Bringing population ecology back to wild bees
Nicholas N. Dorian1*(nicholas.dorian@tufts.edu)
Elizabeth E. Crone1 (elizabeth.crone@tufts.edu)
1Tufts University, Department of Biology, 200 College
Avenue, Medford, Massachusetts United
*Corresponding author: Nicholas N. Dorian
Phone: +1 (203) 561-0280
Type of article: Viewpoint
Running title: Population ecology of wild bees
Keywords: theory, non-lethal studies, pollinators,
conservation, Hymenoptera
Statement of authorship: NND and EEC jointly conceived of these
ideas and wrote the manuscript.
Data accessibility: All literature survey data will be uploaded
to a public repository upon acceptance.
Abstract word count: 138
Main text word count (excluding abstract, acknowledgements,
references, table and figure legends): 1995
Number of references: 37
Number of figures: 2
Number of tables: 0
Number of text boxes: 0
Abstract: In recent years, ecologists have focused on
describing patterns of change in wild bee communities, but we know
little about the population-level mechanisms driving those changes. We
believe this emphasis on community-level patterns stems from two
misconceptions: the perceptions that population-level studies are too
conceptually narrow to provide rigorous inference, and that studying
bees throughout their life cycles is prohibitively challenging without
pinned specimens. Here, we combat these ideas. First, when
population-level studies are couched in ecological theory, they can also
have a broad scope of inference. And second, studies of wild bees
throughout their life cycles are possible because dozens of species can
be identified to species in the field. More generally, we emphasize the
need to link data-rich pattern-oriented approaches in ecology with an
understanding of the basic biology and mechanisms that generate those
patterns.
Problem Statement: In recent years, it has become popular for
ecologists to analyze patterns of biodiversity in relation to ongoing
climate and land use change. An implicit assumption underlying these
studies is that the places and times at which a species is most
conspicuous are the most important for its persistence. However,
ecologists have long known that this relationship is not necessarily
true (e.g. Crouse, Crowder, & Caswell, 1987). If our goals are to
predict future dynamics, mitigate population declines, or manage
invasive species, we also need to understand the population-level
processes behind large-scale patterns.
Context: The mismatch between our knowledge of large-scale
patterns and population-level processes is especially evident in
research about wild bees. In North America, there are nearly 4000
species of wild bees. Over the past 20 years, in response to concerns
over declining wild bee populations (Potts et al. 2010),
ecologists have generated enormous volumes of data at the community
level. To characterize this trend, we read all papers about wild bees
from 2020 published in 19 representative ecology journals (95 articles;
Table S1). More than half of these papers (51/95 articles) described bee
communities in relation to an environmental factor (Figure S1). Studies
typically collected data via lethal sampling of adult bees during
foraging and characterized community composition by identifying pinned
specimens.
These community-level studies have taught us many things about wild
bees: where and when adults occur (Carril et al. 2018), how
biodiversity metrics vary across land-use types (Harrison et al.2018), and changes in abundance of target taxa (LeCroy et al.2020). At the same time, we have learned very little about the
mechanisms driving those patterns. For nearly all wild bees, we have
glaring knowledge gaps about basic biology throughout the life cycle,
including overwintering and nesting habitat. Therefore, we cannot fully
contextualize and interpret community-level patterns. For example, what
do we learn from knowing that bee communities differ by two or ten
species of metallic sweat bees (Dialictus spp.) if we do not know
how these species differ from each other ecologically?
Our viewpoint: We are at an impasse in which ecologists keep
generating community-level data on wild bees without collecting the life
history and population-level knowledge needed to fully understand,
contextualize, and interpret those data. Investing in research mainly at
the community level is a missed opportunity to understand processes
about wild bees across scales of biological organization. In addition,
our lack of understanding of wild bee life cycles limits our ability to
prescribe management to address declines (see, e.g., U.S. Fish and
Wildlife Service 2020).
We believe that an emphasis on community-level studies stems from two
misconceptions. First, population-level studies are perceived as too
conceptually narrow, i.e. a “sample size of one” in the context of bee
communities at landscape scales. And second, studying wild bees is
perceived as prohibitively challenging without pinned specimens.
