Changes in Stomatal Density over Time (1769–2015) in the

Pacific Science (2017), vol. 71, no. 3:319 – 328 doi:10.2984/71.3.6 © 2017 by University of Hawai‘i Press All rights reserved

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A link between levels of atmospheric car-bon dioxide (CO2) and plant stomatal density and /or stomatal index has previously been es-tablished through a comparison of the stoma-tal density of historical herbarium specimens and modern specimens of the same species. In addition, controlled CO2 enrichment studies of living plants have found that increasing CO2 decreases stomatal density ( Woodward 1987, Woodward and Kelly 1995, Kouwen-berg et al. 2003, Haworth et al. 2010). This relationship between stomatal density and at-mospheric CO2 concentration has been used to extrapolate backwards to include the use of fossil material in establishing a link to past cli-mate changes (see Royer 2001, Jordan 2011). In the Holocene period, up to about 1800, the atmospheric CO2 level rarely exceeded

280 ppm (Barnola et al. 1987, Siegenthaler and Sarmiento 1993), steadily climbing to 390 ppm ( IPCC 2013), and now extending beyond 400 ppm ( NOAA 2015).

The control and initiation of leaf stomata in response to environmental stimuli, in par-ticular varying atmospheric concentration of CO2, is complex and may vary between plant groups (Doi et al. 2006, Doi and Shimazaki 2008, Brodribb et al. 2009, Haworth et al. 2010, Brodribb and McAdam 2011, Chater et al. 2011, McAdam et al. 2011, Ruszala et al. 2011, McAdam and Brodribb 2012, Haworth et al. 2013; see also Hill, Guerin et al. 2014, and Hill, Hill, and Watling 2014). A more de-tailed mechanistic treatment of the stomatal control system is discussed by Buckley et al. (2003) and Franks (2004). In addition, it has been suggested that the formation of stomata may also be linked to levels of atmospheric oxygen (O2) (Miziorko and Llorimer 1983), with stomatal initiation affected through changes in the photosynthetic availability of CO2 expressed by the atmospheric CO2 : O2 ratio (Beerling and Woodward 1997, Beerling et al. 1998; see also Haworth et al. 2013). Plant species may also be genetically passive or active with regard to the mechanisms of stomatal control; those with the former (passive system) being more likely to exhibit reductions in stomatal density when grown in

Changes in Stomatal Density over Time (1769 – 2015) in the New Zealand Endemic Tree Corynocarpus laevigatus

J. R. Forst. & G. Forst. (Corynocarpaceae)1

M. F. Large,2,4 H. R. Nessia,2 E. K. Cameron,3 and D. J. Blanchon 2

Abstract: In the Northern Hemisphere several studies have used historic her-barium specimens to examine change in stomatal density over time as related to changes in atmospheric CO2 concentration. In this study we compared stoma-tal density of leaves of the New Zealand endemic tree Corynocarpus laevigatus ( karaka), collected by Banks and Solander on Cook’s first voyage to the South Pacific in 1769 – 1770 with nineteenth-, twentieth-, and twenty-first-century material of the same species. Historical eighteenth- and nineteenth-century herbarium specimens were found to have a significantly higher stomatal density than that seen in twentieth- and twenty-first-century material. Our data are consistent with there being a relationship between stomatal density in leaves of C. laevigatus and atmospheric CO2 concentration over time. To date it is unclear whether other New Zealand native tree species show a similar relationship.

1 Manuscript accepted 29 November 2016.2 Department of Natural Sciences, Unitec Institute of

Technology, Private Bag 92025, Auckland, New Zealand.3 The Herbarium, Tamaki Paenga Hira, Auckland

War Memorial Museum, Private Bag 92018, Auckland, New Zealand.

4 Corresponding author (e-mail: [email protected]).

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atmospheres of elevated CO2 ( Haworth et al. 2011, Haworth et al. 2013). For a detailed summary of the possible control mechanisms and their physiological basis, see Drake et al. (1997), Jarvis et al. (1999), and Haworth et al. (2013).

