Interspecific variation in traits
Hydraulic function varied substantially in Cordia species distributed in tropical forests across a precipitation gradient. Cordia species in drier habitats were more resistant to drought-induced embolism and lost turgor at lower leaf water potentials than those in wetter habitats. Surprisingly, there was not a significant relationship between MAP and other hydraulic traits such as vessel diameter, Ks and KL. These findings indicate that increased drought tolerance does not necessarily require a trade-off in hydraulic capacity.
In general, a greater proportion of variation in hydraulic traits was accounted for by differences between species within a site than differences across sites. This finding suggests that Cordia species may have diversified in hydraulic behavior, corresponding to different niches within each given forest, or else that they previously adapted to diverse conditions, and have recently come to coexist at given sites (Cavender-Bares et al., 2004). Strong within-site variation among species in key functional traits eclipsing the average differences across sites has been reported in studies of diverse species sets examining traits such as leaf mass per area, foliar nutrient concentrations, and seed mass (Wright et al., 2001; Grubb, 2002; Moles et al., 2005). Our data are the first, to our knowledge, to show this pattern in hydraulic traits for species within a wide-ranging genus.
Studies of general trends in xylem anatomy have demonstrated that vessel diameters are, on average, larger in wet habitats than in dry habitats (Dickison, 2000), including for wet vs dry tropical forest taxa (Barajas-Morales, 1985). This trend was also apparent in the larger average vessel diameters at the two moister sites than at Palo Verde. However, the relationship between vessel diameter and precipitation is complex (Baas, 1986) and general trends can mask differences in hydraulic function that occur within a site. We observed a range of vessel diameters within each site, with the greatest range occurring at the driest site. Hydraulic function is influenced by the frequency of vessels in cross-sections as well as vessel diameter. At Palo Verde, species with wider vessels (C. collacocca and C. dentata) had lower VD than species with narrow vessels (C. inermis and C. pringle), resulting in similar Ks values for these species. The exception to this trend was C. alliodora, in which the combination of wide vessels and high VD resulted in a Ks three times higher than other species at Palo Verde. It is possible that some of this variation in vessel anatomy is correlated with seasonal patterns of leaf phenology (Sobrado, 1993; Choat et al., 2005a), but investigation of this relationship will require further detailed comparative observations of leaf shedding in these Cordia species.
There were significant differences in Ks and HV between Cordia species at Palo Verde and at the two wetter forests. However, Ks and KL were highest at the intermediate site (BCI) and there was no relationship between MAP and these hydraulic traits. This may be partly because of the role other environmental factors have played in shaping hydraulic traits. At the wetter sites, it was apparent that light regime also influenced hydraulic parameters, and thus the variation of hydraulic traits is associated with the occurrence of Cordia species in a range of environments in each forest. On BCI, the understorey species C. lasiocalyx had significantly lower Ks than C. alliodora and C. panamensis, which both favor disturbed areas with high light and high evaporative demand. Lower Ks and KL for shade-establishing relative to light-demanding tropical woody species parallels trends for leaf hydraulic conductance (Sack et al., 2005).
The higher HV in Palo Verde species compared with species at wetter sites is consistent with previously observed increases in HV as a genetic or plastic adjustment to increasing evaporative demand and declining soil moisture availability (Shumway et al., 1993; Magnani et al., 2002). However, the bulk of the variation in KL was driven by variation in Ks, indicating that shifts in wood xylem traits are responsible for the diversity of hydraulic capacity, rather than shifts in shoot leaf : sapwood allocation. This contrasts with the relationship observed in Pereskia species occurring across a rainfall gradient, for which KL was strongly related to HV (Edwards, 2006). For Cordia species at Palo Verde (except for C. alliodora), differences in HV were not great enough to compensate for low Ks. As such, KL was lower for the Palo Verde species, meaning that they would generate a greater xylem pressure gradient (more negative Ψx) at a given transpiration rate. Thus, Cordia species from Palo Verde do not rely on high KL to reduce water potential gradients generated by transpiration but rather depend upon greater resistance to embolism to tolerate increasingly negative Ψx as the dry season progresses.
