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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

Regression of DMshell intake on non-toxic prey against gizzard mass.Data from this study on Dosinia was combined with data from van Gils et al. [14] on other non-toxic prey species. Adding the current data to the regression derived by van Gils et al. [14] slightly changes the regression line (though not significantly; from dashed to solid line), but greatly reduces standard error (from light to dark grey area). Parameter estimates are shown in S1 Table (model 3.1). Regressions are linear regressions on log-transformed data. Note that van Gils et al. [14] averaged gizzard mass measurements per bird, whereas we estimated gizzard mass in each trial by interpolating measurements.
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pone.0136144.g003: Regression of DMshell intake on non-toxic prey against gizzard mass.Data from this study on Dosinia was combined with data from van Gils et al. [14] on other non-toxic prey species. Adding the current data to the regression derived by van Gils et al. [14] slightly changes the regression line (though not significantly; from dashed to solid line), but greatly reduces standard error (from light to dark grey area). Parameter estimates are shown in S1 Table (model 3.1). Regressions are linear regressions on log-transformed data. Note that van Gils et al. [14] averaged gizzard mass measurements per bird, whereas we estimated gizzard mass in each trial by interpolating measurements.

Mentions: To confirm that the relation between gizzard mass and dry shell-mass (DMshell) intake rate on Dosinia agreed with the earlier observed relations by van Gils et al. [14], we compared the two outcomes. Van Gils et al. measured maximum DMshell intake rates in 6 captive red knots (C. c. islandica) in the Dutch Wadden Sea on two non-toxic bivalve species, Cerastoderma edule (Linnaeus) and Macoma balthica (Linnaeus). Similar to the present study, they manipulated gizzard masses by placing birds randomly in one of two groups, one with a soft prey diet and the other with a hard-shelled diet. They estimated gizzard mass in each bird as the mean of a series of gizzard measurements in the course of the experimental trials. By comparing linear models, they concluded that DMshell intake was independent of bird individual, prey species and prey size. They found a linear relationship with gizzard mass on log-transformed data (R2 = 0.48, p < 0.001, Fig 3).


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)

Regression of DMshell intake on non-toxic prey against gizzard mass.Data from this study on Dosinia was combined with data from van Gils et al. [14] on other non-toxic prey species. Adding the current data to the regression derived by van Gils et al. [14] slightly changes the regression line (though not significantly; from dashed to solid line), but greatly reduces standard error (from light to dark grey area). Parameter estimates are shown in S1 Table (model 3.1). Regressions are linear regressions on log-transformed data. Note that van Gils et al. [14] averaged gizzard mass measurements per bird, whereas we estimated gizzard mass in each trial by interpolating measurements.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136144.g003: Regression of DMshell intake on non-toxic prey against gizzard mass.Data from this study on Dosinia was combined with data from van Gils et al. [14] on other non-toxic prey species. Adding the current data to the regression derived by van Gils et al. [14] slightly changes the regression line (though not significantly; from dashed to solid line), but greatly reduces standard error (from light to dark grey area). Parameter estimates are shown in S1 Table (model 3.1). Regressions are linear regressions on log-transformed data. Note that van Gils et al. [14] averaged gizzard mass measurements per bird, whereas we estimated gizzard mass in each trial by interpolating measurements.
Mentions: To confirm that the relation between gizzard mass and dry shell-mass (DMshell) intake rate on Dosinia agreed with the earlier observed relations by van Gils et al. [14], we compared the two outcomes. Van Gils et al. measured maximum DMshell intake rates in 6 captive red knots (C. c. islandica) in the Dutch Wadden Sea on two non-toxic bivalve species, Cerastoderma edule (Linnaeus) and Macoma balthica (Linnaeus). Similar to the present study, they manipulated gizzard masses by placing birds randomly in one of two groups, one with a soft prey diet and the other with a hard-shelled diet. They estimated gizzard mass in each bird as the mean of a series of gizzard measurements in the course of the experimental trials. By comparing linear models, they concluded that DMshell intake was independent of bird individual, prey species and prey size. They found a linear relationship with gizzard mass on log-transformed data (R2 = 0.48, p < 0.001, Fig 3).

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