Review

Received: 6 July 2011, Revised: 25 August 2011, Accepted: 8 September 2011 Published online in Wiley Online Library: 6 December 2011

(wileyonlinelibrary.com) DOI 10.1002/jat.1754

A review of poisonous plants that cause

reproductive failure and malformations in the
ruminants of Brazil
Franklin Riet-Correa,* Rosane M. T. Medeiros and Ana Lucia Schild
ABSTRACT: The objective of this review is to provide a report on toxic plants causing reproductive problems in ruminants in
Brazil. Aspidosperma pyrifolium causes abortion or stillbirth in goats, as well as most likely in sheep and cattle, in the semiarid
regions of Northeastern Brazil. Intoxications by Ateleia glazioveana, Tetrapterys acutifolia and T. multiglandulosa result in
abortion and neonatal mortality in cattle and sheep, and the same signs have been experimentally observed in goats. These
three plants can also cause cardiac fibrosis and a nervous disease with spongiosis of the central nervous system. Other plants
known to cause abortion include Enterolobium contortisiliquum, E. gummiferum, Stryphnodendron coriaceum, S. obovatum and
S. fissuratum. These plants can also cause digestive signs and photosensitization. Abortions have been reported in animals
intoxicated by nitrates and nitrites as well. Infertility, abortions and the birth of weak offspring have been reported in
animals intoxicated by plants containing swainsonine, including Ipomoea spp., Turbina cordata and Sida carpinifolia. Trifolium
subterraneum causes estrogenism in cattle. Mimosa tenuiflora and, most likely, M. ophthalmocentra cause malformations and
embryonic mortality in goats, sheep and cattle in the semiarid regions of Northeastern Brazil. Copyright © 2011 John Wiley &
Sons, Ltd.

Keywords: toxic plants; abortion; embryonic mortality; malformations; Aspidosperma; Ateleia; Tetrapterys; Mimosa; Enterolobium;
Stryphnodendron; Ipomoea; Turbina; Sida; Trifolium

INTRODUCTION however, goats were the only animals to abort (Lima and Soto-
Blanco, 2010). Experimental administration of A. pyrifolium
It is estimated that the toxic plants found in Brazil cause the results in abortion in goats (Medeiros et al., 2004), but currently,
death of 975 000–1 365 000 cattle each year (Riet-Correa et al., there are no experiments demonstrating the abortive effects of
2009b). There are at least 129 toxic plant species in Brazil, belong- this plant in sheep and cattle.
ing to 78 genera, and an ever-growing list of newly recognized The primary clinical sign of A. pyrifolium poisoning is abortion
toxic species are reported each year. The aim of this paper is to during any stage of gestation or the premature birth of kids that
review the plants that cause reproductive failure and malforma- die shortly after parturition. This suggests that, in addition to
tions in ruminants in Brazil. causing abortion, the plant can also cause premature parturition
in which many newborns are born alive but die shortly after
birth. If gestation is near term when the plant is eaten, the
ABORTION-INDUCING PLANTS offspring can potentially survive, but if the plant is eaten during
Aspidosperma pyrifolium the first 34 days of gestation, embryonic death results (Medeiros
et al., 2004). There are no documented descriptions of fetal or
Aspidosperma pyrifolium (Fig. 1) is a xerophilous tree of the placental lesions (Medeiros et al., 2004; Silva et al., 2006).
Apocynaceae family that causes embryonic deaths, abortion The toxic component of A. pyrifolium remains unknown,
and premature birth in goats, and probably also sheep and but the monoterpenoid indole alkaloids aspidofractinine, 15-
cattle, in the semiarid region of northeastern Brazil. Poisoning demethoxypyrifoline and N-formylaspidofractine have previ-
occurs primarily during the first months of the dry season, when ously been identified in the plant (Araújo et al., 2007). Leaves
forage becomes scarce from lack of rain. During this period, of the plant were negative for the presence of isocupressic acid,
A. pyrifolium maintains green foliage and is the main available a known abortifacient in pine needles (Riet-Correa et al., 2009b).
source of forage. Abortions also occur throughout the dry Treatment with an extract of A. pyrifolium resulted in maternal
season and at the start of the rainy season. This occurs because toxicity in rats, promoted hemolysis of red blood cells and was
following a rain event the plant rapidly resprouts and is often
eaten by pregnant goats (Medeiros et al., 2004). Abortions are
also observed when pregnant goats are moved to areas severely
invaded by the plant. Previous work has suggested that naive *Correspondence to: Riet-Correa, Franklin, Hospital Veterinário, CSTR, Universidade
goats are more likely to abort than experienced goats (Lima Federal de Campina Grande, Campus de Patos, Patos, PB 58700–000, Paraíba, Brazil.
E-mail: franklin.riet@pq.cnpq.br
and Soto-Blanco, 2010). Abortion associated with the ingestion
of A. pyrifolium has also been observed in sheep and cattle (Silva Hospital Veterinário, CSTR, Universidade Federal de Campina Grande, Campus
et al., 2006). In outbreaks occurring in flocks of sheep and goats,
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de Patos, Patos PB 58700-000, Paraíba, Brazil

