Plant Species as Potential Forage for Honey Bees in the Al-Baha Mountain Region in Southwestern Saudi Arabia

The contribution of bee forages in the form of nectar, pollen, and propolis to beekeeping development depends on plant species diversity. The data concerning the increase in honey production in southwestern Saudi Arabia, which was unexpected with the deterioration of the vegetation cover, becomes a concrete background for this study, which planned to list the bee plant species contributing as sources of nectar, pollen, and propolis. The sampling method followed a purposive random sampling approach, and 20 × 20 m plots were considered with a total of 450 sample plots. Bee forage plants were identified based on flower morphology and honey bees’ actions during floral visits at active foraging hours. A checklist of bee forages containing 268 plants species belonging to 62 families was documented. The number of pollen source plants (122) was more than nectar (92) and propolis (10) source plants. Regarding seasonal distribution, spring and winter were relatively good seasons for honey bees in terms of pollen, nectar, and propolis availability. Generally, this study is an essential step towards understanding, conserving, and rehabilitating plant species providing nectar, forage, and propolis to honey bees in Al-Baha Region of Saudi Arabia.


Introduction
Al-Baha is one of the regions in the Kingdom of Saudi Arabia characterized by arid and semi-arid climatic types. This region has relatively great potential for beekeeping with its rich vegetation and diverse environmental conditions. Vegetation diversity is regarded as one of the most important comparative features distinguishing this region from others; wild plants can be found in the deserts, villages, oases, plains, valleys, and mountains of Al-Baha's landscapes [1]. As a result of its rich floral resource, beekeeping in Al-Baha is one of the most popular and socially accepted livelihood activities in both the Sarawat mountainous and the Tehama coastal areas, which constitute the main apicultural landscapes in the region [2]. A recent study conducted by Al-Ghamdi et al. [3] also reported the existence of enormous honey bee floral resources in the region. However, most of the plant habitats are vulnerable to deterioration and vegetation degradation amid anthropogenic activities, habitat loss, over-exploitation, invasive plant species, and climate change [4].
Honey bee colonies contribute greatly to human well-being by contributing to the provision of ecosystem services and completing plants' life cycles [5][6][7]. Although it is known that the ecosystem contributes positively to the sustainable development of life [8,9], there are no studies confirming the shared contribution of bees to achieve sustainable development goals through the ecosystem. Numerous research endeavors have demonstrated the importance of insect pollinators in achieving multiple sustainable development goals by regulating natural cycles, biological control, pollination, seed dispersal, and even as a biological inspiration [5,10,11]. The role of bees in pollinating plants has been emphasized as a direct contribution to food security and biodiversity. Therefore, sustainable development of honey bee resources and forage starts by identifying and documenting the honey bee plants to assure honey bees' services.
There has been a constant demand for honey bee services since ancient times; however, the honey production sub-sector, which relied on limited floral resources could not fulfill the long-standing demand for honey and related products and byproducts while the country continued importing from abroad. Saudi Arabia currently imports more than 15,000 metric tons of table honey each year. Australia, Turkey, Mexico, Argentina, Pakistan, United States, Germany, and Yemen are the largest honey-producing countries, in order of volume imported to the country. However, this trend shall be changed and the country shall focus on boosting its apicultural production and declare self-dependency by advocating beekeeping development and apicultural resource development endeavors [2]. In doing so, rehabilitation and restoration of apicultural landscapes through reforestation and plantation activities while emphasizing local honey bee floral genetic resources shall draw the attention of development agents. However, so far, information about the high-value nectar and pollen sources, which include indigenous and locally available plant genetic material, is not largely available; when it is available, it is only limited to a few species [3]. Logically, it is worth identifying and documenting the honey bee plant species and creating an area-specific checklist to make use of the resources in times of development needs as part of the beekeeping development effort. The current list of honey bee flora of Al-Baha might not be the most comprehensive of all bee plant species, but it can at least be a foundation list of available honey bee flora for the government-community partnership and non-governmental organizations (NGOs) interested in rehabilitating the honey bee floral resource of this region.
Coupled with the mapping of botanical communities of bee plants in the region, the list can be an excellent developmental aid that contributes to improving the beekeeping conditions and increasing the average output production per colony. Therefore, this study offers a way for future restoration and rehabilitation works to boost the apicultural subsector and hence contributes to achieving some of the nation's development goals, such as Vision 2030. In line with this, the current study is aimed at documenting honey bee flora in arid and semi-arid areas by enlisting bee-plant species in the Al-Baha Region of Saudi Arabia, respective to the different seasons.

