Stomatal density responses to global environmental change

Beerling D. J., Woodward F. I. (1996)

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Advances in Bioclimatology 4 – https://doi.org/10.1007/978-3-642-61132-2_4 –

https://link.springer.com/chapter/10.1007/978-3-642-61132-2_4#citeas

Abstract

The CO₂concentration of the Earth’s atmosphere is steadily increasing as a result of anthropogenic activities such as the combustion of fossil fuels and tropical deforestation which release stored carbon from terrestrial sinks.

This accumulation of CO₂in the atmosphere is the one fact in the global climate change debate upon which all scientists agree (Houghton et al. 1990), whereas the major uncertainties in the debate lie in predicting and observing the effects of this rise in CO₂and other greenhouse gases on global climate.

A reduced order model (ROM) that derives Ca from a single equation incorporating the stomatal data

A reduced order model to analytically infer atmospheric CO2 concentration from stomatal and climate data

Konrad W., Katul G., Roth-Nebelsick A., Grein M. (2017)

Wilfried Konrad, Gabriel Katul, Anita Roth-Nebelsick, Michaela Grein,

^a Department of Geosciences, Faculty of Science, University of Tübingen, Hölderlinstrasse 12, D-72074 Tübingen, Germany

^b Technical University of Dresden, Institute of Botany, Zellescher Weg 20b, Dresden D-01062, Germany

^c Nicholas School of the Environment, Box 90328, Duke University, Durham, NC 27708-0328, U.S.A

^d State Museum of Natural History Stuttgart, Rosenstein 1, Stuttgart D-70191, Germany

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Advances in Water Resources 104: 145-157 – ISSN 0309-1708 – https://doi.org/10.1016/j.advwatres.2017.03.018 –

https://www.sciencedirect.com/science/article/pii/S0309170816305024

Highlights

• Proxy methods for CO₂ reconstruction are central to paleoclimate studies.

• Empirical correlations between CO₂ and stomatal density are routinely employed.

• Leaf-gas exchange theories offer alternatives but parameters unconstrained.

• Constraints imposed with additional carbon isotope composition measurements.

• Closed form analytical expression are derived for operational use.

Abstract:

To address questions related to the acceleration or deceleration of the global hydrological cycle or links between the carbon and water cycles over land, reliable data for past climatic conditions based on proxies are required. In particular, the reconstruction of palaeoatmospheric CO2 content (Ca) is needed to assist the separation of natural from anthropogenic Ca variability and to explore phase relations between Ca and air temperature Ta time series. Both Ta and Ca are needed to fingerprint anthropogenic signatures in vapor pressure deficit, a major driver used to explain acceleration or deceleration phases in the global hydrological cycle.

Current approaches to Ca reconstruction rely on a robust inverse correlation between measured stomatal density in leaves (ν) of many plant taxa and Ca. There are two methods that exploit this correlation: The first uses calibration curves obtained from extant species assumed to represent the fossil taxa, thereby restricting the suitable taxa to those existing today. The second is a hybrid eco-hydrological/physiological approach that determines Ca with the aid of systems of equations based on quasi-instantaneous leaf-gas exchange theories and fossil stomatal data collected along with other measured leaf anatomical traits and parameters.

In this contribution, a reduced order model (ROM) is proposed that derives Ca from a single equation incorporating the aforementioned stomatal data, basic climate (e.g. temperature), estimated biochemical parameters of assimilation and isotope data. The usage of the ROM is then illustrated by applying it to isotopic and anatomical measurements from three extant species. The ROM derivation is based on a balance between the biochemical demand and atmospheric supply of CO2 that leads to an explicit expression linking stomatal conductance to internal CO2 concentration (Ci) and Ca.

The resulting expression of stomatal conductance from the carbon economy of the leaf is then equated to another expression derived from water vapor gas diffusion that includes anatomical traits. When combined with isotopic measurements for long-term Ci/Ca, Ca can be analytically determined and is interpreted as the time-averaged Ca that existed over the life-span of the leaf.

