Functional Ecology 2012, 26, 740–749
doi: 10.1111/j.1365-2435.2012.01967.x
Plant functional trait responses to interannual rainfall variability, summer drought and seasonal grazing in Mediterranean herbaceous communities Lorenzo Pe´rez-Camacho*,1, Salvador Rebollo1, Virginia Herna´ndez-Santana1,2, Gonzalo Garcı´a-Salgado1, Javier Pavo´n-Garcı´a1 and Antonio Go´mez-Sal1 1
Departamento de Ecologı´a, Edificio de Ciencias, Universidad de Alcala´, Ctra. Madrid-Barcelona KM. 33,600, ES-28871 Alcala´ de Henares, Madrid, Spain; and 2Department of Natural Resource Ecology and Management, Iowa State University, 339 Science II, Ames, Iowa 50011, USA
Summary 1. Some plant functional traits evolved with high temporal resource variability and disturbance in ecosystems where these factors are prevalent. Persistence of characteristics of these functional traits in ecosystems may depend on continued resource variability and disturbance, which in turn may promote functional diversity. In Mediterranean ecosystems, experiments that eliminate temporal resource variability and disturbance are needed to detect functional trait dependence on these factors. 2. The purpose of this study was to experimentally assess how interannual rainfall variability, summer drought and seasonal grazing modify the characteristics of functional traits (life span, flowering time, seed size and plant size) in old-field (6–15 years) Mediterranean herbaceous communities. 3. We designed a 9-year factorial field experiment that manipulated Mediterranean rainfall variability in three ways: (i) constant water availability with no summer drought; (ii) autumn and spring water availability but with summer drought; and (iii) no water supplied to rainfall; and grazing regimes: (i) autumn grazing; (ii) spring grazing; and (iii) non-grazing, in each of the three scenarios of water availability. At a community scale, we measured abundance of different categories within four plant functional traits: plant life span (annual and perennial), flowering time of annuals (spring and summer) and seed and plant sizes of spring annuals (small and large). 4. Interannual rainfall variability in autumn and spring (IRVAS), summer drought and grazing reduced perennial cover. IRVAS was necessary for the persistence of small-seeded and small-size spring annuals. IRVAS and summer drought increased spring annuals in grazed treatments. 5. Results suggest that IRVAS, summer drought and grazing favour the coexistence of species, through improved functional diversity in seed and plant sizes and increased abundance of spring annuals, the most species-rich functional group. Both effects may be the reason for the high species richness in grazed Mediterranean herbaceous communities. Key-words: flowering time, irrigation, life span, plant diversity, plant size, precipitation variability and distribution, seed size, sheep grazing
Introduction Understanding the implications of temporal variability of resources and disturbance on the structure and dynamics of biological systems is a key issue in ecology, nature conservation and management. The most distinctive features of the Mediterranean climate are temperature and precipitation *Correspondence author. E-mail:
[email protected]
seasonality, and the unpredictability of precipitation (Aschmann 1973). Such features limit the coincidence of factors determining primary production to two non-continuous and unpredictable periods in the year, autumn and spring, which are separated by a cold winter and a summer drought. In autumn and spring, the large interannual rainfall variability in amount and distribution appears to control germination, duration of vegetative growth and seed production (Espigares & Peco 1993), which may explain the
2012 The Authors. Functional Ecology 2012 British Ecological Society
Mediterranean plant functional trait responses 741 high interannual fluctuations in floristic composition in Mediterranean grasslands (Peco 1989; Espigares & Peco 1995; Peco, Rico & Azca´rate 2009). However, despite the importance of rainfall variability and summer drought on Mediterranean ecosystems, current knowledge is based on correlational studies and greenhouse and laboratory experiments (Pitt & Heady 1978; Pineda et al. 1987; Espigares & Peco 1995; Corbin & D¢Antonio 2004; Clary 2008; Peco, Rico & Azca´rate 2009). In addition, many conceptual models explaining the effects of disturbances, such as grazing, on the structure and dynamic of grassland communities suggest that