Results
Pollen sources were found to be greater in number than the nectar and propolis source plants with recorded numbers of species being 122, 92, and 10, respectively. Similarly, plant family numbers were higher for pollen sources than the nectar and propolis, with 31, 14, and 3 plant family classes, respectively. In the current study, about 62 families were recorded as a source of nectar, pollen, and both nectar and pollen source plants. Asteraceae has the highest number of individual plant species with 35 in total, and all of which are considered as sources of nectar, pollen, or both. The Fabaceae family followed the Asteraceae in bee plant documentation in the region, while the Lamiaceae, Malvaceae, and the Amaranthaceae were found to contribute significantly, in this order of importance, to honey bee resources in the form of nectar and pollen. Euphorbiaceae, Plantaginaceae, Boraginaceae, Brassicaceae, and Acanthaceae were also among the top ten plant families holding major shares in the contribution of honey bee resources in the region. These ratings were based on the number of individual plant species contributing to the bee forage resource in the region. (Tables 1 and 2). Season-wiseanalysis of the distribution of bee plant species found that spring is the most valuable (p < 0.05) flowering season for the bees, followed by winter, autumn, and summer with 170, 128, 96, and 89 flowering plants, respectively. Spring and winter are more precious flowering seasons (p < 0.05) than autumn and summer for beekeepers in Al-Baha region, and the number of bee plants secreting nectar was 54 and 50, respectively (Table 3).          The variations in the distribution of flowering and not-flowering status of plant species were found to be significant (p < 0.05) in spring and winter, while only slight variations were seen between summer and autumn ( Figure 1).
The percentages of plants that did not flower in summer and autumn were observed to be 64.16% and 68.28%, respectively ( Table 3). The diversity index showed that the flowering plant species in spring (H = 2.22) and winter (H = 2.16) were more diverse than the autumn (H = 1.99) and summer (H = 1.94). more precious flowering seasons (p < 0.05) than autumn and summer for beekeepers in Al-Baha region, and the number of bee plants secreting nectar was 54 and 50, respectively (Table 3). The variations in the distribution of flowering and not-flowering status of plant species were found to be significant (p < 0.05) in spring and winter, while only slight variations were seen between summer and autumn ( Figure 1). = Flowering status; Sp = Spring; Wi = Winter; Au = Autumn; Su = Summer. The category "Yes" is quite near to "Winter" and "Spring" while "No" is related to "Autumn" and "Summer", implying that flowering honey bee plants occur more during winter and spring and less in summer and autumn.
The percentages of plants that did not flower in summer and autumn were observed to be 64.16% and 68.28%, respectively ( Table 3). The diversity index showed that the flowering plant species in spring (H′ = 2.22) and winter (H′ = 2.16) were more diverse than the autumn (H′ = 1.99) and summer (H′ = 1.94). more precious flowering seasons (p < 0.05) than autumn and summer for beekeepers in Al-Baha region, and the number of bee plants secreting nectar was 54 and 50, respectively (Table 3).  The category "Yes" is quite near to "Winter" and "Spring" while "No" is related to "Autumn" and "Summer", implying that flowering honey bee plants occur more during winter and spring and less in summer and autumn.
The percentages of plants that did not flower in summer and autumn were observed to be 64.16% and 68.28%, respectively ( Table 3). The diversity index showed that the flowering plant species in spring (H′ = 2.22) and winter (H′ = 2.16) were more diverse than the autumn (H′ = 1.99) and summer (H′ = 1.94).
= Flowering status; Sp = Spring; Wi = Winter; Au = Autumn; Su = Summer. The category "Yes" is quite near to "Winter" and "Spring" while "No" is related to "Autumn" and "Summer", implying that flowering honey bee plants occur more during winter and spring and less in summer and autumn.
On the other hand, spring and winter were found to be the most valuable seasons with a high percentage of plants that flower at 63.43% and 45.48%, respectively (Table 4). Results from the contingency analysis of the Chi-square test revealed that flowering plants behaved significantly (p < 0.05) differently distributed across all the seasons. A higher number of flowering plants were found to be significant in spring and winter with a value of p < 0.05. There is a significant (p < 0.05) clustering in the number of flowering plants in spring and winter compared with summer and autumn, as shown in the correspondence analysis ( Figure 1).
Results of the current study show that wild plant species constitute 84.70%, followed by regional endemic (10.45%), near-endemic (2.99%), and endemic plants (1.87%) of the bee flora of the region. Many bee-forage plants like Ziziphus spina-christi, Vechilia species Senegalia asak, and Senegalia hamulosa are designated as rare and endangered. Some plant species are rare, such as Blepharis edulis and Hypoestes forskaolii, and are considered valuable honey sources with high rates (Figure 2), ( Table 2).
higher number of flowering plants were found to be significant in spring and winter with a value of p < 0.05. There is a significant (p < 0.05) clustering in the number of flowering plants in spring and winter compared with summer and autumn, as shown in the correspondence analysis (Figure 1).
Results of the current study show that wild plant species constitute 84.70%, followed by regional endemic (10.45%), near-endemic (2.99%), and endemic plants (1.87%) of the bee flora of the region. Many bee-forage plants like Ziziphus spina-christi, Vechilia species Senegalia asak, and Senegalia hamulosa are designated as rare and endangered. Some plant species are rare, such as Blepharis edulis and Hypoestes forskaolii, and are considered valuable honey sources with high rates (Figure 2), ( Table 2).

