de la Peña, E., Martín, J., Carranza, J. (2020) Ultrastructural morphological features of the hair in a sexual signal: the dark ventral patch of male red deer. Journal of Zoology ISSN 0952-8369

Chemical signals play a decisive role in communication in many mammal species.In red deer (Cervus elaphus), the dark ventral patch has recently been described asa male chemical signal involved in intrasexual competition. Morphological special-izations of the hair of this area might contribute to retaining the volatile com-pounds found here. In this study, we examined differences in the ultrastructurebetween hair associated with the dark ventral patch and hairs from the dorsolateralregion of the body as a control. We obtained a gallery of images from a scanningelectron microscope to study the possible variation in the detailed anatomy as wellas the surface and pattern of cuticular scales of hairs of the two body regionsexamined. In addition, we used a 2D-3D microscope to measure hair diameter(thickness) and the shape and size of the cuticular scales. We found that the hairsof the dark ventral patch were narrower than those from the dorsolateral region.We also found a different cuticular scale pattern of the dark ventral patch hairs,suggesting a possible specialization for the retention of compounds associated withthis chemical signal. Moreover, some intersexual differences in hair morphologyalso support this idea. This study shows, for the rst time, the differentiation ofhairs related to the dark ventral patch, which contributes to our better understand-ing of this chemical communication in red deer

http://doi.org/10.1111/jzo.12833

Carranza, J., Pérez-Barbería, J., Mateos, C., Alarcos, S., Torres-Porras, J., Pérez-González, J., Sánchez-Prieto, C.B., Valencia, J., Castillo, L., de la Peña, E., Barja, I., Seoane, J.M., Reglero, M.M., Flores, A., Membrillo, A. (2020) Social environment modulates investment in sex trait versus lifespan: red deer produce bigger antlers when facing more rivalry. Scientific Reports 10:9234

Theory predicts that the plastic expression of sex-traits should be modulated not only by their production costs but also by the benefits derived from the presence of rivals and mates, yet there is a paucity of evidence for an adaptive response of sex-trait expression to social environment. We studied antler size, a costly and plastic sex trait, and tooth wear, a trait related to food intake and longevity, in over 4,000 male Iberian red deer (Cervus elaphus hispanicus) from 56 wild populations characterized by two contrasting management practices that affect male age structure and adult sex-ratio. As a consequence, these populations exhibit high and low levels of male-male competition for mating opportunities. We hypothesized that males under conditions of low intra-sexual competition would develop smaller antlers, after controlling for body size and age, than males under conditions of high intra-sexual competition, thus reducing energy demands (i.e. reducing intake and food comminution), and as a consequence, leading to less tooth wear and a concomitant longer potential lifespan. Our results supported these predictions. To reject possible uncontrolled factors that may have occurred in the wild populations, we carried out an experimental design on red deer in captivity, placing males in separate plots with females or with rival males during the period of antler growth. Males living with rivals grew larger antlers than males living in a female environment, which corroborates the results found in the wild populations. As far as we know, these results show, for the first time, the modulation of a sexual trait and its costs on longevity conditional upon the level of intra-sexual competition.

https://doi.org/10.1038/s41598-020-65578-w

Castillo, L., Del Río, L.m., Carranza, J., Mateos, C., Tejado, J.J., López, F. (2020) Ultrasound speed in red deer antlers: a non-invasive correlate of density and a potential index of relative quality.Animal Biodiversity and Conservation 43.2: 255-269.

Deer antlers can be used as an index of individual performance both in ecological and productive contexts. Their quality is often measured only by their biometrical features, such as size, asymmetry or weight. Mechanic characteristics cannot normally be measured without destroying the antler and hence losing the commercial value of the trophies. Here, we studied ultrasonic velocities, density, and tensile strength across various sections of cast antlers of Iberian red deer (Cervus elaphus hispanicus). We found that the speed value depended on the section of the antler and the propagation direction. For antler sections, velocities were lowest for mid–beam and highest for brow tine. Results were similar for density and indirect tensile strength, probably related to differences in functionality among antler sections. Density explained most of the variability of ultrasound–speed. The time elapsed from antler shed affected density more than ultrasound speed. The indirect tensile strength showed a non–linear, decelerating relationship with ultrasound speed. We discuss the applications of ultrasound speed as a non–invasive tool to measure density and physical properties of antlers and antler sections, and their potential use as an index of quality.

https://doi.org/10.32800/abc.2020.43.0255

Linares, O., Carranza, J., Soliño, M., Delibes-Mateos, M., Ferreras, P., Descalzo, E., & Martínez-Jauregui, M. (2020). Citizen science to monitor the distribution of the Egyptian mongoose in southern Spain: who provide the most reliable information?. European Journal of Wildlife Research, 66(4), 1-5.

