Threatened stick-nest rats preferably consume invasive boxthorn over native vegetation on Australia’s Reevesby Island

doi:10.21203/rs.3.rs-1963287/v1

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Threatened stick-nest rats preferably consume invasive boxthorn over native vegetation on Australia’s Reevesby Island

https://doi.org/10.21203/rs.3.rs-1963287/v1

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Due to an abundance of feral predators on the mainland, native rodent species Leporillus conditor (greater stick-nest rats) live almost exclusively on small islands off the coast of South Australia. Many of these islands are heavily degraded novel ecosystems, overrun with African Boxthorn. African boxthorn (Lycium ferocissimum) is an aggressive invasive plant that negatively impacts biodiversity by outcompeting native vegetation and degrading habitat. However, it can also provide habitat and food sources for vulnerable native species. To understand if boxthorn is an important dietary component of the stick-nest rat, we used point-intercept vegetation surveys to estimate relative availability for each plant species in areas inhabited by stick-nest rats. We then collected faecal pellets from the study site and used micro-histological faecal analysis to measure plant use by the animals. This allowed us to calculate the “selection ratio” of plant use (abundance in faecal pellets)/plant availability. We found a strong preference of the stick-nest rat for the highly invasive African boxthorn, with a selection ratio of 4.397. This is valuable information as it suggests that other heavily degraded, African boxthorn-infested ecosystems have the potential to provide suitable habitat for the greater stick-nest rat. However, due to the potential of African boxthorn to continue to invade and inflict damage on the greater ecosystem, further research is crucial to ensure a context specific management plan that maximises the resilience of the greater stick-nest rat, as well as the other native species that rely on these island habitats.

Novel ecosystems are an ensemble of organisms that are both self-sustaining and without historical precedent (Hobbs et al. 2013). They develop naturally as a result of biotic or abiotic changes, such as climate change, dispersal events, and the merging of continents. However, humans have caused the development of novel ecosystems at an unprecedented and problematic rate, by changing both biotic conditions (by facilitating dispersal, land clearing), and abiotic conditions (such as hydrology, nutrient cycles, topography, and climate) (Hobbs et al. 2009). As novel ecosystems are defined by the presence of new (and usually invasive) organisms, they are synonymous with loss of biodiversity and reduced ecosystem value and function. This has certainly been the case in Australia (Carr 1993; Gross 1995; Dickman 1996; CABI 2022). However, due to the extent of environmental damage, some ecologists argue that traditional restoration ecology is not always possible (Hobbs et al. 2009). Introduced species may be necessary to supplement natural ecosystems in cases where functionally equivalent native organisms and processes have been permanently lost or broken, or to compensate for novel stressors.

The value of in-depth botanical analysis for animal conservation is often overlooked as traditional conservation practices emphasise historical continuity over ecosystem interactions. Such practices are problematic, however, as most ecosystems lack intact historic references for restoration and this uncertainty can lead land managers to reinforce gaps in ecosystem functionality (Hobbs et al. 2013). As a result, the reintroduction of locally extinct animal species to “restored” and managed ecosystems is often unsuccessful (Short et al. 2019). Conversely, there is substantial evidence that novel ecosystems, dominated by invasive plant species, can occasionally act as a suitable habitat for some of Australia’s most vulnerable species. A good example is the highly invasive blackberry, Rubus anglocandicans, which, in disturbed novel ecosystems, aids bandicoots and other small mammals by providing a functional equivalent to the vegetation structure present in intact native ecosystems (Packer et al. 2016).

Stick-nest rats (genus Leporillus) are an interesting case of a native Australian species surviving well in novel ecosystems. The greater stick-nest rat, Leporillus conditor (Sturt, 1848) has been translocated successfully and unsuccessfully multiple times, into both novel and restored ecosystems (Short et al. 2019). The two species of Leporillus went extinct on the Australian mainland soon after European colonisation, due to the introduction of feral predators, habitat degradation caused by livestock grazing, and competition with introduced herbivores (Copley 1999a). However, a single natural population of L. conditor was discovered on the Franklin Islands (32.454°S; 133.652°E), located in the Nuyt’s Archipelago off the west coast of Eyre Peninsula (Jones 1922), and was subsequently used as a source population for several translocation efforts, as part of the stick-nest rat recovery plan (Copley 1995). The success of this recovery plan resulted in the down-listing of this species’ conservation status from ‘Endangered’ in 1996 to ‘Vulnerable’ in 2008 to ‘Near Threatened’ in 2016, under the IUCN Red List of Threatened Species (Short et al. 2018). This outcome was due to the success of translocated populations on small islands (St Peter Island, and Reevesby Island) off the coast of South Australia, which are free from feral predators such as cats and foxes (Copley 1999).