Discussion
The current study is aimed at documenting honey bee flora in arid and semi-arid areas by enlisting honey bee plant species in Al-Baha Region of Saudi Arabia, respective of the different seasons. The existing flora in the current study area benefits the honey bees by providing forage resources, namely nectar, pollen, and propolis; ultimately, they were found to be the main rewards offered by flowers to honey bees. Meanwhile, pollen sources outweighed the nectar and propolis sources in the number of plant species. In agreement with the current study, plants certainly provide pollen more than nectar [12]. Based on the honey bee's requirement for forage, adult bees mostly consume more nectar than pollen, whereas larvae need more volume of both pollen and nectar (bee bread)

Discussion
The current study is aimed at documenting honey bee flora in arid and semi-arid areas by enlisting honey bee plant species in Al-Baha Region of Saudi Arabia, respective of the different seasons. The existing flora in the current study area benefits the honey bees by providing forage resources, namely nectar, pollen, and propolis; ultimately, they were found to be the main rewards offered by flowers to honey bees. Meanwhile, pollen sources outweighed the nectar and propolis sources in the number of plant species. In agreement with the current study, plants certainly provide pollen more than nectar [12]. Based on the honey bee's requirement for forage, adult bees mostly consume more nectar than pollen, whereas larvae need more volume of both pollen and nectar (bee bread) [13][14][15][16]. This fact has been proven in the current study, as well as a sustainable mutualism association between the bee and plant species, where bees benefit the plants through pollination while they obtain their basic nutrients from the pollen. Honey bees do not gather the forage resource for their survival only, but for their broods also [17][18][19], which guarantees the continuation of their species.
Similar to the current study, Al-Ghamdi et al. [3] mentioned that bee plants are important in strengthening bee colonies, and mentioned the total number of bee plants found in the Al-Baha Region is 204 plant species under 58 families dominated by nine main honey source plants. The distribution and availability of pollen source plants could be attributed to the fact that the genetic constitution of plants often produces pollen grain for sexual multiplication, and bees benefit from the process of pollination whilst collecting pollen. Understanding the floral resource (nectar, pollen, and propolis) and their flowering season is critically important for the improvement of the management of carrying capacity in their habitats [20]. Similar studies have implied that the flowering calendar varies among species and locations. However, listing and classifying plants based on their potential benefit to honey bees is essential to help support beekeeping [21]. Similar results were reported by Al-Namazi et al. [22]. They found that the plant diversity in southwest Saudi Arabia was about 319 plant species from 75 families and 228 genera, among which only two species are endemic; 14 are endemic to the Arabian Peninsula, five are regional-endemic only found in East Africa and the Arabian Peninsula, and 39 are rare and endangered. The significant number of rare and endangered plant species could raise an alarm to initiate effective remedial measures for the preservation and conservation of the existing flora. Shada Mountain, the highest landscape in the lowlands of Al-Baha Region of southwestern Saudi Arabia, is the most important plant area and was found to have 495 plant species belonging to 314 genera and 76 families, including 19 endemic species and 43 endangered species, accounting for 22% of Saudi Arabia's total flora [23].