Key advantages of the proposed ROM are:

1) the usage of isotopic data provides constraints on the reconstructed atmospheric CO2 concentration from ν,

2) the analytical form of this approach permits direct links between parameter uncertainties and reconstructed Ca, and

3) the time-scale mismatch between the application of instantaneous leaf-gas exchange expressions constrained with longer-term isotopic data is reconciled through averaging rules and sensitivity analysis. The latter point was rarely considered in prior reconstruction studies that combined models of leaf-gas exchange and isotopic data to reconstruct Ca from ν.

The proposed ROM is not without its limitations given the need to a priori assume a parameter related to the control on photosynthetic rate. The work here further explores immanent constraints for the aforementioned photosynthetic parameter.

Stomatal density falls as CO2 levels increase

Stomatal density responses of Egyptian Olea europea L. leaves to CO2 change since 1327 BC

Beerling D. J., Chaloner W. G. (1993)

David J. Beerling, William G. Chaloner,

Annals of Botany 71: 431-435 – https://doi.org/10.1006/anbo.1993.1056 –

https://www.sciencedirect.com/science/article/abs/pii/S0305736483710565

Abstract

We have attempted to separate the effects of CO₂ and temperature change on stomatal density by examining ancient leaf material of Olea europaea L. The distribution of this species is confined to a Mediterranean type climate, so that O. europaea leaves of different ages will have formed under similar temperatures but different CO₂ levels over the last 3000 years.

Stomatal density measurements have been made upon leaves of O. europaea originating from King Tutankhamun’s tomb dating from 1327 BC, and have been compared with values obtained from Egyptian O. europaea material dating from pre-332 BC, 1818 and 1978 AD. Together, the four dates provide a record of how the plant has responded to increases in atmospheric CO₂ concentration during that time.

The results demonstrate that in accordance with similar studies examining the stomatal density response of plants over three time scales (hundreds, thousands and tens of thousands of years) stomatal density falls as CO₂ levels increase. Since we have examined a natural system with leaves developing under similar environmental temperatures the results confirm observations from experimental studies in which plants were grown under the same temperature but different CO₂ regimes.

The influence of temperature, rainfall and CO2 on stomatal traits of modern and fossil leaves

A comparison of stomatal traits between contemporary and fossil leaves of Melaleuca quinquenervia: Do they reflect climate variation?

Hill K. E., Barr C., Tibby J., Hill R. S., Watling J. R. (2019)

Kathryn E. Hill^a, Cameron Barr^b, John Tibby^b, Robert S. Hill^ac, Jennifer R. Watling^ad,

^a School of Biological Sciences, The University of Adelaide, SA 5005, Australia

^b Department of Geography, Environment and Population, The University of Adelaide, SA 5005, Australia

^c South Australian Museum, North Terrace, Adelaide, SA 5000, Australia

^d Manchester Metropolitan University, All Saints Building, Manchester M15 6BH, UK

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Review of Palaeobotany and Palynology 271: 104109 – ISSN 0034-6667 – https://doi.org/10.1016/j.revpalbo.2019.104109 –

https://www.sciencedirect.com/science/article/pii/S0034666719300211

Highlights

• Modern and subfossil leaves of the same species are analyzed for stomatal variation.

• Stomatal measurements were higher and lower than the modern range.

• No effect of climate has been detected on modern stomatal traits.

• Stomatal size is a plastic trait of Melaleuca quinquenervia.

Abstract:

Stomatal traits have been shown to vary in predictable ways in response to environmental change in many plant species. As a consequence, stomatal traits in fossil leaves are sometimes used as proxies for past CO2 and climate.

Here we investigate the influence of temperature, rainfall and CO2 on stomatal traits in plant cuticle fine details of Melaleuca quinquenervia. We use both modern and fossil leaves deposited over the last c. 7500 years to evaluate the effect of CO2, and modern leaves for climate variables.

We found a significant negative relationship between stomatal size and density across both modern and fossil leaves of M. quinquenervia. However, we were unable to find any relationship between stomatal traits and CO2 across a range from 260 to 380 ppm. We were unable to find any robust relationships between stomatal traits and either evaporation or temperature using the modern dataset. Apogeotropic roots account for the lack of stomatal anatomy response to evaporation in sites that experiences inundation.

We conclude that stomatal size is a highly plastic trait in this species and changes do not necessarily reflect functional changes in the leaves.