J. Appl. Toxicol. 2012; 32: 245–254 Copyright © 2011 John Wiley & Sons, Ltd.
 F. Riet-Correa et al.

Figure 1. Aspidosperma pyrifolium: (A) green tree; (B) flowering tree; (C) flower; (D) pod.

lethal to 1-day-old Artemia salina larvae (Lima and Soto-Blanco, amount and duration of plant consumption (Gava and Barros,
2010). In goats, daily doses of 4–10 g of fresh leaves per kilogram 2001; Gava et al., 2001; Raffi et al., 2004; Riet-Correa et al., 2009a).
body weight (b.w.) caused abortion after 18–30 days of ingestion Ateleia glazioveana is the most important toxic plant found in
(Medeiros et al., 2004; unpublished data). Western Santa Catarina and Northwestern Rio Grande do Sul. It
Diagnoses are made using epidemiological data. When making can attain a height of 15 m but is normally 5–10 m tall. This decid-
a diagnosis, plant-caused abortion in sheep and goats should be uous tree has no leaves during the winter months (June to
confirmed and differentiated from other causes of abortion, August). The leaves are palatable, but animals mainly ingest them
including toxoplasmosis. Other causes of abortion resulting from when forage is lacking owing to drought or overgrazing (Gava
infectious diseases have not been identified in sheep or goats and Barros, 2001; Gava et al., 2001). Intoxication by this plant
found in the semiarid regions of Northeast Brazil. Additional causes causes abortions in cattle, sheep and horses. Abortions in cattle
of abortion in cattle in this region include brucellosis and can occur at any time during gestation but generally occur
leptospirosis. between November and May when animals ingest green leaves.
To reduce or avoid the reproductive effects caused by A. If the leaves are mingled with grasses, abortions sometimes
pyrifolium, pregnant goats should not graze in areas where this occur when livestock ingest tree litter during autumn. The
plant grows, primarily during the dry season when forage avail- frequency of abortion varies from 10 to 40% of pregnant cows
ability is low. When it is not possible to avoid grazing in these (Stolf et al., 1994; Gava and Barros, 2001; Gava et al., 2001).
areas, supplemental forage should be given to pregnant goats, Tetrapterys acutifolia and T. multiglandulosa are considered
which may aid in eliminating or partially reducing the consump- shrubs or vines. T. acutifolia is found in the states of Minas Gerais
tion A. pyrifolium. and Espírito Santo, and T. multiglandulosa is located in the states
of Rio de Janeiro, São Paulo and Mato Grosso do Sul. The
frequency of abortions resulting from these plants is variable. In
Ateleia glazioveana and Tetrapterys spp.
an outbreak of poisoning by T. multiglandulosa, 230 out of 290
Ateleia glazioveana (Leg. papilionoideae; Fig. 2), T. acutifolia, and cows (79%) either aborted or delivered weak calves, and seven
T. multiglandulosa (Fig. 3) (Malpighiaceae) cause abortions and cows died from cardiac insufficiency (Carvalho et al., 2006).
neonatal mortality in cattle (Tokarnia et al., 1989; Stolf et al., Recently, another species of Tetrapterys, not yet identified,
1994; Gava and Barros, 2001). Abortion in sheep by A. glazioveana located in the state of Rio de Janeiro was determined to cause
has been reported occasionally (Gava et al., 2003), and both abor- abortions (Peixoto et al., 2011).
tion and neonatal mortality have been induced experimentally in Similar clinical signs and lesions are observed in animals
cattle, sheep and goats (Stolf et al., 1994; Raffi et al., 2004; Garcia y poisoned by A. glazioveana and Tetrapterys spp. Abortions can
Santos et al., 2004; Riet-Correa et al., 2009a; Peixoto et al., 2011). occur during any stage of gestation (Riet-Correa et al., 2009b),
These plants can also cause a disease of the nervous system, but several reports have described a higher rate of incidence
resulting in vacuolation (status spongiosus) of the central nervous between the sixth and ninth months of gestation in cattle (Peixoto
system, and cardiac disease, involving fibrosis of the heart, which et al., 2011). Prior to abortion, some cows demonstrate a stage of
can cause sudden death or congestive heart failure. Considerable lethargy for 1–3 days. Other cows remain lying down for long
overlap exists between the different forms of the disease (Gava periods of time and occasionally exhibit some degree of blindness.
and Barros, 2001; Gava et al., 2001; Carvalho et al., 2006), and Clinical manifestations were not observed in most sheep that
the observed clinical manifestations vary depending on the aborted following experimental ingestion of A. glazioveana or
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Toxic plants affecting reproduction in ruminants