The results of our study are consistent with previous research showing that species occurring in mesic environments are generally less vulnerable to drought-induced embolism than species in xeric environments (Pockman & Sperry, 2000; Maherali et al., 2004). Our findings confirm this pattern among species within a diverse genus. Cordia species occurring at Palo Verde had the most negative P50, and species at La Selva had the least negative P50. The fact that vulnerability to embolism was more tightly correlated with MAP than other hydraulic traits illustrates its importance in determining drought tolerance and is consistent with the strong relationship between P50 and Ψpd observed for Cordia species. Studies of chaparral species have shown that P50 is tightly correlated with the seasonal minimum of predawn water potential, indicating that this parameter is finely tuned to variations in water availability (Pratt et al., 2007). Further, other studies have shown variation in vulnerability to embolism for groups of closely related species growing across precipitation gradients, suggesting that this trait is frequently important for the radiation of a lineage into different moisture regimes (Willson & Jackson, 2006; T. E. Dawson, unpublished).
The differences found across species may reflect the combination of plasticity across environments as well as genetic differences. The available data provide strong circumstantial evidence that variation observed in vulnerability to embolism and leaf tissue water relations parameters may partially arise from adaptation to contrasting moisture regimes. The current phylogeny shows that three species measured at Palo Verde, the driest forest –C. alliodora, C. collococca, and C. dentata– are more distantly related to one another than to at least one species at the intermediate site (Gottschling et al., 2005). Thus, it would appear that the consistently high resistance to embolism observed at Palo Verde is not a result of shared ancestry and the variation is far more likely to be adaptive in nature. Beyond this finding, unfortunately, it is currently not possible to place the variation in functional traits observed for Cordia species within a phylogenetic context, as the most recent Cordia phylogeny incorporates molecular data for only four of the species used in our study (Gottschling et al., 2005). We note that a phylogeographic understanding of trait diversification in these species would be complicated by the fact that much of their evolution may not have taken place in these forests. Given the relatively recent uplift of Panama and Costa Rica, the species examined in this study may have evolved elsewhere and moved into forest habitats that suited their trait combinations, in which case ecological sorting would have played a larger role than adaptation in driving the observed relationships between hydraulic traits and MAP.
Leaf tissue water relations parameters derived from pressure–volume curves differed between species at the three sites. The lower πft, Ψtlp and RWCtlp of species growing at Palo Verde are typical of drought-tolerant species, allowing them to maintain positive turgor as leaf water potential and RWC decline during drought (Sobrado, 1986; Fanjul & Barradas, 1987; Holbrook et al., 1995). We observed a strong correlation between P50 and Ψtlp, suggesting an integration of stem and leaf hydraulic traits conferring drought tolerance in Cordia species across the precipitation gradient. This finding is similar to the correlation of stem cavitation threshold and stomatal closure observed by Brodribb et al. (2003) in a phenologically and taxonomically diverse group of species co-occurring in one dry tropical forest. It is now becoming clear that stem and leaf traits are integrated across species at a number of levels, including flow capacity (Edwards, 2006; Sack & Holbrook, 2006), the coordination of hydraulic and photosynthetic capacity (Brodribb & Feild, 2000; Brodribb et al., 2002; Santiago et al., 2004), and, as shown here, drought tolerance.
In Cordia species at Palo Verde, there was a much larger safety margin between the water potentials at which turgor loss occurred and P50 values, suggesting that water loss from leaves would be reduced by declining stomatal conductance well before water potentials reached dangerous levels in the stems. At the wetter sites, particularly La Selva, lower safety margins may be more acceptable because water stress is less severe and opportunities for mitigation of water stress and refilling of embolized vessels are more frequent.
