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. 2021 Dec 16;10(12):2779. doi: 10.3390/plants10122779

Orchids of Azerbaijani Cemeteries

Attila Molnár V 1,*, Viktor Löki 2, Marc Verbeeck 3, Kristóf Süveges 1
Editor: Robert Philipp Wagensommer 
PMCID: PMC8703613  PMID: 34961250

Abstract

In order to explore their orchid flora, we performed surveys of 96 Azerbaijani burial places in 2018 and 2019. Altogether, 28 orchid taxa were found in 37 visited cemeteries. In the orchid diversity a remarkable pattern was observed: geographic latitude was significantly and positively related to the number of taxa and number of individuals. The most widespread and abundant orchids in Azerbaijani graveyards were Anacamptis pyramidalis and A. papilionacea (found in 23 and 8 cemeteries, respectively). Azerbaijani cemeteries can be important refuges for rare and threatened orchids, e.g., Himantoglossum formosum (three cemeteries), Ophrys sphegodes subsp. mammosa (eight), Orchis adenocheila (two), O. punctulata (three), O. stevenii (one) and Steveniella satyrioides (one). Epipactis turcica, detected in a single locality, was previously unknown to the flora of Azerbaijan. Additionally, we documented orchid tuber (salep) collection in two cemeteries.

Keywords: anthropogenic habitats, Caucasus, Himantoglossum formosum, human-made habitats, Orchidaceae, salep harvesting, Transcaucasia

1. Introduction

The Earth’s surface has changed dramatically in recent centuries, with human activities serve as a leading cause of the drastic reduction in the area of natural habitats [1,2]. In parallel with the degradation and fragmentation of natural environments throughout the world, isolated natural habitat patches as remnants of the original wildlife have been revalued [3]. Anthropogenically influenced habitats now occupy a significant part of the Earth’s surface and expand rapidly [4]. In order to conserve the remaining biodiversity, it is of the utmost importance to identify and protect the remaining habitats with a high conservation value, to develop a sustainable habitat management practice, and to plan future developments in the light of nature conservation priorities [5].

Recently, conservation professionals have recognized that some of the anthropogenically influenced or even human-made habitats, such as abandoned mines and industrial sites [6,7,8], road verges [9,10,11], tree plantations [12,13,14], river dikes [15], burial mounds [16], and urban habitats [17,18], play significant roles in conserving biodiversity. During the last decades, it has become increasingly evident that cemeteries also play an important role in maintaining biodiversity [19]. Although the orchid flora of cemeteries is globally rather poorly known, occurrences of orchids were published from Australian, Asian, and European burial places [20]. Based on previous knowledge on the occurrence and diversity of orchids in Turkish [21,22,23,24], Albanian [25] and central European [26] burial grounds, we predicted potential conservational importance of traditional Caucasian cemeteries. One of the main goals of our study was to search for Himantoglossum formosum, the rarest and perhaps the least known orchid of the Caucasian region [27]. During the 180 years after its description [28], almost nothing was known about the species [29], and it was re-discovered in 1994 [30]. According to recent studies, this is an ancient, phylogenetically isolated [31] and morphologically well separated [32] bona fide species. It is listed as Vulnerable (Rare) in the IUCN Red List of Threatened Plants [33].

The aims of this paper were to survey Azerbaijani cemeteries as orchid habitats, and to test which geographic factors influence the prevalence of orchids in the surveyed cemeteries.

2. Materials and Methods

We studied burial grounds (Azerbaijani: məzarlıq, hereafter cemeteries) regardless of their spatial dimension, position within settlements, or presence of built facilities. We surveyed 96 Azerbaijani cemeteries (Figure 1, Table A1) during 2018 (17–30 May by Molnár V., Löki, Mizsei and Süveges, and 28 June–4 July by Molnár V. and Szabó) and 2019 (29 April–6 May by Verbeeck, Duijnhouwer, Segers and Bobocea) and (31 May–6 June by Verbeeck, Duijnhouwer and Bradeanu). Most cemeteries were visited only once (90 and 3 cemeteries in May 2018 and in April 2019, respectively), but three cemeteries were visited in both years. All orchid taxa and the number of individuals were counted or estimated in the whole area of each visited cemetery. Species were identified based on the comprehensive book of Kuehn et al. [34]. Authors of plant names were listed in Table 1. The geocoordinates and the elevation of the visited cemeteries were determined using a Garmin eTrex Legend handheld GPS device and recorded in WGS84 format. During field trips, particular attention was devoted to documenting salep collection activity in cemeteries.

