An Evaluation of Israeli Forestry Trees and Shrubs As Potential Forage Plants for Bees

An evaluation of Israeli forestry trees and shrubs as potential forage plants for bees

Tamar Keasar(1) and Avi Shmida(2)

(1)  Department of Science Education - Biology, University of Haifa – Oranim, Tivon 36006, and Dept. Life Sciences, Achva College, Mobile Post Shikmim 79800, Israel.

(2)  Department of Evolution, Systematics and Ecology and Center for the Study of Rationality, Hebrew University, Jerusalem 91904, Israel.

Corresponding author: Dr. Tamar Keasar, phone: 972-52-871-8860, fax: 972-4-953-9608; e-mail:

Key words: forestry; honeybee; nectariferous plant; nectar production.

ABSTRACT

Loss and fragmentation of foraging habitats limit honeybee populations in Israel. This problem can be alleviated by the planting of bee forage plants in forests, parks, and along roadsides. To provide recommendations for such planting, we combined a literature survey and qualitative evaluations of experts to compile a list of 266 local wild plant species that have high food potential for bees. We also quantitatively evaluated the food potential of 32 species of trees and shrubs planted by the Israeli Forestry Service. We recorded the following parameters of each species: main flowering season; flower morphology; type of food reward; number of flowers per plant; nectar standing crop; hourly nectar production rate; type of insect visitors; and frequency of insect visits. We ranked the surveyed species according to their potential importance as food plants, assigning high ranks to species that (a) bloom between July and February (the period of dearth in flowering natural vegetation), (b) produce large amounts of nectar, (c) are highly attractive to honeybees. Of the species surveyed, Amygdalus communis, Eucalyptus camaldulensis, Ceratonia siliqua, and Ziziphus spina-christi best combined these benefits. A regression model indicated that nectar production rates, but not the other plant parameters measured, significantly explain differences among species in insect visitation rates. Our study highlights the importance of diversified forestry planting to address agricultural, conservation, and recreational needs.

INTRODUCTION

Populations of honeybees and other pollinating insects have been decreasing worldwide in recent years, limiting the reproduction of food crops and wild plants (Allen-Wardell et al., 1998). A major reason for these population declines is loss and fragmentation of natural and agricultural foraging habitats for bees, along with their flora (Kremen et al., 2002; Goulson, 2003). Food limitation for honeybees may be particularly severe in Israel, because colonies are kept at high densities (95,000 colonies at 6,100 forage points on less than 7,000 km2, Israel Honey Board, 2008).

The planting of forage plants for bees in non-agricultural and open areas can help sustain honeybee populations, and thus improve honey production and pollination services. Such planting is already in practice in field margins and small gardens in some countries (Carvell et al., 2006; Comba et al., 1999; Dag et al., 1998). Recent work has aimed at identifying the plant species that are most attractive to pollinators for such planting (Pontin et al., 2006). Designing forest areas for apiculture has been suggested in the US, especially for small privately owned plots (Hill and Webster, 1995).

The Israeli Forestry Service (Keren Kayemet Leisrael, KKL) is in charge of public planting of trees and shrubs in forests, parks, and along roadsides in Israel. Planting is designed to answer a combination of needs, such as prevention of soil erosion and desertification, stabilization of sand dunes, and formation of recreation sites (http://www.kkl.org.il/kkl/english/main_subject/forest_and_places/fgeneral/kkl%20afforestation%20work.htm). Enhancement of foraging areas for honeybees may also be achieved in planted forests, and requires the use of pollinator-friendly plant species. The present work aims to form recommendations for trees and shrub species that are suitable as food plants for bees, and that also meet additional forestry needs in Israel. This aim is compatible with current KKL policy to diversify the species used in forestry (Ginsberg, 2006).

Our immediate goal was to provide information about the foraging value of a number of specific trees and shrubs for honeybees. We addressed this goal both qualitatively and quantitatively. The qualitative approach consisted of compiling a list of local plant species that are attractive to insects, based on a literature survey, personal information, and consultations with experts. For the quantitative evaluation, we sampled 32 species, in use or under testing by the Israeli Forestry Service, for food value and insect visit rates. We selected only trees and bushes for the quantitative evaluation, while the qualitative list additionally covers herbaceous species. We considered both local and introduced species in the quantitative evaluation, while the qualitative list includes local species only.