grazing effects depend on the abundance and variability of precipitation (Milchunas, Sala & Lauenroth 1988; Behnke, Scoones & Heven 1993; Ellis 1994; Olff & Ritchie 1998; De Bello, Leps & Sebastia´ 2005; Dı´ az et al. 2007; Mashiri, McClaran & Fehmi 2008). Moreover, grazing effects may depend on the grazing season (Gibson et al. 1987; Rebollo et al. 2003; Pe´rez-Camacho & Rebollo 2009). In Mediterranean climates, there are few studies analysing seasonal grazing effects and their interaction with rainfall variability (Rebollo et al. 2003; Pe´rezCamacho & Rebollo 2009). Plants have developed a wide range of strategies, such as characteristics of their functional traits, to cope with both rainfall variability and grazing (Dyksterhuis 1949; Arnold 1955; Go´mez Sal et al. 1986; Milchunas, Sala & Lauenroth 1988; Dı´ az et al. 2007). The characterization of vegetation composition using plant functional traits is interesting and useful because: (i) it provides a mechanistic basis to explain plant dynamics and (ii) it allows us to compare plant responses to the factors among plant communities and at different spatial scales (local, regional or global scale) irrespective of species identity (Dı´ az et al. 2007). Life span and seed and plant size have been proposed as key attributes (Dı´ az et al. 2007) for understanding how plants deal with environmental variability and grazing. They are involved in key processes driving species distribution: seed size is linked to colonization capacity and seedling establishment (Azca´rate et al. 2002; Peco, Rico & Azca´rate 2009); plant size (above-ground) is linked to capacity for light competition and concurrently the susceptibility or avoidance of grazing disturbance or resistance (Milchunas, Sala & Lauenroth 1988; Osem, Perevolotsky & Kigel 2004; Dı´ az et al. 2007); and life span is linked to drought resistance, e.g. drought tolerance and avoidance strategies linked to perennials and spring annuals, respectively (Slatyer 1967; De Bello, Leps & Sebastia´ 2005). Flowering time also is linked to the capacity to cope with drought in annuals, e.g. drought tolerance and avoidance strategies linked to summer and spring annuals, respectively. The objectives of this study were to quantify the effects of: (i) interannual rainfall variability, (ii) summer drought and (iii) seasonal grazing on the abundance of functional groups in a Mediterranean herbaceous community ploughed 6 years prior to the start of study. Functional groups were differentiated according to: plant life span (annuals vs. perennials), flowering time of annuals (spring vs. summer annuals) and seed and plant sizes (height) of spring annuals (small- and
large-seeded spring annuals and small- and large-size spring annuals). To address this aim, we present a 9-year factorial field experiment manipulating Mediterranean rainfall variability, eliminating water deficit periods and creating three scenarios of water availability: (i) constant water availability with no summer drought; (ii) autumn and spring water availability but summer drought; and (iii) no water supplied, plant communities subject to the Mediterranean rainfall regime. We also considered three sheep grazing regimes, in each water availability scenario: (i) only in autumn; (ii) only in spring; and (iii) non-grazing. Summer drought, rainfall variability and seasonal grazing may limit the abundance of annual and perennial herbs (Jackson & Roy 1986; Clary 2008). Additionally, perennials may be the major competitors of annuals in Mediterranean environments (Tozer et al. 2009) and thus, perennial reduction may have a positive effect on abundance of annuals. We therefore predicted the overall effect of these limiting factors (summer drought, rainfall variability and seasonal grazing) on the functional groups of annuals to be a balance between the direct effects of the above factors, and a positive indirect effect owing to the reduction in perennial abundance through decreased competition. The response of each functional group depends on its ability to deal with any particular factor, and this will depend on characteristics of the particular functional trait. Understanding species filtering mechanisms may help explain the high species richness of grazed Mediterranean herbaceous communities and help provide a basis for strategic conservation and land management, as well as a context for future predictive assessments of the consequences of ecological and human changes, such as climate change.
