Optimal prey for red fox cubs – an example of dual optimizing foraging strategy in foxes from a dynamic wetland habitat

The red fox (Vulpes vulpes) is the most abundant mesopredator in the Central-European region. Detailed knowledge about their feeding behavior is important both from ecological and wildlife management reasons. Food choices of foxes are poorly predictable in high-biodiversity marshlands. The main aim of our study was to sample parallel the main food-type abundances in the study area and analyze the diet of fox cubs and cohabiting adults across three years during the period of maternal dependence of the cubs. According to the optimal foraging theory, we predicted that the cubs’ diet would show higher energy content, would be more varied, and the individual prey species fed to the young would be larger. We analyzed the composition of adult fox and cub fecal samples collected separately around dens in a marshland of western Hungary, May 2014, 2017 and 2020, when the abundance values of main food sources differed. Rodents and waterfowl dominated the diet, but their relative occurrence in the samples showed yearly variations. We found that vixens follow a dual optimizing foraging strategy regarding their provisioning of the cubs and their own diet. Adult foxes optimized their diet according to the actual yearly abundances of their main food sources. Additionally, they preferred prey items that can be consumed at the site of capture (large carrion and small individual prey items). Cubs on the other hand were provisioned with optimal high-energy food, even if those in question became less abundant in that year. Vixens mostly fed to their young either larger rodents and waterfowl, or multiple small rodents at a time – these types of prey are both optimal for transportation as a single load. Providing optimal prey at an early age in a changing environment may contribute to the ecological success of the red fox.

Methods
For the assessment of the diet composition and feeding habits of the red fox, we collected 265 intact scat (fecal) samples in three years (Table 1), Y1 (year 1 – 2014), Y2 (year 2 – 2017), Y3 (year 3 – 2020). Scat samples of cubs and an additional 14 partly consumed prey remains were collected in the surroundings of inhabited dens with actual ongoing cub-rearing, within a distance of 3–5 m from one den with cubs per year.

We prepared and analyzed the fecal samples by means of a standard procedure (Jędrzejewska & Jędrzejewski, 1998). Samples were soaked in water, washed through a sieve (0.5 mm mesh) and dried. All prey remains were separated, and using a microscope, all feather, bone, teeth, hair, fish scales and seed remains were identified to the lowest possible taxonomic level by using key features (detailed by Lanszki et al., 2020) and our vertebrate, invertebrate and plant reference collections. Besides their identification, we also collected prey frequency data from the individual fecal samples. Small mammals have paired bone structures (e.g., lower jaws, femurs) that allow an assessment of the minimum number of individuals in a scat through the pairing of left and right-sided bones. Based on the processing, we detected a minimum of one individual per sample for each prey taxon.

赤狐（Vulpes vulpes）是中欧地区数量最为丰富的中型捕食者（mesopredator）。对其摄食行为的详细认知，无论从生态学还是野生动物管理角度均具有重要意义。在高生物多样性沼泽湿地中，赤狐的食物选择极难预测。本研究的核心目标为：同步采样研究区域内的主要食物类群丰度，并在幼崽依赖母兽的三年周期内，分别分析幼崽与同居成狐的食性。基于最优觅食理论（Optimal Foraging Theory），我们提出如下预测：幼崽的日粮将具备更高的能量密度、更为丰富的食物组成，且投喂给幼崽的单个猎物体型更大。我们对2014、2017及2020年5月间，匈牙利西部一片沼泽湿地中洞穴周边分别采集的成狐与幼崽粪便（scat）样本进行了分析，这三年间主要食物源的丰度存在显著差异。结果显示，啮齿类与水鸟在日粮中占主导地位，但二者在样本中的相对出现频率存在年际变化。我们发现，母狐在为幼崽投喂食物与自身觅食两方面，采取了双重最优觅食策略：成狐会根据当年主要食物源的实际丰度优化自身觅食策略，同时偏好可在捕获地点直接食用的猎物（大型腐肉与小型单个猎物）。与之相对，幼崽被投喂的均为最优高能量食物，即便这类食物在当年丰度有所下降。母狐主要为幼崽投喂体型较大的啮齿类与水鸟，或是一次性投喂多只小型啮齿类——这类猎物作为单次运载的最优载荷均十分合适。在多变的环境中，早期为幼崽提供最优猎物或许有助于赤狐的生态成功。

研究方法
为评估赤狐的食性组成与摄食习性，我们在三年间共采集到265份完整的粪便样本（表1），分别为Y1（第1年——2014年）、Y2（第2年——2017年）、Y3（第3年——2020年）。每年我们均在存在幼崽抚育行为的栖息洞穴周边3~5米范围内，采集幼崽的粪便样本以及额外14份部分被食用的猎物残骸。

我们采用标准流程处理并分析粪便样本（Jędrzejewska & Jędrzejewski, 1998）：将样本浸泡于清水中，经0.5毫米孔径的筛网冲洗后烘干。分离所有猎物残骸后，借助显微镜，通过关键分类特征（详细方法见Lanszki等，2020）以及我们的脊椎动物、无脊椎动物与植物标本馆藏，将所有羽毛、骨骼、牙齿、毛发、鱼鳞与植物种子残骸鉴定至尽可能低的分类学级别。除完成物种鉴定外，我们还从单份粪便样本中收集了猎物出现频率数据。小型哺乳动物具有成对的骨骼结构（如下颌骨、股骨），通过配对左右两侧骨骼可评估单份粪便中的最小个体数。经样本处理后，我们在每份样本中为每个猎物类群检测到至少1个个体。