Woody plants supporting insect pollinators in Chagga home Gardens, Northern Tanzania

J. Bio. & Env. Sci. 20 23 175 | Kingazi et al. RE RERE RESEARCH SEARCHSEARCH SEARCH PAPER PAPERPAPER PAPER OPEN ACCESS OPEN ACCESSOPEN ACCESS OPEN ACCESS Woody plants supporting insect pollinators in Chagga home Gardens, Northern Tanzania Nanyika Kingazi *1,2 , RPC. Temu 1 , Agnes Sirima 1 , Mattias Jonsson 3 1 College of Forestry, Wildlife and Tourism, Sokoine University of Agriculture (SUA), Tanzania 2Tanzania Forestry Research Institute (TAFORI), Tanzania 3Department of Ecology, Swedish University of Agricultural Sciences (SLU), Sweden Article published on July 16, 2023 Key words: Woody plants, Insect pollinators, Gardens, Tanzania Abstract Insects play a great role in the pollination of flowers in many agricultural systems, and they rely on floral resources for their survival. However, a significant decline and extinction of these crucial insects have been witnessed globally as a result of fragmentation and/or loss of their habitat such as floral resources using data from the Chagga home garden (CHGs), we aimed at (1) examining the composition and species richness of pollinator forage plants in the CHGs, (2) determining how elevation affects the diversity of pollinator forage species in CHG, (3) determining the temporal availability of pollinator forage plants in the CHGs, (4) determining the pollinator groups foraging on the plants in the CHGs, (5) determining the type of floral rewards for the insect pollinators in CHGs. It was observed that: (1)of the 302 wood species in the CHGs, 293 (97%) from 62 families were pollinator forage of which 170 species (58.02%) were trees while 123 species (41.98%) were shrubs; (2) pollinator forage species diversity decreased with increase in elevation gradient; (3) Flowering of the pollinator forage plants was spread throughout the year; (4) Bees were the most dominant group of plant visitors, visiting about 93% of the plants; (5) the majority of plants provided both pollen and nectar to insect pollinators. The results from this study suggest that traditional agroforestry systems such as Chagga home gardens can contribute to increasing the spatial and temporal availability of diverse floral resources for insect pollinators. * Corresponding Author: Nanyika Kingazi  nanyikakinga[email protected]om Journal of Biodiversity and Environmental Sciences (JBES) ISSN: 2220-6663 (Print) 2222-3045 (Online) Vol. 23, No. 1, p. 175-188, 2023 http://www.innspub.net J. Bio. & Env. Sci. 20 23 176 | Kingazi et al. Introduction The importance of pollinators' protection is underscored by the fact that they are essential for pollination of the majority of the world's wild flowering plants (Ollerton et al., 2011) and 75% of crop species (Klein et al., 2007). With regard to crop pollination, understanding factors influencing pollinator populations in farmlands is critical in designing conservation strategies that ensure their longtime survival in agricultural landscapes (Timberlake & Vaughan, 2019). Insect pollinators are the main pollinator group in agricultural areas and their population is affected by several factors including the availability of floral resources (nectar and pollen) and nesting sites in farmlands (Fowler et al., 2016). One way to ensure the availability of floral and nesting resources for insect pollinators in agricultural areas is by integrating trees and shrubs in farmlands (Bentrup et al., 2019; Centeno-Alvarado et al., 2023). The trees and shrubs in farmlands provide nesting sites and ensure floral resources availability for insect pollinators even when crops are not in bloom (Lowe et al., 2021). However, this depends on whether the integrated trees and shrubs species are suitable for insect pollinators such as supplying food resources in terms of pollen, nectar, or both as well as nest sites. The Chagga home gardens in Tanzania are one of the agricultural land use systems whereby farmers integrate trees and shrubs with crops and livestock in the same unit of land (Mbeyale &mcharo, 2022). The trees and shrubs in Chagga home gardens are either retained or planted for different purposes such