UTILISATION OF SEED RESOURCES BY SMALL MAMMALS: A TWO-WAY INTERACTION

Transcription

1 UTILISATION OF SEED RESOURCES BY SMALL MAMMALS: A TWO-WAY INTERACTION David Elmouttie B.App.Sc (Hons) School of Natural Resource Sciences Queensland University of Technology Brisbane, Australia This dissertation is submitted as a requirement of the Doctor of Philosophy Degree 2009

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3 -_i - Abstract Within the Australian wet tropics bioregion, only hectares of once continuous rainforest habitat between Townsville and Cooktown now remains. While on the Atherton Tableland, only 4% of the rainforest that once occurred there remains today with remnant vegetation now forming a matrix of rainforest dispersed within agricultural land (sugarcane, banana, orchard crops, townships and pastoral land). Some biologists have suggested that remnants often support both faunal and floral communities that differ significantly from remaining continuous forest. Australian tropical forests possess a relatively high diversity of native small mammal species particularly rodents, which unlike larger mammalian and avian frugivores elsewhere, have been shown to be resilient to the effects of fragmentation, patch isolation and reduction in patch size. While small mammals often become the dominant mammalian frugivores, in terms of their relative abundance, the relationship that exists between habitat diversity and structure, and the impacts of small mammal foraging within fragmented habitat patches in Australia, is still poorly understood. The relationship between foraging behaviour and demography of two small mammal species, Rattus fuscipes and Melomys cervinipes, and food resources in fragmented rainforest sites, were investigated in the current study. Population densities of both species were strongly related with overall density of seed

4 -_ii - resources in all rainforest fragments. The distribution of both mammal species however, was found to be independent of the distribution of seed resources. Seed utilisation trials indicated that M.cervinipes and R.fuscipes had less impact on seed resources (extent of seed harvesting) than did other rainforest frugivores. Experimental feeding trials demonstrated that in 85% of fruit species tested, rodent feeding increased seed germination by a factor of 3.5 suggesting that in Australian tropical rainforest remnants, small mammals may play a significant role in enhancing germination of large seeded fruits. This study has emphasised the role of small mammals in tropical rainforest systems in north eastern Australia, in particular, the role that they play within isolated forest fragments where larger frugivorous species may be absent.

5 -_iii - Contents Abstract... i List of Figures... vi List of Tables... ix Statement of Original Authorship... xi Acknowledgments... xii 1. Utilisation of seed resources by small mammals A two way interaction Introduction Habitat fragmentation in tropical systems Current Management of Australian tropical forests Conservation strategies The role of rodents in forest dynamics Seed dispersal and predation Potential positive effects of seed dispersal and predation Potential negative effects of seed dispersal and predation The role of rodents in Australian tropical rainforests Project aims and outcomes The influence of fine scale vegetation structure and floristics on the population structure and distribution of small mammals in isolated rainforest fragments Introduction Materials and methods Study sites Study species... 31

6 -_iv Sampling Methodology Vegetation structure and floristics Small mammal sampling Analysis Results Analysis of structural measures Floristic diversity Small mammal captures Discussion Flora and Fauna distribution and abundance Introduction Methods Resource sampling Small mammal sampling Movement data Analysis Results Resource distribution Small mammal distributions Resource availability and small mammal numbers Demographics and movement Discussion Resource utilisation feeding preferences by small mammals Introduction... 78

7 -_v Methods Analysis Results Discussion Seed germination Impacts of native rodent feeding behaviour on seed germination Introduction Methods Analysis Results ~ Significance of χ 2 statistic evaluated at p = Discussion General Discussion Rainforest fragmentation The interaction between flora and small mammals Management implications Research limitations Future research and conclusions References:

8 -_vi - List of Figures Figure 2.1: Study system. a) Location of three isolated rainforest sites on the Atherton Tableland in relation to the township of Malanda. b) photograph of site two, highlighting the difference between the matrix habitat and rainforest remnants...30 Figure 2.2a: Melomys cervinipes, The Fawn-footed Melomys...32 Figure 2.2b: Rattus fuscipes, The Bush Rat...32 Figure 2.3: Sampling grid design for forest fragments Figure 2.4: Actual stem density measures for each site by strata Figure 2.5: Species diversity per site as measured by the Renyi index Figure 2.6: The number of individuals captured per hectare over the entire study at each rainforest site for each species...43 Figure 2.7: The number of total captures per hectare over the entire study Figure 2.8: Mean recapture rates over the entire study at each rainforest site Figure 3.1: Seed catch design within rainforest patches...58 Figures 3.2: Yearly site resources levels in relation total rodent captures and total individual captures over two year sampling period...64

9 -_vii - Figures 3.3: Yearly site resources levels in relation total Melomys cervinipes individual captures and Rattus fuscipes individual captures over two year sampling period Figures 3.4: Seasonal KTBE resources levels in relation total captures of both rodent species over two year sampling period...65 Figure 3.5: Mean weights (± 1 S.E.) of Melomys captures at each habitat for each sex class..67 Figure 3.6: Mean weights (± 1 S.E.) of Rattus captures at each habitat for each sex class.. 68 Figure 4.1: Site design for seed exclosure experiment each site was divided into equal size segments numbering between trap position with exclosure and control areas located at the central peg position. Sites in these images are not drawn to scale...81 Figure 4.2: Orientation of seed catch in relation to exclosures...82 Figure 4.3: Total mean (± 1 SE) proportion of the remaining fruit and remaining seed within exclosures and controls for each site Figure 4.4: Mean monthly (± 1 SE) proportion of fruit and remaining seed within exclosures and control areas over each sampling period Figure 4.5: Difference in total mean proportion of untouched fruit and remaining seed within exclosures at each sample site..88

10 -_viii - Figure 5.1: Experimental set up for feeding trials..98 Figure 5.2: Mean germination rates of 20 fruit species across four treatments under standardised greenhouse conditions Figure 5.3: Mean germination rates of seed species in four seed type-size classes across four treatments under standard greenhouse conditions

11 -_ix - List of Tables Table 1.1: Examples of fragmented habitats across Australia...5 Table 1.2: Percentage of Australia s floral and faunal diversity located in the wet Tropics Bioregion..6 Table 1.3: Potential positive and negative effects associated with seed dispersal. Each process is further elaborated beneath table..13 Table 2.1: Mean actual stem densities and actual stem density differences between all rainforest sites...38 Table 2.2: Dispersion index values for actual stem density estimates at each site over three height classes using the Standardised Morisita index. 40 Table 2.3: Dispersion index estimates for individual captures and total captures of both M.cervinipes and R.fuscipes at each site using the Standardised Morisita index. 40 Table 2.4: Dispersion index values for ground cover estimates at each site over both height strata using the Standardised Morisita index 41 Table 2.5: Dispersion index estimates for individual captures and total captures of both M.cervinipes and R.fuscipes at each site using the Standardised Morisita index 45 Table 3.1: Dispersion index estimates calculated using the standardised Morisita Index for (KTBE) resources at each study site over a two year period..61

12 -_x - Table 3.2: Dispersion index estimates calculated using the standardised Morisita Index for (KTBE) resources quarterly at each site 61 Table 3.3: Dispersion index estimates calculated using the standardised Morisita Index for M. cervinipes, R.fuscipes and combined total individual captures at each study site over a two year period..62 Table 3.4: Dispersion index estimates calculating using the standardised Morisita Index for M.cervinipes, R.fuscipes and Combined total individual captures at each study site over a two year period 63 Table 3.5: Dispersion index estimates calculated using the standardised Morisita index for quarterly total captures at each site 63 Table 3.6: Proportion of male captures for each sample site through the study period 66 Table 3.7: Average distances moved by individuals (in meters ± 1 S.E.) from February 2003 to November 2003 at each sampling site.69 Table 5.1: Mean percent germination and significance (χ 2 p=0.05) for each fruit species, fruit type/size category and treatment 103

13 -_xi - Statement of Original Authorship The work contained in this thesis has not been previously submitted for a degree or diploma at any other higher education institution. To the best of my knowledge and belief, this thesis contains no material previously published or written by another person except where due reference is made. Signed. Date.

14 -_xii - Acknowledgments This project would not have been possible without the generous assistance of many people. I would like to thank: The Beatties, Williams and Lorenson families, for generously allowing fieldwork to be conducted on their property during the study. The numerous people who helped in the field, Kerrilee Horskins, Dave Hurwood, Samie Maynard, Jo Chambers, Martine Andreaansen and Applied ecology students ( ) and many many more. A special thanks to Craig Streatfeild, I had a ball doing my field work with you mate, thanks for all the memories, fun times and hard work I owe you! The staff at Queensland Parks and Wildlife Services (Lake Eacham, Cairns and Townsville, particularly, all the staff in the lake Eacham nursery and Michelle Nissen for permit assistance. Another special thanks must go to Nigel Tucker, your help in the field was invaluable as was your friendship, I would have had no hope completing without you mate. To my supervisors, John Wilson, Peter Mather and Ian Williamson for their friendship and ongoing assistance, in the design, analysis and the write up stage of the project. Sorry it took so long, but I got there. John, thank you for all your help, from undergraduate to research projects through to postgraduate. You were

15 -_xiii - a great supervisor and a great mate. I could not have made it this far without you and you will not be forgotten. To the whole Ecology and NRS group, thank you for all the good times, help and laughs, I will miss it. To all my friends, thanks for all your support and assistance throughout the years, I hope there are plenty more fun years to come. And most importantly to my family, Nonna, Marc, Danny, Miranda, Jordan, Joshua and most importantly Mum and Dad. Danny, fratello mio, grazie per le tante belle risate e per essere sempre stato tanto orgoglioso di me. Ti voglio bene e mi considero sempre il tuo "fratellino". Marc, Miranda, Jordan e Joshua, avete dato tanta gioia alla mia vita e vi voglio tanto bene. Marc, sei un secondo papa' per me, grazie per tutto il tuo aiuto e per l'esempio che mi hai sempre dato. Spero di divenire almeno in parte, come te. Mia bella Nonna, anche se non sei piu' qui' con noi, sei sempre nel mio cuore e nei miei pensieri. Grazie infinite per tutto quello che hai fatto e continui a fare per me. Ti voglio tanto bene. In special modo, mia bella mamma e caro papa', vi sono cosi' riconoscente e non ci sono parole che possano esprimere quanto siate importanti per me. Grazie per tutto cio' che avete fatto e sacrificato. Non avrei potuto avere genitori piu' cari e sarete per sempre i miei migliori amici. Vi voglio tanto bene. Thank you.

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17 Chapter 1. Introduction Utilisation of seed resources by small mammals A two way interaction 1.1 Introduction Ecosystems around the planet are constantly evolving, changing in structure, complexity and type. Changes to ecosystem composition result in ongoing alteration to both floral and faunal communities that, in turn, can change underlying ecosystem processes, including seed dispersal, seedling establishment and community structure. Historically, these changes have been driven by fluctuations in climatic conditions, severe climatic events (cyclones, floods) and other stochastic factors (Saunders et al. 1991) Since the expansion of the human population around the globe, habitat disturbance from human activities has impacted ecosystem function to a far greater extent than natural disturbance events. Impacts of human activities have occurred over very large geographical areas altering vast areas of land over relatively small time scales. Subsequent modification of habitats has lead to fragmentation of numerous habitats often to a state that is substantially different from pre-fragmentation conditions (Bennett 1990). Historically, this has lead to the creation of ecosystems that appear and function significantly differently to what existed previously.

18 Chapter 1. Introduction In recent years, a significant increase in the rate of habitat fragmentation has resulted from rapid expansion, colonisation and industrialisation by human population. Landscapes around the globe have been altered radically, in some instances, resulting in serious conservation and environmental issues. This rapid rate of human expansion and colonisation of new areas has lead not only to fragmentation and destruction of contiguous natural vegetation but also to creation of exotic habitat types that form a vegetation mosaic (Wilcove et al. 1986, Kozakiewicz 1993, Murcia 1995, Reino et al. 2009). The process is particularly evident in areas that have been heavily settled and utilised for construction of cities, industrial development, agriculture and rural centres. Habitat fragmentation not only alters landscapes by removing existing natural vegetation but also impacts remaining vegetation producing fragmented remnants. Many of the ecological processes that are vital for longevity of ecosystems are often substantially altered in habitat remnants (Saunders et al. 1991). This effect is compounded as remaining floral and faunal communities can be significantly impacted by changes in ecosystem structure and function. Species distributions, their relative abundance and composition are often influenced and modified in a manner that is rarely seen at the same level of scale during natural disturbance events (Saunders et al. 1991, Feeley and Terborgh 2008). Modification and frustration of ecological processes, including colonisation, succession, dispersal and invasion are often evident in fragmentated habitats

19 Chapter 1. Introduction (Bowers et al. 1996, Wiegand et al. 2005, Debuse et al. 2007). Changes in these processes impact both flora and fauna and can have a significant influence on long-term persistence of populations (Lindsay et al. 2008, Segelbacher et al. 2008). Individual species responses however, are difficult to predict and may be negative, positive or they may exhibit no effect to fragmentation (Laurance 1990, Laurance 1994, Bowers et al. 1996, Wiegand et al. 2005, Debuse et al. 2007). Individual species response to fragmentation will depend on environmental and habitat requirements and individual life history traits (Stearns 1992, Carvahlo et al. 2008). Size of remnant habitat patches and their relative degree of isolation can also have a significant influence on population persistence (Lindsay et al. 1998, Segelbacher et al. 2008). Typically, smaller more isolated remnants are likely to show lower probability of maintaining ecosystem function and quality (Saunders et al. 1991). Edge effects, exacerbated by a greater edge to area ratio in smaller fragments can have substantial impacts on habitat quality (Laurance and Yenson 1991). Abiotic factors (solar radiation, wind) influence soil chemical and physical characteristics (Saunder et al. 1991). Species may exhibit altered behaviours, particularly in their use of resources and space (Andreassen et. al. 1998), that in turn influences the interaction among species, eg., competition and predation (Hausmann 2004).

