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Responses of Two Understory Herbs, Maianthemum Canadense And RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY Responses of two understory herbs, Maianthemum canadense and Eurybia macrophylla , to experimental forest warming: Early emergence is the key to enhanced reproductive output 1 Marie-Hélène Jacques 2 , Line Lapointe2,5 , Karen Rice 3 , Rebecca A. Montgomery 3 , Artur Stefanski 3 , and Peter B. Reich 3,4 PREMISE OF THE STUDY: Understory herbs might be the most sensitive plant form to global warming in deciduous forests, yet they have been little studied in the context of climate change. METHODS: A fi eld experiment set up in Minnesota, United States simulated global warming in a forest setting and provided the opportunity to study the responses of Maianthemum canadense and Eurybia macrophylla in their natural environment in interaction with other components of the ecosystem. Ef- fects of +1.7 ° and +3.4 ° C treatments on growth, reproduction, phenology, and gas exchange were evaluated along with treatment eff ects on light, water, and nutrient availability, potential drivers of herb responses. KEY RESULTS: Overall, growth and gas exchanges of these two species were modestly aff ected by warming. They emerged up to 16 ( E. macrophylla ) to 17 d ( M. canadense ) earlier in the heated plots than in control plots, supporting early-season carbon gain under high light conditions before canopy closure. This additional carbon gain in spring likely supported reproduction. Eurybia macrophylla only fl owered in the heated plots, and both species had some aspect of reproduction that was highest in the +1.7 ° C treatment. The reduced reproductive eff ort in the +3.4 ° C plots was likely due to reduced soil water availability, counteracting positive eff ects of warming. CONCLUSIONS: Global warming might improve fi tness of herbaceous species in deciduous forests, mainly by advancing their spring emergence. However, other impacts of global warming such as drier soils in the summer might partly reduce the carbon gain associated with early emergence. KEY WORDS Asparagaceae; Asteraceae; foliar nutrient concentrations; global warming; hardwood forest; phenology; photosynthetic rates; respiratory rates; understory light environment Warming of the climate system is unequivocal ( IPCC, 2007 ). Th e carbon, energy, and nutrient cycling ( Gilliam, 2007 ). Much less is herbaceous layer, with its high species richness, plays an important known about responses to warming of forest herbs compared with role in maintaining the functional integrity of temperate forest co-occuring larger trees. Climate change will require the migration, ecosystems through its interactions with the woody seedlings that acclimation, or adaptation of plant species because temperature is a determine, in part, the future canopy and through its role in crucial factor in determining the distribution of species ( Woodward and Williams, 1987 ). Since several forest understory species are very slow colonizers ( Verheyen et al., 2003 ), it is estimated that 1 Manuscript received 3 February 2015; revision accepted 11 September 2015. 2 Département de biologie and Centre d’étude de la forêt, Université Laval, Québec City, QC, their rate of migration might not match the rate imposed by Canada, G1V 0A6; changes in climate. For these reasons, it is urgent to assess the eff ect 3 Department of Forest Resources, University of Minnesota, St. Paul, Minnesota 55108 of temperature on the reproductive output of herbaceous plants USA; and ( Hovenden et al., 2008 ). So far, both positive and negative eff ects 4 Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, New South Wales, Australia have been reported on the reproductive output for the few herba- 5 Author for correspondence (e-mail: [email protected]) ceous species that have been studied ( Pearson and Shah, 1981 ; doi:10.3732/ajb.1500046 Hovenden et al., 2008 ; De Frenne et al., 2009 , 2010 , 2011 ); early 1610 • AMERICAN JOURNAL OF BOTANY 102 ( 10 ): 1610 – 1624 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America OCTOBER 2015 , VOLUME 102 • JACQUES ET AL. —RESPONSE OF TWO UNDERSTORY HERBS TO WARMING • 1611 spring fl owering species and more northern populations appear to Early senescence of herbaceous species subjected to a higher respond more positively to warming than summer fl owering and temperature regime was also observed ( Farnsworth et al., 1995 ; more southern populations ( De Frenne et al., 2009 ). Jochum et al., 2007 ), possibly indicating the development of a sink Global warming will also likely modify precipitation regimes al- limitation ( Lapointe, 2001 ). Another important component of plant though projection models do not agree, even at the regional scale. response to warming is physiological acclimation, which is the ad- For Minnesota, the PCM B1 model predicts an increased annual justment of photosynthetic and respiratory rates to improve plant rainfall with limited changes in summer precipitations, whereas performance at the new growth temperature ( Lambers et al., 1998 ). GFDL A1F1 scenario predicts a