as providing shade to the crops, especially bananas and coffee, fodder, live fences, and fruits (Soini, 2005). According to Hemp (2005), the Chagga home gardens maintain a high diversity of plants with over 500 plant species (including wood and herbaceous plants). However, despite of the high floral diversity of Chagga home gardens, there is little information concerning their potential in supplying floral and nesting resources to insect pollinators. Previous studies such as Arnold et al. (2021), Sawe et al. (2020), and Elisante et al. (2019) focused on assessing the pollination service of insect pollinator communities in the Chagga home garden and not their ecological habitat (floral resources and nesting sites). The diversity of pollinator forage plants in the landscape reflects the continuous supply of floral resources from different plant species and hence encourages the insect pollinators to remain on site (Mensah et al., 2017a). This is because trees and shrub species differ in flowering time and duration hence due to their intermittently flowering, they provide floral resources for insect visitors throughout the year (Torne-Noguera et al., 2014). Also, floral availability to insect pollinators in the landscape depends on the flowering time and spatial distribution of pollinator forage plants in the landscapes. In the Chagga home garden, farmers play a great role in determining the species composition in their garden since they plant or retain species based on their preferences and needs (Fernandes et al., 1985). However environmental factors such as elevation affects the composition of plant species in the landscape (Malizia et al., 2020). This paper aimed at quantifying the availability of forage resources to insect pollinators in CHGs. A survey was carried out in CHGs to: (1) examine the composition and species richness of pollinator forage plants; (2) determine how elevation affects the diversity of pollinator forage species in CHG; (3) determine the temporal availability of pollinator forage plants in CHG, (4) determine the pollinator groups foraging on the pollinator forage species in CHGs (5) determine the type of floral rewards among insect pollinators forage species in CHGs. The results from this study are a crucial part of formulating efficiency policies, plans, and strategies to manage and conserve insect pollinators in agricultural landscapes in Tanzania. Material and methods This study was conducted in the Moshi rural district in the Kilimanjaro region located on the lower slopes of Mount Kilimanjaro in northern Tanzania (Fig. 1). J. Bio. & Env. Sci. 20 23 177 | Kingazi et al. The district receives a bimodal rainfall pattern with a long rainy season around March and May and short rainfall around November and December (Appelhans et al. 2016; Røhr and Killingtveit 2003). The mean annual rainfall ranges between 600mm to 2000mm while the daily temperature ranges between 15 ◦C to 29 ◦C depending on location and elevation. Generally, agriculture is the main economic activity of the inhabitant in the district largely attributed to supportive climatic conditions for crops and tree growth. Due to shortage of land exacerbated by high population density, farmers tend to maximize their small homestead's land productivity by integrating different types of crops such as bananas, coffee, and beans; livestock such as cows and goats; and multipurpose trees and shrubs on the same piece of land. This system of farming is locally known as Chagga Home Gardens (CHGs). The CHGs are mainly practiced between 800m to 1900m elevation on the slopes of the mountain Kilimanjaro (Hemp, 2005) and the average garden/farm size is 0.68 ha with a range of 0.2 to 1.2 ha per farmer (Hemp, 2005; Fernandes et al., 1985). Fig. 1. Location of the study area showing the study plots (green cycles). Fig. 2. Examples of the structure and composition of Chagga home gardens. J. Bio. & Env. Sci. 20 23 178 | Kingazi et al. Selection of the study gardens Systematic random sampling was used to select 101 CHGs along six road transects that pass across elevation gradients (Fig. 1). The distance from one home garden to another was 1km and the distance