Exposure of a dam to pathogens may potentially affect her fawns positively or negatively. Mammalian females transfer immunologic protection to their offspring via colostrum obtained while nursing. Conversely, chronic diseases in dams may potentially result in small and weak neonates, reduced milk production or quality, or infection. Little is known about how pathogen exposure in adult female white-tailed deer (Odocoileus virginianus) affects offspring survival. Our objective was to assess pathogen exposure for female white-tailed deer and subsequent survival rates of fawns in Dunn and Grant counties, North Dakota, and Perkins County, South Dakota, USA. We collected blood serum from 150 adult female deer during 2014. We compared survival of 49 fawns to maternal exposure to 10 pathogens from 37 of 150 adult females. There was no difference in fawn mass between dams based on antibody status and no difference in fawn survival for nine pathogens. The 12-wk survival for fawns born to mothers with antibodies against bovine herpesvirus 1 (BoHV-1, causing infectious bovine rhinotracheitis) was lower than for fawns born from mothers without antibodies against BoHV-1; however, the indirect or direct impacts of BoHV-1 exposure in mothers on fawn survival are unclear. Although our findings suggest that the cost of exposure to previous diseases may have minimal impact on short-term fawn survival for most pathogens, additional research with increased sample sizes is needed to confirm our findings.
Estimating survival rates and cause-specific mortality of differing age classes in ungulate species permits an improved understanding of population ecology for those species. Although adult female survival tends to have the greatest impact on population growth in ungulate populations, it is generally high and stable, whereas offspring survival is often more variable, resulting in a greater impact on population dynamics (Gaillard et al. 1997; Raithel et al. 2007; Chitwood et al. 2015). Several studies have assessed how landscape factors affect offspring survival (Grovenburg et al. 2012; Gulsby et al. 2017; Gingery et al. 2018; Michel et al. 2018) and which predators are most responsible for mortality events (Gingery et al. 2018; Kautz et al. 2019; Michel et al. 2020). However, recent findings indicate that offspring survival can be inherently low even in the absence of predators, suggesting other factors such as disease exposure may impact fitness (Dion et al. 2020). In a review of deer-predator relationships, Ballard (2011) reported that coyotes (Canis latrans), mountain lions (Puma concolor), and wolves (Canis lupus) may be substantial mortality factors in some areas under certain conditions, but large herbivores at, or near, carrying capacity do not exhibit strong responses to predator removal, as emphasized by Bowyer et al. (2005, 2014, 2020). Predator control is often cited by some members of the hunting public as needed to protect game populations. However, attempts at predator control have largely been shown to be ineffective, are costly, and increasingly are being viewed negatively by the general public (Ballard 2011; Jensen et al. 2023). Smith et al. (2014) reported that bighorn sheep (Ovis canadensis) lambs with pneumonia were predisposed to predation. Deciphering the relative importance of proximate mortality factors on ungulate populations, such as predation, versus potential ultimate mortality factors (e.g., disease) should increase our understanding of ungulate population dynamics and may become important for decision makers setting management policy.
Some pathogens, such as Mycobacterium avium paratuberculosis, may be transmitted in utero, leading to direct health costs to offspring (van Kooten et al. 2006; Nalls et al. 2021). However, previous exposure of a dam to a given pathogen may impact fawn survival in a variety of ways. Maternally derived antibodies may help to prevent infection or reduce the severity of disease in fawns. For example, the presence of maternally derived antibodies to epizootic hemorrhagic disease virus (EHDV) serotype 2 in fawns prevented or significantly reduced clinical disease and length of viremia compared with that of naïve fawns challenged under experimental conditions (Stilwell et al. 2021). Conversely, infection of a dam is likely to come at an energetic cost that may result in the birth of smaller fawns and compromise the dam’s ability to rear young (Verme 1965; Ballard 2011).