Figure 1.

Figure 1

Number of orchid taxa in the cemeteries surveyed.

Table 1.

Orchid taxa recorded in Azerbaijani cemeteries.

Taxon No. of Cemeteries Total Number
of Individuals
Anacamptis pyramidalis (L.) Rich. 23 1901
Anacamptis papilionacea L. 8 567
Ophrys sphegodes subsp. mammosa (Desf.) Soó ex Nelson 8 227
Orchis simia Lam. 7 492
Limodorum abortivum (L.) Sw. 4 23
Anacamptis morio (L.) Bateman et al. 3 514
Anacamptis collina (Banks and Sol. ex Russell) Bateman et al. 3 86
Himantoglossum formosum (Steven) K. Koch 3 27
Orchis punctulata Steven ex Lindl. 3 14
Cephalanthera rubra (L.) Rich. 3 9
Ophrys oestrifera M. Bieb. 3 3
Orchis adenocheila Czerniak. 2 239
Orchis mascula subsp. longicalcarata Akhalk. et al. 2 9
Anacamptis coriophora (L.) Bateman et al. 2 6
Ophrys apifera Huds. 2 3
Orchis caucasica Regel 1 50
Orchis ×chabalensis B. Baumann et al. (O. punctulata × O. stevenii) 1 30
Ophrys sp. 1 24
Dactylorhiza romana (Sebast.) Soó 1 20
Orchis stevenii Rchb. F. 1 20
Epipactis turcica Kreutz 1 7
Anacamptis sp. 1 6
Ophrys caucasica Woronow ex Grossh. 1 5
Epipactis microphylla (Ehrh.) Sw. 1 3
Neotinea tridentata (Scop.) Bateman et al. 1 3
Epipactis sp. 1 2
Cephalanthera damasonium (Mill.) Druce 1 1
Steveniella satyrioides (Spreng.) Schltr. 1 1

To understand the role of geographic factors in determining variation in taxon richness and abundance of orchids across Azerbaijan, we built statistical models with either of these variables as dependent variables, and latitude, longitude and altitude as explanatory variables. Both the number of individuals and the number of taxa had Poisson distributions, but due to the overdispersion in these variables, we used generalized linear model (GLMs) with quasi-Poisson distribution. All models were built in the R statistical environment [35].

3. Results

Numbering (ID), geographic location, and altitude above see level of the cemeteries visited, together with lists of the orchid taxa found in each one, are given in Table A1. In total, 28 orchid taxa were found, and considerable differences can be observed in the number of individuals and frequency of each taxon (Table 1), as well as in orchid species richness and abundance of each cemetery (Table 2).

Table 2.

Descriptive statistics orchid flora of Azerbaijani cemeteries.

Number of cemeteries studied 96
Number of cemeteries hosting orchids 37
Rate of cemeteries hosting orchids 38.5%
Mean (±SD) number of orchid taxa/cemeteries 0.92 (±1.73)
Maximum number of orchid taxa/cemeteries 9
Mean (±SD) number of orchid individuals/cemeteries 44.4 (±173.8)
Maximum number of orchid individuals/cemeteries 1050

Each taxon was found total in 1–24 cemeteries (mean ± SD = 3.2 ± 4.5), with the number of individuals varying from 1 to 1902 (mean ± SD = 150 ± 374). The most widespread and abundant species was Anacamptis pyramidalis (Figure 2A). The number of taxa detected in only one graveyard was 15, whereas four species were found in more than five cemeteries. The highest number of taxa in a given cemetery was 9. In most cases only one taxon (18 cemeteries (15%)) or two taxa (11 cemeteries (9.4%)) occurred. Cemeteries that serve as habitats for five or more taxa were extremely rare (4 (3.4%)). The most orchid-rich cemeteries were found near Lerik (AZ-16, 9 species) Ağabəyli (AZ-52, 8 species), Nohurqishlaq (AZ-93, Figure 2B, 8 species), and DashliJalgan (AZ-90, 5 species).