20 Chapter 1. Introduction Habitat fragmentation in tropical systems Every continent with the exception of Antarctica has seen significant modification as humans have expanded their distribution (Saunders et al. 1991). Globally, the extent of habitat fragmentation differs significantly, with specific habitats in particular areas having been impacted more severely than others (Saunders et al. 1991, Laurance 1991, Laurance and Gascon 1996). Habitats that are rich in economically important resources (i.e. mineral or timber resources), that provide fertile agricultural lands or that contain attributes that make them ideal for urban development (e.g. water, accessibility of land, aesthetic value), have been the habitats most significantly affected by fragmentation. Tropical areas across the planet in particular, have been significantly affected by habitat fragmentation due to favourable conditions for urbanisation, presence of fertile agricultural soils and presence of valuable timber and mineral resources. The Amazon basin in South America has seen ongoing clearing in modern times as agricultural development in the region has expanded and as of 2001, five million km 2 or 14% of this system had been cleared (Laurance 2001). Within the Australian wet tropics bioregion only hectares of once continuous rainforest habitat between Townsville and Cooktown remains to this day and it is now protected under World Heritage listing that was instigated in 1988 (Goosem and Tucker 1995). In Australia, habitat fragmentation has also occurred at a variety of spatial scales across many habitat types (Table 1.1), however the rate at which land has been

21 Chapter 1. Introduction cleared has occurred over a relatively short time period compared with other continents. The most significant clearing occurred post European settlement. Table 1.1: Examples of fragmented habitats across Australia Forest Type Total Area Percentage cleared Naringal, Vic Eucalypt 20000ha ~90% 1 Atherton and Evelyn Tableland - Qld Southern Wheatbelt WA 1 Bennet (1990) 2 Winter et al. (1987) 3 Saunders et al. (1993) Rainforest 79000ha ~96% 2 Eucalypt km 2 ~93% 3 Much of the continuous tropical rainforests of north eastern Australia were exposed to significant fragmentation during the early 1900 s as a consequence of pastoral and agricultural development. This is particularly evident on the Atherton Tableland, an area that contains multiple regional ecosystems of moist tropical highland rainforest and forms a significant component of the Wet Tropics Bioregion. Only 4% of the original rainforest areas remain today on the Atherton Tableland (Winter et al. 1987) with remnant patches now forming only a small proportion of a matrix of rainforest interspersed within agricultural land (sugarcane, banana, orchard crops, townships and pastoral land) (Winter et al. 1987, Goosem and Tucker 1995). 1.3 Current Management of Australian tropical forests In 1988, the Wet Tropics World Heritage area was established giving the area global recognition for its unique floral and faunal assemblages (Goosem and

22 Chapter 1. Introduction Tucker 1995). The significance of the Wet Tropics Bioregion cannot be overstated even though it encompasses less than % of moist tropical forest around the world and covers less than 0.1% of Australia s land surface area. This region constitutes one of the most diverse bioregions on the planet (Table 1.2)(Goosem and Tucker 1995). The flora and fauna of the Australian wet tropics is unique, with many animal and plant species found only in isolated localities across this region. Although the wet tropics bioregion is made up of moist tropical forest, many distinct ecosystems are present that function independently and that sustain unique and diverse communities of organisms. Table 1.2 illustrates the extent of Australia s floral and faunal diversity that is present within the wet tropics bioregion. Table 1.2: Percentage of Australia s floral and faunal diversity located in the wet Tropics Bioregion. Percentage of Australia s diversity Species of Flora and Fauna 65% Fern species 21% Cycad species 37% Conifer species 30% Orchid species 36% Mammal species 30% Marsupial species 58% Bat species 25% Rodent species 50% Bird species 25% Frog species 23% Reptile species 37% Freshwater fish species 60% Butterfly species (Source: Goosem and Tucker 1995)

23 Chapter 1. Introduction Although stringent legislation now exists to protect this bioregion, many regional ecosystems within the wet tropics are still classified as either threatened (< 10% remains) or endangered (< 2% remaining). Much of the vegetation that remains of the smaller less abundant forest types occur in small fragmented remnants on private, freehold, state government or commonwealth land. As a consequence of diverse ownership, management of the remaining natural ecosystems can often be substantially more difficult than management of relatively un-fragmented habitats in the region. On the rich basaltic soils of the Atherton Tableland there are numerous small rainforest patches ranging in size from hectares and these constitute the vast majority of the remaining moist tropical forest vegetation that once occurred widely across the region (Laurance 1991). Fragments are interspersed within a matrix of pastoral and agricultural land and many are significantly isolated from neighbouring similar vegetation fragments (Laurance 1991, Tucker and Murphy 1997). Remnants often support both faunal and floral communities that differ significantly from remaining continuous forests (Laurance 1990). Due to variation in size and structure, limitations on available resources and differences in other ecological factors (e.g. edge effects, floral and faunal population densities), remnants often do not maintain the same ecological appearance as larger forest stands (Saunders et al. 1991, Laurance 1994). This can lead to differences in ecological processes (e.g. seed dispersal) as the density and abundance of certain plant and animal species may be altered signficanly

24 Chapter 1. Introduction between fragments and continuous forests (Laurance 1994). It is therefore important to develop an understanding of the ecological processes that may differ within small rainforests remnant habitats and to determine what effect this will have on the long-term resilience of the whole system, as this has yet to be investigated. 1.4 Conservation strategies Conservation strategies have often focused on reanimating natural processes within fragmented systems (Tucker and Murphy 1997). Due to the extent of fragmentation, current land use and ownership of rainforest remnants in north eastern Queensland it is often difficult from an ecological perspective to manage and restore degraded sites. The goal of many of the restoration projects within the region is to where possible, reinstate natural communities so that faunal and floral diversity represents what was present in the pre-european era (Goosem and Tucker 1995, Tucker and Murphy 1997). To achieve this aim a number of management strategies have been employed on the Atherton Tableland: Current management strategies employed within fragmented ecosystems include: 1. Construction of wildlife corridors between remnant patches and sections of continuous forest. This strategy is aimed at assisting the movement of floral and faunal species between remnant vegetation and corridor vegetation and the practice also increases total available native vegetation when corridors are constructed,

25 Chapter 1. Introduction Creating stepping stones or smaller vegetation fragments across the landscape to reduce patch isolation and the distance between both fragments and continuous rainforest vegetation, to increase faunal and floral dispersal potential, 3. Increasing the size of vegetation remnants and continuous vegetation stands, this expands total resources and the overall amount of native vegetation within a given area. The restoration strategies described above are based on the concept that a positive outcome will be achieved by increasing available habitat or by restoring connections between habitats. Increased connectedness between forest fragments and continuous forest is expected to increase the degree of plant and animal dispersal among fragmented areas. Once initial conservation and restoration activities are implemented, systems are left to increase in complexity and structure naturally. The goal of this approach is that restored habitats should become self reliant and within a relatively short period of time will not be dependent on human intervention (e.g. re-seeding or weeding) as natural processes like seed dispersal will be reanimated. 1.5 The role of rodents in forest dynamics It is important therefore, that when non-continuous forest tracts (remnants) are incorporated into such strategies, that we first develop an understanding of the ecological processes in remnant forests. Many known seed vectors (Cassowaries, possum species) have been shown to be absent from small habitat

26 Chapter 1. Introduction remnants (Laurance 1994). If restoration strategies are to become self reliant, it is essential that we understand what impacts the lack of known seed vectors will have on the system and if alternate species still present in there may be able to facilitate similar processes. Small mammal species may play a significant role in persistence of Australian tropical rainforest fragments as their densities are known to be stable or even to show increases within fragmented systems (Laurance 1994). The relationship that exists however, between seed resources and small mammal activities within Australian tropical rainforests is an issue that has received little attention to date. Although small mammals have been shown to be significant predators and dispersers of seed in many other forest types (Castro et al. 1999, Williams et al. 2000, Bonjorne and Galetti 2007, Forget and Cuijpers 2008), little is known about small mammal foraging patterns, the extent of their seed utilisation or the positive or negative effects associated with mammal seed interactions in Australian rainforests. 1.6 Seed dispersal and predation The vast majority of Australian tropical rainforest seeds and fruits rely on animal vectors for their dispersal, as very few possess adaptations for either wind or water dispersal (Chambers and MacMahon 1994). Anecdotal observations have indicated that 70-80% of seeds, fruits and nuts within Australian rainforest depend solely on animal vectors for their dispersal. In a number of forest systems throughout the world small mammals, particularly rodents, have been identified as significant seed predators that can over utilise and destroy seeds

27 Chapter 1. Introduction rendering them non-viable (Castro et al. 1999, Hulme and Hunt, 1999, Williams et al. 2000). The level of seed utilisation by small rodents on Australian tropical rainforest fruits has not been determined, nor has the potential impact (positive or negative) of foraging on plant propagule dispersal and viability. The effectiveness of seed dispersal by animal vectors within a habitat will depend on a diverse array of potentially conflicting or synergistic processes including: plant species heterogeneity, the distribution of animal vectors, the foraging range of the disperser and the type of seeds that are to be dispersed. Small mammals as a result of their individual life history characteristics and the type of habitat that they utilise, often forage over limited ranges and therefore are unlikely to be major seed dispersing vectors at medium or large spatial scales. It is likely however, that at a local scale they have the potential to over utilise seed resources, harvesting a greater number of available plant propagules than are viable to maintain sustainable germination rates within the system (Castro et al. 1999, Hernandez 2007, Forget and Cuijpers 2008). If true, this has significant implications for regeneration in rainforest systems (Castro et al. 1999). Alternatively, foraging at the local scale has the potential to disperse seeds to areas where germination may be enhanced (Williams et al. 2000), by dispersing seeds to areas of favourable microclimate (Moore et al. 1998) or to areas where germination may be enhanced due to a reduction in competition (Janzen 1970, Connell 1971, McMurray et al. 1997).

28 Chapter 1. Introduction The extent of seed dispersal will also be affected by seed type and size. Rodents may select fruits based on specific seed traits (Zhang and Zhang 2008). Multiseeded and small seeded fruits possessing higher probability of survival after consumption by animals as individual seeds are unlikely to be masticated (Williams et al. 2000). Multi-seeded and small seeded fruits may retain potential to germinate even if they are only partially ingested. Large seeds may have greater probability of being destroyed when fruits are consumed, and this will lead to higher seed damage rates (Williams et al. 2000, Zhang and Zhang 2008). Large seeds and nuts however, have greater potential to be moved and cached, and as every cache is unlikely to be recovered, seeds and nuts from some caches that are not retrieved by rodent seed predators may germinate (McMurray et al. 1997). It is important for a study that aims to determine the impact of the interaction between small mammals and seed resources in rainforest habitats to first identify potential positive and negative effects associated with seed dispersal and seed predation by small mammals, the types of seeds available within the habitat and the structure and potential dispersal ranges of small mammal populations that occur within the system. In Table 1.3, potential impacts of seed dispersal and predation are identified. In is important to note that the importance of each potential process to the system is not equal and will occur at different stages of the seed life cycle. Each process may however influence seed germination and seedling establishment.

29 Chapter 1. Introduction Table 1.3: Potential positive and negative effects associated with seed dispersal and seed predation. Each process is elaborated in more detail below. Process Positive effects Negative effects Endozoochory May increase germination potential of seeds. May lead to the destruction of viable seeds. Seed dispersal Seeds dispersed to favourable areas Seeds dispersed to poor areas Caching Seeds may be dispersed to more suitable microhabitats (caches) that may increase the germination potential of the seeds. Seeds may be dispersed to areas where the microhabitat is not favourable (e.g. absence of mychorriza). Seed cropping General reduction in inter and intra specific competition due to seed cropping. Specific seeds resources may be over-cropped leading to local extinction of species. allelopathy Removal of seeds from under parent plant so as effects of parental allelopathy is reduced. Dispersal of seeds under trees where allelopathic chemicals are secreted may reduce propagule establishment Potential positive effects of seed dispersal and predation 1. Endozoochory is the processes of a seed being consumed by an animal, travelling through the digestive tract, leading to dispersal by defecation. Seed viability and regeneration potential of individual seeds is often enhanced by endozoochory, as abrasion or softening of the seed coat may be required for particular plant species to germinate. For example, mutualistic relationships have been found between mimetic seeds and large avian dispersers. Large terrestrial birds often swallow seeds that have exceptionally hard seed coats and some birds use seeds as grit to grind other foods within the gut (Foster and Delay 1998). This process in

30 Chapter 1. Introduction turn, abrades seed surfaces, enhancing seed germination potential after gut passage (Foster and Delay 1998). 2. Rodent foraging behaviour may increase the extent of seed dispersal across a patch leading to seeds being dispersed to areas within a habitat that are more favourable, increasing germination potential of seeds. Wright et al. (2000) found a positive correlation between the level of seed dispersal within a patch and the number of rodents present within the patch. Other small mammals, eg., Possums can disperse seeds over large areas without significantly lowering germination potential (Williams et al. 2000). 3. Caching or clumping of seeds can increase germination potential. Seeds of Indian ricegrass (Oryzopsis hymenoides) show higher germination rates when placed in scatter-hoards (McMurray et al. 1997). In this example, the percentage of seeds that germinated increased with the size of the hoard, with seeds not placed in a scatter hoard having a substantially lower germination rate. 4. Reduction of competition due to preferential cropping by dominant seed predator species can lead to a reduction in inter-specific competition and hence increase recruitment success by sub-dominant species. For example, rodents reduce germination rates of cheatgrass (an introduced weed in North America) when seeds are placed in a scatter-hoard

31 Chapter 1. Introduction (McMurray et al. 1997). Indian ricegrass (native species) thrive, within scatter hoards however, and have a competitive advantage over cheatgrass in environments that contain scatter-hoarding rodents (McMurray et al. 1997). 5. General reduction of inter and intra-specific competition via seed cropping. Studies by Belsky (1992) in grassland habitats and Bowers et al. (1997) in desert habitats showed that competition was significantly reduced as a result of seed cropping. This in turn lead to an increase in germination rates for remaining seed propagules leading to higher seedling establishment in environments where rodents were present (Belsky 1992, Bowers et al. 1997). 6. The release of sporophyte-derived thelypterins a type of allelochemicals that inhibit the growth of a seedling under the parent plant (Moore et al. 1998). Dispersal of seeds away from the parent plant therefore can increase germination rates. The Janzen (1970) and Connell (1971) hypothesis suggests that seedling establishment and development increases with distance from the parent plant, therefore dispersal should be beneficial to most plant species.

32 Chapter 1. Introduction Potential negative effects of seed dispersal and predation 1. Over-cropping of resources in general may reduce the overall number of available propagules within a patch. In Scots pine forests, rodents and birds have been shown to remove up to 96% of seeds that reach the ground and this has been implicated as a major factor that limits forest regeneration (Castro et al. 1999). 2. Over-cropping of a specific resource can change patch diversity. Within semi-natural woodlands in the U.K, rodents were shown to predate on both Ash (Fraxinus excelsior) and Wych elm (Ulmus glabra) seeds. A preference was shown however, for Wych elm seeds with nearly all seeds removed irrespective of their relative density and/or frequency, suggesting that rodent seed predators may have the potential to influence local plant extinctions (Hulme and Hunt 1999). 3. Endozoochory may also have a negative effect by reducing seed viability and germination potential. Soft seeds or seeds that do not remain viable after passage through an animal s digestive tract will suffer a reduction in germination potential post ingestion. Williams et al. (2000) found that seed predation by small rodents reduced germination potential significantly in 11 plant species. 4. Removal or relocation of viable seeds to non-suitable soil microhabitats can be an important mechanism for determining regeneration potential.

