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The Effect of Digestive Capacity on the Intake Rate of Toxic and Non-Toxic Prey in an Ecological Context.

Oudman T, Hin V, Dekinga A, van Gils JA - PLoS ONE (2015)

Bottom Line: We found that intake of Dosinia exponentially increased with gizzard mass, confirming earlier results with non-toxic prey, whereas intake of Loripes was independent of gizzard mass.Intra- and inter-individual variation in digestive capacity is found in many animal species.We emphasize the potential relevance of individual variation in physiology when studying trophic interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Ecology, NIOZ Royal Netherlands Institute for Sea Research, Texel, The Netherlands.

ABSTRACT
Digestive capacity often limits food intake rate in animals. Many species can flexibly adjust digestive organ mass, enabling them to increase intake rate in times of increased energy requirement and/or scarcity of high-quality prey. However, some prey species are defended by secondary compounds, thereby forcing a toxin limitation on the forager's intake rate, a constraint that potentially cannot be alleviated by enlarging digestive capacity. Hence, physiological flexibility may have a differential effect on intake of different prey types, and consequently on dietary preferences. We tested this effect in red knots (Calidris canutus canutus), medium-sized migratory shorebirds that feed on hard-shelled, usually mollusc, prey. Because they ingest their prey whole and crush the shell in their gizzard, the intake rate of red knots is generally constrained by digestive capacity. However, one of their main prey, the bivalve Loripes lucinalis, imposes a toxin constraint due to its symbiosis with sulphide-oxidizing bacteria. We manipulated gizzard sizes of red knots through prolonged exposure to hard-shelled or soft foods. We then measured maximum intake rates of toxic Loripes versus a non-toxic bivalve, Dosinia isocardia. We found that intake of Dosinia exponentially increased with gizzard mass, confirming earlier results with non-toxic prey, whereas intake of Loripes was independent of gizzard mass. Using linear programming, we show that this leads to markedly different expected diet preferences in red knots that try to maximize energy intake rate with a small versus a large gizzard. Intra- and inter-individual variation in digestive capacity is found in many animal species. Hence, the here proposed functional link with individual differences in foraging decisions may be general. We emphasize the potential relevance of individual variation in physiology when studying trophic interactions.

No MeSH data available.


Related in: MedlinePlus

The predicted optimal proportion of Loripes in terms of dry shell mass in the diet of an energy intake maximizing red knot that has ad libitum access to both Loripes and Dosinia.Red knots with small gizzards are expected to feed exclusively on Loripes, whereas red knots with large gizzards are expected to have a large share of Dosinia in the diet. Grey area shows 95% prediction interval. See S4 File for more details.
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pone.0136144.g004: The predicted optimal proportion of Loripes in terms of dry shell mass in the diet of an energy intake maximizing red knot that has ad libitum access to both Loripes and Dosinia.Red knots with small gizzards are expected to feed exclusively on Loripes, whereas red knots with large gizzards are expected to have a large share of Dosinia in the diet. Grey area shows 95% prediction interval. See S4 File for more details.

Mentions: Gizzard masses of red knots caught in Banc d’Arguin are variable between individuals (mean = 9.89 g, SD = 1.30 g; [15]), ranging from 4 to 15 g (A. Dekinga unpublished data). These differences in gizzard mass may accompany differences in diet preferences, as gizzard mass influences potential intake on Dosinia but not on Loripes. Linear programming models can be used to quantify optimal diet preferences as a function of the constraints on intake rate under the assumption of energy maximization [3, 4, 25]. Oudman et al. [23] use a linear programming model to calculate expected diet preferences for energy intake maximizing red knots foraging on ad libitum Loripes and Dosinia. This model calculates which combinations of intake rates on Dosinia and Loripes are possible given both the shell-mass processing constraint and the toxin constraint on Loripes, and subsequently determines which of these combinations provides the highest energy intake rate. Based on measured values of the shell-mass processing constraint and the toxin constraint on Loripes but without taking gizzard mass into account, they deduce that the optimal proportion of Loripes in the diet is 39% in terms of dry shell mass, when both prey occur in ad libitum abundances. van Gils et al. [24] show how this optimal proportion varies with densities of both prey. Replacing a constant shell-mass processing constraint by the here derived gizzard-mass dependent shell-mass processing constraint (eq. 1) and parameterizing the model with the here obtained values (for a detailed model description, see S4 File) shows that this proportion changes considerably with gizzard mass (Fig 4). The model predicts that energy maximizing birds with a gizzard mass below 5.2 g prefer an exclusive Loripes diet. Red knots with greater gizzard masses are expected to have a lower proportion of Loripes in the diet, which is less than 40% of total DMshell intake rate in birds with a 10 g gizzard. Hence, model predictions show that given the observed variation in gizzard sizes of red knots in the wild, considerable inter- and intra-individual variation in diet preferences can be expected. This result may translate to many other species, because flexibility in digestive organ mass is a general phenomenon [41] being observed in mammals [42], reptiles [9], fish [8] and birds [10]. Toxin constraints are observed widely too, especially in herbivores, e.g. [43], but are not a prerequisite to explain a functional link between individual variation in physiology and diet preferences. For example, external handling constraints may also, in combination with digestive capacity, cause a mixed diet that depends on the strength of the digestive constraint [25].


