Though most human-pet relationships are fulfilling, each year a substantial number of animals are abandoned by their owners or relinquished to animal shelters (Podberscek, 1997; Marston and Bennett, 2003). The number of dogs and cats euthanized annually in the United States is estimated between 5 and 17 million (Carter, 1990; Rowan, 1992) with 3 to 6 million as a result of behaviour problems (Dodman and Shuster, 1998).
Strategies that combat canine and feline problem behaviours will greatly benefit animal welfare. This contribution presents a number of examples of food properties that have been shown to modulate canine and feline (problem) behaviour.
Effects of dietary protein on behaviour
An important component of canine and feline diets is the amount and source of dietary protein, since protein sources can differ in amino acid composition. After ingestion, proteins will be enzymatically degraded and absorbed in the small intestine as tripeptides, dipeptides and amino acids and transported through the portal vein to the liver.
Total dietary protein concentration may affect canine behaviour as found by Dodman et al. (1996). Twelve dogs that exhibited high territorial aggression, dominance aggression, or hyperactivity and 14 control dogs were each fed, at in-home living situations, three diets varying in protein content (180, 250 and 310 g/kg on DM basis) for two weeks.
The low-protein diet and medium-protein diet decreased territorial aggression scores compared with the high-protein diet. No effects of dietary protein content on dogs with dominance aggression or hyperactivity were found. Additional behavioural analysis of the group of dogs demonstrating territorial aggression revealed that five of these dogs showed dominance-related territorial aggression, whereas the other seven dogs showed fear-related territorial aggression. In the latter dogs, territorial aggression decreased when fed the low-protein diet.
Beside total protein content, individual amino acid content may affect behaviour. A number of precursors to neurotransmitters are amino acids, e.g., tryptophan, tyrosine, and histidine for synthesis of serotonin, catecholamines, and histamine, respectively.
Changes in the availability of neurotransmitter precursors such as tryptophan and tyrosine, therefore, may influence behaviour, since behaviour is the result of signal detection, transmission, and processing in the (central) nervous system as brought about by chemical messengers like neurotransmitters and hormones. The effects of the amino acids tryptophan and tyrosine on behaviour will be discussed here as these could be relatively potent dietary modulators of canine and feline behaviour. The reader is referred to Young (1996) for similar reports on choline, histidine and threonine.
A high tryptophan diet has been shown to reduce mouse-killing by rats (Gibbons et al., 1979; Kantak et al., 1980), reduce aggression in vervet monkeys (Chamberlain et al., 1987), and reduce self-injurious behaviour in rhesus monkeys (Weld et al., 1998). In humans, changes in tryptophan levels are associated with alterations in aggression and impulse control disorders (for a review see Young and Leyton, 2002).
An increase in tryptophan intake may also influence dominance in a group by enhancing affiliative behaviour as shown in vervet monkeys (Raleigh et al., 1991). Consistent with observations in primates, a reduced serotonergic function (low cerebrospinal fluid 5-HIAA concentration, a serotonin metabolite) is associated with aggressive behaviour and impaired impulse control in dogs (Reisner et al., 1996). In addition, serotonin receptor concentrations in various brain areas are found to be different in aggressive dogs compared with dogs with no history of neurological and/or behavioural disorders (Badino et al., 2004).
Studies on the effects of tryptophan or tyrosine on behaviour in dogs are limited. DeNapoli et al. (2000) formulated diets with a high or low protein content (approximately 310 or 190 g/kg protein) and with or without 1.45 g/kg tryptophan supplementation to provide varying tryptophan contents and tryptophan:LNAA (large neutral amino acids) ratios.
Each of the four diets was fed in random order for one week to 11 privately owned dogs that displayed high territorial aggression, dominance aggression, or hyperactivity. There was no effect of dietary protein or tryptophan content on the behavioural scores within any of the groups. However, when the results were pooled a lower territoriality aggression score was obtained for dogs fed the high-tryptophan diet compared with dogs fed the low-tryptophan diet, but only when fed a low-protein diet.
In addition, dogs fed the high-protein diet without tryptophan supplementation showed a higher dominance aggression score compared with dogs fed the other dietary treatments.
TRYPTOPHAN AND TYROSINE (STRESS RESPONSE)
Dietary tryptophan may also influence the resistance or tolerance to stress and thus change the behavioural stress response. Koopmans et al. (2005) reported enhanced recovery after social stress as measured by lower plasma cortisol and noradrenaline concentrations in pigs fed a surplus of dietary tryptophan compared with pigs fed diets containing ‘normal’ tryptophan concentrations.
