Simon Pierce

The global spectrum of plant form and function

Earth is home to a remarkable diversity of plant forms and life histories, yet comparatively few essential trait combinations have proved evolutionarily viable in today’s terrestrial biosphere. By analysing worldwide variation in six major traits critical to growth, survival and reproduction within the largest sample of vascular plant species ever compiled, we found that occupancy of six-dimensional trait space is strongly concentrated, indicating coordination and trade-offs. Three-quarters of trait variation is captured in a two-dimensional global spectrum of plant form and function. One major dimension within this plane reflects the size of whole plants and their parts; the other represents the leaf economics spectrum, which balances leaf construction costs against growth potential. The global plant trait spectrum provides a backdrop for elucidating constraints on evolution, for functionally qualifying species and ecosystems, and for improving models that predict future vegetation based on continuous variation in plant form and function.

Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants

Summary 1. Three main directions of adaptive specialization are evident in the world flora, reflecting fundamental trade-offs between economics (conservative vs. acquisitive investment of resources) and size. The current method of ordinating plants according to these trade-offs, CSR classification, cannot be applied to the woody species that dominate many terrestrial ecosystems. 2. We aimed to produce a novel CSR classification method applicable to vascular plants in general. 3. Principal components analysis (PCA) of variation in a range of plant traits for 678 angiosperm, gymnosperm and pteridophyte species was used to determine the limits to multivariate space occupied by functionally diverse species. From this calibration, correlations between PCA axes and values of leaf dry matter content (LDMC; as an index of conservatism in life history), specific leaf area (SLA; indicative of acquisitive economics) and leaf area (LA; photosynthetic organ size) were used to produce predictor regressions from which target species could be compared against the multivariate space. A spreadsheet was developed that returned ternary coordinates and tertiary CSR strategies for target subjects based on LA, LDMC and SLA values. 4. The method allowed classification of target species within a triangular space corresponding to Grime’s theoretical CSR triangle and was sufficiently precise to distinguish strategies between species within genera and within populations of species. It was also largely in agreement with previous methods of CSR classification for herbaceous species. 5. Rapid CSR classification of woody and herbaceous vascular plants is now possible, potentially allowing primary plant functional types and ecosystem processes to be investigated over landscape scales.

Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae

The distinctive foliar trichome of Bromeliaceae has promoted the evolution of an epiphytic habit in certain taxa by allowing the shoot to assume a significant role in the uptake of water and mineral nutrients. Despite the profound ecophysiological and taxonomic importance of this epidermal structure, the functions of nonabsorbent trichomes in remaining Bromeliaceae are not fully understood. The hypothesis that light reflection from these trichome layers provides photoprotection was not supported by spectroradiometry and fluorimetry in the present study; the mean reflectance of visible light from trichome layers did not exceed 6.4% on the adaxial surfaces of species representing a range of ecophysiological types nor was significant photoprotection provided by their presence. Several reports suggesting water repellency in some terrestrial Bromeliaceae were investigated. Scanning electron microscopy (SEM) and a new technique-fluorographic dimensional imaging (FDI)-were used to assess the interaction between aqueous droplets and the leaf surfaces of 86 species from 25 genera. In the majority of cases a dense layer of overlapping, stellate or peltate trichomes held water off the leaf epidermis proper. In the case of hydrophobic tank-forming tillandsioideae, a powdery epicuticular wax layer provided water repellency. The irregular architecture of these indumenta resulted in relatively little contact with water droplets. Most mesic terrestrial Pitcairnioideae examined either possessed glabrous leaf blades or hydrophobic layers of confluent trichomes on the abaxial surface. Thus, the present study indicates that an important ancestral function of the foliar trichome in Bromeliaceae was water repellency. The ecophysiological consequences of hydrophobia are discussed.

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline.

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the worlds largest fish at multiple spatial scales.

Implications for biodiversity conservation of the lack of consensus regarding the humped‐back model of species richness and biomass production

