Dynamics of Pneumonia in a Bighorn Sheep Metapopulation

Abstract: We investigated the dynamics of 8 populations of a bighorn sheep (Ovis canadensis) metapopulation in Hells Canyon, USA from 1997 to 2003. Pneumonia was the most common cause (43%) of adult mortality and the primary factor limiting population growth. Cougar (Puma concolor) predation was the second most-frequent source (27%) of adult mortality but did not reduce the rate of population growth significantly. Most pneumonia-caused mortality occurred in fall and early winter and most cougar predation occurred in late winter and early spring. Average annual survival of adult males (0.84) was lower than females (0.91). Pneumonia was the most common known cause of lamb mortality (86%), and pneumonia-related mortality was detected whenever summer lamb survival was <50%. Pneumonia-caused mortality rates in lambs were high from 21 days to 91 days of age and peaked at 42 days to 70 days. Summer pneumonia epizootics in lambs were independent of pneumonia-caused mortality in adults. Pneumonia-caused mortality occurred at the population level and was not synchronized geographically or temporally among populations. Although catastrophic all-age pneumonia-epizootics have previously been described in bighorn sheep, we found that chronic, although sporadic, pneumonia-caused mortality in adults and lambs can also have important effects on the dynamics of bighorn sheep populations.     

Relationships among fecal lungworm loads, fecal glucocorticoid metabolites, and lamb recruitment in free-ranging Rocky Mountain bighorn sheep

Most wild Rocky Mountain big-horn sheep (Ovis canadensis canadensis) in northern latitudes are infected with lungworms. Indirect effects of lungworms on bighorn sheep are unknown, but high pulmonary burdens might increase stress (i.e., elevated glucocorticoid levels), and chronic stress could in turn decrease fitness. We hypothesized that high lungworm burdens in Rocky Mountain bighorn ewes increase stress, thereby increasing lamb mortality. To test our hypothesis, one subherd of bighorn sheep in Custer State Park, South Dakota was provided a free-choice loose mineral mix containing the anthelmintic fenbendazole every six weeks from March 1999 to August 2000 to eliminate lungworms; another subherd served as the control. Daily, individually marked ewes were located telemetrically from the ground and uniquely marked animals were observed until they defecated. After the herd moved from the area, fecal samples were collected and stored at -23 C. A consistent number of samples per season per herd (x-=16.56+/-3.99 samples) were collected. Fecal larval lungworm levels (LPG) in the treatment subherd were lower than levels in the control subherd; however, there was no difference in fecal glucocorticoid metabolite (FGM) levels between the two subherds. Fecal glucocorticoid metabolite levels varied by season in both subherds, with levels in winter lower than during the other three seasons. Lamb:ewe ratios were not different between the control and treatment subherds at the end of summer 1999. In contrast, the treatment group had a lower lamb:ewe ratio at the end of summer 2000 despite having lower LPG. However, this result was attributed to lower ewe production, not lower lamb survival. The LPG levels were not correlated with FGM concentrations; instead, FGM levels might reflect normal seasonal patterns. Other factors, including contagious ecthyma, were more important for determining lamb mortality than LPG and FGM levels during our study. We suggest further experimental work over a longer duration to address these relationships.     

Mortality Transmitters – New Instrument for Animal Loss Research on Norwegian Ranges

In 1988, 315 lambs from 4 sheep (Ovis aries) herds comprised of 1003 animals were marked with silent mortality transmitters in Gammeldalen in Hedmark County, southern Norway. The aim was to identify causes of death and the so-called “hidden loss” of lambs on summer range. A total of 22 animals, 19 lambs and 3 ewes were found dead. Of these, 18 lambs were marked with radio transmitters. A total of 10 animals died of disease (45.5 %) and 12 were killed by predators (54.5 %). Of the 18 radio-located lambs, 6 died of disease (33.3 %) and 12 due to predators (66.7 %). Various common lamb diseases were diagnosed, e.g. lung, thoracic and intestinal infections. Eleven lambs were killed by lynx (Lynx lynx), a 12th was found chased to exhaustion, presumably by a predator. Use of mortality transmitters is concluded to be useful in investigating sheep losses on Norwegian ranges.     

