Limits...
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

Mean gizzard mass of birds directly after catch, during the first and second series of trials.Directly after catch, the 6 red knots were randomly divided into two groups, group 1 (solid dots and line) and group 2 (open dots and dashed line). Both groups received different diets outside the experimental trials (soft or hard-shelled prey) to manipulate gizzard size. Initial differences in gizzard mass between groups were not significant (F1,4 = 3.9,p = 0.12). After catch, all birds decreased gizzard mass, but group 1 had larger gizzards than group 2 during the first series of trials, and smaller gizzards during the second series (Table 2, models 1.1 to 1.5), showing that the manipulation of gizzard size was successful. Each group consisted of three birds. However, data collected on one bird from group 2 after it became sick during series 2 was omitted from the graphs and the analysis. Error bars show standard error.
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pone.0136144.g001: Mean gizzard mass of birds directly after catch, during the first and second series of trials.Directly after catch, the 6 red knots were randomly divided into two groups, group 1 (solid dots and line) and group 2 (open dots and dashed line). Both groups received different diets outside the experimental trials (soft or hard-shelled prey) to manipulate gizzard size. Initial differences in gizzard mass between groups were not significant (F1,4 = 3.9,p = 0.12). After catch, all birds decreased gizzard mass, but group 1 had larger gizzards than group 2 during the first series of trials, and smaller gizzards during the second series (Table 2, models 1.1 to 1.5), showing that the manipulation of gizzard size was successful. Each group consisted of three birds. However, data collected on one bird from group 2 after it became sick during series 2 was omitted from the graphs and the analysis. Error bars show standard error.

Mentions: The diet treatments successfully resulted in gizzard mass changes in the experimental red knots (Fig 1, model comparison in Table 2, see S1 Table for model estimates). Although all birds initially reduced gizzard mass, a diet of hard-shelled prey resulted in larger gizzards (estimate±SE: 8.3±0.3 g) than soft prey (6.1±0.3 g). Group (group 1 or group 2) had no significant effect on gizzard mass. However, the hard-shelled diet led to a larger rate of gizzard mass increase in group 2 than in group 1 (significant interaction between diet and group, see Table 2 and model estimates in S1 Table), presumably because the birds were less eager to increase gizzard mass soon after the catch (see also Fig 1). The diet-induced rates of change in gizzard mass where comparable to those found earlier (for details see S3 File) [6].


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)

Mean gizzard mass of birds directly after catch, during the first and second series of trials.Directly after catch, the 6 red knots were randomly divided into two groups, group 1 (solid dots and line) and group 2 (open dots and dashed line). Both groups received different diets outside the experimental trials (soft or hard-shelled prey) to manipulate gizzard size. Initial differences in gizzard mass between groups were not significant (F1,4 = 3.9,p = 0.12). After catch, all birds decreased gizzard mass, but group 1 had larger gizzards than group 2 during the first series of trials, and smaller gizzards during the second series (Table 2, models 1.1 to 1.5), showing that the manipulation of gizzard size was successful. Each group consisted of three birds. However, data collected on one bird from group 2 after it became sick during series 2 was omitted from the graphs and the analysis. Error bars show standard error.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136144.g001: Mean gizzard mass of birds directly after catch, during the first and second series of trials.Directly after catch, the 6 red knots were randomly divided into two groups, group 1 (solid dots and line) and group 2 (open dots and dashed line). Both groups received different diets outside the experimental trials (soft or hard-shelled prey) to manipulate gizzard size. Initial differences in gizzard mass between groups were not significant (F1,4 = 3.9,p = 0.12). After catch, all birds decreased gizzard mass, but group 1 had larger gizzards than group 2 during the first series of trials, and smaller gizzards during the second series (Table 2, models 1.1 to 1.5), showing that the manipulation of gizzard size was successful. Each group consisted of three birds. However, data collected on one bird from group 2 after it became sick during series 2 was omitted from the graphs and the analysis. Error bars show standard error.
Mentions: The diet treatments successfully resulted in gizzard mass changes in the experimental red knots (Fig 1, model comparison in Table 2, see S1 Table for model estimates). Although all birds initially reduced gizzard mass, a diet of hard-shelled prey resulted in larger gizzards (estimate±SE: 8.3±0.3 g) than soft prey (6.1±0.3 g). Group (group 1 or group 2) had no significant effect on gizzard mass. However, the hard-shelled diet led to a larger rate of gizzard mass increase in group 2 than in group 1 (significant interaction between diet and group, see Table 2 and model estimates in S1 Table), presumably because the birds were less eager to increase gizzard mass soon after the catch (see also Fig 1). The diet-induced rates of change in gizzard mass where comparable to those found earlier (for details see S3 File) [6].

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