from the road was 100 m. The number of selected CHGs in each road transect depended on the length of the road. Data collection for the whole study was conducted between January and December 2022. Data collection methods In each CHG plot, we started by measuring the size of the home garden, and thereafter identified and counted all trees and shrubs. To determine whether the integrated trees and shrubs are pollinator forage, we monitored their phenology, especially flowering time, and whether they were visited by insect pollinators. This was done by conducting regular visits (at least once per month) in the year 2022. During each visit, we observed and recorded all the flowering trees and shrubs that were visited by insects that are considered pollinators (bees, butterflies, flies, and beetles)(Ollerton, 2017). The insect visitations to the flowers were observed between 9:00 am – 5:00 pm and the plants were considered as pollinator forage if an insect spent at least 5 seconds in the flower (Waykar & Baviskar, 2015). The types of floral rewards (nectar, pollen, or both) were determined by direct observation of the insect visitor’s activity with the flower. When insect’s activity with the flowers extended their proboscis the plant flower was considered a nectar source and when insects carried pollen on their body, the plant was considered a pollen source (Onyango et al. 2019; Waykar and Baviskar 2015). In case where the insect’s activity to the flower extended its proboscis and also carried pollen on its body, the plant was considered both a pollen and nectar source (Onyango et al., 2019). Data analysis Descriptive analysis such as tables and figures was used to summarize the results in an Excel spreadsheet. R software version 4.1.3 (R Core Team, 2022) was used to calculate the Shannon diversity index of pollinator forage species in CHGs as well as calculate the Pearson correlation coefficient between forage species diversity and elevation. Thereafter, we used the function "ggplot2" in R software to plot the correlation between forage species diversity and elevation in the CHGs. Results Pollinator forage species composition in CHG A total of 302 wood species were identified in CHG and out of them, 293 (97%) species belonging to 62 families were insect pollinators forage (Appendix 1). The Fabaceae family had the highest number of forage species (n = 47, 15.8%), followed by Euphorbiaceae and Solanaceae (n = 18, 6.1% each). Most of the pollinator forage species were trees whereby out of 293 insect pollinator forage species, 170 species (58.02%) were trees while 123 species (41.98%) were shrubs. Among the tree forage species, native species were somewhat higher than exotic, whereby out of the 170 tree species, 88 species (51.8%) were native while 82 species (48.2%) were exotic. Similarly, native pollinator shrub species were somewhat higher than exotic whereby out of 123 shrub species, 63 species (51.2%) were native and 60 species (48.8%). Table 1a and 1b indicate the 10 most dominant forage species in CHG based on frequency of occurance in the sample gardens. Table 1. The 10 most dominant insect pollinated tree species in the Chagga home gardens. SN Forage species Family Origin Frequency of occurrence out of 101 plots 1 Grevillea robusta Proteaceae Exotic 81 2 Persea americana Lauraceae Exotic 74 3 Rauvolfia caffra Apocynaceae Native 65 4 Mangifera indica Anacardiaceae Exotic 62 5 Albizia schimperiana Fabaceae Native 61 6 Cordia africana Boraginaceae Native 44 7 Cascabela thevetia Apocynaceae Exotic 41 8 Eriobotrya japonica Rosaceae Exotic 41 9 Markhamia lutea Bignoniaceae Native 40 10 Psidium guajava Myrtaceae Exotic 37 J. Bio. & Env. Sci. 20 23 179 | Kingazi et al. Table 2. The 10 most dominant insect pollinated shrub species in the Chagga home gardens. SN Forage species Family Origin Frequency of occurrence out of 101 plots 1 Duranta repens Verbenaceae Exotic 59 2 Solanum incanum Solanaceae Native 51 3 Lantana camara Verbenaceae Exotic 49 4 Bougainvillea glabra Nyctaginaceae Exotic 30 5 Morus alba Moraceae Exotic 30 6 Caesalpinia decapetala Fabaceae Exotic 29 7 Manihot esculenta Euphorbiaceae Exotic 25 8 Solanum nigrum