THE RESPONSE OF TWO AVIAN NECTARIVORES TO INTERRUPTIONS IN FOOD AVAILABILITY

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GENERAL INTRODUCTION AND OUTLINE OF THE STUDY

Energy is essential for metabolic processes, activity, growth and reproduction of all animals. Thus, animal survival and fitness greatly depend on the regulation of energy intake. It is therefore not surprising that a comprehensive literature has focused on the foraging behaviour of animals that underlies energy and nutrient intake. Optimal foraging theories predict that animal fitness depends on the efficiency of foraging, and that animals forage so as to maximize their fitness (Pyke et al. 1977). When the nutrient or energy content of a food source is low, animals ingest larger amounts. This is commonly known as compensatory feeding, and can be observed in various animal taxa (Karasov and Martínez del Rio 2007). Animals also increase their food intake after periods of food deprivation to compensate for an energy deficit (Zubair and Leeson 1996). When energy demands increase, such as during exercise, reproduction or cold exposure, food intake is also increased (Starck 1999). .
As in a chemical reactor, the performance of animal intestines can be estimated from nutrient conversion efficiency, reaction time, digesta retention time, intestinal volume and the flow rate of digesta (Karasov and Martínez del Rio 2007). After early models of digestion were proposed (Penry and Jumars 1987), later work incorporated nutrient breakdown and absorption into the models to predict the ingestion rate that maximizes an animal’s net rate of nutrient absorption (for a review see McWhorter 2005). Experimental and theoretical studies of animal foraging behaviour and energy assimilation demonstrate the interplay between the behavioural regulation of food intake and digestive efficiency (Martínez del Rio and Karasov 1990). My research focuses on the interaction between compensatory feeding and physiological constraints in nectarivorous birds exposed to energetically challenging conditions. I investigated whether these birds can match energy intake to their energy expenditure when experiencing variations in food quality and availability and metabolic requirements. In the following sections, I will introduce nectar as a food source and the avian nectarivores that consume it, before moving on to energetic challenges in these birds and the outline of my research.

Nectar as food source

Nectar is one of the most common foods, produced by plants as a reward for pollinators or defenders against herbivores (Nicolson 2007a). Nectar consumers come from a wide taxonomic range. A wide variety of insects feeds on nectar, including beetles (Coleoptera), true flies (Diptera), butterflies and moths (Lepidoptera) and bees, wasps and ants (Hymenoptera) (Nicolson 2007a). Vertebrate nectarivores embrace various bird and bat species (Nicolson and Fleming 2003a; Nicolson 2007a).
Many non-flying mammals, including rodents, marsupials and primates, also visit flowers to feed on nectar, and play a role in plant pollination (Wiens et al. 1983; Carthew and Goldingay 1997). Lizards have also been identified as common nectar consumers, especially on islands (Olesen and Valido 2003). In addition, birds and mammals that are specialized on other diets also feed on nectar occasionally (Garber 1988; Symes et al. 2008). Not all nectar consumers benefit the plants: unwanted visitors include nectar thieves, which are morphologically unsuited to pollinate flowers, and nectar robbers, which puncture the base of flowers to access nectar (Nicolson 2007a). What makes floral nectar such a desirable food source? Nectar is an easily digested food and rich in energy. It contains sugars predominantly in the form of the disaccharide sucrose or the monosaccharides glucose and fructose (Nicolson and Fleming 2003a). Nectar may also contain other sugars, such as xylose, which remains puzzling because pollinators are averse to this sugar (Jackson and Nicolson 2002). Besides sugar and water as major components, nectar further contains inorganic ions, enzymes, amino acids and lipids (Nicolson and Fleming 2003a; Nicolson 2007b; Nicolson and Thornburg 2007). Secondary compounds found in nectar, such as phenolics, alkaloids and terpenoids, may be toxic or repellent to some nectar consumers, while they attract others (Nicolson and Thornburg 2007).
Nectar sugars are synthesized in the nectary of flowers or derive from sucrose transported in the phloem sap (Nicolson and Thornburg 2007). The enzyme invertase, which is found in the nectary, hydrolyzes sucrose to its components glucose and fructose, thus determining the relative amount of each main nectar sugar (Pate et al. 1985). A dichotomy between sucrose and hexose nectars is evident in bird-pollinated plant species. In a large data set of 112 plant species in Costa Rica, sucrose was found to be the dominant nectar sugar in plants pollinated by hummingbirds (Stiles and Freeman 1993). The literature review by Nicolson and Fleming (2003a) supports this finding, as sucrose was the dominant nectar sugar found in most of the 278 hummingbird-pollinated plant species investigated in America. Plants pollinated by sunbirds and honeyeaters, on the other hand, showed a bimodal pattern, with about half of the nectars being hexose- dominant, whereas sucrose is the dominant sugar in the other half (Nicolson and Fleming 2003a). This dichotomy is not seen as a consequence of bird physiology, as specialist nectarivorous birds assimilate both sucrose and hexose sugars equally well (Lotz and Nicolson 1996).
However, some occasional avian nectarivores lack the enzyme sucrase and can not hydrolyze sucrose, which appears to lead to aversion of sucrose nectars (Fleming et al. 2008). Plants that are pollinated by birds or mammals produce large volumes of dilute nectar, compared to the smaller volumes of concentrated nectar of insect-pollinated plants (Pyke and Waser 1981; Nicolson and Thornburg 2007). In bird-pollinated flowers, the concentration of nectar ranges mainly from 15–30% w/w sugar (Nicolson and Fleming 2003a; Johnson and Nicolson 2008). However, nectar sugar concentration varies greatly both within and between food plants (Pyke and Waser 1981; Stiles and Freeman 1993; Nicolson and Thornburg 2007). Nectar of southern African passerine-pollinated flowers, for instance, ranges from 6.5% w/w (Aloe speciosa) to 36.7% (Liparia splendens) (Nicolson 2002). Nectar viscosity increases exponentially with concentration, which may affect the extraction of nectar from flowers (Nicolson and Thornburg 2007). Tongue licking frequencies and tongue loads of hummingbirds are influenced by high viscosities of the food source (Hainsworth 1973; Roberts 1995). A biophysical model of hummingbird feeding predicted optimal licking behaviour at nectar concentrations of 20– 25% (Kingsolver and Daniel 1983).