Figure 2. Ateleia glazioveana: (A) trees; (B) flowers; (C) seeds and leaves; (D) growing plant; (E) seed and pod. This figure was published in Riet-Correa
et al. (2009b), and the editors authorized its publication.

Figure 3. Tetrapterys multiglandulosa: (A and D) flowering plant; (B) leaves and flowers; (C) fruits. This figure was published in Riet-Correa et al. (2009b),
and the editors authorized its publication.

Tetrapterys spp. (Raffi et al., 2004; Riet-Correa et al., 2009b). Retained and at lower doses, calves and lambs can survive birth; however,
placentas and bloody vaginal discharge were reported in cattle neonates may be weak and unable to stand or suckle normally,
(Stolf et al., 1994). When ingestion occurs near the end of gestation often dying in a few hours or days (Garcia y Santos et al., 2004;
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 F. Riet-Correa et al.

Raffi et al., 2004; Riet-Correa et al., 2009a). The neonates that are able daily ingestion of 10 and 20 g kg 1 b.w., aborting 42–73 and
to stand may be lethargic and weak. Although a portion of these 17–24 days after the start of ingestion, respectively (Melo et al.,
animals do recover, most die soon after birth (Stolf et al., 1994; 2001). In pregnant sheep given daily doses of 1.5 and 3 g kg 1
Riet-Correa et al., 2009a). b.w. of the dried plant from the 90th day of gestation, abortion
Gross lesions observed in aborted fetuses or animals dying was observed on days 110–134 of gestation. Sheep fed 1 and
soon after birth include subcutaneous edema of the limbs, 1.5 g kg 1 b.w. of the dry plant daily from day 120 of gestation
yellow liquid in the thoracic and abdominal cavities, and occa- delivered lambs with clinical signs of the disease (Riet-Correa
sionally anasarca. The liver is congested, with areas exhibiting et al., 2009a). Tetrapterys sp. was found to cause abortion in cattle
an increased lobular pattern. In the heart, the ventricular walls following daily administration of sprouts and young leaves in doses
may appear thick and firm with myocardial pallor; this is mainly of 2.5, 5 and 10 g kg 1 b.w. for 23–76 days (Peixoto et al., 2011).
observed in the walls of the right ventricle and septum (Raffi A history of plant ingestion and observations of macroscopic
et al., 2004; Garcia y Santos et al., 2004; Riet-Correa et al., 2009a; lesions of the heart and histologic lesions of the heart and brain
Tokarnia et al., 1989). Histologically, the myocardial myofibers in fetuses and neonates are indicative of intoxication by one of
are swollen with pale cytoplasm, particularly around the nuclei. these toxic plants. Currently, a treatment is not available for
The cytoplasm is vacuolated and disorganized and the the poisoning. The only way to prevent intoxication is to keep
myofibers are separated by fibroblasts and collagen. The nuclei pregnant ruminants and horses from consuming these toxic
are enlarged and have an irregular outline, either rounded or plants.
rectangular. Multifocal areas of fibrosis that are associated
with mononuclear infiltration and myofibers necrosis are also
Enterolobium spp. and Stryphnodendron spp.
observed. In the central nervous system, mild to severe status
spongiosus is observed in the deep layers of the cortical gray In Brazil, there is a group of leguminous trees belonging to the
matter, subcortical white matter, and white matter of the cere- family Fabaceae and the subfamily Mimosoideae. This group
bellum, cerebellar peduncles and cervical spinal cord (Tokarnia includes Enterolobium contortisiliquum (= Enterolobium timbouva;
et al., 1989; Garcia e Santos et al., 2004; Raffi et al., 2004; Riet- Fig. 4; Tokarnia et al., 1960, 1999; Grecco et al., 2002; Mendoça
Correa et al., 2009a). Vacuolization can be also observed in et al., 2009), Enterolobium gummiferum (Deutsch et al., 1965),
the basal nuclei, thalamus and rostral colliculi (Riet-Correa Stryphnodendron coriaceum (Fig. 5; Dobereiner and Canela,
et al., 2009a). Areas of malacia have been observed in the thal- 1956; Tokarnia et al., 1991), Stryphnodendron obovatum (Tokarnia
amus and temporal cortex of sheep fetuses. Swollen and vesic- et al., 1998) and Stryphnodendron fissuratum (Ferreira et al., 2009).
ular nuclei are observed in some astrocytes (Riet-Correa et al., These trees produce pods that, when consumed, have been asso-