33 Chapter 1. Introduction Rodents within Neotropical forest have been shown to be significant seed dispersers. Many seeds are dispersed and/or hoarded and relocated subsequently, to areas where germination potential is significantly reduced (McMurray et al. 1997, Brewer and Rejmanek, 1999). Mycorrhize can play an important role in seedling establishment (Bowman and Panton 1993), therefore the dispersal of seeds to habitats in which favourable mycorrhize are absent can lead to low seedling establishment. 5. Allelopathic chemicals may reduce germination potential of dispersed seeds. Certain plant species reduce or inhibit the growth of other species via secretion of allopathic chemicals (Moore et al. 1998). In these cases, seeds that are dispersed away from the parent plants may not establish in areas where allopathic species occur. 1.8 The role of rodents in Australian tropical rainforests Australian tropical forests possess a relatively high diversity of native small mammal species particularly rodents (Table 1.2), that in general, unlike mammalian and avian seed frugivores elsewhere, have been shown to be resilient to the effects of habitat fragmentation, patch isolation and reduction in patch size (Laurance 1994). Small mammals also often become the dominant mammalian frugivores in terms of their relative abundance within fragmented forest patches in Australia (Laurance 1994). This change in faunal diversity has been suggested to result, in part, from the loss or decline of competitor and predator species

34 Chapter 1. Introduction including habitat specialists (Laurance 1990), co-evolved mutualists (Gilbert 1980) and species with larger area requirements (Terborgh 1974). The impact on faunal differences between rainforest fragments and continuous forests on processes such as seed dispersal and seed germination has yet to be quantified. Which animal species disperse and predate on seeds within forest fragments, the level of dispersal and predation and the impact this has on the longevity of forest fragments, needs to be determined. The impact that small mammals may have on seeds resources and forest fragments needs to be investigated as these species have been shown to be the dominant mammalian frugivores within Australian tropical rainforest fragments. It is important therefore, to develop a better understanding of the organism resource interactions that exist between small mammals, remnant vegetation and seed resources prior to implementation of any conservation and or restoration strategies in fragmented habitats. Understanding how rodents forage within fragmented tropical forest systems is an integral component to understanding the impacts and interactions that may occur between the system, seed resources and rodent species. Presented below are four possible mammal/seed interactions. The models presented are based on the same arbitrary area that is within the foraging range of an individual (eg. fragmented patch). The models do not represent all possible outcomes, rather stages through a continuum of possible behaviours.

35 Chapter 1. Introduction A single mammal population forages uniformly throughout the environment, leading to a homogeneous distribution of mammals. This leads to uniform utilisation of seed resources throughout the patch and a uniform distribution of dispersed seed. 2. Multiple local populations with isolated, discrete foraging ranges during resource rich periods and extended overlapping foraging ranges in resource poor periods. Foraging ranges have a high degree of overlap leading to resources being distributed evenly throughout the patch when the overall resource level is low, with limited dispersal of species that seed or fruit in high resource periods. 3. An extension of the above model that consists of multiple local populations that exist with variable foraging ranges depending on resource availability. Foraging ranges however have minimal overlap. Unlike the above scenario this will lead to very low dispersal of seed propagules regardless of resource availability.

36 Chapter 1. Introduction Within an environment resources may be spatially variable (patchily distributed). Mammal population/s move from one high quality patch to another with the number of suitable patches being high. That is the population/s move sequentially throughout the environment, utilising resources within a high quality local area and then move on to the next when they have depleted resources. This may lead to overexploitation of seed resources within local patches, and would limit the extent of seed dispersal between local areas. 1.9 Project aims and outcomes The general aim of the current study was to document and analyse the processes that underlie small mammal seed interactions in Australian rainforest fragments in north east Queensland and to determine the effect of interactions on the distribution and abundance of plant propagules (seed, nuts and fruits) available for forest successional and regenerative processes. The specific aims were to; 1. determine how the structure and floristics of rainforest remnants influence small mammal assemblages in tropical forests in north east Australia (Chapter 2) 2. determine the demography and foraging behaviour of small mammal populations within isolated habitats (Chapter 2 & 3) 3. determine the local spatial distribution of small mammal populations within selected rainforests patches (Chapter 3)

37 Chapter 1. Introduction investigate the relationship between seasonal and temporal abundance of food resources within rainforest patches and the seasonal abundance and distribution of small mammal populations (Chapter 3) 5. investigate the extent of seed utilisation within rainforest patches by small mammals (Chapter 4). 6. determine the effects of frugivory by small mammals on native fruits and nuts thereby developing an indirect estimate of fruit and nut germination by rodents (Chapter 5). The outcomes of this project will aid in development of a detailed understanding of small mammal seed interactions within Australian tropical rainforests remnants specifically to address the following questions; 1. How do native seed resource abundances influence small mammal population sizes and distributions? 2. How effective are small mammals at dispersing native seeds and nuts and what impacts do small mammals have on the germination potential of rainforests fruits? 3. What is the relationship between distribution of food resources and the distribution and foraging range of native small mammals in selected rainforest habitat patches? Developing an understanding of small mammal seed interactions in rainforest patches can provide a foundation for enhancing conservation, restoration and management efforts in these important habitats in north eastern Australia.

38 Chapter 2. Fine scale vegetation structure The influence of fine scale vegetation structure and floristics on the population structure and distribution of small mammals in isolated rainforest fragments 2.1 Introduction There are several factors that can influence the distribution and relative abundance of animal species within a given area. While physiological tolerances and resource availability will influence the distribution of a species at a broad level of scale, the mechanisms that determine the distribution patterns of a species within its geographical range are often much more complex. Processes including relative predation pressure, competition, microclimate and habitat structure all can impact significantly on a species natural distribution, in space and time (Ergon et al. 2001). Within natural systems, the relative impact of each process will vary both spatially and temporally depending on the pressures that are placed on the system. In modern times, large scale human induced habitat modification and fragmentation has placed significant pressure on many ecosystems across the world that has lead to isolation and extinction of many natural populations (Bennett 1999, Pullen 2002, Smith and Hellmann 2002, Feeley and Terborough 2008). These same factors have also significantly altered the way extant animal populations are distributed in space, both within and among remnant vegetation patches.

39 Chapter 2. Fine scale vegetation structure The effect of habitat fragmentation on a species distribution and abundance is influenced by both direct and indirect factors. Habitat fragmentation can affect an organism s specific habitat requirements directly by changing or removing essential resources from the system, while indirect effects such as local extinctions and changes in relative diversity and abundance of potential competitors and predators can also affect individuals or populations (Laurance 1991, Laurance 1994, Diaz et al. 2005). It has been well documented that, as patch area declines, so will the number of species that a patch contains. It is less obvious however, that relative abundance of some species may remain unaffected, or even increase as a result of habitat fragmentation (Lovejoy et. al. 1986, Laurance, 1991, Harrington et al. 2001). This variation can result from a breakdown in many of the mechanisms that govern population size within otherwise continuous ecosystems. This may in part be related to the change in structure and diversity of fragmented habitats relative to continuous habitats (Laurance 1994) with structural and diversity changes favouring certain species and causing the decline of others (Laurance 1991, Laurance 1994, Diaz et al. 2005). Habitat heterogeneity, in particular variability in habitat structure, has often been suggested to play an important role in influencing the distribution of organisms across their natural geographic range. For example, within Chilean forest stands (old growth, mid-successional and primary successional), avian species richness is directly correlated with structural properties of forest stands (Diaz et al. 2005) with species richness changing depending upon density and successional stage.

40 Chapter 2. Fine scale vegetation structure Within fragmented landscapes, variation in habitat structure is often greater as a result of diverse impacts that are associated with edges of remnant patches (Laurance 1991). Within the tropics, forest edges may be significantly different from forest interiors, due to high number of invasive species, changes in vegetation structure, disturbance regimes and species composition (Janzen 1983, Lovejoy et al. 1986, Laurance and Yensen 1991, Smith and Hellmann 2002). This has been suggested as a factor that can affect the pattern of distribution and abundance of small mammal communities within a system (Laurance and Yensen 1991, Smith and Hellmann 2002). Tropical rainforests are widely recognised as the most diverse and heterogeneous ecosystems on the planet, therefore effects of habitat fragmentation and isolation are most often recognised within the tropics (Myers 1988, Diaz et al. 1999, Sherry 2008). Australian tropical rainforests are particularly diverse and although they only comprise 0.1% of Australia s land surface area, they contain the highest diversity of floral and faunal species on the continent (Goosem and Tucker 1995). This is primarily due to a large variation in forest type (regional ecosystems) over relatively small geographical spatial scales. On the Atherton Tableland in north eastern Queensland, four distinct rainforest regional ecosystems have been identified within only a few kilometres of each other, each possessing their own unique structural and floristic characteristics (Goosem and Tucker 1995).

41 Chapter 2. Fine scale vegetation structure Floral diversity has been suggested to play an important role in determining the diversity of fauna within any geographical region. Floristically diverse habitats, including rainforests, often support animal populations at very high densities or have increased probability of sustaining high faunal species diversity. Once they are fragmented however, their floristic diversity can lead to isolated forest fragments becoming very different from pre-fragmented forest stands, with only a small subset of species that survive in the remaining remnants. The decline in diversity within fragmented isolated forests is associated with a number of interconnected factors. Habitat fragmentation often leads to the creation of isolated forest patches too small to support remaining faunal and floral communities (Saunders et al. 1991, Beier and Noss 1998, Harrison and Bruna 1999). This in turn leads to a decline in the number of frugivorous seed dispersers, often vital to the persistence of forest systems and this can limit seed dispersal rates of a number of floral species (Laurance 1994, Hausmann 2004). In some situations the decline in seed dispersers corresponds with an increase in seed predator numbers, compounding the effects of fragmentation (Laurance 1994, Harrington et al. 2001, Anderson et al. 2003, Hausmann 2004). High habitat diversity in a patch, in theory, should result in an area being able to support a larger number of species (Meffe et al. 1997). A study by Laurance and Laurance (1999) demonstrated that rainforest remnants with high floristic diversity and that were not dominated by low diversity regrowth of Acacia spp., supported greater numbers of arboreal small mammal species than did less

42 Chapter 2. Fine scale vegetation structure diverse habitat remnants. Faunal assemblages and species abundance may therefore vary substantially among fragmented habitat patches within the same geographical range due to differences in floristic composition of the remaining vegetation. Variation in habitat structure at a fine scale can also have a significant effect on the distribution, abundance and behaviour of faunal species (Tabeni and Ojeda 2005). Organisms may select habitats with favourable habitat attributes as they provide higher levels of protection from predators (Tabeni and Ojeda 2005). Variation in specific structural attributes however, may also allow an individual to access critical resources more efficiently (Diaz et al. 2005). While the initial impact of habitat fragmentation on the structure of forest communities has been well established, ongoing change in habitat structure may result from variation in biotic (e.g. density of seed dispersers/seed predators) and abiotic (e.g. wind direction and velocity, aspect) factors (Saunders et al. 1991, White et al. 2004). It has been well documented that densities of small mammal species, in Australian tropical rainforests, particularly rodents, are sustained at densities similar or greater than in continuous forests (Laurance 1991, Laurance 1994). Laurance (1994) demonstrated that small mammal species responded positively to forest edges and suggested that habitat structure in these areas was favourable and provided greater food and nesting resources. In earlier studies, comparisons of habitat structure and small mammal densities have only been made between continuous and fragmented systems. The impact of fine scale habitat differences

43 Chapter 2. Fine scale vegetation structure on the distribution and abundance of small mammals within small forest fragments has yet to be investigated. Melomys cervinipes and Rattus fuscipes are rodent species endemic to Australia. While both species can be broadly defined as habitat generalists, they only occur in forested coastal areas in Australia and adjacent ranges (Watts and Aslin 1981, Strahan 2004). M.cervinipes is a small semi-arboreal mammal that nests in burrows, tree hollows or creates nests in small trees (Watts and Aslin 1981, Strahan 2004). R.fuscipes is a ground dwelling small mammal that nests in burrows and is rarely found in vegetation one metre the ground (Watts and Aslin 1981, Strahan 2004). Numerous studies have demonstrated that mammal species with similar life history traits can respond differently to habitat fragmentation (Nupp and Swihart 1996, Bowers and Matter 1997, Conner et al. 2001, Harrington et al. 2001, Lambert et al. 2003, Anderson et al. 2003). Although comparisons have been made between the abundance and distribution of M.cervinipes and R.fuscipes between continuous and fragmented systems (Laurance, 1991, Laurance 1994, Harrington et al. 2001), few studies have focused on the influence of structural and floristic elements in fragmented systems. Laurance (1994) suggested that M.cervinipes populations were associated with tree falls and forest edges, whilst R.fuscipes was an edge restricted species. This was suggested to be related to the structural complexity and floristic diversity of edge habitats within fragmented tropical forest of north Queensland (Laurance 1994).

44 Chapter 2. Fine scale vegetation structure In this chapter, structural and floristic diversity measures will be compared across study sites to determine: a) what differences exist within and among study sites, b) the influences of structural and floristic diversity on distribution and abundance of M.cervinipes and R.fuscipes.

45 Chapter 2. Fine scale vegetation structure Materials and methods Study sites Study sites were located near the township of Malanda (17 22 S, E) on the Atherton Tableland far north Queensland (Figure 2.1). Two distinct rainforest regional ecosystems that are present on the Atherton Tableland were examined in the study, one classified as endangered (regional ecosystem 7.8.3) and the other considered of concern (regional ecosystem 7.8.2). Regional ecosystem 7.8.2, (1b) Complex mesophyll vine forest, is restricted to very wet upland basalt soils (Tracey 1982), while regional ecosystem 7.8.3, (5b) Complex notophyll vine forest, is found on moist basalt lowlands, foothills and upland soils (Tracey 1982). The Atherton Tableland was cleared extensively in the early 1900 s followed by a second phase of clearing in the 1950s. Clearing was undertaken to allow agricultural industries (primarily dairy) to make use of the rich, fertile basaltic soils that dominate the region (Frawley 1983). Extensive clearing on the Tableland has created numerous forest remnants embedded in a mosaic of agricultural land with up to 96% of once continuous rainforest on the Tableland having been cleared or fragmented (Winter et al. 1987).

46 Chapter 2. Fine scale vegetation structure a) Site 1 N Atherton Tableland MALANDA Queensland Site 3 Site 2 TARZALI b) Figure 2.1: Study system. a) Location of three isolated rainforest sites on the Atherton Tableland in relation to the township of Malanda. = Study sites, = Continuous rainforest. b) photograph of site two, highlighting the difference between the matrix habitat and rainforest remnants.

