Introduction
In comparison to mainland habitats, islands often harbor significantly less vertebrate diversity . This is likely due to the difficulty of island colonization, which can necessitate crossing large expanses of water or being introduced by humans . The prevalence of insular mammalian carnivorans (Order Carnivora) is especially low due to factors such as large body size, low carrying capacity, reduced vagility, and high extinction rate, with reduced space and limited prey availability rendering niche differentiation difficult . It is therefore rare for two endemic mammalian carnivores to coexist on the same island.
Counter to these ecological patterns, Channel Island foxes (Urocyon littoralis santacruzae and U. l. santarosae ) and island spotted skunks (Spilogale gracilis amphiala ) coexist on two islands off the coast of southern California: Santa Cruz Island and Santa Rosa Island. Both mesocarnivore taxa are endemic to the Channel Islands, where they have coexisted alongside one another for at least 7,000 years . While island foxes are found on six of eight islands in the archipelago, island spotted skunks are only found on the two largest islands. Throughout their range, both species have undergone significant population fluctuations and currently exhibit low levels of genetic diversity, rendering them of particular conservation concern . These species are also of interest to population ecologists, as they serve as a rare example of mammalian carnivore coexistence in island habitats.
This coexistence occurs amid known competition between island foxes and island spotted skunks. For example, direct competition was observed in the early 1990s following the colonization of two invasive species to the Channel Islands . As populations of feral pigs increased, they served as abundant sources of prey that allowed golden eagles, an apex predator from the mainland, to colonize the archipelago. Golden eagles altered the trophic levels of the islands, turning the resident predators – namely, island foxes – into prey . This intense predation on island foxes changed the competitive hierarchy between the island’s endemic mesocarnivores by almost entirely removing island foxes from the ecosystem. In response, island spotted skunk numbers increased and they became more generalist in their diet and habitat use . The disruption of competitive dynamics between island foxes and island spotted skunks highlights the fragility of trophic structures within the Channel Islands. Additionally, the decrease in island fox populations and subsequent niche broadening of island spotted skunks demonstrates that foxes are likely the dominant competitor and that fine-scale niche partitioning enables coexistence between these two terrestrial carnivores .
Island foxes and island spotted skunks partition resources in numerous ways. While their niches overlap in habitat, temporal use, and diet, they maintain subtle, but important, distinctions. Regarding habitat, island foxes and island spotted skunks cohabitate within the coastal Mediterranean ecosystem on Santa Rosa and Santa Cruz Islands. Yet, island spotted skunks tend to be more specialized in their habitat use, while island foxes utilize all areas across the island . There may be further differences in microhabitat use, with island spotted skunks often found in areas with ground-level cover in the form of rugged terrain or dense vegetation . Regarding temporal dynamics, island spotted skunks are largely nocturnal, whereas island foxes are cathemeral (active during both the day and night; , with differing degrees of seasonality. Finally, island spotted skunks are strictly carnivorous while island foxes are largely omnivorous . Thus, island spotted skunks tend to be more specialist and island foxes more generalist along numerous ecological axes.
Another way to explore niche differentiation between island foxes and island spotted skunks is to consider the composition of their host-associated microbiomes. Microbiomes consist of all the internal and external bacterial taxa that have coevolved alongside their host . These bacteria function in modulating metabolism , responding to disease , aiding in digestion , mediating stress , and determining behavior . As such, characterizing the composition of host-associated microbiomes can provide an array of information about the host species. It can reflect host diet , health status , environmental context , behavior , and even evolutionary history ; Figure 1). While specific bacterial taxa often differ between host species, the functional role of bacteria is largely conserved among closely related hosts . For example, carnivores require different bacteria than herbivores to assist in digestion, but both ultimately help in the breakdown of food. Thus, the interplay between an organism’s phylogenetic history and external environment manifest in the bacterial composition of their microbiome . Through understanding these host-associated microbiomes, we can gain greater insights into the functioning of the whole organism, their evolutionary history, and how they fit within their broader ecosystem.
In the present study, we explored the role of gut microbial communities in niche differentiation between island foxes and island spotted skunks inhabiting Santa Cruz and Santa Rosa Islands. More specifically, we examined the relative contributions of evolutionary history (species) and environmental context (island) by comparing microbial variation across host species and island populations using 16S rRNA amplicon sequencing data. We predicted that the microbiomes of these two species would exhibit high-level similarity due to their shared phylogenetic ancestry as members of the suborder Caniformia within the mammalian order Carnivora , low levels of genetic diversity, and overlapping habitats across two islands. However, we also anticipated finer-scale specialization of microbes at lower taxonomic levels, following divergence of their ancestral lineages roughly 49 million years ago and more recent niche differentiation through subtle differences in diet, space use, and temporal activity patterns. Finally, we hypothesized that comparatively specialist island spotted skunks would exhibit lower microbial variation than more generalist island foxes, particularly in light of skunks’ smaller population sizes. Considered together, these results provide important insights into the unusual coexistence between these two insular mammalian carnivores. This not only broadens our understanding of the eco-evolutionary dynamics operating between hosts and their microbes in wild populations, but may further inform conservation monitoring and management of at-risk species and the symbionts they harbor.