Furthermore, the outcomes of this study showed that about 268 plant species under 62 families were recorded in the study area. They are there for providing bee floral rewards, pollen, nectar, and propolis either in a combined or separate manner in that order of importance of contribution to the wellbeing of honey bees. Similar floral richness to the current study related to different geographic, edaphic, and environmental factors was also reported by Al-Aklabi et al. [24]. The fact is that the research location has varied geographical and climate elements that could explain the variance in the diversity of flowering plants throughout time. The most plant families observed in the region were the Asteraceae, Fabaceae, Lamiaceae, and Malvaceae. These families were found to have the highest number of species in Saudi Arabia, likely due to their long-developed stress and drought tolerance abilities. Similarly, Amaranthaceae, Euphorbiaceae, Plantaginaceae, Boraginaceae, Brassicaceae, and Acanthaceae are known for their adaptation to arid and semi-arid regions, thus holding major shares in the honey bee resource contribution in the current region, which is mainly characterized by dry climates. Similar findings were reported by Kuppler et al. [25] and Zurbuchen and Müller [26].
In our study, spring and winter were relatively good seasons for honey bees in terms of pollen, nectar, and propolis availability. This might be due the relatively conducive plant growing weather conditions in winter and spring. The region's erratic foggy weather in winter and early spring and relatively moderate temperature and rainfall records were reported by National Center for Metrology [27]. Autumn season is frequently coupled with heavy rain and fog, which is still considered favorable for most plants in highland locations and foothills. The impact of environmental conditions on species diversity and richness was reported by Slezák et al. [28] and Al Zandi et al. [29].

Study Sites
The study was conducted in the Al-Baha Region, southwestern Saudi Arabia starting from 2019 to the end of 2021. The ecological area consists of four regions, namely, the Tehama coastal area, the Tehama Foothills, the high-altitude area, and the eastern foothills [24]. The average temperature in the summer ranged between 20-30 • C and 8-20 • C in the winter. Rainfall varies among geographical areas. In the highlands, it ranged from 300 to 550 mm/year, while it was less than 150 mm/year in the Tehama Region. The humidity ranged from 40% to 58% from November to May [27]. The region is known for its erratic foggy weather in winter and early spring while the plant populations thrive well as relatively moderate temperature and rainfall records are common in these seasons. In May, the environmental and geographical characteristics create a favorable ecological niche for diversifying the life forms of plant species. Al-Baha Region has been described in many studies as one of the best ecological landscapes for harboring vast floral and faunal diversity in Saudi Arabia [3,22,27,28]. The sampled sites were mapped using ArcGIS software (Figure 3).

Sampling and Bee Plant Identification
The study concentrated on surveying the bee plant species distributed throughout the region for three consecutive years, from Jan 2019 to Dec 2021. A sampling model was used in many studies on enumerating plant diversity [24,30,31]. The survey covered an area of 180,000 m 2 using a 20 × 20 m quadrat laid purposively to exhaustively include the most possible plant diversity. A total of 450 plots were considered. In areas with homogeneous plant cover, samples were taken randomly, leading to the use of purposive random sampling technique. Plant specimens were collected from the field and immediately pressed to get dried and finally glued on herbarium sheets; then, all specimens were archived and placed in the herbarium of Al-Baha University based on the scientific methods of identification following Collenette [32]. erratic foggy weather in winter and early spring while the plant populations thrive well as relatively moderate temperature and rainfall records are common in these seasons. In May, the environmental and geographical characteristics create a favorable ecological niche for diversifying the life forms of plant species. Al-Baha Region has been described in many studies as one of the best ecological landscapes for harboring vast floral and faunal diversity in Saudi Arabia [3,22,27,28]. The sampled sites were mapped using ArcGIS software (Figure 3).