47 Chapter 2. Fine scale vegetation structure Three isolated rainforest remnants that vary in size were used for the study (Figure 2.1). Site 1, a 6.5ha forest fragment located 8km north-west of Malanda that contains a complex of two regional ecosystems; and Site 2 a 5.5ha forest fragment and Site 3 a 2 ha forest fragment located approximately 3 km south of Malanda consist of regional ecosystem type Sites were surrounded by a matrix of agricultural pastures and in the case of site 1 and 2 were bordered on one edge by a road (figure 2.1). Both sites 1 and 3 had been selectively logged approximately 70 years ago, whilst site 2 had never suffered selective logging Study species Two rodent species were targeted for the study, Melomys cervinipes and Rattus fuscipes. Both are rodents endemic to Australia. Melomys cervinipes has a distribution that ranges over much of the east coast of Australia. Coat colour ranges from light orange to a dark grey brown combined with a grey cream or white ventral surface (Watts and Aslin 1981). Melomys cervinipes is arboreal, restricted to closed forest and feeds primarily on leaves and fruits. The species weight ranges from 35g to 150g. Rattus fuscipes has a distribution that is discontinuous along the Australian east and west coast. The distribution covers much of the east coast of Australia, the south eastern coast of South Australia and the south western coast of Western Australia (Watts and Aslin 1981). Four subspecies are recognised currently, that occur in a range of habitats with the northern-most sub species (Rattus fuscipes coracius) inhabiting closed forest systems, and ranging in weight from g (Watts and Aslin 1981).

48 Chapter 2. Fine scale vegetation structure Figure 2.2a: Melomys cervinipes, The Fawn-footed Melomys. Figure 2.2b: Rattus fuscipes, The Bush rat.

49 Chapter 2. Fine scale vegetation structure Sampling Methodology Vegetation structure and floristics Structural and floristic attributes of the vegetation at each site were assessed on a uniform 25m 2 sampling grid (Figure 2.2). Each site was surveyed and each grid point was within an error of ±1m from a true grid. The central point of the sampling grid was not closer than 12.5m from any edge of a patch. Site 1 contained 103 sampling positions over thirteen transects, site 2 contained 87 sampling positions over nine transects while site 3 had 30 sampling positions over six transects, respectively. All sampling (vegetation structure, floristics, resource and mammal) undertaken during the study used the same established grid points at each site. Figure 2.3: Sampling grid design for forest fragments Within each sampling grid position, aerial photographs of the canopy directly above were taken at three random points. Photographs were taken with a digital camera set at a constant zoom on a tripod. Each photograph was overlaid with a

50 Chapter 2. Fine scale vegetation structure square grid so that density estimates could be calculated. Vegetation that intersected grid squares on photographs was marked, so that percentage foliage cover could be determined. These data were pooled to determine mean Percent Foliage Cover (PFC) estimates of the three sampled points for each position. Point Centre Quarter (PCQ, Krebs 1989) and Diameter at Breast Height (DBH) measures were taken at each sampling position for each of three height classes (1-4m 4-10m & > 10m). These data were used to estimate plant stem density (as per Pollard 1971) and plant basal area at each sampling position. Actual stem density estimates (stem density x basal area) and basal area estimates were calculated for all positions. All trees sampled using the PCQ method, were flagged and later identified to species level for floristic comparisons. Ground cover estimates (0-200mm & 200mm 1m) were also taken at three random points within each sampling position. A 1m 2 Cover board with 100 grid squares was photographed through 2m of standing vegetation. Photographs were taken at an elevation of 1m from the ground. The number of grid intersects covered by vegetation was assessed for each height strata and mean cover estimates were calculated for each sampling position Small mammal sampling An intensive mark-recapture study of mammals was conducted over a two year period between (February 2002 February 2004) at each of the three sites. At each sampling position within each rainforest site an Elliot (box) trap and wire cage trap were used to capture small mammal individuals. Trapping occurred

51 Chapter 2. Fine scale vegetation structure over eight consecutive nights every three months. Traps were baited with a small piece of un-waxed cardboard (~ 2cm 2 ) soaked with linseed oil. Cage traps were baited every night while Elliot traps were baited every second night. Traps were also rebaited if an individual was captured. Each trap was covered with a thick plastic bag to minimise stress to captured individuals resulting from exposure to excessive moisture. On initial capture, captured individuals were marked with a unique nonmigratory sterile micro-chip (compliance No. ISO 11784, Veterinary Marketing Network). Demographic measures of weight (g), sexual condition (immature or mature male, imperforate, perforate or pregnant female) and tail length (mm) were measured. Individuals were then released at point of capture. Individuals recaptured on the same sampling trip were identified, their micro-chip was rescanned (Pocket Reader Ex, Destron Fearing), sexual condition was reassessed and individuals were then released at point of capture. On subsequent sampling trips, all demographic measures were taken for all recaptures when individuals were first captured, so changes in characters could be assessed among sampling trips. Non-target mammal species were marked using a circular ear punch (not micro-chipped) and released at point of capture so that relative population estimates could be obtained for all species captured during the sampling program.

52 Chapter 2. Fine scale vegetation structure Analysis Vegetation structure and floristics were assessed both within sites with the experimental unit being the sampling position and among sites with the experimental unit being the number of sites. Among site comparisons were broken down to individual strata or measurement units. Comparisons within sites of the vertical structure within each site for stem density, basal area and vertical ground structure were also performed. Arcsine transformations were performed for data generated in PFC estimates and Mean cover estimates as data values were percentages that ranged between 0-100%. One-way Analyses of Variance (ANOVA) were used to test significance both within and among sites for all structural elements. Post-hoc analysis was performed using Tukey HSD model. The standardised Morisita index of dispersion, was used to identify levels of dispersion within sites between strata. This index was chosen for the study as it is considered to be one of the best measures of dispersion because it is independent of population density and sample size (Krebs 1989). Morisita index is expressed as: 2 x I d n 2 ( x) x x Where I d = Morisita index of dispersion, n = sample size, x = sum of the quadrat count and x 2 = the sum of the quadrat counts squared. The index also generates confidence intervals for random, clumped and uniform distributions. The

53 Chapter 2. Fine scale vegetation structure standardised Morisita index of dispersion (I p ) ranges from -1.0 to +1.0, with 95% confidence limits at +0.5 and Random patterns give an I p of zero, clumped patterns above zero (+) and uniform patterns below zero (-). Floristic diversity was measured using the Renyi diversity index. The index is based on the concept of entropy and overcomes many of the short comings and inconsistencies that are associated with indices such as Shannon-Wiener index that is strongly influenced by species number and the underlying model and Simpson Yule index that can be influenced by a few dominant species (Southwood and Henderson 2000). It is expressed as: H log 1 s i 1 i Where β is the order or scale parameter (β 0, β 0), log is the logarithm to the base of choice, and ρ i = the proportional abundance of the ith species. Interpretation of the index is based on a qualitative analysis of a graphical output. The scale parameter of the Renyi index varies from 0 to 4, and is a representative scale from rare to common species. The y scale or Renyi index is dictated by the diversity within sites examined. Intersection of curves relative to scale parameters indicates the degree of similarity of measures. Curves that do not intersect are said to be dissimilar.

54 Chapter 2. Fine scale vegetation structure Results Analysis of structural measures Projected foliage cover (PFC) was significantly different among sites (F = , df = 2, p < 0.001). Differences in PFC were attributable however, to only 4 % total difference in cover among the three sites. This was not considered to be biologically significant (Site 1 = ± 0.24, site 2 = ± 0.22 & site 3 = ± 0.73). Stem density (number of stems) and actual stem density (number of stems x basal area) measures were compared among sites. While no significant difference in stem densities was evident among sites (F = 1.481, df = 2, p = 0.228), a significant difference was observed in actual stem density among sites (F = 5.249, df = 2, p = 0.005). Mean actual stem densities and differences between sites are given in Table 2.1 (Post hoc Tukey HSD). Table 2.1: Mean actual stem densities and actual stem density differences between all rainforest sites. Site Mean ± 1 S.E. Comparison site Mean difference ± 1S.E. Sig Site ± Site ± * 0.17 ± Site ± Site ± Site ± * 0.24 ± Site ± * Site ± Site ± ± Site ± * *significant at p = 0.05

55 Actual stem density (±1 S.E) Chapter 2. Fine scale vegetation structure An ANOVA among sites that separated the three height strata indicated that the observed difference was related primarily to the third strata (>10m), (Strata 3: F = 9.34, df = 2, p< 0.001), with no significant difference evident among sites for the lower strata (Strata 2: F = 2.099, df = 2, p = 0.125; Strata 1: F = 0.833, df = 2, p = 0.436). (Figure 2.4) Strata 1 Strata 2 Strata 3 Figure 2.4: Actual stem density measures for each site by strata (mean ± 1 S.E). ( = Site 1, = Site 2, = Site 3). Standardised Morista index of dispersion was calculated for actual stem density at each height strata. These data indicate that at all three sites, actual stem densities formed a clumped distribution for all height strata (Table 2.2)

56 Chapter 2. Fine scale vegetation structure Table 2.2: Dispersion index values for actual stem density estimates at each site over three height classes using the Standardised Morisita index. Note that values generated in the index fall between -1 (uniform) to 1 (clumped), with confidence intervals for random distributions between -0.5 and 0.5. Height Classes 1-4m Site Site Site Vertical mean ground cover estimates were significantly lower in the 0 200mm strata at Site 1 than at Site 2 or 3, (F = , df = 2, p < 0.001). Mean cover estimates in the m strata were higher at Site 2 than at the other two sites (F = 4.048, df = 2, p = 0.019). Within both strata, differences were associated with small standard errors and means that were not more than 8% different for either stratum. (Table 2.3) Table 2.3: Percent ground cover estimates for each site between each strata mm Strata (Mean ± 1 S.E) mm Strata (Mean ± 1 S.E) Site ± ± 1.05 Site ± ± 1.22 Site ± ± 1.38

57 Chapter 2. Fine scale vegetation structure Dispersion estimates were also calculated for both ground cover strata. Stems in both the 0-200mm and mm height strata showed a clumped distribution. This result was similar to that reported for actual stem density. Data were consistent across all three sites (Table 2.4). Table 2.4: Dispersion index values for ground cover estimates at each site over both height strata using the Standardised Morisita index mm Strata mm Strata Site Site Site Floristic diversity Floristic diversity was assessed using the Renyi diversity index. Figure 2.5, presents the Renyi index for the sites examined here. No substantial differences can be discerned between site 3and sites, 1 and site 2, however site 2 was different from site 1.

58 Renyi Index Chapter 2. Fine scale vegetation structure Scale parameter Figure 2.5: Species diversity per site as measured by the Renyi index. ( = Site 1, = Site 2 & = Site 3) Among the 2640 trees sampled across the three sites, 183 discrete species were identified. Of these, 29 species were shared across all sites (16%) however, they accounted for only 48% of the total number of species recorded Small mammal captures Over the course of the mark-recapture study that totalled trap nights (440 traps x 72 nights), 473 individual M.cervinipes and 222 individual R.fuscipes were captured in the three study sites. Trapping also yielded 85 White tail rats (Uromys caudimaculatus), 4 Water rats (Hydromys chrysogaster) and 280 non rodent captures. Non-rodent captures included native mammal species; Long nose bandicoots (Perameles nasuta), Northern brown bandicoots (Isoodon macrourus), Coppery brush tail possums (Trichosurus vulpecula), and a number of reptile and bird species.

59 Number of Individual Captures/ha Chapter 2. Fine scale vegetation structure The number of individual captures of target species was not evenly distributed among sites over the course of the study with site 1 accounting for 281 M.cervinipes and 99 R.fuscipes, site 2 accounting for 285 M.cervinipes and 80 R.fuscipes and site 3 accounting for 107 M.cervinipes and 44 R.fuscipes captures, respectively. The number of individual small mammal captures per hectare increased as patch size decreased for both total captures and for M.cervinipes captures (Figure 2.4). The number of R.fuscipes captures per hectare were approximately 30 % higher at site 3 compared with sites 1and 2, respectively (Figure 2.6) Site 1 Site 2 Site 3 Figure 2.6: The number of individuals captured per hectare over the entire study at each rainforest site for each species ( = M.cervinipes, = R.fuscipes = Total Captures). There was little difference in the number of total captures (recapture) per hectare among sites, with capture rates similar across sites for both M.cervinipes and for

60 No of Total Captures/ha Chapter 2. Fine scale vegetation structure total captures. R.fuscipes captures varied among sites, but the variation observed did not appear to be related to patch size (Figure 2.7) Site 1 Site 2 Site 3 Figure 2.7: The number of total captures per hectare over the entire study at each rainforest site for each species ( = M.cervinipes, = R.fuscipes = Total Captures). Mean recapture rates over the two year trapping period were approximately 15% higher at site 1 for both M.cervinipes and R.fuscipes and declined in relation to patch size except for R.fuscipes at site 3 that showed a higher recapture rate than site 2. (Figure 2.8).

61 Mean racapture rate/ha Chapter 2. Fine scale vegetation structure Site 1 Site 2 Site 3 Figure 2.8: Mean recapture rates over the entire study at each rainforest site for each species ( = M.cervinipes, = R.fuscipes & = Total Captures). The distribution of captures across sites for all species was assessed using Standardised Morisita Index of dispersion. All distribution patterns expressed were random, except for total R.fuscipes captures at site 2 and site 3 that showed clumped distributions (Table 2.4). These distributions were however, on the margins of the confidence intervals for random distribution patterns Table 2.5: Dispersion index estimates for individual captures and total captures of both M.cervinipes and R.fuscipes at each site using the Standardised Morisita index. Rattus Melomys Total Rattus Total Melomys Individuals Individuals Captures Captures Site Site Site

62 Chapter 2. Fine scale vegetation structure Discussion In general, habitat structural elements were not different among sites, with all sites displaying similar structural and floristic characteristics. While projected foliage cover estimates were significantly different among sites, the biological significance of only a 4% difference was considered to be marginal. Furthermore, the site with the higher PFC estimates, did not support the larger number of small mammals in total or per hectare. This suggests that fine scale differences in canopy cover had little, if any, effect on small mammal numbers. Actual stem density (stem density x basal area) estimates were significantly different for the largest height strata. These data are representative of the recent history of the three sites. Few remnant forest patches on the Atherton Tableland are virgin forest, and most have experienced selective logging over the past 100 years, with logging ending only in the last 20 years. Site 2 was one of the few remnants where logging had never been conducted, hence many large trees still remain. This difference was also evident in ground cover estimates, with site 2 having significantly more ground cover for both the strata measured. These factors did not appear however, to directly influence relative small mammal numbers, as individual capture estimates were similar at both site 1 and site 2 for R. fuscipes captures and for sites 2 and 3 for M. cervinipes captures and also for total capture estimates. Recapture data for sites 2 and 3 however, were also most similar, the two sites were most differentiated in terms of vegetation structure.