Intriguingly, the successful translocation sites listed above are highly disturbed novel ecosystems (Robinson et al. 1996). The islands that host translocated populations of L. conditor are heavily infested by African boxthorn, Lycium ferocissimum (Robinson et al. 1996), which is classed as a Weed of National Significance, due to its invasiveness, potential for spread, and economic and environmental impacts (Noble et al. 2014). L. ferocissimum forms dense impenetrable thickets that block access to water points and provide shelter for invasive animals, such as rabbits and foxes. Additionally, its invasive nature allows it to encroach on the nesting sites of native birds and mammals and displace native plant species that provide essential ecosystem functions (CABI 2022). Because of this, it is known to interfere with seal breeding on beaches in the Recherche Archipelago (Gross 1995), Western Australia, as well as penguin breeding on Motunau Island in New Zealand (CABI 2022). However, despite the considerable costs of L. ferocissimum to Australian biodiversity, L. conditor clearly thrives in environments dominated by this species.

Unlike L. ferocissimum, L. conditor is not a “novel” addition to the ecological ensemble of Reevesby Island. A jaw bone attributed to L. conditor was found in 1980 (ten years before reintroduction) after a sand blowout, indicating there was once a natural population of L. conditor on the island (Pedler, Copley 1993). It is unknown when or how this population went extinct, however Dickman (1996) attributed it to the introduction of feral cats (Felis catus), in the 1830s. Reevesby Island became a conservation park in 1974, after 136 years of agricultural use. The feral cat population was eradicated in the 1980s to allow for the translocation of a L. conditor population in 1990. By this time, the island’s ecology was dramatically altered. Some native plant species that are known to have occurred with L. conditor, such as Myoporum insulare, Atriplex paludosa, and Threlkeldia diffusa, were recolonising the abandoned pastures (Robinson et al. 1996), but it is possible that others were permanently lost to grazing or competition. Native plants that remain on the island now grow in novel assemblages, where they must compete with L. ferocissimum.

Due to the high costs of invasive weeds to biodiversity and ecosystem value, it is important for land management that we understand how they are used and why some native animals thrive in their presence (e.g., Why are the invasive plants being used? Are they replacing a lost resource or compensating for a novel stressor? Is the invasive species the reason the equivalent native resource is lost or declining?). This is especially true of L. ferocissimum and its use by L. conditor, as more stick-nest rats now live in boxthorn-infested novel ecosystems than in intact native ecosystems (Short et al. 2019).

A valuable approach to understanding the use of invasive plant species by L. conditor is microhistological faecal analysis. This is an established technique for rodent diet analysis (McIntire 1989; McMurry et al. 1993; Castleberry et al. 2002; Bergstrom 2013; Newmaster et al. 2013; Soininen et al. 2013; Khanam et al. 2015), which relies on the identification of species-specific characteristics of plant cuticle in faecal samples. Cuticle is the waxy, non-cellular layer that conforms to the surface of a terrestrial leaf epidermis, protecting it from desiccation. While most leaf cells are denatured by the digestion process, much of the cuticle remains, still bearing the imprint of the leaf epidermis (Jones and Krockenberger 2007) which can be diagnostic for the plant material eaten. Microhistological faecal analysis is inexpensive and non-invasive to the animals. It has some minor risk of bias due to the differential digestion of plants with cuticles of different fragility (Norbury 1988; Jones, Krockenberger 2007). However, it provides incontrovertible positive evidence, and is generally considered to be a reliable technique for most plant species (Todd, Hansen 1973; Anthony, Smith 1974; Norbury 1988; Ellis et al. 1999; Khanam et al. 2015; Pareja et al. 2021).