The first study to compare historic and modern specimens of the same plant species ( Woodward 1987) examined 240-yr-old spec-imens of seven temperate tree and one shrub species from the University of Cambridge collection. When the historic material was compared with modern representatives of the same species, a reduction in stomatal density of up to 40% was noted. This corresponded with a 21% increase in atmospheric CO2 ( Woodward 1987). Subsequently, several studies of a number of angiosperm and gym-nosperm taxa have demonstrated a decline in stomatal density and /or stomatal index over decades or centuries (e.g., Beerling and Chaloner 1993, Bettarini et al. 1998, Haworth et al. 2010).

To date, most investigations have focused on the Northern Hemisphere. Only one study (Greenwood et al. 2003) investigated these ef-fects in the Southern Hemisphere, comparing specimens of a Queensland tree collected be-tween 1899 and 1988. This is likely to be due to the limited availability of old Southern Hemisphere collections in comparison to the historic herbarium col lections of the North-ern Hemisphere. The earliest examples of scientifically collected Southern Hemisphere (vascular) plant specimens date from the eighteenth-century voyages of exploration.

The first collections were by Joseph Banks and Daniel Solander, who accompa-nied Cook on his first voyage to New Zealand in 1769 – 1770. In 1828 this material went to the British Museum. Two duplicate sets, each of about 200 species, are now held by Auck-land War Memorial Museum Tamaki Paenga Hira, and the Museum of New Zealand Te Papa Tongarewa, Wellington (Oliver 1950). More recently further Banks and Solander material was gifted to New Zealand herbaria from the British Museum, bringing the pres-ent New Zealand total to 313 vascular species comprising over 1,188 sheets at Auckland

Museum, Te Papa, and Allan Herbarium at Lincoln (Brownsey 2012).

To investigate whether a similar link over an identical time period could be made be-tween stomatal density and CO2 concentra-tion in the Southern Hemisphere, we assessed the oldest herbarium material of Corynocarpus laevigatus J. R. Forst. & G. Forst. ( karaka) available (1769 – 1770) and compared this with modern material of the same species.

materials and methods

Methods for Examining Stomata: Agarose Gel Cast

A simple hard cast made from nail varnish has been used in past studies (Miller-Rushing et al. 2009) to make a surface cast of leaf fea-tures such as stomata. However, due to the fragile condition and historical significance of the Banks and Solander specimens, this method was deemed to be too harsh and liable to cause surface tearing or loss of hairs when peeled from the leaf. Likewise the cuticle preparation technique involving acid dissolu-tion of leaf cellular material (Greenwood et al. 2003) was regarded as too destructive for use on the historic collections. In this study a new technique using 10% agarose gel was de-veloped to make a cast of the leaf surface. An example cast taken from a recent herbarium specimen can be seen in Figure 1.

To explore whether the techniques might produce differing density data, a comparison study of both nail-varnish hard casts and aga-rose casts (10% agarose in distilled water, heated until clear, and cooled to ca. 50°C) was undertaken. Modern fresh and dried Corynocarpus laevigatus leaf material was used.

Surface peels from the underside of the same leaf were made using either nail varnish or agarose (the leaves of this species are hypo-stomatous). The agarose gel or nail varnish were applied to each leaf while still a viscous liquid and allowed to set. The cast was then peeled, and the surface that was in contact with the leaf was placed uppermost onto a microscope slide and then observed immedi-ately. Epidermal and guard cells were clearly



Stomatal Density in NZ Corynocarpus · Large et al. 321

visible in agarose casts made from fresh and modern dried material.

It was not possible to clearly see all of the epidermal cells in the historic specimens re-gardless of how these leaves were observed (i.e., by cast or directly). This was true of the Banks and Solander material in particular, so stomatal density (stomata per square milli-meter) was calculated rather than using sto-matal index.

