Predators' consumption of unpalatable prey does not vary as a function of bitter taste perception

Abstract Many prey species contain defensive chemicals that are described as tasting bitter. Bitter taste perception is, therefore, assumed to be important when predators are learning about prey defenses. However, it is not known how individuals differ in their response to bitter taste, and how this influences their foraging decisions. We conducted taste perception assays in which wild-caught great tits (Parus major) were given water with increasing concentrations of bitter-tasting chloroquine diphosphate until they showed an aversive response to bitter taste. This response threshold was found to vary considerably among individuals, ranging from chloroquine concentrations of 0.01 mmol/L to 8 mmol/L. We next investigated whether the response threshold influenced the consumption of defended prey during avoidance learning by presenting birds with novel palatable and defended prey in a random sequence until they refused to attack defended prey. We predicted that individuals with taste response thresholds at lower concentrations would consume fewer defended prey before rejecting them, but found that the response threshold had no effect on the birds’ foraging choices. Instead, willingness to consume defended prey was influenced by the birds’ body condition. This effect was age- and sex-dependent, with adult males attacking more of the defended prey when their body condition was poor, whereas body condition did not have an effect on the foraging choices of juveniles and females. Together, our results suggest that even though taste perception might be important for recognizing prey toxicity, other factors, such as predators’ energetic state, drive the decisions to consume chemically defended prey.</jats:p

Effect of taste perception on avoidance learning in avian predators

Optimoidakseen ravinnonhankintansa yksilön tulisi hankkia mahdollisimman paljon energiaa, samalla minimoiden käytetyn ajan, vaivan ja riskit. Yksi ravinnonhankintakykyyn vaikuttavista ominaisuuksista on makuaisti, jonka ajatellaan kehittyneen ohjaamaan ja säätelemään ravinnon valikointia. Koska useat saalislajit sisältävät karvaan makuisia, myrkyllisiä yhdisteitä, makuaistin tehtävänä on todennäköisesti varmistaa, että saalistajat välttävät myrkillisten saaliiden käyttöä. Koska karvaan maun havaitseminen on tärkeää yksilön selviytymisen kannalta, voisi ominaisuus tarjota myös evolutiivisen edun. Lisäksi, saalistajan maistamiskykyyn perustuvilla ravintovalinnoilla voisi olla merkittävä vaikutus saalispopulaation evoluutioon sekä saalistaja-saalis yhteisevoluutioon. Lajien välisen vaihtelun lisäksi, karvaan maun aistimiskyvyssä on havaittu myös saman lajin yksilöiden välisiä eroja. Kokeellinen tieto lajin sisäisestä vaihtelusta ja sen vaikutuksesta ravinnonhankintaan on kuitenkin edelleen vähäistä ja suurin osa tutkimuksista on toteutettu nisäkkäillä, pääosassa ihmisellä. Ymmärtääkseni lajin sisäisen vaihtelun merkitystä lintujen saalistukseen mittasin talitiaisten (Parus major) kykyä havaita karvasta makua sekä makuaistin tason vaikutusta uuden, myrkyllisen saaliin välttämisnopeuteen. Tutkimukseni ensimmäisenä tavoitteena oli määrittää, esiintyykö talitiaisyksilöiden välillä vaihtelua karvaan maun maistamiskyvyssä ja korreloiko herkkyystaso yksilön iän, sukupuolen tai kunnon kanssa. Nisäkästutkimuksiin perustuen odotin naaraiden maistavan koiraita paremmin poikasten kehityksen turvaamiseksi. Lisäksi, ennustin nuorten yksilöiden olevan vanhoja parempia maistajia, sillä maistamiskyvyn on havaittu heikentyvän yksilön vanhetessa. Seuraavana tavoitteena oli tutkia nopeuttaako hyvä maistamiskyky samojen lintuyksilöiden välttämisoppimista hyvän ja pahan makuisen saalin välillä. Tutkimukseni osoittaa, että talitiaisten karvaan maistamiskyvyssä ilmenee hyvin laajaa yksilöiden välistä vaihtelua. Tulosteni mukaan nuoret yksilöt ovat aikuisia parempia maistajia, mutta yksilön sukupuolen tai kunnon ei havaittu vaikuttavan maistamiskykyyn. Makuaisti yksin ei selittänyt välttämisoppimista. Tutkimukseni kuitenkin osoitti, että yksilön maistamiskyky, ikä, sukupuoli ja kunto vaikuttavat yhdessä monitahoisesti välttämisoppimiseen. Näin ollen vaikuttaisi siltä, että kognition lisäksi myös yksilön fysio- ja morfologia vaikuttavat ravinnon valikointiin. Yksittäisten ominaisuuksien vaikutusta valikointiin on kuitenkin hankala arvioida. Tietojeni mukaan kokeeni osoitti ensimmäisenä tutkimuksena yksilövaihtelun lintujen karvaan maun maistamiskyvyssä sekä vaihtelun vaikutuksen ravinnon valikointiin. Vaihtelun olemassaolo tarjoaa kiinnostavan uuden alueen tuleville lintututkimuksille.To optimize foraging behavior, individuals should forage in a way that maximizes their energy gain and minimizes risks, time, and energy spend on foraging. One of the traits affecting animals’ foraging ability is taste, which has likely evolved to serve as a dominant regulator and driver of diet choices. Since many plants and animals contain toxic bitter chemicals, bitter taste presumably functions to insure that predators avoid the consumption of toxic prey. Thus, being able to identify bitter substances contributes an important survival function and could therefore provide an evolutionary advantage. Moreover, diet choices based on predators’ taste sensitivity could be expected to have a significant effect on the prey population’s evolution and predator-prey co-evolution. In addition to interspecific variation, studies have also revealed individual differences in bitter taste sensitivity. However, the experimental evidence of intraspecific variation and its effect on foraging behavior are still scarce and mostly based on studies using mammals, particularly humans. To understand the effects of intraspecific variation in avian predators I tested great tits’ (Parus major) ability to perceive a bitter taste, and whether the variation in taste sensitivity reflects their ability to avoid unpalatable novel prey. My first aim was to test whether the variation in birds’ bitter taste sensitivity exists and if sensitivity correlates with characters such as age, sex or body condition. Based on studies in mammals, I expected females to be more sensitive compared to males, to ensure proper egg production. Moreover, because the ability to taste usually declines with age, I predicted juveniles to be more sensitive compared to adults. Secondly, I examined if the taste ability of the same individual birds affects their discriminative learning between palatable and unpalatable novel prey. I predicted that birds with higher sensitivity would learn to avoid unpalatable prey, and prefer profitable food, faster than birds with lower sensitivity. I found a great deal of variation in the taste sensitivity of great tit individuals. Juvenile birds had lower taste sensitivity than adults but birds’ sex and body condition did not seem to influence their taste perception. Taste sensitivity alone did not explain avoidance learning. However, my experiment revealed that taste sensitivity, age, sex and body condition all influence birds’ avoidance learning in a complex way. Consequently, it seems that both cognition and individual characters affect diet choice decisions, although a single trait’s effect is hard to estimate. According to my knowledge, this was the first experiment showing intraspecific variation in the ability to taste bitterness among birds, and the consequences of this variation on diet choice. The existence of such variation provides an interesting new area for future investigations of avian research