In this study, we combine point intercept vegetation surveys with microhistological investigations of the degree to which L. ferocissimum is used by the Reevesby Island L. conditor population. This allows us to ask what proportions of native plants and L. ferocissimum are available in areas of L. conditor activity, and whether this availability is reflected in the feeding patterns of L. conditor and hence to understand the risks, and potential opportunities, of boxthorn infestation on this Vulnerable Australian native.

The study site for this research is located on the sand bar bridging the two southern lobes of Reevesby Island (34.534°S; 136.281°E), (Fig. 1), in the Sir Joseph Banks Group, South Australia, near the original homestead. It is defined as the area within a 200-metre radius of the homestead.

Field Design

We use the word “nest” to describe any bush (or dense vegetation cluster) that shows signs of frequent and sustained use or occupancy by L. conditor. These signs include: an abundance of faecal matter and multiple sets of fresh tracks, in addition to signs of gardening, such as the maintenance of an entrance and the construction and maintenance of “highways” (many sets of tracks, following a distinct path that has, in places, been carved, like a tunnel, through the branches of surrounding bushes). In order to gain an understanding of where L. conditor were living, we assessed the area within a 200-metre radius of our base camp and marked the coordinates of all the nests we found (Fig. 1). This methodology allowed us to rapidly identify the areas that L. conditor clearly favoured and the areas they clearly did not.

Vegetation Survey: Point intercept method

Vegetation surveys were necessary to understand what vegetation was available to L. conditor at Reevesby Island. An initial survey of the study site, described above, revealed that the distribution of plant species was not homogeneous and needed to be separated into vegetative communities, for effective sampling. We defined three key vegetative communities and a point intercept plot was created to sample each of them. The point intercept method used for this study is outlined in the Ausplots manual (White et al. 2012), however, due to patchy vegetation, we reduced the sampling intensity and the size of the plots, as outlined below.

Plot 1

When we mapped the nest coordinates, we found that they were highly centralised on a patch of vegetation sheltered in the sand dunes on the sand bar connecting the southernmost lobes of the island. Because of the high levels of L. conditor activity, we selected this patch of vegetation for plot 1. To do this, we placed the 50x50 metre plot over this patch of vegetation on Google Earth, using satellite imagery as a guide. We generated GPS points for each of plot’s four corners, then used pegs and 100-metre tapes to create a plot of six 50 metre transects, spaced ten metres apart, running in a north-south direction. The layout of Plot 1 is illustrated in the Appendix, (Graphs and tables, Fig. 1).

Plots 2 and 3 were 20x50 metres in size, and consisted of three parallel 50 metre transects, spaced ten metres apart. Plot 2 ran parallel with the beach in the north-south direction, on the eastern side of Plot 1, for the purpose of sampling Vegetation type 2. Plot 3 ran in an east-west direction, on the southern side of Plot 1, and was selected for the purpose of sampling Vegetation type 3.

Specimen samples

To identify plant cuticle in L. conditor faecal pellets, it was necessary to create a reference dataset of cuticle morphologies from plants found on Reevesby island. Plant vouchers for the reference data set were collected, labelled, and pressed according to the vouchering method described in Ausplots (White et al. 2012). Plants were identified using standard identification books (Saunders 2018), (Berkinshaw 2010), and a list of plant species on Reevesby Island generated using NatureMaps 3.0. Additional tissue samples for each plant species (leaves and stems, as well as fruits and/or flowers where available) were labelled and stored in vials at the University of Adelaide with 100% ethanol. Leaf and flower tissues were processed and made into slides using the protocol outlined in Storr (1961).