The results for nail varnish density mea-surements (n = 40, range = 173 – 214, mean = 192.8, SD = 11.5) and agarose (n = 40, range = 153 – 214, mean = 191.8, SD = 13.5) were similar. A t test on these data showed no sig-nificant difference between methods (t: 0.364, df = 39, P = .72). Consequently, the agarose cast technique was used throughout this study.

Assessment of Stomatal Variation in Living Plants

A second pilot study was undertaken to assess possible variation in stomatal density in living material of Corynocarpus laevigatus. This in-cluded within-tree variation (including node position on a branch /age of leaf, sun and shade leaves) and between-tree variables (geo-

graphic location). This pilot study also as-sessed dried (herbarium) material and fresh material from the same plants. The results of this study are presented in the Results section.

Examination of Historic Material

Herbarium material collected from New Zea-land earlier than the late nineteenth century is rare. That collected by Joseph Banks and Daniel Solander on Cook’s first voyage on 8 October 1769 and 6 February 1770 represents the earliest material available and is the only material from the nineteenth century. It is thus valuable in terms of historic importance and very limited in quantity.

Initially we investigated all of the New Zealand material collected by Banks and Solander held by the Auckland Museum Her-barium (ak). The majority of material origi-nated from the East Cape region of the North Island of New Zealand (around Tolaga and Anaura Bay) and included 524 sheets repre-senting over 255 vascular plant taxa.

For various reasons (including the fragile nature of the specimens and epidermal condi-tion) we were unable to observe stomata in most of the taxa. One species (Corynocarpus laevigatus, Banks and Solander specimen, AK 103663) ( Figure 2) was chosen for further in-vestigation, based on the intact state of the specimen, size of the leaves, and the presence of readily visible stomata.

It is not certain where this particular specimen was collected. Hatch (1982) in an examination of the unpublished manuscript by Solander (Primitiae Florae Novae Ze-landiae) suggests that Corynocarpus laevigatus was collected from six of the seven landing sites in New Zealand. Three of these were from the East Cape region, and the remaining three from Mercury Bay (Coromandel Penin-sula), Motuaro (Bay of Islands), and Totara-nui (Queen Charlotte Sound).

Two other historic specimens of this spe-cies from the nineteenth century were also available and were included in this study (welt 31914, T. Kirk 1867 Paparoa, Kaipara and welt 31918, W. Petrie 1894, Remuera, Auckland).

Figure 1. Corynocarpus laevigatus leaf epidermal cast taken from the underside of material collected in 2011 ( UNITEC5189). Peel uses 10% agarose gel. Stomata are clearly visible as are some epidermal cells. ( The latter cells were not visible in peels taken from historic mate-rial). Scale = 35 µm.



Recent Herbarium Material

Recent material (twentieth and twenty-first century) from a further 14 specimens was also examined. These specimens were se-lected to represent a wider range of locali-ties and environments and also included samples taken from the same or similar locali-ties as those visited by the eighteenth- and nineteenth-century collectors. A summary of the data obtained from the historic specimens and their modern equivalents is presented in Table 1.

Stomatal Measurements

Given the results of the pilot study, we se-lected five representative leaves from each of the historic and recent herbarium specimens (sample sizes from the historic material were of necessity restricted). Fully expanded leaves from between nodes three and five were taken. Stomata were measured on the abaxial side of each leaf ( leaves are hypostomatous), halfway between the main vein and margin of the leaf, equidistant between the tip and base of the leaf blade.

Allowing for the sample size restrictions mentioned above, the total number of stomata were counted in a field of view at 400× magni-fication using the same microscope (Olympus BH2, BHT 224310) for all observations. A minimum of four fields of view was counted for each leaf examined. These data were con-verted to stomata per square millimeter ( based on the diameter of a field of view at 400× be-ing 0.5 mm).

