Experimental habitat fragmentation disrupts host-parasite interaction over decades via life-cycle bottlenecks

Habitat loss and fragmentation are likely to seriously impact parasites, a
less studied but critical component of ecosystems, yet we lack long-term
experimental evidence. Parasites structure communities, increase
connectivity in food webs, and account for a large proportion of an
ecosystem’s total biomass. Food web models predict that parasites with
multiple obligate hosts are at greater risk of extinction because the
local extinction, or reduction in abundance, of any host will result in a
life-cycle bottleneck for the parasite. We examine the response of a
parasite and its multiple hosts to forest fragmentation over 26 years in
the Wog Wog Habitat Fragmentation Experiment in southeastern Australia.
The parasite is the nematode Hedruris wogwogensis, its intermediate host
is the amphipod, Arcitalitrus sylvaticus, and its definitive host is the
skink, Lampropholis guichenoti. In the first decade after fragmentation,
nematodes completely disappeared from the matrix (plantation forestry) and
all but disappeared from their definitive host (skinks) in fragments, and
by the third decade after fragmentation had not appreciably recovered
anywhere in the fragmented landscape compared to continuous forest. The
low prevalence of the nematode in the fragmented landscape was associated
with the low abundance of one or the other host in different decades: low
abundance of the intermediate host (amphipod) in the first decade and low
abundance of the definitive host (skink) in the third decade. In turn, the
low abundance of each host was associated with changes to the abiotic
environment over time due largely to the dynamically changing matrix as
the plantation trees grew. Our study provides rare long-term experimental
evidence of how disturbance can cause local extinction in parasites with
life cycles dependent on more than one host species through population
bottlenecks at any life stage. Mismatches in the abundance of multiple
hosts over time are likely to be common following disturbance, thus
causing parasites with complex life cycles to be particularly susceptible
to habitat fragmentation and other disturbances. The integrity of food
webs, communities, and ecosystems in fragmented landscapes may be more
compromised than presently appreciated due to the sensitivity of parasites
to habitat fragmentation.