A minimum of ten faecal pellets were collected per nest. At each nest, fresh faecal pellets were collected using forceps, and labelled with the nest number and location. The first step was to wash faecal pellets in cold RO water to minimise contamination. The disaggregation process was to dissolve the faecal pellets in warm water (Pearson, Dodson 1993; McCarthy et al. 1996). However, this method proved ineffective for fresh faecal pellets, resulting in breakage of cuticle, as well as being slow and labour intensive. Instead, we developed a more reliable protocol that resembled the treatment of the reference cuticles, as follows: Faecal pellets were placed into labelled test tubes with a mixture of two parts 35% hydrogen peroxide (w/v) and one part 80% ethanol (v/v) at 90°C until the pellet dissolved. It was often necessary to use forceps to gently pull the pellet apart, breaking the mucus membrane coating. Any remaining aggregation, usually due to adhesion to mucous membrane, is easily dealt with using light water pressure and a small brush over a sieve. The remaining material is a mix of plant cuticle, seeds, small pieces of wood and bark, lignin coils, small rocks, and other plant material, such as mesophyll. This is then washed and stained using toluidine blue for one-two minutes and rinsed again. The dissolved scat is then placed in a petri dish to be manually cleaned and sorted under a dissecting microscope. Seeds and woody material were separated, labelled, and placed in long-term storage. Once cleaned and sorted, cuticle was transferred to a microscope slide, smoothed flat with a brush, covered with a glass coverslip, and inspected under a compound light microscope.

Plant cuticle from the scat material was prepared and identified under with reference to plant voucher slides. It was quantified by counting square millimetres of each species on each slide. This was then calculated into percentage values for further analysis (see section 2.7).

Microscope methods:

For this study we used an AX70 (Olympus, Australia) microscope with a UC50 (Olympus, Australia) camera attached, and CellSens (Olympus, Australia) image software. Any image stacking was done using Helicon Focus 7.6.4.

Statistics:

To understand the selective consumption of plants by L. conditor on Reevesby Island, we used Design I, described by Manly et al. (2003) as a statistical design for quantifying habitat use and availability at the population level. The resource selection function was computed using adehabitatHS version 0.3.14 package with design I data type (Calenge 2017) in the R computing environment 3.6.1 (R Development Core Team 2019).

Identification of cuticle

In order to be able to determine what plant species L. conditor were consuming, it was necessary to have a systematic method for comparing the fragments of cuticle in the faecal pellets with the reference cuticle, for identification. Due to the fragmented nature of the digested cuticle, we sought multiple identification characters to ensure that we identified as much of the cuticle as possible. The key identifiers used in this study were differential absorption of stain, unspecialised epidermal cells, stomata, subsidiary cells (Fig. 2) and trichomes (Fig. 3). The methods for identifying cuticle based on differential absorption of stain and unspecialised epidermal cells are outlined in Storr (1961), and Metcalfe and Chalk (1950), respectively. Stomata and subsidiary cells, and trichomes are illustrated below. We measured identifiers for each species and created an identification table for key plant species (table 1).

Table 1

Summary of Stomata and Trichome identification characteristics for key Reevesby Island species. All measurements recorded as µm.

A = abundant; SC = single celled; CG = capitate-glandular; PG = Pilate-glandular; MC = multicellular; UC = unicellular; SB = Salt bladder; V = vesicular

Plant species	Stomata (mature)			Trichomes
Plant species	Subsidiary cells	Guard cells	Size	Description	Base width	Head
Myoporum insulare	anisocytic	symmetrical	30	CG	50	90
Tetragonia implexicoma	anomocytic	symmetrical	30–40	UC, V, SB papillate	-	200 wide
Lycium ferocissimum	anomocytic	asymmetrical	40	unicseriate UC, A, cylindrical	20	240 long
Atriplex paludosa	unknown	symmetrical	30	unicseriate PG, MC	-	200 long
Enchylaena tomentosa	unknown	symmetrical	20–31	PG vesicular	20	80–100
Carpobrotus rossii	paracytic	symmetrical	50–60	none present/preserved
Salicornia quinqueflora	paracytic	symmetrical	20	none present/preserved
Senecio lautus	anomocytic	symmetrical	20–39	none present/preserved

Three vegetation types were present in the areas we surveyed. Each group contains a distinctive subset of plant species and exists in a specific set of abiotic conditions (Table 2). For the sake of simplicity, density is not a defining parameter, which means density gradients occur across the vegetation groups.

Vegetation type 1 is the least abundant within the study area. It is located where there is some protection from the strong ocean winds and salt spray. The dominant species are Myoporum insulare and Lycium ferocissimum (as medium to large bushes) and Muehlenbeckia gunnii and Tetragonia implexicoma (as ground cover and in the canopy as creepers/vines). Leporillus faecal pellets and tracks are a common occurrence within patches of this vegetation type, but rarely found outside of them.

