Feeding preferences of experienced and naïve goats and sheep for the toxic plant Ipomoea carnea subsp. fistulosa

Comportamento ingestivo de caprinos e ovinos habituados e não habituados a ingerir Ipomoea carnea subsp. fistulosa

Abstracts

Ipomoea carnea is a toxic plant that grazing goats and cattle may learn to ingest with repeated exposure. The objective of this study was to evaluate the feeding preferences of experienced and non-experienced (naïve) goats and sheep for I. carnea. The study used 3 groups of 5 goats (Group 1, experienced that were previously poisoned by the plant; group 2, naïve; Group 3, experienced eaters, composed of animals adapted to eat the fresh plant) and 2 groups of sheep (group 4, experienced that were previously poisoned by the plant; and group 5, naïve). For the test, the animals were placed daily for 10 minutes and 4 days in a rectangular stall (5x7m) with 4 feeders, each with 200g of a different food (Ipomoea carnea, commercial concentrate food, recently harvested green grass (mainly Brachiaria spp.), and Cynodon dactylonhay. The intake of concentrate food was significantly higher (P<0.05) than the consumption of green grass, hay and I. carnea. In a second 4 day trial, in which the commercial concentrate food was replaced by freshly harvested Amorimia septentrionalis, the ingestion of green grass (Brachiaria spp.) was significantly higher (P<0.05) than the consumption of other foods. In both trials there was no significant difference in food consumption between eaters and naïve animals. The results suggest that experienced or naïve sheep and goats do not prefer I. carnea when it is offered with other foods or forages, suggesting that animals will avoid the plant and not become poisoned if other food options are available.

feeding behavior; Ipomoea spp; poisonous plants; swainsonine-containing plants

Ipomoea carnea é uma planta tóxica para caprinos e bovinos, que podem desenvolver o hábito de ingeri-la de forma compulsiva. O objetivo deste estudo foi avaliar o comportamento ingestivo de caprinos e ovinos habituados e não habituados a ingerir I. carnea. O estudo utilizou três grupos de cinco caprinos (Grupo 1, animais previamente intoxicados pela planta; Grupo 2, controle; Grupo 3, animais adaptados a ingerir a planta fresca) e dois grupos de cinco ovinos (Grupo 4, animais previamente intoxicados pela planta; e Grupo 5, controle). Para o teste, os animais foram introduzidos por 10 minutos, durante 4 dias consecutivos, em uma baia retangular (5x7m), com 4 caixas de alimentação, cada uma com 200g de um alimento diferente (Ipomoea carnea; concentrado comercial; capim verde recém colhido, principalmente Brachiaria spp.; e feno de Cynodon dactylon). A ingestão de concentrado foi significativamente maior (P<0,05) do que o consumo de capim verde, feno e I. carnea. Em um segundo ensaio de 4 dias, em que o concentrado foi substituído por Amorimia septentrionalis recém-colhida, a ingestão de capim verde (Brachiaria spp.) foi significativamente maior (P<0,05) do que o consumo dos outros alimentos. Em nenhuma das duas espécies, houve diferenças no comportamento ingestivo entre animais habituados e não habituados a ingerir I. carnea. Os resultados sugerem que ovinos e caprinos habituados e não habituados a ingerir I. carnea não preferem a planta quando é oferecida com outros alimentos ou forragens, o que sugere que os animais irão evitar a planta e não haverá intoxicação se outras opções de alimentos estão disponíveis.

comportamento ingestivo; Ipomoea spp; plantas tóxicas; plantas que contêm swainsonina

INTRODUCTION:

Ipomoea carnea subsp. fistulosa (Figure 1) is a swainsonine-containing plant that induces glycoprotein storage disease in ruminants characterized by neurologic signs that cause the death of numerous goats in Northeastern and Northern Brazil (ARMIÉN et al., 2007; OLIVEIRA et al., 2009). Swainsonine causes cellular accumulation of oligosaccharides due to inhibition of several important enzymes, resulting in cellular vacuolization and death in the central nervous system and in other systems (DE BALOGH et al., 1999). Consumption of the plant is an important cause of losses in goats in the north and northeastern Brazilian regions (ARMIÉN et al., 2007; OLIVEIRA et al., 2009; PIMENTEL et al., 2012) and has been also diagnosed in cattle in the Pantanal region of Mato Grosso (ANTONIASSI et al., 2007). Normally, grazing livestock do not ingest I. carnea, but anecdotal accounts by livestock producers suggest that goats and cattle that start to consume the plant develop the habit to ingest it compulsively, even with sufficient alternative forage (ARMIÉN et al., 2007; TOKARNIA et al., 2007; OLIVEIRA et al., 2009, 2011). This behavior, defined by farmers as addiction (or strong preference), is not observed in sheep (ADRIEN et al., 2013b).