2009a). Diffuse vacuolation of hepatocytes can be observed ciated with digestive signs, photosensitivity and abortion in
in the liver following intoxication (Riet-Correa et al., 2009a). cattle. E. contortisiliquum has also been associated with diarrhea
Electron microscopy of the myocardium reveals that cardiac and abortion in goats (Benício et al., 2005) and with photosensi-
fibers exhibit different degrees of degeneration, with abundant tivity in sheep (Bezerra, 2011). Despite numerous poisoning out-
glycogen deposits in monoparticulate form. In some fibers, the breaks by these plants that are associated with abortion, abortive
mitochondria are severely swollen, demonstrating disorganiza- properties have only been confirmed for S. obovatum in cattle
tion of the cristae, and the sarcomeres are partially disorganized (Tokarnia et al., 1998), S. fissuratum in goats (Albuquerque et al.,
at the periphery. Cisterns of the smooth endoplasmic reticulum 2011) and Enterolobium contortisiliquum in guinea pigs (Bonel-
are often dilated. Throughout the ultrastructure of the nervous Raposo et al., 2008). As experimentally induced abortions occur
system, vacuoles observed from the histologic analysis corre- in surviving animals displaying other signs of toxicosis, previous
spond to intramyelinic edema. These vacuoles are formed by work has suggested that, when poisoning occurs within the
the splitting of myelin sheaths at the intraperiod lines (Garcia y natural environment, the plant toxin affects both the mother
Santos et al., 2004; Riet-Correa et al., 2009a). Histologic lesions and the fetus. These abortions seem to occur as a result of fetal
are not observed in the placenta (Riet-Correa et al., 2009a; Peixoto death, while the mother survives (Bonel-Raposo et al., 2008;
et al., 2011). Albuquerque et al., 2011). In the case of abortion induced by
The gross and histologic lesions observed in fetuses and S. fissuratum, retained placenta and endometrial bacterial infec-
newborns are similar to those observed in adults poisoned by tion have been observed to potentially aggravate the toxicosis
Tetrapterys spp. and A. glazioveana. Abortions seem to be caused (Albuquerque et al., 2011).
by cardiac and nervous lesions inflicted by the unknown toxin Triterpenoid saponins were isolated from S. fissuratum (Haraguchi
passing through the placental barrier (Garcia y Santos et al., et al., 2006; Yokosuka et al., 2008) and E. gummiferum (Carvalho,
2004; Raffi et al., 2004; Riet-Correa et al., 2009a; Peixoto et al., 2011). 1981) pods. The saponins isolated from E. gummiferum (Carvalho,
The toxin(s) in Tetrapterys spp. and A. glazioveana remain(s) 1981) were considered pathogenic for guinea pigs (Bonel-Raposo
unknown. Leaves of A. glazioveana were negative for the pres- et al., 2008). Of the different types of triterpene bisdesmosides,
ence of isocupressic acid (Riet-Correa et al., 2009b). Previous saponins identified from E. contortisiliquum, enterolosaponin A and
research has demonstrated that the toxic compound in A. contortisilioside B were toxic to macrophages, and contortisilioside
glazioveana is stable at 100  C. Additionally, rats, mice, rabbits A and C were toxic to both macrophages and murine lymphoma
and guinea pigs are not susceptible to the cardiotoxic and cells (Mimaki et al., 2003, 2004). Currently, triterpenoid saponins
neurotoxic effects of the plant when administered orally (Leite isolated from S. fissuratum pods have not been assessed for their
et al., 2002). Single or multiple doses of 22–35 g kg 1 b.w. of toxic potential. The pods of S. obovatum caused abortion in cows
the green plant as well as single doses of 9–28 g kg 1 dry plant following 20–30 days of ingesting daily doses of 5 g kg 1 b.w.
have been reported to cause abortion or delivering of weak (Tokarnia et al., 1998). Abortions were observed in goats consuming
calves (Stolf et al., 1994; Garcia y Santos et al., 2004). The green pods of S. fissuratum after ingesting daily doses of 3.25 g kg 1 b.w.
leaves of T. multiglandulosa caused abortion in goats following for 2 days (Albuquerque et al., 2011). Guinea pigs fed a ration
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Toxic plants affecting reproduction in ruminants