Nectarivorous birds

Nectarivory has evolved independently in three major radiations of birds: sunbirds (Nectariniidae) in Africa and Asia, honeyeaters (Meliphagidae) in Australasia, and hummingbirds (Trochilidae) of the Americas. These avian nectarivores show morphological and physiological adaptations to their nectar-feeding lifestyle, such as brightly coloured plumages (Johnsgard 1983; Longmore 1991; Hockey et al. 2005), long straight or curved bills (Temeles and Kress 2003), specialized tongues (Hainsworth 1973; Schlamowitz et al. 1976; Downs 2004) and a gut adapted to nectar digestion (Richardson and Wooller 1986; Mbatha et al. 2002). Sunbirds, honeyeaters and hummingbirds are equally efficient in sugar uptake, assimilating between 95 and almost 100% of ingested sugar (Lotz and Schondube 2006). However, the ingestion of copious amounts of characteristically dilute nectar results in high energy costs for food warming (Lotz et al. 2003). Nectarivorous birds are also challenged by the elimination of excess water, and chronic diuresis is an inevitable consequence of their dilute food (Martínez del Rio et al. 2001; Nicolson 2007a). Avian nectarivores have remarkably low nitrogen requirements, much lower than predicted by their body mass (Paton 1982; Roxburgh and Pinshow 2000; McWhorter et al. 2003).
Their rates of endogenous protein turnover and loss of nitrogen in excreta are low (see McWhorter et al. 2003 for a review). It has been suggested that this is an evolutionary adaptation to their diet, which is low in protein (Tsahar et al. 2005). The amino acid content of floral nectar, although sometimes high (Nicolson 2007b), is insufficient to meet the nitrogen needs of nectarivorous birds; they rely on additional protein sources, such as pollen and arthropods (Paton 1982; Roxburgh and Pinshow 2000; Van Tets and Nicolson 2000). Their simple gut structure, adapted to the nectar diet, appears to make avian nectarivores less efficient at extracting protein than insectivorous birds (Roxburgh and Pinshow 2002): although the transit time of insects is longer in sunbirds than in similar-sized insectivores, only 60% of nitrogen is extracted by the sunbirds. Nectarivorous birds are generally smaller than non-nectarivorous birds, with the family Trochilidae being the smallest sized birds in the world (Pyke 1980). Hummingbirds weigh 2–20 g, sunbirds 5–22 g and honeyeaters, being the largest of the nectar-feeding birds, weigh 8–250 g (Nicolson and Fleming 2003a). The small size of avian nectarivores is often associated with predicted low capacities for energy storage (e.g. Brown et al. 1978; Nicolson and Fleming 2003a). However, small hummingbirds may store considerable amounts of fat to provide energy for migration (Hiebert 1993). At the same time, fat storage implies higher flight costs, while a lower body mass reduces energy requirements (Calder et al. 1990; Chai et al. 1999). Small body size further entails energetic lifestyles and high mass-specific metabolic rates (Nicolson and Fleming 2003a). The energy balance of avian nectarivores is therefore likely to be affected by adverse environmental conditions, which makes them ideal subjects for investigating responses to energy stress.

