Impact of BVDV infection of white-tailed deer during second and third trimesters of pregnancy

While it has been demonstrated that persistent bovine viral diarrhea virus (BVDV) infections can be established in white-tailed deer (Odocoileus virginianus) following in utero exposure in the first trimester of gestation, there is little to no information regarding the outcome of infection in later stages of pregnancy in deer. Our goal was to observe the impact of infection of white-tailed deer in the second and third trimesters of pregnancy. Five white-tailed deer in the second trimester of pregnancy and four in the third trimester were infected with a BVDV type 2 virus previously isolated from a BVDV-infected deer harvested from the wild. Infection of deer in the second trimester of pregnancy resulted in loss of the pregnancy in three of five deer. Fawns born to the two remaining deer appeared normal and were born BVDV antigen-negative with neutralizing serum antibodies against BVDV. Infection of does in the third trimester of pregnancy did not result in fetal death or persistent infection and all does gave birth to live, healthy fawns that were BVDV antigen-negative and born with antibodies against BVDV. These results, combined with those previously reported regarding BVDV infection in the first trimester of pregnancy, suggest that the impact of BVDV infection of pregnant white-tailed deer is very similar to that observed in pregnant cattle.     

Prevalence of infectious agents in free-ranging white-tailed deer in northeastern Mexico

The objectives of this study were to determine the prevalence of antibodies against brucellosis, leptospirosis, infectious bovine rhinotracheitis virus, and bovine viral diarrhea virus (BVDV) in white-tailed deer (Odocoileus virginianus) in northeastern Mexico. Deer (n=521) were captured from helicopter using a netgun on 15 ranches covering 62,114 ha in the states of Coahuila, Nuevo Leon, and Tamaulipas during spring 2004. The prevalence of antibodies against Leptospira, infectious bovine rhinotracheitis, BVDV, and brucellosis were 5.6, 41.1, 63.5, and 0%, respectively, indicating that white-tailed deer and cattle may share disease agents when cohabiting in northeastern Mexico.     

Febrile response and decrease in circulating lymphocytes following acute infection of white-tailed deer fawns with either a BVDV1 or a BVDV2 strain

Although commonly associated with infection in cattle, bovine viral diarrhea viruses (BVDV) also replicate in many domestic and wildlife species, including cervids. Bovine viral diarrhea viruses have been isolated from a number of cervids, including mule deer (Odocoileus hemionus), European roe deer (Capreolus capreolus), red deer (Cervus elaphus), white-tailed deer (Odocoileus virginianus), and mouse deer (Tragulus javanicus), but little information is available regarding clinical presentation and progression of infection in these species. In preliminary studies of experimental infection of deer with BVDV, researchers noted seroconversion but no clinical signs. In this study, we infected white-tailed deer fawns that were negative for BVDV and for antibodies against BVDV, with either a type 1 or a type 2 BVDV that had been isolated from white-tailed deer. Fawns were monitored for changes in basal temperature, circulating lymphocytes, and platelets. The clinical progression following inoculation in these fawns was similar to that seen with BVDV infections in cattle and included fever and depletion of circulating lymphocytes. Because free-ranging cervid populations are frequently in contact with domestic cattle in the United States, possible transfer of BVDV between cattle and cervids has significant implications for proposed BVDV control programs.     

Serological evidence of bovine herpesvirus 1-related virus infection in the white-tailed deer population on Anticosti Island, Quebec

High white-tailed deer (Odocoileus virginianus) population densities and the occurrence of harsh environmental conditions are present on Anticosti Island, located in the Gulf of Saint-Lawrence (Quebec, Canada). This island is the northernmost region of white-tailed deer distribution in northeastern North America. The aim of this work was to determine whether a herpesvirus serologically related to bovine herpesvirus 1 (BHV1) may occur in a stressed white-tailed deer population. One hundred one deer sera were collected from apparently healthy animals during the hunting season from September to late November 1985. Fifty-three percent of tested deer were positive to the seroneutralization test using Colorado strain of BHV1 virus. Higher percentages of seropositivity were observed in animals of both sexes greater than 4-yr-old. Analysis of antibody titers in seropositive animals according to age suggests that BHV1-related viral infection is endemic in the Anticosti Island deer population. It is postulated that environmental stress may induce immunosuppression of certain infected and/or carrier animals in their population that shed virus for long periods of time.     