Figure 1:
Ipomoea carnea var. fistulosa. Municipality of Castanhal, state of Pará.

There is no treatment for the poisoning, and control methods include the development of conditioned food aversions (ADRIEN et al., 2013a; OLIVEIRA et al., 2013, 2014; PIMENTEL et al., 2012, 2013).Studies have shown that goats that were naïve but exposed to the plant, then conditioned to avoid eating it, did not ingest the plant for at least 2 years and 8 months. However, aversion was not effective in goats that have developed the habit of consuming the plant for long periods of time (OLIVEIRA et al., 2014). There are indications that the maintenance of the conditioned aversion in goats is favored by the availability of other forages (OLIVEIRA et al., 2014). The aversive treatment reduced goats' consumption of the plant during the rainy season, but during the dry season the goats again consumed the plant, as it was the only green forage available (PIMENTEL et al., 2013). It appears that hunger due to shortage of forage, associated with large amounts of the plant in the field, are the main factors leading goats and cattle to ingest I. carnea (ANTONIASSI et al., 2007; ARMIÉN et al., 2007; OLIVEIRA et al., 2009). However, young goats may consume I. carnea even with good forage availability (OLIVEIRA et al., 2014).

Sheep may be intoxicated spontaneously (TOKARNIA et al., 1960) or experimentally (ARMIÉN et al., 2011) with high doses of I. carnea. However, on farms where sheep are raised together with goats the poisoning occurs in goats, but not in sheep (TORTELLI et al., 2008). The difference in the occurrence of the poisoning in the two species may be explained by their different eating habits, food preferences or susceptibility to the poisoning. An increased understanding of goats' and sheep preferences for I. carnea, and how those preferences may vary with previous experience with the plant, is important to develop grazing management options to reduce animal losses. Thus, the objective of this study was to evaluate the feeding preference of experienced and non-experienced (naïve) goats and sheep for I. carnea, and to determine if there was learned compulsive eating or preference of this plant by experienced goats and sheep.

MATERIAL AND METHODS:

Animals

Fifteen goats and 10 sheep were divided into 5 groups: Group 1 was formed by 5 goats that were intoxicated by swainsonine in a previous experiment (OLIVEIRA et al., 2015, unpublished); they had received ground I. carnea equivalent to 3mg/kg bw of swainsonine (four goats) for 41-43 days, or 1mg kg^-1 of swainsonine for 61 days (one goat). The administration of the plant was suspended after the first clinical signs of poisoning were observed (rough hair coat, weight loss, and nervous signs associated mainly with cerebellar and brain stem lesions as difficulties in standing, ataxia, hypermetria, wide-based stance, lateral gait, intention tremors, spastic paresis or weakness, abnormal postural reactions, nystagmus, loss of equilibrium and falling to the side or backward). In Group 1, animals were allowed to recover from clinical signs for 31 to 51 days after the end of the administration, and then the animals ingested 200g of green leaves of I. carnea for 15 days to reinforce the experience. Group 2 was formed by 5 naïve goats that never ingested I. carnea; these animals were raised on a pasture of native vegetation (caatinga) of the Brazilian semiarid. Group 3 was formed by 5 goats that grazed 3 days a week for 2 hours daily, for at least 2 months, in an area severely invaded by I. carnea (PIMENTEL et al., 2013) and they all consumed the plant regularly. No clinical signs were observed in this group; Group 4 was formed by 4 sheep that received ground I. carnea from days 43 to 93 at the daily dose equivalent to 3mg kg^-1 bw of swainsonine plus one sheep that received 1mg kg^-1 bw for 107 days (OLIVEIRA et al., 2015, unpublished). The administration of the plant was suspended after the observation of the first clinical signs of poisoning. After the recovery from clinical signs, 1 to 49 days after the end of the administration, the animals ingested, daily, 200g of green leaves of I. carnea for 15 days to reinforce the experience. Group 5 was formed by 5 naïve sheep that never ingested I. carnea. In groups 1 and 4, dry I. carnea was administrated by mixing the plant with commercial concentrate ration, which was given in an amount equivalent to 1.5% of body weight and was ingested spontaneously by all animals.

Test pen and foods offered

For the test, the animals were individually placed in a rectangular pen (5x7m) with 4 feeders, identified from 1 to 4, distributed equidistant from one another, on each side of the pen, positioned so that the animal entering the pen could initially choose any of the feeders.

