Inorganic elements and compounds that play a role in animal growth and metabolism are termed minerals. Minerals are critical to physiological processes of animals, including mineralization of bones, enzyme and protein production, osmotic control, immune system response, and cellular respiration [1] [2]. In a biological context, minerals are usually categorized as macro- and micro-, or trace, minerals. Macrominerals are required in dietary concentrations >100 ppm, whereas trace minerals are needed in lesser quantities.

Despite the importance of minerals in the diet, mineral requirements for most species of wildlife are poorly documented [3]. Over 60 different elements have been documented in the mammalian body [4], but it is unclear what, if any, purpose many of these minerals serve. Furthermore, there are discrepancies in the literature on how many minerals are essential in the diet [1] [5] [6]. Overall, our understanding of mineral requirements in wildlife is hindered by complex interactions among mineral, environmental, and physiological factors [7].

When animals are unable to meet nutrient requirements, their physiological function may be negatively impacted. Extreme deficiencies may lead to mortality, but most cases of deficiency are less severe and are often manifested in rough coat or hair, anemia, lowered immunity, and general unthriftiness [1] [8]. Geographic variation in mineral availability can predispose certain populations to subclinical mineral deficiencies [2]. Some regional mineral deficiencies of ungulates are well documented and easily diagnosed from clinical symptoms [9]. However, other regional mineral deficiencies can go largely unnoticed, given their lack of definitive symptoms [2] [9] [10].

There is a growing body of work showing intraspecific ungulate morphology is correlated with soil and vegetation at a regional scale [11] - [16]. These regional size differences in ungulate morphology are thought to be nutritionally mediated, but a direct link with forage composition is largely unknown. Much research on regional differences in ungulate body and ornament size (i.e., horns and antlers) focuses on macronutrients, such as energy and protein [17] [18] [19], even though a common symptom of mineral deficiencies is stunted growth [20]. This is not altogether surprising, given the scarcity of information on diagnosing mineral deficiencies in wildlife [9] [21]. White-tailed deer (Odocoileus virginianus) are well studied but only limited baseline values for diagnosing mineral abnormalities have been published [1]. Any effects of mineral deficiencies on size variation are unknown.

The goal of our study was to further our knowledge on the impacts of mineral health on the morphology of free-ranging populations of white-tailed deer. Specifically, we evaluated the hypothesis that morphological size differences of deer are associated with mineral deficiencies. In South Texas, deer found in the Coastal Sand Plain ecoregion appear physically smaller than deer in neighboring regions with less sandy soils. We predicted that deer from the site with smaller average deer morphology sizes would have higher incidence of serum mineral deficiencies.

Asymptotic body mass and hind foot length, for both females and males, differed between sites (Table 1). Asymptotic body mass of female deer at the inland site was 10% larger than the coastal site (t_329.08 = −149.42, P < 0.001; Figure 2;

Table 1). Hind foot asymptotic length was 3% and 4% greater at the inland as compared to the coastal site for females (t_355.67 = −189.41, P < 0.001) and males (t_857.00 = −265.17, P < 0.001), respectively. Male deer achieved an asymptotic body mass (t_388.00 = −14.24, P < 0.001) and antler size (t_760.12 = −28.76, P < 0.001) 20% and 8% greater at the inland than the coastal site, respectively (Figure 3).

Sixteen of 24 (67%) deer captured at the coastal site had deficient copper serum levels, and only 3 of 21 (14%) of the deer caught at the inland site were deficient (0.67 versus 0.14, P < 0.001, Fisher’s exact test, Table 2). Seven of 21 (33%) deer at the inland site had higher than normal serum potassium levels, whilst none of the deer at the coastal site (0%) deviated from the normal range (0.33 versus 0.00, P = 0.003, Fisher’s exact test). No other differences in serum mineral abnormalities between sites were observed (P ≥ 0.07, Fisher’s exact test).

All deer exhibited multiple serological mineral abnormalities, suggesting our current knowledge of normal ranges is incomplete. Mineral toxicities result in readily visible symptoms and often morbidity, while symptoms of deficiencies are less severe [20]. Therefore, we believe most of the discrepancies in serum mineral values we observed above the “normal range” reflect a lack of knowledge regarding mineral balances in wildlife, not true abnormalities. We encourage wildlife health practitioners to publish more normal mineral values as there is a

consensus that current knowledge is lacking, yet little sharing of knowledge is evident. For the remainder of our discussion, we focus on the observed deficiencies, as these more likely are indicative of population mineral health and are often

manifested in the lowered growth that we observed.