Vegetation type 2 is the most prevalent in the study area, occupying the exposed dunes. It is defined by the dominance of Leucophyta brownii and Olearia axillaris (as low shrubs) and Spinifex hirsutus (tufty grass). There is a substantial variation in density within this group, however, dominant species remain a fixed parameter. Due to accessibility and time constraints this vegetation type was sampled in a low-density area.

Vegetation type 3 occupies low-lying salt and mud flats on the island in areas that are likely to become hypersaline due to inundation and subsequent evaporation of sea water. The dominant species are Salicornia quinqueflora (a small succulent shrub), Atriplex paludosa (marsh saltbush), Tetragonia implexicoma and Olearia axillaris.

Table 2

Summary of surveyed vegetation on Reevesby Island. Showing percentage of vegetation cover as informed by the point intercept survey.
Species	Plot 1	Plot 2	Plot 3	Total sampled vegetation
Atriplex paludosa	-	-	18.5%	6.2%
Carpobrotus rossii	3.5%	5.3%	-	2.9%
Dianella revoluta	1.5%	1.7%	2.2%	1.8%
Enchylaena tomentosa	0.9%	6.7%	10.9%	6.1%
Euphorbia paralias	-	7.0%	-	2.3%
Ficinia nodosa	1.2%	3.5%	-	1.6%
Leucophyta brownii	2.9%	30.2%	1.1%	11.4%
Lycium ferocissimum	13.5%	1.7%	-	5.1%
Muehlenbeckia gunnii	20.2%	1.7%	3.3%	8.4%
Myoporum insulare	15.8%	3.5%	10.9%	10.1%
Nitraria billardierei	0.3%	-	-	0.1%
Olearia axillaris	9.7%	12.3%	14.1%	12.0%
Rhagodia crassifolia	-	-	21.7%	7.2%
Salicornia quinqueflora	0.9%	-	17.4%	6.1%
Senecio lautus	3.5%	3.5%	-	2.3%
Spinifex hirsutus	1.5%	22.8%	-	8.1%
Tetragonia implexicoma	23.7%	-	-	7.9%
Threlkeldia diffusa	1.2%	-	-	0.4%

Vegetation availability in areas of L. conditor activity

Vegetation availability and use are shown in Fig. 4, and the selection ratio is presented in Fig. 5. L. ferocissimum is by far the most used resource, comprising 45.3% used material despite only representing 13.5% of the available vegetation in plot 1 and 5.1% of total sampled vegetation, as measured in the point intercept survey (Table 2). This gives it a selection ratio of 4.4 (Table 3).

Table 3

Outcome of Manly selection ratio design I
Species	Used	available	selection ratio	standard error	p-value
Atriplex paludosa	0.007	0.005	1.362	1.441	0.801
Carpobrotus rossii	0.013	0.011	1.192	0.896	0.83
Dianella revoluta	0	0.005	0	-	-
Enchylaena tomentosa	0.034	0.016	2.1	2.25	0.379
Ficinia nodosa	0	0.021	0	-	-
Leucophyta brownii	0	0.053	0	-	-
Lycium ferocissimum	0.517	0.118	4.397	0.89	0
Muehlenbeckia gunnii	0	0.342	0	-	-
Myoporum insulare	0.161	0.086	1.884	0.469	0.059
Olearia axillaris	0.235	0.075	3.139	0.825	0.01
Rhagodia crassifolia	0	0.011	0	-	-
Salicornia quinqueflora	0	0.005	0	-	-
Senecio lautus	0.013	0.059	0.217	0.086	0
Spinifex hirsutus	0	0.016	0	-	-
Tetragonia implexicoma	0.02	0.172	0.117	0.031	0
Threlkeldia diffusa	0	0.005	0	-	-

Table 4

**Summary of plant cuticle found in** Leporillus conditor **faecal material from Reevesby Island**.
Species	type	quantity mm²	percentage of total
Lycium ferocissimum	Leaf	353	28.2%
Lycium ferocissimum	Flower	215	17.2%
Lycium ferocissimum	total	568	45.4%
Olearia axillaris	Leaf	258	20.6%
Myoporum insulare	Leaf	177	14.1%
Salicornia quinqueflora	Leaf	153	12.2%
Enchylaena tomentosa	Leaf	37	3.0%
Tetragonia implexicoma	Leaf	22	1.8%
Carpobrotus rossii	Leaf	14	1.1%
Senecio lautus	Leaf	14	1.1%
Atriplex paludosa	Leaf	8	0.6%

