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Timing is everything: An overview of phenological changes to plants and their pollinators
Michelle J. Solga1, Jason P. Harmon2,4, Amy C. Ganguli1,3
1 Range Science Program
North Dakota State University
NDSU Dept. 7630; P.O. Box 6050
Fargo, ND 58108-6050
2 Department of Entomology
North Dakota State University
NDSU Dept. 7650; P.O. Box 6050
Fargo, ND 58108-6050
3 Department of Animal and Range Science
New Mexico State University
P.O. Box 30003
Las Cruces, NM 88003-8003
4 Corresponding author: Email: Jason.Harmon@NDSU.edu; 701-231-5083
Michelle Solga was a graduate student in the School of Natural Resource Sciences at North
Dakota State University, Fargo, ND.
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Jason Harmon is an Assistant Professor in the Entomology Department at North Dakota State
University, Fargo, ND.
Amy Ganguli is an assistant professor in the Department of Animal and Range Science at New
Mexico State University, Las Cruces, NM.
Word Count: 5,592
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Abstract
Plant-pollinator interactions are a critical component of a healthy plant community and a healthy
ecosystem. However, these interactions are at risk due to many factors, including potential
phenological mismatches that may disrupt the timing of successful pollination. Environmental
variables influence both when plants flower and when insects pollinate, and if those variables
change, so might the timing of each species. If those changes do not track each other, plants and
pollinators may not be active at the same time, potentially causing substantial problems to both
groups. Yet, there is little consensus thus far about how the timing of plants and pollinators has
been changing and how that might ultimately influence this important ecological interaction.
Here, we review the evidence for phenological shifts in both species and find that there is
evidence of change, but that it is extremely species-specific with some species advancing their
activities, some delaying, and some staying about the same. We also provide some management
guidelines to help promote healthy plant-pollinator relationships in light of the potential
variability in phenological shifts and the other threats these species face in natural areas.
Index terms: mutualism, phenological shifts, pollinator conservation, pollinator management
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Plant-pollinator mutualisms are among the best known and most important ecological
interactions. Approximately 75% of flowering plants engage in some sort of plant-pollinator
interaction (National Research Council 2007), and those interactions play a critical role in the
reproduction of the plants being pollinated and the larger plant community (Kearns et al. 1998).
The economic benefits of insect pollinators have been well documented in agricultural systems
as many of the world’s crop species depend on animal pollinators either partially or completely
(Losey and Vaughan 2006, Klein et al. 2007, Gallai et al. 2009). However, plant-pollinator
relationships are also critical to the health and sustainability of natural areas. Besides the genetic
and reproductive benefits plants receive from pollination (Kearns et al. 1998, Harmon et al.
2011), animal pollinators play less obvious, though often imperative, roles in maintaining plant
diversity and conservation (e.g. Travers et al. 2011) and as critical parts of the food-webs that
sustain insects, fish, and wildlife (Black et al. 2011, Gilgert and Vaughan 2011). While harder to
quantify, these ecological services are also incredibly valuable (Losey and Vaughan 2006,
Gilgert and Vaughan 2011). Despite their importance, plant-pollinator interactions are facing
serious threats, and it is becoming increasingly important to understand these mutualistic species
and the pressures they face so that we may best design scientific investigations and management
strategies to ensure their long-term sustainability.
Over 200,000 animal species may act as plant pollinators (Buchmann and Nabhan 1996),
and the dangers they face are seemingly just as diverse. The iconic honey bee (Apis mellifera),
for example, faces challenges from a variety of sources that may be contributing to their decline
as part of colony collapse disorder (Watanabe 1994). Other bees have specific habitat
requirements that are often in short supply (Gilgert and Vaughan 2011). Moreover, land-use
change and other anthropogenic disturbances are substantial disruptions to all pollinators (Black
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et al. 2011, Gilgert and Vaughan 2011), which includes bees, moths, butterflies and the other
groups of insect that can help pollinate plants (Harmon et al. 2011).
More recently, concerns have arisen about a very different type of threat, specifically that
the timing of when plants and pollinators are active and receptive to pollination may be changing
and could ultimately become mismatched so that they can no longer interact effectively (Sparks
and Menzel 2002, Memmott et al. 2007, Hegland et al. 2009, Solga 2012). For successful plant-
pollinator interactions, this timing is crucial: plants need to be in flower at the same time as their
pollinators are active or both organisms will likely suffer. Phenology is the area of study that
investigates the timing of such life cycle events and how they respond to the changing seasons or
climatic conditions (Forrest and Miller-Rushing 2010). The phenology of both plants and their
insect pollinators can be regulated by a variety of environmental cues, including photoperiod,
temperature, and precipitation (reviewed in Solga 2012). Recent evidence of changes in
temperature, precipitation, and other potential phenological cues (IPCC 2007) increases the
concern that the timing of plants and pollinators may also be changing and that these changes
could lead to mismatches that threaten plant-pollinator interactions.