Long-term trends on age-specific morphology show deer on the coastal site were physically smaller than deer on the inland site. Previous work suggests these observed size differences are nutritionally, rather than genetically, mediated [34]. Observational studies cannot prove causality, but the higher incidence of copper deficiency at the coastal site suggests copper might be limiting deer growth in coastal habitats. In wild ungulates, hypocuprosis most often results in suppressed growth, lowered reproductive output, and increased risk to secondary factors, such as predation and infectious diseases [2] [35]. Previous research has shown recruitment rates obtained from aerial surveys are lower at the coastal than at the inland site [36]. Furthermore, captive feeding trials corroborate that normal reference ranges for serum copper concentration in adult white-tailed deer are ~1 ppm [37]. Thus, we believe the copper deficiencies we report here are truly deficiencies and not a result of inaccurate reference values.

Copper deficiencies have been observed in many species of livestock and in humans [38]. Ruminants can experience either primary or secondary hypocuprosis [39]. Primary copper deficiencies are caused by inadequate dietary copper. It is unknown what level of dietary copper is optimal for white-tailed deer, however, for cattle, 10 ppm of dietary copper is sufficient [40]. Native range plants growing on our study areas, as well as throughout Texas generally have low levels of copper (≤6 ppm on average) which could predispose herbivores to copper deficiencies [41] [42]. Secondary deficiencies result from lowered copper absorption in the digestive tract. Interactions between minerals may hinder absorption of copper in ruminants [38] [39]. In the presence of elevated sulfur and molybdenum levels, thiomolybdates are formed [43] [44]. These thiomolybdates react with copper to form insoluble complexes that are indigestible [45]. Therefore, optimal diets for cattle should have a copper to molybdenum ratio around 6:1, as ratios ≤2:1 routinely cause hypocuprosis. Additionally, elevated levels of dietary sulfur can result in the formation of copper sulfide in the digestive tract, which reduces the absorption of copper [46]. There are no published normal ranges of molybdenum serum concentrations for white-tailed deer, so we were unable to determine if the proportion of deer with abnormal molybdenum serum levels differed between sites. The molybdenum concentrations in serum, however, were higher at the coastal site than the inland site.

Our data based on the animal as an indicator approach indicated that copper might be a limiting nutrient for white-tailed deer in coastal regions along the Gulf of Mexico. Observational studies, however, cannot show causality and further work in controlled settings are needed to fully describe the relationship between growth and copper deficiencies in white-tailed deer. White-tailed deer consume highly diverse diets [47] and copper concentrations vary by forage class [48]. It is possible that deer at the coastal site are consuming less dietary copper, or more molybdenum, as an artifact of maximizing intake of digestible energy, or some other nutrient. Given normal mineral concentrations are poorly documented in white-tailed deer, it is possible that the deer at our coastal site represent the lower end of acceptable copper serum levels. Even with these caveats, our study suggests trace minerals are relevant in wildlife management and discussions pertaining to regional nutritional differences should include aspects of mineral levels in the future.

All 45 deer we sampled exhibited serum mineral concentrations outside of the normal range. Therefore, it is likely many species of wildlife, including white-tailed deer, have broader normal ranges of serum mineral levels than previously documented. Incidence of copper deficiencies was greater at the site with the smallest average deer morphology and a common symptom of copper deficiencies is suppressed somatic growth. Bioavailability of copper depends on the chemical structure of the copper, interactions with numerous other minerals, and other environmental and physiological factors [49]. Although, copper is potentially limiting deer growth, we do not recommend simply providing copper supplementation, given the complexities involved in trace mineral absorption. Rather we suggest managers should focus efforts on providing a diversity of palatable forage, allowing deer to self-regulate their dietary mineral intake.

We thank M. Rice, K. Gann, P. Ortega, Jr., and the many technicians and volunteers from Southwest Texas Junior College, Stephen F. Austin State University, Sul Ross State University, Tarleton State University, Texas A&M University, Texas A&M University-Kingsville, Texas State University, and Texas Tech University for helping collect data. M. Robinson, J. Haynes, and S. Vásquez provided logistical and mechanical support during deer captures. A. Bhandari, J. Sawyer, and the members of the DeYoung research group provided comments on a previous draft that improved this manuscript. Discussions with D. Agnew, J. Buchweitz, L. Howard, R. Sadler, K. Thompson, and especially M. Clancy were helpful in understanding the relationships between serum and liver mineral values. Funding was provided by the East Foundation. This is publication number 064 of the East Foundation and 21-111 of the Caesar Kleberg Wildlife Research Institute.

The authors declare no conflicts of interest regarding the publication of this paper.

Rankins, S.T., DeYoung, R.W., Foley, A.M., Ortega-S., J.A., Fulbright, T.E., Hewitt, D.G., Hilton, C.D., Schofield, L.R. and Campbell, T.A. (2023) Regional Copper Deficiency in White-Tailed Deer. Open Journal of Ecology, 13, 9-21. https://doi.org/10.4236/oje.2023.131002