Figure 4. Enterolobium contortisiliquum: (A) branches and pods during the dry season, after the leaves fall; (B) leaves and pods; (C) the tree after
the leaves fall.

Figure 5. Stryphnodendron coriaceum: (A) leaves; (B) pods; (C) the tree during the rainy season, before seeding.
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 F. Riet-Correa et al.

containing 4% of E. contortisiliquum pods aborted 6–15 days common plant in certain regions of Brazil where malformations
following the start of ingestion (Bonel-Raposo et al., 2008). in goats and sheep occur frequently, and M. tenuiflora is less com-
Definitive diagnosis of poisoning is evaluated by observing mon or not present at all relative to M. ophthalmocentra. The
the presence of the plant, the ingestion of pods, and the occur- administration of M. ophthalmocentra seeds to rats resulted in
rence of abortion associated with other clinical signs, including embryonic death, poor fetal development and malformations
digestive signs, and photosensitization. Currently, treatment is similar to those observed in rats that ingested M. tenuiflora seeds,
not available for poisoning by these plants. To prevent ingestion, suggesting that M. ophthalmocentra poisoning is also a source of
ruminants should not be placed in pastures during the season the malformations observed in ruminants in the semiarid region
when the pods are falling. of Brazil (Pessoa et al., 2011).
Both sheep and goats are frequently affected by M. tenuiflora-
induced malformations, whereas these malformations affect cat-
Nitrate Poisoning tle less often. The number of affected newborns presenting with
Nitrate poisoning occurs primarily in cattle and at a lower malformations is quite variable. In some herds, the malforma-
frequency in sheep and goats. There are a number of plant species tions are sporadic, affecting 1–10% of the animals, whereas
that accumulate toxic levels of nitrates. Nitrate accumulation varies other herds may have a higher incidence that can affect up to
widely among forage species, but these levels are often related to 100% of newborns (Medeiros et al., 2005; Nóbrega et al., 2005;
factors such as drought, specifically when plant growth is limited Riet-Correa et al., 2004, 2006; Dantas et al., 2010). Higher inci-
while the uptake of nitrate is not reduced. High levels of nitrates dence rates have been observed in sheep and goats fed diets
may be present at the end of a dry season, particularly in the flush supplemented with grain or byproducts at the end of the dry
of new growth following the first rains. Nitrate concentrations may season in areas invaded by M. tenuiflora. Although precipitation
also be elevated in soils that are heavily fertilized with nitrogen- may be insufficient to induce growth in other forage plants, the
based fertilizer or organic matter of animal origin. Nitrate poison- plant may resprout following a rain event. If this situation occurs,
ing has been reported in several different Brazilian regions. In the animals supplemented with concentrated food may come into
state of Paraíba, cattle were poisoned by Echinochloa polystachya heat after ingesting M. tenuiflora as the only available source of
and Pennisetum purpureum at the end of the dry season, immedi- green forage during the beginning of gestation (Riet-Correa
ately after the first rains (Medeiros et al., 2003). Cattle intoxication et al., 2009b; Dantas et al., 2010).
was also observed in the state of Ceará, when Pennisetum Lambs, kids and calves can be born with diverse bone malfor-
purpureum was cultivated in the exposed bottoms of large, dry mations: permanent flexure of the forelimbs (arthrogryposis;
ponds after a prolonged drought. It is likely that the bottoms of Fig. 7A and B), which may also be shortened or twisted; malfor-
these ponds contained large amounts of nitrogen-rich organic mations of the bones of the head and face, including micro-