Epidemiology of chronic wasting disease in captive white-tailed and mule deer

The natural occurrence of chronic wasting disease (CWD) in a 1993 cohort of captive white-tailed deer (Odocoileus virginianus) afforded the opportunity to describe epidemic dynamics in this species and to compare dynamics with those seen in contemporary cohorts of captive mule deer (O. hemionus) also infected with CWD. The overall incidence of clinical CWD in white-tailed deer was 82% (nine of 11) among individuals that survived >15 mo. Affected white-tailed deer died or were killed because of terminal CWD at age 49-76 mo (x = 59.6 mo, SE = 3.9 mo). Epidemic dynamics of CWD in captive white-tailed deer were similar to dynamics in mule deer cohorts. Incidence of clinical CWD was 57% (4/7) among hand-raised (HR) and 67% (4/6) among dam-raised (DR) mule deer; affected HR mule deer succumbed at 64-86 mo of age (x = 72 mo; SE = 5 mo), and affected DR mule deer died at age 31-58 mo (x = 41.3 mo; SE = 6.1 mo). Sustained horizontal transmission of CWD most plausibly explained epidemic dynamics, but the original source of exposures could not be determined. Apparent differences in mean age at CWD-caused death among these cohorts may be attributable to differences in the timing or intensity of exposure to CWD, and these factors appear to be more likely to influence epidemic dynamics than species differences. It follows that CWD epidemic dynamics in sympatric, free-ranging white-tailed and mule deer sharing habitats in western North American ranges also may be similar.     

Wasting and neurologic signs in a white-tailed deer (Odocoileus virginianus) not associated with abnormal prion protein

A captive adult male white-tailed deer (Odocoileus virginianus) with wasting and neurologic signs similar to chronic wasting disease (CWD) was evaluated by histopathology, histochemistry, and immunohistochemistry (IHC) for disease-associated prion protein (PrP(d)). On histologic examination, the brainstem had areas of vacuolation in neuropil and extensive multifocal mineralization of blood vessels with occasional occlusion of the lumen. Some of the clinical and pathologic features of this case were similar to the CWD of white-tailed deer. However, the tissues were negative for PrP(d) by IHC. Because the lesions were more prominent in the obex region of the brainstem, it is speculated that this would have resulted in clinical signs similar to CWD in white-tailed deer. To our knowledge, neither cerebrovascular mineralization nor clinicopathologic changes resembling CWD have previously been described in white-tailed deer without the presence of PrP(d). Such a case should be considered in a differential diagnosis of CWD of white-tailed deer.     

Prevalence of chronic wasting disease and bovine tuberculosis in free-ranging deer and elk in South Dakota

Heads of hunter-harvested deer and elk were collected throughout South Dakota (USA) and within established chronic wasting disease (CWD) surveillance areas from 1997-2002 to determine infection with CWD and bovine tuberculosis (TB). We used immunohistochemistry to detect CWD-infected individuals among 1,672 deer and elk sampled via geographically targeted surveillance. A total of 537 elk (Cervus elaphus nelsoni), 813 white-tailed deer (Odocoileus virginianus), and 322 mule deer (O. hemionus) was sampled for CWD. Estimated overall prevalence and associated confidence intervals (95%) in white-tailed deer was 0.001% (0-0.007%). Similarly, estimated overall prevalence in elk and mule deer was 0.0% (0-0.004%) and 0.0% (0-0.011%), respectively. A total of 401 elk, 1,638 white-tailed deer, and 207 mule deer was sampled for TB. Estimated overall prevalence of infection with TB in elk harvested in South Dakota was 0.0% (0-0.009%). Similarly, estimated overall prevalence of TB in white-tailed deer and mule deer harvested throughout South Dakota was 0.0% (0-0.002%) and 0.0% (0-0.018%), respectively.     