decrease in annual and in sum- Although photosynthesis and respiration are both known to be mer precipitations ( Handler et al., 2014 ). Because both models temperature sensitive, there is growing evidence that both pro- predict increases in temperature during the summer and more cesses acclimate, sometimes even to the extent of homeostasis, in frequent extreme events, it seems reasonable to suggest that un- plants exposed to a moderate range of temperature ( Campbell derstory species will experience more frequent and/or more se- et al., 2007 ; Sendall et al., 2015 ). We conducted a study on the eff ect vere drought in the future. Such changes can have direct adverse of experimental warming on two understory species widespread eff ects and might dampen any positive impact of warming on ni- in the southern boreal forests of North America: Maianthemum trogen supply through increased soil net nitrogen mineralization canadense Desfontaines and Eurybia macrophylla (L.) Cassini. Th e ( Griffi n, 1981 ; Rustad et al., 2001 ; Schimel et al., 2007 ; Manzoni study system, the B4WarmED experiment, is a free-air warming et al., 2012 ). facility used to study the eff ect of a warming climate on the regen- Whether growth responses to warming of understory herbs dif- eration of woody species ( Reich et al., 2015 ; Rich et al., 2015 ). fers from that of sympatric trees remains unclear. So far, the general Because the warming system is installed in a forest, it allows us to response of plant productivity in climate warming experiments study not only the eff ect of warming on the two species of interest, has been positive, but because many of the studies used in meta- but also its interaction with the soil system and other herbaceous analyses were conducted in Arctic ecosystems, these results are not and woody species. We tested the following series of hypotheses necessarily indicative of temperate forest herbs ( Arft et al., 1999 ; ( Fig. 1 ). Rustad et al., 2001 ; Dormann and Woodin, 2002 ; Walker et al., Direct and indirect eff ects of warming on the ecosystem compo- 2006 ). A recent meta-analysis used the plant functional group ap- nents will likely translate into changes in growth and reproduction proach and included 127 studies, many at mid-latitudes ( Lin et al., of the studied species. Some of these eff ects are expected to improve 2010 ). Th at study found that the increase in biomass of herbaceous growth and reproductive output of the herbaceous species, e.g., in- species (+5.2%) was smaller than the increase of woody species creased nutrient availability and earlier emergence, whereas factors (+26.7%) although much of this difference was explained by the such as lower water availability or lower light due to shading by fact that the eff ect on herbaceous species from studies of lower lati- taller plants are expected to negatively affect the two studied tudes was negative. Milder eff ects or negative eff ects of warming on species. Furthermore, some factors might have no net eff ect on car- herbaceous plants, where they cohabit with woody species, might bon gain, for instance, acclimation of the gas exchange rates. Spe- be explained through competitive interactions with plants of higher cifi cally, the objectives of the current study were to quantify the strata. Th e smaller size of herbaceous plants makes them more vul- impact of 3 years of warming on M. canadense and E. macrophylla nerable to shading from taller plants ( Castro and Freitas, 2009 ), and growth and reproduction. Furthermore, we tested if light availabil- their shallow roots make them more vulnerable to drier soil condi- ity in the understory both in the spring and in the summer, plant tions ( Jackson et al., 1996 ). phenology, leaf photosynthetic and respiratory rates and/or plant Climate change is expected to lengthen the growing season in nutrient concentration were modulated by the warming treatments. temperate climates. Earlier emergence of spring herbs following an Th is study quantifi es the growth response of two herbaceous species increase in temperature has been reported ( Farnsworth et al., 1995 ; to warming and helps to unravel some of the factors and mecha- De Frenne et al., 2011 ) and can be a great advantage since many nisms that contribute to this response. understory herbs produce most of their photosynthates before the closure of the canopy ( Bazzaz and Bliss, 1971 ; Brown et al., 1985 ; Lapointe, 2001 ). However, this advantage can be reduced if trees MATERIALS AND METHODS leaf out earlier, thus reducing the duration of the high light period for herbaceous growth ( Routhier and Lapointe, 2002 ). Herbaceous Biology of the studied species — Maianthemum canadense (false species that emerge during or aft er canopy closure exhibit limited lily of the valley; Liliaceae) is a rhizomatous clonal plant 5 to 20 cm changes in phenology ( Ishioka et al., 2013 ). Th e response of the high. Th e species is found in moist woods and thickets where it phenology of the overstory to warming is more complex than that sometimes forms continuous mats ( Gleason and Cronquist, 1963 ).
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