The Effect of Digestive Capacity on the Intake Rate of Toxic and Non-Toxic Prey in an Ecological Context.

Oudman T, Hin V, Dekinga A, van Gils JA - PLoS ONE (2015)

The predicted optimal proportion of Loripes in terms of dry shell mass in the diet of an energy intake maximizing red knot that has ad libitum access to both Loripes and Dosinia.Red knots with small gizzards are expected to feed exclusively on Loripes, whereas red knots with large gizzards are expected to have a large share of Dosinia in the diet. Grey area shows 95% prediction interval. See S4 File for more details.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4543589&req=5

pone.0136144.g004: The predicted optimal proportion of Loripes in terms of dry shell mass in the diet of an energy intake maximizing red knot that has ad libitum access to both Loripes and Dosinia.Red knots with small gizzards are expected to feed exclusively on Loripes, whereas red knots with large gizzards are expected to have a large share of Dosinia in the diet. Grey area shows 95% prediction interval. See S4 File for more details.
Mentions: Gizzard masses of red knots caught in Banc d’Arguin are variable between individuals (mean = 9.89 g, SD = 1.30 g; [15]), ranging from 4 to 15 g (A. Dekinga unpublished data). These differences in gizzard mass may accompany differences in diet preferences, as gizzard mass influences potential intake on Dosinia but not on Loripes. Linear programming models can be used to quantify optimal diet preferences as a function of the constraints on intake rate under the assumption of energy maximization [3, 4, 25]. Oudman et al. [23] use a linear programming model to calculate expected diet preferences for energy intake maximizing red knots foraging on ad libitum Loripes and Dosinia. This model calculates which combinations of intake rates on Dosinia and Loripes are possible given both the shell-mass processing constraint and the toxin constraint on Loripes, and subsequently determines which of these combinations provides the highest energy intake rate. Based on measured values of the shell-mass processing constraint and the toxin constraint on Loripes but without taking gizzard mass into account, they deduce that the optimal proportion of Loripes in the diet is 39% in terms of dry shell mass, when both prey occur in ad libitum abundances. van Gils et al. [24] show how this optimal proportion varies with densities of both prey. Replacing a constant shell-mass processing constraint by the here derived gizzard-mass dependent shell-mass processing constraint (eq. 1) and parameterizing the model with the here obtained values (for a detailed model description, see S4 File) shows that this proportion changes considerably with gizzard mass (Fig 4). The model predicts that energy maximizing birds with a gizzard mass below 5.2 g prefer an exclusive Loripes diet. Red knots with greater gizzard masses are expected to have a lower proportion of Loripes in the diet, which is less than 40% of total DMshell intake rate in birds with a 10 g gizzard. Hence, model predictions show that given the observed variation in gizzard sizes of red knots in the wild, considerable inter- and intra-individual variation in diet preferences can be expected. This result may translate to many other species, because flexibility in digestive organ mass is a general phenomenon [41] being observed in mammals [42], reptiles [9], fish [8] and birds [10]. Toxin constraints are observed widely too, especially in herbivores, e.g. [43], but are not a prerequisite to explain a functional link between individual variation in physiology and diet preferences. For example, external handling constraints may also, in combination with digestive capacity, cause a mixed diet that depends on the strength of the digestive constraint [25].

Bottom Line: We found that intake of Dosinia exponentially increased with gizzard mass, confirming earlier results with non-toxic prey, whereas intake of Loripes was independent of gizzard mass.Intra- and inter-individual variation in digestive capacity is found in many animal species.We emphasize the potential relevance of individual variation in physiology when studying trophic interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Ecology, NIOZ Royal Netherlands Institute for Sea Research, Texel, The Netherlands.

ABSTRACT
Digestive capacity often limits food intake rate in animals. Many species can flexibly adjust digestive organ mass, enabling them to increase intake rate in times of increased energy requirement and/or scarcity of high-quality prey. However, some prey species are defended by secondary compounds, thereby forcing a toxin limitation on the forager's intake rate, a constraint that potentially cannot be alleviated by enlarging digestive capacity. Hence, physiological flexibility may have a differential effect on intake of different prey types, and consequently on dietary preferences. We tested this effect in red knots (Calidris canutus canutus), medium-sized migratory shorebirds that feed on hard-shelled, usually mollusc, prey. Because they ingest their prey whole and crush the shell in their gizzard, the intake rate of red knots is generally constrained by digestive capacity. However, one of their main prey, the bivalve Loripes lucinalis, imposes a toxin constraint due to its symbiosis with sulphide-oxidizing bacteria. We manipulated gizzard sizes of red knots through prolonged exposure to hard-shelled or soft foods. We then measured maximum intake rates of toxic Loripes versus a non-toxic bivalve, Dosinia isocardia. We found that intake of Dosinia exponentially increased with gizzard mass, confirming earlier results with non-toxic prey, whereas intake of Loripes was independent of gizzard mass. Using linear programming, we show that this leads to markedly different expected diet preferences in red knots that try to maximize energy intake rate with a small versus a large gizzard. Intra- and inter-individual variation in digestive capacity is found in many animal species. Hence, the here proposed functional link with individual differences in foraging decisions may be general. We emphasize the potential relevance of individual variation in physiology when studying trophic interactions.

No MeSH data available.


Related in: MedlinePlus