Introduction

Pollination is primarily an animal-mediated phenomenon (Waser and Ollerton, 2006, cited in Wilmer, 2011). It is ecologically important as it is an essential component of reproduction through seeds for majority of plant species (Knight et al., 2005). Pollinators provide an essential ecosystem service that result in the outcrossing and sexual reproduction of many plants (Kudom and Kwapong, 2010). Wilmer (2011) reports, “many kinds of pollinators have been recorded for flowering plants including ants, bats, bees, beetles, birds, butterflies, and moths” (Wilmer, 2011).

Sunbirds are recognized as a very active pollinators of plants with bird-pollinated flowers (Wolf et al., 1975). Interestingly, flowers pollinated by birds (usually described as Ornithophilous flowers) are usually easily distinguished by a set of characteristics. These bird-pollinated flowers are mostly brightly coloured with the primary colour being red; making them attractive to birds and having a positive impact on the number of visitation towards these plants (Laubhann and Puff, 2002). Since birds are large, warm-blooded and require more energy compared to insects; therefore, plants with bird-pollinated flowers are often larger and tend to produce more nectar and often produce larger flowers to accommodate their avian visitors. However, there are bird-pollinated flowing plants like Lobelia cardinalis which secret no nectar; rather attract humming birds by mimicking more abundant, nectar producing flowing plants (Brown and Brown, 1979).

Sunbirds (Nectariniidae) are small birds with long, curved beaks. There are many species of sunbirds and they are one of the two major groups of pollinating (flower-visiting) birds in Africa. Constantly on the move, they feed on nectar and insects and can hover around briefly, (Fanshawe and Stevenson, 2002: cited in Wilmer, 2011).

Flowers differ in their morphology in several ways (tube-like structures to narrow tubes, spiral shapes, funnel-like, brush-like, amongst others). According to (Vogel, 1954, cited in Wilmer, 2011), colour and floral structure, including nectar production are some of the main factors determining the type of bird visitor that patronizes a flower. Plants may also invest more into floral structures in order to attract one particular bird visitor more than another (Stiles, 1978, cited in Wilmer, 2011). Thus it has been observed that, different floral structures attract different types of bird visitors (Vogel, 1954 cited in Wilmer, 2011). For example; narrow-tubular and brush flowers normally attract small birds with long beaks and tongues.

Competition is an interaction that may occur between individuals or species surviving on the same limited resource (energy, nutrients and space) (Gill, 1978). Competition can either be interspecific (between species) or intraspecific (within species). The principle that similar organism requires similar niche makes competition evident. Sunbirds are no exception to this; hence in the event of competition, different species device different means or strategy to cope with competition for limiting resources. Lara et al. (2015) reported that “species show a differential use of resources in the face of interspecific competition as a fundamental manner of achieving species coexistence” (Hutchinson, 1961; Schoener, 1974; Pyke, 1982). In order for some species to avoid or limit competition they often rely on resource partitioning; hence, this can be explained in both space and time.

Variation in floral types is the basis of the concept of pollination syndromes. This implies that different kinds of plants attract different visitors, cementing the mutualism and by implication, tend to make flowers increasingly specialist, and visitors increasingly selective (Wilmer, 2011). Characteristics of ornithophilous flower species are described as: (i) red corolla or calyces or bracts of spikes; (ii) long stout corolla tube; (iii) tightly imbricate spikes with stout long peduncle; (iv) high nectar production rate; and (v) low sugar concentration of floral nectar (Kato et al., 1993). Selection of plant species for this study was guided by principles (i), (ii) and (iii) above. Thus, in this study, we selected four plant species (Erythrina sp., Lilium sp., Callistemon citrinus and Spathodea campanulata) growing sympatrically in Kibale National Park, Uganda.The study investigated sunbirds visitation (species type, frequency and rate) to four sympatric plant species and partitioning of visitation over time of the day was also examined.

2 Materials and Methods

Materials which were used during our field work was; Binoculars, field note book, timer (wristwatch) and pen etc.

2.1 Study area

This study site is located in Kibale National Park, in western Uganda closed to the equatorial region. The Kibale National Park covers an area of 766 km² with geographical coordinates: 0^ʹ13ʹ-41ʹN, 30^°19ʹ-30^°32ʹ E. Kibale forest area was gazetted as a National Park in 1993 (Figure 1). The moist evergreen forest is transitional between lowland rain forest and montane forest (Chapman and Chapman, 1997).

The study was conducted in the vicinity of Makerere Biological Field Station. The altitude varies from 1 590 m in the northern extreme of the forest to 1 110 m in the southern part. The terrain of Kibale Forest is characterized by numerous hills, valleys, swamps and streams.