Stomatal density changes under different CO2 and temperature conditions through the Quaternary

The impact of atmospheric CO2 and temperature change on stomatal density; observations from Quercus robur lammas leaves

Beerling D. J., Chaloner W. G. (1993)

David J. Beerling,William G. Chaloner,

Environmental Research Centre, Department of Geography, University of Durham, Science Laboratories, South Road, Durham DH1 3LE and Department of Biology, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK

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Annals of Botany 71: 231-235 – https://doi.org/10.1006/anbo.1993.1029 –

https://www.sciencedirect.com/science/article/abs/pii/S0305736483710292

Abstract

A comparative study of leaves formed on shoots during the spring and summer (lammas) of Quercus robur from three contrasting geographical locations (Cardiff, Durham and London) gives a measure of the effect of temperature on stomatal density. This is of value in attempting to distinguish the effects of CO₂ and temperature on observed stomatal density changes under different CO₂ and temperature conditions through the Quaternary.. These leaves of normal and lammas shoots will have developed under similar CO₂ levels but different environmental temperatures.

Our results demonstrate that leaves formed under the warmer summer temperatures had reduced stomatal densities and indices from all sites, compared with their spring counterparts. This trend was also detected from measurements of spring and summer leaves made upon herbarium material collected from the same tree in 1840. The results suggest that for Q. robur temperature overrides the influence of irradiance intensity and small seasonal (⩽ 10 ppmv) variations of CO₂ concentration in determining stomatal density.

In accordance with previous work we have also documented a decline in stomatal density since 1840 by examining herbarium leaf material in response to the rising atmospheric CO₂ concentration determined from ice core studies. In conclusion, if we are to understand changes in stomatal density as a response to CO₂ linked temperature changes (the ‘greenhouse effect’) it is important to distinguish the effects of these two environmental parameters on plants.

CO2 changes reconstructed from the stomatal density record of fossil leaves

Rapid lateglacial atmospheric CO2 changes reconstructed from the stomatal density
record of fossil leaves

Beerling D. J., Birks H. H., Woodward F. I., (1995)

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Journal of Quaternary Science 10: 379–384 – ISSN 0267-8179 –

file:///C:/Users/wille/Downloads/Rapid_late_glacial_atmospheric_CO2_chang.pdf

The stomata of ALETHOPTERIS SULLIVANTII and NEUROPTERIS SCHEUCHZERI are actinocytic-haplocheilic similar to those found in various modern cycads and conifers

STOMATAL STRUCTURE OF ALETHOPTERIS SULLIVANTII AND NEUROPTERIS SCHEUCHZERI, PENNSYLVANIAN PTERIDOSPERM FOLIAGE

Reihman M. A., Schabilion J. T. (1985)

American Journal of Botany 72(9): 1392-1396 – https://doi.org/10.1002/j.1537-2197.1985.tb08396.x –

https://bsapubs.onlinelibrary.wiley.com/doi/10.1002/j.1537-2197.1985.tb08396.x

Abstract

The stomatal apparati of the pteridosperm foliage taxa Alethopteris sullivantii (Lesquereux) Schimper and Neuropteris scheuchzeri (Hoffman) forma decipiens (Lesquereux) Gastaldo were examined from Middle Pennsylvanian coal balls collected from central Iowa.

Standard light optics, Nomarski, and SEM were utilized to study cellulose acetate peels and macerated cuticle material. The stomatal apparati of both taxa are actinocytic-haplocheilic and are similar to those found in various modern cycads and conifers. The previous report by Stidd and Stidd of paracytic-syndetocheilic stomata in A. sullivantii resulted from misinterpretation of the guard cell’s configuration and differentially thickened walls.

Stomata in fossil Syzygium (Myrtaceae)