matter after being covered by water for many years. Based on gnathia, primary cleft lip that occurs with hypoplasia, or
clinical signs, a presumptive diagnosis of nitrate poisoning was unilateral or bilateral aplasia of the incisive bone (Fig. 7 C), and
made in a pasture severely invaded by Amaranthus spp. in Rio secondary cleft palate (palatoschisis); and malformations of the
Grande do Sul (Medeiros et al., 2003; Riet-Correa et al., 2009b). In spine (e.g., kyphosis, scoliosis, torticollis or hyperlordosis).
the state of Santa Catarina, abortions have been associated with Animals are sometimes born blind, with varying degrees of
nitrate poisoning in cattle grazing on oats (Avena sativa) and/or opacity of the cornea and/or microphthalmia (Fig. 7D), while
ryegrass (Lolium multiflorum; Jönck et al., 2011). Abortions occur others present with ocular dermoids. Additional malformations
because nitrate is able to cross the placenta, causing fetal methe- that are observed include acephaly, bicephaly, hydranencephaly,
moglobinemia followed by fetal anoxia and death. Methemo- hypoplasia of the tongue, meningocele and syringocele. Some
globinemia also impairs oxygen transport across the placenta, animals display variations of these malformations. The majority
contributing to fetal hypoxia and death (Knight and Walter, 2001). of animals with malformations of the head and spine die, but
many that only exhibit flexion of the forelimbs are able to
survive with this defect (Medeiros et al., 2005; Nóbrega et al.,
MALFORMATION-INDUCING PLANTS 2005; Riet-Correa et al., 2004, 2006; Dantas et al., 2010).
The primary toxin in M. tenuiflora remains unknown, but
Mimosa tenuiflora
alkaloids that are derived from tryptamine have been isolated
Mimosa tenuiflora (Fig. 6) and, most likely, M. ophthalmocentra from the leaves and seeds of this plant (Gardner et al., 2011).
(Fabaceae-mimosoideae) cause malformations and embryonic The occurrence of animal malformations in areas of M. tenuiflora
death in sheep, goats and cattle. With goat and sheep populations or M. ophthalmocentra growth is suggestive of poisoning. Similar
of 10 160 737 and 6 717 980 animals, respectively, the annual congenital defects can be produced by other factors, but the
losses owing to malformations are estimated at 273 120 kids and high frequency of defects observed in the semiarid rangelands
259 582 lambs in northeastern Brazil (Riet-Correa et al., 2007). of northeastern Brazil along with the experimental data on
The critical period of insult during gestation is currently unknown, reproduction following M. tenuiflora administration suggest that
but the suspected time of maximum susceptibility is during the a large majority of the malformations are caused by this plant.
first 60 days. Various malformations were observed in goats that Pregnant sheep and goats should not be allowed to graze in
only ate M. tenuiflora as green forage during all stages of gestation areas inhabited by M. tenuiflora, particularly during the first
(Pimentel et al., 2007) and in rats that received a diet containing 60 days of gestation. In the majority of farms located in north-
10% M. tenuiflora seeds between days 7 and 21 of gestation eastern Brazil, bucks and rams remain with the ewes and
(Medeiros et al., 2008). A high frequency of embryonic deaths nannies throughout the entire year. Based on this information,
has been induced in goats following the administration of adoption of a breeding season that allows for the avoidance of
M.tenuiflora as the only source of green forage during the first exposure to M. tenuiflora during early gestation would reduce
60 days of pregnancy (Dantas, 2010). M. ophthalmocentra is a the frequency of these malformations.
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Figure 6. Mimosa tenuiflora: (A) growing green plant; (B) pods and seeds; (C) flowering trees; (D) flowers.