Solanaceae Native 25 9 Tithonia diversifolia Asteraceae Exotic 22 10 Coffea arabica Rubiaceae Exotic 21 Effect of elevation on diversity and spatial distribution of insect pollinator forage species Although in CHGs farmers play a great role in the type of species to include in their garden, it seems that the composition of pollinator forage species in CHGs is also affected by elevation. Some species were dominant in the lower elevation but were not present or not performing well in the mid or higher elevation and vice versa (Tables 7,8 and 9). There was a significant negative correlation between forage species diversity and elevation whereby as elevation increased, pollinator forage diversity decreased (Fig. 5, R = -0.29, p = 0.002 Fig. 3. Relationship between forage species shannon diversity and elevation (m). Table 3. The 10 most dominant pollinator forage trees and shrub species in lower elevation <1000m in CHG. SN Tree forage species Family Floral reward Shrub forage species Family Floral reward 1 Cascabela thevetia Apocynaceae Nectar Lantana camara Verbenaceae Nectar 2 Senna siamea Fabaceae Pollen Solanum incanum Solanaceae Pollen 3 Grevillea robusta Proteaceae Nectar and pollen Bougainvillea glabra Nyctaginaceae Nectar and pollen 4 Mangifera indica Anacardiaceae Nectar Duranta repens Verbenaceae Nectar and pollen 5 Leucaena leucocephala Fabaceae Nectar and pollen Manihot esculenta Euphorbiaceae Nectar 6 Cordia africana Boraginaceae Nectar and pollen Senna occidentalis Fabacea Pollen 7 Commiphora zanzibarica Burseraceae Nectar and pollen Tithonia diversifolia Asteraceae Nectar and pollen 8 Markhamia lutea Bignoniaceae Nectar and pollen Caesalpinia decapetala Fabaceae Nectar and pollen 9 Rauvolfia caffra Apocynaceae Nectar and pollen Vernonia brachycalyx Asteraceae Nectar and pollen 10 Persea americana Lauraceae Nectar and pollen Caesalpinia pulcherrima Fabaceae Nectar and pollen Table 4. The 10 most dominant pollinator forage trees and shrub species in CHGs in mid-elevation 1001 - 1500m. SN Tree forage species Family Floral reward Shrub forage species Family Floral reward 1 Grevillea robusta Proteaceae Nectar and pollen Duranta repens Verbenaceae Nectar and pollen 2 Persea americana Lauraceae Nectar and pollen Solanum incanum Solanaceae Pollen 3 Albizia schimperiana Fabaceae Nectar and pollen Caesalpinia decapetala Fabaceae Nectar and pollen 4 Mangifera indica Anacardiaceae Nectar Lantana camara Verbenaceae Nectar 5 Rauvolfia caffra Apocynaceae Nectar and pollen Morus alba Moraceae Nectar and pollen 6 Cordia africana Boraginaceae Nectar and pollen Bougainvillea glabra Nyctaginaceae Nectar and pollen 7 Cedrela toona Meliaceae Pollen Manihot esculenta Euphorbiaceae Nectar 8 Markhamia lutea Bignoniaceae Nectar and pollen Vernonia brachycalyx Asteraceae Nectar and pollen 9 Senna spectabilis Fabaceae Pollen Coffea arabica Rubiaceae Nectar and pollen 10 Margaritaria discoidea Phyllanthaceae Nectar and pollen Stachytarpheta jamaicensis Verbenaceae Nectar and pollen J. Bio. & Env. Sci. 20 23 180 | Kingazi et al. Table 5. The 10 most dominant pollinator forage trees and shrub species in CHGs in higher elevation>1500m. SN Tree forage species Family Floral reward Shrub forage species Family Floral reward 1 Eriobotrya japonica Rosaceae Nectar and pollen Duranta repens Verbenaceae Nectar and pollen 2 Persea americana Lauraceae Nectar and pollen Lantana camara Verbenaceae Nectar 3 Grevillea robusta Proteaceae Nectar and pollen Coffea arabica Rubiaceae Nectar and pollen 4 Rauvolfia caffra Apocynaceae Nectar and pollen Solanum incanum Solanaceae Pollen 5 Albizia schimperiana Fabaceae Nectar and pollen Morus alba Moraceae Nectar and pollen 6 Prunus persica Rosaceae Nectar and pollen Stachytarpheta jamaicensis Verbenaceae Nectar and pollen 7 Cussonia arborea Araliaceae Pollen Cyphomandra betacea Solanaceae Nectar and pollen 8 Callistemon speciosus Myrtaceae Nectar and pollen Rubus fruticosus Rosaceae Nectar and pollen 9 Psidium guajava Myrtaceae Nectar and pollen Tithonia diversifolia Asteraceae Nectar and pollen 10 Mangifera indica Anacardiaceae Nectar Euphorbia pulcherrima Euphorbiaceae Nectar and pollen Temporal availability of