63 Chapter 2. Fine scale vegetation structure If vegetation structure has affected small mammal distributions, then structural elements and small mammal assemblages should show similar dispersion patterns. All measures of vegetation structure yielded clumped distributions that were not consistent with the sampled small mammal dispersion patterns. Total R. fuscipes captures at both sites 2 and 3 were clumped however, all other measures of rodent dispersion indicated that individuals were distributed randomly. Both M. cervinipes and R. fuscipes have large natural geographical ranges and occur in a number of different forest types; therefore the effect of vegetation structure may not affect densities of species that are considered to be habitat generalist species. Laurance (1991, 1994) suggested that M.cervinipes and R.fuscipes were edge dominated species and that M.cervinipes populations were also related to tree falls and canopy gaps. These findings are not supported in this study as no association was found between and fine scale structural elements of sites and rodent distributions. Furthermore, if these species were related to edge habitats it would be expected the measures of dispersion would be clumped rather than random within study sites. Many studies have suggested that floristic diversity can have a significant effect on animal assemblages (Nupp and Swihart 1996, Bowers and Matter 1997, Conner et al. 2001, Harrington et al. 2001, Lambert et al. 2003, Anderson et al. 2003). Siemann et al. (1998) suggested that floristic diversity can influence animal diversity and species distribution patterns significantly because more

64 Chapter 2. Fine scale vegetation structure diverse systems should possess a greater number of resources and hence should therefore be able to support a greater number of individuals. Floristic diversity is inherently high within tropical systems, but different sections of forest within the same forest type or regional ecosystems can exhibit broad differences in floristic diversity. Although floristic diversity is known to decrease with fragmentation (Saunders et al. 1991, Beier and Noss 1998, Harrison and Bruna 1999), floral diversity in tropical fragments remains inherently high. It is often difficult therefore, to determine the impact of habitat diversity in these systems. Data from the present study show clearly that although floristic diversity was different between sites 2 and site 3, approximately 50% of all plant taxa recorded were shared at all three sites. These taxa, only contributed 16% to total floral diversity of the individual sites. Hence in systems like tropical rainforests, the effect that floristic diversity has on small mammal assemblages is often difficult to quantify without first understanding the influence that floral diversity has on contributing essential resources to the system. Comparative assessment of floristic and structural elements at the three sites indicated that vegetation among sites was generally similar. Fine scale differences that were evident among sites for some measures were not considered to be marked enough to have a significant biological impact on small mammal density or structure as the mean difference for all these measures was small and no pattern was evident between relative population density and greater or lower estimates. These data do suggest however, that two distinct processes were

65 Chapter 2. Fine scale vegetation structure occurring at the sampled sites. Site 1, and to a lesser extent site 2, possessed a higher number of total small mammal individuals per hectare than did site 3. Recapture rates at these two sites however, were much lower. This suggests that populations of small mammals (at sites 2 and 3) possessed higher turnover rates. This may be due to a greater dispersal rate out of patches due to competition for food resources or a greater vulnerability of local food availability leading to forced dispersal. Populations at site 1 were more stable across years with a greater proportion of total individual numbers recaptured over multiple years. The pattern of population cycle observed here can be explained in a number of ways. The effect of competitive interactions or predation may influence turnover rates in certain populations. It has been well documented that in Australian tropical rainforests, large predators and competitors maintain lower densities in smaller habitat patches and a strong relationship usually exists between habitat patch size and their relative density (Laurance 1990, Laurance 1994, Harrington. et al. 2001). If competitive and predation pressures were the driving force in the leading to dispersal in the current system, it would be more likely that this would occur from the largest fragment (site 1) as this patch had the greatest probability of supporting larger numbers of resident or migratory predators and competitors. Food resources are more likely to influence population density over greater time periods, with areas that have a lower degree of temporal variability in food resources being more likely to sustain populations at a relatively constant level.

66 Chapter 2. Fine scale vegetation structure Fluctuations in seasonal food resource availability can play a very important role in determining population numbers and population stability (Murdoch 1970, Dobson and Kjelgaard 1985, Sinclair 1989, Boag and Wiggett 1994 and Dobson 1995). Habitats that have resource curves represented by extreme amplitude shifts are unlikely to be able to sustain individuals that depend on important resources compared with sites with more predictable resources. As rodents are known to respond quickly to changes in resource availability and can adjust their reproductive output to meet local resource conditions, the number of individuals that pass through the system can be high (Watts and Aslin 1981). Conversely, habitats where resource loads are relatively stable are more likely to maintain populations at some relative equilibrium, with a greater proportion of individuals remaining residents across years and across generations. Sites 2 and 3 represent a single regional ecosystem, whilst site 3 is a complex of two regional ecosystems. Although Floristic analysis failed to identify significant differences between sites, the persistence of populations in site 1 may be associated with prolonged fruiting and flowering due to a slightly varied floristic composition. The next chapter investigates the extent of temporal and spatial resource fluctuations at each of the three study sites examined. The relationship between resource variation and small mammal distribution and abundance is also examined.

67 Chapter 3. Flora and Fauna distribution and abundance Flora and Fauna distribution and abundance 3.1 Introduction The distribution of both flora and fauna within a geographic range will depend on a number of related factors, including microclimate, predation pressure, competition, habitat structure and the distribution of resources including food, water, and mates (Begon et al. 1996, Ergon et al. 2001). As both animal and plant species depend on being able to access and secure sufficient resources readily, the temporal and spatial distributions of resources are fundamental factors that will influence the natural distribution of any given species. Animal distributions often fluctuate spatially over shorter time periods than will plant distributions. This is because most animal species can adapt quickly to changes in resource availability and also are often more mobile. Thus, a heterogeneous distribution of resources across an individual animal s geographical range is likely to lead to a heterogeneous or patchy animal distribution within that range (Kareiva 1990). This in turn may influence how resources are utilised within an animal s given range and ultimately, this can affect habitat structure. It has long been acknowledged that levels of important environmental resources can be significant determinants of population persistence (Murdoch 1970, Dobson and Kjelgaard 1985, Sinclair 1989, Boag and Wiggett 1994 and Dobson 1995). Numerous studies have associated variation in critical resource abundance on population size and persistence in mammals (Alder 1994,

68 Chapter 3. Flora and Fauna distribution and abundance Finkelstein and Grubb 2002, Elmouttie and Wilson 2005, Horskins 2005, Streatfeild 2009). This is particularly evident in small mammals, as it is common for small mammal population densities to fluctuate extensively over time (Watts and Aslin 1981, Horskins 2005). Variation in population size is also often associated with environmental conditions that are present within a habitat at a given time (Ergon et al. 2001, Singh and Kushwaha 2005, Sing and Kushwaha 2006). Pathogens, predators and more commonly resource availability are all key factors that potentially influence population persistence (Ergon et al. 2001) and may dramatically alter their demography. Spatial and temporal resource heterogeneity can also influence species distribution patterns and foraging behaviour within a natural range. Many species possess a range of behaviours and foraging strategies that allow them to utilise different habitats that vary in structure, complexity, resource abundance and type (Kincaid and Cameron 1985, Stearns 1992, Dubowy 1997, Schmidt- Nielsen 1997, Elmouttie and Wilson 2005, Streatfeild 2009). Other species are less flexible however, and can only occupy areas with specific resource attributes (Kincaid and Cameron 1985, Stearns 1992, Dubowy 1997, Schmidt-Nielsen 1997). Relatively few studies have investigated the factors that influence the fine-scale distribution of small mammals in detail. Numerous examples exist however of both habitat specialists and generalist small mammal species that vary their foraging behaviour to cope with spatial resource heterogeneity (Watts and Aslin 1981, Lacher and Mares 1996, Alder 1994, Tobin et al. 1996, Elmouttie and Wilson 2005, Streatfeild 2009).

69 Chapter 3. Flora and Fauna distribution and abundance Broadly speaking, generalist species are capable of breeding across the year and can adapt to utilising a range of resources, whether they are preferred or not (Stoddart 1979). In contrast, specialists are species that usually have a defined breeding season that is determined by availability of a particular important resource or a suite of resources. Specialist species also often depend on particular resources for their survival (Stoddart 1979). Generalist small mammal species can often cope with large seasonal fluctuations in resource availability (Post et al. 1998; Pierce et al. 1998). Many generalist small mammals possess flexible foraging and behavioural strategies that allow them to engage in energy expensive activities (e.g. reproduction) at the most efficient times during an individual s life cycle (Strickberger 1989, Stearns 1992, Begon et al. 1996, Post et al. 1998; Pierce et al. 1998). The potential to adjust foraging behaviour is especially important in this regard, as the time and energy spent acquiring food resources can be substantial (Bulmer 1994, Harris 1995, Caughley and Gunn 1996). The foraging strategy that is employed by any animal species can, in part, be influenced by temporal and spatial habitat heterogeneity (Weins 1997). Environments that have highly variable climates, for example many temperate regions, often exhibit high levels of temporal resource heterogeneity. In contrast, most tropical regions exhibit relatively low levels of temporal resource heterogeneity, with some resources available all year round. Certain habitat types can exhibit high natural spatial resource heterogeneity, for example deserts

70 Chapter 3. Flora and Fauna distribution and abundance may contain discrete patches of resources that are separated by vast distances of resource poor areas (Ward and Saltz 1993). In recent times however, the spatial heterogeneity of critical resources have increased significantly in many fragmented systems that naturally exhibited low levels of heterogeneity before habitat fragmentation (Wiens 1997). Natural temporal and spatial fluctuations in resource availability have resulted in the evolution of a diverse range of foraging strategies (McIntyre and Wiens 1999). There are five broadly defined foraging behaviours that organisms may adopt to address spatial and temporal variability in resource levels: migration (Terrill 1990), hibernation or torpor (Schmidt-Nielsen 1997), food storing or caching (Smith and Reichman 1984; Vander Wall 1994; Benderkoff et al. 1996), range expansion (Warburton et al. 1998) and prey or dietary switching (Warburton et al. 1998). While each of these strategies can be used in isolation, they are often combined in more complex strategies that enable individuals to exploit specific habitats while minimising their energy expenditure (Kincaid and Cameron 1985, Dubowy 1997, Schmidt-Nielsen 1997). The type of foraging regime that is adopted will depend on the life history characteristics of the species, the extent of temporal and spatial heterogeneity within its environment and the morphological, structural and physiological adaptations possessed by the individual (McIntyre and Wiens 1999). Environments that are associated with extreme temporal variation may result in individuals migrating to an alternative habitat that at the time, has sufficient

71 Chapter 3. Flora and Fauna distribution and abundance quantities of important resources. Environments that do not exhibit the same degree of spatial and temporal resource heterogeneity however, allow organisms to utilise less expensive foraging behaviours for example dietary switching or range expansion (Caughley and Sinclair 1994; Warburton et al. 1998). Dietary switching combined with range expansion are the most frequent foraging strategies identified in temporally stable habitats, (i.e. habitats where food resources are present all year), for example tropical rainforests. Organisms may switch between food resources such that they are consumed at disproportionately high levels when they are abundant and disproportionately low levels, when they are rare (Caughley and Sinclair 1994; Warburton et al. 1998). This may occur while individuals expand and contract their foraging range, thus permitting a relatively constant supply of food remaining available to each individual. This type of strategy is most effective where resources fluctuate asynchronously in either space or time (Caughley and Sinclair 1994; Warburton et al. 1998). As most small mammals have relatively high metabolic rates that require high energetic demands, diet switching behaviour is common to allow a relatively constant energy intake to be maintained across the year, without reducing activity levels (Schmidt-Nielsen 1997). This type of foraging behaviour can impact indirectly on floral communities within an individuals foraging range, by varying the rate of dispersal of different seed types, depending on; the availability of food and how far an individual foraging range extends relative to an individual plants flowering period.

72 Chapter 3. Flora and Fauna distribution and abundance Although many small mammals particularly rodents have flexible foraging behaviours that allow them to adapt to a range of conditions and are more commonly generalist species there are a number of examples of species that require specific habitat attributes. Species that coexist in one habitat type and have similar behaviours and perceived requirements in that habitat may not be able to coexist in another habitat due to intolerance to certain conditions. Rattus fuscipes and Melomys cervinipes are two such species that have overlapping geographical ranges through much of eastern Queensland, Australia but do not coexist elsewhere due to the absence of M.cervinipes across southern Australia. Rattus fuscipes is an example of a habitat generalist small mammal species with a disjunct natural distribution that extends along most of the east coast of Australia (not including Cape York Peninsula) and the south west coast of Western Australia (Watts and Aslin 1981). Rattus fuscipes is found in many habitat types that range from dry sandy coastlines to wet tropical rainforests in the Atherton Tableland region of North Queensland. Throughout much of the coastal plans and ranges of Queensland, a congener M.cervinipes is also found (Watts and Aslin 1981; Strahan 1993, Strahan 2004). While R. fuscipes has an extensive natural distribution, M.cervinipes, distribution in contrast is relatively limited and distributed from the northern coast of N.S.W to Cape York Peninsula (Watts and Aslin 1981). The species inhabits a range of environments from open eucalypt forests to closed tropical forest systems (Watts and Aslin 1981). Within the range where the two

73 Chapter 3. Flora and Fauna distribution and abundance distributions overlap, diets are very similar, with both species feeding primarily on rainforests fruits and nuts (Watts 1977). Tolerance of R. fuscipes to a greater range of environmental conditions may be linked to its ability to breed across the year, depending on relative resource availability because it can utilise a broad range of food types and can modify its foraging behaviour. In contrast, M.cervinipes has a more restricted breeding season, smaller litter sizes and has a substantially longer gestation period (38 days / days) (Watts and Aslin 1981). Less flexible life history traits may therefore restrict the type of potential habitats M.cervinipes can occupy and restrict the species distribution. Environments like tropical rainforests provide ideal habitat to study how organisms forage in relation to food availability, as food resources vary, however some level of resource is always available. Species may cope with these fluctuations by either expanding their range and/or switching between food resources across the year. Here I investigate how the foraging behaviour of M. cervinipes and R. fuscipes is influenced by resource availability and distribution within the three isolated habitat fragments. The objectives were to determine: a) if a species foraging behaviour varies seasonally, b) how the population responds to seasonal resource fluctuations and c) to assess whether individuals or populations are restricted to specific areas within forest fragments.

