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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

Dry shell mass (DMshell) intake rate on a Dosinia diet (A) and on a Loripes diet (B).Lines connect all trials of the same bird when it was in the small gizzard group (open dots) and in the large gizzard group (solid dots). Intake of Dosinia was higher for birds with large gizzards, whereas intake of Loripes was not affected by gizzard size (model 2.1 in S1 Table). Loripes intake rate was generally lower than Dosinia intake rate. These results confirm that intake of Dosinia is limited by a digestive constraint, whereas intake of Loripes is limited more stringently, presumably by its toxic load, and independent of gizzard mass.
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pone.0136144.g002: Dry shell mass (DMshell) intake rate on a Dosinia diet (A) and on a Loripes diet (B).Lines connect all trials of the same bird when it was in the small gizzard group (open dots) and in the large gizzard group (solid dots). Intake of Dosinia was higher for birds with large gizzards, whereas intake of Loripes was not affected by gizzard size (model 2.1 in S1 Table). Loripes intake rate was generally lower than Dosinia intake rate. These results confirm that intake of Dosinia is limited by a digestive constraint, whereas intake of Loripes is limited more stringently, presumably by its toxic load, and independent of gizzard mass.

Mentions: Gizzard mass manipulations had an effect on intake rate (expressed as DMshell), dependent on prey species (model 2.1 in Table 2, see S1 Table for model estimates). As expected, DMshell intake of toxic Loripes did not change with an increase in gizzard mass (estimated change from 1.25 to 1.31 mg/s, t = 0.65, p = 0.52), whereas intake of non-toxic Dosinia did increase with gizzard mass (estimated change from 2.00 to 3.12 mg/s, t = 3.73, p<0.001). DMshell intake on a Loripes diet was lower than on a Dosinia diet for small gizzard birds (estimated difference -0.75 mg/s, t = -3.21, p = 0.002) as well as for large gizzard birds (estimated difference -1.81 mg/s, t = -8.37, p<0.001). These results are depicted in Fig 2, where gizzard masses are shown on a continuous scale. The results indicate that the shell-mass processing constraint was alleviated with an increase in gizzard mass, as predicted, and that the toxin constraint was independent of gizzard mass. To test if morphological characters of individual birds other than gizzard size influenced intake rate, the explanatory variables body mass, bill length, tarsus length and wing length of the individual birds were separately added to model 2.1. None of these variables improved the statistical fit of the model (results not shown).


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)

Dry shell mass (DMshell) intake rate on a Dosinia diet (A) and on a Loripes diet (B).Lines connect all trials of the same bird when it was in the small gizzard group (open dots) and in the large gizzard group (solid dots). Intake of Dosinia was higher for birds with large gizzards, whereas intake of Loripes was not affected by gizzard size (model 2.1 in S1 Table). Loripes intake rate was generally lower than Dosinia intake rate. These results confirm that intake of Dosinia is limited by a digestive constraint, whereas intake of Loripes is limited more stringently, presumably by its toxic load, and independent of gizzard mass.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136144.g002: Dry shell mass (DMshell) intake rate on a Dosinia diet (A) and on a Loripes diet (B).Lines connect all trials of the same bird when it was in the small gizzard group (open dots) and in the large gizzard group (solid dots). Intake of Dosinia was higher for birds with large gizzards, whereas intake of Loripes was not affected by gizzard size (model 2.1 in S1 Table). Loripes intake rate was generally lower than Dosinia intake rate. These results confirm that intake of Dosinia is limited by a digestive constraint, whereas intake of Loripes is limited more stringently, presumably by its toxic load, and independent of gizzard mass.
Mentions: Gizzard mass manipulations had an effect on intake rate (expressed as DMshell), dependent on prey species (model 2.1 in Table 2, see S1 Table for model estimates). As expected, DMshell intake of toxic Loripes did not change with an increase in gizzard mass (estimated change from 1.25 to 1.31 mg/s, t = 0.65, p = 0.52), whereas intake of non-toxic Dosinia did increase with gizzard mass (estimated change from 2.00 to 3.12 mg/s, t = 3.73, p<0.001). DMshell intake on a Loripes diet was lower than on a Dosinia diet for small gizzard birds (estimated difference -0.75 mg/s, t = -3.21, p = 0.002) as well as for large gizzard birds (estimated difference -1.81 mg/s, t = -8.37, p<0.001). These results are depicted in Fig 2, where gizzard masses are shown on a continuous scale. The results indicate that the shell-mass processing constraint was alleviated with an increase in gizzard mass, as predicted, and that the toxin constraint was independent of gizzard mass. To test if morphological characters of individual birds other than gizzard size influenced intake rate, the explanatory variables body mass, bill length, tarsus length and wing length of the individual birds were separately added to model 2.1. None of these variables improved the statistical fit of the model (results not shown).

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