pollinator forage species in CHG The general pattern of flowering time of pollinator forage species indicates the availability of forage resources throughout the year (Fig. 3). The flowering time for most species overlapped, however, the period from November to January was the one at which most pollinator forage species produced flowers (from 95 to 82 species for native and 92 to 88 species for exotic). The distribution of duration of the flowering period of pollinator forage species revealed great variation between native and exotic species (Fig. 4). The duration of the flowering period for most native species is 3 and 12 months while for exotic species, the majority of them flower throughout the year (12 months). Fig. 4. Flowering time of pollinator forage plants in CHGs. Fig. 5. Duration of the flowering period of pollinator forage species in CHGs (months). Pollinator groups visited forage plants The Pollinator forage species in the CHGs were visited by different insect pollinator groups during the survey (Fig. 7). Bees were the most dominant group that visited 275 (141 native, 134 exotic) out of 293 forage species in CHGs, followed by butterflies that visited 127 (61 native, 65 exotic) pollinator species. Wasps visited 74 (37 native, 37 exotic) plant species while flies visited 61 (26 native, 35 exotic). Beetles were the least pollinator group that visited only 50 (20 natives, 50 exotic) forage species out of 293. Of the 275 forage species visited by bees, 152 were trees and 123 were shrubs. Butterflies visited 66 trees and 61 shrubs. Wasps, flies and beetles visited 40 and 35, 35 and 28, and 23 and 28 trees and shrubs respectively. Fig. 6. Number of pollinator forage species that were visited by different pollinator groups. Floral rewards from pollinator forage species in the home gardens The pollinator forage species in the CHG provided different floral resources (nectar, pollen, or both) to insect pollinators. Majority of them 189 (63.6%) out of 293 pollinator forage species provided both pollen and nectar to insect pollinators. In the remaining plants, 26 (9.4%) species provided only pollen while 78 (26.9%) species provided only nectar (Fig. 6). J. Bio. & Env. Sci. 20 23 181 | Kingazi et al. Fig. 7. Number of pollinator forage plants in the CHG and type of their floral rewards to insect pollinators. Table 6. The 10 most dominant species provided both nectar and pollen to insect pollinators. SN Forage species Family Life form Origin Estimated number of flowers/inflorescences 1 Grevillea robusta Proteaceae Tree Exotic >1000 2 Persea americana Lauraceae Shrub Exotic >1000 3 Rauvolfia caffra Apocynaceae Tree Native >1000 4 Albizia schimperiana Fabaceae Tree Native >1000 5 Duranta repens Verbenaceae Shrub Exotic 100-1000 6 Cordia africana Boraginaceae Tree Native >1000 7 Eriobotrya japonica Rosaceae Tree Exotic >1000 8 Markhamia lutea Bignoniaceae Tree Native >1000 9 Psidium guajava Myrtaceae Tree Exotic >1000 10 Leucaena leucocephala Fabaceae Tree Exotic >1000 Table 7. The 10 most dominant species provided only nectar to insect pollinators. SN Forage species Family Life form Origin Estimated number of flowers/ inflorescences 1 Mangifera indica Anacardiaceae Tree Exotic >1000 2 Lantana camara Verbenaceae Shrub Exotic 100 - 1000 3 Cascabela thevetia Apocynaceae Tree Exotic >1000 4 Manihot esculenta Euphorbiaceae Shrub Exotic 100-1000 5 Acrocarpus fraxinifolius Fabaceae Tree Exotic >1000 6 Manihot glaziovii Euphorbiaceae Tree Exotic >1000 7 Diospyros fischeri Ebenaceae Tree Native >1000 8 Cestrum nocturnum Solanaceae Shrub Exotic 100-1000 9 Odontonema cuspidatum Acanthaceae Shrub Exotic 100-1000 10 Harrisonia abyssinica Rutaceae Tree Native >1000 Table 8. The 10 most dominant species provided only pollen to insect pollinators. SN Forage species Family Life form Origin Estimated number of flowers/ inflorescences 1 Solanum incanum Solanaceae Shrub Native 10-100 2 Senna siamea Fabaceae Tree Exotic >1000 3 Senna spectabilis Fabaceae Tree Exotic >1000 4 Solanum nigrum Solanaceae Shrub Native 10-100 5 Senna occidentalis Fabaceae Shrub Exotic 100-1000 6 Cedrela toona Meliaceae Tree Exotic >1000 7 Trichilia emetica Meliaceae