74 Chapter 3. Flora and Fauna distribution and abundance Methods Resource sampling Resource availability at each site was assessed in the same uniform 25m 2 sampling grid as described earlier (Chapter 2). Two 1m 2 seed traps were placed perpendicular to each central sampling point within each grid quadrant. Each seed trap was located 6.5m from the central sampling position and stood 1.5m above the forest floor, where they were erected on a central fixed pole (Figure 3.1). A steel frame was then constructed on the top of the pole and attached at each corner using steel guides. The 1m 2 frame was then lined with 50% synthetic shade cloth mesh (2mm mesh size) so that fruits, seeds and nut falling from the canopy above were captured, while any moisture would pass through the mesh. Adjacent low lying vegetation was cleared from around each seed trap so that any foraging animals could not gain access to fruits captured in traps. In total, 206 seed traps were erected at site 1, 174 at site 2 and 60 at site 3 (Figure 3.1). Figure 3.1: Seed trap design within rainforest patches.

75 Chapter 3. Flora and Fauna distribution and abundance Rainforest seed resources were censuses at three monthly intervals from May 2002 February All captured food resources were identified and counted to estimate resource levels in each fragment at the time. Weights and biomass measures were not recorded as fruits degraded quickly in the moist environment. Identified resources were then separated into resources known to be eaten (KTBE) by the study species and those that were not. KTBE seed resources were identified using Fruits of the Rainforest (Cooper and Cooper 2004) and Finkelstein and Grubb (2002). Anecdotal evidence of rodent feeding (fruits found to be consumed - gnaw marks present) were also used to identify KTBE resources. Professional staff from Lake Eachem Nursery were consulted on what resources were KTBE) as was Mr Nigel Tucker (20 years field experience) Small mammal sampling Small mammal sampling was conducted as described earlier (Chapter two). All mammal sampling was conducted on the same grids used for floristics and resource sampling. The same small mammal data set used in the chapter 2 analysis was used here Movement data The distances moved by individuals were assessed for each trapping period in 2003 season. Distance moved by recaptured individuals within sampling trips was assessed using the individual as the unit of replication. Multiple data for the same individual were averaged and only included once in the analysis.

76 Chapter 3. Flora and Fauna distribution and abundance Analysis Resource distributions were assessed both within sites with the experimental unit being sampling position, and among sites, with the experimental unit being the number of sites. Linear regression analysis was used to determine relationships between food resources and relative small mammal abundance. Movement data were assessed for all recaptured individuals using straight line distance travelled within a sampling period. From the initial point of capture, distance travelled across the sampling grid was calculated for each recaptured individual. Means of all distance travelled were generated for each individual at each given site. Differences in movement were asseded using a One-way Analysis of Variance (ANOVA). One-way ANOVA s were also used to determine differences in mean weight across all sites for both study species.

77 Chapter 3. Flora and Fauna distribution and abundance Results Resource distribution A standardised Morisita Index of dispersion was used to calculate a dispersion index for (KTBE) resources at each site for each year. A clumped distribution was recorded across all sites for both the first and second study years (Table 3.1). Table 3.1: Dispersion index estimates calculated using the standardised Morisita Index for (KTBE) resources at each study site over a two year period. Year One Year two Site Site Site The distribution of KTBE resources was determined quarterly at each site. As for the yearly analysis, all dispersion indices generated a clumped distribution. (Table 3.2) Table 3.2: Dispersion index estimates calculated using the standardised Morisita Index for (KTBE) resources quarterly at each site. May-02 Aug-02 Nov-02 Feb-03 May-03 Aug-03 Nov-03 Feb-03 Site Site Site

78 Chapter 3. Flora and Fauna distribution and abundance Small mammal distributions A standardised Morisita Index of dispersion was also used to calculate the distribution of individual small mammal captures at each site for each of the two sampling years. Across all sites, random distributions were generally found for M. cervinipes, R. fuscipes and combined species captures, however uniform distributions were recorded for both M. cervinipes and R. fuscipes individuals at sites 1 and 3 (Table 3.3). Table 3.3: Dispersion index estimates calculated using the standardised Morisita Index for M. cervinipes, R. fuscipes and combined total individual captures at each study site over a two year period. Year 1 Year 2 Melomys Rattus Total Melomys Rattus Total Site Site Site The distribution of total small mammal captures (recaptures) was also calculated using a standardised Morista Index for the two year sampling period. Unlike individual capture data (Table 3.3), random distributions were recorded for both species across all sites. (Table 3.4)

79 Chapter 3. Flora and Fauna distribution and abundance Table 3.4: Dispersion index estimates calculating using the standardised Morisita Index for M. cervinipes, R.fuscipes and Combined total captures (recaptures) at each study site over a two year period. Year 1 Year 2 Melomys Rattus Total Melomys Rattus Total Site Site Site The distribution of total captures was determined quarterly at each site. Random distributions were recorded for 14 of the 21 measures with the remaining measures showing clumped distributions. (Table 3.5) Table 3.5: Dispersion index estimates calculated using the standardised Morisita index for quarterly total captures at each site. May-02 Aug-02 Nov-02 Feb-03 May-03 Aug-03 Nov-03 Feb-03 Site Site Site Resource availability and small mammal numbers Yearly resource data for all sites were compared with small mammal capture rates and a significant regression was observed between KTBE resources and both the number of overall small mammal captures and the total number of individual captures. (Total captures: r 2 = , n = 6, F = , df = 1,4, p <

80 Captures Chapter 3. Flora and Fauna distribution and abundance ; Individuals: r 2 = , n = 6, F = , df = 1,4, p = 0.014). (Figure 3.1) r 2 = r 2 = Resources Figures 3.2: Yearly site resources levels in relation total rodent captures ( ) and total individual captures ( ) over two year sampling period. Melomys cervinipes captures were significantly influenced by the abundance of KTBE resources (M. cervinipes individual captures: r 2 = , n = 6, F = , df = 1,4, p = 0.002). Rattus fuscipes individual captures were however, not significantly related to KTBE resource levels (R. fuscipes individual captures: r 2 = 0.398, n = 6, F = 2.645, df = 1,4 p = 0.179) (Figure 3.2)

81 Total captures Captures Chapter 3. Flora and Fauna distribution and abundance r 2 = r 2 = Resources Figures 3.3: Yearly site resources levels in relation total M. cervinipes ( ) individual captures and R. fuscipes ( ) individual captures over two year sampling period r² = Resources Figures 3.4: Seasonal KTBE resources levels in relation total captures of both rodent species over two year sampling period.

82 Chapter 3. Flora and Fauna distribution and abundance A significant relationship was observed between Seasonal KTBE resources (3 monthly and small mammal captures (3 monthly) r 2 = , n = 21, F = 37.67, df = 1,18, p < Demographics and movement Although the number of individuals per hectare varied among sites (Chapter 2), the composition of the populations remained relatively similar. Sex ratios for M. cervinipes and R. fuscipes captures were male biased with the exception of site 2 where R. fuscipes captures showed a female bias (Table 3.6) Table 3.6: Proportion of male captures for each sample site through the study period. Melomys cervinipes Rattus fuscipes Site % 55.3% Site % 43.8% Site % 54.8% The mean weight of individuals was significantly different for M.cervinipes captures across the three sampled sites (F = 5.238, df = 2, 656, p = 0.006). These differences were not evident across all sexual conditions (Figure 3.5), with mean weights being similar for immature males, mature males and perforate females at each site. Mean weights of imperforate females and pregnant females was found to differ (Imperforate females: F = 3.968, df = 2,182, p = 0.021; Pregnant females: F = 4.407, df = 2,45, p = 0.018).

83 Mean Weight (± 1 S.E) Chapter 3. Flora and Fauna distribution and abundance IM MM IF PF PR Sexual Condition Figure 3.5: Mean weights (± 1 S.E.) of M. cervinipes captures at each habitat for each sex class. ( = Site 1, = Site 2, = Site 3) (IM = Immature males; MM = Mature males; IF = Imperforate female; PF = Perforate female; PR = Pregnant female) The mean weight of individuals was similar for R.fuscipes captures across the three sampled sites (F = 1.685, df = 2,207, p = 0.188). While mean weights differed for imperforate females (Imperforate females: F = 5.469, df = 2,44, p = 0.008), they were similar for all other sexual conditions. No pregnant females were recorded at site 1 during the study (Figure 3.6).

84 Mean Weight (± 1 S.E.) Chapter 3. Flora and Fauna distribution and abundance IM MM IF PF PR Sexual Condition Figure 3.6: Mean weights (± 1 S.E.) of R. fuscipes captures at each habitat for each sex class. ( = Site 1, = Site 2, = Site 3) (IM = Immature males; MM = Mature males; IF = Imperforate female; PF = Perforate female; PR = Pregnant female) Melomys cervinipes individuals moved significantly less than R. fuscipes individuals across all sites (Site 1: F = , df = 1,103, p < 0.001, Site 2: F = , df = 1,72, p < 0.001, Site 3: F = , df = 1,41, p < 0.001)(Table 3.6).

85 Chapter 3. Flora and Fauna distribution and abundance Table 3.7: Average distances moved by individuals (in meters ± 1 S.E.) from February 2003 to November 2003 at each sampling site. Site 1 Site 2 Site 3 M. cervinipes R. fuscipes M. cervinipes R. fuscipes M. cervinipes R. fuscipes Feb 29.1± ± ± ± ± ±6.25 (n=12) (n=12) (n=12) (n=7) (n=7) (n=4) May 36.2± ± ± ± ± ±9.4 (n=11) (n=12) (n=16) (n=9) (n=9) (n=5) Aug 36.7± ± ± ± ± ±16.9 (n=19) (n=8) (n=12) (n=5) (n=3) (n=5) Nov 43.2± ± ± ± ± ±12.7 (n=22) (n=9) (n=7) (n=6) (n=5) (n=5) The mean distance moved by each species did not differ between sites Melomys cervinipes (F = 3.464, df = 2,9 p = 0.077), Rattus fuscipes (F = 2.378, df = 2,9, p = 0.148). There was also no significant difference in the distance moved by individuals within sites between trapping periods for either species across all sites. Melomys cervinipes (Site 1: F = 1.023, df = 3,60, p = 0.389, Site 2: F = 0.372, df = 3,43, p = 0.774, Site 3: F = 0.334, df = 3,20, p = 0.794) R. fuscipes (Site 1: F = 0.896, df = 3,37, p = 0.452, Site 2: F = 1.626, df = 3,23, p = 0.211, Site 3: F = 0.190, df = 3,15, p = 0.902).

86 Chapter 3. Flora and Fauna distribution and abundance Discussion Australian tropical rainforests are structurally complex, heterogeneous environments that contain many fruiting and flowering plants (Goosem and Tucker 1995, Cooper and Cooper 2004). Due to a high level of plant heterogeneity within these habitats the distributions of food resources for small mammals and other frugivorous species is often patchy, depending on season and climatic conditions (Crome 1975, Harrington et al. 2001, Streatfeild 2009). Certain plants species will fruit and flower at higher rates than others during particular time periods, with the production of fruit depending on plant successional characteristics, season, light seed type and size (Goosem and Young 1989, Stocker et al. 1995, Dennis and Marsh 1997, Boulter et al. 2006). Many tropical rainforest plants are known masting species, a characteristic that leads to heavy fruiting and flowering periods occurring for a particular species simultaneously, across a given area (Stocker et al. 1995, Dennis and Marsh 1997, Boulter et al. 2006). Masting leads to large amounts of a particular fruit type being available during specific time periods that may not occur in other areas within a site where that plant species is not found or is in low abundance. Plant species that produce large amounts of fruits in a particular season however, may not produce similar amounts of fruits every year, and often skip fruit production between years (Crome 1975, Stocker et al. 1995, Boulter et al. 2006). This will influence the distribution of fruit resources throughout a site and in turn may influence the distribution of frugivorous species that utilise these resources (Dennis and Marsh 1997).

87 Chapter 3. Flora and Fauna distribution and abundance During the current study, all dispersion measures for KTBE resources were found to be clumped irrespective of site, year or season. Interestingly the level of production was significantly lower in year 1 than in year 2, however the distribution of KTBE resources was similar. Although seed resources where present in the vast majority of seed traps during the study, heavy fruiting events within specific areas were common where certain plant species were producing large amounts of fruit. Therefore significant variation was recorded in fruit abundance from one seed trap to the next. During the sampling period, masting was evident in many plant species (e.g. Litsea leefeana, Castanospora alphandii, Neisosperma poweri) at all sites, leading to distinct areas within each site showing significantly higher resource availability than others. Seed traps were rarely found however, without some seed resources present, so although seed resources were clumped, some resources were available in each sampling site at all times. Observed distributions of the two rodent species were, in general random, with only a few cases of uniform or clumped distributions recorded during the sampling periods. Melomys cervinipes and R. fuscipes individuals were found to move relatively short distances within a sampling period, with the mean distance travelled by each species being similar across the year and between sites. This suggests that both species distribution patterns in the rainforest fragments were not influenced directly by specific high resource areas, rather individuals foraged across a given area as long as sufficient resources were available locally, within their foraging range.

88 Chapter 3. Flora and Fauna distribution and abundance Random dispersion indices for rodent species individual captures and total captures suggest that population structures were not related to the proximity of other individuals. This also suggests that populations do not favour particular areas of the patch relative to resource availability or geographic region of a patch (i.e. patch edge), because if this were the case a clumped distribution pattern would be expected. Marked animals examined here only travelled relatively short distances within trapping periods and individuals were trapped both in the centre of individual sites all the way to site edges. Similar patterns of dispersion were observed irrespective of site and time, with quarterly dispersion indexes indicating that rodents were most commonly distributed randomly across a site. The dispersion patterns observed here contrast with previous studies. Laurance (1994) suggested that R. fuscipes and M. cervinipes responded positively to the edges of tropical forest. In Lawrence s study, M. cervinipes were also associated positively with recent tree falls that occur with an increased frequency near forest edges (Laurance, 1994). This pattern however, was not observed here with captures of M. cervinipes distributed randomly irrespective of the distribution of structural variable (Chapter 2) proximity to the edge of a site. While Laurence (1994) also indicated that R. fuscipes may be an edge dominant species that prefers habitat edges and associated matrix habitats, in the current study R. fuscipes were found to be distributed randomly across all study sites and individuals showed no preference for fragmented habitat edges.