Before the start of the experiment, all animals were trained for 25 days to become familiar with the location of the feeders in the stall and to consume the various foods offered in the feeder. To this end, after an overnight fast, each food was offered to each animal individually for 5 days by putting 50g of the food in each one of the four feeders and allowing the animal access for ten minutes a day. Animals quickly learned to investigate each feeder.

During the first preference test, the following 4 foods were tested: freshly harvested leaves of I. carnea; a commercial concentrate food; recently harvested green grass (mainly Brachiaria spp.); and Cynodon dactylon(variety Tifton) hay. During the second 4 day period, 4 foods were again offered except the commercial concentrate food that was not offered and freshly harvested Amorimia (Mascagnia) septentrionalis was substituted in its place.

Preference test

The animals were fasted for at least 12 hours before the test. During the first four days test, 4 different foods were tested (commercial concentrate, fresh grass, hay, and I. carnea), by putting 200g of each food in each feeder. Every day each food was rotated to a different feeder, and each animal was introduced into the stall for 10 minutes, and the order they examined the different feeders was noted. At the end of the 10 minutes the amount of each food that remained in the feeders was weighed to determine the amount consumed. During the second test from day 5 to day 8 the most palatable food (commercial concentrate food) was removed and substituted by green leaves of A. septentrionalis. Amorimia septentrionalis is a native plant that contains relatively low amounts of monofluoroacetate (LEE et al., 2012), and is considered moderately palatable to grazing livestock (DUARTE et al., 2013). The amount offered to animals in these preference trials, even if totally consumed, was not sufficient to intoxicate the animals (DUARTE et al., 2013).

Swainsonine concentrations of freshly harvested leaves of I. carnea were determined by liquid chromatography and mass spectrometry (GARDNER et al., 2001).

Statistical analysis

The fixed effects of position, day, treatment (i.e., different foods), and the day × treatment interaction on proportion consumed (% of offered) were assessed using a generalized linear mixed model with a β distribution, a logit link, and Laplace estimation. Pen (i.e., different animals) was a random effects blocking factor. Pair wise comparisons among treatment means within a given day were adjusted for family wise Type I error (α = 0.05) using the Tukey-Kramer method. The analysis was done using the GLIMMIX procedure in SAS/STAT 12.1 (SAS Inst. Inc., Cary, NC).

RESULTS:

In 8 samples of the leaves of I. carnea used in this experiment, the mean concentration of swainsonine was 0.05%±0.05 with a range from non-detected to 0.155%. During the assessment of feeding preferences in the first trial, when the foods tested were I. carnea, concentrate food, green grass and hay, the intake of the concentrate food was significantly higher (P<0.05) that the consumption of green grass, hay and I. carnea (Figure 2). The second most consumed food by animals in all groups was green grass, with a significant difference (P<0.05) with the amounts of hay and I. carnea consumed by Group 4 (sheep poisoned previously by dry I. carnea) and 5 (control sheep) (Figure 2 D and E).

Figure 2:
Preference tests (% consumed) to evaluate goat and sheep preferences for a concentrate food, I. carnea, hay, and green grass, during four consecutive days. The treatments were: Group 1 (A), experienced goats that were previously poisoned by the plant; group 2 (B), naïve goats; Group 3 (C), experienced goat eaters not previously poisoned by the plant; group 4 (D), experienced sheep that were previously poisoned by the plant; and group 5 (E), naïve sheep.

In trial 2 when the most preferred food (concentrate) was substituted by Amorimia (Mascagnia) septentrionalis, the ingestion of green grass (Brachiaria spp.) was significantly higher (P<0.05) than the consumption of the other foods (A. septentrionalis, I. carnea, and hay) in the 5 groups (Figure 3), with no differences (P>0.05) among the hay, I. carnea and A. septentrionalis.

Figure 3:
Preference test to evaluate the preference for the consumption of I. carnea, A. septentrionalis, hay, and green grass, during four consecutive days in groups 1 (A), 2 (B), 3 (C) 4 (D), and 5 (E).

In both trials no significant differences in food consumption were observed between eaters and naïve animals.

