for food would probably have

no effect on the spatial arrangement of nests, because size

difference was also correlated with pairwise diet similarity,

probably acting as a buffer against intra-specific competi-

tion (see above).

Conclusions

Our hypotheses are only partially supported by our data.

Both morphological distance and nest distance can poten-

tially be important in shaping resource use overlap in

wasps, though probably only under certain conditions such

as highly clumped distribution of nests and size-based prey

selection, which in turn are possible only in particular

environmental contexts.

Furthermore, possible differences in prey availability

around the nesting sites may also explain some of the

observed difference in individual specialization patterns.

At the species-level, prey preference (i.e., comparison

between actual and potential prey) and/or prey selection

(i.e., laboratory experiments) was studied in detail for at

least 10 species of digger wasps (reviewed in Polidori et al.

2010). Though prey availability largely explains prey

selection in some cases (e.g., Stubblefield et al. 1993), in

some others it only weakly accounts for prey selection,

such as in C. rubida (Polidori et al. 2010), Sceliphron mud-

dauber wasps (Polidori et al. 2007), S. speciosus (Hastings

et al. 2010) and S. continuus (Santoro et al. 2011), in which

a strong bias towards certain taxa, particular ethological/

ecological prey traits, prey size distribution, or variance in

prey taxa microhabitats are clearly more important. In

addition, in B. merceti a significant role for prey avail-

ability was determined, although the analysis was carried

out at the family level (Asıs et al. 2011), without providing

further details of prey selection at the species level.

Because of these variable results, taxonomic prey oppor-

tunism (i.e., concordance between actual and potential prey

452 Popul Ecol (2012) 54:443–454

123

frequencies) was recently discussed as a doubtful phe-

nomenon in apoid wasps (see Polidori et al. 2010). For

example, an increasing importance is being given to the

‘‘sensory window’’ hypothesis, which states that different

taxa are included or excluded in the diet depending on

chemical recognition thresholds, regardless of abundance

(Anton and Gnatzy 1998; T. Schmitt, personal communi-

cation). Despite no studies having yet been undertaken, at

the individual level, prey availability would probably have

a significant role if different prey species form distinct

patches in the environment (and individual wasps hunt on

different patches) (see above), or due to intra-specific

variance in sensory recognition dynamics or handling

abilities.

Acknowledgments Thanks are due to the Town Hall of Valencia

and the Generalitat Valenciana for issuing the permits necessary to

carry out part of this work in La Mallada Larga (El Saler). We express

our gratitude to M. Portillo (Universidad de Salamanca, Spain) for his

help in determination of prey flies. The research was supported by

funding from the Junta de Castilla y Leon (SA094A09) and from and

by a post-doctoral contract to CP (Program JAE-Doc ‘‘Junta para la

Ampliacion de Estudios’’ funded by the Spanish Research Council

(CSIC) and the FSE). Experiments comply with the current Spanish

law.

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