89 Chapter 3. Flora and Fauna distribution and abundance Laurance (1994) compared large continuous rainforest to isolated rainforest fragments. Although the current study made no comparison with continuous rainforests, the data presented here indicate that M. cervinipes and R. fuscipes population densities are more likely governed by resource availability, rather than forest structural elements, edge effect or matrix habitats. Population densities of both species in this study were directly correlated with KTBE resources, both yearly and seasonally (Figues 3.2, 3.3 and 3.4). The number of small mammal individuals captured was significantly related to the relative availability of KTBE resources. Regression analysis showed a strong relationship between the number of individual rodents captured and the total number of captures in relation to resource availability during each sampling period. Known to be eaten resources fluctuated significantly at each site between years and seasons as did small mammal numbers and although this variation was not uniform among all sites (decline in resources for one site was not proportional to another), the relationship between small mammal numbers and KTBE resources remained. Lack, (1954) suggested that the vast majority of vertebrate populations were limited by food resources and population densities would respond accordingly. Numerous studies have investigated this finding and concluded similar results (Johns 1989, Johnson and Sherry 2001, Lopez-Bao et al. 2008). Rodent species in agricultural and natural habitats have been shown to be particularly responsive to increased food availability, increasing reproductive output and in turn

90 Chapter 3. Flora and Fauna distribution and abundance increasing population density (Wilson and Whisson 1993, Nupp and Swihart 1996, Horskins et al. 1998). Results from this study suggest that like other rodents M.cervinipes and R.fuscipes also respond to resource availability, resulting in significant population fluctuations from season to season. Individual species data indicate that M. cervinipes numbers were strongly correlated with resource abundance however R. fuscipes numbers showed a weaker relationship. This difference may be due to a significant decline in the number of R. fuscipes captures within site two during the second year of the study with population numbers declining by 60% from the previous year. During this period, a significant decline in KTBE resources at site two was recorded and this corresponded with a substantial decline in rainfall for the corresponding period. On ground resource availability was notably lower and it is hypothesised that R. fuscipes could have been out competed for food resources by arboreal and semi arboreal species (i.e. M. Cervinipes, Uromys caudimaculatus). The demographics of each population were found to be similar among sites for all species, with limited variation recorded for sex ratios or weights irrespective of site or population density. Sex ratios were comparable at each site with the exception of R. fuscipes captures at site two. Male biased dispersal is common in mammals (Greenwood 1980), particularly in fragmented habitats where populations are structured with a female bias (Banks et al. 2005a,b). Interesting, in the current study, sex ratios with the exception of R. fuscipes at site two were

91 Chapter 3. Flora and Fauna distribution and abundance male biased suggesting female biased dispersal. These results may be related to high rates of male immigration from neighbouring fragments. Banks et al. (2005b) demonstrated that remnant fragments with high immigrant influxes had sex ratios biased towards the dispersing sex. Horskins (2005) established that M.cervinipes rarely utilised matrix habitats and were confined to closed forest systems, suggesting that a significant dispersal of rodents from neighbouring habitats is unlikely. Variation in sex ratios may be related to resource availability and quality. Johnson et al. (2001) and Johnson and Richie (2002) demonstrated that sex ratios of common brush tail possums (Trichosurus vulpecular) were male biased in response to resource competition between females. Wilson and Whisson (1993) also demonstrated that Rattus sordidus populations had biased sex ratios in relation to food availability. This suggests that females may have the potential to bias sex ratios, via, maternal sex bias or during conception as a response to local ecological conditions. The mean weight of individuals was similar for sexual conditions with the exception of M. cervinipes pregnant females and imperforate females and R. fuscipes imperforate females (Figure 3.5 and 3.6). The difference in mean weights can most likely be attributed to sampling error or low population densities rather than a lack of resources at a site leading to reduced individual weights. These differences occurred at different sites and were not related to

92 Chapter 3. Flora and Fauna distribution and abundance lower weights at a particular site or did not correspond with lower weights in other sex classes. These data indicate that population densities of M. cervinipes and R. fuscipes within isolated rainforest remnants are strongly related to resource availability within their foraging range. Foraging ranges did not vary within sites from season to season, indicating that individuals do not significantly expand or contract their foraging ranges relative to food availability within a given area. Of the four foraging models presented earlier, it seems likely that both M.cervinipes and R.fuscipes, populations display a pattern similar to the first model. In this scenario the patch system can be viewed as one large population with minimal division of resources. It should be noted, the models relate to foraging behaviour and are not a representation of population structuring in relation to mating systems. Interestingly, foraging ranges determined in this study were smaller than those reported previously for both species previous (Strahan 2004). Previous studies have not investigated however, the foraging ranges of these species in tropical fragments rather they have focused on more open forest systems or continuous forest (Strahan 2004). As neither species utilises matrix habitat (Horskins 2005), it is not unexpected that foraging ranges are smaller within small fragments. It is also common for small mammals to reduce their foraging range in resource rich environments (Lacher and Mares 1996)

93 Chapter 3. Flora and Fauna distribution and abundance Irrespective of patch size, populations of both species were maintained densities at a relatively high level across the study. This suggests that even small rainforest remnants (< 6 hectares) have the potential to sustain small mammal populations for extended periods. While population densities of both species declined during the second study year, the mean weight of individuals and the standard errors associated with weights remained relatively constant for all sexual conditions. This suggests that individuals that remained within populations at each site sourced sufficient resources to maintain condition. The data from this study suggests that small mammals within isolated fragments utilise resources within their local area and may contract and expand their foraging ranges to acquire sufficient resources per individual. It is important therefore to determine the impact that this may have on the underlying seed resource within a rainforest fragment, as small mammal populations may be: a) over-utilising available resources during period of resource shortage placing extensive pressure on plant seed propagules, b) over-utilising specific resources to maintain their populations during resource poor periods or c) small mammals may not significantly impact the distribution and abundance of seed resources and may only utilise a small proportion of available resources within a given area. The extent of seed utilisation within rainforest fragments and the impact of seed utilisation by small mammals will be investigated in the next chapter.

94 Chapter 4. Resource utilisation feeding preferences Resource utilisation feeding preferences by small mammals 4.1 Introduction Numerous studies have investigated the impact of small frugiverous rodents on seed utilisation rates in tropical systems (Bernardi Horn et al. 2007, Forget and Cuijpers 2008, Zhang and Zhang 2008, Munoz et al. 2009). Utilisation rates in Australian tropical forests however, are relatively unknown. The effect of frugivorous rodents on plant propagules in relation to relative seed availability and seed abundance is an issue that has received little attention within Australian systems. A significant number of studies have investigated seed utilisation and frugivory and have focused on systems where plant diversity is low and that contain plant species with seeds possessing similar physical characteristics (e.g. grasslands, woodlands) (McMurray et al. 1997; Williams et al. 2000; Wright et al. 2000). Furthermore, many of these studies have focussed on caching behaviour and the impacts of seed caches on seed germination potential (McMurray et al. 1997; Brewer and Rejmanek 1999). Inferences have commonly been drawn between rodent seed utilisation behaviour within these systems and tropical complex systems. Significant research in tropical systems illustrates rodents may interact with seed resources within complex system such as rainforests in a substantially different manner, making cross system inferences unsubstantiated ( Mendoza and Dirzo 2007, Forget and Cuijpers 2007, Cole 2009).

95 Chapter 4. Resource utilisation feeding preferences Within rainforest systems plant seeds are often imbedded within fleshy fruits that depend on frugivores for germination and dispersal rather than abiotic vectors (e.g. wind, water, gravity) (Chambers and MacMahon 1994). Within small fragments many of the large and known seed dispersers are not present due to resource limitation (Laurance 1991, Laurance 1994). The density of smaller mammals often increases in small fragments (Laurance 1991, Harrington et al. 2001) however the impact of such faunal variation on Australian tropical rainforest is yet to be determined. There are numerous seed mammal interactions that have yet to be determined in Australian tropical systems. Specifically, the rate of utilisation, by small frugivores (e.g. native rodents) on seed resources is unknown in Australian tropical systems. The impact that rodents may have on the range of seed types and structures present in these habitats is also poorly understood. In addition little data are available on seed cropping and removal rates by native mammals so seed fate within rainforest patches can be determined. It is imperative that studies investigate these interactions so that a better understanding can be for developed tropical systems, particularly within already vulnerable, modified and fragmented systems. Although both R. fuscipes and M. cervinipes are common small mammal species across much of eastern Australia, little is known about their foraging and feeding behaviour and their impacts on rainforest seed resources within their natural range. Anecdotal evidence suggests that both rodent species crop and utilise a

96 Chapter 4. Resource utilisation feeding preferences significant proportion of available seed resources within a given area. Their relative impact on seed resources and seed banks within remnant rainforest habitat patches is of potential concern, as it has been suggested that their population sizes can be significantly higher within isolated remnant patches than in un-fragmented habitats, because competitor and predator numbers are often lower in abundance or absent from these systems (Laurance 1990; Lawrence 1994). As the relative population density of small mammals in fragmented rainforest patches is often higher than in continuous systems (Laurance 1994, Harrington et al. 2001), the impact of these species on plant propagules could be significant. Small mammal/seed utilisation may therefore, potentially have long-term significant implications for rainforest regeneration and long-term persistence if small mammals over utilise seed resources and reduce seed germination rates. Furthermore, if seed utilisation rates by small mammal s impact negatively on the underlying propagule base within fragmented systems, future restoration efforts may have to address rodent densities so that the limited seed propagules in restored forests are not destroyed. In this chapter I examine the relative impact of R. fuscipes and M. cervinipes on natural seed resource levels in each rainforest fragment. I also aim to assess the relative impact that larger frugivores may have on baseline seed resource levels so that comparative data can be formed for multiple seed types and frugivorous species.

97 Chapter 4. Resource utilisation feeding preferences Methods Study sites were divided initially into equal sub-segments numbering between 14 and 15 trap positions, forming seven segments at site 1, six segments at site 2 and two segments at site 3 (Figure 4.1). Exclosure and control areas were established at the central trap position within each sub-segment adjacent to each of the two seed traps at the central trap position Site hectares Site hectares Exclosure Seed traps Trap position Control 1 Transect Site 3 2 hectares Figure 4.1: Site design for seed exclosure experiment each site was divided into equal size segments numbering between trap position with exclosure and control areas located at the central peg position. Sites in these images are not drawn to scale.

98 Chapter 4. Resource utilisation feeding preferences Each exclosure was 2 x 1m in size and constructed from 40 mm x 25mm welded wire mesh designed to allow foraging M. cervinipes and R. fuscipes individuals to enter the sampling plot while at the same time excluding all other foraging mammals and birds (Figure 4.2). The size of welded wire mesh used was determined by skull measurements (Watts and Aslin 1981) and a series of in field trials where the largest animals of each species were placed in cages to determine if they could pass through uninhibited. Uromys, caudimaulatus, the only other common frugiverous rodent in the area is substantially larger than both study species (1000 grams) and could not pass through exclosures. Exclosures were designed to allow falling fruit to enter the sampling plot during the experimental period. A control area of equal size to the exclosures (2 x 1m) was delineated that allowed access to all foraging animal species and falling seeds (Figure 4.2). Figure 4.2: Orientation of seed trap in relation to exclosures.

99 Chapter 4. Resource utilisation feeding preferences At the commencement of each trapping period, all seed resources at individual sites were collected, sorted and counted from each seed traps at each trap position as outlined earlier (Chapter three). Seed resources in each sub-segment (figure 4.1) were then grouped and the proportion of each seed resource species per segment was calculated and scaled to determine their relative abundance per square metre. Any seed resource items found to be at a density of one seed resource per metre squared or greater was placed in both the exclosure and control area for a period of one month. This density was used so that whole numbers were available for analysis. Each seed type placed within each exclosure and corresponding control plot were distributed at a density calculated for the relevant sub-segment they had been found in, so that the overall density of any particular resource represented that present naturally within that sub-segment. Seed traps beside each of the exclosure and control plots were also monitored over the experimental period to determine the resources that had fallen within each exclosure and control plots during the experimental period. These data were then added into the final analysis. At the conclusion of the 30 day experimental period all resources within the exclosures, control plots and adjacent seed catchers were collected, counted and relative consumption determined to assess relative small mammal utilisation rates among sites. Seed utilisation was separated into two classes, full consumption of fruit and seeds within and consumption of fruit without

100 Chapter 4. Resource utilisation feeding preferences consuming embedded seeds. This design allowed for the following statistics to be estimated: = number of fruits at commencement of experiment = is the number of resources that had fallen across the experimental period = represents the number of resources that remained at the end of experimental = exclosure and = control, Total Resource Utilisation: Utilisation by R. fuscipes and M. Cervinipes: Utilisation by species other than M. cervinipes and R. fuscipes 4.3 Analysis Non parametric Wilcoxin signed ranks analysis was used to determine differences in utilisation rates between control and exclosure plots annually and seasonally. Analysis of levels of fruit utilisation (fruit consumed without seeds) and total utilisation (fruit and seeds) were also analysed using Non parametric Wilcoxin signed ranks analysis.

101 Mean proportion ± (1 SE) Chapter 4. Resource utilisation feeding preferences Results Total mean proportion of both number of fruits remaining and number of seeds remaining differed significantly between control and exclosure plots at each of the three sites (Figure 4.3). Total amount of fruit remaining was significantly higher in exclosures for all sites (site 1, Z = , p <0.001; site 2, Z = , p < 0.001; site 3, Z = , p = 0.012). The amount of seed remaining was also higher in exclosure areas at all sites (site 1, Z = , p < 0.001; site 2, Z = , p < 0.001; site 3, Z = , p = 0.018). 1.0 RSC CON RSE EXC Site 3.00 Figure 4.3: Total mean (± 1 SE) proportion of the remaining fruit and remaining seed within exclosures and controls for each site. ( = Remaining seed within exclosures, = fruit within exclosures, = remaining seed within controls & = untouched fruit within controls)

102 Chapter 4. Resource utilisation feeding preferences This pattern of utilisation was consistent across each of the four sampling periods, with the average amount of fruit remaining being significantly higher in exclosures than in controls for each monthly sampling period (Feb-Mar - n = 15, Z = , p = 0.001; May-Jun - n = 15, Z = , p = 0.005; Aug-Sep - n = 15, Z = , p = 0.002; Nov-Dec - n = 15, Z = , p = 0.001). Utilisation patterns were similar for seed as they were for fruits with the number of seed remaining higher within exclosure plots for each sampling period (Feb- Mar - n = 15, Z = , p = 0.001; May-Jun - n = 15, Z = , p = 0.001; Aug-Sep - n = 15, Z = , p = 0.001; Nov-Dec - n = 15, Z = , p = 0.001). (Figure 4.4) This suggests that M. cervinipes and R. fuscipes remove flesh from fruits and rarely consume the seeds within them.

