Journal of Species Research 4(2):159-168, 2015

Morphological characteristics of major airborne pollen in Korea peninsula

Hye-Kyoung Moon1, Min-Jung Kong1, Jun-Ho Song1, Sun-Yu Kim2, Jin-Suk Kim2, Eun-Hee Jung2, Chan-Ho Park2, Byoung-Yoon Lee2 and Suk-Pyo Hong1,*

1Laboratory of Plant Systematics, Department of Biology and Institute of Basic Sciences, Kyung Hee University, Seoul 130-701, Korea 2National Institute of Biological Resources, Plant Resources Division 42 Nanji-ro, Seo-gu, Incheon 404-708, Korea

*Correspondent: [email protected]

Although airborne pollen is invisible to the eye, it has been known as a major source to respiratory aller­ gic reactions. For this reason, airborne pollen is monitoring in many countries to predict pollen concentra­ tion based on locality and season. However, the morphological characteristics of airborne pollen and their potential tendency as an allergen are still obscure. In the present study, we selected 52 airborne pollen­ sam­ ples based on previously reported data and investigated their detail pollen characteristics using LM and SEM. Major airborne pollen in Korea has sorted in 19 families (most angiosperms except four gymnosperm­ families), and all pollen grains are small to medium in size (P=17.34 - 49.86 μm) apart from the bisaccate­ pollen grains of Pinaceae (P=46.49-106.20 μm). The aperture number and shape vary from sulcate to poly­ porate. While the inaperture pollen has found only in gymnosperm (Cupressaceae and Taxaceae), triporate­ or polyporate is common pollen type in angiosperm. The sexine ornamentations could divide into several­ types, but the most sculpturing types are inconspicuous like psilate, rugulate and granulate. Reticulate pol­ len grains as a semitectum have occurred the species of genera Platanus and Fraxinus only. To estimate the possible relationships between pollen features and allergen, the results are discussed in botanical context. Keywords: airborne pollen, botany, morphological features

Ⓒ 2015 National Institute of Biological Resources DOI:10.12651/JSR.2015.4.2.159

among the countries. Certain plants groups like genera Introduction Alnus, Ambrosia, Artemisia, Betula, Humulus, Pinus, and Quercus are well known as airborne pollen in the Airborne pollen has been assessed as the subject of al­ world (Anderson et al., 1978; Mardones et al., 2013). lergy research over the past two decades (Raynor et al., However, Olea europaea is one of the main causes of 1976; Anderson et al., 1978; Irani et al., 2013; Mardones allergy in Mediterranean countries and some areas of et al., 2013). Since the pollinosis has become serious al­ North America (Bousquet et al., 1985; Wheller, 1992) lergic disease, most studies about airborne pollen have and Cryptomeria japonica is the most popular pollinosis been accomplished for the clinical reason. Thus, many in Japan (Wang et al., 2013). Thus, the constant research researches were carried out to monitor and count the air­ of airborne pollen is necessary at the regional range (Puc borne pollen to predict pollen concentration exactly (Jung and Kasprzyk, 2013; Velasco-Jiménez et al., 2013). In and Choi, 2013; Velasco-Jiménez et al., 2013). However, Korea major airborne pollen was captured from 20 to the pollen concentrations are not always related with al­ 30 plants group, in which Pinus, Quercus and Humulus lergen reaction, furthermore the pollinosis is not the spe­ showed high pollen concentration (Oh and Lee, 1997; cies specific response. For example, the pollen grains Oh et al., 2006; Jung and Choi, 2013). In particular, the of Pinus group have rather lower allergenicity in Korea weed plants like Ambrosia and Humulus are focused albeit to high concentration during spring time (Oh and as severe airborne pollen since the patients at autumn Lee, 1997). gradually increased from the year 2,000 in Korea (Oh et In fact, the pollinosis is affected by various biotic and al., 2009). Since the airborne pollen has been observed abiotic factor and the major pollinosis plants are different mainly by light microscope, the identification of plants 160 Journal of Species Research Vol. 4, No. 2 is rather restricted at higher plants group. Thus, we carry Table 1. The character states of main pollinosis plants accord­ out the detail palynological study based on common air­ ing to their growth form in Korea. - The numbers are not exactly matched with species by overlapping counts. borne pollen in Korea to provide the pollen characteris­ tics of airborne pollen which may help to identify plants Gymnosperm Angiosperm at species level, and to figure out the possible link bet­ 12 spp 28 spp (tree) 12 spp (herb) ween morphological features and allergen. Floral sexuality: Hermaphrodite 0 3 5 Unisexual 12 27 7 Materials and Methods Sexual system: Cosexual 10 25 9 To observe morphological characteristics of airborne Dioecious 3 4 3 pollen in Korea, we selected 52 species of 35 genera from Anthersis time: 19 families based on previously reported data (Table 2; March-May 11 28 0 Oh et al., 2006; Mardones et al., 2013). Most materials June-August 0 0 10 were taken from the dried specimen from the following September-November 1 0 6 herbaria: KB, KH, and KHUS (acronyms follow Thiers, Pollination type