Our overall objectives are to review the threat that changing phenologies may present to
plant-pollinator interactions and to provide some ideas as to what conservation or management
actions can be implemented to help conserve pollinators and ensure successful pollination. We
first evaluate the evidence for changes in the timing of flowering plants and then insect
pollinators individually. If a mismatch is going to develop there needs to be change by
individuals in at least one of these groups. We then integrate changes to both plants and
pollinators together, primarily by reviewing specific case-studies. Finally, we discuss
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management considerations that could help strengthen the health of plant-pollinator interactions
as they face environmentally-induced phenological changes as well as other potential threats.
Evidence for change in flowering phenology
Our first goal is to understand the current evidence for changes in flowering phenology
over time. It is usually difficult to quantify such long-term ecological changes, but fortunately
there have been opportunities to continue or re-establish data on first flowering dates for some
plant communities. Past observations made by naturalists like Aldo Leopold and his daughter
Anna in Wisconsin over a 61 year period (Bradley et al. 1999) and author Henry David Thoreau
in Massachusetts during the mid-19th century (Miller-Rushing and Primack 2008, Willis et al.
2008), among others, have given us valuable records of first flowering dates and the ability to
determine how flowering phenology has changed across plant species in particular locations.
Observations of first flowering date gives us a good sense of phenological change and it is the
best and longest data we have available, but since it only addresses when things start and not
how long flowering happens, it is only a partial picture of phenological changes.
A recent meta-analysis (Wolkovich et al. 2012) has used a very large database of
observational measurements to show that there is an overall advancement in the timing of both
flowering and leafing in plants. This paper does an exceptional job of demonstrating that across
all of the observational data they could find there is an overall significant advancement in the
phenology of plants in response to changing temperature. These results mean that we would
expect that most plants are flowering earlier than they have in the past; however this overall
effect doesn’t address the species-to-species variation we might find. The overall trend may be
advancement by a given amount, but how many of the plants in a given community are changing
by that same, average amount? How many are flowering even earlier? How many might not be
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responding or may even be delaying the timing of their flowering? By looking at the distribution
of species responses we can get a sense of how each plant in a broader group are changing their
first flowering dates and get a first response to some of these additional, complementary
questions to the established overall effect.
To characterize the distribution of changes to plant species we reviewed six studies that
quantify the change in first flowering date for multiple plants in a given location (Bradley et al.
1999, Abu-Asab et al. 2001, Fitter and Fitter 2002, Cook et al. 2008, Bai et al. 2011, Dunnell and
Travers 2011; Table 1). Our criteria for choosing data sets includes that they have at least 10
plant species within the same area, that they cover at least a 10 year stretch of time, and that they
report the change in individual flowering plant species over time. We wanted to focus our study
on plants relevant to animal pollination, so we were able to exclude some obvious wind-
pollinated plant communities. However for the studies we did use, we did not further evaluate
the relative importance of animal-pollinated out-crossing for each plant species.
To facilitate comparing data across studies, we calculated frequency distributions of the
observed changes in flowering phenology (in days) within each community (as in Fitter and
Fitter 2002). Because our main purpose is to get an overview of these qualitative distribution
patterns across species and studies, we treated all published information the same, however, there
is a great deal of variation among species and studies, with authors finding some patterns to be
statistically significant and others not. To calculate our graph of changes in days we performed
different transformations depending on the published analysis. Studies that took the average first
flowering date for a past time period and then found the difference with an average date for a
more recent period needed no transformation, however in one study (Dunnell and Travers 2011),
we used their data to calculate the recent average flowering date and subtracted the reported
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average from the older period. Other studies used linear regression to look at first flowering date
over time and reported the slope of that analysis. To put the data in the same format, we
multiplied those reported slopes with the total number of years in the study to arrive at an overall
change in flowering (in days) over the entire study as predicted by regression analysis. It is
completely possible that the transformations we performed induced biases; however, with the
data we have we cannot differentiate potential biases from our transformation from potential
biases of the data itself since it was collected and reported in different ways or from other
potential differences among the studies themselves. Therefore we make only rough qualitative
comparisons across studies and do not try to make formal statistical analyses of the data.