Figure 2.

Figure 2

Orchids in Azerbaijani cemeteries. (A) Anacamptis pyramidalis population in the cemetery of Əngixaran (AZ–61). (B) Cemetery of Nohurqishlaq (AZ-93), habitat of Orchis punctulata, O. stevenii and their hybrids (Orchis ×chabalensis). (C) Viable population of Himantoglossum formosum was found on a few tens of square meter of refuge under some old oak trees in cemetery of Zizik (AZ-74). (D) Spurs of salep harvesting in the cemetery of Ağabəyli (AZ-52). (E) Effect of fencing around cemetery against grazing: plant cover is considerable lower outside (left) than inside (right, with flowering individuals of Anacamptis pyramidalis) of cemetery of Zurnabad (AZ-32). (F) Inflorescence of Steveniella satyrioides. (G) Occurrence of Epipactis turcica was formerly unknown from Azerbaijan (Tengealti, AZ-85). (H) A very localized and rare endemic species, Himantoglossum formosum in cemetery of Zizik (AZ-74). Photo credit: A, C, D, G and H by A. Molnár V.; B and F by M. Verbeeck; E by V. Löki.

The harvest of orchid tubers (“salep”) was observed in two cemeteries during 2018. In Ağabəyli cemetery (AZ-52, Figure 2D) three species (Anacamptis papilionacea, Orchis adenocheila, O. simia), and in Dashli Jalgan cemetery (AZ-90) five species (Anacamptis collina, A. papilionacea, Ophrys sphegodes subsp. mammosa, Orchis simia, Neotinea tridentata), were collected. Both of these localities host notable orchid populations with eight and five species, respectively.

The number of orchid taxa and individuals found in Azerbaijani cemeteries was significantly positively related to latitude (Table 3 and Table 4, respectively), but not to longitude and altitude. When non-significant predictors were removed from the model in a stepwise manner (based on the largest p-values), only latitude remained in the final model as a significant predictor of orchid species richness and abundance.

Table 3.

Effect of geographic location on number of orchid taxa per cemetery. Parameter estimates, their standard errors (SE), associated t-values (t) and significance levels (p) are presented.

Full Model Minimal Model
Estimate SE t p Estimate SE t p
Intercept −0.2317 0.2018 −1.148 0.251 −0.1916 0.2017 −0.95 0.342
Altitude 0.0850 0.1746 0.487 0.627
Latitude 0.5750 0.1943 2.960 0.003 0.5471 0.1968 2.78 0.005
Longitude 0.3305 0.1916 1.725 0.084

Table 4.

Effect of geographic location on number of orchid individuals in Azerbaijani cemeteries.

Full Model Minimal Model
Estimate SE t p Estimate SE t p
Intercept 3.8439 0.3783 10.161 <0.001 3.8765 0.3788 10.234 <0.001
Altitude 0.0784 0.1801 0.435 0.6635
Latitude 0.2891 0.1930 1.498 0.1342 0.5770 0.2032 2.839 0.0045
Longitude 0.6063 0.2023 2.997 0.0027

4. Discussion

During our work, it has been proved that Muslim Azerbaijani cemeteries host significant orchid populations. The key conservation importance of Azerbaijani cemeteries can be explained by two facts: (1) Religious privileges protected these sacred sites and their natural values, because they have largely been exempt from forest and agricultural utilization ever since; and (2) the mostly fenced area of cemeteries provide protection against excessive grazing (Figure 2E).

Azerbaijani cemeteries provide shelters for several valuable populations of rare and threatened orchids. From a conservation point of view, one of the most valuable species is the Eastern Caucasian endemic Himantoglossum formosum (Figure 2H), which was found in three of the visited cemeteries (Zizik, AZ-74, Figure 2C; Yasab, AZ-78; Piral, AZ-79). Viable populations of the rare Orchis adenocheila were found in two cemeteries (Lerik, AZ-16; Ağabəyli, AZ-52). The occurrence of Steveniella satyrioides was detected in cemetery of Lerik (Lerik, AZ-16, Figure 2F). The occurrence of Epipactis turcica (Figure 2G) was also found near Tengealti (AZ-85); this taxon was formerly unreported in Azerbaijan.

