ArticlePDF Available

Conservation ecology of bees: Populations, species and communities

July 2009
Apidologie 40(3):211-236

DOI:10.1051/apido/2009015

Authors:

Tomás Murray

National Biodiversity Data Centre, Ireland

Michael Kuhlmann

Kiel University

Simon G Potts

University of Reading

Recent concerns regarding the decline of plant and pollinator species, and the impact on ecosystem functioning, has focused attention on the local and global threats to bee diversity. As evidence for bee declines is now accumulating from over broad taxonomic and geographic scales, we review the role of ecology in bee conservation at the levels of species, populations and communities. Bee populations and communities are typified by considerable spatiotemporal variation; whereby autecological traits, population size and growth rate, and plant-pollinator network architecture all play a role in their vulnerability to extinction. As contemporary insect conservation management is broadly based on species- and habitat-targeted approaches, ecological data will be central to integrating management strategies into a broader, landscape scale of dynamic, interconnected habitats capable of delivering bee conservation in the context of global environmental change.

Conceptual framework for studying impacts of land-use change on bee conservation; incorporating the biology of the organisms involved, in addition to ecosystem service provision and its positive feedback into economics and conservation policy. Numbers in boxes refer to the relevant section in the text. Modified from Kremen et al. (2007).

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Apidologie 40 (2009) 211–236 Available online at:

INRA/DIB-AGIB/EDP Sciences, 2009 www.apidologie.org

DOI: 10.1051/apido/2009015 Review article

Conservation ecology of bees: populations, species and

communities*

Tomás E. Murray1, Michael Kuhlmann2,SimonG.Potts3

1Crops Research Centre, Teagasc, Oak Park, Carlow, Co. Carlow, Ireland

2Department of Entomology, Natural History Museum, Cromwell Road, London SW7 5BD, UK

3Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of

Reading, Earley Gate, Reading RG6 6AR, UK

Received 30 October 2008 – Accepted 13 February 2009

Abstract – Recent concerns regarding the decline of plant and pollinator species, and the impact on ecosys-

tem functioning, has focused attention on the local and global threats to bee diversity. As evidence for bee

declines is now accumulating from over broad taxonomic and geographic scales, we review the role of

ecology in bee conservation at the levels of species, populations and communities. Bee populations and

communities are typiﬁed by considerable spatiotemporal variation; whereby autecological traits, popula-

tion size and growth rate, and plant-pollinator network architecture all play a role in their vulnerability

to extinction. As contemporary insect conservation management is broadly based on species- and habitat-

targeted approaches, ecological data will be central to integrating management strategies into a broader,

landscape scale of dynamic, interconnected habitats capable of delivering bee conservation in the context

of global environmental change.

conservation /biodiversity /population /community /plant-pollinator

1. INTRODUCTION

Concerns about a potential pending global

‘pollinator crisis’ have been raised for over a

decade, based on the evidence available at the

time (Buchmann and Nabhan, 1996; Kearns

et al., 1998; Kremen and Ricketts, 2000;Diaz

et al., 2005), though such a crisis was ques-

tioned by Ghazoul (2005); but see Steﬀan-

Dewenter et al., (2005). Prior to 2006, doc-

umentation of bee declines were limited to

a few case studies and were generally taxo-

nomically restricted and considered only spe-

ciﬁc locations (e.g. bumblebees, Peters, 1972,

Williams P.H., 1986; honeybees, Williams I.H.

et al., 1991; solitary bees, Westrich, 1989), and

were not often published in mainstream scien-

tiﬁc literature (e.g. Rasmont, 1988;Falk,1991;

Corresponding author: T.E. Murray,

tomas.murray@teagasc.ie

* Manuscript editor: Robert Paxton

Banaszak, 1995).Theneedformoreacom-

prehensive understanding of the global sta-

tus and trends of pollinators triggered a num-

ber of projects and studies aiming to provide

large-scale and taxonomically diverse assess-

ments. In Europe, the ALARM project1pro-

vided the ﬁrst national-scale assessments of

shifts in whole bee communities in the UK and

Holland (Biesmeijer et al., 2006) and demon-

strated severe declines in bee diversity, abun-

dance and ranges and also concurrent declines

in bee-pollinated ﬂowering plants. In North

America, a synthesis of existing information

was undertaken (National Research Council,

2006) and concluded that there were long-term

declines in honeybees and some wild bees

(most notably bumblebees). Recognition of

widespread loss of pollinators and pollinator

1Assessing Large-scale Risks to biodiversity with

tested Methods, www.alarmproject.net

Article published by EDP Sciences

212 T.E. Murray et al.

services by the Convention on Biological Di-

versity (through the Agricultural Biodiver-

sity programme and International Pollinator

Initiative2) resulted in FAO coordinating the

‘Rapid Assessment of Pollinators’ status’ re-

port (2008) which aims to compile global ev-

idence of the extent of pollinator shifts and

loss of pollination services. Together these

sources, and many other studies (e.g. Klein

et al., 2002;Larsenetal.,2005; Williams N.M.

and Kremen, 2007), provide an overwhelming

evidence-base for marked declines of many

taxa of bees across the world.

The loss of bee species from communities

may not be a random process e.g. large-bodied

bees with higher pollination eﬃciencies can be

more extinction prone (Larsen et al., 2005),

and so has important implications for pol-

lination services to crops and wild ﬂowers

(Memmott et al., 2004). Drivers of local bee

extinctions can act diﬀerentially on particular

bee traits such as size, foraging and nesting

behaviour. For instance, in Californian agro-

ecosystems, Larsen et al. (2005) reported that

large-bodied bees were more extinction-prone,

and Memmott et al. (2004) demonstrated that

larger bees (such as bumblebees) tend to be

more highly linked in plant-pollinator webs.

Similarly wildﬁres were found to disassem-

ble Swiss and Israeli bee communities in a

non-random fashion, with extinction probabil-

ities related to nesting guild, phenology, for-

aging behaviour and size (Potts et al., 2005;

Moretti et al., 2009). However, the sensitiv-

ity of particular bee species to the wide range

of natural and anthropogenic drivers remains

largely unknown. It is therefore essential to

understand the basic ecology of bees in order

to predict how they respond to environmental

change and how these changes can be miti-

gated against.

A general conceptual framework has been

proposed to facilitate our understanding of

how bees, and other “mobile-agent-based

ecosystem service providers”, are aﬀected by

land-use change (Kremen et al., 2007). The

model describes interactions between bees, the

temporal and spatial availability of resources,

2http://www.cbd.int/programmes/areas/agro/

pollinators.aspx

biotic and abiotic factors aﬀecting bee ﬁtness,

the delivery of pollination services and how

these are all potentially aﬀected by land-use

change, policy and market forces (Fig. 1). By

adopting this model, i.e. incorporating individ-

ual behaviour, population biology and commu-

nity dynamics, this review aims to highlight

speciﬁc areas of bee ecology that will have the

greatest impact on the development and appli-

cation of conservation strategies.

2. AUTECOLOGY AND

CONSERVATION

It is now widely accepted that sensible

management begins with a sound, fundamen-

tal understanding of a species’ ecological

interactions and natural history (Simberloﬀ,

1988; Brussard, 1991; Schultz and Hammond,

2003). Nonetheless, detailed autecological

study, like systematics, seems to lack the ca-

chet of academic respectability that ensures

practitioners of regular funding or even em-

ployment (Kim and Byrne, 2006). Unsurpris-

ingly, we are woefully short on autecological

information for rare and little-known species,

but it is also true for many of the more charis-

matic bees, such as bumblebees (e.g. Kosior

et al. 2007; Williams P.H. and Osborne, 2009).

These autecological data are of critical im-

portance for calculating a suite of parameters

which can be used to predict extinction risk

as elements in population viability analysis

(PVA) and identify traits correlated with vul-

nerability to extinction in phylogenetic com-

parative approaches (Schultz and Hammond,

2003; Fisher and Owens, 2004). Even basic

ecological knowledge gleaned from the liter-

ature can be utilized to predict the risk of

extinction and prioritise species of conserva-

tion concern. In the Lepidoptera, for example,

traits associated with vulnerability to extinc-

tion, although frequently highly taxon depen-

dent, typically include: dispersal ability, larval

speciﬁcity, adult habitat breadth and length of

ﬂight period (Kotiaho et al., 2005).

It is important to note that autecological

studies do not need to be mundane exercises in

data gathering; rather, the autecological traits

discussed below should be used to generate

Conservation ecology of bees 213

Figure 1. Conceptual framework for studying impacts of land-use change on bee conservation; incorpo-

rating the biology of the organisms involved, in addition to ecosystem service provision and its positive

feedback into economics and conservation policy. Numbers in boxes refer to the relevant section in the text.

Modiﬁed from Kremen et al. (2007).

testable hypotheses to drive several research

projects. In the absence of detailed autecologi-

cal information and long-term population data,

we will continue to be forced to make sev-

eral assumptions when both interpreting pre-

cipitous declines in numbers and when recom-

mending appropriate management actions.

2.1. Socioecology

The primary eﬀect of sociality on bee con-

servation biology is its impact on a species’

population biology and genetics (reviewed in:

Pamilo et al., 1997; Chapman and Bourke,

2001; Zayed, 2009). What best deﬁnes a pop-

ulation of bees is fundamentally tied to its

level of social organisation and the resul-

tant reproductive potential of each individual

(Crozier and Pamilo, 1996). Thus, a popu-

lation of a solitary species, where each in-

dividual may reproduce, would be a popu-

lation of individuals; whereas a population

of eusocial bees would be a population of

colonies, as within a colony one or few re-

lated queens reproduce and most individuals

are non-reproductive workers. Consequently,

the ratio of the eﬀective to the census popula-

tion size can rapidly decrease with increasing

social organisation (Pamilo and Crozier, 1997;

Chapman and Bourke, 2001). Similarly, the

ease with which we can establish the popula-

tion size, and therefore the conservation status,

of a taxon typically decreases with increasing

social complexity.

Although the majority of bees are soli-

tary, all levels of social organisation occur

within the Apoidea (Michener, 1974; Crozier

and Pamilo, 1996). Some families of bees, the

sweat bees (Halictidae) in particular, are note-

worthy among insects due to their substan-

tial interspeciﬁc (Danforth, 2002; Brady et al.,

2006) and intraspeciﬁc (Soucy, 2002)vari-

ability in social behaviour. The behavioural

plasticity observed within halictid social be-

haviour is of particular relevance as an exam-

ple of how some species can exhibit more than

one type of sociality across geographic and

214 T.E. Murray et al.

climatic gradients e.g. both Lasiglossum cal-

ceatum and Halictus rubicundus are social in

lower altitudes and solitary at higher altitudes

(Sakagami and Munakata, 1972; Eickwort

et al., 1996). In the absence of detailed auteco-

logical information for many rare species, util-

ising methods such as phylogenetic compara-

tive approaches (e.g. Fisher and Owens, 2004)

in well-described groups such as the sweat

bees could highlight previously unreported

socially polymorphic taxa in other families

and stimulate further ecological research. For

those species where sociality has been con-

ﬁrmed, establishing both the level and plastic-

ity of social organisation is an important ﬁrst

step in any conservation programme. As men-

tioned, the eﬀective population size, and there-

fore the vulnerability, of a species depends

not only on the number of nests, but also on

the mode of colony foundation, number of re-

productive individuals and reproductive skew

among these individuals (see Sect. 3.2 Mating

systems).