103 Mean monthly proportions (± 1 SE) Chapter 4. Resource utilisation feeding preferences SRC CON SRE EXC Feb-Mar May-Jun Aug-Sep Nov-Dec Month Figure 4.4: Mean monthly (± 1 SE) proportion of fruit and remaining seed within exclosures and control areas over each sampling period. ( = Remaining seed within exclosures, = untouched fruit within exclosures, = remaining seed within controls & = untouched fruit within controls) Across the three sample sites the number of seed propagules that remained was greater than the number of whole fruits within exclosures (site 1, n = 28, Z = , p < 0.001; site 2, n = 24, Z = , p < 0.001; site 3, n = 8, Z = , p = 0.012, Figure 4.5)

104 Mean total proportion (± 1 SE) Chapter 4. Resource utilisation feeding preferences Site 3.00 Figure 4.5: Difference in total mean proportion of untouched fruit and remaining seed within exclosures at each sample site ( = Remaining seed within exclosures, = untouched fruit within exclosures)

105 Chapter 4. Resource utilisation feeding preferences Discussion Seed utilisation rates differed between exclosures and control plots at all three experimental sites, with fruits and seed propagules within open control plots being utilised at a significantly greater rate than in exclosure plots. Approximately 80 percent of seeds were harvested from within control plots, while less than 10 percent were harvested from exclosures. This suggests that both R. fuscipes and M. cervinipes do not play a significant role in seed dispersal within Australian tropical rainforests, with limited seeds being moved from where they are fed upon. These data suggest however, that larger frugivores may disperse seeds although viability of seeds post-dispersal is unknown. Fruit consumption by both R. fuscipes and M. cervinipes was also found to be significantly lower than in plots that could be accessed by other larger frugivores, however at least 50% of fruits were consumed within exclosure plots across the three sites. Within exclosure plots, seeds within fruits were rarely consumed. This indicates that M. cervinipes and R. fuscipes apparently feed primarily on the pericarp of fruits and rarely consume seeds. The only fruit species where seeds were regularly consumed by M. cervinipes and R. fuscipes were small seeded species, primarily Ficus spp. In contrast, whole fruits (pericarp and seeds) within control plots were consumed or removed at significantly higher rates than exclosure plots. Therefore, even within fragmented systems where small mammals are dominant in terms of relative abundance, larger frugivores within, still constitute

106 Chapter 4. Resource utilisation feeding preferences the major consumers of individual fruit resources. Interestingly, the impact of rodent frugivores in this study was found to be significantly lower on seed propagules than documented in other systems (McMurray et al. 1997, Farwig et al. 2008). Unlike rodents in other systems that tend to consume seeds for nutritional reasons, rendering seeds non-viable (Price and Jenkins 1986, Tobin et al. 1996, Elmouttie and Wilson 2005, Farwig et al. 2008), M.cervinipes and R.fuscipes were rarely found to consume the reproductive component of fruits in this study. Thus their foraging and feeding behaviours may not significantly impact on germination rates of individual seeds as they do not damage the reproductive component of fruits. Rates of consumption within exclosure plots by M. cervinipes and R. fuscipes may also be lower than was estimated here, because frugivorous insects were not excluded from either control or enclosure plots. As individual fruits could not be tracked during this experiment it was not possible to determine, which frugivores were responsible for consumption of individual fruits within control plots. Throughout the study period non-target mammal captures of White tail rats (Uromys caudimaculatus), Coppery brush tail possums (Trichosurus vulpecula) and frugivorous bird species, Eastern Whipbirds (Psophodes olivaceus) and Australian Brush Turkeys (Alectura lathami) were commonly recorded in the sites. Numerous other frugivorous birds such as Orange-footed Scrubfowl (Megapodius reinwardt) and the Lemuroid Ringtail Possum (Hemibelideus lemuroides) were also observed at the sites across the study period.

107 Chapter 4. Resource utilisation feeding preferences The fate of individual seeds within fruits removed from plots could also not be determined as many bird and mammalian frugivores are known to pass seeds through their digestive systems with seeds remaining viable (Foster and Delay 2008). Few studies have investigated the effects of endozoochory by native rodents within Australian rainforests and it is therefore difficult to determine if dispersed seeds were still viable. Removed seeds and fruits from exclosure plots also may have been hoarded across the site. Numerous studies have indicated the importance of caches and scatter hoarding rodents for seed germination and dispersal (McMurray et al., 1997; Theimer 2001). A study in tropical north Queensland by Thiemer (2001) demonstrated that U. caudimaculatus cached seeds of the large seeded rainforest plant Beilschmiedia bancroftii into scatter hoards. Although none of the seeds cached and followed during the study survived to germination, a comparison of seed, cache and seedling distributions indicated that most seedlings of B. bancroftii arose from rat-cached seeds (Thiemer 2001). McMurray et al. (1997) demonstrated that native grass species can outcompete introduced grasses in scatter hoards, with seed germination rates increasing in seed caches. In this study, North American native Indian ricegrass (Oryzopsis hymenoides) was shown to thrive within scatter hoards and had a competitive advantage over introduced cheatgrass in environments that contain scatterhoarding rodents (McMurray et al., 1997). Further investigation of seed fate will be required in Australian tropical rainforests to determine the impact of the high

108 Chapter 4. Resource utilisation feeding preferences seed utilisation rates measured here, approximately 90% of native seeds in control plots. Rodent species have long been implicated as potential seed predators in natural systems and hence they can place very large pressure on seed propagules and have the potential to over harvest forest seeds (Hulme and Hunt 1999, Howe and Brown 2000). Over time their behaviours in theory can influence habitat structure and local plant species diversity. Rodents may also increase levels of propagule mortality (McMurray et al. 1997, Hulme and Hunt 1999, Howe and Brown 2000). Results of the current study suggest however, that smaller frugivorous native rodent species in the sampled rainforest remnants may not always have a detrimental impact on rainforest seed resources. While they may not act as significant dispersers of seeds, they could still play an important role in seed germination. It has been well established that removal of the pericarp from fleshy fruits aids in germination of Australian rainforest fruits (Goosem and Tucker 1995) and is often necessary for seeds to germinate. Therefore, rodent feeding behaviour observed here may be beneficial to rainforest fruits as seeds were often left relatively untouched with the pericarp removed. The next chapter will investigate the effect, if any, of feeding by M. cervinipes and R. fuscipes on rainforest fruit species to determine if germination potential of partially consumed fruit was comparable with untouched or whole fruits.

109 Chapter 5. Seed germination Impacts of feeding Seed germination Impacts of native rodent feeding behaviour on seed germination 5.1 Introduction Human activity has resulted in fragmentation of many natural habitats and thus has significantly influenced fundamental ecological processes within many ecosystems that remain today (Saunders et al. 1991). The extent and impact of fragmentation on animal and plant populations often varies among ecosystems due to both ecological and social factors (Saunders et al. 1991, Laurance and Gascon 1996, Feeley and Terborgh 2008). Habitats that have a greater economic value (agricultural potential, timber or mineral resources) or social value (climate and aesthetics) are often impacted by habitat fragmentation to a greater extent than less valued areas (Myers 1988). The structural complexity, diversity and social and economic importance of rainforests has resulted in them being one of the most heavily exploited ecosystems on the planet (Myers 1988, Laurance and Yensen 1991). Tropical rainforest on the Atherton Tableland is no exception (Winter et al. 1997). The numerous isolated remnant tropical rainforest patches that remain are dispersed within a matrix of agricultural pasture and urban development (Winter et al. 1997, Horskins 2005). Remnant patches often differ significantly in the species assemblages they support from that which existed in the past (Harrington et al. 2001). Due to changes in the floral and faunal assemblages present within

110 Chapter 5. Seed germination Impacts of feeding isolated forest fragments, many natural ecological processes, (e.g. seed dispersal and succession) may be significantly disrupted in comparison with continuous forest fragments (Saunders et al. 1991, Laurance 1994, Galindo-Gonzalez et al. 2000). The effects of rainforest habitat fragmentation can be much more significant than simply loss of continuous habitat. The resulting variation in patch size, patch shape and degree of isolation of rainforest remnants has been shown to substantially modify many processes that operate within forests (Saunders et al. 1991, Laurance 1994, Golindo-Gonzalez et al. 2000). Plant succession can be limited due to a lack of seed propagules, seed dispersal is impacted due to loss of frugivorous species and the limited distances that seeds can be moved (Laurance 1994, White et al. 2004). Germination rates are often substantially lower as many plants depend on specific frugivores to enhance germination (Chamber and MacMahon 1994) and many species are not viable within small forest patches (Laurance 1994). These factors all influence the structure and potential long term viability of forest fragments (Saunders et al. 1991, White et al. 2004). Most habitat fragmentation studies in rainforests have concentrated on interactions between birds, bats and large terrestrial mammals on the forest system (Saunders et al. 1991). Particular emphasis has been placed on processes like seed dispersal and germination (Galindo-Gonzalez et al. 2000, Kollmann 2000), and how fragmentation may affect larger animals that contribute to these processes in continuous forests. It has been demonstrated that many of the

111 Chapter 5. Seed germination Impacts of feeding organism-resource interactions can be altered significantly in fragmented forest habitats as populations of larger frugivores decline (Laurance 1991, Laurance 1994). The organism-resource interaction that exists between more resilient species is poorly understood however, with little focus being placed on the role that these species may play within fragmented habitats. In Australian rainforests, the relative abundance of small mammals has been demonstrated not to change significantly and can even increase after habitat fragmentation (Laurance 1994). Small mammal populations may even develop into the dominant mammalian frugivores, in terms of their relative abundance within small isolated habitat fragments (Laurance 1994, Harrington et al. 2001, Streatfeild 2009). Changes in faunal assemblages are due in part to the loss or decline in the number of competitors and predators including many that are habitat specialists (Laurance 1990), co-evolved mutualists (Gilbert 1980) or species with large area requirements (Terborgh 1974). If we are to develop appropriate conservation strategies for rainforest habitat remnants, it is important to understand the impact that all animal species have on fragmented systems. Due to the potential increase in population densities of small mammals it is particularly important to determine the effect of these species in fragmented rainforest systems. The utilisation studies presented in previous chapters indicate that M. cervinipes and R.fuscipes utilise only a small proportion of available seed resources within forest remnants. These studies also indicate that both species feed primarily on the pericarp of fruits removing the

112 Chapter 5. Seed germination Impacts of feeding flesh for consumption and then discarding the seeds. It is important therefore to develop estimates of the impacts that rodents may have on seed germination as their feeding behaviour may significantly influence propagule establishment. This chapter will investigate the impact that M. cervinipes and R. fuscipes have on germination rates of native fruits with seeds too large to be ingested. Of particular interest is the effect that they have on seed germination on a range of fruits types, sizes and structure.

113 Chapter 5. Seed germination Impacts of feeding Methods A vegetation survey (as outlined in Chapter 2) identified the most common fruit species present within the three experimental sites that covered a range of fruit types and sizes (Table 1). Four fruit categories were identified for use in the study that were representative of fruits available to rodents within patches. Fruits were categorised on the basis of their size and pericarp (fleshy or hard pericarps). Fruit categories identified: Large fleshy fruits (LF), large hard fruits (LH), small fleshy fruits (SM) and small hard fruits (SH). Between 120 and 160 fresh, undamaged fruits of each fruit species were collected for this study as they became available across the year (Table 5.1). No choice feeding trials were undertaken with M. cervinipes and R. fuscipes individuals. No choice trials were conducted as the experiment was designed to determine the impacts of rodents on a number of fruit species. No determination of the relative consumption of other fruits was undertaken. Stainless steel rodent cage traps were used to house rodents for feeding trials (Figure 5.1). Cage traps were arranged on a black plastic lining within rainforest fragments. Traps were covered with a waterproof tarpaulin to keep caged rodents dry and warm (Figure 5.1). A wild rodent was placed in each cage trap and fed a peanut paste rolled oats mixture for 12 hours. During this period animal health was monitored. The individual was then left without food for a further 12 hours, following which individual fruits (depending on size) of a single fruit species were added to the cage and the rodent left to feed for 12 hours. Water was supplied for the entire

114 Chapter 5. Seed germination Impacts of feeding period that experimental rodents were in the cage trap. On completion of the trial, each individual was released at point of capture and all seed and fruit remains were collected. Three replicate feeding trials were conducted for each rodent and seed species combination. All rodents used in feeding trials were live trapped within the site and no rodent was used in more than a single trial. Each trial was conducted in the area where individual fruits and rodents for the trial were collected. Figure 5.1: Experimental set up for feeding trials. Twenty damaged fruits from the pooled replicates for each rodent and fruit combination were planted in standard potting mixture as outlined by Goosem and Tucker (1995) and maintained under nursery conditions for up to 9 months to allow natural germination to occur. Two types of controls were used: (a) twenty

115 Chapter 5. Seed germination Impacts of feeding undamaged fruits of each species were planted and maintained as described above and (b) twenty undamaged fruits of each species were treated according to local nursery methods for germination of rainforest species as detailed in Goosem and Tucker (1995), prior to being planted out and maintained as described above. Goosem and Tucker (1995) recommend different treatments for different rainforest plant species, but all treatments involve damaging or removing the outer tissue layers of the fruit in some way. 5.3 Analysis One way Analysis of Variance (ANOVA) were used to determine differences in germination rates between treatments for pooled fruit species analysis and for fruit species category analysis. Chi-square analysis was used to determine significance of treatment for individual fruit species.

116 Chapter 5. Seed germination Impacts of feeding Results In all rodent feeding trials, seeds were rarely damaged. Generally only the pericarp of the fruit was consumed. Germination rate was very low under natural conditions for 17 of the 20 rainforest fruit species used in this study(figure 5.2), however germination rate was significantly increased by rodents feeding on fruit (F = 73.30, df = 3;55, P < 0.001). The degree of increase in seed germination rate was similar for both rodent species and was equivalent to the level of germination attained using standard pre-germination nursery procedures that require damage to outer layers of the fruit (Figure 5.2).

117 Mean germination rate (± 1 SE)/20 seeds Chapter 5. Seed germination Impacts of feeding Melomys Rattus Control Nursery Treatment` Figure 5.2: Mean germination rates of 20 fruit species across four treatments under standardised greenhouse conditions. (Melomys = fruit fed on by M. cervinipes, Rattus = fruit fed on by R.fuscipes, Control = Undamaged fruit, Nursery = fruit treated according to Goosem and Tucker (1995)) Increase in germination rate was also independent of fruit type/size (M. cervinipes: F=2.206, df = 3,55, P=0.126; R. fuscipes : F=1.535, df = 3,55, P = 0.249) for both rodent species (Figure 5.3) and occurred in the majority (17 of 20) of the fruit species trialled (Table 5.1).

118 Chapter 5. Seed germination Impacts of feeding Figure 5.3: Mean germination rates of seed species in four seed type-size classes across four treatments under standard greenhouse conditions. ( = Nursery, = Control, = M. cervinipes & = R. fuscipes) (LF = Large Fleshy Fruits, LH = Large Hard Fruits, SF = Small Flesh Fruits, SS = Small Fleshy Fruits)