Given the importance of fawn survival in understanding population dynamics for white-tailed deer (Odocoileus virginianus), and the difficulties in determining proximate versus ultimate factors affecting neonate survival, our objectives were to use baseline information on pathogen exposure for adult female white-tailed deer established by Moratz et al. (2019) to compare exposure rates to survival rates of their fawns in Dunn and Grant counties located in western North Dakota and Perkins County in northwestern South Dakota, USA. We predicted that fawns born from dams previously infected with pathogens that impart passive transmissible immunity (e.g., EHDV and bovine parainfluenza virus) would display increased survival compared with fawns born from mothers without evidence of such exposure. We also predicted that fawns born from dams with persistent chronic diseases that do not impart passive transmissible immunity (e.g., anaplasmosis and infectious bovine rhinotracheitis [IBR]) would display decreased survival compared with fawns born from dams free of these diseases.
MATERIALS AND METHODS
We assessed pathogen exposure in female white-tailed deer in Grant and Dunn counties, North Dakota, and Perkins County, South Dakota, USA in 2014 (Fig. 1), as part of a previously published population study (Moratz et al. 2019). These three study areas are within the unglaciated physiographic region referred to as the Missouri Slope (Seabloom 2020). The region has a semiarid continental climate with hot summers and cold winters. Annual precipitation ranges from 35 to 40 cm (Jensen 1972). Native vegetation is predominated by mixed- and short-grass prairie, with cottonwood (Populus deltoides) river bottoms along major river systems. As of 2000, approximately 27% of this region remained in native vegetation (Jensen 2001). We captured 50 female (>1.5-yr-old) white-tailed deer in each county by using aerial net-gunning from 24 February to 2 March 2014. We collected blood at time of capture and centrifuged it into cellular and serum fractions that were, respectively, discarded and frozen at −80 C. Vaginal implant transmitters (VITs; Advanced Telemetry Systems, Inc., Isanti, Minnesota, USA) were implanted at time of capture in a subset of 20 females to aid in neonate capture, help determine fawning habitat, and evaluate survival rates in each study area (Brackel et al. 2021).
We also opportunistically searched for neonates near expelled VITs, in areas of known fawning habitat, and near females who showed postpartum behavior such as isolation or fleeing short distances when approached (Rohm et al. 2007; Grovenburg et al. 2010) and then captured neonates by hand or net. Upon capture, we restrained and blindfolded neonates, determined sex and general body condition, recorded body mass (in kilograms), measured hoof growth (in millimeters; Brinkman et al. 2004), and fitted individuals with an M4210 expandable breakaway radio-collar (Advanced Telemetry Systems, Inc.). We wore sterile rubber gloves, used no-scent spray, stored radio-collars and other equipment in natural vegetation, and kept handling time under 5 min, when possible, to reduce capture-related mortality. If individuals were wet from rain or afterbirth, or were too large to fit in the weighing bag, we only determined sex and then radio-collared the neonate. We followed all handling methods described by the American Society of Mammalogists guidelines for mammal care and use (Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2016) and were approved by the South Dakota State University Institutional Animal Care and Use Committee (approval no. 13-091A).
We estimated fawn age by using hoof growth measurements (Brinkman et al. 2004). We then backcalculated birth mass for individuals we estimated to be >1 d old by using estimated age and assumed neonates gained 0.215 kg/d (Verme 1963). We assigned mean mass and mean hoof measurements of neonates captured within the same week to neonates that were too wet or too large to weigh or take hoof measurements. Finally, we assigned capture mass as birth mass for individuals estimated to be ≤1 d old. We monitored fawns daily during the first 30 d by using aerial telemetry, omnidirectional whip antennas, and handheld telemetry equipment and then monitored them two or three times per week to the age of 12 wk. We investigated mortalities immediately after detecting a mortality signal and transported carcasses to the North Dakota Game and Fish Department Wildlife Health Laboratory in Bismarck to confirm proximate cause of death. Natural causes of mortality were disease, predation, and unknown mortalities. We classified hunter harvest and vehicle collision mortalities as human-related mortalities.
