Effects of intraspecific competition and body mass on diet specialisation in a mammalian scavenger

1. Animals that rely extensively on scavenging rather than hunting must exploit resources that are inherently patchy, dangerous, or subject to competition. Though it may be expected that scavenging species should therefore form opportunistic feeding habits in order to survive, a broad population diet may mask specialisation occurring at an individual level.

2. To test this, we used stable isotope analysis to analyse the degree of specialisation in the diet of the Tasmanian devil, one of few mammalian species to develop adaptations for scavenging.

3. We found that the majority of individuals were dietary specialists, indicating that they fed within a narrow trophic niche despite their varied diet as a population.

4. Even in competitive populations, only small individuals could be classified as true trophic generalists; larger animals in those populations were trophic specialists. In populations with reduced levels of competition, all individuals were capable of being trophic specialists.

5. Heavier individuals showed a greater degree of trophic specialisation, suggesting either that mass is an important driver of diet choice or that trophic specialisation is an efficient foraging strategy allowing greater mass gain.

6. Devils may be unique among scavenging mammals in the extent to which they can specialise their diets, having been released from the competitive pressure of larger carnivores.

Methods
Using bulk stable isotope analysis, we aimed first to test our hypothesis that individual Tasmanian devils are capable of dietary specialisation in both trophic level (detected via stable-nitrogen isotope values) and feeding area (detected via stable-carbon isotope values), despite feeding broadly as a population. Second, we tested whether the degree of specialisation varied with inherent characteristics (sex, age, and size) or environmental effects (site and intraspecific competition level).

Whisker sample collection

We sampled 71 individual devils between 1st August and 4th October 2018, captured overnight in custom-made PVC pipe traps, across seven study sites in north-western Tasmania. Sex, mass, and head width were recorded, and age was assessed based on the extent of canine eruption and other markers modified from Pemberton (1990). The longest posterior mystacial whisker (A - F) was collected by cutting as close to the skin as possible with scissors, and its position was recorded. Two study sites (Dip River and New Haven) were classified as having lowered intraspecific competition, following severe population decline in 2013 and 2014, respectively, after the introduction of Devil Facial Tumour Disease (DFTD) (C. Hughes, unpublished data). All other sites were classified as having normal competition.

Whisker preparation

Each whisker was measured to the nearest 0.5 mm and an estimated intradermal length was added to calculate its estimated total length (M. Attard, unpublished data). The amount of time each whisker represented was then modelled based on a discrete von Bertalanffy equation (von Bertalanffy 1957; Hall-Aspland et al. 2005; T.L. Rogers et al. 2016) so that the whiskers could be sectioned into lengths representing a period of a few days. Whiskers were cleaned to remove lipids and other debris by washing once in ultrapure water and twice in a 2:1 chloroform:methanol solution for 20 mins each. Three segments of each whisker weighing between 0.2 and 0.5 mg (mean = 0.32 ± 0.08 mg) were cut and placed in tin capsules for analysis. Each isotope segment (n = 213) represented approximately 2.7 ± 1.5 days of growth (and thus assimilated diet), falling between 19th May and 1st September 2018. A buffer section of approximately 11.3 ± 2.2 days of growth was also cut between each isotope segment, ensuring a greater degree of independence between samples. In total, the three analysed segments represented approximately one month of isotope data.

Potential food item collection and preparation

Potential Tasmanian devil food items were opportunistically collected, usually as roadkill, from study sites and the rural areas surrounding Smithton, Irishtown, Roger River, and Montagu between 2016 and 2019 and frozen at -20°C. A feather from each bird was collected and soaked once in ultrapure water and twice in a 2:1 chloroform:methanol solution for 20 minutes each. Two samples of the rachis weighing between 0.2 and 0.5 mg were cut and placed into tin capsules for analysis. A sample of muscle tissue (usually from the thigh or torso) was cut from each mammal and snake, rinsed thoroughly twice in ultrapure water, and left to air dry. The outer edges of the muscle sample were then cut using a scalpel to remove as much potentially contaminated tissue as possible. Invertebrates were cleaned by rinsing twice thoroughly in ultrapure water and analysed whole. Mammal, snake, and invertebrate samples were then placed in a freeze-dryer (Alpha 1-4 LSCbasic, CHRIST) for at least 12 hours and ground into a powder using an oscillating mill (MM 200, Retsch). Two samples of powder weighing between 0.2 and 0.5 mg from each individual were taken and placed into tin capsules for analysis.

Stable isotope analysis

All whisker and food item samples were combusted in an elemental analyser (Flash 2000 Organic Elemental Analyser, Thermo Scientific) and the nitrogen and carbon isotope ratios (δ15N and δ13C) were determined using a continuous flow isotope ratio mass spectrometer (Delta V Advantage, Thermo Scientific) at the Bioanalytical Mass Spectrometry Facility, University of New South Wales, Australia. Isotope ratios are expressed using standard delta notation as parts per thousand (‰) and corrected to atmospheric N2 (Air) for δ15N and Vienna Pee Dee Belemnite (VPDB) for δ13C values (Bond and Hobson 2012). Instrument drift and measurement error were corrected using international standards USGS40 (δ15NAIR = -4.52 ± 0.06‰; δ13CVPDB-LSVEC = -26.39 ± 0.04‰) and USGS41a (δ15NAIR = 47.55 ± 0.15‰; δ13CVPDB-LSVEC = 36.55 ± 0.08‰) (Qi et al. 2003; Qi et al. 2016).

Specialisation

Nitrogen and carbon specialisation indices (NSI and CSI) were calculated for each devil to describe the variance in δ15N and δ13C values over a one-month period (Roughgarden 1972). The degree of specialisation was calculated using the equation:

where SI is the specialisation index; INW is the individual niche width, the variance of isotopic values along the whisker; and BINW is the between-individual niche width, the total variance of isotopic values within the sampled population. BINW was calculated for the total population across all seven study sites as these sites are not discrete, with individuals frequently traveling between neighbouring sites (C. Hughes, unpublished data). Individuals that occupied over 50% of the total niche width (TNW = INW + BINW) were classified as nitrogen or carbon generalists (SI > 0.5), while those restricted to less than 20% of the total niche width were classified as specialists (SI < 0.2), based upon conventions introduced in the southern elephant seal (Hückstädt et al. 2011). Individuals with a specialisation index between 0.2 and 0.5 were classified as intermediates.