Materials and methods STUDY SITE
The experiment was conducted at ‘El Encı´ n’ experimental farm (IMIDRA), located in central Spain (4035¢N, 325¢O, altitude 565 m). Climate is semi-arid continental Mediterranean, characterized by: (i) wet and cool winters (21 December – 21 March), with mean rainfall of 122 mm, and mean minimum and maximum temperatures of 0 and 11 C, respectively; (ii) dry and hot summers (21 June – 21 September), with mean rainfall of 56 mm, and mean minimum and maximum temperatures of 13 and 32 C, respectively, and at least 3 months of dry weather below herbaceous vegetation wilting point (Mauri 2000); and (iii) high interannual rainfall variability with 23% variation coefficient in the last 30 years. Average rainfall and temperature per year are 424 mm and 13 C, respectively. Rainfall and temperature during the experimental period were similar to those registered in the last 30 years (Fig. 1). Topography is flat, on a quaternary alluvial terrace. Soils are well drained with 31Æ8% and 26Æ4% sand and clay content, respectively, and pH = 8Æ1. Native vegetation is an Ulmus minor Mill. forest, which has long been converted into arable farmland. In 1991, cultivation was abandoned. Annuals dominate the current herbaceous plant community, which has high plant species richness: 103 species have been recorded in the study period (10 years) (see Table S1 in Supporting Information). We found 23 perennials, four of which were woody species. The vegetation growth season is associated with rainfall distribution throughout the year.
2012 The Authors. Functional Ecology 2012 British Ecological Society, Functional Ecology, 26, 740–749
742 L. Pe´rez-Camacho et al. 46 m
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Fig. 1. Climographs of the experimental period in the study area: (a) average data for monthly precipitation, maximum and minimum temperatures (white bars, dashed and solid lines, respectively) and (b) annual precipitation along the studied years.
Germination of spring annuals and regrowth of most perennials happens soon after the first autumn rains (September–October) (Ortega, Levassor & Peco 1997). Growth is rather slow during the winter months, but the vegetation is usually well established by early February. Growth is faster in spring, being the peak growth and seed set in May–June for spring species. By the end of June, most herbaceous vegetation is dry and most seeds have been dispersed. Summer annuals germinate in autumn and spring, and they appear as seedlings and juveniles in late spring, when most of the spring species have died. Summer species growth is faster during the summer if enough moisture is available, with a growth and seed set peak in September–October. Given the life cycle of annual plants, the period from September to August was considered a study year. Nomenclature of taxa: Tutin et al. (1964–1980); Castroviejo (1986–2010); Valde´s, Talavera & Ferna´ndez-Galiano (1987).
EXPERIMENTAL DESIGN
A factorial irrigation · grazing experiment was established in a 0Æ5ha area in autumn 1997, that is, 6 years after the last ploughing event (1991). The whole area was fenced to exclude wild herbivores such as rabbits and hares. Three irrigation regimes and three sheep grazing regimes were combined in a total of nine treatments (Fig. 2). Each treatment was allocated to one plot in a randomized block design with two replicates per treatment (a total of 18 plots). Plot size was 161 m2 (14 · 11Æ5 m), 2 m apart from each other to reduce the effects between plots. The experiment was run for 9 years (1997–2006).
Fig. 2. Experimental design: two blocks with nine factorial combinations of three irrigation and three sheep grazing regimes (plots) each. Six fixed sampling points per plot were monitored in 6 out of 9 years of treatments.
Henceforth, year 0 will refer to the period from September 1996 to August 1997 (the year before starting with irrigation and grazing treatments) and year 9 to the period from September 2005 to August 2006. At year 0, plant community was dominated by spring annuals (Rebollo et al. 2001) although herbaceous perennial cover was 17%. The species composition was homogeneous, and the cover of the functional groups was similar in the 18 plots.