The result is six histograms that demonstrate the distribution of changes in flowering
phenology across 738 plant species in six geographical locations (Figure 1). The individual
distributions for each study provide an interesting picture of how many species within a given
area have changed in their flowering dates by a given amount.
In trying to compare results across studies it can be difficult to make strong inferences
without accurately accounting for the length of time of the study, the actual changes in
temperature and other environmental cues within each site, as well as additional characteristics
of both the sites and the plants themselves (for a discussion and thorough example of dealing
with these issues, see Wolkovich et al. 2012). However, we wanted to provide crude estimates of
what happened across these different distributions, so we provide some descriptive statistics of
species response in relation to changes within or beyond 5 days. Five days is somewhat arbitrary
and can be more or less meaningful depending on the length of the study or the amount of
temperature change a given study site has observed. However we found a characteristic divide in
our data that makes 5 days a useful measure of comparison.
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Across all studies almost half (48.5%) of the species flowered within five days of their
historical flowering dates, indicating little or no evidence of a phenological change over the
observed time period. A similar proportion (41.4%) flowered earlier in the season (>5d earlier)
and the remaining 10.0% began flowering later in the season (>5d later). Two studies had
notably greater proportions of species that flowered more than five days early (65.1% - Abu-
Asab et al. 2001 and 75.0% - Bai et al. 2011), and one study had relatively more species that
delayed flowering by greater than five days after using our standardization method (26.5% -
Dunnell and Travers 2011). These results are consistent with other studies investigating
individual plant species or small communities that have reported similar patterns in flower
timing in response to recent environmental change (Inouye et al. 2003, Crimmins et al. 2010,
Gordo and Sanz 2010, Lesica and Kittelson 2010, Crimmins et al. 2011).
Evidence for change in insect pollinator phenology
Similarly, we reviewed the literature to determine the evidence for changing phenology
in potential insect pollinators. Unfortunately, compared to plants, there have been fewer data sets
for groups of insects that span a decade or more. However, using the criteria above we identified
three studies on butterflies (Roy and Sparks 2000, Forister and Shapiro 2003, Stefanescu et al.
2003) and one on wild bees (Bartomeus et al. 2011) (Table 1). Only the bee study was done in
the context of pollination, so we cannot say for certain that all these species are important
pollinators. All four studies looked at the date of first appearance for their insects with the first
three using observations from monitoring efforts and the fourth relying on first museum
specimens collected within each year. Data were transformed as above, but given the relatively
small number of species observed, we could not use the fine-scaled distributions as we did with
plants. Instead we made our distributions extremely course by combining the information in to
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three broad, somewhat arbitrary categories. Again, our primary goal is to view the distribution of
species-specific responses, especially within studies as opposed to making quantitative statistical
inferences. The results from Stefanescu et al. (2003) are slightly different in that species showing
a non-significant change in first appearance are placed in the “little to no change” category.
As we saw for first flowering dates in plants, the way the first flight of insects changed
over time was highly variable (Table 2) with the relative proportion of species in our three
arbitrary categories in approximately the same ratio for insects (44.0% >5d earlier, 48.8% little
to no change, 7.1% >5d later) as it was for plants. Two of the four studies (Stefanescu et al. 2003
and Bartomeus et al. 2011) had greater proportions of their species with a large phenological
advance. However in the case of Bartomeus et al. (2011), this was likely an artifact of our
reporting predicted days changed over their very long study period as opposed to the more
accurate slope values reported in the study.
Evidence for change in plant-pollinator phenology
While the previous studies looked at either plants or pollinators individually, few studies
thus far have looked for changes in pollinators and plants simultaneously. An exception is
Bartomeus et al. (2011), where museum specimens identified changes in first capture (as an
estimate of first flight) in a community of generalist bees in the Northeastern United States, and
these changes were compared to published data for plants that are pollinated by these generalist
bees in the same area. Overall, they concluded that these pollinators and their plants were
changing at about the same rate.
Further evidence is provided from case studies of particular plants and pollinators. For
example, an out-crossing plant, yan hu suo (Corydalis ambigua), suffered from low seed-set
when it advanced its flowering date due to warmer spring temperatures, but its primary
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pollinator, bumblebee queens, did not advance its emergence date (Kudo et al. 2004). Likewise,
the solitary bee pollinator of yellow star-of-Bethlehem (Gagea lutea) was not available for
pollination when this plant advanced its bloom times (Kudo et al. 2004). In a similar case, the
glacier lily (Erythronium grandiflorum) experienced pollination limitation early in its bloom
period due to unavailability of bumblebee queens to pollinate its flowers (Thomson 2010).