Department of Agricultural and Environmental Sciences (DiSAA), University of Milan, Milan, ItalyThe humped-back model of species richness and biomassproduction (Grime 1973, 2001; Al-Mufti et al. 1977) pre-dicts that taxonomic richness may be greatest at intermedi-ate biomass production and at intermediate intensities offactors that limit production, such as disturbance or stress.This model has, over the last four decades, become widelysupported as observational evidence has accumulated froma range of plant, animal and microbial communities interrestrial and aquatic habitats world-wide (reviewed byGrime & Pierce 2012). The humped-back curve is notalways evident (Mackey & Currie 2001; Mittelbach et al.2001; Hughes et al. 2007), but several authors (Moore K Guo & Berry 1998; Keddy 2005) have notedthat this is symptomatic of studies that investigate arestricted biomass range, such as within communitiesrather than across highly diverse habitat types, and thesestudies potentially bias meta-analyses. Furthermore, obser-vations from natural habitats are sometimes specificallyexcluded from meta-analyses in favour of culture experi-ments (Cardinale et al. 2011) which, it has been argued(Grime & Pierce 2012), defeats the aim of understandingphenomena occurring in nature. In order to provide alarge-scale observation of the productivity–richness rela-tionship in nature, Adler et al. (2011) measured speciesrichness and biomass production in situ for herbaceousvegetation across five continents. They concluded that pro-ductivity–richness relationships are ‘weak and variable’, atboth local and global scales.Adler et al. (2011) plotted their entire global data set asa single scatterplot, with regressions then fitted to within-site data (this is reproduced in Fig. 1a). When I producedthe same scatterplot of species richness and biomass fromthe data (available as an appendix to the original publica-tion), a cloud of data points was evident that, as Adleret al. (2011) state, was not well fitted by a humped-shapecurve (Fig. 1b).However, the humped-back model does not state thatthe productivity–richness relationship is a simple curve.Rather, it describes an upper limit to the potential diversi-ties that may develop along the biomass gradient (Grime2001; Grime & Pierce 2012), or in other words, a boundarythat separates productivity–richness relationships that arepossible (below the curve) from those that are not (above).This is something of which Adler et al. (2011) were aware:‘an alternative hypothesis states that productivity sets theupper limit on richness, with stochastic forces such as dis-turbance causing deviations below this limit’. Grace(2001), one of the co-authors of Adler et al. (2011), hadpreviously noted ‘weak regression relationships betweenbiomass and richness despite strong constraints on bound-ary relationships’ which he described as a ‘unimodalenvelope’.Indeed, a humped-back relationship may be lackingwhen measurements are taken in years that differ from thetypical local climate, but may reappear when conditionsreturn to those more typical and favourable for the estab-lishment and growth of local ecotypes (Laughlin & Moore2009). Grime (2001) also noted that ‘where vegetation issubject to such vicissitudes, it is not to be expected thatthe maximum in biomass and litter measured in anyone year will be predictably related to species richness’.Additionally, attainment of the maximum potential speciesrichness depends on the size of the local species pool(Grime 2001). For example, Foster (2001) found thatexperimental addition of seed of 34 species to a prairieincreased species richness markedly at lower productivities,but much less so at higher productivities. He concludedthat potential species richness is constrained by competi-tion at higher productivities but is sensitive to the size ofthe local species pool towards lower productivities. House-man & Gross (2006) similarly augmented the local speciespool available to a mid-successional old-field site thatincluded a range of microsites of varying productivity. Theproductivity–richness relationship was negative and linearwhen the species pool was restricted, but a larger speciespool allowed richness to increase only at intermediate pro-ductivities, resulting in a humped-back curve. They termedthe curve ‘saturated’ to denote its status as an upperpotential limit to richness. Olde Venterink et al. (2001)had previously labelled the curve as ‘filled’ for similar rea-sons, reflecting Grace’s (2001) ‘unimodal envelope’. Simi-

Whale sharks target dense prey patches of sergestid shrimp off Tanzania

Large planktivores require high-density prey patches to make feeding energetically viable. This is a major challenge for species living in tropical and subtropical seas, such as whale sharks Rhincodon typus. Here, we characterize zooplankton biomass, size structure and taxonomic composition from whale shark feeding events and background samples at Mafia Island, Tanzania. The majority of whale sharks were feeding (73%, 380 of 524 observations), with the most common behaviour being active surface feeding (87%). We used 20 samples collected from immediately adjacent to feeding sharks and an additional 202 background samples for comparison to show that plankton biomass was ∼10 times higher in patches where whale sharks were feeding (25 vs. 2.6 mg m−3). Taxonomic analyses of samples showed that the large sergestid Lucifer hanseni (∼10 mm) dominated while sharks were feeding, accounting for ∼50% of identified items, while copepods (<2 mm) dominated background samples. The size structure was skewed towards larger animals representative of L.hanseni in feeding samples. Thus, whale sharks at Mafia Island target patches of dense, large, zooplankton dominated by sergestids. Large planktivores, such as whale sharks, which generally inhabit warm oligotrophic waters, aggregate in areas where they can feed on dense prey to obtain sufficient energy.

Population structure and residency of whale sharks Rhincodon typus at Utila, Bay Islands, Honduras

There were 479 reported whale shark Rhincodon typus encounters between 1999 and 2011 at the island of Utila, which forms part of the Meso-American Barrier Reef System (MBRS) in the western Caribbean Sea. The majority of R. typus were found to feed on small bait fish associated with various tuna species. Ninety-five individual R. typus, ranging from 2 to 11 m total length (LT ), were identified through their unique spot patterns. A significant male bias (65%) was present. There was no significant difference between the mean ± s.d. LT of female (6·66 ± 1·65 m) and male (6·25 ± 1·60 m) R. typus. Most R. typus were transient to Utila, with 78% sighted only within a single calendar year, although some individuals were sighted in up to 5 years. Mean residency time was modelled to be 11·76 days using maximum likelihood methods.