2.2. Parasitism

An adjunct to the levels of social organisa-

tion found within bees are their varying forms

of parasitism, namely: usurpation and rob-

bing, social parasitism and cleptoparasitism

(Michener, 2007). In all cases, the parasite

beneﬁts from the resources gathered and/or

constructed by the host, with the host presum-

ably incurring a ﬁtness cost in the process. It

is estimated that 15–20% of all bee species are

parasites (Wcislo and Cane, 1996), with the

percentage of parasitic species tending to in-

crease with latitude (Wcislo, 1987; Petanidou

et al., 1995). Despite the relative abundance

and mostly temperate distribution of parasitic

bees, relatively little is known about their bi-

ology as their population sizes rarely become

large enough for detailed study (Scott et al.,

2000; Bogusch et al., 2006).

The term ‘coextinction’ was coined after

Stork and Lyal (1993) drew attention to the

likelihood that many parasites may go extinct

when their hosts go extinct. In a recent re-

view, Koh et al. (2004) found that approxi-

mately 5000 insect species are likely to be en-

dangered as a direct consequence of the en-

dangerment of their hosts and that at least 100

species of beetles, lice and butterﬂies have

probably gone extinct in the last 200 years

due to the extinction of their hosts. Although

it is diﬃcult to generalise about the pattern

and degree of specialisation across parasitic

bee taxa (e.g. Bogusch et al., 2006), most stud-

ies have revealed a strict concordancebetween

physiology and behaviour of parasite and host

(Wcislo, 1987; Scott et al., 2000). Therefore,

determining the degree of specialisation be-

comes increasingly important as it is proba-

bly proportional to the probability of host and

parasite becoming coextinct. Furthermore, due

to their generally lower population sizes, de-

clines in parasite populations may frequently

precede those of their host populations, as ob-

served by Rasmont et al. (2005) in Belgium

where declines of megachilid and anthophorid

cleptoparasites were found to be dispropor-

tionably higher than those of their hosts.

2.3. Floral resources and specialisation

Bees are herbivores that feed their lar-

vae with a mixture of pollen and nectar or,

rarely, plant oils (Michener, 2007). Robertson

(1925) was one of the ﬁrst to recognize that

bees do not collect pollen on ﬂowers ran-

domly but that some species demonstrate ﬂo-

ral speciﬁcity when harvesting pollen only

on a limited number of plant taxa. He in-

troduced the terms monolecty, oligolecty and

polylecty to distinguish between pollen spe-

cialists and generalists, respectively. This clas-

siﬁcation inadequately reﬂects the complex

relationships between bees and their pollen

hosts and was updated by Cane and Sipes

(2006), and recently modiﬁed by Müller and

Kuhlmann (2008;Tab.I).

Even generalist bees show a restricted

range of pollen sources (Westrich, 1989;

Müller, 1996, Müller and Kuhlmann, 2008);

pollen might not be an easy to use protein

source. Praz et al. (2008) demonstrated that

several specialized bee species fail to de-

velop on non-host pollen, indicating that the

pollen of some plant taxa, e.g. Asteraceae,

Conservation ecology of bees 215

Table I. Classiﬁcation of ﬂoral speciﬁcity of pollen collection by Robertson (1925), Cane and Sipes (2006),

and an updated classiﬁcation proposed by Müller and Kuhlmann (2008)(diﬀerences in terminology and

deﬁnitions in italics).

Robertson (1925) Cane and Sipes (2006) Müller and Kuhlmann (2008)

Monolecty Monolecty

Pollen collection on only one plant

species even in the presence of one

or more sympatric species of the same

genus

Monolecty

Pollen collection on only one plant

species even in the presence of one

or more sympatric species of the same

genus (see also Narrow oligolecty)

Oligolecty Narrow oligolecty

Pollen collection from two to several

species belonging to one plant genus

Narrow oligolecty

Pollen collection from two to several

species belonging to one plant genus

(pollen collection on only one plant

species in the absence of co-ﬂowering

congenerics is referred to as a special

case of narrow oligolecty)

Oligolecty

Pollen collection from two to several

species belonging to one to four genera

belonging to one family

Broad oligolecty

Pollen collection from two to several

genera belonging to one plant tribe,

subfamily or family

Eclectic oligolecty

Pollen collection from two to four plant

genera belonging to two or three plant

families

Eclectic oligolecty

Pollen collection from two to four plant

genera belonging to two or three plant

families

Polylecty s.l.

Mesolecty

Pollen collection from more than four

plant genera belonging to two or three

plant families or big tribes

Mesolecty

Pollen collection from more than four

plant genera belonging to two or three

plant families

Polylecty with strong preference

Pollen collection from several plant

families, but one plant clade (family,

subfamily, tribe, genus or species)pre-

dominates

Polylecty

Pollen collection from various genera

belonging to four to <25% of available

plant families

Broad polylecty

Pollen collection from various genera

belonging to >25% of available plant

families

Polylecty s.s.

Pollen collection from various genera

belonging to at least four plant families

possesses unfavourable or protective proper-

ties that render its digestion diﬃcult. This sug-

gests that the successful utilization of pollen

by bees in general might require special phys-

iological adaptations to cope with toxic sec-

ondary chemicals of their hosts. Selection

should favour the evolution of such adap-

tations and eventual host speciﬁcity in bees

(Praz et al., 2008) if they ﬁt the physiological-

eﬃciency hypothesis (Cornell and Hawkins,

2003), which predicts a physiological trade-

oﬀin the ability to eﬃciently utilize alterna-

tive hosts as a consequence of these adapta-

tions (Singer, 2008).

216 T.E. Murray et al.

The quantitative pollen requirements of

bees are little known. In a study of 41 bee

species Müller et al. (2006) revealed that 85%

of them require the whole pollen content of

more than 30 ﬂowers to provision a brood cell

and some species even needed the pollen of

more than a thousand ﬂowers to rear a single

larva. In combination with the often restricted

foraging range of small bees (see Sect. 3.1

Dispersal), this implies that tens of thousands

of ﬂowers of a certain plant must be avail-

able within range to sustain a viable popu-

lation of an oligolectic bee species. Hence,

the loss of plant diversity and ﬂower quantity

due to habitat destruction and fragmentation

of the landscape is assumed to be responsible

for the decline of many bee species (Müller

et al., 2006). Social bee species are typically

polylectic (Michener, 2007) and are generally

be believed to be less prone to local extinction.

However, Kleijn and Raemakers (2008)have

recently shown that bumblebee species whose

populations are in decline use a narrower spec-

trum of host plants than bumblebees with sta-

ble populations.

Specialized bees generally do not switch to

other host plants, even if their preferred plants

are not in ﬂower (Strickler, 1979; Williams

N.M., 2003). Hence, selection for synchrony

of bee emergence with host plant ﬂowering

that is positively aﬀecting individual ﬁtness

(Powell and Mackie, 1966) can be expected,

especially in arid and semi-arid environments

with highly variable precipitation. Anecdo-

tal observations and experimental data sug-

gest that in arid environments rainfall triggers

the emergence of oligolectic bees in particular

(reviewed in Danforth, 1999). Evidence from

western South Africa challenges this view

(Mayer and Kuhlmann, 2004) and contradicts

the assumption that bees react to the same

environmental cues for emergence as their

host plants for ﬂowering e.g. rainfall (Linsley,

1958; Wcislo and Cane, 1996; Tauber et al.,

1998). However, generally it is hypothesized

that host plant synchrony might be a mecha-

nism for an elevated rate of speciation in desert

bees (Minckley et al., 2000; Danforth et al.,

2003) explaining the higher bee species diver-

sity in semi-arid and arid environments. Thus,

oligolectic bees that are strictly dependent on

their host plants are most species rich in desert

and Mediterranean environments, and less di-

verse in temperate biota (Moldenke, 1979).

2.4. Nesting resources

Nesting resources for bees include the sub-

strates within, or on which, they nest and also

the materials required for nest construction.

Bees are extremely diverse in their nesting

ecology and comprise a number of distinct

guilds (O’Toole and Raw, 1991): miners, car-

penters, masons, social nesters and cuckoos.

Mining bees include all Andrenidae, Melitti-

dae, Oxaeidae, Fideliinae and most Halictidae,

Colletidae and Anthophorini species. Miners

excavate tunnels in the ground or soft rocky

substrates and line their tunnels with glandu-

lar secretions. Carpenter bees also excavate

nests, but use wood as a substrate, and in-

clude species in the genera Xylocopa,Cer-

atina (Apidae) and Lithurgus (Megachilidae).

In contrast, mason bees (most Megachilidae)

utilise pre-existing holes which can be in the

form of hollow plant stems, abandoned in-

sect nest burrows in the ground or woody

substrates, small cavities or cracks in rocks

and even snail shells. Masons then line the

inside of the pre-existing hole with materi-

als such as leaves or soil. Within the ma-

son guild, the leaf-cutter bees use only freshly

gathered leaf or petal material to line their

nests and are members of the Megachile and

Creightonella genera of the Megachilidae. So-

cial nesters tend to use relatively large pre-

existing cavities to establish social colonies

and include three taxa within the Apidae: hon-

eybees (Apis), bumblebees (Bombus) and stin-

gless bees (Meliponini). One guild of bees, the

cuckoo bees or cleptoparasites, are found in

several families and do not construct their own

nests but instead parasitize the nests of other

bees by laying their eggs on larval provisions

provided by the host.

Potts et al. (2005) demonstrated that the

availability of both nesting substrates and con-

struction materials were primary determinants

of overall bee community composition. Fur-

thermore, the dominant ecological perturba-

tion, ﬁre, resulted in a marked turnover of

Conservation ecology of bees 217

nesting resources, resulting in large shifts

in the relative proportions of nesting guilds.