The long-term survival of these orchid populations in cemeteries strongly depends on long-established, sustainable management practices and traditional burial habits [22,36]. Establishment of graves (especially modern graves covered by marble or concrete tombstones) on the most valuable parts of these cemeteries is expressly undesirable from a conservation perspective, as well as the use of herbicides or electric trimmers. However, mowing or moderate grazing of grassy areas around the burial ground is preferred and encouraged for a more efficient conservation of the local biodiversity and valuable flora elements. Based on their diverse and abundant orchid community in some of the visited cemeteries, we strongly recommend the local councils and the nature protection authorities to protect certain burial places, especially near Lerik (AZ-16), Ağabəyli (AZ-52), DashliJalgan (AZ-90), Nohurqishlaq (AZ-93), and Nugadi (AZ-92).

A special threatening factor of tuberous orchids, namely the harvest of their tubers (making salep for culinary purposes [37]) was observed in Azerbaijani cemeteries. On the one hand, the right of local human communities to continue using traditional natural resources is unquestionable and seems also sustainable [38,39]. On the other hand, the effects of tuber collection on populations of frequent and widespread orchids is little known, while the sustainability of salep harvesting is at least controversial [40,41,42,43,44,45,46,47]. However, destroying the rarest taxa (Himantoglossum formosum, Orchis adenocheila) should definitely be avoided.

Acknowledgments

The authors are grateful to Edvárd Mizsei, Éva Szabó, Luc Segers, Roel Duijnhouwer, Alin Bradeanu and Mihai Bobocea for their assistance during the field work, to Attila Takács for editing the map of surveyed cemeteries and to the anonymous reviewers for their valuable suggestions and useful recommendations. We would like to express our gratitude to C. A. J. Kreutz (The Netherlands) for identification of Epipactis turcica, and to Orsolya Vincze for her linguistic corrections of the earlier version of our manuscript.

Appendix A

Table A1.

Numbering (ID), geographic location, altitude, year of observation and orchid taxa of the 96 cemeteries studied in Azerbaijan. A dash “–” indicates that no orchid taxa were recorded. Generic name abbreviations: A.—Anacamptis, C.—Cephalanthera, D.—Dactylorhiza, E.—Epipactis, H.—Himantoglossum, L.—Limodorum, O.—Orchis, Op.—Ophrys, S.—Steveniella.

