Article

Pyrogallol Poisoning of Pigeons Caused by Acorns

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Abstract

Green acorns are known to contain high concentrations of pyrogallol. Here, we describe an extended case report of two pigeons found dead with a filled muscular stomach of acorns. The following pathologic findings were observed: irritation of mucosal membranes in the gastrointestinal tract, blackish discolored chyme, hyperemic organs, and general edemas. The muscular stomach (ventriculus) was filled with pieces of acorns, and the abdominal cavity contained bloody aqueous fluid. In order to uncover the cause of death, we determined pyrogallol in liver and kidney of one dead pigeon and in ventriculus contents of both pigeons by gas chromatography/mass spectrometry. A further aim of our study was to compare pathologic findings and pyrogallol concentrations in kidney, liver, and ventriculus of poisoned pigeons with those of healthy pigeons. The pyrogallol concentrations in samples of dead pigeons were 16-1200-fold higher than in control animals fed grass and maize-corn. Altogether, the acorn-filled ventriculus, the pathologic findings, the well nourished state, and the high pyrogallol concentrations in the dead pigeons suggest an acute pyrogallol poisoning by acorn. With respect to controls, we conclude that pyrogallol concentrations of 6 ng/g of kidney, 8 ng/g of liver, and 2 ng/g of gastric content do not affect the health of pigeons.