Predators' consumption of unpalatable prey does not vary as a function of bitter taste perception

Many prey species contain defensive chemicals that are described as tasting bitter. Bitter taste perception is, therefore, assumed to be important when predators are learning about prey defenses. However, it is not known how individuals differ in their response to bitter taste, and how this influences their foraging decisions. We conducted taste perception assays in which wild-caught great tits (Parus major) were given water with increasing concentrations of bitter-tasting chloroquine diphosphate until they showed an aversive response to bitter taste. This response threshold was found to vary considerably among individuals, ranging from chloroquine concentrations of 0.01 mmol/L to 8 mmol/L. We next investigated whether the response threshold influenced the consumption of defended prey during avoidance learning by presenting birds with novel palatable and defended prey in a random sequence until they refused to attack defended prey. We predicted that individuals with taste response thresholds at lower concentrations would consume fewer defended prey before rejecting them, but found that the response threshold had no effect on the birds' foraging choices. Instead, willingness to consume defended prey was influenced by the birds' body condition. This effect was age- and sex-dependent, with adult males attacking more of the defended prey when their body condition was poor, whereas body condition did not have an effect on the foraging choices of juveniles and females. Together, our results suggest that even though taste perception might be important for recognizing prey toxicity, other factors, such as predators' energetic state, drive the decisions to consume chemically defended prey. Lay Summary: Individual differences in predators' bitter taste perception do not influence the consumption of chemically defended prey. Many prey species have bitter-tasting defenses that generate aversive responses in predators. We show that great tits vary in their response to bitter taste, but this does not influence the number of novel defended prey they attack during avoidance learning. This suggests that other factors, such as the current physiological state, have a larger impact on predators' foraging decisions.Peer reviewe