We sent serum to the University of Minnesota Veterinary Diagnostic Laboratory (St. Paul, USA) where it was tested for antibodies to Anaplasma spp. via a competitive ELISA, Borrelia burgdorferi via immunofluorescent antibody test, bovine parainfluenza virus 3 via hemagglutination inhibition, bovine viral diarrhea virus types 1 and 2 via serum neutralization (SN), epizootic hemorrhagic disease virus via agar gel immunodiffusion, bovine herpes virus 1 (BoHV-1, causing IBR) via SN, Leptospira bratislava and Leptospira pomona via modified agglutination test, and Neospora caninum via ELISA. Serum was also sent to the National Veterinary Services Laboratory (U.S. Department of Agriculture, Ames, Iowa, USA) where it was tested for antibodies to the gammaherpesviruses causing malignant catarrhal fever via peroxidase-linked assay and virus neutralization and to West Nile virus via plaque reduction neutralization test. Serum was also tested for antibodies against eight other pathogens that were excluded from this paper because no antibodies were detected in any individual (Moratz et al. 2019).
We grouped fawns based on the presence or absence of detectable antibodies in their dams for each pathogen. We used a t-test in Program R (R Core Team 2019) to compare body mass of fawns born from mothers testing positive for serum tests for parasite and disease agents to mothers testing negative. We grouped fawns by survival status to 12 wk of age and assessed differences in survival by using the chisq.test function in Program R. We also assessed the relationship between the number of pathogens detected per dam and fawn survival by using a logistic model in Program R. We used a Bonferroni correction factor to account for the increased number of comparisons. Thus, we considered relationships important at α=0.004. Although siblings were probably represented in our dataset, we did not verify sibling status via genetics or direct observation. In addition, relatively small sample sizes (i.e., low number of fawns that died) would preclude use of a more statistically rigorous analysis. Therefore, we acknowledge the potential for pseudoreplication in our dataset.
We captured fawns from 23 May to 20 June 2014. We detected and radio-collared 51 fawns by using VITs, plus three fawns from radio-collared dams not fitted with VITs. One fawn was abandoned within 1 d of capture, radio signal of three fawns was lost, and permission to recover one fawn from private land was denied; these five fawns were subsequently censored from further analyses. Mean body mass for the fawns from known dams was 3.5 kg (SD=0.70, n=49) and mean age at capture was 1.5 d (SD=0.72, n=54). There was no difference in fawn body mass based on the dam’s antibody status to any pathogen (P≥0.347; Table 1). The number of pathogens detected per dam ranged from zero to six (SD=7.2, n=37). There was variation in the percentage of surviving fawns born to dams where no pathogens were detected (∼73%, n=11), one pathogen was detected (50%, n=10), two pathogens were detected (60%, n=10), and more than two pathogens were detected (67%, n=18), but there was no relationship between the number of pathogens detected per dam and fawn survival (β=0.011, P=0.946, n=49).
Of the remaining 49 fawns, 19 (39%) died within the first 12 wk of life. We assessed mortality of fawns <3 mo old, based upon positive or negative serum titers for parasite and disease agents found in the dam. In total, 4 (21%) of 19 fawns that died and 11 (34%) of 32 fawns that lived were from dams that did not test positive for any disease agents. The only titer found in mothers that was related to fawn mortality was BoHV-1 (causing IBR), with fawns born from dams that tested positive displaying increased mortality (χ2=10.796, df=1, P=0.001, n=49; Table 2).
Six fawn mortalities were associated with BoHV-1–positive dams: each was a singlet fawn, coming from different dams. Titer values for BoHV-1–positive dams averaged 1:13.3 (range, 1:8–1:32). Four fawns were females and two were males. We measured body mass for five fawns (&xmacr;=3.7 kg, SD=1.40, n=5) and mean age at capture was 1.3±1.0 d (n=6). We classified proximate cause of five of these mortalities as coyote predation and one mortality as an unknown cause (Moratz 2016). Mean age at death of these six fawns was 8.7 d (range, 2–20 d) with two, three, and one of the mortalities occurring in Dunn, Grant, and Perkins counties, respectively.