Figure 7. Different malformations in ruminants caused by Mimosa tenuiflora: (A) calf and (B) goat with permanent flexure of the forelimbs; (C) goat
with cleft palate owing to aplasia of the right incisive bone; (D) sheep with severe microphthalmia.

OTHER PLANTS AFFECTING REPRODUCTION and cattle in southern Brazil (Colodel et al., 2002b; Driemeier
et al., 2000; Seitz et al., 2005); Ipomoea carnea subsp. fistulosa
Swainsonine-containing Plants (Fig. 8B), affecting goats in northeastern Brazil (Armien et al.,
Swainsonine-containing plants found in Brazil include Sida 2007; Riet-Correa et al., 2009b) and Marajo Island (Oliveira et al.,
carpinifolia (Fig. 8A), which affects goats, horses, deer, sheep 2009) and cattle in central-western Brazil (Antoniassi et al., 2007);
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 F. Riet-Correa et al.

Figure 8. Flowers and leaves of several Brazilian plants containing swainsonine: (A) Sida carpinifolia; (B) Ipomoea carnea; (C) Ipomoea sericophylla; (D)
Turbina cordata.

Ipomoea riedelii and I. sericophylla (Fig. 8 C), which affect goats in treated animals are generally not able to stand and suckle
the semiarid region of northeastern Brazil (Barbosa et al., 2006); normally (Gotardo et al., 2011).
and Turbina cordata (Fig. 8D), affecting goats, cattle and horses The concentration of swainsonine in Brazilian plants is variable.
in the semiarid region of Brazil (Dantas et al., 2007). Reproductive Samples of I. riedelii and I. sericophylla collected in 2002 contained
changes characterized by infertility, abortions, stillbirths and birth 0.14 and 0.11% swainsonine, respectively, whereas in 2003,
of weak offspring may occur following the consumption of S. car- the concentrations were 0.01 and 0.05% for I. riedelii and
pinifolia (Colodel et al., 2002b; Driemeier et al., 2000; Seitz et al., I. sericophylla, respectively (Barbosa et al., 2006). S. carpinifolia
2005), I. carnea subsp. fistulosa (Schwarz et al., 2003; Hueza et al., and I. carnea contained 0.006% (Colodel et al., 2002a) and
2007) and, most likely, I. riedelii, I. sericophylla and T. cordata 0.0029% swainsonine (Haraguchi et al., 2003), respectively. The
(Riet-Correa et al., 2009b). Abortions have been experimentally in- swainsonine concentration in T. cordata is highly variable,
duced in goats (Gotardo et al., 2011) and sheep (Armién et al., ranging from less than 0.001 to 0.14% (Dantas et al., 2007).
2011) ingesting large amounts of I. carnea subsp. fistulosa. Rats Currently, there is no information regarding the dose of
fed I. carnea subsp. fistulosa demonstrated high rates of em- swainsonine required to induce reproductive problems across
