Volume 34 (2), 2014 Natural Areas Journal 227 Natural Areas Journal 34:227–234 • Timing is Everything: an Overview of Phenological Changes to Plants and Their Pollinators Michelle J. Solga1 1Range Science Program North Dakota State University NDSU Dept. 7630 P.O. Box 6050 Fargo, ND 58108-6050 Jason P. Harmon2,4 Amy C. Ganguli1,3 2Department of Entomology North Dakota State University NDSU Dept. 7650 P.O. Box 6050 Fargo, ND 58108-6050 3Department of Animal and Range Science New Mexico State University P.O. Box 30003 Las Cruces, NM 88003-8003 • 4 Corresponding author: Jason.Harmon@ NDSU.edu; 701-231-5083 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 INTRODUCTION Plant-pollinator mutualisms are among the best known and most important ecological interactions. Approximately 75% of flower- ing 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 spe- cies 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 con- servation (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 seem- ingly just as diverse. The iconic honey bee (Apis mellifera), for example, faces challenges from a variety of sources that may be contributing to its 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 et al. 2011; Gilgert and Vaughan 2011), which includes bees, moths, butterflies and the other groups of insect that can help pollinate plants (Har- mon et al. 2011). More recently, concerns have arisen about a very different type of threat, specifically that the timing of when plants and pollina- tors are active and receptive to pollination may be changing and could ultimately be- come mismatched so that they can no lon- ger interact effectively (Sparks and Menzel 2002; Memmott et al. 2007; Hegland et al. 2009; Solga 2012; Wolkovich et al. 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 C O N S E R V A T I O N I S S U E S 228 Natural Areas Journal Volume 34 (2), 2014 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 chang- ing 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 pres- ent 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 pollina- tors individually. If a mismatch is going to develop, there needs to be change by indi- viduals 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 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 phenol- ogy over time. It is usually difficult to quan- tify such long-term ecological changes, but fortunately there have been opportunities to continue or re-establish data on first flowering dates for some plant communi- ties. Past observations made by naturalists like Aldo Leopold and his daughter Anna in Wisconsin over a 61 year period (Brad- ley et al. 1999), and author Henry David Thoreau in Massachusetts during the mid- nineteenth 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 give us a good sense of phenologi- cal 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 advance- ment 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 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 include that they have at least 10 plant spe- cies within the same area, that they cover at least a 10 year stretch of time, and that they report the change in individual flow- ering plant species over time. We wanted 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 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). Volume 34 (2), 2014 Natural Areas Journal 229 to focus our study on plants relevant to animal pollination, so we were able to ex- clude 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 was to get an overview of these qualitative distribution patterns across spe- cies 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 transforma- tions 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 transfor- mation; however, in one study (Dunnell and Travers 2011), we used their data to calculate the recent average flowering date and subtracted the reported 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 per- formed 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 compari- sons across studies and do not try to make formal statistical analyses of the data. The result is six histograms that demon- strate the distribution of changes in flow- ering 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 infer- ences without accurately accounting for the length of time of the study, the actual changes in temperature and other environ- mental 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 five 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 characteris- tic divide in our data that makes five days a useful measure of comparison. Across all studies, almost half (48.5%) of the species flowered within five days of their historical flowering dates, indicat- ing little or no evidence of a phenological change over the observed time period. A similar proportion (41.4%) flowered ear- lier 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; 75.0% – Bai et al. 2011), and one study had relatively more species that delayed flowering by greater than five days after using our standardiza- tion 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. How- ever, using the criteria above, we identi- fied 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 con- text of pollination, so we cannot say for certain that all these species are important pollinators. All four studies looked at the adult insects’ date of first appearance 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 infor- mation into three broad, somewhat arbitrary categories: (1) phenological advances (> 5 days earlier); (2) little to no change (± 5 days); or (3) phenological delays (> 5 days later). 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; 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 stud- 230 Natural Areas Journal Volume 34 (2), 2014 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, U.k., (B) Minnesota and North Dakota, U.S.A., (C) Washington, D.C., U.S.A., (D) Beijing, China, (E) Wisconsin, U.S.A., and (F) New York, U.S.A. Volume 34 (2), 2014 Natural Areas Journal 231 ies thus far have looked for changes in pollinators and plants simultaneously. An exception is Bartomeus et al. (2011), where museum specimens were used to identify 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 pollinator, bumblebee queens, did not advance their emergence date (Kudo et al. 2004). Likewise, the solitary bee pol- linator 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 dem- onstrate 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 be- tween these two species occurred, this generalist pollinator was able to use other local flowering resources that were avail- able, 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 varia- tion in plant-pollinator phenology within species. For example, geographic location influences how the arrival of a humming- bird 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. However, at the northern edge, first flowering has become increas- ingly 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 implement- ed to counteract current threats, includ- ing 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 pol- linators require certain habitat conditions and resources to thrive and reproduce. Management efforts targeting pollinator conservation typically emphasize pro- tecting and enhancing existing pollinator habitat through a variety of best manage- ment 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 exca- vate 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. 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 prac- tices 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 Phenological Advances Little to No Change Phenological Delays (>5 days earlier) (±5 days) (> 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%) 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. 232 Natural Areas Journal Volume 34 (2), 2014 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 surface, can also be damaged by fire (Cane 2011). Pollinators are also known to be vulnerable to pesti- cides 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 livestock stocking rates can cause compaction of the soil, making it difficult for ground nesting bees to excavate their nests (Kearns and Inouye 1997). Over- wintering 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 exca- vating by ground nesting bees (Campbell et al. 2007). 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. Pol- linators require an abundance and diversity of floral resources spanning the entire du- ration of their respective life cycles (Potts et al. 2009; Dicks et al. 2010). Pollinators, especially bees, depend on nectar and pol- len 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 spe- cies and life cycle requirements, a succes- sion 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 pro- moted 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 phenologi- cal changes, there is a great deal of spe- cies-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 least the potential to disrupt plant and pollinator species, thereby threat- ening their interactions and the health of the ecosystems they reside in. Therefore, it is imperative that we develop manage- ment strategies to counteract current and future threats to preserve the ecosystem diversity and function that comes from healthy pollination interactions. ACKNOWLEDGMENTS The authors thank Carolyn Griygiel and Jack Norland for their comments on this project; Josh Campbell and Ron Hiebert for their work as editors; and David Inouye and an anonymous reviewer for their help- ful suggestions. This work was funded in part by the North Dakota Agricultural Experiment Station. Michelle Solga was a graduate student in the School of Natural Resource Sci- ences at North Dakota State University, Fargo, ND. 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