In healthy stress-vulnerable humans, supplementation of dietary tryptophan reduced plasma cortisol concentrations during a stress-inducing mental arithmetic task (Markus et al., 2000) and Markus et al. (2000) suggested that tryptophan supplementation above normal dietary concentrations could improve the ability of an individual to cope with stress. In line with this, depressed humans show decreased plasma tryptophan concentrations in comparison to normal subjects (Branchey et al., 1984).
In rats, a high-tyrosine diet prevents adverse behavioural and neurochemical effects (e.g., immobility during swim test, depletion of brain noradrenaline) of various acute stressors including hypothermia (Rauch and Lieberman, 1990), restraint, and tail-shock (Lehnert et al., 1984; Reinstein et al., 1984). Increases in brain tyrosine have little or no effect on catecholamine synthesis (Young, 1996), but the situation may be different during stress when brain noradrenaline turnover increases and noradrenaline concentrations decrease (Brady et al., 1980; Lehnert et al., 1984).
An enhanced noradrenergic activity is part of a normal adaptive stress response (Yeghiayan et al., 2001). Results reported suggest that a high-tyrosine diet may be beneficial during severe stress, since it prevents depletion of the substrate required for catecholamine synthesis in times of high catecholaminergic activity and demand.
Little research has been conducted on the effect of tryptophan and/or tyrosine addition on the stress response of cats and dogs. In cats, resistance to stress is affected by dietary protein source. Cats fed a diet with soya concentrate as a protein source were physiologically more stressed during two hours of immobilisation compared with those fed a diet containing similar protein content (30.7%) but with casein as protein source (Thibault and Roberge, 1988). Besides variation in the amino acid content (per 100 g protein, 1.5 g tryptophan and 3.9 g tyrosine for the soy diet and 1.3 g tryptophan and 5.8 g tyrosine for the casein diet) differences in digestibility of the protein source may further affect the amount of amino acids supplied to the brain for neurotransmitter synthesis.
Effects of dietary lipids on behaviour
The central nervous system has the greatest concentration of lipids after adipose tissue (Carrié et al., 2000b). The structural constituents in the grey matter of the brain and retinal tissues in mammals are derived from dietary linoleic acid (18:2n-6) and α- linolenic acid (18:3n-3). Both are polyunsaturated fatty acids (PUFA) that can be metabolised to long-chain PUFA by sequential alternating enzymatic desaturation and elongation.
n-3 AND n-6 POLYUNSATURATED FATTY ACIDS (LEARNING)
There is ample scientific literature available in which the effects of both dietary deficiency and supplementation of PUFA on animal performance in cognitive or behavioural tests are evaluated (for reviews, see Wainwright, 1992; McCann and Ames, 2005).
For example, learning ability of rodents decreased when fed n-3 fatty acid deficient diets (Bourre et al., 1989; Moriguchi et al., 2000) and increased when fed docosahexaenoic acid (DHA) supplemented diets (Lim and Suzuki, 2001) compared with rodents fed diets adequate in n-3 fatty acid concentrations.
Other studies, however, did not find effects of dietary n-3 PUFA manipulation on learning performance as tested with a Morris water-maze in rats (Wainwright et al., 1999) or mice (Wainwright et al., 1997). Dietary PUFA seem to affect animal cognition but can also cause behavioural changes. Rats fed n-3 PUFAdeficient diets showed increased aggression scores in a resident intruder test (DeMar et al., 2006) and increased expression of stress-related behaviours during several stress tests (Takeuchi et al., 2003) compared with male rats fed adequate amounts of n-3 PUFA.
Similarly, anxiety was found to be increased in mice fed a diet deficient in n-3 PUFA (Carrié et al., 2000a), though others did not observe any effects of dietary PUFA on anxiety in mice (Francès et al., 1996) or rats (Chalon et al., 1998). At present, scientific evidence available on the effect of n-3 PUFA on trainability in dogs is limited to conference proceedings of Kelley et al. (2004; 2005). No information is available on the influence of PUFA on learning in cats.
Effects of dietary carbohydrates on behaviour
Food intake behaviours are controlled by feelings of hunger (Rowland et al., 1996) and satiety (Blundell, 1991), but may be modulated by psychological and social factors (Read, 1992). Numerous central and peripheral signal molecules are involved in the regulation of eating (for reviews, see Bray, 2000; de Graaf et al., 2004; Strader and Woods, 2005). The rate and site of degradation of nutrients largely determines the postprandial physiological state of an animal and in this way the extent and duration of satiety and motivation to forage and feed.