2011), and some plants were collected in natural popula­ Abiotic (wind) 12 27 12 tions of Korea by the authors. For pollen measurements Biotic (insect) 0 1 0 (polar axis=P, equatorial diameter=E), all materials were prepared by standard acetolysis method (Erdtman, 1960). The permanent glycerin jelly slides were observed (Table 1). All pollen grains were dispersed as monad under light microscopy (LM, BX41 Laboratory­ Micro­ and the pollen size varied from small to large (P=17.34- scope, Olympus, Melville, USA) and measured the pol­ 106.20 μm; Walker and Doyle, 1975) with peroblate to len size like polar axis, equatorial diameter, and aperture prolate shape (P/E ratio=0.38-1.70). Reasonably, the length using captured images with ×400 or ×1,000 mag­ pollen characteristics could be analyzed according to nifications by a digital camera for microscopes (MDX- their classification. So, here we described detail pollen 30, Shinwoo Optics, Anyang, Korea) and the image ana­ morphological features with following plants categories: lysis software (I-Works Lite, Saramsoft, Anyang, Korea). gymnosperm and angiosperm. For scanning electron microscopic observation, some acetolysed pollen grains were suspended in ethanol, air Gymnosperm dried on a stub and coated with plati­num prior to obser­ In total, 12 species are belong to the gymnosperm. All vation with a field emission scanning electron micro­ species are trees and wind pollinated (Table 1). The com­ scope (FE-SEM, S-4700, Hitachi Ltd., Tokyo,­ Japan) at mon sexual system within gymnosperm is monoecy ex­ an accelerating voltage of 10 kV with 10-13 mm work­ cept dioecious plants of Ginkgo, Juniperus, and Taxus. ing distance. The fragile pollen like gymnosperm­ group The pollen size varied from small to large (P=22.78- was prepared with critical point-dried technique to ob­ 106.20 μm) with peroblate to prolate shape (P/E ratio= serve natural shape and ornamentation of pollen­ using 0.38-1.27). Ginkgo biloba is easy to recognize with boat FE-SEM (Moon et al., 2008; see also Table 1). For cri­ shape and sulcate pollen grains, the family Pinaceae tical point-dried, the collected anthers were rehydrated­ are distinct from other taxa by having bisaccate pollen with Agepon® (Agfa Gevaert, Leverkusen, Germ­any; grains. In fact, the pollen size of gymnosperm other than Agepon wetting agent : distilled water, 1 : 200) before Pinaceae could be interpreted as small to medium (P= dehydrated through an acetone series (in 50%, 70%, 90%, 22.78-38.55 μm). Juniperus chinensis has ulcerate pollen and absolute acetone 30 min in each solution). The com­ grains while other taxa of Cupressaceae have inaperture pletely dehydrated materials were dried with carbon di­ pollen grains (Table 2). The pollen surface ornamenta­ oxide (SPI-13200J-AB) and observed using FE-SEM tion was unnoted but additional projection on the surface after following same steps which described above. could be defined as granulate, verrucate, gemmate, and The pollen terminology follows the online edition of papillate (Fig. 1). the Glossary of Pollen and Spore Terminology (Punt et al., 2007). Angiosperm Dicotyledon: Most airborne pollens (37 taxa, 21 gen­ Results era of 12 families) are included and their major sexual system is monoecious (Table 1). Andromonoecy (male In total 52 taxa out of 19 families were investigated and hermaphrodite flowers in same individual) found August 2015 Moon et al.-Morphology of Korean airborne pollen 161

(KH) (KH) (KH) (KH)

(KH U S)

(KH)

(KH) (KH U S)

(KB)

(KH)

(KH) (KH) (KH)

(KH)

(KH)

(KH)

(KH)

(KH)

KKS100032 KKS100025 KKS10017 KKS100007 KKS100003 s.n. HOH980414 1406 H120915-3 KSO130626-1 KKS100056 SHY2-1854 JSJ110111 , , , (KH U S) L100283 ,