Intraspecific variation in hydraulic traits for C. alliodora
With the exception of drought-induced embolism, there was a striking lack of variation in hydraulic traits between populations of C. alliodora growing across a broad precipitation gradient. This suggests that plasticity and ecotypic divergence in traits conferring high wood hydraulic capacity are not key requirements for its extensive distribution. Rather, C. alliodora may owe its success to an ability to maintain high Ks and KL across a wide gradient in water availability while vulnerability to embolism and leaf-tissue parameters vary according to site water availability. This pattern is consistent with previous studies that have correlated the high stem and leaf hydraulic capacity of C. alliodora with high rates of photosynthesis (Santiago et al., 2004), high leaf vein density, and large stomatal pore area (Sack et al., 2005; Sack & Frole, 2006). These traits would contribute to the well documented success of C. alliodora as a fast-growing early successional species in wet and dry environments (Huante et al., 1995; Kapp et al., 1997; Hiremath et al., 2002).
Several studies have reported a correlation between vulnerability to embolism and water availability within a species (Franks et al., 1995; Alder et al., 1996; Mencuccini & Comstock, 1997; Sparks & Black, 1999). Generally, these studies have demonstrated that populations from drier environments are less vulnerable than those from wetter environments. This is consistent with the results of our study, with populations of C. alliodora at the wetter sites having higher P50 than those at drier sites. At Palo Verde, the high embolism resistance of C. alliodora is consistent with its ability to tolerate greater xylem tensions (daily Ψmin = –3.1 MPa). Borchert (1994) observed that C. alliodora growing at a nearby site in the Guanacaste province (Hacienda La Pacifica) desiccated strongly (stem Ψmin < –4.0 MPa) in the dry season and maintained leaves for longer than many co-occurring deciduous species. Resistance to embolism found in the BCI population (P50 =–2.9 MPa) was high relative to other tree species at this site (Machado & Tyree, 1994; Meinzer et al., 2003; Lopez et al., 2005). This may be linked with unusual leaf phenology of C. alliodora on BCI; the high resistance to embolism would allow for the maintenance of a canopy during the dry season. A similar leaf phenology is apparent in individuals growing at La Selva, although the P50 of this population was only –1.8 MPa. The fact that this phenology remains viable at La Selva despite higher P50 probably relates to the mild dry seasons and low frequency of drought experienced at this site.
There did not appear to be a trade-off between hydraulic efficiency and vulnerability to embolism across populations of C. alliodora. Indeed, the combination of higher efficiency and lower vulnerability to embolism in the Palo Verde population is unusual. However, the absence of a strong relationship between Dh or Ks and vulnerability to embolism is consistent with the air seeding hypothesis, which relates vulnerability to drought-induced embolism to the porosity of pit membranes rather than the diameter of xylem conduits (Tyree & Zimmermann, 2002). It is likely that observed differences in vulnerability to embolism are related to pit membrane structure and contact area between vessels (Choat et al., 2003, 2005b; Wheeler et al., 2005). However, the measurements of Ks in the present study included open vessels and it is possible that hydraulic limitations resulting from pit membrane resistance were not fully taken into account, masking a trade-off in hydraulic safety and efficiency across populations of C. alliodora.
Future common-garden experiments are needed to determine the degree to which the variation of hydraulic traits observed across populations of C. alliodora, and across Cordia species, are the result of ecotypic differentiation or phenotypic plasticity. Although previous studies have provided evidence that Atlantic and Pacific populations of C. alliodora are genetically distinct (Greaves & McCarter, 1990; Chase et al., 1995), this does not confirm that differences in vulnerability to embolism are genetically driven. Within other species, common-garden experiments demonstrate that differences in vulnerability to embolism are often maintained when water availability is held constant (Neufeld et al., 1992; Franks et al., 1995; Sparks & Black, 1999, T. E. Dawson, unpublished) indicating that variation in vulnerability to embolism is more likely to be under genetic control than the result of phenotypic plasticity. This view is consistent with experiments showing that P50 differed between four Eucalyptus clones, but that within each clone, there was no difference in P50 between populations growing at mesic and xeric sites (Pammenter & Vander Willigen, 1998). Future study of the possible genetic basis for diversification of hydraulic traits will help to explain not just the evolution of variation in plant function, but also the ability of related species to establish in given moisture regimes, and, thereby, potentially to elucidate both their biogeographical distribution and their ability to coexist within species-rich tropical communities (Harms et al., 2001; Engelbrecht et al., 2006).