Plant use

L. ferocissimum is by far the most used resource by Leporillus, comprising 45.4% of used material (Table 4) despite representing only 13.5% of the vegetation from plot 1 and 5.7% of total sampled vegetation (Table 3). Due to its abundant representation in the scat material, L. ferocissimum was broken into two subclasses based on cuticle type: “Leaf”, and “Flower”. Leaf cuticle comprised 62.2% of L. ferocissimum cuticle, and the remaining 37.9% can be attributed to flowers (Table 4).

Figure 5 and Table 2 show that Atriplex paludosa (marsh saltbush), Carpobrotus rossii (Australian pig face), L. ferocissimum, Enchylaena tomentosa (ruby saltbush), Olearia axillaris (coastal daisy-bush), and Myoporum insulare (native juniper) have selection ratios > 1. T. implexicoma and M. gunnii are the only species that seem to be selected against. They comprise 23.68% and 20.18% of the total available vegetation in plot 1, but only 1.75% and 0% of the used resources (Fig. 7). Of all the available species, these have the most fragile cuticle, and are the most susceptible to damage during digestion and lab processes. As such, it may be reasonable to class the “used” data for these species as missing, or incomplete. However, studies show that the effects of differential preservation are usually minor (Todd, Hansen 1973; Anthony, Smith 1974; Norbury 1988; Ellis et al. 1999; Khanam et al. 2015; Pareja et al. 2021) and, as the other plant cuticles are more robust, they are unlikely to be impacted by this secondary selective process.

The aim of this study was to understand the selective use of plants by Leporillus conditor on Reevesby Island. We found clear evidence of a reliance of L. conditor on the invasive Lycium ferocissimum (African boxthorn), which the animal appears to strongly preference over other native vegetation both in terms of habitat and food. In fact, L. ferocissimum represented only 13.45% of surveyed vegetation in plot 1, but accounted for 45.37% of faecal cuticle, meaning that L. conditor clearly seeks it out preferentially over the other species. Additionally, traces of L. conditor activity were most common within the vegetative community associated with L. ferocissimum. This confirms the hypothesis that L. conditor prefer L. ferocissimum over the available native vegetation on Reevesby Island. However, it is not clear if the selective use is driven by a dietary preference or if the dietary bias (represented in the faecal pellets) is a side-effect of habitat selection.

Fast-growing invasive bushes are known to increase the diversity and abundance of native mammals in degraded ecosystems. Packer et al. (2016) found that, in functionally intact native systems in the Mount Lofty Ranges, where native vegetation supports high levels of diversity, the presence or absence of Rubus anglocandicans (blackberry) led to no significant difference in abundance or diversity of mammals. However, in highly degraded systems within the same region, mammal abundance and diversity were directly correlated with blackberry dominance as it provides a multi-layered structure and dense understorey where native vegetation complexity has been lost (Packer et al. 2016). This has been shown to play a critical role in the persistence of faunal diversity at genetic, species and ecosystem levels (Li et al. 2014) (Kennedy et al. 2013; Li 2013). The same may be true of L. ferocissimum on Reevesby Island. Its thickets provide dense multi-layered vegetation structures. These structures prove ideal habitat for small mammals, such as L. conditor. However, on Reevesby island L. conditor appears to favour L. ferocissimum even where intact native understory and complex vegetation structures are available.

At the Arid Recovery native mammal re-introduction site in the arid region of northern South Australia (Moseby et al. 2011), L. conditor demonstrated a preference for low, dense shrubs as the base for nest sites (O’Neill 1999; Short et al. 2019), due to the protection they offer against predators, especially avian predators (O’Neil 1999; Copley 1988; Moseby 2019). While L. ferocissimum provides low, dense cover (Fig. 6), so do other plants that grow within the same microhabitat. In particular, Myoporum insulare (native juniper) and Olearia axillaris (coastal daisy-bush) are both widely available in Vegetation type 1. On their own, each of these plants likely provide less cover than L. ferocissimum, but in combination with other species, such as, T. implexicoma (bower spinach) and M. gunnii (coastal lignum) they can provide ample cover from avian predators (Fig. 7). M. insulare and O. axillaris have selection ratios > 1. However, these figures are calculated for plot 1. When the wider community is taken into account, the selection ratio for L. ferocissimum increases while it decreases for O. axillaris. This is because O. axillaris is widely distributed across the three vegetation types while stick-nest rat activity and African boxthorn are both centralised around plot 1, which indicates a strong relationship between the two species.