, C100505 , , (KH) KKS100060

Voucher information Voucher s.n. et al. et al. ParkSH80299 ParkSH80238 et al. et al. et al. 80529-175 et al. s.n. et al. Yang Yang Byeon, Hong & Oh, Park, Anonymous, Oh Yang & Kim, Yang Hong, Shin & Lee, Nam (KH U S) Park, Yang & Kim, Yang Lee, Jang Yang & Kim, Yang Lee Yang & Kim, Yang Yang & Kim, Yang Hong Hong Ko, Surface ornamentation psilate - verrucate psilate - verrucate perforate psilate reticulate granulate granulate granulate reticulate rugulate - perforate rugulate granulate - rugulate psilate microgemmate granulate granulate - psilate perforate granulate - verrucate granulate granulate papillate granulate granulate - psilate (6 - 8)

Aperture leptoma leptoma sulcate tricolpate triporate ulcerate tri - tetracolpate leptoma leptoma tetra - heptaporate inaperture leptoma triporate inaperture polyporate tetra - pentaporate inaperture triporate inaperture diporate inaperture P/E ratio - 1.50 1.11 0.38 - 0.70 0.61 - 0.93 0.45 - 0.67 0.94 - 1.43 0.85 - 1.12 0.90 - 1.16 0.65 - 0.91 0.62 - 0.82 0.78 - 1.08 0.94 - 1.07 0.55 - 0.93 0.97 - 1.15 0.93 - 1.16 1.09 - 1.40 0.71 - 1.32 0.95 - 1.14 0.87 - 1.26 0.97 - 1.27 1.00 - 1.32 0.94 - 1.24 3.41 4.15 1.55 2.87 3.21 11.36 7.45 1.60 2.57 8.72 1.78 1.54 1.18 4.64 1.92 2.62 2.12 2.78 0.73 2.62 16.33 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 111.42 70.38 42.69 19.05 20.73 30.87 127.20 64.40

24.02 27.76 75.01 30.97 29.54 14.25 38.59 36.03 23.95 20.98 35.27 19.39 22.64 Equatorial diameter 5.35 1.74 1.39 2.08 3.42 17.52 9.11 8.32 2.07 2.28 5.15 1.86 1.80 1.44 4.42 1.49 2.56 1.90 2.55 1.22 81.39 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± Polar axis 57.30 22.78 21.73 21.35 31.60 106.20 61.06 46.49 22.07 27.17 53.12 32.87 30.49 17.34 33.72 26.51 27.97 21.80 38.55 19.78 25.3

(L.)

(Thunb. ex

(L.) Rich. L.

(Hance)

L. Sieboid & s L. Planch. var. Planch. var. (Roxb.) G.Don Siebold & Zucc. & Siebold Siebold & Zucc. L.

Siebold & Zucc. Poir. L. Pers. (Spach) Rupr. (Spach) Rupr.

Mill. (L.) H.Karst.

(Rehder) Nakai

Scientific name Overview of morphological characteristics major airborne pollen in Korea. Cryptomeria japonica Alnus hirsuta Pinus rigida Ulmus davidiana japonica Ginkgo biloba Pinus koraiensis Pinus Platanus occidentalis Cannabis sativa Celtis sinensis Franco Makino Boehmeria tricuspis Cedrus deodara Juniperus chinensis Metasequoia glyptostroboides Hu & W.C.Cheng dicstichum Taxodium Platycladus orientailis Platanus orientali Humulus japonicus Zucc. L.f.) D.Don Pinus densiflora Morus australis Taxus cuspidata Taxus Picea abies Pinales: Cupressaceae Fagales: Betulaceae Rosales: U lmaceae Gymnosperms Ginkgoales: Ginkgoaceae Angiosperms - Dicotyledon Proteales: Platanaceae Rosales: Cannabaceae Rosales: U rticaceae Pinales: Pinaceae Rosales: Moraceae s.str. Pinales: Taxaceae Table 2. Table 162 Journal of Species Research Vol. 4, No. 2

(KH)

(KH)

(KH) (KH) (KH) (KH)

s.n. (KH U S) (KH U S) (KH U S)

(KH) (KH)

(KH) (KH U S)

(KH U S)

(KH)

(KH) (KH)

(KH)

K0409-002 (KH) Chang4691 Chang4616 Chang4468 (KH)

WR-06057-026 H030905-1 H980511 H040821-1 K0304031 H050514-1 JSJ110092 238 L90082 , , , , , WR-080507-013 12610003 , 484 s.n. , , 110619-013 , , , , , (KH) (KH) JKS1627 JKS1607

Voucher information Voucher et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. s.n. s.n. et al. Chang & Lee, Chang, Yang Cho Chang, Park Roh Anonymous, 1997. 5. 11, Anonymous, 1997. 5. 11, Shin Hong (KH U S) Hong Ko, Hong Oh Lee Cho & Kim, Ko, Jung & Moon, Hyun Chang & Lee, Lee Hong Chang & Lee,

