The ‘spatial storage effect’. The missing link in the conservation of temperate woodland annual plant species?

Annual plants in temperate woodlands can make a substantial contribution to native plant biodiversity (~35%). They are probably disappearing before our eyes with barely anyone noticing. Local extinction in temperate ecosystems is occurring because ‘safe sites’ for germination are disappearing. Ground-dwelling animals that dig soils no longer exist across much of the range. Such diggings provide bare patches of soils for annuals to germinate on. Fire is rare in many fragmented woodlands. Fire removes litter and may also cue germination. The loss of safe sites because of fundamental changes in ecosystem disturbance regimes may deprive may species of the microhabitats they need to survive – scientists call this mechanism of species persistence the “spatial storage effect”. This study is a first in temperate Australia. We aim to improve the conservation management of native annuals by asking: (1) Are native annuals declining because their cues for germination have declined (due to loss of native digging animals, fire exclusion)? (2) Does modification of microsite patch-type (safe sites) effect germination and early seedling survival and growth of native annuals? (3) Have annuals disappeared altogether after decades of disturbance exclusion because seeds lying dormant in the soil have now disappeared?

Levenhookia dubia (Hairy Stylewort)

We can report that this project has made strong conceptual and practical advances in the field of spatial coexistence, particularly as this theoretical idea relates to conservation of annual plants. To summarise our findings:

1. over the life of our project, field floristic surveys conducted annually have confirmed that annual plant species, once known to occupy woodlands in our study area (and often times contributing up to ~35% of diversity), are now largely absent. There was inter-annual variation in abundance and composition of annual species in high quality woodlands – this is tied to variation in rainfall; as might be expected, there were more annuals in wetter years (2021) than in drier year. Hence, we find evidence that temporal coexistence is promoted by variation in rainfall. However, spatial coexistence is minimal in sites where disturbance has long been absent and, as a result, many species once encountered in woodlands were not seen at all.
2. assessments of patch-types for gemination (such as bare ground, leaf litter, moss cover) highlight how little bare ground is now present in fragmented woodlands. We hypothesised that bare ground is an important microsite to allow annual germination – and that this will be patchily distributed across years due to the digging activities of animals. The near absence of this patch type compromises successful recruitment and reduces fitness of annuals, potentially contributing to their decline.
3. soil seedbank studies confirm that annual species (the focus of our study) are largely absent from those sites that have remained undisturbed (by fire or digging animals) for long periods. Long periods equates to decades rather than years. Hence, coexistence is compromised when disturbance is eliminated, and annuals have seeds with a limited longevity or lifespan. This means that we cannot assume annual species can be recovered after indefinite periods without disturbance. Again, local extinctions in Red Gum woodlands have likely occurred, extinctions that are almost entirely impossible to confirm other than doing detailed work like we have done during this project. This gets back to our original question and motivation for the study: are annual species disappearing before our eyes, with no-one even noticing. We think to that question is a resounding yes.
4. re-introduction of disturbance, specifically soil digging, cannot recover annuals where they have been lost from the soil seed bank. Our field disturbance trials (where we disturbed soil vs removed vegetation without soil disturbance) provided little positive contribution to species coexistence by native annuals. What did respond were exotic annuals (mostly grasses) that have invaded grassy woodlands. These species are not dependent on bare ground for invasion – giving them a real advantage in ecosystems rarely disturbed. Hence, we believe the resilience thresholds of many annuals have now been exceeded.  Do we have to accept that this important contributor to local diversity has been lost and may never be recovered? We think the answer is yes.
5. re-introduction of disturbance, specifically fire, has just been implemented. We will be in a better position to now understand if fire cues germination of recalcitrant annual seeds i.e. the type of disturbance affects the likelihood of spatial coexistence.A new Honours student will help answer this question.

Siloxerus multiflorus (Small Wrinklewort)

In summary, we add to research that highlights the important feedbacks between disturbance agents, particularly animal diggings, and species coexistence. Animals create patchy opportunities for species to persist; their loss has removed an important mechanism to allow such persistence. Annuals have not been robust to long periods without disturbance and their recovery cannot rely on just the re-introduction of soil disturbance. It may require the reintroduction of propagules to targeted microsites. Success is not guaranteed given the dominance of exotic annual species. Our work is a cautionary tale: biodiversity declines are happening before our eyes, almost unnoticed, and may be very hard to reverse. Identifying landscapes where similar processes may play out, but have yet to do so, should be a priority for land managers and conservation biologists alike.