bryonic death and perinatal mortality. The pups were smaller the different species. There may not be a safe dose of
(decreased body weight), weak and displayed hyperflexion of swainsonine for pregnant livestock if the duration of exposure
the carpal joints of the forelimbs (Schwarz et al., 2003). Hueza is sufficient to cause enzymatic inhibition and lesion formation
et al. (2007) demonstrated that swainsonine passes through the (Gotardo et al., 2011).
placental barrier, affecting fetal development, and that milk
excretion participates in the perinatal toxicosis induced by I.
carnea. Experimentally, kids born to does that ingested I. carnea
Estrogenic Plants
during pregnancy displayed arthrogryposis and retrognathia, sug-
gesting that swainsonine may induce malformations (Shumaher- Estrogenism was previously reported during the 1970s in Rio
Henrique, 2005). Similar malformations and abortions have been Grande do Sul in a pasture composed of 95% T. subterraneum
reported in sheep and cattle poisoned by locoweed (James et al., var. Yarloop and 5% Lolium multiflorum (Pimentel et al., 1977).
1967). Goats chronically poisoned by I. carnea subsp. fistulosa that The disease affected mainly heifers and caused cystic ovaries,
are not ingesting the plant any more, but display mild intention hyperemia of the vaginal mucosa, edematous and thickened
tremors, exhibit infertility and birth of weak offspring that die uterine horns, enlarged and edematous udders, dilation of the
shortly following birth. This observed reproductive failure is prob- cervical canal, and excess mucus secretions in the vagina. Low
ably related to nutritional deficiency associated with difficulties conception rates, alterations in the estrous cycle, and anestrous
in grazing owing to the intention tremors (Oliveira et al., 2011). were also observed (Pimentel et al., 1977). T. subterraneum has
Chronically affected goats also demonstrate a high susceptibility now been fully replaced with other Trifolium species, including
to infections by gastrointestinal nematodes (Oliveira et al., 2011). T. repens and T. pretense, and estrogenism is no longer being
Additionally, the offspring of pregnant goats administered I. reported in these pastures. Estrogenism has never been reported
carnea subsp. fistulosa during gestation have significant behav- in sheep in southern Brazil. This is most likely because sheep
ioral alterations and life-threatening developmental delays, as throughout this region are mainly raised on native pastures.
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wileyonlinelibrary.com/journal/jat Copyright © 2011 John Wiley & Sons, Ltd. J. Appl. Toxicol. 2012; 32: 245–254
Toxic plants affecting reproduction in ruminants

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