Surface ornamentation granulate granulate - undulate microechinate microechinate regulate - perforate microechinate microechinate - perforate granulate microgemmate - granulate perforate granulate - gemmate granulate - gemmate granulate granulate - rugulate reticulate microechinate granulate - gemmate granulate - rugulate granulate - rugulate granulate - rugulate granulate - rugulate granulate - psilate granulate - rugulate microechinate 8) 20) 50) > > > (6 - 8) (8 - 10) ( ( (

(tetra)

Aperture polyporate triporate polyporate polyporate tricolpate tricolpate tricolpate tricolpate tricolpate triporate tricolpate tricolpate tricolpate triporate triporate tricolpate triporate triporate triporate polyporate triporate triporate polyporate P/E ratio 1.04 - 1.22 0.81 - 1.02 0.98 - 1.09 0.83 - 1.62 0.94 - 1.35 1.21 - 1.43 1.10 - 1.42 1.24 - 1.70 1.05 - 1.31 0.74 - 0.93 0.87 - 1.22 0.80 - 1.46 0.90 - 1.32 0.83 - 1.01 0.73 - 1.00 1.09 - 1.47 0.86 - 1.03 0.78 - 1.23 0.75 - 1.00 1.04 - 1.25 0.82 - 1.08 0.82 - 0.97 1.05 - 1.30 1.22 2.11 2.05 6.25 2.17 3.02 3.50 4.14 1.27 3.54 1.99 3.34 2.54 2.38 1.78 1.50 2.16 2.72 2.20 2.31 1.92 1.83 2.40 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 22.23 25.91 29.87 38.10 24.48 30.16 39.27 31.91 30.44 38.01 30.34 19.65 34.66 26.11 27.91 29.82 22.74 27.79 26.14 34.84 30.07 23.58 40.78 Equatorial diameter 2.09 2.19 1.78 3.62 2.23 3.73 4.53 4.22 2.13 2.51 2.86 2.71 2.39 2.12 2.03 3.16 1.64 1.70 2.39 3.60 2.33 1.22 3.01 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± Polar axis 24.89 30.94 24.82 38.62 27.59 32.28 49.86 44.89 33.98 31.60 33.07 22.53 37.63 23.87 23.25 36.72 21.08 24.22 28.12 39.54 27.08 21.04 47.26

Siebold & C.DC. Fisch. ex L. var. Blume var. Blume var. Blume var. Blume var. Maxim. Carruth. Fisch. ex L. Roxb. var. Roxb. var. (Siebold & Blume

Sukaczev var. Sukaczev var. Blume Thunb. Regel Murray Pall. Blume Cham. (Hance) Hemsl.

L. Makino Dode (Maxim. & Rupr.) (Maxim. & Rupr.)

(Miq.) H.Hara

Scientific name Overview of morphological characteristics major airborne pollen in Korea. Continued. Amaranthus lividus Betula schmidtii Chenopodium album centrorubrum Quercus mongolica Quercus Ledeb. Fraxinus chinensis rhynchophylla Quercus variabilis Quercus Quercus aliena Quercus Betula davurica Platycarya strobilacea Zucc. Carpinus laxifolra dentata Quercus Corylus sieboldiana manshurica Carpinus cordata Corylus heterophylla Trautv. Quercus acutissima Quercus Corylus sieboldiana sieboldiana Zucc) Blume Pterocarya stenoptera Pterocarya Acer negundo Juglans regia Betula ermanii Betula platyphylla japonica serrata Quercus C.K.Schneid. Juglans manshurica Caryophyllales: Amaranthaceae Caryophyllales: Lamiales: Oleaceae Fagales: Fagaceae Fagales: Juglandaceae Sapindales: Sapindaceae Table 2. Table August 2015 Moon et al.-Morphology of Korean airborne pollen 163

in Celtis, dioecy (male and female flowers in different individual) occurred in Acer and Morus, and hermaph­ (KH U S)

(KH U S) (KH U S) rodite was found in Ulmus. The pollen size varied from

(KH U S)

(KH U S) (KH U S) (KH U S) small to medium (P=19.78-49.86 μm) with peroblate (KH) to prolate shape (P/E ratio=0.71-1.70). Tricolpate was common aperture type together with triporate but, poly­ H120915-2 04630002 H090515 H070708-2 H090723 KS110923-1 402002 H040821 , , , , , , , , porate and diporate pollen also found (Table 2). The ret­