Forty-eight hours of food deprivation elevates the threshold for the suppression of prey catching by stimulation of the mammillary bodies (Adamec, 1976). Similarly, contact play, which seems correlated to the probability of a kill, could be predicted according to the prey size and the hunger level of the cat (Hall and Bradshaw, 1998). The influence of dietary cellulose content on food intake in cats was investigated by Prola et al. (2006). They found that gastric fill appears to limit food intake in cats. Gastric fill may be more effective in reducing food intake in cats than in dogs (Dobenecker and Kienzle, 1998; Prola et al., 2006).
Satiety and hunger are rarely considered as contributing factors to the expression of canine behaviour. Dietary fibre (non-starch polysaccharides, resistant starch and nondigestible oligosaccharides) may play an important role in maintaining satiety and lowering feeding motivation between meals.
There are few studies available in the literature reporting effects of fibrous dietary ingredients on feed intake and/or feeding motivation in dogs (Jewell and Toll, 1996; Butterwick and Markwell, 1997; Jackson et al., 1997; Dobenecker and Kienzle, 1998; Howard et al., 2000), while no information exists on the role of dietary fibres on behaviour. In non-lactating sows, the effects of fibrous ingredients on behaviour have been studied.
In practice, diets for sows are formulated to meet the daily nutrient requirements for maintenance and reproduction. These diets do not necessarily result in a sufficient level of satiety between meals and as a result sows may have a persistent high feeding motivation throughout the day contributing to the development of stereotyped behaviour (Lawrence and Terlouw, 1993).
Sows fed high-fibre diets (mostly sugar beet pulp) showed a reduction in stereotyped behaviour (Ramonet et al., 1999; Bergeron et al., 2000), in aggression and foraging (Danielsen and Verstergaard, 2001), and spent increased time lying down (Robert et al., 1993) compared with sows fed a low-fibre diet (for more examples see Meunier-Salaün et al., 2001). Differences in feelings of hunger are the most likely cause of these observed behavioural changes in sows (de Leeuw et al., 2005). The effect of fibrous ingredients on behaviour is not generic for all fibre sources, e.g., solvent-extracted coconut meal and soybean hulls as a dietary fibre source do not appear to affect physical activity in pigs (Rijnen et al., 2003b), whereas sugar beet pulp silage does (Rijnen et al., 2003a).
In addition to the observed behavioural changes in home-pens, behaviour tests may elicit different behavioural patterns depending on the state of hunger or satiety. One of the tests used in an open-field test, i.e., social isolation in an unfamiliar environment, elicits complex behaviour patterns in various animal species that may reflect, among other things, exploratory motivation and fear (Andersen et al., 2000).
Compared with pigs fed a starch diet, pigs fed a high fibre diet (sugar beet pulp) with high satiating properties appeared less aroused in an open-field test and less motivated to escape from the environment, suggesting reduced levels of stress or fear (Doornhegge et al., unpublished results). This observation agrees with findings in rats. Injection of ghrelin, a hormone correlated to hunger or appetite (Wren et al., 2001), was found to increase anxiety in rats as measured with an open-field test and elevated plus-maze (Carlini et al., 2002).
Several physical and chemical properties of dietary fibres may influence the duration of postprandial satiety and postponing interprandial feelings of hunger. Dietary fibre with a high water-holding capacity can cause an increased stimulation of gastric stretch receptors stimulating gastric satiation (Pappas et al., 1989). Soluble fermentable non-starch polysaccharides can delay passage rate of digesta and nutrient absorption (Johansen et al., 1996). Volatile fatty acids (VFA) derived from the microbial fermentation of dietary fibre can stimulate L-cells in the terminal ileum and colon to secrete the satiety gut hormone peptide tyrosine-tyrosine (PYY) (Anini et al., 1999; Cuche et al., 2000; Karaki et al., 2006).
In addition, secretion of glucagon-like peptide-1 by L-cells (Kieffer and Habener, 1999) can be increased when feeding a diet supplemented with fermentable dietary fibre (Massimino et al., 1998; Cani et al., 2004). Glucagon-like peptide-1 and PYY increase delay in gastric emptying (Anvari et al., 1998; Moran et al., 2005) and increase small intestinal transit time (Wen et al., 1995; Daniel et al., 2002). These increases may prolong gastric distension and signals of satiation (Holt et al., 1979) and prolong contact between nutrients and intestinal chemoreceptors involved in maintaining satiety (Houpt, 1982). A delay in gastric emptying will also extend the duration of digestion and absorption of nutrients (Östman et al., 2005).
