Orchids of Azerbaijani Cemeteries

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.


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] Plants 2021, 10, 2779 2 of 10 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.

Materials and Methods
We studied burial grounds (Azerbaijani: m@zarlıq, 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.
Plants 2021, 10, x FOR PEER REVIEW 2 of 10 cies [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.

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  [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.   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].

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). 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) Agab@yli (AZ-52, 8 species), Nohurqishlaq (AZ-93, Figure 2B 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).
The number of orchid taxa and individuals found in Azerbaijani cemeteries was significantly positively related to latitude (Tables 3 and 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.

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; Agab@yli, 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), Agab@yli (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.