Factors associated with lamb mortalities in Muzaffarnagari sheep

The Muzaffarnagari sheep, a mutton-producing breed of India, is generally known for its fast growth rate and high feed conversion efficiency. The study identified the causes of perinatal and postnatal deaths and factors contributing to the cause of mortalities in lambs. Data were recorded for 4628 lambs born to Muzaffarnagari ewes in single-sire matings from 165 rams, between 1978 and 2002. The least-squares means for overall lamb mortality from birth to 1 year of age in the flock was 12.6% (582/4628), while the overall pre- and post-weaning mortality rate averaged 6.6% and 6.0%, respectively. The mortality rate of the lambs declined as the lambs grew older. The major causes associated with lamb losses were pneumonia (31.4%), digestive disorders (14.6%), starvation (9.6%), endoparasitism (5.0%), septicaemia and toxaemia (10.1%), accidental (2.1%) and undetermined causes (27.2%), respectively. The main causes of early lamb mortality (within 15 days of birth) were pneumonia followed by starvation. The highest lamb mortalities occurred within the first 15 days of life. The year of birth of the lamb significantly affected (P < 0.01) the cumulative lamb mortality rate at all ages. The sire of the lamb also had a significant (P < 0.01) effect on lamb mortality rate at all ages. Lambs reared under an intensive feeding management system had a remarkably (P < 0.01) lower mortality rate than lambs maintained under a semi-intensive management system, at 3 months of age and later. The lamb losses were significantly (P < 0.01) higher in ram lambs than in females during the post-weaning stages. The linear regressions of lamb birth weight and dam weight at lambing were highly significant (P < 0.01) with lamb mortality rate during pre- and post-weaning stages. Logistic regression analyses revealed lambs maintained under a semi-intensive system, to be at a greater risk of dying from all ailments than lambs maintained under intensive feeding systems. Male lambs had greater risk of death from respiratory, digestive and other causes, compared to their female counterparts. The findings of this study revealed causes of pre-weaning lamb mortalities to be mainly due to a low birth weight and non-parasitic diseases (predominantly pneumonia). These factors must be considered in any lamb production system.     

A METHOD FOR CALCULATING THE EFFECT OF A DIE-OFF FROM STRANDING DATA

A method was developed for estimating the mortality during a die-off of marine mammal species from longitudinal stranding data. A deterministic mathematical model of the stranding process was used to calculate the mortality during a die-off. The model incorporated natural and anthropogenic mortality rates, the number of stranded carcasses before, during, and after the die-off, the duration of the die-off, and detection probability of a stranded carcass. The model was applied to data for the bottlenose dolphin ( Tursiops truncatus ) along the Atlantic coast of the United States. The mortality rate during the epizootic of 1987 and 1988 was calculated using the model. Sensitivity analyses indicated that precise estimates of natural and anthropogenic mortality rates were important for obtaining precise additional mortality rates during the die-off. For stranding data to be useful in this model, data should be collected in a consistent manner and effort within a defined area prior to, throughout, and after a die-off. Survey effort also should be measured.     

Early neonatal lamb mortality: postmortem findings

An investigation of stillbirth and early neonatal lamb mortality was conducted in sheep flocks in Norway. Knowledge of actual causes of death are important to aid the interpretation of results obtained during studies assessing the risk factors for lamb mortality, and when tailoring preventive measures at the flock, ewe and individual lamb level. This paper reports on the postmortem findings in 270 liveborn lambs that died during the first 5 days after birth. The lambs were from 17 flocks in six counties. A total of 27% died within 3 h after birth, 41% within 24 h and 80% within 2 days. Most lambs (62%) were from triplet or higher order litters. In 81% of twin and larger litters, only one lamb died. The most frequently identified cause of neonatal death was infectious disease (n=97, 36%); 48% (n=47) of these died from septicaemia, 25% (n=24) from pneumonia, 22% (n=21) from gastrointestinal infections and 5% (n=5) from other infections. Escherichia coli accounted for 65% of the septicaemic cases, and were the most common causal agent obtained from all cases of infection (41%). In total, 14% of neonatal deaths resulted from infection by this bacterium. Traumatic lesions were the primary cause of death in 20% (n=53) of the lambs. A total of 46% of these died within 3 h after birth and 66% within 24 h. Severe congenital malformations were found in 10% (n=27) of the lambs, whereas starvation with no concurrent lesions was the cause of death in 6% (n=17). In 16% (n=43) of the lambs, no specific cause of death was identified, lambs from triplet and higher order litters being overrepresented among these cases. In this study, the main causes of neonatal lamb mortality were infection and traumatic lesions. Most neonatal deaths occurred shortly after birth, suggesting that events related to lambing and the immediate post-lambing period are critical for lamb survival.     