The preferential use of L. ferocissimum as a nest plant by stick-nest rats is consistent with observations by Copley (1999b), who carried out annual population surveys throughout the 1990s. He found that stick-nests were most numerous around the bases of L. ferocissimum bushes, and, when the population reached its peak in 1997, multiple stick platforms were evident amongst the higher branches of many of these bushes. (Copley 1999b; Short et al. 2019). Stick platforms in higher branches may be a strong sign of preference as raised shelters are likely to be more difficult to build and more exposed to the elements and avian predators, such as Tyto alba (barn owl) which is a known cause of Leporillus mortalities on Reevesby Island (see supplementary figure). There are also hints in the literature that stick-nest rats may favour L. ferocissimum on St Peter Island (32.277°S; 133.590°E). A 2006 survey of pitfall traps and Elliott traps at St Peter found that L. conditor were most abundant in localised patches of L. ferocissimum and Atriplex paludosa, despite this being a small minority of the island's vegetation (Stewart 1996; Copley 1999b; Short et al. 2019). However, these are primarily zoological/animal studies and detailed accounts of plants and plant use are not provided.

Stick-nest rats may favour L. ferocissimum bushes because the large thorns provide more protection from predators than the plants that are native to the animal’s offshore island refuges. This is the case at Low Head in Tasmania, where L. ferocissimum is a favoured nesting bush for little penguins, Eudyptula minor, as it provides better protection against cats and foxes than available native vegetation (Woehler et al. 2021). A preference for thorns and spines by L. conditor is supported by Short et al. (2018), who found that prickly Acacia tetragonophylla bushes were the primary nesting shrubs used by L. conditor at Heirisson Prong (Introduced in 1999, last sighting in 2007), in Shark Bay, Western Australia. While L. ferocissimum is not present at Heirisson Prong (Short et al. 2018), one of the researchers involved in the reintroduction described A. tetragonophylla as “prickliest dense shrub available in Shark Bay” and stated that it “proved quite useful for nest sites” (O'Neil 2020).

In North America, a preference for spiney plants is demonstrated by many species of Neotoma, a rodent which is ecologically very similar to Leporillus. This species which builds nests in the bases of prickly pear (Opuntia spp.) or cholla cactus (Cylindropuntia spp.) where they are protected from predators by the cactus spines (Vorhies, Taylor 1940; Macêdo, Mares 1988). It is possible that, on the mainland, species of Leporillus would behave similarly to Neotoma, and seek out thorns and spines where available. However, there is no clear evidence of this in the fossil record. A palaeobotanical analysis of 16 fossil Leporillus middens from White Range, in Central Australia, found Acacia aneura and unidentified Hakea species to be among the most consistently abundant taxa in the processed material (Webeck, Pearson 2005). Acacia aneura (Mulga Wattle) was also found to account for the bulk of the material in middens from the Young Range, along with unidentified Grevillea and Maireana species (Pearson, Dodson 1993). Acacia aneura does not have protective spines, and, as many, but not all species belonging to the genera Hakea, Grevillea, and Maireana have sharp leaves or spines, it is impossible to say if this is a factor. However, the dietary value of these plants is not in question. Acacia aneura is well known for its value as a food plant for many of Australia’s First Nations Peoples, and Hakea, and Grevillea both produce highly palatable, nectar rich flowers.