Statistical Analysis

Some samples were of unequal size due to the very limited availability of the historical herbarium material. Consequently, analysis of variance (ANOVA) and t tests (with equal and unequal sample size) were performed on the data using PAST ( Hammer et al. 2001). Full data sets are available from the authors.

results

Pilot Analysis of Density Variation within Trees

internode position. Stomatal density was measured using the agarose technique. Only mature expanded leaves were taken from each of internodes 3, 4, and 5. The internode samples were then compared using a one-way ANOVA, which indicated density variation between these internodes was not significant at 95% ( F = 0.012; df = 2, 117; P = .99).

shade versus sun leaves. Mature leaves from internode 5 were selected from the same tree. Leaves were from full sun or full shade positions. Stomatal density was measured using the agarose technique.

Figure 2. Corynocarpus laevigatus J. R. Forst. & G. Forst.( karaka) collected by Joseph Banks and Daniel Solander on Cook’s voyage to New Zealand in 1769 – 1770. Labels read: “Ex Herbario Musei Britannici. Corynocarpus laevigata Forst. New Zealand 1769 – 70. Banks & Solander”; AK 103663 Auckland Museum Herbarium, Auckland, New Zealand. Corynocarpaceae. Corynocarpus laevigatus J. R. Forst & G. Forst.




There was little variation in stomatal den-sity between shade leaves (n = 40, range = 122 – 280, mean = 177.8, SD = 31.7) and those from full sun (n = 40, range = 107 – 280, mean = 175.9, SDev = 32.5). A t test on these data in-dicated variation was not significant at 95% (t: 0.284, df = 39, P = .78).

fresh versus dried material. Leaves were taken from the same tree and same in-ternode. Stomatal density was measured us-ing the agarose technique. One set of leaves was dried and mounted as herbarium speci-mens, the other set was measured fresh. Sto-matal densities from fresh leaves (n = 50,

range = 102 – 260, mean = 170.3, SD = 42.5) and dried leaves (n = 50, range = 107 – 260, mean = 174.3, SD = 39.6) were similar. A t test on these data showed variation was not significant at 95% (t: 0.483, df = 39, P = 0.63). Leaf shrinkage that might cause changes in density proved to be negligible.

Pilot Analysis of Density Variation between Trees

geographic variation. Mature leaves from internodes 4 or 5 were selected from trees growing in seven localities including Auckland (Mt. Albert, Birkenhead, Unitec,

TABLE 1

A List of Herbarium Specimens Used in This Study Including Collector and Year of Collection

Locality Collector and YearMean

Density Range SD (n)