Experimental oral transmission of chronic wasting disease to reindeer (Rangifer tarandus tarandus)

Chronic wasting disease (CWD), a transmissible spongiform encephalopathy of cervids, remains prevalent in North American elk, white-tailed deer and mule deer. A natural case of CWD in reindeer (Rangifer tarandus tarandus) has not been reported despite potential habitat overlap with CWD-infected deer or elk herds. This study investigates the experimental transmission of CWD from elk or white-tailed deer to reindeer by the oral route of inoculation. Ante-mortem testing of the three reindeer exposed to CWD from white-tailed deer identified the accumulation of pathological PrP (PrP(CWD)) in the recto-anal mucosa associated lymphoid tissue (RAMALT) of two reindeer at 13.4 months post-inoculation. Terminal CWD occurred in the two RAMALT-positive reindeer at 18.5 and 20 months post-inoculation while one other reindeer in the white-tailed deer CWD inoculum group and none of the 3 reindeer exposed to elk CWD developed disease. Tissue distribution analysis of PrP(CWD) in CWD-affected reindeer revealed widespread deposition in central and peripheral nervous systems, lymphoreticular tissues, the gastrointestinal tract, neuroendocrine tissues and cardiac muscle. Analysis of prion protein gene (PRNP) sequences in the 6 reindeer identified polymorphisms at residues 2 (V/M), 129 (G/S), 138 (S/N) and 169 (V/M). These findings demonstrate that (i) a sub-population of reindeer are susceptible to CWD by oral inoculation implicating the potential for transmission to other Rangifer species, and (ii) certain reindeer PRNP polymorphisms may be protective against CWD infection.     

Prion protein gene heterogeneity in free-ranging white-tailed deer within the chronic wasting disease affected region of Wisconsin

Chronic wasting disease (CWD) was first identified in Wisconsin (USA) in whitetailed deer (Odocoileus virginianus) in February 2002. To determine if prion protein gene (Prnp) allelic variability was associated with CWD in white-tailed deer from Wisconsin, we sequenced Prnp from 26 CWD-positive and 100 CWD-negative deer. Sequence analysis of Prnp suggests that at least 86-96% of the white-tailed deer in this region have Prnp allelic combinations that will support CWD infection. Four Prnp alleles were identified in the deer population, one of which, resulting in a glutamine to histidine change at codon 95, has not been previously reported. The predominant allele in the population encodes for glutamine at codon 95, glycine at codon 96, and serine at codon 138 (QGS). Less abundant alleles encoded QSS, QGN, and HGS at the three variable positions. Comparison of CWD-positive with CWD-negative deer suggested a trend towards an over-representation of the QGS allele and an under-representation of the QSS allele.     

Metals in obex and retropharyngeal lymph nodes of Illinois white-tailed deer and their variations associated with CWD status

ABSTRACT

Prion proteins (PrP^C) are cell membrane glycoproteins that can be found in many cell types, but specially in neurons. Many studies have suggested PrP^C‘s participation in metal transport and cellular protection against stress in the central nervous system (CNS). On the other hand PrP^Sc, the misfolded isoform of PrP^C and the pathogenic agent in transmissible spongiform encephalopathies (TSE), has been associated with brain metal dyshomeostasis in prion diseases. Thus, changes in metal concentration associated with protein misfolding and aggregation have been reported for human and animal prion diseases, as well as for other neurodegenerative disorders, such as Parkinson's and Alzheimer's disease. The use of metal concentrations in tissues as surrogate markers for early detection of TSEs has been suggested. Studies on the accumulation of metals in free-ranging white-tailed deer have not been conducted. This study established concentrations of copper, iron, manganese, and magnesium in 2 diagnostic tissues used for CWD testing (obex and retropharyngeal lymph nodes (RLN)). We compared these concentrations between tissues and in relation to CWD status. We established reference intervals (RIs) for these metals and explored their ability to discriminate between CWD-positive and CWD-negative animals. Our results indicate that independent of CWD status, white-tailed deer accumulate higher concentrations of Fe, Mn and Mg in RLN than in obex. White-tailed deer infected with CWD accumulated significantly lower concentrations of Mn and Fe than CWD-negative deer. These patterns differed from other species infected with prion diseases. Overlapping values between CWD positive and negative groups indicate that evaluation of these metals in obex and RLN may not be appropriate as a diagnostic tool for CWD infection in white-tailed deer. Because the CWD-negative deer were included in constructing the RIs, high specificities were expected and should be interpreted with caution. Due to the low sensitivity derived from the RIs, we do not recommend using metal concentrations for disease discrimination.     