Other resources shown to aﬀect bee nest-

ing success include: the abundance, size and

species of trees in tropical forests for stingless

bees (Eltz et al., 2002; Samejima et al., 2004);

cavity shape and size for honeybees (Schmidt

and Thoenes, 1992; Oldroyd and Nanork,

2009), and the diameter of pre-existing holes

for colletid bees (Scott, 1994); soil hardness,

slope and aspect of the ground for halictid bees

(Potts and Willmer, 1997); and soil texture for

solitary bees (Cane, 1991).

The diversity of nesting strategies and the

specialisation of guilds means that the avail-

ability of the correct quantity and quality of

resources, both in space and time, are key de-

terminants for which species a landscape can

support (Tscharntke et al., 2005). Any envi-

ronmental disturbance (e.g. habitat loss, frag-

mentation, agricultural intensiﬁcation, or ﬁre)

will alter the distribution of nesting resources.

As bees are central place foragers and have

species-speciﬁc ﬂight distances, the location

of the nest determines what ﬂoral resources are

potentially available. The nesting traits of bee

species will therefore determine their sensi-

tivity to environmental change (Moretti et al.,

2009). In order to manage the landscape for

bee conservation it is therefore essential to un-

derstand how land use change aﬀects nesting

resources and how this interacts with the avail-

ability of other resources such as nectar and

pollen.

3. POPULATION BIOLOGY AND

CONSERVATION

Species are driven to extinction by both

human-mediated deterministic factors and

stochastic factors (Frankham et al., 2002). In

general, a species’ population size is initially

reduced by deterministic factors such as habi-

tat loss, fragmentation, overexploitation, intro-

duced species, pollution and climate change.

Populations may then further decline to a point

of ‘no return’ where demographic, environ-

mental and genetic stochasticity and catastro-

phes eventually drive them to extinction. Con-

sequently, as both absolute population size

and spatio-temporal variability in population

size are universally the most important pre-

dictors determining extinction risk, their accu-

rate estimation is of paramount importance to

conservation biology (Frankham et al., 2002;

O’Grady et al., 2004).

Insect populations commonly experience

large annual ﬂuctuations in population size,

arising from natural variation in population

growth and measurement errors in population

estimates (e.g. Schultz and Hammond, 2003).

Unfortunately, bee populations and commu-

nities are no exception, displaying consider-

able spatio-temporal variation in abundance

and composition (Williams N.M. et al., 2001;

Roubik, 2001; Eltz, 2004; Tylianakis et al.,

2005; Petanidou et al., 2008). The highly vari-

able nature of these ecological data compli-

cates the determination of the conservation

status of a species, as devastating declines may

occur, but remain undetected until a suﬃcient

period of time has elapsed after monitoringthe

population. Unfortunately, this typically leaves

managers and policy makers in a reactive pos-

ture as the decline might be demonstrated, but

only after it has already seriously weakened

the population.

Although in many cases an experimental

approach may be more appropriate, in prac-

tice, especially for rare species, the logistics,

lack of replication and spatial scales involved

have driven the proliferation of modelling ap-

proaches to test hypotheses about the causes

of decline and the response of populations to

management practices or future changes in the

environment (e.g. risk-based viable population

monitoring, Staples et al., 2005). In a review

of the ecological tools available to conserva-

tionists to intervene in the extinction process,

or even predict precipitous declines, Norris

(2004) outlines a ‘toolbox’ for the manage-

ment of threatened species: statistical mod-

els of habitat use, demographic models and

behaviour-based models. In particular, popu-

lation viability analysis (PVA) is one of the

most widely applied demographic models in

conservation (Lande et al., 2003), and as re-

cent modiﬁcations to PVA now allow for less

intensive data (e.g. shorter time series and

population surveys) more often available for

insect populations, it has been successfully

218 T.E. Murray et al.

applied to endangered insects, particularly but-

terﬂies (e.g. Schultz and Hammond, 2003;

Schtickzelle and Baguette, 2004).

There are innumerable parameters that may

be discussed in relation to studying the pop-

ulation biology of a single species. Below we

highlight three keys areas of study that can sig-

niﬁcantly inﬂuence the estimation of popula-

tion size, growth rate and persistence of bee

populations.

3.1. Dispersal

Female bees forage from a single loca-

tion, their nest, and as such are central place

foragers (Schoener, 1979). Theoretical stud-

ies frequently emphasise the role of disper-

sal ability and emigration between patches in

predictions of minimum viable population size

(Hanski and Pöyry, 2006), thus information

of their ﬂight range is vital for bee conserva-

tion to make sure their habitat requirementsare

met within their range of activity (Westrich,

1996;Cresswelletal.,2000). Known forag-

ing distances of bees range from 0.1 km to

a maximum of 45.5 km in Eufriesea surina-

mensis, with values for most species below

1 km (summarized in Greenleaf et al., 2007)

and a strong correlation exists between the in-

tertegular span (ITS) and foraging range that

can be used as a valuable tool to predict for-

aging ranges based on a simple measurement

of ITS. In addition, knowledge about the for-

aging range is also important for estimation of

area requirements of bees for providing opti-

mal pollination service in agriculture (Kremen

et al., 2004). For conservation measures it is

vital to take into account that species with a

small foraging range require more diverse re-

sources per unit area than species with simi-

lar needs but greater range (Cresswell et al.,

2000). Thus, for many species local habitat

structure appears to be more important than

large-scale landscape composition (Gathmann

and Tscharntke, 2002).

However, considering the abundance of

data on the relationship between body size

and foraging distance (e.g. Greenleaf et al.,

2007), little data exist on how species’ forag-

ing ranges relate to male- or female-mediated

gene ﬂow between populations. In the Eu-

glossini, long-distance gene ﬂow across the

Andes was related to body size, with larger

body sizes potentially conferring a disper-

sal advantage in terms of thermal tolerance

and energy reserves for long-distance disper-

sal (Dick et al., 2004). In contrast, the level

of population genetic subdivision (e.g. Fst)

within the honeybee Apis mellifera was almost

twice as high in South Africa (0.105) com-

pared to Germany (0.064), despite the fact that

the sampled subpopulations in South Africa

were geographically closer together (Moritz

et al., 2007). Generalisations regarding gene

ﬂow and body size may be spurious, as a

species’ dispersal ability may equally be de-

termined by a range of other socio-ecological

factors, such as nest-site philopatry, lecty and

tolerance to inbreeding depression (Packer and

Owen, 2001; Packer et al., 2005). Resolving

the determinants of gene ﬂow between popu-

lations is of critical importance to all species-

based conservationprogrammes and should be

a fruitful avenue for future research in bee con-

servation.

Regardless of the lack of data regarding

gene ﬂow, population viability and minimum

habitat requirements of bees (e.g. Larsen et al.,

2005), small and isolated bee populations can

persist for relatively long periods of time

provided that the habitat remains unchanged

(Kratochwil and Klatt, 1989). Basically bees

are physiologically highly capable of ﬂying

long distances increasing the likelihood that

a habitat is (re)colonized. Solitary bees have

been found on lightships in the North Sea and

Baltic Sea up to 10 km oﬀthe coast, bum-

blebees even up to 30 km distance from the

nearest land, but most of the specimens were

close to the end of their reproductive phase

and thus not of signiﬁcance for colonization

(Haeseler, 1974). Capacity for (re)colonization

is correlated to distance and habitat frag-

mentation (Steﬀan-Dewenter and Tscharntke,

1999;Steﬀan-Dewenter and Westphal, 2008)

but even areas neighbouring ancient suitable

bee habitats are slowly recolonized (Forup

et al., 2008) and isolated habitats like islands

(Haeseler, 1976,1978) are hardly reached

by most bee species, limiting the potential

success of ecological restoration measures

Conservation ecology of bees 219

(Kuhlmann, 2000; Franzén et al., 2009). De-

spite the fact that the colonization ability of

bees seems to be generally low, massive and

short-term range extensions are known from

a few species like Andrena fulva and Bom-

bus hypnorum in NW Germany about a cen-

tury ago (Wagner, 1938) and, more recently,

Andrena cineraria (Haeseler, 1973), Halic-

tus scabiosae (Frommer and Flügel, 2005)

and Colletes hederae (Kuhlmann et al., 2007;

Frommer, 2008).

3.2. Mating systems

In the context of population biology, the

eﬀective population size, population growth

rate and variance in population growth rate

of a species depend not only on the num-

ber of individuals and nests, but also on the

level polygamy and inbreeding present within

the population (Pamilo and Crozier, 1997;

Chapman and Bourke, 2001). Due to the hap-

lodiploid nature of bees, the eﬀect of inbreed-

ingoneﬀective population size is a function

of the sex ratio and level of polygamy (see

Zayed, 2009). Brieﬂy, as females are diploid,

they contribute twice the genetic diversity to

a population than haploid males, thus mul-

tiple mating by females increases the eﬀec-

tive population size, but multiple mating by

males decreases it, as several females in a

population would carry the sperm of a single

male (Crozier and Pamilo, 1996; Hedrick and

Parker, 1997).

The majority of the 20–30000 estimated

bee species are solitary (Michener, 2007),

yet knowledge of solitary bee mating sys-

tems is still quite limited compared to social

species; the assumption that females of most

species are monogamous remains (Eickwort

and Ginsberg, 1980). Currently, there is in-

suﬃcient genetic pedigree (genetic analysis of

mother and oﬀspring) data or behavioural ob-

servations to support this assumption (Paxton,

2005). For example, Blanchetot’s (1992)ge-

netic pedigree study of the solitary leafcutter

bee Megachile rotundata supports monoandry

in this bee, whereas in the primitively euso-

cial sweat bee Lasiglossum malachurum both

ﬁeld observations (Knerer, 1992) and genetic

pedigree data (Paxton et al., 2002) indicate that

polyandry is common in this species. More

data on other solitary and primitively social

species are necessary before any generalisa-

tions over female mating systems can be made.

In contrast, better data on female mating

systems exist for the eusocial bumblebees,

honeybees and stingless bees. Single mating

by females appears to be the norm for most

bumblebees (Schmid-Hempel and Schmid-

Hempel, 2000), but there are exceptions (Bom-

bus hypnorum; Paxton et al., 2001). Honey-

bees are highly polyandrous (Schlüns et al.,

2005), whereas stingless bees are typically

monoandrous (Paxton et al., 1999; Peterset al.,

1999). Given this disparity in female mating

frequency, it is notable that both honeybees

and stingless bees are exceptional in thatmales

only mate once (Roubik, 1989; Koeniger,

1991); whereas, for most species, males prob-

ably mate repeatedly (Paxton, 2005).

Despite diﬃculties in systematically

recording mating behaviour, there is a clear

need to conﬁrm where, when and how often

mating occurs, especially as the reproductive

rates of solitary bees can be surprisingly low

(Minckley et al., 1994). Furthermore, the

presence of distinct intraspeciﬁc variability in

male mating behaviour, associated with (e.g.