We believe that population-level studies of wild bees can be done in a
way that leads to general inference (not a sample size of one). We also
believe that, if we overcome the misconception that studies of bee
populations are too narrow in scope, it will be straightforward to
overcome the technical limitations to doing field work with wild bees.
Rather than being an especially striking example of the focus on process
over pattern, wild bees could become an example of balancing breadth
with depth to understand how local processes determine landscape-level
patterns.
Overcoming the perception of narrowness: Population-level
studies can have a broad scope of inference if they are grounded in
testable ecological theory. In this framework, generalization comes from
studies that test general hypotheses and theoretical predications using
single species. Generalization also comes from comparative approaches
that leverage each of these cases as building blocks to construct
“rules of thumb” about ecological processes (Grainger et al.2022). As a result, population-level studies throughout the life cycle
can simultaneously teach us rules for how populations operate and
communities assemble, and generate quantitative guidelines for
species-specific conservation.
In many other fields of ecology, there is a long tradition of leveraging
single-species studies to learn rules about how populations operate. For
example, herbaceous perennial plants are model systems for testing life
history theory. By the 1990s, ecologists had generated enough
population-level data to conduct comparative studies across dozens of
taxa (Silvertown et al. 1996; Salguero-Gómez et al. 2017).
Similarly, butterfly populations are longstanding model systems for
movement (Kareiva & Shigesada 1983; Schultz & Crone 2001) and
metapopulation dynamics (Baguette et al. 2003; Matter et
al. 2004). And, bumble bees have been foundational in our understanding
of foraging ecology (Thomson et al. 1987; Harder 1990) and
pollination biology (Waser & Price 1981; Ogilvie & Thomson 2016).
Studies with bumble bees in these areas represented about one-quarter of
our literature search (21/95 articles).
However, the idea of grounding population-level studies in theory is not
widespread among bee ecologists interested in conservation or other
responses to environmental change. From our literature survey, one
quarter of articles (23/95) investigated bee populations, but half of
these (11/23 articles) were largely descriptive, e.g., describing the
range of a species, characterizing diet breadth, or reporting
fecundities. Describing patterns at the population level is not a fix to
describing patterns at the community level. The kinds of
population-level studies that provide broad inference about wild bees
are those that test theoretically-motivated predictions.
Wild bees as model systems for ecological theory: In this
context, wild bees could be excellent systems for testing several areas
of ecological theory. The second half of population-level studies in our
sample (12/23 articles) exemplify this viewpoint, mainly testing theory
about 1) nutritional ecology and 2) drivers of vital rates (Fig. 1).
Studies in these two areas help us interpret findings from
landscape-level studies as follows:
Nutritional ecology : Wild bees are elegant systems for asking
questions about nutritional ecology because offspring are fed discrete
amounts of pollen, and diet contents can be inferred from foraging
females or nest contents (Cane & Sipes 2006). Past work has focused
on the use of novel pollen sources, dietary mixing, and nutritional
needs across life stages (Praz et al. 2008; Filipiak 2019;
McAulay et al. 2020). From this work, we learn how patterns of
bee biodiversity are shaped by landscape features like floral
resources.
Drivers of vital rates: Vital rates are the demographic
parameters like survival and reproduction that govern progression
through the life cycle. Knowing how environmental factors like
resource availability and natural enemies influence bee vital rates
(Roulston & Goodell 2011; Crone & Williams 2016) is key for
contextualizing and forecasting patterns of bee abundance across on
the landscape.
We think wild bees would be excellent model systems in at least three
additional areas, none of which came up in our 95-article sample
(Fig.1). While these areas have a rich tradition in many fields of
ecology, they have generally received less attention in bees, and so
could be especially valuable for future research:
- Voltinism and phenology ( e.g. timing of life cycle
events ): Standing variation in bee voltinism—the number of
generations occurring within a year—makes it straightforward to
study mechanisms underpinning widespread changes in phenology
(Bartomeus et al. 2011; Duchenne et al. 2020). For
instance, some wild bees produce offspring that emerge after one or
two years (Forrest et al. 2019), and ecological theory predicts
that producing offspring with mixed emergence times can act as a
bet-hedging strategy in variable environments. Wild bees could be used
to test bet-hedging theory and also to understand how phenological
variation confers resilience to bee populations in general.