The Egyptian mongoose (Herpestes ichneumon L.) is a medium-size carnivore widely distributed in Africa and in a small part of southern Europe, the Iberian Peninsula, where mongoose populations have recently expanded. The mongoose is relatively easily detectable because of its diurnal habits and because it is the only species of Herpestidae occurring in the Iberian Peninsula. Therefore, its distribution could be monitored through citizen science. In this sense, information provided by stakeholders that make frequent use of natural environments, including hunters, landowners, or wildlife rangers, would be potentially very valuable. Nevertheless, the accuracy of the information provided by these stakeholders as regards mongoose occurrence has never been tested. To do so, we compared mongoose occurrences gathered through field transects (i.e., 2-km walking surveys in which direct observations and indirect signs were recorded) carried out in 218 Andalusian municipalities during 2010–2015 with those obtained through questionnaires conducted in 2016 to hunters (n = 251), landowners (n = 116), and wildlife rangers (n = 133). We did not find any significant difference between mongoose distribution estimated by the reference method (i.e., field surveys) and by questionnaire to wildlife rangers. In contrast, mongoose occurrences reported by hunters and landowners were significantly correlated among them, but not with those collected in field transects (nor with those provided by the rangers). This suggests that a participatory network for monitoring mongoose distribution could rely on the information provided by wildlife rangers. Previous studies showed that hunters can provide useful information from less accessible areas like private estates where official data are not collected. In this sense, our results suggest that further effort is needed to incorporate hunters and landowners in a participatory network to monitor mongoose distribution, and this could include collaborative actions to promote their involvement in addition to increasing their skills in mongoose detection.

https://doi.org/10.1007/s10344-020-01408-8

de la Peña, E., Martín, J., Barja, I., Carranza, J. (2020)  Testosterone and the dark ventral patch of male red deer: the role of the social environment. Sci Nat 107, 18

The expression of male sexual traits, which is stimulated by testosterone, entails significant costs for individuals. Consequently, natural selection is expected to favour the modulation of sexual trait development according to the balance between its costs and benefits. The proportion of rivals in a population may affect this balance by increasing or decreasing the reproductive benefits associated with the development of sex traits. Here, we explore the relationship between testosterone level and sex trait size under two populational conditions of mate competition: fenced (i.e. high male-male competition; all male age groups are present) and unfenced (i.e. low competition; most males present are juveniles). Our model species is the Iberian red deer (Cervus elaphus hispanicus), and the sex trait is the dark ventral patch that males exhibit during the rutting season. Our results showed that the positive relationship between testosterone levels and the size of the dark ventral patch depends on the environmental level of male-male competition. Only in populations where the operational sex ratio was high (i.e. high proportion of rival males), individuals with high levels of testosterone developed the sex trait. Conversely, when mate competition was low, there was no significant relationship between testosterone level and trait size. This result reinforces the idea that the effect of testosterone in promoting the development of sex traits may be mediated by the intensity of mate competition in the population, as well as the role of sexual selection in the evolution of the dark ventral patch in red deer.

https://link.springer.com/article/10.1007%2Fs00114-020-01674-1

Pérez-Barbería, F.J., William Mayes, R., Giráldez, J., Sánchez-Pérez, D. (2020) Ericaceous species reduce methane emissions in sheep and red deer: Respiration chamber measurements and predictions at the scale of European heathlands. Science of The Total Enviroment  714,  136738