Amegilla dawsoni, Alcock, 1997) or without

(e.g. Andrena agilissima, Paxton et al., 1999)

size diﬀerences, represents a unique opportu-

nity to further advance our understanding of

how mating behaviour can inﬂuence repro-

ductive success at a population level, and how

this inﬂuences our estimation of population

size and growth rate for conservation.

3.3. Predators, parasites and pathogens

Major factors limiting bee populations such

as nest site or nest material (e.g. Potts

and Willmer, 1997), climatic conditions (e.g.

Pekkarinen, 1997) and pollen availability (e.g.

Minckley et al., 1994) have received rela-

tively detailed study compared to how preda-

tors, parasites and pathogens aﬀect bee mor-

tality, population dynamics and community

composition. The potential for parasites and

pathogens to limit, or regulate, bee populations

is now glaringly apparent considering that

220 T.E. Murray et al.

Varroa destructor parasitic mites, for exam-

ple, destroyed 25–80% of managed honey-

bee colonies, and nearly all feral colonies, in

parts of the United States during the mid-

1990s (Sammataro et al., 2000). The epidemic

of ‘Colony Collapse Disorder’ destroyed 50–

90% of US colonies in aﬀected apiaries in

2006/07, and also has been suggested to

involve a contagious pathogen (Cox-Foster

et al., 2007). It is possible that such marked

declines may also occur in many populations

of non-managed bees over similar geographic

scales (e.g. Andrena scotica;Paxtonetal.,

1997), but such declines are frequently un-

recorded or may be obscured by the consider-

able spatiotemporal variation in abundance ob-

served in many species (Williams N.M. et al.,

2001; Roubik, 2001; Tylianakis et al., 2005).

Furthermore, even sub-lethal eﬀects of in-

fection may alter plant-pollinator interactions

and, therefore, ecosystem functioning (Eviner

and Likens, 2008). For example, the ability

of Bombus terrestris foragers to discriminate

rewarding ﬂowers based on either colour or

odour decreased after being infected by the

protozoan parasite Crithidia bombi (Gegear

et al., 2006).

Better data on the potential of parasites and

pathogens to aﬀect ecological interactions be-

tween species are available for the eusocial

bumblebees. At the regional scale (50 km2),

parasite diversity is proportional to regional

bumblebee host distribution and local abun-

dance; parasite load (the average number of

parasite species per individual worker) is in-

versely proportional to host species diversity

(Durrer and Schmid-Hempel, 1995;Schmid-

Hempel, 2001). These data support the hy-

pothesis that widely distributed (common)

host species may be adapted to a wider vari-

ety of parasites, pathogens or strains of both,

whereas locally occurring (rare) host species

may be adapted to a subset of the parasites

present (Price et al., 1986,1988). When both

rare and common host species coexist, the

common species is expected to have a com-

petitive advantage due to both its adaptation

to a wider variety of parasites, and by main-

taining a greater diversity of potentially more

virulent parasites within regions. However,

aside from cases of pathogen spillover from

introduced species (see Stout and Morales,

2009); there is currently little evidence re-

garding the role of parasites and pathogens

as drivers of decline in bumblebees (Goulson,

2003; Williams P.H. and Osborne, 2009). Us-

ing a novel comparative approach to inves-

tigate the role of pathogens in eusocial lin-

eages, Boomsma et al. (2005) propose a series

of testable hypotheses regarding eusocial bee

pathogens in comparison to eusocial wasps,

ants and termites: orally transmitted diseases

should be more common, more virulent and

endemic than those found in ants and termites;

the incidence of macroparasites (e.g. mites,

nematodes, parasitoids) should be intermedi-

ate between wasps and termites; and verti-

cal transmission of parasites should be more

common in bees and wasps, particularly in

colonies with multiple queens.

Other than phenomenological reports, lit-

tle data exist on the impact of parasites or

pathogens on the population dynamics in soli-

tary bees. For example, the Stylopidae have the

highest diversity of any strepsipteran family

(ca. 160 species) and are exclusive endopar-

asites of bees (Pohl and Beutel, 2008), yet

aside from their ability to eﬀectively neuter

their host (Wülker, 1964;Askew,1971), rel-

atively little is known about their impact on

host populations (Kathirithamby, 1989). In the

context of social evolution, predators, particu-

larly ants, cause signiﬁcant levels of mortality

in solitary versus social ground-nesting bees

and are, therefore, constraints on independent

nesting. Over a ﬁve-week period, all nests con-

taining only one female of the facultatively

social halicitid bee Megalopta genalis failed

to survive brood predation by ants, whereas

nests containing multiple females all survived

(Smith et al., 2007). Similarly, Zammit et al.

(2008) recorded colony survival and brood

production rates in predator-excluded versus

control nests of the cooperatively nesting al-

lodapine bee Exoneura nigrescens: 77.8% of

nests protected from ants survived, with an

average 3.55 brood per nest, compared to

41% survival and 1.56 brood per nest in un-

protected nests. Likewise, for eusocial bees,

high predation rates have been recorded by

predators such as the bee wolf, Philanthus

spp.; typically-sized aggregations of these

Conservation ecology of bees 221

crabronid wasps have been estimated to con-

sume 1015 bumblebees per hour (Dukas,

2005) and around 30000 honeybees per day

(Simonthomas and Simonthomas, 1980). It is,

therefore, unsurprising that in a recent meta-

analysis on the impact of predation on ecosys-

tem functioning, Knight et al. (2006) found

that predators had a substantial negative im-

pact on pollinator visitation rate and reproduc-

tive success of plants. However, the relative

importance of top-down (predators, parasites

and pathogens) versus bottom-up factors (ﬂo-

ral and nesting resources) in regulating bee

populations is still largely unknown.

4. COMMUNITY ECOLOGY AND

CONSERVATION

The response of individuals, populations

and communities of bees to changes in land-

use is primarily driven by the spatial and tem-

poral distribution of ﬂoral, nesting and over-

wintering resources in relation to the foraging

and dispersal abilities of bees (Kearns et al.,

1998;Kremenetal.,2007). Using concepts

from network theory, recent advances in the

study of plant-pollinator networks have con-

siderably improved our ability to deﬁne and

predict interactions between species at a com-

munity level and how the number, strength

and symmetry of these interactions inﬂuence

community tolerance to extinction (Memmott

et al., 2004;Larsenetal.,2005; Bascompte

and Jordano, 2007), especially in the context

of global environmental change (Tylianakis

et al., 2008).

4.1. Local scale: availability of critical

resources

At the individual site or local scale, man-

agement and land-use practices determine the

community composition of both pollinators

and plants, and the extent to which biotic

and abiotic factors aﬀect both groups (Kremen

et al., 2007;Fig.1). Whether clumped in

discreet patches or dispersed throughout the

landscape, the distribution of ﬂoral and nest-

ing resources largely dictates the structure and

composition of bee communities. In relation to

ﬂoral resources, including oils and resins, bees

are obligate pollen-foragers and generally both

bee and ﬂower abundance and species richness

are positively associated (Wcislo and Cane,

1996;Steﬀan-Dewenter and Tscharnke, 2001;

Potts et al., 2003; Holzschuh et al., 2007).

For example, ﬂower species richness, nectar

resource diversity and nectar energy content

explained 23% of the variation in bee com-

munity structure across six distinct Mediter-

ranean habitats (Potts et al., 2006). Ultimately,

increasing ﬂoral diversity provides a wider

array of foraging niches for diﬀerent func-

tional groups of ﬂower visitors (Fenster et al.,

2004). Agri-environment schemes that alter

the spatial and temporal distribution of ﬂoral

resources frequently have the greatest impact

on pollinator community composition. For ex-

ample, in a study of 42 wheat ﬁelds in Ger-

many, organic ﬁelds had over twice the species

richness and twenty times the percentage cover

of ﬂowering plants compared to conventional

ﬁelds, resulting in three times the species rich-

ness and almost eight times the abundance

of bees in organic versus conventional ﬁelds

(Holzschuh et al., 2007).

The availability of nesting resources also

plays a key role in structuring bee commu-

nities (Cane, 1991; Eltz et al., 2002; Potts

et al., 2005). In parallel with ﬂoral resources,

the temporal and spatial distribution of nest-

ing resources may determine the bee com-

munity composition in a given location. Eltz

et al. (2002) found that the abundance, size and

species of trees in tropical forests of Southeast

Asia inﬂuenced the density of stingless bee

nests. Similarly, in a hyperdiverse Mediter-

ranean bee assemblage, the amount of ex-

posed soil, the number of sloped surfaces and

the number of cavities available as nest sites

accounted for 26% of the variation in commu-

nity composition (Potts et al., 2005). However,

compared to ﬂoral resource use, relatively few

data exist on the nesting requirements for

many species. This may be due to the vari-

ety and often cryptic nature of bee nesting

habits, ranging from burrows in the soil, in

small pre-existing cavities in wood or stone,

to nests constructed of excreted wax in larger

cavities found in trees, rocks or rodent nests

(see Sect. 2.4). Further studies are needed to

assess whether nest sites are limiting resources

222 T.E. Murray et al.

and what factors within a bee’s ﬂight rangede-

termine nest site selection.

In addition, indiscriminate use of pesticides

and herbicides can both increase mortality

rates (Johansen, 1977) and considerably re-

duce the availability ﬂowering plants in agri-

cultural areas (Firbank et al., 2003; Morandin

and Winston, 2005). However, the intensity

of pesticide and herbicide use is often asso-

ciated with increased agricultural intensiﬁca-

tion and subsequent decline in ﬂoral and nest-

ing resources (Kremen et al., 2002; Schweiger

et al., 2005; Williams N.M. and Kremen,

2007). Therefore, separating the relative ef-

fects of each factor on bee community com-

position will improve future decisions about

eﬀective management of pollinators in agricul-

tural habitats.

4.2. Landscape scale: habitat loss,

fragmentation and land-use

Native habitat loss and fragmentation re-

sulting from human activity are two of the pri-

mary factors driving declines of native species

worldwide (Pimm et al., 2001). The synergis-

tic eﬀect of loss and fragmentation reduces

gene ﬂow and recolonisation between patches,

lowering persistence of both subpopulations

and networks of meta-populations (Hanski,

1998). Currently, there is no consensus on how

bee communities respond to habitat fragmen-

tation as empirical studies reveal a range of re-

sponses to fragment size, from positive (Cane

and Tepedino, 2001;Donaldsonetal.,2002)

to negative (Steﬀan-Dewenter et al., 2002;

Klein et al., 2003; Ricketts, 2004;Tab.II).