Our goal was to assess the potential effect that maternal exposure may have on fawn survival. However, our limited sample size, the inability to account for sibling status, and the inability to assess the potential for co-infection among individuals limits the scope of our analysis. Our results provided only minimal evidence for our predictions; for 10 of 11 pathogens evaluated, there was no correlation between a dam’s antibody status and the likelihood that her fawn would survive to 12 wk of age. Furthermore, exposure history in the dam had no significant effect on birthweights. Hence, these findings fail to demonstrate a readily apparent cost of short-term fawn survival for most pathogens. Although younger dams and dams stressed by severe winters produce smaller litters and neonates (Ditchkoff 2011), even severely stressed and emaciated dams produce live neonates (Verme 1965). It would therefore seem that severe winters stressed dams, and, in turn, survival of their subsequent neonates may be affected by a plethora of mortality factors (e.g., weather, predation; Ciuti et al. 2015).
Of the pathogens for which we screened, most demonstrated no detectable effect on neonate survival; the one exception was BoHV-1, causing IBR. Infectious bovine rhinotracheitis is common in cattle production systems such as feedlots and is characterized by respiratory disease, abortions, still births, and gastrointestinal distress (Yates 1982). Its role in free-ranging white-tailed deer is poorly understood, but clinical signs of IBR in mule deer (Odocoileus hemionus) include transient anorexia, depression, excessive salvation, increased respiratory rate, dyspnea, and occasional cough (Chow and Davis 1964). Serology studies have found antibody rates more than 50% in some areas (Quebec, Canada: Sadi et al. 1991; Washington, USA: Myers et al. 2015); 19% of all does from this study had detectable antibodies to BoHV-1 (Moratz et al. 2019). Five of six fawns born to I BoHV-1 antibody-positive dams died from apparent predation, whereas cause of death in the sixth fawn was not determined. In cattle, BoHV-1 infection is life-long, and stress may play a role in recrudescence of the disease (Yates 1982). Although speculative, it is possible that stress to the dam, either natural or caused by handling, resulted in symptoms that directly compromised the fawn’s fitness, or her ability to rear young. In addition, the incubation period for IBR is 2–4 d (Chow and Davis 1964). With the short incubation period, and clinical expression of IBR causing inflammation impacting the fawn’s ability to nurse and digest food, transmission of the disease from the dam may influence the neonate’s survival. Mean age at death of the six fawns born from BoHV-1–infected dams was 8.7 d; therefore, the potential for BoHV-1 infection to be related to the proximate cause of death (i.e., mortality) via increased susceptibility is plausible. However, this relationship is admittedly speculative at best.
Our study was limited to 12-wk and positive effects of the dam’s exposure history on fawn survival would probably require a longer period to be detected. The likelihood of exposure to pathogens increases with time, and several vector-borne diseases, such as borreliosis, are highly seasonally dependent. Regardless, because the role of maternal exposure in modifying clinical outcomes has been demonstrated for some pathogens under experimental settings (Stilwell et al. 2021), this study is an early attempt in extrapolating such an understanding to a free-ranging deer in a natural setting.
Although the effects of epizootic outbreaks on populations are easily observable, the subtle effects of diseases on population dynamics are not well understood and may be underestimated (Leopold 1933). We were only able to minimally detect positive or negative benefits to the neonate from the dams’ prior exposure to these pathogens for most of the pathogens tested. However, IBR (BoHV-1 infection) may warrant additional attention regarding potential negative impacts. A comprehensive longer term study may help to further decode this important aspect of population ecology. Our results provide limited evidence that maternal exposure of white-tailed deer to certain pathogens (i.e., BoHV-1) may predispose their offspring to predation, further supporting Smith et al. (2014) who found that bighorn sheep offspring with pneumonia were also predisposed to predation. However, further research is needed to assess disease prevalence and predation in fawns because our relatively small sample size, the inability to account for litter size, and the potential of co-infection limit our ability to derive statistically sound conclusions.
We thank the North Dakota Game and Fish (NDGF) Department; South Dakota Department of Game, Fish and Parks; the Department of Natural Resource Management at South Dakota State University; and numerous private landowners for help with the project. We thank field technicians R. Johnson, R. Kelble, A. Dwire, A. Kauth, S. Bard, and C. Argabright. Special thanks to NDGF technicians J. Mortenson and A. Pachl. This project was funded by Federal Aid to Wildlife Restoration administered through NDGF Department (study W-67-R) and South Dakota Department of Game, Fish and Parks (study 7555).