Aspects of fruit digestion and selection in selected Southern African avain frugivores.

Abstract

Fruit-frugivore interactions play a central in maintaining the structure and diversity of ecosystems through their effects on seed dispersal. Because fruit selection and thus fruit removal represents the first stage in the seed dispersal process, understanding factors affecting fruit selection can play an important role in the formulation of sound conservation efforts especially light of the on-going habitat change. However, to date, the research is inconclusive as to factors affecting fruit selection as results have revealed inconsistent and controversial with a huge variation in fruit selection patterns between species and within individuals of the same species. The huge inter- and intra-specific variation in fruit selection patterns precludes any generalizations on fruit selection notwithstanding the research effort addressing the issue. One factor that could be attributed to this pattern is that most studies on fruit selection patterns in frugivorous birds have studied fruit attributes or physiological adaptations of frugivores to fruits in isolation. Because fruit profitability is affected by both pre- and post-ingestional factors, studying these factors in isolation deprives us of fresh insights into the fruit-frugivore interaction. Therefore by relating the physiological aspects of frugivores to fruit characteristics, this study aims to provide a link between the physiology of birds and their feeding ecology. Cape white-eyes (Zosterops virens), red-winged starlings (Onychognathus morio) and speckled mousebirds (Colius striatus) were used for this study. In the first part of this thesis, transit times and digestive efficiencies of birds fed equicaloric glucose and sucrose artificial fruit diets of varying concentrations were determined. Three concentrations were used: low (6.6%), medium (12.4%) and high (22%). Digesta transit times of birds increased with an increase in concentration for all diets but were generally higher on glucose diets. This finding has been widely reported in

other similar studies. The increase in digesta transit times with an increase in sugar concentration may be due to high nutrient density on high concentration diets which require a longer processing time. Intake rates, on the other hand, decreased with an increase in sugar concentration. The inverse relationship between food intake and nutrient levels has often been attributed to compensatory feeding which posits that birds respond to nutrient dilution by increasing intake to allow a constant flux of assimilated energy. Indeed, speckled mousebirds and Cape white-eyes maintained a constant assimilated energy intake on sucrose diets by modulating food intake rates. The apparent assimilation efficiencies of glucose diets for all species were comparable and typical of those found in other frugivorous birds. However, red-winged starlings displayed low assimilation efficiencies for sucrose diets and lost significant body mass on all sucrose diets. The lack of significant sucrase activity in this species was attributed to this finding. This study showed the importance of digestive physiology in explaining fruit selection patterns in frugivorous birds. The second part of this thesis assessed the deterrence effects of tannins which are ubiquitous secondary compounds in plant material and are known for their ability to bind to protein which reduces nitrogen availability in the diet. In this study, birds were fed artificial fruit diets containing varying levels of tannins (0%, 2.5% and 5%) in paired choice tests. It was predicted that tannins would have no effect at low concentrations but at higher concentrations would act as deterrents although the levels at which they would become deterrents would differ among species. Red-winged starlings preferred the control diet, were indifferent to the medium tannin diet and were deterred by the high tannin diet whereas speckled mousebirds and Cape white-eyes were not deterred at all concentrations. The discrepancy in the results was attributed to differences in taste sensitivity, tolerance levels and detoxification mechanisms of secondary compounds between species.

Occasional geophagy and consuming a broad diet were also implicated in producing the results obtained. Plant secondary compounds in fruits are diverse and their effects are similarly diverse and there is a possibility that different groups of secondary compounds generate disparate effects. Similar studies on other types of secondary compounds may thus contribute towards a broader understanding of the role of secondary compounds in mediating fruit-frugivore interactions. Overall, this study showed how diet affects ability to handle secondary compounds in fruits. The third part of this thesis addressed the influence of ethanol concentration on fruit selection in frugivorous birds. Because ethanol is ubiquitous in fruits and its concentration is positively correlated to fruit sugars, it has been suggested that because frugivores could use its odour to locate fruiting plants, they should select fruit with high ethanol concentrations. The aim of this study was to test this hypothesis by determining whether frugivorous birds show a preference for fruit laden with alcohol at levels equivalent to those of over-ripe fruits. Birds were provided with two artificial fruit diets in pairwise choice tests: an experimental diet containing 1% ethanol and an artificial fruit diet with no ethanol. For all species, there were no significant differences in the amount of fruit consumed between the two food types. These findings provided corroborating evidence to the suggestion that birds are unlikely to prefer over-ripe fruits compared to ripe fruits due to the negative impacts associated with ingesting ethanol at high concentrations. However, it could be possible that the lack of preference observed in this study was because the ethanol concentrations used were too low to be detected. Overall, this study suggests that at high concentrations, ethanol in fruits acts as a deterrent rather than an attractant. The last part of this thesis was conducted to determine the use of taste and olfaction by red-winged starlings in making foraging decisions. To determine whether they use taste in fruit selection, they were concurrently offered a control artificial fruit diet with another artificial fruit diet flavoured with different concentrations of ethanol and various fruit essences. To test whether they were able to use olfaction to locate food, they were provided with two choices: artificial fruit suspended over either banana and orange fruit essences and ethanol of varying concentrations or a control artificial fruit (without essence). It was hypothesized that (1) red-winged starlings have tasting ability which helps them in selecting fruits to feed on and that (2) red-winged starlings use olfaction to locate food. Results were consistent with the first hypothesis but inconsistent with the second one. Thus, red-winged starlings use taste when selecting fruits to feed on but do not use olfaction to locate fruit sources. The latter was unexpected because birds with olfactory bulb sizes similar to theirs exhibit advanced olfactory abilities. It was speculated that the lack of olfactory abilities in starlings could be attributed to the fact that this study was conducted outside of this species’ breeding season when olfactory abilities were likely to be lowest and also to that olfactory abilities may not have been important at the scale investigated in this study. Overall, the study showed that the sense of taste in birds plays an important role in making foraging decisions than currently appreciated. Overall, this thesis demonstrated the value of relating physiological attributes of frugivores to fruit attributes in acquiring deeper understanding of fruit-frugivore interactions. One particular advantage of the methodology employed in this study was that it controlled for covariance among fruit characters and also removed the confounding effects of as seed size and secondary compound composition. The shortcoming of this approach is related to the applicability of the results to the field conditions. Therefore an approach combining laboratory and field observations may produce results that may be important in informing us about how to manage our ecosystems.