Voucher information Voucher iculate pollen sculpturing pattern was found in Platanus et al. et al. et al. et al. et al. et al. et al. et al. and Fraxinus while other taxa had granulate, microechi­ Hong Hong Hong Hong Hong Hong Hyun Hong nate or microperforate surface ornamentation. Only 9 species are accessed as herb. Three sexual sys­ tems are recognized: monoecy, dioecy and hermarphro­ dite. Pollen grains were small at average (P=17.34-26.50 μm) except Chenopodium (P=30.94 μm). All taxa have porate aperture shape of pollen but number of apertures varies between three to many (>50). Asteraceae pollen grains are characterized by conspicuous echinate on the pollen surface. Surface ornamentation areolate areolate verrucate - microechinate microechinate echinate - perforate echinate - perforate reticulate echinate - perforate Monocotyledon: The pollen of Miscanthus and Pen- nisetum has monoporate aperture with areolate surface patterns while Carex neurocarpa has polyporate pollen standard deviation by μm. Herbarium acronyms follow Index Herbariorum http:// ± grains. The pollen size was medium (P=38.36-42.14 μm)

(6 - 8) (5 - 6) and more or less spherical shape. Aperture (ulcerate) (ulcerate) tricolporate monoporate tricolporate polyporate polyporate tricolpate monoporate tricolporate Discussions

Flora characteristics of the general airborne pollen in Korea P/E ratio 0.87 - 1.39 0.94 - 1.17 0.80 - 1.34 0.90 - 1.36 0.92 - 1.12 0.94 - 1.32 0.98 - 1.20 0.90 - 1.34 Not surprisingly, the major airborne pollen grains in Korea are closely related with wind pollination, the all examined taxa are known as wind-pollinated plants exc­

1.56 2.58 1.38 3.37 1.16 2.36 3.57 1.77 ept Fraxinus sieboldiana only. Most gymnosperms (ca. ± ± ± ± ± ± ± ± 98%) are wind pollinated species, while 18% of angio­ sperm families are related with wind pollination (Fae­ 24.46 35.32 21.56 40.457 26.06 26.84 41.14 20.86

Equatorial diameter gri and van der Pijl, 1979; Owens et al., 1998; Cul­ ley et al., 2002; Friedman and Barrett, 2008; Lu et al., , (Stevens, 2001 onwards). The measurements are provided as mean as provided are measurements The onwards). 2001 (Stevens,

2011). In general­ wind-pollinated plants should produce 2.22 3.29 2.59 4.76 2.01 2.38 2.82 2.57 large quant­ities of pollen to increase pollination success, ± ± ± ± ± ± ± ± so the pol­len grains are relatively small in size (Crud­

Polar axis en, 2000). Furthermore, wind-pollination mechanism 26.50 38.36 22.25 45.15 25.12 30.75 42.14 23.02 could be associated­ with specific reproductive organ like reduced or absent of perianth and pendulous or cat­ kin-like inflorescence­ structure (Culley et al., 2002). In (L.)

total, 78% of airborne pollen grains in Korea are distin­

L. guished as the tree plant. It is quite high amount in com­ (Maxim.) Blume

Andersson

Pamp. parison with woody rate (ca. 20%) in Korea as a whole Maxim. L. (Park, 2007). It is also noticeable that the shrub (ca. 50% within tree category) is most common growth form of trees in Korea, but only the three shrubs of Corylus were Scientific name Overview of morphological characteristics major airborne pollen in Korea. Continued. identified in airborne pollen grains (Kim and Kim, 2011). Although the hermaphroditism is rather common in Plantago asiatica Fraxinus sieboldiana Spreng. Artemisia princeps Pennisetum alopecuroides Miscanthus sinensis Kom. Ambrosia artemisiifolia Ambrosia neurocarpa Carex Artemisia stolonifera Lamiales: Plantaginaceae Scientific names were sorted by orders from APG system sweetgum.nybg.org/ih/ Polaes: Poaceae Asterales: Asteraceae Angiosperms - Monocotyledon Poales: Cyperaceae

Table 2. Table herb, the uni­sexual plants are a predominant for the herb 164 Journal of Species Research Vol. 4, No. 2