ID Settlement Latitude, Longitude Alt. (m) Year Taxa (Number of Individuals)
01 Şorsulu 39.42429° N, 48.82938° E 26 2018
02 TəzəAlvadı 39.09155° N, 48.61027° E 2 2018
03 Lənkəran 38.77246° N, 48.83487° E 29 2018
04 Lənkəran 38.74200° N, 48.83201° E 19 2018
05 Velədi 38.72414°N, 48.82849°E 15 2018
06 Şürük 38.69889° N, 48.78815° E 21 2018
07 Telman 38.65184° N, 48.80355° E 1 2018
08 Kəkülus 38.61265° N, 48.84406° E 17 2018
09 Kərgəlan 38.73326° N, 48.79404° E 0 2018
10 Shaglakuche 38.72074° N, 48.76931° E 58 2018
11 Shaglakuche 38.71618° N, 48.76020° E 60 2018
12 Shaglakuche 38.71618° N, 48.74096° E 80 2018
13 Shaglakuche 38.71839° N, 48.72004° E 97 2018
14 Lerik 38.80257° N, 48.45105° E 803 2018 O. mascula (4)
15 Lerik 38.77126° N, 48.41079° E 1108 2018
16 Lerik 38.76576° N, 48.42419° E 1062 2018, 2019 A. papilionacea (2019: 3), A. pyramidalis (2018: 500, 2019: 300), D. romana (2019: 20), Op. caucasica (2019: 5), Op. sphegodes subsp. mammosa (2018: 50, 2019: 100), O. adenocheila (2018: 5, 2019: 200), O. mascula (2019: 5), O. simia (2018: 50, 2019: 200), S. satyrioides (2019: 1)
17 Ambu 38.75581° N, 48.44571° E 1238 2018
18 Gosmalijion 38.69194° N, 48.40264° E 1308 2018
19 Laman 38.85799° N, 48.39724° E 800 2018
20 Aran 38.87474° N, 48.39668° E 780 2018
21 Aran 38.87868° N, 48.39648° E 780 2018
22 Bülüdül 38.83971° N, 48.30756° E 805 2018 A. pyramidalis (7), L. abortivum (4)
23 Züvüç 38.86909° N, 48.30655° E 885 2018
24 Yardımlı 38.88330° N, 48.28216° E 1020 2018
25 Yardımlı 38.90051° N, 48.25522° E 827 2018
26 Yardımlı 38.90921° N, 48.24933° E 720 2018
27 Perimbel 38.90218° N, 48.09793° E 1366 2018
28 Yardımlı 38.91879° N, 48.31857° E 580 2018
29 Yeyənkənd 38.98335° N, 48.57487° E 102 2018 L. abortivum (8)
30 Allahyarlı 39.00025° N, 48.60194° E 66 2018
31 Göygöl 40.57610° N, 46.30989° E 720 2018
32 Zurnabad 40.51304° N, 46.24282° E 958 2018 A. pyramidalis (100), Op. sphegodes subsp. mammosa (8)
33 Dağ Kəsəmən 41.08915° N, 45.38852° E 401 2018
34 Poylu 41.15871° N, 45.44410° E 328 2018
35 Köçəsgər 41.05043° N, 45.50680° E 456 2018
36 Qaraxanlı 41.05042° N, 45.68841° E 346 2018
37 Tovuz 40.97800° N, 45.62000° E 440 2018
38 İbrahimhacılı 40.89159° N, 45.74460° E 548 2018
39 Ağaməmmədli 40.85088° N, 45.73310° E 581 2018 A. morio (1)
40 Yanıqlı 40.84016° N, 45.67080° E 669 2018 A. pyramidalis (100), O. simia (20)
41 Məşədilər 40.87028° N, 45.74312° E 548 2018
42 Düyərli 40.91173° N, 45.85246° E 369 2018
43 Gəncə 40.71074° N, 46.42177° E 370 2018
44 Şiştəpə 40.83121° N, 45.87962° E 592 2018 A. morio (8)
45 Şəmkir 40.80390° N, 46.01184° E 559 2018
46 Çinarlı 40.78807° N, 46.10889° E 431 2018
47 Ağsu 40.53386° N, 48.33778° E 152 2018 A. pyramidalis (25), O. simia (20)
48 Ağsu 40.56429° N, 48.38220° E 152 2018
49 Muğanlı 40.63904° N, 48.50003° E 732 2018
50 Muğanlı 40.66912° N, 48.52951° E 878 2018
51 Böyük Xınıslı 40.65781° N, 48.61163° E 870 2018 A. papilionacea (1)
52 Ağabəyli 40.66747° N, 48.57887° E 927 2018 A. collina (1), A. papilionacea (465), A. pyramidalis (150), Op. apifera (1), Op. sphegodes subsp. mammosa (3), O. adenocheila (39), O. punctulata (1), O. simia (26)
53 Şamaxı 40.64936° N, 48.62496° E 783 2018
54 Muğanlı 40.67730° N, 48.55807° E 971 2018 A. pyramidalis (9), Op. apifera (2)
55 Suraxanı 40.71495° N, 48.47015° E 900 2018 A. pyramidalis (1)
56 Kalva 40.72985° N, 48.48152° E 907 2018 A. pyramidalis (1)
57 Xatman 40.72947° N, 48.49023° E 862 2018
58 Dilman 40.72596° N, 48.49876° E 831 2018
59 Məlhəm 40.69225° N, 48.62865° E 1115 2018 A. papilionacea (1)