- Habitat selection at multiple spatial scales : Bees are
central-place foragers, meaning nesting habitat is not necessarily the
same as foraging habitat. This contrast makes bees well suited for
teasing apart drivers of habitat selection. Mechanistic studies in
bees could build habitat selection theory by testing whether
predictions for long-lived vertebrates (Mayor et al. 2009) hold
for short-lived invertebrates. For conservation, these studies would
teach us explicitly about both foraging and nesting habitat needs
(Antoine & Forrest 2020).
- Movement ecology : Adult bees make two kinds of movements during
their lives: daily foraging to flowers and less frequent dispersal to
new nesting sites. One general question is whether the same rules
determine movement during these two behavioral modes. For
conservation, understanding the interplay between foraging and
dispersal is key to contextualizing range shifts (Marshall et
al. 2020) and identifying future reserve placement (Hannah et
al. 2007).
Overcoming limitations of fieldwork with wild bees : Studying
wild bee populations requires working with living specimens in the
field. In the 20th century, it was not uncommon for
entomologists to study wild bees throughout their life cycle (e.g.,
Linsley et al. 1952; Eickwort 1975; Batra 1980). However, recent
population-level studies of wild bees are quite taxonomically
restricted. In our sample, the theory-motivated population-level studies
worked with just three genera of wild bees: Bombus (5
papers), Osmia (6 papers), and Ceratina (1 paper).
Although these genera are valuable model systems, they limit our
potential scope of inference compared to the enormous taxonomic and
ecological diversity found within wild bees.
We believe that one reason why studies of bees are taxonomically
restricted is the perception that wild bee species can only be
identified with a microscope. While this perception is true for many
species, it is also true that many wild bee species can be identified
while alive using field marks—features like coarse morphology,
phenology, behavior, and habitat associations unique to each species.
Radical as it may sound, this is not a new idea for insects. Butterfly
and dragonfly watchers have transitioned over the past 25 years from
nets and kill jars to field marks and binoculars. We can do the same for
bees.
To illustrate this possibility, we have compiled a starting list of
field-identifiable bee species in eastern North America. Out of
~400 candidate species, at least 70 can be recognized
from field marks, and they are distributed across the bee phylogeny
(Fig. 2; see Table S2 for list). If we extrapolate across North America,
this means that, conservatively, about 20% of 4000 bee species could be
studied at the population level.
Once we recognize that bees can be identified in the field, we can use
old-school methods to study them throughout their life cycles. Methods
like mark-recapture, nest excavations, and trap nests, which were
commonplace in 20th century natural history studies of
bees (Linsley et al. 1952), are still some of the best suited
tools for studying wild bee populations (Iles et al. 2019;
Williams et al. 2019; Wong & Forrest 2021)(Fig. 1).
An ecologist looking for a study species might carefully select one from
our field-identifiable list that typifies a theoretical question of
interest—for example, variation in voltinism, use of habitat types
sensitive to climate or land use change, or spatial scales of foraging
(see examples in Figure 1). Choosing a species that can be used to test
theory is a classic approach in ecology, however, based on our
conversations with early-career ecologists interested in pollinator
conservation, this approach seems to be lost from the current paradigms
of studying wild bees.
Conclusions: Although an emphasis on studying large-scale
patterns over population-level processes is particularly striking in
wild bees, it is currently a widespread trend across ecology. We want to
remind ecologists that relying only on large-scale studies to understand
large-scale processes is unnecessarily restrictive. Population-level
studies at smaller scales can help us interpret and contextualize
large-scale patterns by testing theory-motivated mechanisms. Studies
throughout the life cycle are also especially urgent for filling
knowledge gaps for taxa (like bees) that are of conservation importance
but whose basic biology is poorly understood. We are not saying this is
easy—it is always challenging to balance theory with natural history
in a meaningful way. However, such studies are far more feasible than
ecologists studying wild bees tend to assume. For all taxonomic groups,
we need to remember to balance breadth with depth to meaningfully
understand and address the biological impacts of global change.
Acknowledgements: We thank Max McCarthy for many helpful
conversations about our list of field-identifiable bees. We also thank
the Crone-Orians lab group for feedback on this manuscript.