This variability parallels that found in other

animal groups (e.g. Vandergast and Gillespe,

2004) and indicates that responses may diﬀer

depending on life history and other species-

speciﬁc attributes, such as dispersal ability and

ﬂoral speciﬁcity (Cane and Tepedino, 2001;

Zayed et al., 2005). A further complication oc-

curs when the response of a taxon is obscured

by the composition of the surrounding matrix

of habitats and its inﬂuence on the availabil-

ity of ﬂoral and nesting resources (Eltz et al.,

2002;Caneetal.,2006; Williams N.M. and

Kremen, 2007). Therefore, our limited knowl-

edge of dispersal (see Sect. 3.1) and popula-

tion structure (see Zayed, 2009) prevent re-

liable estimation of the carrying capacity of

diﬀerent habitats and habitat mosaics, further

complicating the assessment of their conserva-

tion value.

Globally, conversion of native habitats to

agriculture is the primary form of land-use

change and the largest cause of native habi-

tat loss and fragmentation (Tilman et al.,

2001; DeFries et al., 2004). The dominance

of agro-ecosystems worldwide means that in-

creasingly bee populations exist at the in-

terface of agricultural and natural habitats

or within agricultural areas. Although mass-

ﬂowering crops can be beneﬁcial in some

cases (e.g. Westphal et al., 2003,2009), de-

clines in both bee abundance and species

richness with increasing agricultural inten-

sity have been reported from a wide va-

riety of agro-ecosystems (Steﬀen-Dewenter

and Tscharntke, 1999;Kremenetal.,2002;

Ricketts, 2004; Chacoﬀand Aizen, 2006).

Generally, agro-ecosystems that contain a mo-

saic of semi-natural habitats throughout the

landscape can maintain signiﬁcant levels of

bee diversity and abundance (Tscharntke et al.,

2005;Winfreeetal.,2007), even at re-

gional scales (Tylianakis et al., 2005). Results

from the recently completed European Union

Greenveins project demonstrated that, for tem-

perate European agro-ecosystems, once re-

gional eﬀects (i.e. country) were removed,

variables describing land-use intensity and the

spatial distribution of semi-natural habitats at

the landscape scale (4 km2) were superior to

local scale variables (0.008 km2) in explaining

bee community composition (Schweiger et al.,

2005). In a separate analyses of the same data,

Hendrickx et al. (2007)aﬃrm that land-use

intensity and proximity to semi-natural habi-

tats best explained bee species richness across

landscapes, but loss of bee species richness

was not solely the result of declines within

habitats, but was also due to increased homog-

enization of community composition between

habitats.

4.3. Plant-pollination networks

As there is a distinct lack of data

on how pollinator communities disassemble;

Conservation ecology of bees 223

Table II. Attributes of habitat fragmentation studies for native bee communities. Modiﬁed from Cane (2001).

Country Habitat Cause of

fragmentation

Parameter No. of

sites

No. of

bee taxa

Abundance of

non-Apis bees

Trend Ref.

Argentina Dry thorn

scrub

Agricultural

clearing

Fragment size 8 43 481 Species richness

declined with

decreasing fragment size.

Aizen and

Feinsinger

(1994)

Brazil Rainforest Experimental

deforestation

Fragment size 4 16 1092 Abundance decreased

with fragment size.

Powell and

Powell (1980)

Brazil Rainforest Experimental

deforestation

Fragment size 7 16 290 Abundance increased

with fragment size.

Becker et al.

(1991)

Brazil Atlantic

forest

Agricultural

clearing

Fragment size

and level of disturbance

9 21 3653 No eﬀect of

fragmentation due to

high variability of

species composition and

abundance between sites.

Tonhasca et al.

(2002)

Costa Rica Agricultural

(coﬀee)

Agricultural

clearing

Distance to

forest patch

16 40 618 Species richness

was signiﬁcantly higher

in farms within 100 m

from forest patches.

Ricketts (2004)

Costa Rica Tropical

forest

Agricultural

clearing

Fragment size, shape,

isolation and context

22 117 1537 Fragment size,

shape, isolation and

context aﬀected

community composition, but not

abundance or species richness.

Brosi et al.

(2008)

Europe (7)* Agricultural

(various)

Agricultural

clearing

Land-use intensity;

habitat diversity;

distance to

semi-natural habitat

24 115 >14529 ∗∗ Across landscapes,

bee species richness

increased with habitat

diversity and proximity

of semi-natural habitat,

but decreased with increasing

land-use intensity.

Hendrickx et al.

(2007)

Germany Agricultural

(cereals)

Agricultural

clearing

Distance to

semi-natural grassland

40†23 212 Species richness

and abundance decrease

with increasing isolation.

Steﬀan-

Dewenter

and Tscharntke

(1999)

Germany Agricultural

(cereals)

Agricultural

clearing

% semi-natural

grasslands within 3 km

15 36 1340 Abundance and diversity

of solitary bees were

correlated with %

semi-natural areas up

to 750 m, no eﬀect found

for Bombus or Apis.

Steﬀan-

Dewenter et al.

(2002)

224 T.E. Murray et al.

Table II. Continued.

Country Habitat Cause of

fragmentation

Parameter No. of

sites

No. of

bee taxa

Abundance of

non-Apis bees

Trend Ref.

Indonesia Rainforest Agricultural

clearing

Land-use

intensity

12 22 401 Solitary bee abundance,

not species richness,

increased; social bee

abundance and species

richness decreased.

Klein et al.

(2002)

Indonesia Agricultural

(coﬀee)

Agricultural

clearing

Amount of shade,

distance to forest

patch

24 29 >895‡Solitary bee diversity

increased with less shade;

social bee diversity

decreased with distance

to forest patch.

Klein et al.

(2003)

South Africa Renosterveld

shrubland

Agricultural

clearing

Fragment size 24 19 - Vegetation cover had

a greater eﬀect than

fragment size on bee

species richness and composition.

Donaldson

et al. (2002)

U.S.A. Scrub desert Urbanisation Fragment size

and age

59 62 2512 Species richness

decreases and density

increases with smaller

fragment size. Fragment

size and age had

greatest eﬀect on

ground-nesting specialists.

Cane et al.

(2006)

U.S.A. Agricultural

(sunﬂower)

Agricultural

clearing

% of semi-natural

habitat within 3 km

16 33 5732 Species richness

and abundance increased

with increasing %

semi-natural habitat.

Greenleaf

and Kremen

(2006)

U.S.A. Various Agricultural

clearing,

urbanisation

% of forest habitat

within 1.6 km

40 130 2551 Species richness and

abundance decreased with

increasing forest cover,

but increased with agriculture

and urbanisation.

Winfree et al.

(2007)

U.S.A. Agricultural

(tomato,

melon, pepper)

Agricultural

clearing

% of forest habitat

within 0.5–3 km

29 54 4592 No eﬀect of % of

forest habitat and

species richness on crops.

Winfree et al.

(2008)

* Belgium, Czech Republic, Estonia, France, Germany, Netherlands, Switzerland.

** The number of non-Apis bees was not indicated; therefore bees of 8.5–12 mm in length identiﬁed by Schweiger et al. (2005) were excluded.

†40 habitat ‘islands’ consisting of 4 mustard and 4 radish plants.

‡The number of non-Apis eusocial bees was not indicated.

Conservation ecology of bees 225

predictions arising from the recent prolifera-

tion of simulation studies based on networks

of plant-pollinator interactions may be a valu-

able source of testable hypotheses (reviewed

in Bascompte and Jordano, 2007). At the com-

munity level, interactions between species are

the “glue of biodiversity” (Thompson, 2005)

and mutualistic networks provide well-deﬁned

and predictable patterns of interdependence

between species. Speciﬁcally, plant-pollinator

networks can be described by two proper-

ties: they are very heterogeneous, with a few

species much more connected than by chance;

and they are highly nested, whereby special-

ists interact with distinct subsets of the species

interacting with generalists (Bascompte and

Jordano, 2007). As a result of this asymme-

try in specialisation, plant-pollinator networks

are reciprocally redundant and predicted to be

relatively tolerant to extinction, as only the mi-

nority of plant species are likely to lose all

their pollinator species as pollinator communi-

ties disassemble (Memmott et al., 2004). No-

tably, community resilience in plant-pollinator

networks is predicted to be enhanced by in-

creased species diversity and the number of

species interactions (Okuyama and Holland,

2008). Furthermore, understanding the nested

structure of plant-pollinator networks can ex-

plain why the reproductiveoutput of both spe-

cialist and generalist plant species is similarly

aﬀected by habitat fragmentation (Ashworth

et al., 2004); how invasive species rapidly be-

come integrated into existing plant-pollinator

networks (Memmott and Waser, 2002;see

Stout and Morales, 2009); the rate of com-

munity disassembly with habitat loss (Fortuna

and Bascompte, 2006); and how the structure

of plant-pollinator networks remain largely

stable, despite considerable temporal variation

in the number, strength and symmetry of plant-

pollinator interactions (Petanidou et al., 2008).

Currently, the only empirical study of bee

community disassembly and its eﬀect on pol-

lination is that of Larsen et al. (2005). Us-

ing wild bee data from Kremen et al. (2002),

the study found that the relationship between

species richness and pollination is approxi-

mately concave up, indicating that the ﬁrst

species extinction could lead to rapid reduc-

tion in pollination. Two main factors corre-

lated with the loss of pollination function

in bee communities: the non-random loss of

species and the absence of strong density de-

pendence following species loss. Bee species

did not disappear randomly from sites; in-

stead species were lost in an ordered fash-

ion, with the largest, more eﬃcient pollinators

more likely to experience local extinction. Ac-

cordingly, 86% of sites experienced a greater

loss of pollination function than would be ex-

pected by random species loss. This study af-

ﬁrms the sentiment expressed by Memmott

et al. (2004), that plant-pollinator networks

may be tolerant, but not immune, to extinction.

Clearly, there is a dire need for empirical data

regarding critical thresholds of species extinc-

tion and collapse of plant-pollination networks

(Fortuna and Bascompte, 2006).

4.4. Climate change

Thomas et al. (2004) predicted that by 2050

climate change, even in the absence of other

drivers of extinction, would doom 15–37% of

all species to eventual extinction. The predic-

tion is based on the application of an estab-

lished ecological pattern, the species-area re-

lationship, to data on the current distributions

and climatic envelopes of 1103 species. Al-

though their approach has been heavily crit-

icised (e.g. Lewis, 2006), the study did raise

critical questions regarding the response of

species to climate change, such as: how many

species have distributions primarily governed

by climate; and to what extent do current dis-

tributions truly reﬂect limits of climate toler-

ances?