A B C

D E F

G H I

Fig. 1. SEM micrographs of airborne pollen grains of Gymnosperm. A-C. Juniperus chinenesis. C-F. Metasequoia glytostroboides. G-I. Pi- nus rigida. plants in air­borne pollen of Korea (Table 1). However, tization rate was not correlated with amount of pollen in all hermaph­rodite plants are also characterized by easi­ the air (Oh et al., 2009). ly shaking flo­wers with reduced perianth, which may fit Fraxinus sieboldiana is an only plant of insect-pollina­ with wind-­pollination. In fact, the plants which is relat­ tion but possibly ambophilious species (both insect and ed with polli­nosis in Korea had certain morphological wind pollinated; Wallander, 2001; 2008). Like this case, charactersitics to transfer pollen in the air more effec­ most taxa of Salicaceae are ambophily, which could in­ tively like wind-­pollinated plants, pendulous male struc­ duce a strong allergenicity (Oh et al., 2012). According tures, and tall trees (Friedmans and Barrett, 2009). It is to the recent studies, many plants showed ambophilous well known assumption that the evolution of wind pol­ pollination as a possible transitional state to wind-polli­ lination required typi­cal abiotic conditions like low hu­ nation (Linder, 1998). Pollination mechanism is not fixed midity, low precipitation, open vegetation and intercom­ trait of plants and the wind-­pollination of angiosperms patible, gregarious plants (Niklas, 1987; Culley et al., evolved from insect-pollination (Faegri and van der Pijl, 2002). In Korea, airborne pollens appeared from Febru­ 1979; Owens et al., 1998; Culley et al., 2002; Friedman ary to November according to their flowering season (Oh and Barrett, 2009; Lu et al., 2011). Although many air­ et al., 2012). However, we found that airborne pollens borne pollen grains are related with wind-pollinated came out at temper­atures over 10°C, notably herb can be plants, insect pollinated plants have strong potential to observed in higher temperature (≥20°C) during June to become severe airborne pollen with wind-pollinated as September with the moderately high precipitation (over well (Culley et al., 2002). For that reason, continuous 100 mm per month; http://www.kma.go.kr/). In addition, monitoring of airborne pollen is fundamental and care­ the airborne pollen of Asteraceae showed high sensitiza­ ful observation of floral features should accompany to tion rate in comparison with other plants, but this sensi­ predict potential plants species of airborne pollen. August 2015 Moon et al.-Morphology of Korean airborne pollen 165

A B C

D E F

G H I

Fig. 2. SEM micrographs of airborne pollen grains of woody plants. A, B. Acer negundo. C. Celtis sinensis. D, E. Fraxinus sieboldiana. F, G. Pterocarya stenoptera. H, I. Quercus aliena.

Palynological characteristics of airborne pollen in pollen grains with monoaperture or inaperture. The pol­ Korea len charactersitcs are rather stenopalynous in Gymno­ sperm. However, the various combinations of each pol­ The major airborne pollen of Korea could be charact­ len characteristics could help to identify exact species; erized by rather small in size with unnoted surface pat­ for example, boat shape pollen with sulcate aperture is terns. However, we could define several pollen types a diagnostic feature of Ginkgo biloba. Within Pinaceae, according to their number of aperture and surface orna­ size of pollen with attached angle and location of sacci mentations. The saccate pollen grains, most distinctive provide additional information for species identification type of pollen in extant plants, found in Pinaceae and (Table 2). Podocarpaceae. According to the distribution patterns of Within angiosperms the pollen morphology shows these two families, the saccate pollen as an apomor­phic great diversity according to the taxa. As a member of condition is a useful diagnostic character of Pinaceae in monocotyledon Poaceae have monoporate pollen with northern hemisphere while Podocarpaceae are restricted areolate surface ornamentation, while other angiosperms in southern hemisphere (Rai et al., 2008; Doyle, 2010). possessed mainly triporate or tricolpate (Table 2; Figs. 1-­ Interestingly, the main pollinosis plants of Pinaceae pos­ 3). Morus bombycis is easily distinguished by diporate sessed the saccate pollen grains in Korea. Although the pollen grains. The polyporate was general aperture type in size of pollen is rather large in the saccate pollen, the airborne pollen. However, Juglandaceae may have poly­ sacci could play to increase buoyancy in the air (Schwen­ porate pollen with more or less circumaperturate (Straka, demann et al., 2007; Doyle, 2010). In fact, Pinaceae pol­ 1964) and the number of apertures is less than ten. On len showed highly concentrated during spring time alb­ the other hand, the airborne pollen from Amaranthaceae eit to their lower allergen (Oh et al., 2012). Except Pina­ and Plantaginaceae is characterized by pantoporate pol­ ceae, all other gymnosperms have more or less spherical len. Consequently, the number and arranging pattern of 166 Journal of Species Research Vol. 4, No. 2