Combined use of leaf size and economics traits allows direct comparison of hydrophyte and terrestrial herbaceous adaptive strategies

BACKGROUND AND AIMS Hydrophytes generally exhibit highly acquisitive leaf economics. However, a range of growth forms is evident, from small, free-floating and rapidly growing Lemniden to large, broad-leaved Nymphaeiden, denoting variability in adaptive strategies. Traits used to classify adaptive strategies in terrestrial species, such as canopy height, are not applicable to hydrophytes. We hypothesize that hydrophyte leaf size traits and economics exhibit sufficient overlap with terrestrial species to allow a common classification of plant functional types, sensu Grimes CSR theory. METHODS Leaf morpho-functional traits were measured for 61 species from 47 water bodies in lowland continental, sub-alpine and alpine bioclimatic zones in southern Europe and compared against the full leaf economics spectrum and leaf size range of terrestrial herbs, and between hydrophyte growth forms. KEY RESULTS Hydrophytes differed in the ranges and mean values of traits compared with herbs, but principal components analysis (PCA) demonstrated that both groups shared axes of trait variability: PCA1 encompassed size variation (area and mass), and PCA2 ranged from relatively dense, carbon-rich leaves to nitrogen-rich leaves of high specific leaf area (SLA). Most growth forms exhibited trait syndromes directly equivalent to herbs classified as R adapted, although Nymphaeiden ranged between C and SR adaptation. CONCLUSIONS Our findings support the hypothesis that hydrophyte adaptive strategy variation reflects fundamental trade-offs in economics and size that govern all plants, and that hydrophyte adaptive strategies can be directly compared with terrestrial species by combining leaf economics and size traits.

Laser photogrammetry improves size and demographic estimates for whale sharks.

Whale sharks Rhincodon typus are globally threatened, but a lack of biological and demographic information hampers an accurate assessment of their vulnerability to further decline or capacity to recover. We used laser photogrammetry at two aggregation sites to obtain more accurate size estimates of free-swimming whale sharks compared to visual estimates, allowing improved estimates of biological parameters. Individual whale sharks ranged from 432–917 cm total length (TL) (mean ± SD = 673 ± 118.8 cm, N = 122) in southern Mozambique and from 420–990 cm TL (mean ± SD = 641 ± 133 cm, N = 46) in Tanzania. By combining measurements of stranded individuals with photogrammetry measurements of free-swimming sharks, we calculated length at 50% maturity for males in Mozambique at 916 cm TL. Repeat measurements of individual whale sharks measured over periods from 347–1,068 days yielded implausible growth rates, suggesting that the growth increment over this period was not large enough to be detected using laser photogrammetry, and that the method is best applied to estimating growth rates over longer (decadal) time periods. The sex ratio of both populations was biased towards males (74% in Mozambique, 89% in Tanzania), the majority of which were immature (98% in Mozambique, 94% in Tanzania). The population structure for these two aggregations was similar to most other documented whale shark aggregations around the world. Information on small (<400 cm) whale sharks, mature individuals, and females in this region is lacking, but necessary to inform conservation initiatives for this globally threatened species.

How well do seed production traits correlate with leaf traits, whole-plant traits and plant ecological strategies?

AbstractThe principal axes of variation in plant function include the economics spectrum and size variation, both of which are implicated in primary ecological strategies. However, it is unclear to what extent vegetative traits and primary strategies correlate with reproductive traits, particularly for seed production. Fifteen traits, including whole-plant, leaf and seed traits (mass, number, total mass of seeds, volume and variance), were measured for 371 species from a range of habitats in Italy. Classification of Grime’s competitor, stress-tolerator, ruderal (CSR) strategies was applied from leaf area, leaf dry matter content and specific leaf area data. Relationships between vegetative traits, CSR values and seed traits were determined using principal components analysis (PCA) and Pearson’s correlation coefficients. PCA1 was an axis of economics, significantly correlated (positively) with leaf carbon concentration and S-selection, and (negatively) with leaf nitrogen concentration, flowering period and R-selection, but not seed traits. PCA2 was a plant size axis, significantly positively correlated with canopy height, leaf mass, C-selection and to a lesser extent seed size traits and total mass of seeds. PCA3 was a specific seed size-seed output axis, correlated positively with seed mass and volume, and negatively with seed number and variance. The loading of seed production traits on a general plant size axis alongside C-selection demonstrates that seed production traits are integral to CSR strategies. However, the stronger contribution of seed traits to a specific axis of variability is suggestive of reproductive variability beyond the CSR strategy, as predicted by the twin-filter model.