Prion sequence polymorphisms and chronic wasting disease resistance in Illinois white-tailed deer (Odocoileus virginianus)

Nucleic acid sequences of the prion gene (PRNP) were examined and genotypes compiled for 76 white-tailed deer from northern Illinois, which previously tested positive for chronic wasting disease (CWD), and 120 negative animals selected to control for geographic location and age. Nine nucleotide polymorphisms, seven silent and two coding, were found in the sampled population. All observed polymorphisms except two of very low frequency were observed in both negative and positive animals, although five polymorphic loci had significantly different distributions of alleles between infected and non-infected individuals. Nucleotide base changes 60C/T, 285A/C, 286G/A, and 555C/T were observed with higher than expected frequencies in CWD negative animals suggesting disease resistance, while 153C/T was observed more than expected in positive animals, suggesting susceptibility. The two coding polymorphisms, 285A/C (Q95H) and 286G/A (G96S), have been described in white-tailed deer populations sampled in Colorado and Wisconsin. Frequency distributions of coding polymorphisms in Wisconsin and Illinois deer populations were different, an unexpected result considering the sampled areas are less than 150 km apart. The total number of polymorphisms per animal, silent or coding, was negatively correlated to disease status. The potential importance of silent polymorphisms (60C/T, 153C/T, 555C/T), either individually or cumulatively, in CWD disease status has not been previously reported.     

Prion protein gene sequence and chronic wasting disease susceptibility in white-tailed deer (Odocoileus virginianus)

ABSTRACT

The sequence of the prion protein gene (PRNP) affects susceptibility to spongiform encephalopathies, or prion diseases in many species. In white-tailed deer, both coding and non-coding single nucleotide polymorphisms have been identified in this gene that correlate to chronic wasting disease (CWD) susceptibility. Previous studies examined individual nucleotide or amino acid mutations; here we examine all nucleotide polymorphisms and their combined effects on CWD. A 626 bp region of PRNP was examined from 703 free-ranging white-tailed deer. Deer were sampled between 2002 and 2010 by hunter harvest or government culling in Illinois and Wisconsin. Fourteen variable nucleotide positions were identified (4 new and 10 previously reported). We identified 68 diplotypes comprised of 24 predicted haplotypes, with the most common diplotype occurring in 123 individuals. Diplotypes that were found exclusively among positive or negative animals were rare, each occurring in less than 1% of the deer studied. Only one haplotype (C, odds ratio 0.240) and 2 diplotypes (AC and BC, odds ratios of 0.161 and 0.108 respectively) has significant associations with CWD resistance. Each contains mutations (one synonymous nucleotide 555C/T and one nonsynonymous nucleotide 286G/A) at positions reported to be significantly associated with reduced CWD susceptibility. Results suggest that deer populations with higher frequencies of haplotype C or diplotypes AC and BC might have a reduced risk for CWD infection – while populations with lower frequencies may have higher risk for infection. Understanding the genetic basis of CWD has improved our ability to assess herd susceptibility and direct management efforts within CWD infected areas.     

Landscape Features Fail to Explain Spatial Genetic Structure in White-Tailed Deer Across Ohio,USA

Landscape features influence wildlife movements across spatial scales and have the potential to influence the spread of disease. Chronic wasting disease (CWD) is a fatal prion disease affecting members of the family Cervidae, particularly white-tailed deer (Odocoileus virginianus), and the first positive CWD case in a wild deer in Ohio, USA, was recorded in 2020. Landscape genetics approaches are increasingly used to better understand potential pathways for CWD spread in white-tailed deer, but little is known about genetic structure of white-tailed deer in Ohio. The objectives of our study were to evaluate spatial genetic structure in white-tailed deer across Ohio and compare the support for isolation by distance (IBD) and isolation by landscape resistance (IBR) models in explaining this structure. We collected genetic data from 619 individual deer from 24 counties across Ohio during 2007–2009. We used microsatellite genotypes from 619 individuals genotyped at 11 loci and haplotypes from a 547-base pair fragment of the mitochondrial DNA control region. We used spatial and non-spatial genetic clustering tests to evaluate genetic structure in both types of genetic data and empirically optimized landscape resistance surfaces to compare IBD and IBR using microsatellite data. Non-spatial genetic clustering tests failed to detect spatial genetic structure, whereas spatial genetic clustering tests indicated subtle spatial genetic structure. The IBD model consistently outperformed IBR models that included land cover, traffic volume, and streams. Our results indicated widespread genetic connectivity of white-tailed deer across Ohio and negligible effects of landscape features. These patterns likely reflect some combination of minimal resistive effects of landscape features on white-tail deer movement in Ohio and the effects of regional recolonization or translocation. We encourage continued CWD surveillance in Ohio, particularly in the proximity of confirmed cases. © 2021 The Wildlife Society. This article has been contributed to by US Government employees and their work is in the public domain in the USA.     