DISCUSSION:

Previous reports suggested that after starting to eat I. carnea, goats develop a preference or even strong preference to the plant (ARMIÉN et al., 2007; TOKARNIA et al., 2007; OLIVEIRA et al., 2009). In this experiment goats and sheep from all treatment groups, including those with substantial prior experience with the plant to the point of intoxication, consumed I. carnea in a lesser amount than the highly palatable concentrate food and green grass, indicating that the animals do not develop a preference for I . carnea under these experimental conditions. These results suggest that if goats and sheep have sufficient high quality concentrate food or green grasses, they will not eat I. carnea in high enough quantities to become intoxicated. To occur intoxication, animals must ingest relatively large amounts of I. carnea. TOKARNIA et al. (1960) observed the first clinical signs of poisoning in two goats after they had been ingesting the plant as sole food source for 35 and 46 days, respectively.In another experiment, goats showed the first clinical signs 21 to 42 days after the ingestion of daily doses of 24 to 96g of the green plant kg^-1 bw (ARMIÉN et al., 2007). In Mozambique, 2 goats ingesting daily doses of 50g of green plant/kg bw showed first clinical signs after 39 and 54 days, respectively (DE BALOGH et al., 1999).

The swainsonine concentration in the plant is no doubt a factor in whether animals become intoxicated; however, despite the variations found between different samples from the same location, the mean swainsonine concentrations of plants from different places showed little variation. In the state of Paraiba, samples of I. carneacausing outbreaks in the northeastern region contained 0.07+0.06% swainsonine (PIMENTEL et al., 2012) and samples collected in the same experimental area where the plant was collected for this preference experiment contained 0.05+0.05% swainsonine (PIMENTEL et al., 2013). In the Northern region, concentrations of swainsonine in I. carnea from different places were 0.05+0.01% (ADRIEN et al., 2013a), 0.05+0.03% (OLIVEIRA et al., 2014), and 0.07+0.08% (OLIVEIRA et al., 2015). Samples collected in the Southern region contained 0.06+0.004% swainsonine (ADRIEN et al., 2013b).

In goats, another factor determining the occurrence of the disease is year-round availability of the plant. The plant is always growing in wet areas (e.g., edges of ponds), and stays green for the whole year including during the dry season when there is a shortage of other forage (ANTONIASSI et al., 2007; OLIVEIRA et al., 2009; PIMENTEL et al., 2012). Hunger due to shortage of forage is obviously the main factor to induce grazing goats to ingest I. carnea, and consumption by some individuals within a herd will induce others to ingest the plant through social facilitation; however, young, inexperienced goats may initiate ingestion even with ample forage availability (OLIVEIRA et al., 2014). Nevertheless, as these pen trials have demonstrated, goats show little preference for I. carnea when given a choice of other foods, and thus it seems unlikely that with sufficient availability of other forage, goats will ingest enough of the plant to become intoxicated.

Poisoning by I. carnea is frequent in goats in northern and northeastern regions of Brazil, but not in sheep. Even though some livestock producers raising animals along the borders of the São Francisco river (states of Pernambuco, Bahia, and Alagoas) mention the occurrence of the disease in sheep (personal communication), there is only one report of two cases of poisoning in sheep (TOKARNIA et al., 1960), which suggests that sheep may be more resistant to the poisoning than goats or that they typically avoid the plant. ADRIEN et al. (2013b) in experiments to induce a conditioned aversion in sheep to the plant, observed that even sheep adapted to consume I. carnea, ingested limited amounts of plant when placed into invaded areas with large amounts of I. carnea. In the present experiment, the only difference noted between goats and sheep was when the foods tested were a highly palatable concentrate food, green grass and hay. In this case, the intake of green grass by sheep from groups 4 and 5 was significantly greater than their intake of I. carnea, whereas there was no difference in the consumption of green grass and I. carnea in the goats.

The anecdotal accounts of strong preference by grazing animals to swainsonine-containing plants have not been verified in experimental settings (RALPHS et al., 1990; PFISTER et al., 1992). However, strong preference to foods are a complex interaction of many factors, difficult to study even in highly controlled research settings with rodents (CORWIN et al., 2011). To answer this question definitively will likely require research in which rodents self administer purified swainsonine, similar to strong preference studies with compounds of abuse in which rats are first trained to press a lever for intravenous infusions (e.g., QUICK et al., 2011).

CONCLUSION:

In conclusion sheep and goats with extensive experience in consuming I. carnea showed no preference for fresh plant when it was offered with other foods. These results suggest that grazing animals will not become poisoned if other foods or forages are available.

ACKNOWLEDMENTS

This research was supported by the National Institute for Science and Technology for the Control of Plant Poisonings, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grant 573534/2008-0.

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Publication Dates

• Publication in this collection
  Sept 2015

History

• Received
  17 Nov 2014
• Accepted
  24 Jan 2015