Despite the importance of atmospheric methane as a potent greenhouse gas and the significant contribution from ruminant enteric fermentation on methane emissions at a global scale, little effort has been made to consider the influence that different plant-based natural diets have on methane emissions in grazing systems. Heathland is an ericaceous dwarf-shrub-dominated habitat widespread across the northern hemisphere, in Europe, provides valuable ecosystem services in areas with poor soils, such as water flow regulation, land-based carbon skin, energy reservoir and habitat of key game species. We (i) measured methane emissions from red deer (Cervus elaphus) and sheep (Ovis aries) fed mixed diets of natural grass plus ericaceous species (either Calluna vulgaris or Vaccinium myrtillus) using open-circuit respiration chambers; and (ii) modelled the results to estimate methane emissions from red deer and sheep populations inhabiting heathland habitats across Europe under different scenarios of grass-based mixed diets with varying proportions of ericaceous species. Our results indicated that methane emissions per unit of digestible organic matter intake decreased as the proportion of ericaceous species in diet increased, but this relationship was complex because of the significant interaction between the proportion of ericaceous species in the diet and digestible organic matter intake. According to our estimates red deer and sheep populations across European heathlands produce 129.7 kt·y−1 methane (se = 1.79) based on a hypothetical grass-ericaceous species mixed diet containing 30% of ericaceous species; this is 0.5% of total methane emissions from human activity across Europe (24,755 kt·y−1), and a reduction in methane emissions of 63.8 kt·y−1 against the same deer and sheep populations, if assumed to consume a grass-only diet. We suggest the implementation of carbon credits as a measure to value the relevance of heathland systems to promote biodiversity and its potential contribution to reduce methane emissions in ruminant grazing systems.

https://doi.org/10.1016/j.scitotenv.2020.136738

Van Beeck Calkoen, S.T.S., Mühlbauer, L., Andrén, H., Apollonio, M., Balciauskasf, L., Belotti, E., Carranza, J.,  Cottam, J., Filli, F., Gatiso, T.T., Hetherington, D.,  Karamanlidis, A.A., Krofel, M., Kuehl, H.S., Linnell, J.D.C., Müller, J., Ozolinst, J., Premier, J., Ranc, N., Schmidt, K., Zlatanova, D., Bachmann, M., Fonseca, C., Lonescu, O., Nyman, M., Sprem, N., Sunde, P., Tannik, M., Heurich, M., (2020) Ungulate management in European national parks: Why a more integrated
European policy is needed. Journal of Environmental Management 260, 110068

1. Primary objectives of national parks usually include both, the protection of natural processes and species conservation. When these objectives conflict, as occurs because of the cascading effects of large mammals (i.e., ungulates and large carnivores) on lower trophic levels, park managers have to decide upon the appropriate management while considering various local circumstances.
2. To analyse if ungulate management strategies are in accordance with the objectives defined for protected areas, we assessed the current status of ungulate management across European national parks using the naturalness concept and identified the variables that influence the management.
3. We collected data on ungulate management from 209 European national parks in 29 countries by means of a large-scale questionnaire survey. Ungulate management in the parks was compared by creating two naturalness scores. The first score reflects ungulate and large carnivore species compositions, and the second evaluates human intervention on ungulate populations. We then tested whether the two naturalness score categories are influenced by the management objectives, park size, years since establishment, percentage of government-owned land, and human impact on the environment (human influence index) using two generalized additive mixed models.
4. In 67.9% of the national parks, wildlife is regulated by culling (40.2%) or hunting (10.5%) or both (17.2%). Artificial feeding occurred in 81.3% of the national parks and only 28.5% of the national parks had a non-intervention zone covering at least 75% of the area. Furthermore, ungulate management differed greatly among the different countries, likely because of differences in hunting traditions and cultural and political backgrounds. Ungulate management was also influenced by park size, human impact on the landscape, and national park objectives, but after removing these variables from the full model the reduced models only showed a small change in the deviance explained. In areas with higher anthropogenic pressure, wildlife diversity tended to be lower and a higher number of domesticated species tended to be present. Human intervention (culling and artificial feeding) was lower in smaller national parks and when park objectives followed those set by the International Union for the Conservation of Nature (IUCN).
5. Our study shows that many European national parks do not fulfil the aims of protected area management as set by IUCN guidelines. In contrast to the USA and Canada, Europe currently has no common ungulate management policy within national parks. This lack of a common policy together with differences in species composition, hunting traditions, and cultural or political context has led to differences in ungulate management among European countries. To fulfil the aims and objectives of national parks and to develop ungulate management strategies further, we highlight the importance of creating a more integrated European ungulate management policy to meet the aims of national parks.