Although the uncertainty in their models

preclude any ﬁrm generalisation, Dormann

et al. (2008) found that climate accounted

for 64.1% of the variation in the pattern of

species richness at the landscape scale for wild

bees in temperate Europe, compared to land-

scape structure (27.7%), soil (7.1%) and land-

use intensity (1.2%). Furthermore, in a re-

cent study simulating phenological shifts with

a real community of plants and pollinators,

Memmott et al. (2007) estimate that, over the

past 100 years, global warming has advanced

the ﬁrst ﬂowering date of plants and the sea-

sonal ﬂight activity of some pollinating insects

226 T.E. Murray et al.

(mostly butterﬂies) by, on average, 4 days per

degree C in temperate zones, resulting in be-

tween 17–50% of all pollinator species experi-

encing a disruption in food supply.

Broad trends regarding the impact of cli-

mate change on plant-pollinator networks are

emerging (Tylianakis et al., 2008), but as

any alteration in climate will be superim-

posed upon other, multiple interacting drivers

of global change, signiﬁcant challenges in pre-

dicting future responses remain.

5. HOW ECOLOGY INFORMS BEE

CONSERVATION STRATEGIES

Knowledge of the basic ecology of bees

is essential for underpinning the development

and implementation of conservation strategies

(Byrne and Fitzpatrick, 2009). Understanding

the factors that regulate bee populations and

communities, and the sensitivity of bee traits

to these factors, allows speciﬁc management

options to be identiﬁed for individual species

and entire assemblages. A ﬁrst step is to iden-

tify the resource requirements of the target

bee taxa to ensure that the appropriate quan-

tity and quality of these are provided spa-

tially and temporally. These include both for-

age (pollen, nectar) and nesting (substrates and

construction materials) resources and the pro-

vision of suitable abiotic conditions (microcli-

mate and local topography). The distribution

of resources must fall within the forage and/or

dispersal ranges of the bee species considered,

as diﬀerent parts of the landscape often pro-

vide complementary resources, leading to the

concept of partial habitats (Westrich, 1989).

Assessing the resource distributions within the

landscape may reveal that a single limiting

resource is missing which can then be sup-

plemented through management practices (e.g.

provision of ﬂower-rich ﬁeld margins) to sup-

port bee conservation (see below).

A supply of optimal resources is not enough

on its own; it is also important to understand

how bees respond to landscape-scale changes

in their environment. The geographic scale

over which negative pressures aﬀect bees, cou-

pled with individual species’ ability to dis-

perse throughout the landscape, will determine

whether bees can avoid irreversible popula-

tion decline. For instance, habitat loss and

fragmentation can result in resource deple-

tion, and thresholds for foraging and nest-

ing resources will determine the carrying ca-

pacity of remaining habitats. Habitat area is

known to impact on bee community compo-

sition (Steﬀan-Dewenter, 2003) and minimum

patch sizes are important for the persistence of

these communities (Hanski and Pöyry, 2006;

Kremen et al., 2004). The conﬁguration of

the landscape, and how bees are able to dis-

perse through the landscape, will determine

whether spatially fragmented resources are

available (Steﬀan-Dewenter and Tscharntke,

2002; Tscharntke and Brandl, 2004). The pro-

tection of key habitats and connectivity within

the landscape (Gilbert et al., 1998;Tewksbury

et al., 2002) therefore represents an important

tool for bee conservation (see below). Other

pressures such as grazing (Vulliamy et al.,

2006) and ﬁre (Potts et al., 2003) modulate the

availability of resources in the landscape and

managing grazing regimes and burning prac-

tices can fundamentally alter habitat quality

for bees. Daily activity patterns and seasonal

phenology may also determinethe level of risk

of bee exposure to pesticides and other agro-

chemicals (Brittain et al., unpubl. data). Al-

tering the timing of pesticide application from

midday to early morning or late evening can

ensure that the window of maximum toxicity

does not overlap with the times when bees are

foraging on crops (Kevan, 1975). Similarly,

modifying the types and application regime

of herbicides can facilitate the maintenance of

diverse ﬂower communities within intensive

agro-ecosystems (Westbury et al., 2008).

There are two broad and complementary

categories of bee conservation approaches,

both of which can be more eﬀective when

informed by bee ecology: species-targeted

approaches and habitat-targeted approaches.

Species-targeted approaches focus on individ-

ual species, or broader taxa, and often pro-

vide some kind of legal protection which aims

to prevent activities causing direct mortal-

ity to individuals (including collection) (see

Byrne and Fitzpatrick, 2009). One example

is the Biodiversity Action Plan (BAP) in the

UK which includes 17 species of bees (www.

ukbap.org.uk). BAP is the UK Government’s

Conservation ecology of bees 227

response to the Convention on Biological

Diversity and is a detailed plan for the pro-

tection of the UK’s biological resources. Each

UK BAP priority species action plan has an

overview of the status of a species, infor-

mation on the threats facing it, actions to

achieve the action plan, and broad policies

developed to conserve it. The core of the

bee BAPs is based on detailed autecology

of the target species or, if this is not avail-

able, then this is an initial priority step in de-

veloping a conservation plan. Another form

of species protection is the IUCN Red Lists

which include bees in several countries (e.g.

Finland, Germany, Hungary, Ireland, Nether-

lands, Slovenia, Sweden, Switzerland and UK;

see Byrne and Fitzpatrick, 2009). These prior-

ity species lists can clearly direct prioritization

of conservation actions at national levels, but

action should not be exclusive to listed species

(Fitzpatrick et al., 2007).

Complementing the species-targeted ac-

tions are habitat-based approaches which fo-

cus on conserving and restoring important bee

habitats. In some cases these will be specif-

ically for bees, but in many cases they are

aimed at enhancing wider biodiversity, which

may also include bees. Many national pro-

tected areas and networks are natural or semi-

natural areas designated on the basis of priority

habitats (e.g. Special Areas of Conservation

in Europe, EC Habitats Directive 92/43/EEC)

which in many terrestrial systems often in-

clude diverse ﬂoral resources which can sup-

port bees. In addition to protected areas, more

ubiquitous habitats can be managed for con-

servation purposes. The UK BAP, for in-

stance, includes a number of Habitat Action

Plans which have detailed actions and targets

for conserving these habitats; important bee

habitats included are calcareous grasslands,

hedgerows, and heathlands. In addition to nat-

ural areas, agro-ecosystems can be eﬀectively

managed for bees by exploiting the known

ecological requirements of bee taxa. Agri-

environment schemes aim to enhance general

farmland biodiversity and in the UK include

several bee-speciﬁc options. The English En-

try Level Stewardship (Defra, 2005) ﬁnan-

cially supports farmers to manage their farms

in a way which enhances the resources avail-

able for bees, for instance option EF4 involves

sowing ﬁelds with pollen and nectar ﬂower

mixes. The options developed in this agri-

environment scheme, and others in Europe and

elsewhere, were mostly founded upon rigorous

scientiﬁc work on bee ecology to identify the

speciﬁc ﬂoral resource requirements for bees

in both arable (Meek et al., 2002) and inten-

sive grassland systems (Potts et al., in press).

6. CONCLUSIONS

Combinations of protected area networks

and bee-friendly habitats within agricul-

ture will become increasingly important for

bee conservation as the impacts of global

environmental change manifest themselves

(Tylianakis et al., 2008). Currently, high qual-

ity habitats for bees may become unavailable

as bee climatic envelopes shift and/or habitats

become degraded. By taking a wider landscape

approach and linking up fragments of (semi-)

natural landscape with linear features, such as

hedgerows and ﬁeld margins, it will be possi-

ble to increase landscape connectivity and al-

low bees to forage and disperse to more suit-

able areas under global change (Gilbert et al.,

1998; Tewksbury et al., 2002). Indeed, under-

standing the traits inﬂuencing the sensitivity of

bees to climate change is essential if we are to

manage our bee communities in the future.

ACKNOWLEDGEMENTS

The authors would like to thank L. Nilsson, T.

Eltz and R. Paxton for insightful comments that im-

proved the manuscript, and the editors for the invi-

tation to contribute to this special issue.

Écologie de la conservation des abeilles : popula-

tions, espèces et communautés.

Apoidea /biodiversité /protection /relation

plante insecte /pollinisateur

Zusammenfassung –Ökologische Aspekte des

Schutzes von Bienen: Populationen, Arten, Art-

gemeinschaften. Die meisten der bereits ausge-

storbenen oder vom Aussterben bedrohten Arten

sind Insekten. Nichtsdestotrotz ist der Schutz von

Insekten bisher weitgehend vernachlässigt worden.

Die Befürchtungen jedoch, dass Pﬂanzen und ihre

228 T.E. Murray et al.

Bestäuber Rückgänge verzeichnen und dementspre-

chend Ökosystemfunktionen negativ beeinﬂussen

können, hat letztendlich die lokalen und globalen

Bedrohungen der Bienendiversität ins Schlaglicht

gerückt. Anzeichen für den Rückgang von Bienen

häufen sich sowohl in taxonomischer als auch in

geographischer Hinsicht. Wir geben hier eine Über-

sicht über die Rolle ökologischer Faktoren im Bie-

nenschutz, wobei wir besonders die Frage der Ar-

ten, Populationen und Artgemeinschaften beleuch-

ten.

Erfolreicher Artenschutz erfordert zunächst ein

grundlegendes Verständnis von zwischenartlichen

Wechselwirkungen und von autökologischen Merk-

malen (Abb. 1und Tab. I). Das Aussterben von

Bienenarten ist in vielen Fällen nicht dokumen-

tiert und demzufolge sind vergleichende Analysen

wichtig, um autökologische Faktoren erkennen zu

können, die mit der Anfälligkeit zum Artenrück-

gang verknüpft sein können. Bienenpopulationen

und Bienengemeinschaften zeichnen sich durch er-

hebliche raumzeitliche Schwankungen hinsichtlich

ihrer Häuﬁgkeit und Zusammensetzung aus, so dass

die Variabilität dieser ökologischen Daten dazu füh-

ren kann, dass lange Beobachtungszeiträme not-

wendig sind, um faktische Rückgange sichtbar ma-

chen zu können. Im Idealfall würde die Bestim-

mung kritischer Werte der Populationsgrössen und

des Populationswachstums experimentelle Ansätze

erfordern. In der Praxis werden aufgrund der lo-

gistischen Anforderungen, dem Problem fehlender

Wiederholungen und den räumlichen Grössenord-

nungen jedoch meist Modellansätze bevorzugt, um

Populationsrückgänge und Antworten auf regeln-

de Massnahmen sichtbar zu machen. Wir diskutie-

ren hier die Erfassung von drei Schlüsselparame-

tern für die Abschätzung von Populationsgrössen

und Wachstumsraten: Ausbreitungsrate, Paarungs-

system, sowie Prädatoren, Parasiten und Pathogene.