FIGURE 3. Different stomatal morphologies across subgenera in Syzygium Gaertn. (A) Paracytic stomata in Syzygium branderhorstii Lauterb. (subgenus Syzygium), with large double-lid-cell in center (scale bar = 20 μm). (B) Paracytic stomata in Syzygium paniculatum Gaertn. (subgenus Syzygium), with highly sinuous epidermal cells and a double-lid-cell on the right (scale bar = 40 μm). (C) Anisocytic and cyclostaurocytic stomata in Syzygium claviflorum (Roxb.) Wall. Ex A.M.Cowan & Cowan (subgenus Perikion) with large double-lid-cell in center-right (scale bar = 40 μm). (D) Paracytic, anisocytic, and occasionally staurocytic stomata in Syzygium suborbiculare (Benth.) T.G.Hartley & L.M.Perry (subgenus Syzygium) with double-lid-cell at the bottomcenter (scale bar = 40 μm). (E) Cyclostaurocytic stomata on the cuticle of Syzygium hemilamprum (F.Muell.) Craven & Biffin (subgenus Acmena) (scale bar = 50 μm). (F) Cyclostaurocytic stomata in Syzygium smithii (Poir.) Nied. (subgenus Acmena); note the ring-like arrangement of subsidiary cells with straighter edges than the surrounding epidermal cells (scale bar = 40 μm).

Identifying fossil Myrtaceae leaves: the first described fossils of Syzygium from Australia

Tarran M., Wilson P. G., Paull R., Biffin E., Hill R. S.(2018)

Myall Tarran, Peter G. Wilson, Rosemary Paull, Ed Biffin, Robert S. Hill,

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American Journal of Botany: 105(10) – DOI: 10.1002/ajb2.1163 –

https://www.researchgate.net/publication/328024004_Identifying_fossil_Myrtaceae_leaves_the_first_described_fossils_of_Syzygium_from_Australia

FIGURE 4. General features of fossil and extant cuticles. (A) Light micrograph (LM) of adaxial cuticle from K707, holotype of Syzygium christophelii sp. nov. Mid-center-right is an oil gland. Lidcells are distinguished from hair bases in that they have at least one, usually two or more, cells in the middle of a large ring of subsidiary cells; in contrast, a hair base extends over a smaller ring of radially arranged cells that form a “star-like” pattern in their center (scale bar = 50 μm). (B) LM of abaxial cuticle of Syzygium christophelii, specimen K757; note the random orientation of stomata, damage to cuticle, and lack of recognizable hair-base structures (scale bar = 100 μm). (C) LM of the adaxial cuticle of Syzygium smithii (Poir.) Nied (subgenus Acmena), with a lid-cell structure in the top right. Again, note the absence of recognizable hair-base structures (scale bar = 50 μm). (D) LM of abaxial cuticle of S. smithii showing stomatal surface, again noting the random orientation of stomata, sinuous epidermal cell walls, and absence of recognizable hair-base structures (scale bar = 100 μm). (E) LM of adaxial cuticle of Eugenia reinwardtiana (Blume) A.Cunn. ex DC. (Tribe Myrteae), Australia’s only endemic species of Eugenia, showing regular trichome bases, with distinctive “star-like” underlying epidermal cell morphology (scale bar = 50 μm). (F) LM of cuticle of extant species of Backhousia citriodora F.Muell. showing dense trichomes and stomata on the abaxial cuticle surface. Note elongated epidermal cells in non-stomatiferous area, probably indicating an underlying vein. Note also two different sizes of hair bases, with larger ones occurring in the non-stomatiferous zones overlying the vein (scale bar = 50 μm).

Abstract and figures

Premise of the Study

Although leaves of Myrtaceae are easily identified to family level, very few studies have convincingly identified fossil Myrtaceae leaves to living genera. We used a broadly comparative approach with a large data set of extant taxa to confidently assign the mummified remains of myrtaceous leaves from early Miocene sediments at Kiandra (New South Wales, Australia) to a living genus.

Methods

Fossils were identified using a nearest living relative approach, against a database of 232 extant broadleaf rainforest species of Myrtaceae. Leaf cuticles were prepared from 106 species, sourced from herbarium specimens as well as some living individuals, and a further 127 records were assembled from the literature. A set of simple but phylogenetically informative cuticular characters were observed, described, and recorded under both scanning electron microscopy and standard light microscopy.