Characterisation of neurons expressing calbindin immunoreactivity in the ileum of the unweaned and mature sheep

We have identified the enteric neuron types expressing immunoreactivity for the calcium-binding protein calbindin D28k (CALB) in cryostat sections and whole-mount preparations of myenteric (MP) and submucosal (SMP) plexuses of sheep ileum. We wished to determine whether CALB-IR in the sheep enteric nervous system was expressed in Dogiel type II cells, as in guinea-pig and rat ileum, and could therefore be used as a marker for intrinsic primary afferent neurons. The neurochemical coding of CALB-containing myenteric and submucosal neurons in ileum of unweaned lamb and mature sheep and its co-localisation with various neural markers was studied immunohistochemically. An antiserum against neuronal nuclear protein (NeuN) failed to detect the entire neuronal population; it was expressed only in 48% of neuron-specific enolase (NSE)-immunoreactive (NSE-IR) neurons. Human neuronal protein appeared to occur in the large majority or all neurons. Almost all CALB-IR neurons were: (1) radially multidendritic; (2) eccentric multidendritic; (3) Dogiel type II. CALB-IR occurred in 20–25% of myenteric and 65–75% of submucosal neurons in lamb and mature sheep, with higher values in mature sheep. Nearly all CALB-IR neurons were common choline acetyltransferase (cChAT)-IR, whereas only about 20% of cChAT-IR somata were CALB-IR. In lamb and mature sheep, 90% of MP CALB-IR neurons were peripheral choline acetyltransferase (pChAT)-IR. In lamb SMP, 80±13% of CALB-IR cells were also pChAT-IR, whereas all those in mature SMP were pChAT-IR. Fewer myenteric CALB-IR neurons exhibited tachykinin (TK) in mature sheep (49%) than in lamb (88%). This was also the case for submucosal ganglia (mature sheep, 63%; lamb, 89%). In lamb MP, 77±7% of CALB-IR cells were NeuN-positive. In mature sheep, 73±10% of CALB-IR somata were NeuN-IR, but NeuN failed to stain SMP neurons. In the MP of suckling and mature sheep, Dogiel type II CALB-IR neurons were calcitonin gene-related peptide (CGRP)-IR. In the SMP at both stages, Dogiel type II CALB-IR somata (about 50% of CALB-IR neurons) were also CGRP-IR. Only small proportions of CALB-IR neurons showed immunoreactivity for calretinin or nitric oxide synthase (NOS), although large populations of CALB and NOS neurons occurred in the ganglia. Thus, CALB is a marker of most Dogiel type II neurons in the sheep but is not confined to Dogiel II neurons. CGRP is a more selective marker of Dogiel type II neurons, being only found in this neuron type.This work was supported by a grant from the Ministero dellIstruzione, dellUniversità e della Ricerca (MIUR)     

Distribution of mucus glycoprotein in four compartments of lamb and sheep stomach

The regional distribution of mucus glycoprotein in lamb before weaning and sheep was studied. Mucus glycoprotein was present in the forestomach region of lamb and glandular stomach (abomasum) of lamb and sheep. Ester sulfates were found in all mucus glycoproteins obtained.     

Implications of Conflicting Associations of the Prion Protein (PrP) Gene with Scrapie Susceptibility and Fitness on the Persistence of Scrapie

Background

Existing mathematical models for scrapie dynamics in sheep populations assume that the PrP gene is only associated with scrapie susceptibility and with no other fitness related traits. This assumption contrasts recent findings of PrP gene associations with post-natal lamb survival in scrapie free Scottish Blackface populations. Lambs with scrapie resistant genotypes were found to have significantly lower survival rates than those with susceptible genotypes. The present study aimed to investigate how these conflicting PrP gene associations may affect the dynamic patterns of PrP haplotype frequencies and disease prevalence.