In comparatively natural or restored habitats such as the Franklin Islands and Arid Recovery, L. conditor’s diet consists almost entirely of the leaves and fruits of succulent plants, especially Enchylaena tomentosa (Ruby Saltbush), Rhagodia crassifolia, Nitraria billardierei, Carpobrotus rossii and Tetragonia implexicoma (Robinson et al. 1996; Copley 1999a; Ryan et al. 2003). These plants are all readily available on Reevesby Island, and there is evidence that many of them are eaten by stick-nest rats, only not with the same selective preference as L. ferocissimum. Ruby saltbush, which has a selection ratio of 2.10, was present in faecal pellets collected from nests where the plant was not recorded. This indicates that it is actively selected as part of L. conditor’s diet. This is consistent with Moseby (2019) and Ryan et al. (2012), who both cite it as a dietary favourite. It is possible that this selection ratio would be higher if we had included seeds in the analysis to account for fruit eating.

A preference for flowers could go some way to explain the selective use of L. ferocissimum by stick-nest rats, as 37.85% of L. ferocissimum material present in faecal pellets came from flowers. In Australia, L. ferocissimum usually produces flowers and fruit in Summer, but it is capable of flowering at any time given sufficient moisture (Erkelenz 1993). The faecal pellets for this study were collected in the middle of the Winter, and flowers were abundant. We attempted to collect only fresh faecal pellets. However, it is not clear how long pellets last in this environment, and it is possible that older scats were rehydrated by the rain and were collected as they appeared fresh. Nevertheless, it is possible that results may be different (for all species) if scats are collected at other times of the year. L. ferocissimum fruit is likely to represent a significant food source, as the palatability of the fruit and subsequent consumption of seeds is a key dispersal method for the species. Further analysis of seeds from faecal pellets would be necessary to discern the value of L. ferocissimum berries for L. conditor on Reevesby Island. However, L. ferocissimum leaves alone represent 28.19% of the sampled faecal material, which still points towards higher consumption of this species than any other plant.

It is difficult to know if L. ferocissimum is replacing pre-disturbance structural complexity on Reevesby Island, as there is no historical reference for precolonial vegetation for this location. The Franklin Islands are the best reference for intact Leporillus island habitat, so that a study of the plant use on the entire surface of these islands would provide a better indication of how L. conditor use native coastal vegetation in the absence of boxthorn. It would also reveal if they relied on resources there that are absent or degraded on Reevesby Island. It is also worth noting that, although the Franklin Islands are the last remaining natural refuge, and there is evidence of a historic L. conditor population on Reevesby Island, small islands do not necessarily represent the preferred habitat for this species. Evidence of stick-nest rats using native vegetation for both food and nutrients suggests that L. conditor on Reevesby Island are unlikely to require boxthorn for their survival. However, it seems likely that, at the very least, boxthorn increases the carrying capacity of both Reevesby Island and St Peter Island, which may benefit population stability.

The clear preference of stick-nest rats (Leporillus conditor) for African boxthorn (Lycium ferocissimum) demonstrates that one of Australia’s most noxious weeds can support a vulnerable species of mammal. As with blackberry (Rubus anglocandicans), this may have important implications for faunal genetic diversity and population stability. It may necessitate changes to land management, including reduced boxthorn control on offshore islands that host stick-nest rat populations. However, more research is needed in order to understand the extent to which this invasive species supports stick-nest rats, and for what reasons. The most pertinent questions are: Are stick-nest rats using resources on East and West Franklin islands that are less available on the other islands? Could these resources be cultivated on Reevesby and St Peter Islands in place of boxthorn? Are ecosystems containing African boxthorn able to support larger, or more stable populations of stick-nest rats than natural island ecosystems? How are other native plants and animals that inhabit these islands being impacted by boxthorn? And how are these species interactions likely to be impacted by the changing climate? The answers promise to provide new perspectives on how conservation efforts can leverage the existence of weeds in novel ecosystems that are otherwise considered as degraded.

Acknowledgments

Australian Research Council Centre of Excellence for Australian Biodiversity and Heritage (CE170100015) and Future Fellowship FT180100634

VW was funded by the Australian Research Council Centre of Excellence for Australian Biodiversity and Heritage (CE170100015) and Future Fellowship FT180100634

Field volunteers: Baillie Trenwith, Holly Kraehe, Czes Klopotowski

Competing interests:

The authors declare no competing interests.

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Threatened stick-nest rats preferably consume invasive boxthorn over native vegetation on Australia’s Reevesby Island

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Introduction

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Vegetation Survey: Point intercept method

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Vegetation availability in areas of L. conditor activity

Plant use

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