FIGURE 5. Cuticle damage in the form of cork warts. (A) Light micrograph (LM) of the abaxial cuticle of fossil holotype specimen K707, showing a section of extreme cuticle damage. In the top right corner of the image, a large number of stomata have been damaged by possible fungal or insect attack, and formed stomatal cork warts (scale bar = 100 μm). (B) LM of more damage on the abaxial cuticle of K707 showing a large cork wart in the middle-top-left, with smaller damage marks surrounding (scale bar = 100 μm). (C) LM of adaxial cuticle of extant species Syzygium anisatum (Vickery) Craven & Biffin, showing large-and small-scale damage, which disturbs the otherwise consistent patterns of the epidermal cell impressions on the adaxial cuticle (scale bar = 100 μm). (D) LM of cork wart on the adaxial cuticle of extant species Syzygium paniculatum Gaertn., and a lid-cell to the left. These are the only structures other than epidermal cells commonly visible on the adaxial cuticles of extant Syzygium species (scale bar = 50 μm).

Key Results

A new fossil species of Syzygium Gaertn. is described from mummified remains found in early Miocene (21.5–21.7 Ma) sediments. The fossil taxon is here named Syzygium christophelii sp. nov., in honor of the late Australian paleobotanist David Christophel.

Conclusions

These fossils represent some of the most confidently described Myrtaceae leaf fossils published to date and are the first and oldest described fossil record of Syzygium from Australia. While several fossil parataxa have been illustrated from New Zealand, and several fossil species of Syzygium have previously been proposed in the literature, many of these fossils lack characters for a confident diagnosis.

FIGURE 6. Cyclostaurocytic stomata on fossil taxa. (A) Scanning electron micrograph (SEM) of fossil Holotype K707 showing the underside of the abaxial cuticle and the internal impression of several stomata and epidermal cells (scale bar = 20 μm). (B) SEM of a single stomate showing the arrangement of four subsidiary cells around the guard cells of the stomate (scale bar = 10 μm). (C) Light micrograph (LM) of abaxial cuticle of K707, showing stomatal arrangement and a doublelid-cell at center left (scale bar = 50 μm). (D) LM close-up view of abaxial cuticle of K707 showing subsidiary cell arrangements of three stomata, with four or more subsidiary cells in a ring around the guard cells (scale bar = 20 μm). (E) LM of parataxon “CUT-M-DIE” taken from Pole et al. ‘s (2008) study of Miocene New Zealand fossil Myrtaceae cuticles, compared most favorably with species from Syzygium subgenus Acmena, showing what they called “tangenticytic” stomatal complexes, which we find to be synonymous with the “cyclostaurocytic” stomatal definition proposed by Soh and Parnell (2011) (original scale bar included = 50 μm). (F) LM close-up view of subsidiary cell arrangement of stomate on abaxial cuticle of parataxon “CUT-M-DIE” taken from Pole et al. ‘s (2008) study of Miocene New Zealand fossil Myrtaceae, showing the four or more subsidiary cells in a band around the guard cells (original scale bar included = 20 μm).

Stomata in fossil Laurelia (Atherospermataceae)

Fig. 3. Laurelia otagoensis leaf epidermal cuticles and fruits. A, OU32328, adaxial epidermis. B, OU32680, abaxial epidermis showingdifferentiated laterocytic to staurocytic subsidiary cells. C, OU32328, abaxial surface showing stomate and thickened trichome base. D, OU32412,abaxial surface with almost dicyclic staurocytic stomate, polar t-pieces and polar rods.

Fruits and leaves with cuticle of Laurelia otagoensis sp. nov. (Atherospermataceae) from the early Miocene of Otago (New Zealand)

Conran J. G., Bannister J. M., Lee D. E. (2013)

John G. Conran, Jennifer M. Bannister, Daphne E. Lee,

Alcheringa 37: 496–509 – ISSN 0311-5518 – https://doi.org/10.1080/03115518.2013.798765 –

https://www.tandfonline.com/doi/abs/10.1080/03115518.2013.798765

Fig. 5. Extant Atherospermataceae leaf and fruit characteristics. A, Doryphora sassafras Endl., pseudocarps formed by the urceolate hypanthium.B, Atherosperma moschatum Labill., mature pseudocarp releasing plumose achenes. C–H, Laurelia novae-zelandiae A. Cunn. C, Cleared leafshowing festooned semicraspedodromous venation and gland-tipped marginal teeth. D, Heavily thickened trichome base. E, Cleared leaf showingvenation. F, Plumose achene. G, Adaxial epidermis with hypodermis. H, Abaxial epidermis with stomata. I–L, Laurelia sempervirens (Ruiz &Pav.) Tul. I, Cleared leaf showing venation. J, Plumose achene. K, Adaxial epidermis. L, Abaxial epidermis with stoma and striated subsidiarycells. M–P, Laureliopsis philippiana (Looser) Schodde. M, Cleared leaf showing venation. N, Plumose achene. O, Adaxial epidermis with oilgland. P, Abaxial epidermis with stomata and striated subsidiary cells. Vouchers listed in Table 1. Scale bars for A–B, E, I, M = 10 mm; C, F, J, N= 5 mm; D, G–H, K–L, O–P = 50 μm.