Die Antwort von Einzeltieren, Populationen und

Artgemeinschaften von Bienen auf anthropogen be-

dingte Umweltveränderungen ist primär bedingt

durch die räumliche und zeitliche Verteilung von

ﬂoralen sowie Nist- und Überwinterungsresourcen,

die jeweils in Beziehung stehen zum Sammelver-

halten und der Ausbreitungsfähigkeit der Bienen.

Obwohl die primären Faktoren, die die Verteilung

dieser Resourcen bestimmen, bekannt sind, näm-

lich Habitatverlust, bzw. Fragmentierung, ergeben

empirische Daten bezüglich der Antwort der Bie-

nengemeinschaften auf diese Faktoren kein einheit-

liches Bild (Tab. II). Netzwerktheoretische Ansät-

zen in Untersuchungen zur Architektur von Pﬂan-

zen/Bestäuber Netzwerken lassen jetzt Fortschrit-

te erkennen und haben unsere Fähigkeit verbes-

sert, Interaktionen zwischen Arten auf der Ebe-

ne von Gemeinschaften deﬁnieren und vorherse-

hen zu können. Mit Blick auf die globalen Um-

weltveränderungen wird die akkurate Abschätzung

der Zahl, Stärke, Symmetrie und Variabilität die-

ser Interaktionen und ihr Einﬂuss auf die Toleranz

von Bienengemeinschaften gegen das Aussterben

zunehmend an Bedeutung gewinnen. Da gegenwär-

tige Artenschutzmassnahmen im wesentlichen den

Schutz von einzelnen Arten oder von Habitaten im

Blick haben, werden ökologische Daten entschei-

dend sein für die Integration dieser beiden Manage-

mentstrategien auf einer breiteren, landschaftsori-

entierten Ebene von dynamischen und untereinan-

der verbundenden Habitaten, die dann dazu beitra-

gen können, dass Bienenschutz im Kontext globaler

Umweltveränderungen möglich wird.

Artenschutz /Biodiversität /Population /Arten-

gemeinschaft /Pﬂanzen-Bestäuber

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Significance of honeybee pollination in increasing seed yield of Trifolium alexandrinum (Fabales: Fabaceae) and its impact on economic sustainability of smallholder farmers

Article

Full-text available

Oct 2024

A major limitation to producing high seed yields in berseem clover (Trifolium alexandrinum L.) is failure to set seed, predominantly due to lack of pollination. Despite the importance of berseem clover as a leading forage legume, the contribution of pollinators to seed set is scarce. In Pakistan, the honeybee population is declining mainly because of the extensive use of neonicotinoid pesticides and habitat fragmentation. This, combined with the region’s harsh environment and the use of inferior, locally bred genotypes, has resulted in low seed yields. Insufficient seed availability leads to limited forage supply, resulting in poor livestock nutrition, which subsequently impacts livestock health and productivity, and reduces farmers’ income. The present study estimated the seed production of 3 berseem clover genotypes resulting from honeybees [Apis mellifera L. (Hymenoptera: Apidae)] pollination in 2 growing seasons (2012–2014) in the central Punjab region of Pakistan. Experiments had 2 pollination treatments (open pollination and honeybee inclusion) and 3 seed genotypes, viz. farmer own-saved, market, and the improved variety cultivars. For both growing seasons, honeybee pollination resulted in significant increases in seed yields ranging from 35% to 67%, regardless of seed genotype. With the exception of the number of seed heads/m2, all seed yield parameters also increased significantly in response to honeybee inclusion. The combination of improved variety and honeybee inclusion resulted in the production of a maximum number of seeds per head (45.3), 1,000-seed weight (3.7 g), and estimated seed yield (375.5 kg/ha). In addition, the increase in estimated net income of seed ranged from PKR 82,485 Rs/ha (US

844/ha) to PKR 168,975 Rs/ha (US

1728/ha) with the use of honeybees as an insect pollinator across all the seed genotypes. Honeybee pollination has broader implications for mixed farming systems by playing a key role in preserving biodiversity and promoting sustainable agriculture. It also enhances the quality and quantity of berseem crops by increasing the production of high-quality seeds and forage leading to improved livestock productivity and family food security which strengthens the economic resilience of rural communities.

Biology and Behaviour of European Wild Bees

Chapter

Feb 2025

European first documented studies on wild bee biology date back to the ancient Greek philosophers, and since then we have accumulated—mainly in the last century—a great amount of information on the behavioural ecology of these insects. European wild bees, which span six different families (Andrenidae, Apidae, Colletidae, Halictidae, Megachilidae, Melittidae) for roughly 2000 species, show an impressive diversity of behavioural and ecological traits. Here, we present an organized review of European wild bees about their nesting habits, social behaviour, mating strategies, food resource use, and diversity of natural enemies. We highlighted relevant biological traits and provided extensive specific examples that can be used as an easy-to-explore guide. European bee fauna encompasses ground-nesting and aerial-nesting species, solitary and eusocial species, oligolectic and polylectic species, and species with diverse mating strategies. There is considerable variability within families and even within genera. Consequently, a wide range of morphological and physiological adaptations have evolved within this group. Additionally, the natural enemies of European wild bees include a taxonomically diverse array of ecto- and endo-parasitoids, parasites, kleptoparasites, and predators. We recognize that there is still an important lack of knowledge on the behavioural ecology of many species, with negative consequences for the assessment of their vulnerability to environmental changes and adequate conservation planning.

A survey of native bees (Hymenoptera Anthophila) at lakeplain prairie and prairie fen habitats in Michigan

Article

Full-text available

Feb 2025

Michigan’s lakeplain prairie and prairie fen natural communities contain refugia for many at-risk species of insects, including species that are listed at the federal and state level. Wild bees are a group of insects crucial for maintaining robust plant-pollinator communities. Numerous species of bees are presumed to be in decline. However, baseline community surveys are lacking and needed to document the status of species occupying these natural communities. In 2021, Michigan Natural Features Inventory completed wild bee surveys in lakeplain prairie (lakeplain wet-mesic prairie and lakeplain wet prairie) and prairie fens in Michigan using a combination of aerial netting and bowl trapping. A total of 1,118 wild bees, representing 104 unique species or morphospecies, were collected during these surveys, including new state records for Dufourea marginata (Cresson, 1878) and Sphecodes nigricorpus Mitchell, 1956 (Hymenoptera: Anthophila). The baseline inventory of wild bees in 2021 provides valuable information on species presence at these locations and suggests that they may act as refuges for rare species of native bees in the state. Continued management of lakeplain prairie and prairie fen natural communities should take into consideration wild bee communities and strive to ensure populations maintain stable numbers.

Mitochondrial DNA: a promising tool for characterising the population of the Tiúba stingless bee, Melipona fasciculata (Apidae, Meliponini)

Article

Full-text available

Jan 2024

The Melipona fasciculata popularly known as Tiúba, is a specie of stingless bee that is distributed in the north of Brazil, over-represented in Maranhão State. This bee is of great importance to stingless bees (SLB) beekeepers, as it produces a large quantity of honey with an excellent taste. The genetic diversity of the Tiúba populations was examined with molecular approach using the mitochondrial DNA (mtDNA) marker. A total of 30 samples from cities in Maranhão State were analysed for the mtDNA intergenic region located between the cytochrome c oxidase I (COI). The molecular analyses identified 8 haplotypes, 3 of which are shared between locations, where the commercialization of beehives is very common and the commercialization of beehives is very common. The populations of Imperatriz and São Bento have the highest diversity indices, and the neutrality tests showed that the populations might be expansion. The fixation index of the study populations showed a high differentiation rate of 0.6218. These Tiúba populations exhibit a high level of genetic structuring, as well as potentially being in a population expansion phase.

A Review on the Sublethal Effects of Pure and Formulated Glyphosate on Bees, with a Focus on Social Bee Species

Article

Dec 2024

Glyphosate, one of the most widely used herbicides globally, has been extensively applied in agriculture due to its efficacy in weed control. However, recent studies have raised concerns about its sublethal effects on non-target organisms, particularly social bee species such as honeybees (Apis mellifera), bumblebees (Bombus spp.), and stingless bees (e.g., Melipona, Trigona). While glyphosate's primary mechanism targets the shikimate pathway, which is absent in animals, emerging evidence suggests it can indirectly impact bees by altering their gut microbiota, immune responses, and behavior. Research shows that even at sublethal doses, glyphosate can impair navigation, learning, and foraging efficiency, leading to reduced colony growth and survival rates. Field and laboratory studies indicate that the impact is exacerbated when bees are exposed to formulated products containing surfactants, which increase glyphosate’s toxicity. Furthermore, the disruption of social behaviors within colonies, such as communication through the waggle dance in honeybees, has profound implications for hive health and productivity. Despite growing evidence, there remain significant gaps in our understanding of glyphosate’s long-term and chronic effects, especially across diverse ecosystems and bee species. Current research is limited by a lack of longitudinal field studies that assess the cumulative impact of low-dose exposure over multiple generations. Most studies have focused on honeybees, with less attention given to wild and native bee populations, which may respond differently to glyphosate. To address these challenges, future research must prioritize mechanistic studies, explore eco-friendly alternatives to glyphosate, and implement integrated pest management strategies to reduce agrochemical dependence. Collaboration among scientists, policymakers, and stakeholders is critical to developing evidence-based regulations that protect pollinator health. Given the essential role bees play in global food security through pollination, protecting these vital species from the sublethal effects of glyphosate is not only an ecological imperative but also a socioeconomic necessity. Immediate actions in research, policy reform, and sustainable agricultural practices are needed to mitigate the risks posed by glyphosate and safeguard the future of pollinators.

Moths versus Bees: Contrasts in Habitat Preferences Across Barrens of the Northeastern USA

Article

Full-text available

Nov 2024

Bees and moths are globally important pollinators. Xeric barrens in the largely mesic northeastern USA support high levels of pollinator diversity, including rare bees and moths. We investigated the response of bee vs. moth communities to abiotic and vegetation drivers in barrens across the region. We sampled local environmental conditions, vegetation, bees, and moths for 2–4 years in 19 preserves. Employing random forest analysis, we tested the role of 29 abiotic and vegetation predictors of bee vs. moth abundance, species richness, Shannon‐Wiener Index, evenness, and species composition. Variables related to climate, canopy cover, and soils were the most important predictors of abundance, diversity, and species composition for both bees and moths. Vegetation variables, such as species richness of shrubs and hostplants, were also important for bees. The direction of these relationships contrasted sharply between bees and moths: bees were more abundant and species rich in more open, sandy sites and moths the opposite. Habitat preferences for a subset of moth xeric specialists were much more similar to bees than to other moths, with a preference for open, sandy conditions. Contrasts between bees and moths in habitat preferences likely stemmed from differences in their life histories: bees rely on flowers for feeding and porous substrates for nesting, whereas most moth adults feed on flowers, but many moth caterpillars use woody plants as hosts. In sharp contrast to the results for abundance and richness, bees and moths responded similarly for the Shannon‐Wiener Index, which raises important general questions about the conservation value of these two metrics. Our results suggest that, because of differences in habitat preferences among pollinators, barrens management for both open and more closed habitats is likely to promote the highest abundance and diversity of local bee and moth pollinator communities jointly.