More generally, we sought to identify which plant/flower traits most affect pollinator attraction in an interspecific comparison. These traits should be measured in the evaluation of further potential plant species. For this purpose we recorded several floral and plant parameters, which were previously shown to influence pollinator attraction to plants within species: The number of flowers per plant (Brody and Mitchell, 1997; Goulson et al., 1998), nectar standing crops (Hodges, 1995; Pappers et al., 1999), nectar production rates (Delph and Lively, 1992; Mitchell, 1993), and parameters of floral morphology (Conner and Rush, 1996; Galen and Stanton, 1989). We tested the contribution of these parameters to the variability in visit rates among the plant species of our survey.

METHODS

Qualitative evaluation

A list of local bee forage plants was compiled based on data by Dag et al. (1993, 1998), Fahn (1948), Gindel (1951), Lupo & Eisikowitch (1987), Reves (2004), and Zohary (1947). It was updated based on consultations with researchers from the Israeli Agricultural Research Organization (Arnon Dag, Haim Efrat, Sima Kagan, Yossi Slabezki), Tel Aviv University (Dan Eisikowitch) and Haifa University (Ofrit Shavit). We also consulted with the following beekeepers: Tomer Erez (Klil), Shalom Israeli (Ayelet Hashachar), Yehuda Kendel (Kfar Pines), Pini Nahmani (Yokneam), Shmuel Nir (Eilon), Noga Reuven (Manot), Hagai Schitzer (Gamla), Ya'akov Stam (Kfar Kish), Uri Surkin (Ein Harod Meuchad), Dan Weil (Yad Mordechai Pollination Services) and Eitan Zion (Yad Mordechai Apiary). The updating process allowed us to reduce an initial list of 562 potential honeybee forage plants to 266 species. Data on the plants’ distribution and abundance in Israel and on their phenology were obtained from our Ecological Data-Base of the Israeli Flora (Shmida and Ritman, 1985).

Quantitative evaluation

Selection of plant species

The surveyed plant species are a subset of the assemblage of trees and shrubs that are grown in KKL’s nurseries for wide-scale planting in forests, open areas, roadsides and parks, or for experimental planting and evaluation. We surveyed species that were considered attractive for bees, based on qualitative preliminary observations by our team and by the staff of KKL, the Shaham agricultural extension service, and the Volcani Center Dept. of Horticulture. We biased the survey toward plants that bloom in summer, autumn, and winter (July – February), since this is the period of dearth in floral food resources in Israel. The food potential of several Eucalyptus species for bees was assessed by a different research team (Eisikowitch and Dag, 2003). We therefore restricted our survey of Eucalyptus sp. to four common species that were sampled in autumn. On each day of the survey, 2-3 individuals of one species were observed. Most species were studied for two days (totaling 4-6 individuals), but some of the species were observed more intensively (see Table 2). Most observations were carried out in KKL nurseries, forests, and parks in Israel’s coastal plain and Negev desert. Repeated observations were conducted at different locations and flowering seasons to reduce local effects. The survey species, numbers, and months of observation are detailed in Table 2.

Plant and flower morphology

We counted the total number of flowers of surveyed individuals whenever possible, and estimated the number of flowers by counting a sector of the plant in individuals that were too large for complete counting. We recorded the following parameters of floral morphology in ten flowers from each of three individuals per species: total length of the flower (from the base of the tube to the tip of the corolla); length of the tube; and maximal diameter of the corolla.

Nectar measurements

When sampling three individuals of a species, we determined nectar standing crops for ten flowers per plant on each sampling day. When sampling two individuals, we measured nectar standing crops from 16 flowers per plant. Thus, nectar measurements are based on 30-32 flowers per sampling day. We used 1-µl or 5-µl micropipettes to measure nectar volumes, and Bellingham-Stanley hand-held refractometers to measure sugar (w/w %) concentrations. Sugar concentrations could be measured only for nectar standing crops that exceeded 1/3 µl. We bagged ten sampled, depleted flowers (3-5 per plant) with bridal-veil netting (Wyatt et al., 1992), and harvested them again after 24 h. The nectar that accumulated in the sampled flowers represents the plant’s 24 h nectar production. We divided the produced nectar volume by the covering time to obtain hourly per-flower nectar production rates. We calculated mean per-plant nectar production rates for each species by multiplying the mean per-flower production rate by the mean number of flowers per plant. The logarithm of this rate was defined as the species’ nectar score.