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... Tannins, a diverse group of water-soluble phenolics, are thought to be provide a defense against herbivory by reducing protein digestibility (Zucker 1983;Hagerman and Klucher 1986;Mehansho et al. 1987). They are also potential toxins that cause direct detrimental effects to gastrointestinal mucosa and epithelia, kidney and liver failure, intrinsic nitrogen loss, and disturbance of sodium balance (Fowler and Richards 1965;Glick and Joslyn 1970;Freeland et al. 1985;Robbins et al. 1987; Thomas et al. 1988;Dietz et al. 1994;Dearing 1997a;Meiser et al. 2000). In fact, 3% quebracho (a type of condensed tannins) added to the control diet causes a significant de-crease of survival rate of the prairie vole Microtus ochrogaster (Lindroth and Batzli 1984), and similar results are reported in other rodents (rat, Joslyn and Glick 1968;hamster, Mehansho et al. 1984;mouse, Freeland et al. 1985; the meadow vole Microtus pennsylvanicus, Dietz et al. 1994). ...
... Negative nitrogen balances have been reported only by Short (1976) in fox squirrels to which acorns were fed. Contrary to this finding, lethal damage, such as gastrointestinal lesions, kidney failure, and steep reduction in body weight, has been reported in livestock (Fowler and Richards 1965;Basden and Dalvi 1987) and avian species (Dixon et al. 1997;Johnson et al. 1993;Meiser et al. 2000). These interspecific differences in response of mammals to acorn feeding may be related to proline-rich proteins (PRPs), which are produced in saliva by some mammalian species. ...
... Mammalian herbivores producing PRPs are expected not to suffer heavy damage from natural diets containing tannins, unlike animals without PRPs (Robbins et al. 1991;Juntheikki 1996). Cattle, sheep, and avian species, which suffer acorn poisoning (Fowler and Richards 1965;Johnson et al. 1993;Dixon et al. 1997; Meiser et al. 2000), do not produce PRPs. The gray squirrel and fox squirrel have not been investigated for the production of PRPs. A. speciosus does possess PRPs (Shimada et al., unpublished manuscript). ...
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... Secondary chemical compounds (e.g., tannins and other polyphenols) may also affect seed removal (e.g. Robbins et al., 1991;Dearing, 1997;Meiser et al., 2000;Burritt and Provenza, 2000;Dearing et al., 2000;Shimada and Saitoh, 2003). Tannins, a diverse group of soluble phenolic compounds, are thought to be defenses against herbivory (Robbins et al., 1991;Dearing, 1997;Meiser et al., 2000;Shimada and Saitoh, 2003). ...
... Robbins et al., 1991;Dearing, 1997;Meiser et al., 2000;Burritt and Provenza, 2000;Dearing et al., 2000;Shimada and Saitoh, 2003). Tannins, a diverse group of soluble phenolic compounds, are thought to be defenses against herbivory (Robbins et al., 1991;Dearing, 1997;Meiser et al., 2000;Shimada and Saitoh, 2003). Rodents often avoid acorns with high tannin concentration (Shimada, 2001;Shimada and Saitoh, 2003). ...
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Seed traits are important factors affecting seed predation by rodents and thereby the success of recruitment. Seeds of many tree species have hard hulls. These are thought to confer mechanical protection, but the effect of endocarp thickness on seed predation by rodents has not been well investigated. Wild apricot (Prunus armeniaca), wild peach (Amygdalus davidiana), cultivated walnut (Juglans regia), wild walnut (Juglans mandshurica Maxim) and Liaodong oak (Quercus liaotungensis) are very common tree species in northwestern Beijing city, China. Their seeds vary greatly in size, endocarp thickness, caloric value and tannin content. This paper aims to study the effects of seed traits on seed removal speed of these five tree species by small rodents in a temperate deciduous forest, with emphasis on the effect of endocarp thickness. The results indicated that speed of removal of seeds released at stations in the field decreased significantly with increasing endocarp thickness. We found no significant correlations between seed removal speed and other seed traits such as seed size, caloric value and tannin content. In seed selection experiments in small cages, Père David's rock squirrel (Sciurotamias davidianus), a large-bodied, strong-jawed rodent, selected all of the five seed species, and the selection order among the five seed species was determined by endocarp thickness and the ratio of endocarp mass/seed mass. In contrast, the Korean field mouse (Apodemus peninsulae) and Chinese white-bellied rat (Niviventer confucianus), with relatively small bodies and weak jaws, preferred to select small seeds like acorns of Q. liaotungensis and seeds of P. armeniaca, indicating that rodent body size is also an important factor affecting food selection based on seed size. These results suggest endocarp thickness significantly reduces seed removal speed by rodents and then negatively affects dispersal fitness of seeds before seed removal of tree species in the study region. However, effect of endocarp thickness on final dispersal fitness needs further investigation because it may increase seed caching and survival after seed removal.
... There are two main subgroups of tannins: condensed (not readily susceptible to degradation) and hydrolyzable tannins (susceptible to acid, base, or enzyme-catalyzed hydrolysis) (Hagerman 2011). Hydrolysis of tannins in the mammalian digestive tract releases phenolic acids that may be locally toxic to the gut microbiota and may damage the gastrointestinal mucosa and epithelium (McLean and Duncan 2006;Meiser et al. 2000). These products of hydrolysis may also be absorbed from the intestine and cause systemic harm (Niho et al. 2001). ...
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Dietary tannins are ubiquitous in woody plants and may have serious negative effects on herbivores by inducing a loss of dietary protein and producing toxins if they are hydrolyzed in the gut. Many herbivorous mammals counter the negative effects of tannins through tannin-binding salivary proteins (TBSPs) that inactivate tannins by forming insoluble complexes and prevent them from interacting with other more valuable proteins. Howlers are the most folivorous New World primates and ingest foods with varying tannin content. We studied the presence of TBSPs in six wild mantled howlers (Alouatta palliata mexicana) immediately after capture and in captivity when fed on two diets composed of natural ingredients: a mixture of fruit and leaves or only leaves. Protein concentration was determined in whole saliva samples, followed by gel electrophoresis. We identified two protein bands of 17 and 25 kDa that have tannin-binding capacity. Although the monkeys ate almost twice as much condensed tannins in the leaf diet than in the fruits and leaves diet (7 vs. 4 g/d dry matter) the salivary protein concentration did not differ between the two diets (leaf diet: 3.29 ± SE 0.82 vs. fruit and leaves diet: 3.42 ± SE 0.62 mg/ml) and we found no additional protein bands in response to either diet. We suggest that the continuous expression of TBSPs is part of a dietary strategy that enables howlers to consume diets with variable tannin contents, thus partly explaining their dietary flexibility. Although the importance of salivary proteins to arboreal primates is broadly accepted, to our knowledge this is the first report of TBSPs in any Neotropical primate.
... Skin irritation is defined as a locally arising and non-immunogenic inflammatory reaction, which appears shortly after stimulation and usually disappears in a few days (Harvell et al., 1995). As an acid, PYR has been shown to cause irritation of mucosal membranes in the gastrointestinal tract (Meiser et al., 2000;Gosselin et al., 1981). Therefore, the acidic nature of PYR may be responsible for its irritant effects. ...
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... Tannins are a widespread group of PSMs that are broadly distributed in various plant parts (Waterman and Mole 1994). Ingesting tannins, a diverse group of watersoluble phenolics with high affinity for proteins, may have negative effects on herbivores, such as reduction in protein digestibility (Robbins et al. 1987;Chung-MacCoubrey et al. 1997;Shimada and Saitoh 2003), damage to the gastrointestinal mucosa and epithelium (Meiser et al. 2000), or endogenous nitrogen loss (Shimada and Saitoh 2003). ...
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Mammalian herbivores adopt various countermeasures against dietary tannins, which are among the most widespread plant secondary metabolites. The large Japanese wood mouse Apodemus speciosus produces proline-rich salivary tannin-binding proteins in response to tannins. Proline-rich proteins (PRPs) react with tannins to form stable complexes that are excreted in the feces. Here, we developed a new method for estimating the tannin intake of free-living small rodents, by measuring fecal proline content, and applied the method to a field investigation. A feeding experiment with artificial diets containing various levels of tannic acid revealed that fecal proline content was clearly related to dietary tannin content in three species (A. speciosus, Apodemus argenteus, and Myodes rufocanus). We then used fecal proline content to estimate the tannin intakes of these three forest-dwelling species in a forest in Hokkaido. In the autumn, estimated tannin intakes increased significantly in the Apodemus species, but not in M. rufocanus. We speculated that an increase in tannin intake during autumn may result from consumption of tannin-rich acorns. This hypothesis was consistent with population fluctuation patterns of the three species, which were well-synchronized with acorn abundance for the Apodemus species but not for M. rufocanus.
... 9 Pigeons poisoned with green acorns, which contain high concentrations of pyrogallol, developed gastroenteritis. 10 The characteristic lesion in mice 5 and chickens 11 fed toxic quantities of tannic acid experimentally is periacinar hepatic necrosis. Australian king parrots affected by wasting and diarrhoea in the ACT in 1990 and 1991 had been feeding on acorns, most had diarrhoea and some exhibited dysentery, but none had nephrosis or periacinar hepatic necrosis. ...
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