Transmission of elk and deer prions to transgenic mice

Chronic wasting disease (CWD) is a fatal prion disease in deer and elk. Unique among the prion diseases, it is transmitted among captive and free-ranging animals. To facilitate studies of the biology of CWD prions, we generated five lines of transgenic (Tg) mice expressing prion protein (PrP) from Rocky Mountain elk (Cervus elaphus nelsoni), denoted Tg(ElkPrP), and two lines of Tg mice expressing PrP common to white-tailed deer (Odocoileus virginianus) and mule deer (Odocoileus hemionus), denoted Tg(DePrP). None of the Tg(ElkPrP) or Tg(DePrP) mice exhibited spontaneous neurologic dysfunction at more than 600 days of age. Brain samples from CWD-positive elk, white-tailed deer, and mule deer produced disease in Tg(ElkPrP) mice between 180 and 200 days after inoculation and in Tg(DePrP) mice between 300 and 400 days. One of eight cervid brain inocula transmitted disease to Tg(MoPrP)4053 mice overexpressing wild-type mouse PrP-A in approximately 540 days. Neuropathologic analysis revealed abundant PrP amyloid plaques in the brains of ill mice. Brain homogenates from symptomatic Tg(ElkPrP) mice produced disease in 120 to 190 days in Tg(ElkPrP) mice. In contrast to the Tg(ElkPrP) and Tg(DePrP) mice, Tg mice overexpressing human, bovine, or ovine PrP did not develop prion disease after inoculation with CWD prions from among nine different isolates after >500 days. These findings suggest that CWD prions from elk, mule deer, and white-tailed deer can be readily transmitted among these three cervid species.     

Prion sequence polymorphisms and chronic wasting disease resistance in Illinois white-tailed deer (Odocoileus virginianus)

Nucleic acid sequences of the prion gene (PRNP) were examined and genotypes compiled for 76 white-tailed deer from northern Illinois, which previously tested positive for chronic wasting disease (CWD), and 120 negative animals selected to control for geographic location and age. Nine nucleotide polymorphisms, seven silent and two coding, were found in the sampled population. All observed polymorphisms except two of very low frequency were observed in both negative and positive animals, although five polymorphic loci had significantly different distributions of alleles between infected and non-infected individuals. Nucleotide base changes 60C/T, 285A/C, 286G/A and 555C/T were observed with higher than expected frequencies in CWD negative animals suggesting disease resistance, while 153C/T was observed more than expected in positive animals, suggesting susceptibility. The two coding polymorphisms, 285A/C (Q95H) and 286G/A (G96S), have been described in white-tailed deer populations sampled in Colorado and Wisconsin. Frequency distributions of coding polymorphisms in Wisconsin and Illinois deer populations were different, an unexpected result considering the sampled areas are less than 150 km apart. The total number of polymorphisms per animal, silent or coding, was negatively correlated to disease status. The potential importance of silent polymorphisms (60C/T, 153C/T, 555C/T), either individually or cumulatively, in CWD disease status has not been previously reported.Key words: CWD, PRNP, synonymous polymorphism, cumulative polymorphisms, haplotype     

Tonsillar biopsy test for chronic wasting disease: Two sampling approaches in mule deer and white-tailed deer

Preclinical antemortem testing of deer (Odocoileus spp.) for chronic wasting disease (CWD) can be important for determining prevalence rates and removing infected individuals from wild populations. Because samples with high numbers of tonsillar follicles are likely to provide earlier detection of CWD than samples with fewer follicles, the method of obtaining follicular samples may be critical when investigating disease prevalence. Between January 2003 and January 2005, white-tailed deer (O. virginianus) in southeast and southwest Minnesota and white-tailed and mule deer (O. hemionus) in Wind Cave National Park, South Dakota, were sampled using dorso-lateral and ventral-medial approaches for collecting tonsillar follicles. We obtained significantly more follicles using a dorso-lateral (median number of follicles = 19) rather than a ventral-medial (median number of follicles = 5.5) approach. No differences were observed in collection of tonsillar follicles that were related to sex, age class, or species of deer. We recommend the dorso-lateral approach for assessing CWD prevalence in deer populations.     

