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Within-season flowering interruptions are common in the water-limited Sky Islands

Abstract

Within-season breaks in flowering have been reported in a wide range of highly variable ecosystems including deserts, tropical forests and high-elevation meadows. A tendency for interruptions in flowering has also been documented in southwestern US “Sky Island” plant communities, which encompass xeric to mesic conditions. Seasonal breaks in flowering have implications for plant reproductive success, population structure, and gene flow as well as resource availability for pollinators and dependent animals. Most reports of multiple within-season flowering events describe only two distinct flowering episodes. In this study, we set out to better quantify distinct within-season flowering events in highly variable Sky Islands plant communities. Across a >1,200 m elevation gradient, we documented a strong tendency for multiple within-season flowering events. In both distinct spring and summer seasons, we observed greater than two distinct within-season flowering in more than 10 % of instances. Patterns were clearly mediated by the different climate factors at work in the two seasons. The spring season, which is influenced by both temperature and precipitation, showed a mixed response, with the greatest tendency for multiple flowering events occurring at mid-elevations and functional types varying in their responses across the gradient. In the summer season, during which flowering across the gradient is limited by localized precipitation, annual plants exhibited the fewest within-season flowering events and herbaceous perennial plants showed the greatest. Additionally, more distinct events occurred at lower elevations. The patterns documented here provide a baseline for comparison of system responses to changing climate conditions.

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References

  • Aronson J, Kigel J, Shmida A, Klein J (1992) Adaptive phenology of desert and Mediterranean populations of annual plants grown with and without water stress. Oecologia 89:17–26

    Article  Google Scholar 

  • Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15:257–267

    Article  Google Scholar 

  • Bawa KS, Kang H, Grayum MH (2003) Relationships among time, frequency, and duration of flowering in tropical rain forest trees. Am J Bot 90:877–887

    Article  Google Scholar 

  • Bowers JE, Dimmit MA (1994) Flowering phenology of six woody plants in the northern Sonoran Desert. B Torrey Bot Club 121:215–229

    Article  Google Scholar 

  • Bronstein JL (1995) The plant-pollinator landscape. In: Hansson L, Fahrig L, Merriam G (eds) Mosaic landscapes and ecological processes. Chapman & Hall London, pp 256–288

  • Brown DE (1982) Biotic communities: southwestern United States and northwestern Mexico. University of Utah Press, Salt Lake City

    Google Scholar 

  • Bullock SH, Solis-Magallanes JA (1990) Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:22–35

    Article  Google Scholar 

  • Burgess TL (1995) Desert grassland, mixed shrub savanna, shrub steppe, or semidesert scrub? In: McClaran MP, Van Devender TR (eds) The desert grassland. The University of Arizona Press, Tucson, pp 31–67

    Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615. doi:10.1126/science.1232728

    Google Scholar 

  • Crimmins TM, Crimmins MA, Bertelsen CD, Balmat J (2008) Relationships between alpha diversity of plant species in bloom and climatic variables across an elevation gradient. Int J Biometeorol 52:353–366

    Article  Google Scholar 

  • Crimmins TM, Crimmins MA, Bertelsen CD (2010) Complex responses to climate drivers in onset of spring flowering across a semi-arid elevation gradient. J Ecol 98:1042–1051

    Article  Google Scholar 

  • Crimmins TM, Crimmins MA, Bertelsen CD (2011) Onset of summer flowering in a ‘Sky Island’ is driven by monsoon moisture. New Phytol 191:468–479

    Article  Google Scholar 

  • Crimmins TM, Crimmins MA, Bertelsen CD (2013) Spring and summer patterns in flowering onset, duration, and constancy across a water-limited gradient. Am J Bot 100(6):1–11

    Article  Google Scholar 

  • Ehleringer J (1985) Comparative microclimatology and plant responses in Encelia species from contrasting habitats. J Arid Environ 8:45–56

    Google Scholar 

  • Ehleringer JR, Phillips SL, Schuster WSF, Sandquist DR (1991) Differential utilization of summer rains by desert plants. Oecologia 88:430–434

    Article  Google Scholar 

  • Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439

    Article  Google Scholar 

  • Etheredge D, Gutzler DS, Pazzaglia FJ (2004) Geomorphic response to seasonal variations in rainfall in the Southwest United State. Geol Soc Am Bull 116:606–618

    Article  Google Scholar 

  • Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919

    Article  Google Scholar 

  • Goodrich DC, Faures J, Woolhiser DA, Lane L, Sorooshian S (1995) Measurement and analysis of small-scale convective storm rainfall variability. J Hydrol 173:283–308

    Article  Google Scholar 

  • Hunter RB (1989) Competition between adult and seedling shrubs of Ambrosia dumosa in the Mojave Desert Great Basin. Nature 49:79–84

    Google Scholar 

  • Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362

    Article  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Llorens L, Peñuelas J (2005) Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. Int J Plant Sci 166:235–245

    Article  Google Scholar 

  • MacMahon JA, Schimpf DJ (1981) Water as a factor in the biology of North American desert plants. In: Evans DD, Thames JL (eds) Water in desert ecosystems. Dowden, Hutchinson, Ross, Stroudsburg, PA, pp 114–171

    Google Scholar 

  • MacMahon JA, Wagner FH (1985) The Mojave, Sonoran and Chihuahuan Deserts of North America. In: Evenari M, Noy-Meir I, Goodall DW (eds) Hot deserts and arid shrublands. Ecosystems of the world, vol 12A. Elsevier, Amsterdam, pp 105–202

    Google Scholar 

  • Maestre FT, Salguero-Gómez R, Quero JL (2012) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Philos Trans R Soc B 367:3062–3075