60 Qəleybuğurd 40.75093° N, 48.56726° E 912 2018 L. abortivum (10)
61 Əngixaran 40.67143° N, 48.65670° E 978 2018 A. papilionacea (2), A. pyramidalis (140), Op. sphegodes subsp. mammosa (8), Op. oestrifera (1)
62 Gandov 40.81714° N, 48.31921° E 952 2018
63 Müşkəmir 40.81919° N, 48.33202° E 1100 2018
64 Lahıc 40.84393° N, 48.37823° E 1214 2018 A. coriophora (1), A. pyramidalis (7)
65 Qaraqaya 40.79417° N, 48.30885° E 1111 2018
66 Talıstan 40.79954° N, 48.20033° E 827 2018
67 Talıstan 40.80186° N, 48.20287° E 850 2018
68 İkinci Yeniyol 40.75425° N, 48.26252° E 850 2018 A. pyramidalis (12), Op. oestrifera (1)
69 Təzəkənd 40.73435° N, 48.27164° E 671 2018 A. papilionacea (10), A. pyramidalis (2)
70 Sabir 40.59207° N, 48.70527° E 567 2018
71 Digah 41.38517° N, 48.47876° E 662 2018 A. pyramidalis (3)
72 Qirmizi Qəsəbə 41.37358° N, 48.51741° E 607 2018
73 Ağbil 41.42650° N, 48.56662° E 410 2018 C. damasonium (1), E. sp. (2)
74 Zizik 41.38543° N, 48.57021° E 482 2018, 2019 H. formosum (2018: 21, 2019: 7), Op. sphegodes subsp. mammosa (2018: 1)
75 Avadjuk 41.47244° N, 48.39413° E 670 2018 A. pyramidalis (1)
76 Hil 41.46756° N, 48.35726° E 770 2018
77 Hil 41.46891° N, 48.33767° E 768 2018 -
78 Yasab 41.49661° N, 48.31670° E 787 2018, 2019 H. formosum (2018: 4, 2019: 0)
79 Piral 41.50062° N, 48.29514° E 838 2018 A. pyramidalis (13), H. formosum (2)
80 Hazra 41.50588° N, 48.25472° E 725 2018 A. pyramidalis (2)
81 Laza 41.29840° N, 48.11429° E 1703 2018
82 Urva 41.40196° N, 48.34058° E 1046 2018
83 Qusar 41.41850° N, 48.40676° E 768 2018 C. rubra (2)
84 Pirvahid 41.32669° N, 48.65619° E 370 2018 A. pyramidalis (6)
85 Tengealti 41.23764° N, 48.62676° E 701 2018 A. pyramidalis (10), C. rubra (5), E. turcica (7), L. abortivum (1)
86 Sirt-Chichi 41.22650° N, 48.67541° E 672 2018
87 Chichi 41.21673° N, 48.67737° E 538 2018 A. pyramidalis (2), C. rubra (2), E. microphylla (3)
88 Gilanov 41.23790° N, 48.75276° E 325 2018
89 Mashrif 41.09305° N, 48.96764° E 420 2018
90 Dashli Jalgan 41.08023° N, 48.98348° E 180 2018 A. collina (77), A. papilonacea (35), Neotinea tridentata (3), Op. sphegodes subsp. mammosa (96), O. simia (11)
91 Tıxlı 40.90958° N, 49.10128° E 593 2018 A. collina (8), A. sp. (6), Op. sp. (24)
92 Nugadi 41.31504° N, 48.59641° E 506 2018 A. pyramidalis (800), O. cf. caucasica (50), O. simia (200)
93 Nohurqishlaq 40.95280° N, 47.92485° E 749 2019 A. coriophora (5), A. pyramidalis (5), A. morio (505), Op. sphegodes subsp. mammosa (10), Op. oestrifera (1), O. ×chabalensis (O. punctulata × O. stevenii) (30), O. punctulata (10), O. stevenii (20)
94 Chukhur Gabala 40.87934° N, 47.69153° E 404 2019 A. pyramidalis (5)
95 Şəfili 40.84899° N, 47.69877° E 354 2019 A. papilionacea (50), Op. sphegodes subsp. mammosa (1), O. punctulata (3), O. simia (15)
96 Gosmalijion 38.67424° N, 48.37322° E 1450 2018

Author Contributions

Conceptualization: A.M.V.; formal analysis: K.S.; investigation: A.M.V., V.L., M.V. and K.S.; writing—original draft preparation: A.M.V.; writing—review and editing: V.L., M.V. and K.S.; visualization: A.M.V., V.L. and M.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Research, Development and Innovation Office of Hungary (grant number NKFI-OTKA K132573).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data analyzed in this study are available in Appendix A.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data analyzed in this study are available in Appendix A.


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