Antibodies to ruminant alpha-herpesviruses and pestiviruses in Norwegian cervids

A serologic survey revealed that Norwegian populations of free-ranging reindeer (Rangifer tarandus tarandus), roe deer (Capreolus capreolus), red deer (Cervus elaphus), and moose (Alces alces) have been exposed to alpha-herpesviruses and pestiviruses. A total of 3,796 serum samples collected during the period 1993-2000 were tested in a neutralization test for antibodies against bovine herpesvirus 1 (BHV-1) or cervid herpesvirus 2 (CerHV-2), and 3,897 samples were tested by a neutralization test and/or enzyme-linked immunosorbent assay for antibodies against bovine viral diarrhea virus (BVDV). Antibodies against alpha-herpesvirus were found in 28.5% of reindeer, 3.0% of roe deer, and 0.5% of red deer, while all moose samples were negative. In reindeer, the prevalence of seropositive animals increased with age and was higher in males than females. Antibodies against BVDV were detected in 12.3% of roe deer, 4.2% of reindeer, 2.0% of moose and 1.1% of red deer. The results indicate that both alpha-herpesvirus and pestivirus are endemic in reindeer and pestivirus is endemic in roe deer in Norway. The viruses may be specific cervid strains. Seropositive red deer and moose may have become exposed as a result of contact with other ruminant species.     

Chronic wasting disease: Fingerprinting the culprit in risk assessments

Transmissible spongiform encephalopathies (prion diseases) in animals may be associated with a zoonotic risk potential for humans as shown by the occurrence of variant Creutzfeldt-Jakob disease in the wake of the bovine spongiform encephalopathy epidemic. Thus, the increasing exposure of humans in North America to cervid prions of chronic wasting disease (CWD) in elk and deer has prompted comprehensive risk assessments. The susceptibility of humans to CWD infections is currently under investigation in different studies using macaques as primate models. The necessity for such studies was recently reinforced when disease-associated prion protein and its seeding activity were detected in muscles of clinically inconspicuous CWD-infected white-tailed deer (WTD). Increasing evidence points to the existence of different CWD strains and CWD prions may also change or newly emerge over time. Therefore, CWD isolates examined in macaques should be characterized as precisely as possible for their molecular identity. On this basis other CWD field samples collected in the past, present or future could be systematically compared with macaque-tested inocula in order to assess whether they are covered by the ongoing risk assessments in primates. CWD typing by Fourier transform-infrared spectroscopy of pathological prion protein may provide a method of choice for this purpose.     

Effects of chronic wasting disease on reproduction and fawn harvest vulnerability in Wisconsin white-tailed deer

Chronic wasting disease (CWD) is a fatal, transmissible spongiform encephalopathy that affects free-ranging and captive North American cervids. Although the impacts of CWD on cervid survival have been documented, little is known about the disease impacts on reproduction and recruitment. We used genetic methods and harvest data (2002-04) to reconstruct parentage for a cohort of white-tailed deer (Odocoileus virginianus) fawns born in spring 2002 and evaluate the effects of CWD infection on reproduction and fawn harvest vulnerability. There was no difference between CWD-positive and CWD-negative male deer in the probability of being a parent. However, CWD-positive females were more likely to be parents than CWD-negative females. Because our results are based on harvested animals, we evaluated the hypothesis that higher parentage rates occurred because fawns with CWD-positive mothers were more vulnerable to harvest. Male fawns with CWD-positive mothers were harvested earlier (>1 mo relative to their mother's date of harvest) and farther away from their mothers than male fawns with CWD-negative mothers. Male fawns with CWD-positive mothers were also harvested much earlier and farther away than female fawns from CWD-positive mothers. Most female fawns (86%) with CWD-positive mothers were harvested from the same section as their mothers, while almost half of male and female fawns with CWD-negative mothers were farther away. We conclude that preclinical stages of CWD infection do not prohibit white-tailed deer from successfully reproducing. However, apparently higher harvest vulnerability of male fawns with CWD-positive mothers suggests that CWD infection may make females less capable of providing adequate parental care to ensure the survival and recruitment of their fawns.