16 B&S *East Cape? New Zealand, Banks & Solander, AK103663

J. Banks/ D. Solander

1769 – 1770

315.2 249 – 412 36.4 30

4 Kai *Kaipara, WELT31914 T. Kirk 1867 302.4 285 – 310 9.4 106 Rem *Remuera Auckland,

WELT31918W. Petrie 1894 325.8 290 – 341 17.1 10

2 Kai Otamatea Kaipara, AK125765 R. C. Cooper 1965 232.1 198 – 265 19.8 105 Birk Birkenhead Point Reserve,

Auckland, UNITEC692K. D. Aitken 2003 218.4 152 – 280 36.7 20

1 Kai Muriwai Kaipara, AK283988 E. K. Cameron 2003 200.0 183 – 218 10.5 1013 Hick Hicks Bay N. East Cape,

AK311411P. J. deLange 2010 190.1 153 – 224 18.2 40

14 Ana Anaura Bay S East Cape, AK311460

P. J. deLange 2010 250.4 234 – 290 17.2 15

15 Tol Tolaga Bay S East Cape, AK311462

P. J. deLange 2010 249.4 214 – 290 24.3 15

7 Wai Waiatarua, Scenic Drive, Auckland, UNITEC5205

M. F. Large 2011 220.7 199 – 255 19.7 20

8 Wai Waiatarua, Waitakere estate, Auckland, UNITEC5204

M. F. Large 2011 217.1 178 – 265 21.4 20

9 Wai Waiatarua, Parkinsons lookout, Auckland, UNITEC5203

M. F. Large 2011 187.6 148 – 249 32.4 20

10 MtAlb Mt. Albert, Owairaka Park, Auckland, UNITEC5176

Z. Lin 2011 167.6 107 – 260 40.9 40

11 MtAlb Mt. Albert, Carrington Rd, Auckland, UNITEC5188

R. V. Harris 2011 234.4 183 – 295 35.2 20

12 MtAlb Unitec Campus, Auckland, UNITEC5189

Z. McGrath / O. Colenso

2011 172.8 107 – 255 29.6 40

17 Wel Ngaio, Wellington, UNITEC4714 D. J. Blanchon / P. J. Edmonds

2011 153.7 92 – 204 30.9 60

3 Kai Mataia, Glorit, Kaipara, UNITEC7388

D. J. Blanchon 2015 214.0 193 – 229 12.9 10

Note: Summary statistics for stomatal density (calculated as stomata per mm2) are included as: mean; range; standard deviation; and sample size (n = fields of view). Some sampling was restricted due to limitations of the specimen. Material is ordered oldest to youngest. The eighteenth- and nineteenth-century material is in bold and designated by *. Modern specimens are in roman type.



Waiatarua), East Cape (Anaura Bay, Tolaga Bay), and Wellington. Twenty density mea-surements were made for each specimen using the agarose gel technique. A one-way ANOVA between modern samples indicated that density variation between these samples was significant at 95% (F = 13.17; df = 9, 390; P < .001). Figure 3 presents a visual summary (samples 10, 11, 12 Mt Alb from Mt Albert; 5 Birk from Birkenhead; 14 Ana from Anaura Bay; 15 Tol from Tolaga Bay; 7, 8, 9 Wai from Waiatarua; 17 Wel from Wellington).

old versus recent material. Stoma-tal density within modern material of Corynocarpus laevigatus ranged from 92 to 295 sto-mata per mm2.

For the collected locations (summarized in Table 1) mean stomatal densities ranged from 154 to 252 stomata per square millimeter over 14 specimens. Within the eighteenth-century herbarium material, stomatal density ranged between 249 and 407 with an average of 315 stomata per square millimeter. The nineteenth-century material ranged from 285 to 351 with averages of 302 and 327 stomata per square millimeter.

The eighteenth- and nineteenth-century specimens [Banks and Solander (1769 – 1770), Kirk (1867), and Petrie (1894)] clearly had a higher mean stomatal density than modern specimens of twentieth- and twenty-first-century origin: with a 51% – 21% decrease be-tween eighteenth-century and modern mate-

rial; and a decrease between the nineteenth century and modern material of 53% – 23% (or ca. 48% – 23% if only similar-locality material is considered). See Table 1 for a summary.

Over all, although there was variation within twentieth- and twenty-first-century material, in particular between locations, the degree of variation does not hide the differ-ence between modern and historic material ( Figure 3).

discussion

The finding of a decrease in stomatal density between eighteenth-century and modern ma-terial of Corynocarpus laevigatus is consistent with the findings of similar Northern Hemi-sphere studies (e.g., Woodward 1987, Beer-ling and Chaloner 1993, Bettarini et al. 1998). This study is the first of its kind from New Zealand and represents the earliest record (1769/70) for the Southern Hemisphere.

Our data are consistent with stomatal density in the leaves of Corynocarpus laevigatus being sensitive to atmospheric CO2 concen-tration ( Figure 4).