Peptide tyrosine has been shown to cross the blood-brain-barrier and act on the arcuate nucleus of the hypothalamus, stimulating neurons that create a sensation of satiety and inhibiting neurons that stimulate feeding behaviour (Batterham et al., 2002). This mechanism was studied by Moran et al. (2005) in rhesus monkeys where intramuscular injections of PYY reduced gastric emptying and resulted in a decrease in food intake across the 6-hr period of food access.
However, this decrease in food intake was not sustained over multiple administrations across successive days. In addition, fatty acids infused in the ileum have been shown to stimulate the release of PYY sufficient to delay gastric emptying in dogs (Pappas et al., 1986). Finally, VFA (mainly acetate) may become a source of energy at times when glucose supply from the small intestine is decreasing (Bergman, 1990; van Leeuwen et al., 2006).
The degree of satiety in animals such as pigs has been shown to affect behaviour, including aggressive and stereotyped behaviour. Although likely, it is unknown whether canine behaviour can be affected by degree of satiety and further research is required. Assuming that behaviours in dogs are more favourable during times of satiety than during times of hunger as observed in pigs (e.g., aggression), specific dietary fibres through their potential to prolong satiety may assist in preventing unwanted canine behaviours.
Effects of micronutrients on behaviour
According to Benton (1992), the first symptoms associated with micronutrient deficiency are psychological. Indeed, scientific literature is starting to report examples in which behavioural effects are found in individuals with a low intake of micronutrients.
For instance, diets rich in vitamins and minerals have been reported to decrease anti-social behaviour in schoolchildren (Schoenthaler and Bier, 2000) and supplementation of vitamins, minerals and essential fatty acids decreased anti-social behaviour, including violence, of young adult prisoners (Gesch et al., 2002). In addition, supplementation of vitamins to raise nutrient intake to the equivalent of a well balanced diet has been shown to increase intelligence in schoolchildren (Schoenthaler et al., 2000).
For a critical review about the effects of micronutrients on mood, memory, attention, learning and including possible underlying mechanisms see Benton (2001). Micronutrients like antioxidants and mitochondrial cofactors are involved in the attenuation of age-dependent cognitive decline. Dogs develop similar cognitive deficits and neuropathology as can be seen in aging humans suffering from dementia (Adams et al., 2000; Studzinski et al., 2005).
Milgram and co-workers initiated a series of experiments with young and aged Beagle dogs to study dietary interventions on age-related cognitive decline. Results showed that canine food enriched with antioxidants and mitochondrial co-factors decreased the rate of cognitive decline in aged Beagle dogs under laboratory conditions and improved age-related behavioural changes in older privately owned dogs (for reviews, see Roudebush et al., 2005; Zicker, 2005).
The present contribution provides a brief discussion of possible dietary factors that may modulate canine and feline behaviour. Dietary component may have varying effects on behaviour and further research should investigate, for example, the effect of high carbohydrate (or reduced crude protein and crude fat) intake by carnivores on behaviour.
Effect on behaviour is rarely taken into account as a response criterion to novel feeds, which has been criticized (Lieberman, 1999; Reeds, 2000). Although a diet may offer complete and balanced nutrition, it may result in increased, unwanted behaviour.
For example, the minimum quantity of tryptophan in a commercial canine dry expanded diet that has passed a maintenance AAFCO feeding protocol has been reported to be 0.21 g/1000 kcal ME (NRC, 2006).
The criteria for passing an AAFCO maintenance feeding protocol, however, do not take into account animal behaviour although it is fairly well established that dietary tryptophan concentration may have a major effect on behaviour of the animal.
In addition, it is unknown whether the minimal concentration of tryptophan in a typical dog food meets the requirements of the wide variety of dogs, e.g., from emotionally stable to anxious individuals, under different conditions, e.g. from stress-free to stressful.
Besides tryptophan, total crude protein, amino acids, carbohydrate composition, micronutrients as well as antioxidants and fatty acid content in the diet may all have effects on feline and canine behaviour.
Authors: G. BOSCH1, B. BEERDA2, A.F.B. VAN DER POEL1 and W.H. HENDRIKS1
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1 Animal Nutrition Group, Department of Animal Sciences
2 Animal Production Division, Animal Sciences Group, Wageningen University and Research Centre, Wageningen, The Netherlands