A B C

D E F

G H I

J K L

Fig. 3. SEM micrographs of airborne pollen grains of herb plants. A-C. Ambrosia artemisiifolia. D. Boehmeria spicata. E, F. Chenopodium album var. centrorubrum. G. Humulus japonicus. H, I. Miscanthus sinensis. J-L. Pennisetum alopecuroides. aperture could help to identify taxa. Although the sur­ weed, and Artemisia taxa become more serious pollino­ face patterns of airborne pollen are most unnoted like sis during autumn (Oh et al., 2012) and the echinate sur­ granulate, psilate, and rugulate, some taxa could be easi­ face ornamentation could act as a stimulus for allergy ly defined with their unique sexine ornmentation. With­ by accumulated more allergen in the pollen ectexine (de out relationships of pollination mechanism both taxa of Dios Alché et al., 1999). However, the pollen wall is not Fraxinus­ have reticulate pollen grains with tricolpate an immediate cause for pollinosis, and thus the careful pol­len. The reticulate pollen was also found in Platanus. approaches are needed to determine genuine relationship The lumen size of Platanus is short and middle of muri between the pollen structure and allergen. is angled like hive shape. The surface ornamentation of Ambrosia artemissiifolia is conspicuous echinate. Other taxa of Asteraceae, Artemisia princeps and A. stolonifera, Acknowledgements also have echinate surface pattern like Ambrosia but the spine length is rather short. Ambrosia, as a worldwide This research was funded by the National Institute of August 2015 Moon et al.-Morphology of Korean airborne pollen 167

Biological Resources of the Ministry of Environment Modern pollen distributions in Qinghai-Tibetan Plateau in Korea (NIBR No. 2012-02-060). H.-K. Moon is a and the development of transfer functions for reconstruc­ postdoctoral fellow at Kyung Hee University (NRF- ting Holocene environmental changes. Quaternary Sci­ 2012R1A6A3A01040422). ence Reviews 30(7):947-966. Mardones, P., M. Grau, J. Araya, A. Cordova, I. Pereira, P. Penailillo, R. Silva, A. Moraga, R. Aguilera-Insunza, J.J. References Yepes-Nunez and I. Palomo. 2013. First annual register of allergenic pollen in Talca, Chile. Allergologia et Im­ Anderson, E.F., C.S. Dorsett and E.O. Fleming. 1978. The munopathologia 41(4):233-238. airborne pollens of Walla Walla, Washington. Annals of Moon, H.K., S. Vinckier, J.B. Walker, E. Smets and S. Huys­ Allergy, Asthma & Immunology 41(4):232-235. mans. 2008. A search for phylogenetically informative Bousquet, J., B. Guerin, B. Hewitt, S. Lim and F.B. Michel. pollen characters in the subtribe Salviinae (Mentheae: 1985. Allergy in the Mediterranean area III: Cross-reac­ Lamiaceae). International Journal of Plant Sciences 169 tivity among Oleaceae pollen. Clinical & Experimental (3):455-471. Allergy 15(5):439-448. Niklas, K.J. 1987. Pollen capture and wind-induced move­ Cruden, R.W. 2000. Pollen grains: Why so many? Plant Sys­ ment of compact and diffuse grass panicles: Implications tematics and Evolution 222(1):143-165. for pollination efficiency. American Journal of Botany Culley, T.M., S.G. Weller and A.K. Sakai. 2002. The evolu­ 74(1):74-89. tion of wind pollination in angiosperms. Trends in Ecol­ Oh, J.W. and H.B. Lee. 1997. Aerobiological study for air­ ogy & Evolution 17(10):361-369. borne pollen and mold in Kuri-shi, Kyunggi-do. Pediat­ De Dios Alché, J., A.J. Castro, A. Olmedilla, M.C. Fernández, ric Allergy and Respiratory Disease 7(1):57-68. R. Rodríguez, M. Villalba and M.I. Rpdríguez-García. Oh, J.W., H.B. Lee, I.J. Kang, S.W. Kim, K.S. Park, M.H. 1999. The major olive pollen allergen (Ole e I) shows Kook, B.S. Kim, H.S. Baek, J.H. Kim, J.K. Kim, D.J. both gametophytic and sporophytic expression during Lee, K.R. Kim and Y.J. Choi. 2012. The revised edition anther development, and its synthesis and storage takes of korean calendar for allergenic pollens. Allergy, Asth­ place in the RER. Journal of Cell Science 112(15):2501- ma and Immunology Research 4(1):5-11. 2509. Oh, J.W., I.J. Kang, S.W. Kim, M.H. Kook, B.S. Kim, J.T. Doyle, J.A. 2010. Function and evolution of saccate pollen. Cheong and H.B. Lee. 2009. The association between New Phytologist 188(1):6-9. the concentration of pollen and outbreak of pollinosis Erdtman, G. 1960. The acetolysis method, a revised descrip­ in childhood. Pediatric Allergy and Respiratory Disease tion. Svensk Botanisk Tidskrift 54(4):561-564. 19(1):4-11. Faegri, K. and L. van der Pijl. 1979. The principles of polli­ Oh, J.W., I.J. Kang, S.W. Kim, M.H. Kook, B.S. Kim, K.S. nation ecology. Pergamon Press Ltd., New York. Shin, Y.S. Hahn, H.B. Lee, M.H. Shon, J.T. Cheong, Friedman, J. and S.C.H. Barrett. 2009. Wind of change: new H.R. Lee and K.E. Kim. 2006. The correlation between insights on the ecology and evolution of pollination and increased sensitization rate to weeds in children and the mating in wind-pollinated plants. Annals of Botany 103 annual increase in weed pollen in Korea. Pediatric Aller­ (9):1515-1527. gy and Respiratory Disease 16(2):114-121. Irani, C., M. Karam, Z. Baz, H. Maatouk and F. Zaitoun. Owens, J.N., T. Takaso and C.J. Runions. 1998. Pollination 2013. Airborne pollen concentrations and the incidence in conifers. Trends in Plant Science 3(12):479-485. of allergic asthma and rhinoconjunctivitis in Lebanon. Park, C.-W. 2007. The Genera of Vascular Plants of Korea. Revue Française d’Allergologie 53(5):441-445. Academy Publishing Co., Seoul. Jung, I.Y. and K.R. Choi. 2013. Relationship between air­ Puc, M. and I. Kasprzyk. 2013. The patterns of Corylus and borne pollen concentrations and meteorological param­ Alnus pollen seasons and pollination periods in two Pol­ eters in Ulsan, Korea. Journal of Ecology and Environ­ ish cities located in different climatic regions. Aerobiolo­ ment 36(1):65-71. gia 29(4):495-511. Kim, J.S. and T.Y. Kim. 2011. Woody Plants of Korean Pen­ Punt, W., P.P. Hoen, S. Blackmore, S. Nilsson and A. Le insula. Dolbegae, Paju. Thomas. 2007. Glossary of pollen and spore terminology. Linder, H.P. 1998. Morphology and the evolution of wind Review of Palaeobotany and Palynology 143(1):1-81. pollination. In: S.J. Owens and P. Rudall (eds.), Repro­ Rai, H.S., P.A. Reeves, R. Peakall, R.G. Olmstead and S.W. ductive Biology in Systematics, Conservation and Eco­ Graham. 2008. Inference of higher-order conifer rela­ nomic Botany, Royal Botanic Gardens, Kew, Richmond. tionships from a multi-locus plastid data set. Botany 86 pp. 123-135. (7):658-669. Lu, H., N. Wu, K.B. Liu, L. Zhu, X. Yang, T. Yao, L. Wang, Q. Raynor, G.S., J.V. Hayes and E.C. Ogden. 1976. Temporal Li, X. Liu, C. Shen, X. Li, G. Tong and H. Jiang. 2011. variability in airborne pollen concentrations. Annals of 168 Journal of Species Research Vol. 4, No. 2