    Article  Google Scholar 

  • McGinnies WG (1981) Discovering the desert. University of Arizona Press, Tucson

    Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  Google Scholar 

  • Miller-Rushing AJ, Inouye DW (2009) Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am J Bot 96:1821–1829

    Article  Google Scholar 

  • Newstrom LE, Frankie GW, Baker HG, Colwell RK (1994) Diversity of long-term flowering patterns. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: Ecology and natural history of a neotropical rain forest. University of Chicago Press, Chicago, pp 142–160

    Google Scholar 

  • Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:23–51

    Article  Google Scholar 

  • Oleson JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582

    Article  Google Scholar 

  • Opler PA, Frankie GW, Baker HG (1976) Rainfall as a factor in the release, timing, and asynchronization of anthesis by tropical trees and shrubs. J Biogeogr 3:231–236

    Article  Google Scholar 

  • Prieto P, Peñuelas J, Ogaya R, Estiarte M (2008) Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Ann Bot 102:275–285

    Article  Google Scholar 

  • Reynolds JF, Kemp PR, Tenhunen JD (2000) Effects of long-term rainfall variability on evapotranspiration and soil water distribution in the Chihuahuan Desert: a modeling analysis. Plant Ecol 150:145–159

    Article  Google Scholar 

  • Reynolds JF, Kemp PR, Ogle K (2004) Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141:194–210

    Article  Google Scholar 

  • Sala OE, Lauenroth WK (1985) Root profiles and the ecological effect of light rainshowers in arid and semiarid regions. Am Midl Nat 114:406–408

    Article  Google Scholar 

  • Salguero-Gómez R, Siewert W, Casper BB, Tielbörger K (2012) A demographic approach to study effects of climate change in desert plants. Philos Trans R Soc B 367:3100–3114

    Article  Google Scholar 

  • Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426

    Google Scholar 

  • Shreve F (1951) Vegetation of the Sonoran Desert. Carnegie Institution of Washington, Washington, DC

    Google Scholar 

  • Smith SD, Nowak RS (1990) Ecophysiology of plants in the intermountain lowlands. In: Osmond CB, Pitelka LF, Hidy M (eds) Plant biology of the basin and range. Springer, Berlin, pp 179–241

    Chapter  Google Scholar 

  • Smith SD, Monson RK, Anderson JE (1997) Physiological ecology of North American desert plants. Springer, Berlin

    Book  Google Scholar 

  • Solbrig OT, Orians GH (1977) The adaptive characteristics of desert plants: a cost/benefit analysis of photosynthesis leads to predictions about the types and distributions of desert plants. Am Sci 65:412–421

    Google Scholar 

  • Szarek SR, Woodhouse RM (1976) Ecophysiological studies of Sonoran Desert plants. I. Diurnal photosynthesis patterns of Ambrosia deltoidea and Olneya tesota. Oecologia 26:225–234

    Article  Google Scholar 

  • Tevis L (1958) Germination and growth of ephemerals induced by sprinkling in a sandy desert. Ecology 39:681–688

    Article  Google Scholar 

  • Venable DL, Pake CE (1999) Population ecology of Sonoran Desert annual plants. In: Robichaux RB (ed) The ecology of Sonoran Desert plants and plant communities. University of Arizona Press, Tucson, pp 115–142

    Google Scholar 

  • Walter H (1971) Natural savannahs as a transition to the arid zone. In: Ecology of tropical and subtropical vegetation. Oliver & Boyd, Edinburgh, pp 238–265

  • Went FW (1948) Ecology of desert plants. I. Observations on germination in the Joshua Tree National Monument, California. Ecology 29:242–253

    Article  Google Scholar 

  • Went FW (1949) Ecology of desert plants. II. The effect of rain and temperature on germination and growth. Ecology 30:1–13

    Article  Google Scholar 

  • Went FW (1957) The experimental control of plant growth. Varronica Botanica, Waltham

    Google Scholar 

  • Whittaker RH, Niering WA (1965) Vegetation of the Santa Catalina Mountains, Arizona: a gradient analysis of the south slope. Ecology 46:429–452

    Article  Google Scholar 

  • Whittaker RH, Buol SW, Niering WA, Havens YH (1968) A soil and vegetation pattern in the Santa Catalina Mountains, Arizona. Soil Sci 105:440–450

    Article  Google Scholar 

  • Xavier-Picó F, Retana J (2001) The flowering pattern of the perennial herb Lobularia maritima: an unusual case in the Mediterranean basin. Acta Oecol 22:209–217

    Article  Google Scholar 

Download references

Acknowledgments

We are thankful to the staff and associated researchers of the University of Arizona Herbarium for assistance with plant identification. We are also grateful to J.F. Weltzin, A.H. Rosemartin, and the staff of the USA National Phenology Network National Coordinating Office, who are consistently supportive of this research and frequently provide thoughtful comments and suggestions. We also sincerely appreciate M. Borgstrom’s guidance with statistical tests. Finally, this manuscript was dramatically improved by the input from two anonymous reviewers.

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Correspondence to Theresa M. Crimmins.

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Crimmins, T.M., Bertelsen, C.D. & Crimmins, M.A. Within-season flowering interruptions are common in the water-limited Sky Islands. Int J Biometeorol 58, 419–426 (2014). https://doi.org/10.1007/s00484-013-0745-9

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  • DOI: https://doi.org/10.1007/s00484-013-0745-9

Keywords

  • Arid
  • Elevation gradient
  • Flowering phenology
  • Interrupted flowering
  • Phenology
  • Semi-arid
  • Water-limited