At other times, pollinators might demonstrate plasticity in their phenology so that they
can keep pace with a changing host plant and thereby avoid a mismatch. The mutualism between
pollinating flies and their host plants Adonis ramose and Anemone flaccid at an alpine site did
not show any mismatch due to earlier spring season arrival dates, which may indicate that this
pollinator is responding to the same cues or that it has been able to quickly adapt to its plants’
emergence (Kudo et al. 2004).
Under certain conditions, a mismatch may actually not be detrimental. Hoplitis fulgida, a
solitary bee, completely missed the flowering period of its host legume Lathyrus, during one
season at several alpine sites (Forrest and Thomson 2011). Even though a complete decoupling
between these two species occurred, this generalist pollinator was able to use other local
flowering resources that were available and Lathyrus avoided pollination limitation because of
frequent pollination by other visiting insects (Forrest and Thomson 2011).
Just as we highlighted the variation that can occur among different species, there is good
reason to expect additional variation in plant-pollinator phenology within species. For example,
geographic location influences how the arrival of a hummingbird and the availability of its early-
season nectar resources have changed over time (McKinney et al. 2012). At the southern edge of
the hummingbird’s breeding range neither arrival nor first flowering dates have changed.
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However, at the northern edge first flowering has become increasingly earlier resulting in a
shorter overlap between flower and hummingbird.
Management Considerations
To safeguard plant-pollinator mutualisms and other interactions within ecosystems,
conservation measures must be implemented to counteract current threats, including those from a
changing environment. Challenges exist for managers who are balancing conservation efforts
with limited funding, time, and often the availability of suitable habitat. We first discuss general
practices that can enhance the overall health of the plant-pollinator relationship and then
highlight practices relevant to changing phenology in particular.
Just like other animal species, insect pollinators require certain habitat conditions and
resources to thrive and reproduce. Management efforts targeting pollinator conservation typically
emphasize protecting and enhancing existing pollinator habitat through a variety of best
management practices. For example, pollinators require a variety of resources to use as sites for
building their nests or laying their eggs and these resource needs should be incorporated into
pollinator conservation plans (Mader et al. 2011). Most native bees either nest in the ground or
use cavities in dead wood for nests (Vaughan and Black 2007); ground nesting bees require open
areas of ground that have the appropriate soil texture that enables bees to tunnel to build their
nests, whereas certain cavity nesting bees require old dead trees to excavate for nests. Wood
block nests provided by humans are used by some nesting bees and can provide a ready material
in areas such as grasslands that may otherwise be devoid of trees, shrubs, or dead wood
resources. Butterflies on the other hand require specific host plants on which to lay their eggs as
once the larvae emerge from eggs they will require plant leaves to provide them with vital food
resources.
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Habitat management practices such as mowing, haying, grazing, prescribed fire, and
pesticide application can directly and indirectly affect pollinators and should therefore be
appropriately timed (Black et al. 2011, Cane 2011). Mortality induced from direct exposure to
management practices is perhaps easier to mitigate though proper timing than indirect exposure.
Mowing, haying, and grazing of plants can potentially harm pollinators while depriving them of
food (Noordijk et al. 2009). Improper timing of prescribed fire may also negatively affect ground
nesting bees, especially solitary bees, because the heat can reach shallower nesting species (Potts
et al. 2003). Cavity nesting bees, depending on how closely their nests are located to the ground,
can also be damaged by fire (Cane 2011). Pollinators are also known to be vulnerable to
pesticides in their habitat (National Research Council 2007). Butterflies in various stages of
development can be directly affected by receiving pesticide spray meant for insect pests of plants
(Russell and Schultz 2010). Developing bees are particularly sensitive to pesticides contained in
pollen that is deposited in their nests (Kearns and Inouye 1997).
Management practices can also indirectly affect pollinators if not coordinated with plant-
pollinator life cycles. For example, untimely mowing, haying, or grazing may remove plants that
provide vital oviposition sites for butterflies and nesting sites for bees (Vaughan and Black 2007,
Black et al. 2011). Heavy stocking rates can cause compaction of the soil, making it difficult for
ground nesting bees to excavate their nests (Kearns and Inouye 1997). Overwintering or
oviposition sites for butterflies can be threatened if fire occurs during the immature stages of
their lifecycle (Swengel 2001, Cane and Neff 2011). Prescribed fire should also be avoided when
plants are in susceptible growth stages or blooming, however proper frequency and timing can
supply an eruption of forbs the following spring (Kearns and Inouye 1997, Potts et al. 2003) or
expose bare ground for excavating by ground nesting bees (Campbell et al. 2007).