Methodology/Principal Findings

A deterministic mathematical model was developed to explore how the associations between PrP genotype and both scrapie susceptibility and postnatal lamb mortality affect the prevalence of scrapie and the associated change in PrP gene frequencies in a closed flock of sheep. The model incorporates empirical evidence on epidemiological and biological characteristics of scrapie and on mortality rates induced by causes other than scrapie. The model results indicate that unfavorable associations of the scrapie resistant PrP haplotypes with post-natal lamb mortality, if sufficiently strong, can increase scrapie prevalence during an epidemic, and result in scrapie persisting in the population. The range of model parameters, for which such effects were observed, is realistic but relatively narrow.

Conclusions/Significance

The results of the present model suggest that for most parameter combinations an unfavourable association between PrP genotype and post-natal lamb mortality does not greatly alter the dynamics of scrapie and, hence, would not have an adverse impact on a breeding programme. There were, however, a range of scenarios, narrow, but realistic, in which such an unfavourable association resulted in an increased prevalence and in the persistence of infection. Consequently, associations between PrP genotypes and fitness traits should be taken into account when designing future models and breeding programmes.     

Fatal congenital Neospora caninum infection in a lamb

Neospora caninum tissue cysts were found in the brain and spinal cord of a 1-wk-old lamb that was unable to stand after birth. The lamb was originally diagnosed as having toxoplasmosis, but ultrastructural and immunohistochemical techniques used in the present study permitted a definitive diagnosis of Neospora caninum tissue cysts in the brain and spinal cord of this lamb. This is the first report of N. caninum in sheep.     

Behavioural reactions of desert bighorn sheep to avian scavengers

I report previously undocumented encounters between avian scavengers and desert bighorn sheep ( Ovis canadensis nelsoni ). These encounters are of interest because they occurred only during the nursery season when lamb mortality was high. Desert bighorn sheep responded to the presence of avian scavengers with typical anti-predator behaviours, which may indicate that avian scavengers are potential predators or that desert bighorn sheep are unable to distinguish between avian scavengers and avian predators.     

Ovulation level and prolificacy in ewes depending on their age, birth type and percentage of prolific genotype

During December mating periods of 2000-2003, wool and meat breeds crossed with East Friesian milk sheep and rams of prolific breeds (Finn or Romanov) were examined laparoscopically. Ovine ovaries were examined between 4 and 9 days after mating. The litter size was recorded and compared with the number of ovulations. The fertility of the analyzed animals was 69.6%, with 192.6% prolificacy. The difference between the average number of corpora lutea found on ovaries and the mean number of lambs born was 0.35 and ranged from 0.32 to 0.41 according to age group, from 0.22 to 0.41 according to sheep birth type, and from 0 to 0.52 lamb per ewe according to percentage of prolific breeds.     

Risk factors associated with lambing traits

The objective of this study was to establish the risk factors associated with both lambing difficulty and lamb mortality in the Irish sheep multibreed population. A total of 135 470 lambing events from 42 675 ewes in 839 Irish crossbred and purebred flocks were available. Risk factors associated with producer-scored ewe lambing difficulty score (scale of one (no difficulty) to four (severe difficulty)) were determined using linear mixed models. Risk factors associated with the logit of the probability of lamb mortality at birth (i.e. binary trait) were determined using generalised estimating equations. For each dependent variable, a series of simple regression models were developed as well as a multiple regression model. In the simple regression models, greater lambing difficulty was associated with quadruplet bearing, younger ewes, of terminal breed origin, lambing in February; for example, first parity ewes experienced greater (P<0.001) lambing difficulty (1.56±0.02) than older ewes. The association between lambing difficulty and all factors persisted in the multiple regression model, and the trend in fixed effects level solutions did not differ from the trend observed in the simple regression models. In the simple regression analyses, a greater odds of lamb mortality was associated with male lambs (1.31 times more likely of death than females), lambs of very light (2 to 3 kg) and very heavy (>7.0 kg) birth weights, quadruplet born lambs and lambs that experienced a more difficult lambing (predicted probability of death for lambs that required severe and veterinary assistance of 0.15 and 0.32, respectively); lambs from dual-purpose breeds and born to younger ewes were also at greater risk of mortality. In the multiple regression model, the association between ewe parity, age at first lambing, year of lambing and lamb mortality no longer persisted. The trend in solutions of the levels of each fixed effect that remained associated with lamb mortality in the multiple regression model, did not differ from the trends observed in the simple regression models although the differential in relative risk between the different lambing difficulty scores was greater in the multiple regression model. Results from this study show that many common flock- and animal-level factors are associated with both lambing difficulty and lamb mortality and management of different risk category groups (e.g. scanned litter sizes, ewe age groups) can be used to appropriately manage the flock at lambing to reduce their incidence.     