Irrigation regimes The irrigation treatments included three regimes: (i) all-year irrigation; (ii) autumn-and-spring irrigation with summer drought; and (iii) non-irrigation (typical conditions of the Mediterranean climate). Soil moisture was monitored once a week using the Time Domain Reflectometry technique (TDR device: TRIME-FM version P2; IMKO Micromodultechnik GmbH, Ettlingen, Germany). Soil moisture was kept within optimal levels for plants (around 20%) in the first sixteen centimetres of soil during irrigation periods. Irrigation was weekly when necessary to complement rainfall, in order to maintain soil moisture above 20%. Therefore, the amount and distribution of irrigation varied depending on rainfall distribution of each year. Irrigation treatments were applied by four sprinklers (671 L h)1 each) per plot, placed at 1Æ5 m height, allowing homogeneous distribution of water. Each irrigation pulse was 25 L m)2. All-year irrigation ensured stable water availability for plants when rainfall did not provide it throughout the year. This treatment eliminated rainfall unpredictability and summer drought, the most critical events for plants in Mediterranean ecosystems. Autumn-and-spring irrigation took place from September 15th to October 31st and from March 10th to May 10th, during the most critical period for seed germination–seedling establishment (autumn) and plant growth–seed production (spring), but summer drought persisted. The non-irrigation treatment had no
2012 The Authors. Functional Ecology 2012 British Ecological Society, Functional Ecology, 26, 740–749
Mediterranean plant functional trait responses 743 water supplied and was subjected to the Mediterranean unpredictable fluctuating rainfall regime. The mean water content added per year in the all-year and autumn-and-spring irrigation treatments represented a surplus of 97Æ3% and 18% of annual precipitation with respect to non-irrigated plots, respectively.
Grazing management Grazing treatments comprised three seasonal sheep grazing regimes: autumn or spring grazing and non-grazing. Each grazing regime consisted in one grazing episode per year lasting c. 1 week. Sheep assigned to each plot were randomly selected each day to avoid individual effects. Stocking rates were 4Æ3 sheep ha)1 year)1 for autumn grazing (November) and 5Æ2 sheep ha)1 year)1 for spring grazing (April), given the higher forage availability in spring. Mean removed biomass by sheep with respect to plant biomass in autumn and spring at grazing time was 46% and 28%, respectively.
MEASUREMENTS
We set up a regular grid of six fixed sampling points per plot to monitor vegetation parameters. We present data for year 0 (1997) and 6 out of 9 years of treatments (1998, 1999, 2001, 2002, 2003 and 2006, being years 1, 2, 4, 5, 6 and 9, respectively). Years 2000 (3), 2004 (7) and 2005 (8) were not sampled although treatments were applied. Plant species cover was recorded in a 50 · 50 cm quadrat at each sampling point. The cover of each plant species was visually estimated as aerial cover, so total species cover could be higher than 100%, even where small bare patches occurred. In order to take into account the main seasonal production peak of each species, the vegetation was monitored during the two main primary production and flowering peaks: spring (May) and late summer (September). For each species, we selected the highest cover score to use it in statistical analyses, that is, from spring or late summer monitoring, which allowed sorting annuals according to their flowering time: spring vs. summer annuals. Thus, most spring annuals were not present as green plants during late summer monitoring, in which case spring data were used.
PLANT FUNCTIONAL TRAITS IN THE COMMUNITY
We sorted the species into functional groups according to a hierarchical scheme of functional traits. First, we sorted species according to their life span into annuals and perennials. Secondly, we sorted annuals according to their flowering time: spring vs. summer annuals. And thirdly, we sorted spring annuals, the most abundant herbaceous species, according to two size traits: (i) seed mass, frequently used as a surrogate for seed size (e.g. Thompson, Band & Hodgson 1993) [small-seeded (