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To overcome mismatches that may occur due to changing environmental conditions,
managers can create a buffer to safeguard pollinators against potential limitations in floral
resources within their habitats. Pollinators require an abundance and diversity of floral resources
spanning the entire duration of their respective life cycles (Potts et al. 2009, Dicks et al. 2010).
Pollinators, especially bees, depend on nectar and pollen resources for their energy needs and to
nourish their offspring whereas most butterflies require nectar as adults but use specific host
plants as plant-eating juvenile caterpillars (Kearns and Inouye 1997).
To provide for a variety of pollinator species and life cycle requirements, a succession of
blooming resources spanning the entire growing season can be implemented (Vaughan and Black
2006, USDA 2008). Pollinator species vary in different regions of the country and their life
cycles span fairly short time periods, many times only a few weeks. For pollinator habitats to
flourish, be sustainable, and provide for the needs of a wide assortment of pollinators, an array of
plant species needs to be promoted so that the needs of all specialist and generalist pollinators are
met. Ultimately a well-timed heterogeneous floral bloom that is available to pollinators
throughout the growing season will likely provide the diversity of pollen and nectar resources
required for them to not only prosper, but also to face future habitat alterations that
environmental change may generate.
Conclusion
Although there is evidence that some plants and pollinators are undergoing phenological
changes, there is a great deal of species-specific variation in how things have changed over the
last 50-100 years. Future efforts to understand this variation (e.g. Altermatt 2010, Diamond et al.
2011) and its implications will help us make better predictions and more refined conservation
policies. In the meantime, the evidence reviewed here implies that phenological change has at
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least the potential to disrupt plant and pollinator species, thereby threatening their interactions
and the health of the ecosystems they reside in. Therefore, it is imperative that we develop
management strategies to counteract current and future threats to preserve the ecosystem
diversity and function that comes from healthy pollination interactions.
Acknowledgments
This work was funded in part by the North Dakota Agricultural Experiment Station.
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Table 1. Characteristics of the six studies used to identify changes in flowering phenology across
plant species in a given location (Figure 1) and the four studies used to identify changes in insect
pollinator phenology (Table 2).
Phenology Articles Species Study Duration Analysis Location & Latitude
Flowering Plants
Fitter and Fitter 2002 385 1954-2000 Subtraction Oxfordshire, UK; 51.8ºN
Dunnell &Travers 2011 178 1910-2010 Subtraction MN & ND, USA; 46.9ºN
Abu-Asab et al. 2001 100 1970-1999 Regression Washington DC, USA; 38.9ºN
Bai et al. 2011 48 1963-2007 Regression Beijing, China; 39.9ºN
Bradley et al. 1999 55 1936-1998 Regression WI, USA; 43.5ºN
Cook et al. 2008 19 1928-2002 Regression NY, USA; 41.8ºN
Insect Pollinators
Roy & Sparks 2000 35 1976-1998 Regression British Isles, UK; 54ºN
Forister & Shapiro 2003 23 1972-2002 Regression CA, USA; 38.6ºN
Stefanescu et al. 2003 19 1988-2002 Regression El Cortalet, Spain; 42.2ºN
Bartomeus et al. 2011 10 1880-2010 Regression Northeast USA; 36-50ºN
23
Table 2. Change in potential insect pollinators over time. The number is the number of species
found within that category (calculations used to standardize reported data found in text) and the
percentage is the percentage of species within a given study found in each category.
Phenological Advances
(>5 days earlier)
Little to No Change
(±5 days)
Phenological Delays
(> 5 days later)
Roy & Sparks 2000 12 species (34%) 23 species (66%) 0 species (0%)
Forister & Shapiro 2003 5 species (22%) 12 species (52%) 6 species (26%)
Stefanescu et al. 2003 11 species (69%) 5 species (31%) 0 species (0%)
Bartomeus et al. 2011 9 species (90%) 1 species (10%) 0 species (0%)
24
0
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-25
-15
-5
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25
35
First Flowering Date Shifts (Days)
Plant Species (#)
AB
CD
EF
Figure 1. The distribution of phenological changes in first flowering dates for plant species with
the dashed line at 0 represents no change, negative numbers representing earlier flowering dates
and positive numbers representing later following dates for studies conducted in (A)
Oxfordshire, UK, (B) Minnesota and North Dakota, USA, (C) Washington, DC, USA, (D)
Beijing, China, (E) Wisconsin, USA, and (F) New York, USA.