Abstract

Laurelia otagoensis sp. nov. Conran, Bannister & D.E. Lee (Laurales: Atherospermataceae) is described from the earliest Miocene Foulden Maar diatomite deposit, Otago, New Zealand.

The new species is represented by mummified fossil leaves with well-preserved cuticle and associated clusters of achenes bearing persistent, long plumose styles. This basal angiosperm family is of significance because of its classic southern disjunctions and ecological importance in extant Gondwana-type rainforests, but has a very sparse fossil record.

The present study describes one of very few convincing leaf fossils for Atherospermataceae and the only definitive fossil fruits. The presence of fossil Laurelia in Oligo–Miocene New Zealand combined with fossil leaf impressions from the late Eocene, Miocene dispersed cuticle and pollen from the Oligocene to Holocene shows that the family has had a long history in Cenozoic New Zealand. These new fossils also support palaeoclimatic data suggesting warmer conditions in the earliest Miocene of New Zealand.

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Stomata non-areolate, subsidiary cells more or less differentiated from those of the epidermis, irregularly laterocytic to staurocytic with varying numbers of cells, in some cases bicyclic.

Stomata in fossil monocots

Leaf and inflorescence evidence for near-basal Araceae and an unexpected diversity of other monocots from the late Early Cretaceous of Spain

Sender L. M., Doyle J. D., Upchurch G. R. Jr., Villanueva-Amadoz U., Diez J. B. (2019)
Luis Miguel Sender, James A. Doyle, Garland R. Upchurch Jr, Uxue Villanueva-Amadoz, José B. Diez,

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Journal of Systematic Palaeontology 17(15): 133-1346 – ISSN: 1477-2019 (Print) – 1478-0941 (Online 2018) – https://doi.org/10.1080/14772019.2018.1528999 –

https://www.tandfonline.com/doi/full/10.1080/14772019.2018.1528999

Abstract

Phylogenetic analyses imply that monocots were a key group in the early radiation of angiosperms, yet they are much rarer than other major clades in the Early Cretaceous macrofossil record.

Here we describe a well-preserved leaf and several inflorescences related to the near-basal monocot family Araceae and abundant monocot leaves of uncertain affinities from two latest Albian localities in north-eastern Spain. Orontiophyllum ferreri sp. nov. has a multistranded midrib, several orders of parallel-pinnate veins, two orders of transverse veins, and paracytic-oblique stomata. This suite of characters (but with both anomocytic and paracytic-oblique stomata) is characteristic today of Orontium in the near-basal araceous subfamily Orontioideae, and later Cretaceous and early Cenozoic leaves assigned to Orontiophyllum have similar architecture.

Sedimentology and anatomy suggest a (semi)aquatic ecology. Other monocot leaves at the same locality are linear and parallel-veined but have similar stomata. Although anomocytic stomata have been proposed as ancestral in monocots, O. ferreri, the associated linear leaves, Albian–Cenomanian cuticles from Australia and Portugal, and extant data are consistent with the hypothesis that variable paracytic-oblique stomata are ancestral. 

Turolospadix bogneri gen. et sp. nov., from the other locality, includes spadices of ebracteate flowers with four tepals, a central gynoecium, and a long stipe (vs a spathe attached just below the fertile zone as in most Araceae). Phylogenetic analyses indicate that the character combinations seen in O. ferreri and T. bogneri are ancestral for Araceae, and they could be either sister to Araceae or nested within a basal grade of the family. Together with fossils from the Aptian–Albian of Brazil and Portugal, the Spanish fossils indicate that Araceae are among the oldest extant monocot families, but they were associated with diverse linear-leaved monocots of uncertain affinities.