Impact of Phytophthora-dieback on birds in Banksia woodlands in south west Western Australia

Highlights

• We investigate how Phytophthora cinnamomi affects vegetation and bird communities.

• Diseased sites had reduced plant richness, cover at all strata and flowering.

• Bird community composition differed significantly between diseased and healthy sites.

• Average species richness and nectarivore abundance was lower in diseased sites.

• P. cinnamomi is a threat to birds by reducing canopy cover and nectar availability.

Abstract

Invasive plant pathogens have impacted forest and woodland systems globally and can negatively impact biodiversity. The soil-borne plant pathogen Phytophthora cinnamomi is listed as one of the world’s worst invasive species and alters plant community composition and habitat structure. Few studies have examined how these Phytophthora-induced habitat changes affect faunal communities. We examined bird communities in Banksia woodland with, and without, Phytophthora dieback in a biodiversity hotspot, southwestern Australia. Seven sites along dieback fronts, with paired 1-ha plots in diseased and healthy vegetation, were surveyed monthly for birds over seven months. Vegetation assessments showed that diseased sites had reduced plant species richness, litter, shrub, tree and canopy cover, high bare ground and significantly lower flowering scores, than healthy sites. Bird community composition differed significantly between diseased and healthy sites, although total bird abundance, total species richness and foraging guilds, did not. Average species richness of birds per survey and the abundance of brown honeyeaters, western spinebills and silvereyes was lower in diseased than healthy sites. The tawny-crowned honeyeater had higher abundances in diseased sites. Similarity matrices of habitat structure, flowering scores and bird assemblages were congruent, indicating that habitat structural differences were influencing bird community composition. Our results suggest that this pathogen is potentially a serious threat to avian biodiversity and especially for nectarivores, and populations in fragmented landscapes. Since elimination of the pathogen is not currently possible, management should focus on methods of preventing its spread until techniques to eliminate the pathogen are developed.

Introduction

Invasive species have the ability to rapidly transform community composition and ecosystem-level processes (Vitousek et al., 1997). Invasive plant pathogens have impacted many forest and woodland communities at regional scales, resulting in major alterations to ecosystem structure, plant community diversity, plant productivity and vegetation structure and floristics (Castello et al., 1995, Mack et al., 2000). Some of the structural and floristic changes wrought by invasive plant pathogens include the loss of keystone or nectar-producing species, loss of canopy or overstorey cover and decreases in litter cover (Hansen, 2008, Smith et al., 2009, Tomback and Achuff, 2010). These structural and floristic changes are likely to influence faunal communities (Barringer et al., 2012, Mckinney et al., 2009), but the indirect effects of invasive plant pathogens on faunal communities remains poorly studied and poorly understood. Given the large scale over which invasive plant pathogens can infest areas (e.g. Lovett et al., 2006, Meentemeyer et al., 2004), such pathogens present a potential threat to many faunal communities, and hence global biodiversity, and there is an urgent need to evaluate, and better understand the indirect effects of invasive plant pathogens on faunal communities (Lovett et al., 2006, Monahan and Koenig, 2006).

Ecosystem structure and function can be permanently changed when keystone species are damaged, or removed by pathogens (Barringer et al., 2012, Lovett et al., 2006). The catastrophic ecological impacts on forests in North America, of the introduced chestnut blight fungus, Cryphonectria parasitica, are a well-known example (Rizzo et al., 2002). American chestnut trees, Castanea dentata, in eastern forests were all but eliminated following the swift extension of the pathogen in the early 1900s (Grunwald, 2012). More recently, the plant pathogen Phytophthora ramorum is responsible for causing the sudden oak death epidemic and decimating oak forests in the western United States (Grunwald, 2012, Rizzo et al., 2005). There is evidence that this pathogen has strong indirect impacts on vertebrate communities with models predicting negative impacts to the populations of several oak-dependent bird species (Monahan and Koenig, 2006).

A forest pathogen that is of great conservation threat to native and agricultural systems worldwide is Phytophthora cinnamomi, a soilborne water mould (Class Oomycetes) that is listed as one of the world’s 100 worst invasive alien species (Lowe et al., 2000, Hansen, 2008). The epidemic of P. cinnamomi ‘dieback’ (the process of an area becoming infested with P. cinnamomi) is a major concern in southern Europe (Brasier, 1996, Vettraino et al., 2002), USA (Mircetich et al., 1977), Mexico (Tainter et al., 2000), New Zealand (Podger and Newhook, 1971), South Africa (van Broembsen and Kruger, 1985) and Australia, where it is listed as a key threatening process (Cahill et al., 2008). The presence of P. cinnamomi dieback in a community is often highly visible with old diseased areas typically displaying reduced biomass and reduced structural complexity as a result of the death and subsequent disappearance of susceptible plant taxa (Shearer et al., 2007).

Although many studies have examined the effects of P. cinnamomi on vegetation, relatively few have examined its effects on fauna populations and communities (Cahill et al., 2008). The significant alterations to habitat and floristics associated with P. cinnamomi dieback have been predicted to substantially affect fauna through changes to important resources, such as food and nesting sites (Garkaklis et al., 2004, Wilson et al., 1994). Studies in southern Australia have tended to support these predictions, with declines in species richness and abundance of faunal communities recorded in areas with P. cinnamomi dieback (Armstrong and Nichols, 2000, Laidlaw and Wilson, 2006, Nichols and Bamford, 1985, Nichols and Burrows, 1985, Wilson et al., 1994), primarily due to changes in habitat structure. The negative effects of P. cinnamomi-induced floristic changes on faunal communities are likely to be significant given the wide range of plant species that are susceptible to P. cinnamomi (Garkaklis et al., 2004). Despite this, few studies have examined whether P. cinnamomi-induced changes to habitat affect faunal communities (but see Laidlaw and Wilson, 2006).

To address the questions of whether P. cinnamomi-induced changes to both habitat structure and floristics affect faunal communities, we examined the response of the bird community in Banksia woodlands to P. cinnamomi dieback. Banksia woodlands are low open woodlands with high species richness, confined to coastal and sub-coastal southern Australia, where the canopy is dominated by Banksia species and the understory contains many other proteaceous species (Bishop et al., 2010). These woodlands also support a diverse nectarivorous bird community (Newland and Wooller, 1985, Ramsey, 1989) that is predicted to be particularly susceptible to P. cinnamomi dieback (Cahill et al., 2008) because most major nectar-producing proteaceous plants are highly susceptible to P. cinnamomi (Shearer et al., 2007). We surveyed the bird community, and habitat structure, floristics and flowering to examine how P. cinnamomi dieback affected the bird community by asking the following questions: (1) Are there differences in bird community composition, the abundance of foraging guilds or individual species between Banksia woodlands with and without P. cinnamomi dieback? (2) Are any differences in the bird community related to alterations in habitat structure from P. cinnamomi dieback? and (3) Are any differences in the bird community related to dieback-induced changes in floristics and flowering?