Sampling and Bee Plant Identification
The study concentrated on surveying the bee plant species distributed throughout the region for three consecutive years, from Jan 2019 to Dec 2021. A sampling model was used in many studies on enumerating plant diversity [24,30,31]. The survey covered an area of 180,000 m 2 using a 20 × 20 m quadrat laid purposively to exhaustively include the most possible plant diversity. A total of 450 plots were considered. In areas with homogeneous plant cover, samples were taken randomly, leading to the use of purposive The plant species valuable to bees were identified based on flower avaliability, bees' action during foraging hours on the flowers, presence of pollen in the corbiculae, and the old regional beekeepers' experience (who observe how the bees take resources from the flowers: when the bees send their proboscis to a flower, it implies that the plant is a nectar source. It is a pollen source if the bees uptake the pollen powder in their body and collect it in the pollen basket. It is also clear when bees collect the propolis and can be observed by the researchers [33]). After data collection, we classified the bee plants into different groups according to the type of collected forages as follows: nectar (N) source, pollen (P) source, and both pollen and nectar source plants. The latter group was marked according to the main dominance source as follows: N + P (the main source of the forage was nectar and some pollen was observed) or P + N (the main source of the forage was pollen and some nectar was observed). Careful observations were made on the bees' actions while collecting resources for bee forage source plant categorization. The propolis (Po) source plants were determined by the observations made on bees' visits to vegetative parts of plants collecting the plant secretions from leaves, stems, fruits, and branches (Supplementary Data: images showing bees on the forage plants). Observations on honey bee visits were conducted during foraging hours respective of the different seasons: every two hours from 5:30 AM to 6:30 PM in spring, summer and autumn, and every one hour from 9:00 AM to 5:00 PM in winter. In most parts of the region, the cold stresses of the winter season are common during early morning and late afternoon. Data were filtered and managed using Microsoft Office Excel 2013. The responses of nominal variables like the seasonal distribution of flowering plants in spring, summer, autumn, and winter were tested using Chi-square (χ 2 ) tests of contingency analysis, followed by correspondence analysis to show the relationship between the variables. Shannon's diversity index (H ) of flowering plants in different seasons was applied to test the species richness among the flowering seasons using Multivariate Statistical Package (MVSP) version 3.22 [34].
Shannon's diversity index [35] where pi is the proportion of individuals of species in its species. All statistical analysis was performed in JMP statistical software version 5 to analyze the variation among variables [36].

Conclusions
Al-Baha Region is found to be a potential place for beekeeping practices and producing honey in local as well as international markets. The high demand by many local consumers is an indicator of its high preference. The plant diversity and environmental factors could be the secret behind the quantity and quality of the Al-Baha honey. The conservation of honey bee plant species is critical due to the increase in genetic loss of important honey bee plant species from naturally existing forests. The narrow population of these economic plant species cast a shadow on the purchasing process of honey products and increased price rate. All the bee forage plants under danger and deterioration can be propagated and conserved using in situ and ex situ techniques. Apart from this, variation of plants in blooming seasons may support the continuous flow of honey throughout the year. For sustainable and continuous honey production, urgent action has to be taken to protect the bee forage plant populations in arid and semi-arid areas of Al-Baha, as the floral diversity is dwindling due to harsh ecosystem components. Furthermore, the current research outcome exposes the increasing demand to conserve the floral diversity through the anticipation of think tanks from all related sectors, including scientists in collaboration with government and non-government agencies. Moreover, awareness creates endeavors in conservation for the local inhabitants of the Kingdom of Saudi Arabia.