2.2 Data collection

Four different plants: African tulip tree or flame tree (Spathodea campanulata), Bottle brush (Callistemon citrinus), Erythrina sp. and Cana lily (Lilium sp.) from different locations around the park were selected. In our preliminary observation, these plant species attracted the same group of birds (sunbirds) with the same flower colours (red) which is the most attractive colour for birds (Pickens, 1951; Raven, 1972). For each plant species, 3 individuals were randomly selected and 10 flowers or inflorescences from each individual plant were randomly selected in order to assess the number of visit to flowers. For accuracy of data collection, one day of observation to a particular plant and identification of sunbirds visiting these plants was undertaken by each project team member alternatively. Actual data collection was conducted from 17^th to 20^th July 2014. For each plant species, the number of visits made by different sunbird species and individuals was recorded for 18 hours on the 4 focal plants. The time intervals for observation were 7:30-9:00 am, 9:30-11:00 am, 11:30-1:00 pm and 2:30-4:00 pm. Equal time interval of observation in different times of the day was developed as indicated in the matrix below (Table 1). Scan samples using binoculars were carried out every 10 minutes to record the behaviour of visiting sunbirds across the same time periods. Activities recorded were legitimate visits, illegitimate visits, feeding and perching.

2.3 Data analysis

All data generated from the primary and secondary sources were entered and organized in Microsoft Excel 2010. Descriptive statistics such as bar charts, tables and graphs were used to illustrate patterns and trends. Inferential statistics (Chi-square and Kruskal-Wallis tests) were used to test aspects of behaviour and visitation respectively.

3 Results

In this study, a total of eight species of sunbirds visiting the four plant species were found. Olive-bellied sunbird was the only visitor to all the four plant species, whilst the Green-headed, Collared, Olive, Copper and Blue-throated sunbirds were observed to have visited 3 out of the 4 plant species. In contrast, the Green-throated sunbird was the only one which restricted its visits to only one plant species (Spathodea). Seven out of the eight species of sunbirds visited Erythrina and Callistemon while six and two sunbird species visited Spathodea and Lilium respectively (Table 2).

Olive-bellied sunbird and Green-headed sunbirds had the highest frequency of visit to all plants with 133 and 132 respectively. However, Blue-throated sunbird and Green-throated sunbird had lowest frequency of visitation with 7 and 4 visits respectively (Figure 2).

Table 3 depicts a total of 1 485 flowers visited by eight species of sunbirds during 72 hours of observation.  Olive-bellied and Green-headed sunbirds were the most regular visiting birds with flower visits of 418 and 383 respectively. Blue-throated and green-throated sunbirds visited least regularly with a score of 22 and 17 flower visits respectively. The flowers of Erythrina and Callistemon received the highest number of visits with 461 and 464 respectively, and Lilium received the least number of visits 211.

Erythrina and Callistemon had the highest visitation rate per hour per flower (0.9 each) and Lilium with 0.4 visitation rate per hour per flower was the lowest (Table 4).

3.1 Pattern of visitation over time of day

When data for all sunbird visits to all plant species were pooled together, there was no significant difference in the median number of visits over time periods during the day (Kruskal-Wallis test: H=1.29, df=3 and P=0.73). However, there were several notable trends between plant species (Figures 3a-d) when assessing the visit behaviour of the most regular sunbird visitors. In Erythrina, early visitation by Olive-bellied sunbirds quickly diminished when Green-headed sunbird activity increased but increased again around noon; this coincided with a rapid decrease by the third main visitor, the Collared sunbird (Figure 3a). For Spathodea, the two main visitors were the Green-headed and Olive-bellied sunbirds and both displayed the same visit pattern, scarce early morning visitation was followed by an increase to a peak around mid-day and a decline thereafter (Figure 3b). All five main visitors to Callistemon were most active between 07:30 and 09:00 (Figure 3c). Only the Collared sunbird exhibited variation in visits after that time; whilst all other sunbird species ceased visiting by late morning, Collared sunbird visits picked up again towards mid-day. Olive-bellied sunbirds made over 92% (see Table 3) of visits to Lilium, peaking between 11:30 and 13:00 (Figure 3d).

3.2 Behavioural patterns

Of the behavioural data collected, a notable pattern was observed for feeding and perching; the proportion of visits for perching and feeding differed significantly (Chi-Sq = 7.988, df = 3, P=0.046). At all time period sunbirds of all species at all plants were largely feeding and the majority of visits involved probing for nectar.

