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.