Journal of Environmental Management; Ungulate management in European national parks Why a more integrated European policy is needed (1)

Pérez-González, J. &  Carranza, J. (2020) Offspring sired by subordinate red deer males under controlled conditions: did some females prefer not to mate with the alpha male? acta ethologica ISSN: 0873-9749 (Print) 1437-9546 (Online)

Both male-male competition and female choice are important forces in sexual selection that may act in concert. In red deer (Cervus elaphus), rutting activities related to male-male competition are highly conspicuous and have received most research attention. However, there is increasing evidence that females can gain by selecting mates. Due to the additive genetic benefits of a sire’s dominance rank, females may prefer them as mates, so that selection for male traits associated with dominance can be reinforced by female choice. On the other hand, recent evidence suggests that females might prefer male features not related to dominance and thus affect the distribution of mating outcomes. This predicts mating with less dominant males, but no study has so far investigated to which extent some females may do so when the dominant male is available. Here we use controlled captivity conditions to study whether females mate with subordinate males when dominant males are present. By means of parentage analyses conducted after genotyping the offspring, we found that dominant males did not sire all the offspring, the mean percentage of offspring sired by subordinate males being 13.03%. This result has consequences for the evolutionary reinforcement of components of sexual selection in red deer and might be used as a starting point for future studies on the red deer mating system and sexual selection.

https://link.springer.com/article/10.1007/s10211-020-00336-9

de la Peña, E., Martín, J., Barja, I., Pérez-Caballero, R., Acosta, I. & Carranza, J. (2020) The immune challenge of mating effort: steroid hormone profile, dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer Integrative Zoology 2020; 15: 262–275

Testosterone secretion may regulate the reproductive effort and the development of sexual traits, but it may also involve costs at the immunological and metabolic levels.  However, the evidence for this trade-off in wild populations is scarce. Similarly, cortisol also plays an important role in mediating the reproductive and immune functions. In this study, we analyzed whether the endoparasite burden relates to hormonal levels (fecal testosterone and cortisol metabolites) and/or morphological sexual traits (size of the dark ventral patch, a trait that indicates reproductive effort in males) in male Iberian red deer (Cervus elaphus hispanicus). For this purpose, we sampled male red deer harvested during hunting actions in two types of populations in southwestern Spain that differed in structure affecting the level of male-male competition for mates. We used coprological analyzes to estimate the parasite burden mainly of gastrointestinal and bronchopulmonary nematodes and of protozoa, and assessed testosterone and cortisol metabolite levels from fecal pellets. We found a positive relationship of host parasitation with both testosterone levels and the size of the dark ventral patch, but these relationships depended on the intensity of male-male competition in the population, being only found under the high-competition level. These results are discussed under the hypothesis of the testosterone immunocompetence handicap, suggesting a cost at the immunological level, and, therefore, higher susceptibility to parasite infection in males that make a greater reproductive effort. However, this effect seems to be modulated by the social environment (male-male competition) that might lead to different optima in testosterone production and sexual trait development

https://onlinelibrary.wiley.com/doi/abs/10.1111/1749-4877.12427

de la Peña, E., Martín, J. & Carranza, J. (2019) The intensity of male-male competition may affect chemical scent constituents in the dark ventral patch of male Iberian red deer. PLoS ONE 14(9), e0221980.

During the mating season, Iberian red deer males (Cervus elaphus hispanicus) present a large visible dark ventral area in their abdomen. This characteristic dark-haired area is formed by the impregnation of the hair with sprayed urine and gland secretions and contains volatile compounds that can be used in intraspecific communication. Here, we used gas chromatography-mass spectrometry (GC-MS) to describe the lipophilic chemicals from the dark ventral patch of males from different populations with different levels of intrasexual competition. Amongst all the compounds found, m-cresol, benzoic acid, cholesterol and 4hydroxy-benzenopropanoic acid were the most abundant. The proportions of these compounds varied with age as well as with the level of intra-sexual competition, independently of age. In particular, red deer males experiencing higher intra-sexual competition had lower proportions of aromatic compounds (especially m-cresol) but higher proportions of carboxylic acids on their dark bellies. Males in a high male-male competition situation, invest in volatile compounds that can reveal their age, dominance status and condition, and that, in addition, enhance this signal. On the contrary, males from low intra-sexual competition populations have chemical profiles more characteristic of young individuals. This research shows a first glance of how secretion of volatile compounds of male deer can be modulated due to the intensity of male-male competition in the population.

https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0221980