4 Discussion

In this study, we found evidence for partitioning of visitation to four sympatric plants with sunbird species visiting between one and four of our focal plant species and exhibiting temporal trends. This might be due to intense competition among flower visiting sunbirds, variation in availability of nectar and difference in feeding and flower characteristics. However Brown and Brown (1979), had observed non selective foraging and visitation by all humming bird species to all nine flowing plant species in White Mountains of Arizona, due to their similar appearance and nectar rewards. A total of 8 species of sunbirds were recorded visiting the focal plant species. The Olive-bellied sunbird was the most common visitor, and was the only species to visit all four plant species, suggesting a very generalist feeding habit. The Green-throated sunbird was the only one which restricted its visits to flowers of only one species (Spathodea). The reason for this might be due to their feeding characteristics in which this sunbird visits this particular plant only to forage for supplementary food; in conformity with Fry et al. (2000), who found that Green-throated sunbirds mostly favour insects over nectar as a primary source of food. Or due its morphological details of its bill and flower which influences its foraging success (Gill and Wolf, 1978).

Seven out of the eight species of sunbirds visited Erythrina and Callistemon while six and two sunbird species visited Spathodea and Lilium respectively. This could be due to the ease of nectar accessibility from the former species as well as the quantity of nectar produced and stored in their flower. In the other two plants, the nectar is either not easy to access or there is low amount of nectar produced by the flower. This can be related to the work of (Vogel, 1954 cited in Wilmer, 2011), which states that different floral structures attract different types of bird visitors. For example; narrow-tubular and brush flowers normally attract small birds with long beaks and tongues. Wilmer (2011) stated that across nectar producing plants, the amount or volume of nectar is abundant in some plants and low in others, which makes a difference in the rate of visitation.

The rate of visitation per hour per flower was not consistent in all the focal plants and this may also reflect nectar availability at different times of the day. Total flower visitation for all sunbirds to our focal plants across all time intervals showed no significance difference, but clear patterns in visitation over time were evident within plant species. Activity of sunbirds on flowers was highest early in the morning in both Erythrina and Callistemon; the subsequent decline may be because these species do not replenish nectar later in the day. The same is true in Frost and Frost (1980), where feeding activity was higher in the morning due to high nectar availability. In contrast, a mid-day peak in visitation for Spathodea and Lilium suggests that these plants may have continuous nectar secretion during the day. This is supported by Bibby et al. (1992), who stated that birds are more active during early morning and late in the afternoon.

In Erithrina, visitation by Green-headed sunbirds increases as the morning progresses, whereas, Olive-bellied and Collared sunbird visitations begin to drop at the same time. This could be explained by the fact that during our observations, Green-headed sunbirds were highly territorial, chasing all other sunbirds while they approach to access food. And it has higher visitation rate to all our focal plants than the other seven sunbirds. This might be due their high energy demand as a result of competitive behaviour. Territoriality behaviour in male Golden-winged sunbirds in Kenaya, allows then to forage 72% more each than nonterritorial ones (Gill and Wolf, 1979), to maintain the energy balance (Gill, 1978). Additionally, the activity of Olive-bellied sunbirds is high during the mid-day in all focal plant species whereas the other sunbirds become less active. This indicates that the Olive-bellied sunbird may be less competitive, switching its foraging preferences, so it avoids competition from other sunbird species by foraging when the activity of the others decreased.

Feeding and perching activities, when compared with total visitation revealed that most of the visitors came to forage for nectar on our focal plants; thus potentially allowing pollination to take place. This supports the statement by (Waser and Ollerton, 2006 cited in Wilmer, 2011) that pollination is primarily an animal-mediated phenomenon, and that birds are recognized as very active pollinators of plants (Laubhann and Puff, 2002); hence in this instance sunbirds, constantly arrived to feed on nectar and (Fanshawe and Stevenson, 2002 cited in Wilmer, 2011).

Overall, our study produced patterns of visitation in all focal plant species by the eight sunbird species which suggests that some partitioning of visitation occurs between species and over time of day. There are aspects of nectar resource availability, together with competition and/or territoriality that require further investigation to discover the factors influencing interactions between co-occurring sunbirds and sympatric plant species competing for pollination services. Further studies might also involve investigating variation in pollen placement on visiting birds, an initial part of our preliminary discussions for this project, and plant reproductive success through pollinator efficiency measures. The relationship between visitor behaviour and plant morphology can provide information on increasingly specialized mutualisms and the drivers of evolutionary change.

Author’s contributions

All authors have designed and conducted the data collection and together undertake the data analysis task. In addition, all authors read and approved the final manuscript.

Acknowledgment

We would like to express our heartfelt gratitude to Tropical Biology Association (TBA) for the golden opportunity of attending this course. Also, many thanks go to Dr Nigel Mann and Dr Bruce Anderson for their unreserved assistance during the field observation and their supervision. Our deepest appreciation goes to Dr Clive Nuttman for his continuous follow-up and genuine support throughout our project.

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