Pregnancy rate after the transfer of sheep embryos originated from randomly chosen oocytes matured and fertilized in vitro

Randomly chosen sheep oocytes isolated from 2- to 5-mm follicles of hormonally nonstimulated slaughtered females were matured and fertilized in vitro. Using heparin for the induction of ram sperm capacitation, a fertilization rate close to 80% was recorded. After the transfer of 29 embryos cultured to the 2- to 4-cell stage to 4 recipients, each delivered 1 lamb. In another experiment, 34 2-cell embryos stage were transferred (1 to each oviduct) to 17 synchronized recipients; 8 pregnancies were established and each of 5 recipients delivered a single lamb. The remaining 3 recipients aborted at the third month of gestation. These results show that sheep embryos can be produced in vitro from randomly chosen oocytes and by using relatively simple procedures. However, the viability of the embryos was low, with approximately only 15% developing to term after transfer at the 2-cell stage.     

Toxoplasmosis in Sheep

The presence of Toxoplasma gondii in the diaphragm was correlated with the dye test titres in 174 sheep. In 94 of these the presence of the parasite was also correlated with the haemoglobin (Hb) type. T. gondii was recovered from 3 % of the sheep with titres < 1/16, compared with 30 % of those with titres 1/16 and 70 % of those with titres ≥ 1/32. The results indicate that the distinction between serologically positive and negative individuals at a final serum dilution of 1/16 is justified. Some evidence was found that the parasite is easier to recover from dye test positive mature sheep than from dye test positive lambs. Of the 174 sheep, 143 were examined at random among 186 sheep culled or cast for age during a 4-year period from 1 flock in which the prevalence of Toxoplasma antibodies was representative for flocks in the southern Norway, and T. gondii was recovered from 53 (37 %) of these. It was concluded that 10—15 % of the lamb carcases and 25—37 % of the carcases from mature sheep in this country have T. gondii in their muscles detectable by the peptic digestion technique. A possible genetical influence on the infection was indicated by the higher frequency of recoveries of T. gondii from sheep with Hb type B than from sheep with the Hb types A or AB, but the number of individuals with Hb type B was too small to demonstrate statistically significant differences. The epidemiological importance of infected sheep carcases is discussed.     

Q fever: hazard from sheep used in research.

The recent recognition that Q fever is endemic in Ontario and the known occupational risk of Q fever to research personnel working with sheep prompted a study to determine the prevalence of antibodies to the causative organism, Coxiella burnetti, in animals and staff at a Toronto animal research institute. Of 37 sheep 34 (92%) were found to be seropositive--that is, to have a titre of complement-fixing antibody to the phase II antigen of 1:8 or greater. Of 331 staff members tested, 18% were found to be seropositive, compared with 0.6% of a random sample of Toronto blood donors. The highest rate of seropositivity, 68%, was in the 28 animal attendants tested. Seropositivity was associated with working with sheep or fetal lamb tissue (p less than 0.0001) and with visiting the animal facility (p less than 0.001). Of the 59 seropositive staff members 63% had had no direct contact with sheep. There were 12 clinically apparent cases of Q fever, 2 of which required admission to hospital. Q fever remains a serious occupational hazard to staff working in research laboratories using sheep, even to those with indirect exposure to infected animals.     