Table of Contents :

• List of Tables
• List of Figures
• Acknowledgements
• Declaration
• Disclaimer
• Publications and manuscripts in preparation
• SUMMARY
• GENERAL INTRODUCTION AND OUTLINE OF THE STUDY
• Nectar as food source
• Nectarivorous birds
• Energetic challenges in avian nectarivores
• Study species
• Objectives of my research
• References
• CHAPTER FOOD INTAKE OF WHITEBELLIED SUNBIRDS (CINNYRIS TALATALA): CAN MEAL SIZE BE INFERRED FROM FEEDING DURATION?
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental design
  • Data processing
  • Statistical procedures
  • 1) Meal size and feeding behaviour
  • 2) Differences between the sexes and body mass relationships
  • 3) Daily rhythm, feeding patterns and consumption on the different diets Results
  • 1) Meal size and feeding behaviour
  • 1.1) Feeding duration
  • 1.2) Feeding frequency
  • 2) Differences between the sexes and body mass relationships
  • 3) Daily rhythm, feeding patterns and consumption on the different diets Discussion
  • Meal size and feeding duration
  • Viscosity effects and compensatory feeding
  • Daily rhythm in feeding patterns
  • Differences between the sexes and individual variation
  • Acknowledgements
  • References
  • Figure legends
  • Figures
• CHAPTER CHANGES IN NECTAR CONCENTRATION: HOW QUICKLY DO WHITEBELLIED SUNBIRDS (CINNYRIS TALATALA) ADJUST FEEDING PATTERNS AND FOOD INTAKE?
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental procedure
  • Data collection
  • Definitions and processing of feeding data
  • Definitions and processing of bird mass data
  • Statistical procedures
  • Results
  • Differences between treatments
  • Food intake
  • Feeding frequency
  • Mean feeding duration
  • How fast do birds adjust feeding patterns and food intake?
  • 2.5% treatment
  • 8.5% treatment
  • 30% treatment
  • Control treatment
  • Sucrose intake, body mass and flight activity on the different treatments
  • Discussion
  • Differences between treatments
  • How fast do birds adjust feeding patterns and food intake?
  • Sucrose intake, body mass and flight activity on the different treatments
  • Acknowledgements
  • References
  • Tables
  • Figure legends
  • Figures
• CHAPTER THE RESPONSE OF TWO AVIAN NECTARIVORES TO INTERRUPTIONS IN FOOD AVAILABILITY
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental procedure and processing of data
  • Statistical analysis
  • Results
  • Food intake
  • Adjustment of feeding behaviour in sunbirds
  • Body mass
  • Discussion
  • Adjustment of food intake after the fast
  • Does the fast lead to an energy deficit?
  • Physiological constraints to food intake
  • How do whitebellied sunbirds adjust their food intake?
  • Acknowledgements
  • References
  • Figure legends
  • Figures
• CHAPTER LOW TEMPERATURE CHALLENGES IN SUNBIRDS: EFFECTS ON FOOD INTAKE, FEEDING PATTERNS AND BODY MASS OF CINNYRIS TALATALA AND CHALCOMITRA AMETHYSTINA
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental procedure
  • Data collection
  • Data processing
  • Statistical analysis
  • Results
  • Food and sugar intake
  • Feeding patterns
  • Body mass
  • Sugar assimilation in whitebellied sunbirds
  • Gut morphology, sucrase activity and predicted maximal intake
  • Discussion
  • Compensatory feeding
  • Physiological constraints to food intake
  • Maximal food intake in sunbirds
  • Energy-saving mechanisms
  • Feeding patterns
  • Conclusion
  • Acknowledgements
  • References
  • Table
  • Figure legends
  • Figures
• CHAPTER TEMPERATURE CHALLENGES IN BROWN HONEYEATERS (LICHMERA INDISTINCTA): ACUTE COLD EXPOSURE AND POSSIBLE EFFECTS OF ACCLIMATION
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental procedure
  • Part I: Acute cold exposure
  • Part II: Repeated cold exposure
  • Diet density, sugar assimilation and gut physiology measurements
  • Data processing
  • Statistical analysis
  • Results
  • Food and sugar intake
  • Part I: Acute cold exposure
  • Part II: Repeated cold exposure
  • Body mass
  • Part I: Acute cold exposure
  • Part II: Repeated cold exposure
  • Sugar assimilation
  • Gut morphology, sucrase activity and predicted maximal intake
  • Discussion
  • Compensatory feeding and physiological constraints
  • Did honeyeaters exhibit energy-saving mechanisms?
  • Did honeyeaters acclimate to the cold?
  • Acknowledgements
  • References
  • Table
  • Figure legends
  • Figures
• CHAPTER NECTAR EXTRACTION BY SUNBIRDS: DOES LICKING BEHAVIOUR CHANGE WITH NECTAR CONCENTRATION AND AFTER A FASTING PERIOD?
  • Abstract
  • Introduction
  • Materials and methods
  • Study animals and their maintenance
  • Experimental procedure
  • Part I: Licking behaviour and sugar concentration
  • Part II: Licking behaviour and a fasting period
  • Data processing
  • Statistical analysis
  • Results
  • Part I: Licking behaviour and sugar concentration
  • Part II: Licking behaviour and a fasting period
  • Discussion
  • The effect of sugar concentration on licking behaviour
  • The effect of experimental devices on licking behaviour
  • Licking behaviour and a fasting period
  • Differences in licking behaviour between species
  • Conclusion
  • Acknowledgements
  • References
  • Table
  • Figure legends
  • Figures
  • CONCLUSION
  • The importance of studying animal responses to energy challenges
  • Suitability of avian nectarivores for my study
  • The response of sunbirds and honeyeaters to energy challenges
  • Individual variation
  • The integration of physiology and behaviour
  • Directions for future research
  • References

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