Insect visits

We observed each plant for insect visits for 10 minutes on each observation day. The observation unit was a patch of flowers on the plant that allowed convenient recording of visits. A visit was defined as a touch of the corolla, the stigma, or the stamen by an insect. We did not record numbers of arrivals to the patch, which generally correlate with the number of visits (Bar-Shai, 1995). Observations were conducted during peak pollinator activity (typically between 10-12 am). We classified the pollinators into the following functional groups: honeybees, large bees (larger than honeybees), small bees (smaller than honeybees), flies, butterflies, and beetles. We noted nectar-extraction behavior and loading of pollen sacs. Accordingly, we classified the visitors’ food reward as pollen, nectar, or both. We recorded the number of flowers observed per individual (usually 100), and calculated the 60-minute visit rate per flower.

Insect visit rates may vary widely between dates and locations because of differences in weather conditions, proximity to honeybee colonies, or composition of the surrounding plant community. To partially correct for these confounds, we used Rosmarinus officinalis as a reference species. Immediately after recording insect visits to a survey species, we counted visits to nearby R. officinalis shrubs using the same protocol. R. officinalis was selected as a reference because it is abundant, has a long flowering season (August – April) and is frequently visited by honeybees. R. officinalis did not grow in all the survey sites, and some of the survey species were observed outside its flowering season. The reference observations could thus only be obtained for some of the survey plants (see Table 5).

Regression model

We tested which floral and plant parameters best predicted insect visitation rate on a between-species basis, and thus should be measured in future evaluations of additional plant species. We defined the mean per-species visit rates as the dependent variable in a regression model. Mean per-species nectar standing crops, nectar production rates per flower, number of flowers, nectar score, flower length, tube length, and corolla diameter were treated as independent variables.

RESULTS

Qualitative survey

Table 1 lists 266 species from the native floral that were proposed as bee forage plants in the qualitative survey, out of an initial list of 562 potential plants. The table also reports these species’ main food reward, and scores for their distribution and abundance in Israel. The seasonal distribution of blooming peaks of the potential forage species is shown in Fig. 1. The seasonal frequency of species at peak bloom is also plotted for the whole flora of Israel, for the sake of comparison. The plots show that the period between July and February is characterized by a low number of flowering local species in general, and bee forage plants in particular. This period comprises a dry season between July and November, and a rainy, cold one between December and February. These seasons of floral dearth are therefore difficult for honeybee survival, and forage plants that flower during the dearth period should be particularly useful. We therefore biased our quantitative survey towards the subset of forage plants in Table 1 that bloom outside spring. With this consideration in mind, we also included non-native species in the quantitative evaluation. We relied on the information of Table 1 to focus on species that are widespread in Israel, and attractive to insects. These considerations further aided in the selection of species for the quantitative survey.

Quantitative evaluation

The species that were included in the quantitative survey are listed in Table 2. Species that were studied during the period of floral dearth are shaded in the Table. Table 3 lists the plants’ growth form, cultivation status, height (measured for only part of the species), number of flowers per plant, and the parameters of floral morphology. Column 2 of Table 4 provides a classification of the survey species according to their main food reward to pollinators (nectar (N), pollen (P), or both (N+P)). This classification is based on qualitative observations of pollinator behavior, and does not express the amount of nectar and pollen produced per plant. A quantitative assessment of a plant’s food potential should take into account its average size (i.e., number of flowers, Table 3) and the quantity of food reward produced per flower (Table 4). In the present study, we quantified per-flower nectar production, but not per-flower pollen yields. The product of the mean number of flowers per plant and the mean per-flower nectar production rate provides an estimate of per-plant nectar production rates (Table 4, column 6). We observed large variations in per-plant production rates both within and among species. To facilitate among-species comparisons, we defined a plant’s “nectar score” as the base-10 logarithm of its mean per-plant production rate (Table 4, column 7). Nectar scores for our survey species ranged between 1.5 and 4.5, i.e., across three orders of magnitude of per-plant nectar production rates. The species with the highest nectar scores (above 4.0) appear shaded in Table 4. These species have large numbers of flowers per plant, high nectar production rates per flower, or both. Table 5 lists the main pollinator groups for each of the studied species, mean visit rates, and, when available, insect visitation rates relative to visits to R. officinalis.