Evidence that primary infection of Charollais sheep with Toxoplasma gondii may not prevent foetal infection and abortion in subsequent lambings

A study carried out on a sheep farm examined whether Toxoplasma gondii foetal infection and associated abortion occur in successive lambings. We identified 29 ewes that gave birth to lambs on at least 2 successive years over our study period, 2000-2003. Tissue samples from the progeny of these ewes were analysed by PCR to determine infection status with T. gondii. T. gondii-infected lambs were born in 31% of successive pregnancies. T. gondii-positive lambs were aborted in successive pregnancies in 21% of lambings during study period, 2000-2003. The frequency of successive abortions within this flock over the period 1992-2003 was 18%. If a lamb was congenitally infected there was a high risk (69%) that the successive lamb from that ewe would also be congenitally infected. Similarly, if a lamb was aborted there was a high risk (55%) of abortion in the next lamb produced. These data suggest that life-long immunity to T. gondii infections may not always be acquired following an initial infection and raises the question as to whether the mechanisms of T. gondii transmission prior to and during ovine pregnancies are fully understood.     

Influence of climatic factors on the development of pneumonia in lambs

Pneumonia is responsible for important economical losses in the sheep industry in Spain and many other sheep-rearing countries, being the main cause of lamb death, and of losses due to condemnations in abattoirs and of drug costs. This respiratory syndrome is a complex disease involving the relationship between host and environment. The present study analyses the influence of environmental factors on the development of pneumonia in lambs. Statistically significant correlations were found between pneumonia as a cause of lamb death and climatic factors such as rainfall, humidity and intensity and direction of wind. The type of farm building was also an important factor to take into account in order to improve the prevention of pneumonia in lambs. Moreover, the age of the lambs was seen to be a significant item in the study of pneumonia. Respiratory pathology increased from 23 days of age. This fact permits the implementation of measures from birth to 23 days with a view to reducing pneumonia and its negative influence on lamb production. The paper discusses the practical implications of these findings for sheep production.     

Influence of climatic factors on the development of pneumonia in lambs

Pneumonia is responsible for important economical losses in the sheep industry in Spain and many other sheep-rearing countries, being the main cause of lamb death, and of losses due to condemnations in abattoirs and of drug costs. This respiratory syndrome is a complex disease involving the relationship between host and environment. The present study analyses the influence of environmental factors on the development of pneumonia in lambs. Statistically significant correlations were found between pneumonia as a cause of lamb death and climatic factors such as rainfall, humidity and intensity and direction of wind. The type of farm building was also an important factor to take into account in order to improve the prevention of pneumonia in lambs. Moreover, the age of the lambs was seen to be a significant item in the study of pneumonia. Respiratory pathology increased from 23 days of age. This fact permits the implementation of measures from birth to 23 days with a view to reducing pneumonia and its negative influence on lamb production. The paper discusses the practical implications of these findings for sheep production.     

Genomic association with pathogen carriage in bighorn sheep (Ovis canadensis)

Genetic composition can influence host susceptibility to, and transmission of, pathogens, with potential population‐level consequences. In bighorn sheep (Ovis canadensis), pneumonia epidemics caused by Mycoplasma ovipneumoniae have been associated with severe population declines and limited recovery across North America. Adult survivors either clear the infection or act as carriers that continually shed M. ovipneumoniae and expose their susceptible offspring, resulting in high rates of lamb mortality for years following the outbreak event. Here, we investigated the influence of genomic composition on persistent carriage of M. ovipneumoniae in a well‐studied bighorn sheep herd in the Wallowa Mountains of Oregon, USA. Using 10,605 SNPs generated using RADseq technology for 25 female bighorn sheep, we assessed genomic diversity metrics and employed family‐based genome‐wide association methodologies to understand variant association and genetic architecture underlying chronic carriage. We observed no differences among genome‐wide diversity metrics (heterozygosity and allelic richness) between groups. However, we identified two variant loci of interest and seven associated candidate genes, which may influence carriage status. Further, we found that the SNP panel explained ~55% of the phenotypic variance (SNP‐based heritability) for M. ovipneumoniae carriage, though there was considerable uncertainty in these estimates. While small sample sizes limit conclusions drawn here, our study represents one of the first to assess the genomic factors influencing chronic carriage of a pathogen in a wild population and lays a foundation for understanding genomic influence on pathogen persistence in bighorn sheep and other wildlife populations. Future research should incorporate additional individuals as well as distinct herds to further explore the genomic basis of chronic carriage.