Self-supervised Component Segmentation To Improve Object Detection and Classification For Bumblebee Identification

Preprint

Full-text available

Mar 2025

The performance of computer vision models for object detection and classification is heavily influenced by the number of classes and quality of input images, particularly in biological applications such as species-level identification of bumblebees. Bee identification is time-consuming, costly, and requires specialized taxonomic training. Different deep learning based computer vision models have been proven to overcome this methodological bottleneck through automated identification of bee species from captured images. However, accurate identification of bee species in images containing multiple objects of various classes poses significant challenges due to ambiguity, poor image quality, and noisy backgrounds. Existing pipelines (baselines) primarily rely on object detection to crop bees from images and classify the species for each cropped instance. This approach is limited by the inclusion of noisy backgrounds, low resolution, and poor image quality. To address these limitations, we propose an enhanced pipeline that integrates object detection with segmentation to generate body masks for bees and remove background noise. This process is complemented by a classification model that identifies the top k species for each masked image. The proposed methodology significantly improves both detection and classification performance in most cases, demonstrating its potential to advance automated identification of bee species in complex image datasets. For the cases where the baselines performed much better, we investigated using a state-of-the-art explainable AI model (Grad-CAM) to explain the reason.

ARI KOVANLARININ ÇEVRESEL VE AKUSTİK VERİLERE DAYALI DURUM ANALİZİ: NORMAL VE ÖZEL KOŞULLARIN KARŞILAŞTIRILMASI

Article

Mar 2025

Arı kolonilerinin sağlık ve faaliyetlerine ilişkin sürekli ve doğru bilgi elde etmek, arı popülasyonlarının korunması ve sürdürülebilir tarım uygulamalarının desteklenmesi için hayati öneme sahiptir. Çalışmamız, çevresel ve akustik sensör verilerini bütünleştirerek arı kolonilerinin durumunu etkin şekilde izlemeyi hedeflemektedir. Özellikle çalışmada CO2 konsantrasyonu, TVOC konsantrasyonu, sıcaklık ve nem gibi çevresel parametrelerin yanı sıra akustik verilerin analizi de yer almaktadır. Kullanılan yöntem, çeşitli çevresel sensörlerden elde edilen verilerin zaman serisi analizi ve ses dosyalarından spektral özelliklerin çıkarılmasını içermektedir. Analiz sürecinde, normal ve özel koşulları ayırt etmek için aykırı değer analizi uygulanmıştır. Sonuçlarımız, çevresel parametrelerde zamanla önemli değişiklikler olduğunu göstermektedir. Özellikle, özel koşullarda CO2 ve TVOC konsantrasyonlarında önemli artışlar gözlemlenmiştir (CO2: 1200 ppm'den 1450 ppm'ye, TVOC: 0 ppb'den 450 ppb'ye). Ayrıca, ses analizi, iki koşul arasında belirgin spektral özellik farkları göstermiştir. Sonuç olarak, araştırmamız, çevresel ve akustik sensör verilerinin birleşiminin arı kolonilerinin durumunu kapsamlı ve doğru izlememize olanak sağladığını doğrulamaktadır. Bulgular, bu tür bir yaklaşımın izleme uygulamaları için değerli bir araç olabileceğini önermektedir.

The buzz around flower shapes: how Asteraceae corolla dimensions influence pollinator interest in urban green areas

Article

Feb 2025

Adequate understanding of plant-pollinator dynamics should be included in any planning of urban green areas so that pollinator biodiversity is supported. Among the factors contributing to plant-pollinator dynamics, this preliminary study specifically examined the impact of corolla tube dimensions on the frequency of insect visitations for foraging. This was accomplished by measuring the corolla dimensions of different Asteraceae species within Ridley Park, UK, and conducting 36 days of non-consecutive observational surveys. Insect identity and visitation frequency to forage on the focal Asteraceae species were recorded. Insect visitors were categorised into three broad taxonomic groups according to comparative proboscis lengths: bumblebees (longer), flies (shorter), and other insects (various; control). The results revealed that Diptera (flies) accounted for the majority of visits, with significant associations found between fly visitation rates and shorter corolla tube lengths/widths. For bumblebees, although trends suggested a potential association between increased visitation rates and larger corolla sizes, no statistically significant relationships were observed for either ray or disk corolla tube lengths. The findings indicate that corolla morphology may play a role in shaping insect foraging in urban green areas. By increasing plant diversity, particularly by incorporating species with a range of corolla dimensions, it may be possible to support a broader spectrum of pollinators. These insights can assist urban park authorities in selecting plant species that promote pollinator biodiversity, contributing to healthier and more resilient urban ecosystems.

Bee Diversity and Abundance During Peach Bloom in South Carolina, United States

Article

Oct 2024

Peach ( Prunus persica [L.] Batsch) is an important speciality fruit crop in the United States. Peach is self‐compatible, but bee pollination enhances fruit sets and diverse populations improve pollination efficiency. However, the bee diversity and abundance in peach orchards in South Carolina are unknown. To understand this, we sampled bees during peach tree bloom at two locations in South Carolina—the Clemson University Musser Fruit Research Center (MFRC) and a peach farm in Ridge Spring, South Carolina. Overall, a total of 651 bees were collected from peach orchards, of which Bombus (37%) and Apis (32%) were the most dominant genera, followed by Eucera (14%), Andrena (8%) and Habropoda (5%). Diversity indices indicate higher species richness and diversity at the Ridge Spring farm than at MFRC. Dominant species at the MFRC were Apis mellifera (36.77%), Bombus bimaculatus ( 29.1%), B. griseocolis (12%) and Eucera hamata (8%). In contrast, the Ridge Spring farm was dominated by A. mellifera (24.17%), Habropoda laboriosa (12%), Andrena barbara (12%), E. atriventris (11.72%) and B. bimaculatus (11.35%). In comparing the effectiveness of sampling methods, blue vane traps (BVTs) captured more bees than aerial sweep netting. Furthermore, BVTs predominantly captured larger‐sized bees, while smaller‐sized bees were more frequently collected using sweep netting. Throughout peach bloom, differences in bee abundance were observed over time as well. Our study sheds light on the bee diversity and abundance in South Carolina peach orchards, revealing variations between locations. This knowledge of bee diversity and abundance will provide baseline information on bee communities in peach orchards and will help develop suitable pollinator conservation programs.

The Bees of the World

Book

Jan 2007

Bob Surname

Life histories and parasite pressure across the major groups of social insects.

Chapter

Sep 2005

These proceedings contain 18 papers that discuss topics on speciation and adaptation; life history, evolution, phenotypic plasticity and genetics; sexual selection and reproductive biology; insect-plant interactions; insect-natural enemy interactions; and social insects. A series of empirical case studies in evolutionary ecology using insects as model systems are also presented.

SCALE-DEPENDENT EFFECTS OF LANDSCAPE CONTEXT ON THREE POLLINATOR GUILDS

Article

May 2002

Introduction to Conservation Genetics

Book

Mar 2002

The biological diversity of our planet is being depleted due to the direct and indirect consequences of human activity. As the size of animal and plant populations decrease, loss of genetic diversity reduces their ability to adapt to changes in the environment, with inbreeding depression an inevitable consequence for many species. This textbook provides a clear and comprehensive introduction to the importance of genetic studies in conservation. The text is presented in an easy-to-follow format with main points and terms clearly highlighted. Each chapter concludes with a concise summary, which, together with worked examples and problems and answers, emphasise the key principles covered. Text boxes containing interesting case studies and other additional information enrich the content throughout, and over 100 beautiful pen and ink portraits of endangered species help bring the material to life.

The Geographic Mosaic of Coevolution

Book

Jan 2005

John N. Thompson

Habitat requirements of central European bees and the problems of partial habitats

Article

Jan 1996

Paul Westrich

Host-plant coevolution and the diversity of bees in relation to the flora of North America

Article

Jan 1979

A.R. Moldenke

Bumblebees: Behaviour, Ecology, and Conservation

Book

Jan 2010

Dave Goulson

Bumblebees are familiar and charismatic insects, occurring throughout much of the world. They are increasingly being used as a model organism for studying a wide range of ecological and behavioural concepts, such as social organization, optimal foraging theories, host-parasite interactions, and pollination. Recently they have become a focus for conservationists due to mounting evidence of range coBIOL15ANIB and catastrophic extinctions with some species disappearing from entire continents (e.g. in North America). Only by improving our understanding of their ecology can we devise sensible plans to conserve them. The role of bumblebees as invasive species (e.g. Bombus terrestris in Japan) has also become topical with the growing trade in commercial bumblebee nests for tomato pollination leading to establishment of non-native bumblebees in a number of countries. Since the publication of the first edition of the book, there have been hundreds of research papers published on bumblebees. There is clearly a continuing need for an affordable, well-illustrated, and appealing text that makes accessible all of the major advances in understanding of the behaviour and ecology of bumblebees that have been made in the last 30 years.

Phenology and Trap Selection of Three Species of Hylaeus (Hymenoptera: Colletidae) in Upper Michigan

Article

Jan 1994

Virginia L Scott

The biology and social behaviour of Evylaeus malachurus (K.) (Hymenoptera; Halictidae) in different climatic regions of Europe

Article

Jan 1992

G. Knerer

Overwintered gynes establish haplometrotic nests in spring. A single brood of workers is produced in the northern region; two broods are common in C Europe and S Spain; up to three broods occur in some parts of the Mediterranean area. Nests in the first phase contain 3-12 cells, arranged in a comb and surrounded by a cavity. Nests of later phases are deeper with increasing numbers of cells. The caste system is based on conspicuous morphometric and physiological differences. Gynes are reared on big pollen balls, and required a diapause before nest foundation in spring. Queens lay virtually all diploid eggs for worker and gyne production. Workers are raised on small provisions, lack a diapause, but commence activities immediately after emergence. Their main tasks include foraging, defence and construction. Males acount for only 2% of the first brood, but their numbers increase throughout the summer. Populations of nests in the last phase can range from a handful to close to 90 bees. Productivity is commensurate, exending from a low of half a dozen gynes to more than several hundred sexuals. Fecundity of this magnitude explains the colonising efficacy of the species, both with regards to newly created nest sites and old aggregations recently devastated by the depredations of brood parasites. -from Author