Tree Native >1000 8 Cedrela odorata Meliaceae Tree Exotic >1000 9 Jacaranda mimosifolia Bignoniaceae Tree Exotic >1000 10 Sorindeia madagascariensis Anacardiaceae Tree Native >1000 Discussion Many previous studies have reported a positive relationship between floral resources with abundance and diversity of insect pollinators (Plascencia & Philpott, 2017; Fowler et al., 2016; Grundel et al., 2010). This study provides evidence for the potential of traditional agroforestry systems to supply forage resources to insect pollinators by exploring the availability of insect pollinator forage species in Chagga home gardens. It was found that 1) 97% of woody plants in Chagga home gardens were pollinator forage plant species; 2) pollinator forage plant's flowering period was spread throughout the year 3) the majority of plants provided both pollen and nectar to insect pollinators 4) Bee was the most dominant group visiting 93% of all pollinator forage plants 5) Nesting sites were mainly provided by native tree species and 6) pollinator forage species diversity decreased with increase in elevation gradient. Two hundred and ninety-three wood species (accounting for 97% of all wood plant richness in the selected CHG) with highly diversified families were identified as sources of nectar and/or pollen for insect pollinators. The diversity of pollinator forage plants suggests the diversity of flowers and differences in plant nectar and/or pollen quality (Hülsmann et al., 2015; Di Pasquale et al., 2013; Blüthgen & Klein, 2011) which are prerequisites to attracting and maintaining insect pollinator population. Floral resources (nectar and/or pollen) from different pollinator forage plants may be more nutritious than nectar and pollen from single plant species (Blüthgen & Klein, 2011). J. Bio. & Env. Sci. 20 23 182 | Kingazi et al. Therefore, the diversity of pollinator forage plants in the Chagga home gardens provides balanced nutrition for insect pollinators through nectar and/or pollen from different plant species (Blüthgen & Klein, 2011). In this study, it was found that pollinator-foraging plants in the Chagga home garden flower intermittently throughout the year as expected in a landscape with high plant diversity (Mensah et al., 2017). The variation flowering period in addition to the diversity of pollinator forage plants in CHG increases the temporal availability of forage resources to insect pollinators (Blüthgen & Klein, 2011). Some of the pollinator forage plants flower at the same time providing insect pollinators an advantage for resource specialization and differential visiting (Taki et al., 2011). Moreover, the majority of plants in CHG provided both pollen and nectar resources to insect pollinators. Insect pollinators especially bees need both pollen and nectar to meet their nutritional needs (IPBES, 2016). Hence, integrating different wood species in their farmland encourage insect to remain in their fields and pollinate crops. Bees were the most dominant pollinator group visited almost all pollinator forage plants in CHG. This may be because bees are generalist foragers as they fully depend on nectar and pollen for their survival (Rollin et al., 2013). The high abundance of plants that supports bees could be beneficial for crop pollination since bees are the most important pollinator group in agricultural areas (Patel et al., 2021). Moreover, trees especially old natives were the ones providing nesting sites to insect pollinators. This suggests that planting trees in farmlands help in conserving insect pollinators by providing them with nesting site. The decrease in diversity of pollinator foraging plants as the elevation gradient increase may be due to the harsh climatic condition that does not support some plants to survive and perform well. Conclusion This study suggests that traditional agroforestry systems such as Chagga home gardens can support insect pollinators. Given the pollinator forage plant species richness in the Chagga home garden, different forage species produce different flowers that provide diverse nutritional resources to insect pollinators. 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