Grazing by wild red deer can mitigate nutrient enrichment in protected semi-natural open habitats

Eutrophication through atmospheric nutrient deposition is threatening the biodiversity of semi-natural habitats characterized by low nutrient availability. Accordingly, local management measures aiming at open habitat conservation need to maintain habitat-specific nutrient conditions despite atmospheric inputs. Grazing by wild herbivores, such as red deer (Cervus elaphus), has been proposed as an alternative to mechanical or livestock-based measures for preserving open habitats. The role of red deer for nutrient dynamics in protected open habitat types, however, is yet unclear. Therefore, we collected data on vegetation productivity, forage removal, quantity of red deer dung and nutrient concentrations in vegetation and dung from permanent plots in heathlands and grasslands (eight plots à 225 m2 per habitat type) on a military training area inhabited by a large population of free-ranging red deer over one year. The annual nutrient export of nitrogen (N) and phosphorus (P) by red deer grazing was higher than the nutrient import through red deer excreta, resulting in an average net nutrient removal of 14 and 30 kg N ha−1 a−1 and 1.1 and 3.3 kg P ha−1 a−1 in heathlands and grasslands, respectively. Even when considering approximate local atmospheric deposition values, net nutrient depletion due to red deer grazing seemed very likely, notably in grasslands. Demonstrating that grazing by wild red deer can mitigate the effects of atmospheric nutrient deposition in semi-natural open habitats similarly to extensive livestock grazing, our results support the idea that red deer are suitable grazing animals for open habitat conservation. Supplementary Information The online version contains supplementary material available at 10.1007/s00442-022-05182-z.


Appendices
Appendix A1 Faecal N concentrations observed in red deer dung and predicted based on plant N concentration Tables   Table S1 Summary      = 0.941 + 0.479 * Then we calculated the ratio of observed faecal N concentration to expected faecal N concentration (Christianson and Creel 2010).
We explored differences between the observed and expected N concentrations in red deer dung using N concentration as response and data type (observed/expected) as well habitat type (grassland/heathland) and sampling date (five levels) and all interactions as explanatory variables. As we had collected the dung samples at site level, the expected faecal N concentrations calculated from hand-pluck samples for each of the two plots per sampling site were averaged. Accordingly, sampling site sufficed as random factor.
In heathlands, the faecal N concentration predicted based on plant N concentration in hand pluck samples was significantly lower than the observed faecal N concentration except for the winter period Oct-Apr, in which the difference was not significant, and the spring period Apr-May, in which the expected N was higher than the observed N (Online Resource Fig. S3, Tables S5, S6). In grasslands, the expected faecal N concentration was significantly lower than the observed N concentration in red deer dung for all sampling dates. The ratio of observed:expected faecal N averaged per period ranged between 0.92 and 1.43 in heathlands and between 1.53 and 1.72 in grasslands (Online Resource Table   S1).
From the difference between observed faecal N and faecal N predicted based on plant N we deduce that the diet red deer actually consumed often had a better forage quality than the vegetation we cut on our plots when collecting the hand-pluck samples. The ratio of observed:expected faecal N was higher than 1.5 in grasslands throughout the year, but rather close to one in heathlands except for the summer periods. As red deer are intermediate feeders (Hofmann 1989), able to switch between bulk feeding and concentrate selecting strategies, it is likely that they did not take bites randomly as we did when collecting the hand-pluck samples at plot-scale, but grazed more selectively choosing plants with elevated N concentration (Langvatn and Hanley 1993;Semiadi et al. 1995). Especially female red deer are highly selective in foraging, mostly from late winter until parturition (Čupić et al. 2021). The generally more balanced ratio of observed:expected faecal N in heathlands probably resulted from a lower availability of plants with high N concentration in this habitat, which is characterized by extremely low soil nutrient levels (Riesch et al. 2018). That the ratio of observed:expected faecal N concentration in heathlands was higher during summer than during the rest of the year could be a result of red deer feeding in other habitats in that time of the year, which is likely, as significant red deer forage removal occurred in heathlands only during the winter period (Riesch et al. 2019). Our main quantitative result that the nutrient export mediated by red deer exceeded the import in both habitat types gains even more relevance under the assumption that study plots might have received red deer dung at least partially produced from vegetation with higher nutrient concentrations growing at other places.
We are, however, aware that our comparison of observed to expected faecal N is based on rather rough estimates, as we used a regression for predicting faecal N from plant N derived from a limited data set (n = 58, r 2 = 0.64 (Moen and DelGiudice 1997)) comprising different ruminant species. In addition, faecal N might actually be higher than predicted when animals feed on vegetation high in secondary plant compounds, such as tannins and other phenolics (Moen and DelGiudice 1997). The N concentration in dung is usually interpreted as a proxy for diet digestibility, but when secondary plant compounds reduce the digestibility of dietary N while increasing faecal N concentration, this might not be valid (Leslie et al. 2008;Arturo et al. 2015). Secondary plant compounds are supposed to be low or absent in a grass-based diet (Gordon 2003;Verheyden-Tixier et al. 2008 Additionally, irrespective of diet N, animals are able to extract a higher fraction of N in winter, leading to lower faecal N concentrations (Arnold et al. 2015), which might have contributed to the closer observed:expected faecal N ratio in heathlands in winter. While these considerations do not compromise our quantitative assessment of nutrient fluxes and stoichiometry, we are hence cautious with inferences regarding the digestibility of red deer diets in our study system.

Table S3
Aboveground net primary productivity (ANPP, kg ha -1 ; Riesch et al. 2019) in heathlands and grasslands and the associated amount of nitrogen (N) and phosphorus (P) in the vegetation biomass based on plant N and P concentrations (cf . Table S1), as well as the net nutrient removal by wild red deer (cf. a Weight data were missing for some animals, so that mean and sum were calculated based on n=185 in NB, n=197 in LH, n=278 in ST and n=219 in SB b To approximate the total weight of all culled animals, we added the mean weight for each animal for which weight data were not available c Based on 2.8% N in body tissue (Whitehead 2000) d Based on 1.0% P in body tissue (Whitehead 2000)