Allergy, Asthma & Immunology 36(6):386-396. Wallander, E. 2001. Evolution of wind-pollination in Fraxi- Schwendemann, A.B., G. Wang, M.L. Mertz, R.T. McWil­ nus (Oleaceae): an ecophylogenetic approach. Göteborg liams, S.L. Thatcher and J.M. Osborn. 2007. Aerodyna­ University, Sweden. mics of saccate pollen and its implications for wind pol­ Wallander, E. 2008. Systematics of Fraxinus (Oleaceae) and lination. American Journal of Botany 94(8):1371-1381. evolution of dioecy. Plant Systematics and Evolution Straka, H. 1964. Palynologia Madagassica et Mascarenica. 273(1):25-49. Fam. 126: Sarcolaenaceae (Chlaenaceae). Pollen et Spo­ Wang, Q., S. Nakamura, S. Lu, D. Nakajima, M. Suzuki, K. res 6(1):289-301. Sekiguchi and M. Miwa. 2013. Diurnal and nocturnal be­ Thiers, B. 2011. Index herbariorum, a global directory of haviour of airborne Cryptomeria japonica pollen grains public herbaria and associated staff. New York Botanical and the allergenic species in urban atmosphere of Saita­ Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ ma, Japan. Asian Journal of Atmospheric Environment ih/ (accessed: 25 May 2015). 7(2):65-71. Velasco-Jiménez, M.J., P. Alcázar, E. Domínguez-Vilches Wheeler, A.W. 1992. Hypersensitivity to the allergens of the and C. Galán. 2013. Comparative study of airborne pol­ pollen from the olive tree (Olea europaea). Clinical & len counts located in different areas of the city of Córd­ Experimental Allergy 22(12):1052-1057. oba (south-western Spain). Aerobiologia 29(1):113-120. Walker, J.W. and J.A. Doyle. 1975. The basis of angiosperm Submitted: June 1, 2015 phylogeny: palynology. Annals Missouri Botanical Gar­ Revised: July 23, 2015 den 62(3):664-723. Accepted: July 27, 2015