The finding of similar results in Southern Hemisphere plants as those reported in the Northern Hemisphere is not surprising. De-spite 95% of global fossil-fuel emissions be-ing generated in the Northern Hemisphere, atmospheric CO2 levels have been shown to

Figure 3. “Box and whiskers” plot for Stomatal Density ( y-axis) recorded as number mm−2. X-axis is location aligned with time. (Order is oldest collected material on the left to youngest on the right). Black /gray, eighteenth- and nineteenth-century samples. White, modern twentieth- and twenty-first-century samples. The ends of the whisker are set 1.5*IQR (inter-quantile range) at the upper and lower quartile, above the third quartile, and 1.5*IQR below the first quartile. Outliers are marked by x. The thick, continuous line represents the first quartile of the older herbarium material. The variation seen between geographic locations may be seen in the following: 10, 11, 12 Mt Alb, Mt. Albert; 5 Birk, Birkenhead; 14 Ana, Anaura Bay; 15 Tol, Tolaga Bay; 7 wai, 8 Wai, 9 Wai, Waiatarua; 17 Wel, Wellington.




be only an average of ca. 3 ppm higher than those at southern high latitudes ( Heimann and Keeling 1986, Keeling and Heimann 1986, Tans et al. 1990, Broeckner and Peng 1992; see also Siegenthaler and Sarmiento 1993). Furthermore, it has been estimated that natural preindustrial atmospheric CO2 concentrations were actually slightly higher in the Southern Hemisphere than in the Northern Hemisphere (Keeling and Hei-mann 1986, Taylor and Orr 2000).

Another Southern Hemisphere study (Greenwood et al. 2003) also recorded a de-crease, but in stomatal index. Their data cover a shorter interval from 1899 to 1988 for Queensland collections of the Australian evergreen rain-forest tree Neolitsea dealbata (R. Br.) Merr. (Lauraceae, hairy-leaved bolly gum). These data in addition to the results we present in this paper, suggest that a critical period for change in stomatal density was after the nineteenth century.

It is important to consider other possible explanations for the variation in stomatal den-

sity of Corynocarpus laevigatus, such as genetic variation and polyploidy. The genus Corynocarpus J. R. Forst. & G. Forst. consists of fi ve tree species, distributed through the south-western Pacifi c (Australia, New Guinea, Solo-mon Islands, New Britain, New Ireland, and the Bismarck Archipelago, New Caledonia, Vanuatu to New Zealand). The diploid Corynocarpus laevigatus is the sole representative in New Zealand and is endemic to the main and offshore islands. There is no evidence or likelihood of hybridity (Philipson 1986, Molloy 1990, Dawson 1997, Wagstaff and Dawson 2000).

The natural distribution of Corynocarpus within New Zealand has been confused by human transportation. The plant is of cultural signifi cance to Mäori, being an important food source before European settlement, and is known to have been cultivated and moved by them (Molloy 1990, Leach and Stowe 2005, Atherton et al. 2015). Recent work using the nuclear WAXY and ITS loci has identifi ed slight genetic variation in particular

Figure 4. Stomatal density alongside atmosphere CO2 concentration over time. Data are for the same samples, in the same locality order, as given in Figure 3. Some years are represented by multiple samples from different locations. Median densities [in dark gray (or green)] are as for the Figure 3 box plot. Upper and lower quartiles for these same data are in light gray. CO2 concentration data are from Keeling et al. (2005) and Dlugokencky (2016) adjusted to rep-resent yearly averages. These data are from the earliest measured (1958) to the present and do not include the estimates of ca. 280 ppm (Barnola et al. 1987, Siegenthaler and Sarmiento 1993) for the nineteenth century.

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between the Kermadec Islands and the main-land New Zealand populations, but no signifi-cant variation was noted within the main New Zealand population (Atherton et al. 2015), making it unlikely that genetic variation is the driver for the observed differences in stomatal density. At this stage it is not clear if other members of the New Zealand native flora show similar reactions to rising atmosphere CO2.

acknowledgments

We thank Mary Yan, Odette Rizk, Kerry Everett, Andrew Wooding, Peter Lockhart, Trish McLenachan, Linton Winder, and Richard Winkworth for technical assistance or comments on the manuscript. We thank Te Papa Tongarewa Museum of New Zea-land for loan of herbarium material and the anonymous reviewers for their helpful comments.

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